- Hystrix, the Italian Journal of Mammalogy

Transcription

ISSN 0394-1914
HYSTRIX
the Italian Journal of Mammalogy
Volume 26(1) • 2015
published by
Associazione Teriologica Italiana
HYSTRIX
Volume 26(1) • 2015
Edited and published by Associazione Teriologica Italiana
Editor in Chief
Giovanni Amori
CNR-ISE, Istituto per lo Studio degli Ecosistemi
viale dell’Università 32, 00185 Roma, Italy
email: [email protected]
Associate Editors
Francesca Cagnacci, Trento, Italy (Editorial Committee coordinator)
Kenneth B. Armitage, Lawrence, USA
Andrea Cardini, Modena, Italy
Paolo Colangelo, Rome, Italy
Paolo Ciucci, Rome, Italy
Richard Delahay, Exeter, United Kingdom
Nicola Ferrari, Milan, Italy
Marco Festa Bianchet, Sherbrooke, Canada
Tim Flannery, Melbourne, Australia
Philippe Gaubert, Paris, France
Colin P. Groves, Canberra, Australia
John Gurnell, London, United Kingdom
Boris Kryštufek, Ljubljana, Slovenia
Nick Milne, Perth, Australia
Alessio Mortelliti, Canberra, Australia
Jorge M. Palmeirim, Lisboa, Portugal
Pasquale Raia, Naples, Italy
F. James Rohlf, New York, United States
Francesco Rovero, Trento, Italy
Danilo Russo, Naples, Italy
Massimo Scandura, Sassari, Italy
Lucas Wauters, Varese, Italy
Assistant Editors
Leonardo Ancillotto, Rome, Italy
Roberta Chirichella, Sassari, Italy
Simona Imperio, Jenne (Rome), Italy
Giulia Sozio, Teramo, Italy
Bibliometrics Advisor
Nicola De Bellis, Modena, Italy
Technical Editor
Damiano Preatoni, Varese, Italy
Impact Factor (2014) 2.860
HYSTRIX, the Italian Journal of Mammalogy is an Open Access Journal published twice per year (one volume, consisting of two issues) by Associazione
Teriologica Italiana. Printed copies of the journal are sent free of charge to members of the Association who have paid the yearly subscription fee of 30 e.
Single issues can be purchased by members at 35 e. All payments must be made to Associazione Teriologica Italiana onlus by bank transfer on c/c n. 54471,
Cassa Rurale ed Artigiana di Cantù, Italy, banking coordinates IBAN: IT13I0843051080000000054471.
The Italian Theriological Association is available to promote exchanges with journals published by other scientific associations, museums, universities, etc.
For information please contact the ATIt secretariat.
Associazione Teriologica Italiana secretariat can be contacted at [email protected]
Information about this journal can be accessed at http://www.italian-journal-of-mammalogy.it
The Editorial Office can be contacted at [email protected]
Associazione Teriologica Italiana Board of Councillors: Adriano Martinoli (Università degli Studi dell’Insubria, Varese) President, Anna Loy (Università degli Studi del Molise) Vicepresident, Gaetano Aloise (Università della Calabria), Dario Capizzi (Agenzia Regionale dei Parchi del Lazio),
Roberta Chirichella (Università degli Studi di Sassari), Daniele Paoloni (Università degli Studi di Perugia), Danilo Russo (Università degli Studi di
Napoli), Stefania Mazzaracca Secretary/Treasurer, Giovanni Amori (CNR-ISE, Rome) Director of Publications, Damiano Preatoni (Università degli
Studi dell’Insubria, Varese) Websites and electronic publications, Filippo Zibordi (Parco Naturale Adamello Brenta) Communication Office, Librarian.
cbe Published under Creative Commons Attribution 3.0 License © Associazione Teriologica Italiana onlus, all right reserved – printed in Italy
This Journal adheres to the Open Access initiative and is listed in the Directory of Open Access Journals (doaj.org)
ISSN 0394-1914
HYSTRIX
Volume 26(1) • 2015
published by
Associazione Teriologica Italiana
©c b e 2015 Associazione Teriologica Italiana onlus. All rights reserved.
This Journal as well as the individual articles contained in this issue are protected under copyright and Creative Commons license by
Associazione Teriologica Italiana. The following terms and conditions apply: all on-line documents and web pages as well as their parts
are protected by copyright, and it is permissible to copy and print them only for private, scientific and noncommercial use. Copyright
for articles published in this journal is retained by the authors, with first publication rights granted to the journal. By virtue of their
appearance in this Open Access journal, articles are free to be used, with proper attribution, in educational and other non-commercial
settings. This Journal is licensed under the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Italy License. To view a copy of
this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/it/ or send a letter to Creative Commons, 444 Castro Street, Suite 900,
Mountain View, California, 94041, USA.
Publication information: Hystrix, the Italian Journal of Mammalogy is published as a printed edition (ISSN 0394-1914) twice per year. A
single copy of the printed edition is sent to all members of Associazione Teriologica Italiana. The electronic edition (ISSN 1825-5272), in
Adobe® Acrobat® format is published “online first” on the Journal web site (http://italian-journal-of-mammalogy.it). Articles accepted for
publication will be available in electronic format prior to the printed edition, for a prompt access to the latest peer-reviewed research.
Best Paper Award
Associazione Teriologica Italiana established a Best Paper Award for young researchers. Eligible researchers are leading authors less than
35 years old, and within 7 years from their PhD (but young researcher at an even earlier stage of their career, i.e. without a PhD, are also
eligible), who have expressed interest in the award in the Communications to the Editor (step 1 of the online submission procedure; for
details, see the Electronic Publication Guide; http://www.italian-journal-of-mammalogy.it/public/journals/3/authguide.pdf).
If the eligible leading researcher is not the corresponding author, the latter should express interest on the leading researcher’s behalf.
Criteria are innovation, excellence and impact on the scientific community (e.g., number of citations).
The award will be assigned yearly, in the second semester of the year following that of reference (i.e., Best Paper Award for 2013 will be
assigned in the second semester of 2014). The Editorial Commitee is responsible to assign the award. A written motivation will be made
public on the journal website.
Finito di stampare nel mese di giugno 2015 - Typeset in LATEX
Stampa: Edizioni Belvedere, via Adige, 45 – 04100 Latina (Italia)
Impact Factor 2014
New Impact Factor assignment
Dear Members, Readers, Authors
We are pleased to highlight that Hystrix, the Italian Journal of Mammalogy, has increased its impact factor considerably,
reaching 2.86. I wish to thank you all for contributing to achieve this result.
As an independent, peer-reviewed Open Access
journal, whose publication fully relies on the voluntary
work of members of Associazione Teriologica Italiana
(the Italian Mammal Society), Hystrix has reached this
goal after years of efforts to raise publication quality. The
quality improvement in the last years is shown in Fig. 1,
where a sharp increase of citations for 2014 can be clearly
seen.
The increase of citations can be attributed mostly to
two issues, 23(1) and 24(1), respectively focusing on
large carnivores and geometric morphometrics. Both
were warmly welcomed by the scientific community.
The growth of our Journal is best seen in terms of
internationalization, as measured by authors’ country origins as well as the proportion of citing papers by country
(Tab. 1). Though most of Hystrix publications are still authored by Italian researches, only 17% of citing Authors
are located in Italy.
This underlines the increasing reputation of Hystrix
in the international community of mammal researchers.
More interestingly, many citations came from other scientific fields: our Journal belongs to a “generalist” category (i.e. “zoology”), nonetheless it is cited in Journals
classified in other fields such as ecology, biology, evolutionary biology, multidisciplinary sciences, genetics and
anatomy, to remark the broad potential appeal of mammal
studies.
Based on these premises, our goal is now to further
consolidate and improve the quality of Hystrix publications and we are sure that your qualified scientific contribution will help us keeping up the good work together.
Sincerely,
the Editorial Board
Hystrix, the Italian Journal of Mammalogy
Figure 1: Number of citations per year, since 2007.
Source: Thomson Reuters Web of Science
Table 1: Origin of Authors publishing on Hystrix and citing
papers for 2012-2013.
Source: Thomson Reuters Web of Science
Publishing Authors
Country
%
Italy
28
Australia
8
United Kingdom 8
Germany
8
Austria
7
France
6
USA
6
Other countries
29
Citing Authors
Country
%
USA
22
United Kingdom 18
Italy
17
Spain
10
Austria
7
France
7
Australia
6
Other countries
13
1
Workshop announcement
The impact of climate changes on animal populations
Workshop at the “Ettore Majorana Centre”, Erice, 9-14 November 2015
From November 9 to 14, the “Ettore Majorana” Foundation and Centre for Scientific Culture, directed by Prof.
Antonino Zichichi will host an International Workshop on the
impacts of climate change on animal populations.
The workshop constitutes the final outcome of a National
Interest Research Project (PRIN) funded by the Italian Ministry of Research and University, and realized by five research groups from the Universities of Sassari, Pavia, Insubria, Palermo, and from the Institute of Atmospheric Sciences
and Climate of the National Research Council.
This workshop aims at providing a forum to discuss recent advancements in the understanding of the interaction
between climate, environment and populations of many model
species belonging to upper vertebrates (birds and mammals),
in particular in the Mediterranean environment.
The organizers plan to develop an interdisciplinary approach inviting specialists not only from the behavioural ecology but also from plant ecology and climatology communities, in an evolutionary biology perspective.
The workshop is directed by Marco Apollonio (University of Sassari), Mauro Fasola (University of Pavia), Stefano
Grignolio (University of Sassari), Jost von Hardenberg (CNR–
ISAC), Adriano Martinoli (Insubria University), Maurizio
Sarà (University of Palermo). The invited lecturers, and the
main lecture topics are reported below.
Dal 9 al 14 Novembre il Centro di Cultura Scientifica
fondazione “Ettore Majorana”, diretto dal Prof. Antonino
Zichichi, ospiterà un Workshop Internazionale sugli effetti
dei cambiamenti climatici sulle popolazioni animali.
Il Workshop costituisce l’evento finale di un Progetto di
Ricerca di Interesse Nazionale (PRIN), finanziato dal Ministero dell’Istruzione, dell’Università e della Ricerca, e realizzato
da cinque gruppi di ricerca appartenenti alle Università di
Sassari, Pavia, Insubria, Palermo e dall’Istituto di Scienze
dell’Atmosfera e del Clima del Consiglio Nazionale delle
Ricerche.
L’obiettivo del Workshop è quello di offrire un contesto
per la discussione dei recenti sviluppi nella ricerca sulle interazioni tra clima, ambiente e popolazioni, considerando
numerose specie modello appartenenti ai vertebrati superiori
(uccelli e mammiferi), con particolare riferimento agli ambienti mediterranei.
Gli organizzatori si prefiggono di sviluppare un approccio
interdisciplinare al problema, invitando esperti non solo nel
campo dell’ecologia comportamentale, ma anche specialisti
di ecologia vegetale e climatologia, in un contesto legato alla
biologia evoluzionistica.
Il Workshop è diretto da Marco Apollonio (Università di
Sassari), Mauro Fasola (Università di Pavia), Stefano Grignolio
(Università di Sassari), Jost von Hardenberg (CNR–ISAC),
Adriano Martinoli (Università dell’Insubria), Maurizio Sarà
(Università di Palermo). Gli esperti invitati, così come gli
argomenti dei loro interventi sono riportati di seguito.
Walter Arnold (University of Veterinary Medicine, Vienna, Austria)
Adaptation of mammals to changing temperature.
Carl Beierkuhnlein (University of Bayreuth, Germany)
Biogeography in the era of big data.
Stan Boutin (University of Alberta, Canada)
Climate changes and mammals: evolutionary versus plastic responses.
Viktor Brovkin (Max Planck Institute for Meteorology, Hamburg, Germany)
Large-scale interactions between climate and vegetation.
J. Hans C. Cornelissen (University of Amsterdam, Netherlands)
Climate change and temperate forest.
Göran Ericsson (Swedish University of Agricultural Sciences, Umea, Sweden)
Climate effects on large mammal populations in Northern Europe.
Brian Huntley (Durham University, United Kingdom)
Modelling the spatio-temporal dynamics of southern African bird species’ responses to environmental change.
Raimundo Real Giménez Departamento de Biologia Animal, University of Malaga, Spain
Including species interactions and adaptation when modelling biogeographical responses to climate change.
Yukihiko Toquenaga (School of Life and Environmental Science, Tsukuba Ibaraki, Japan)
Impact of climate change on waterbirds populations.
Further information on the Workshop, as well as the program
and participation instruction, can be found online at:
Ulteriori informazioni sul Workshop, incluso il programma
dettagliato e le istruzioni per l’iscrizione, sono reperibili online:
http://www.climateandpopulations.it
Information on the “Ettore Majorana” Foundation and Centre
for Scientific Culture can be found at:
Informazioni relative al Centro di Cultura Scientifica fondazione
“Ettore Majorana” sono reperibili online:
http://http://www.ccsem.infn.it
3
ATIt joins Citizen Science project
Citizen Science: a free application to collect
mammals presence records
Citizen Science: una “app” gratuita per inviare
dati di presenza di mammiferi
A citizen science mammal survey campaign entered its
testing phase, under the LIFE13 ENV/IT/842 CSMON
project, in synergy with Associazione Teriologica Italiana
Avviata la sperimentazione per promuovere una campagna di segnalazione promossa in sinergia da ATIt e il
Progetto LIFE13 ENV/IT/842 CSMON
Thanks to a collaboration between Associazione Teriologica Italiana and the CSMON LIFE Project, a free “app” for
smartphones is available, to collect and archive in a freely
searchable repository on the Internet presence records of
some italian mammal species.
A first testing phase has been started, dealing with 15
Mammal species (red fox, weasel, badger, polecat and stone
marten among Carnivores, hedgehog among Erinaceomorpha,
brown and Apennine hare among Lagomoprphs, common
and edible dormouse, porcupine among Rodents, wild boar,
roe and red deer among Ungulates).
Anyone, downloading the “app” and following the instructions for its usage, could contribute to collect valuable
information on these species distribution. It will be also possible to report occurrences of alien species such as the Eastern
grey squirrel (targeted by a specific campaign, in partnership
with the LIFE U-SAVEREDS project), to increase knowledge
on one of the most important causes of biodiversity loss.
The main goal of the initiative is to follow species distribution in space and time, for a better understanding of conservation issues as well as to promptly identify changes in population dynamics, pointing out areas of criticality in which
timely actions are needed. The data collection campaign also
aims to draw the general public to conservation anf management topics concerning italian wildlife, of which mammals
constitute one of the most outstanding and symbolic components. Data collection is now limited to some of the most
common, easily recognizable species, just to promote an easy
start for the highest number of participants: in the future, a
more in-depth platform (Therio.it) is under development, and
it will work in synergy with the existing smartphone application. The “app” can be downloaded for free on the CSMON
LIFE project (http://www.csmon-life.eu). To send records,
join the “Mammiferi” campaign, attaching a photograph of
the recorded individual, or otherwise any recognizable sign
of presence, such as porcupine quills or footprints for badger
or roe deer.
All the records sent will be validated by an experts panel
from Associazione Teriologica Italiana, and will participate
in the National Biodiversity Portal of the Ministry of the
Environment.
For further information: http://www.csmon-life.eu/pagina/
app/45
Grazie ad una collaborazione tra l’Associazione Teriologica Italiana e il Progetto LIFE CSMON, è disponibile gratuitamente una “app” per smartphone ideata per raccogliere
in un unico archivio, liberamente consultabile in rete, dati di
presenza di alcune specie di mammiferi italiani.
Per una prima fase di sperimentazione, sono state selezionate 15 specie di Mammiferi (volpe, donnola, tasso, puzzola
e faina tra i Carnivori, riccio tra gli Erinaceomorfi, lepre
comune e lepre appenninica tra i Lagomorfi, moscardino,
ghiro e istrice tra i Roditori, cinghiale, capriolo, cervo tra
gli Ungulati). Chiunque, scaricando la “app” e seguendo
le indicazioni per il suo utilizzo, potrà contribuire a fornire
informazioni preziose sulla distribuzione di queste specie.
Sarà anche possibile segnalare la presenza di specie alloctone, come ad esempio nutria e scoiattolo grigio (oggetto di
una specifica campagna di monitoraggio in collaborazione
con il Progetto LIFE U-SAVEREDS), che rappresentano uno
dei principali fattori di perdita di biodiversità.
Lo scopo dell’iniziativa è quello di seguire la distribuzione
delle specie nel tempo e nello spazio, al fine di comprenderne lo stato di conservazione e individuare tempestivamente le variazioni nelle dinamiche di popolazione determinando eventualmente aree critiche sulle quali intervenire prioritariamente. Obiettivo della campagna è anche quello di avvicinare un pubblico sempre più vasto alle problematiche di
tutela e gestione della fauna italiana, di cui i mammiferi sono
una delle componenti più vulnerabili, simboliche e rappresentative. La campagna è per ora limitata alla segnalazione
di alcune delle specie più comuni e facilmente riconoscibili
proprio con l’intento di promuovere un avvicinamento facilitato rivolto al numero più ampio possibile di persone:
per il futuro è in via di sviluppo una piattaforma (Therio.it)
che lavorerà in sinergia con la “app”. L’applicazione può
essere scaricata gratuitamente sul sito del LIFE CSMON
(http://www.csmon-life.eu). Per inviare le segnalazioni occorre aderire alla campagna “Mammiferi” allegando una foto
dell’animale o dei segni riconoscibili della sua presenza: per
esempio, si potranno allegare foto degli aculei dell’istrice o
dell’impronta di un tasso o di un capriolo.
Le segnalazioni pervenute, dopo una verifica da parte degli esperti dell’Associazione Teriologica Italiana, che garantisce
il supporto scientifico all’iniziativa, confluiranno nel Portale
Nazionale della Biodiversità del Ministero Ambiente.
Maggiori informazioni sul sito del Progetto CSMON:
http://www.csmon-life.eu/pagina/app/45
5
10th ATIt Congress
X Congresso Italiano di Teriologia
Riserva Naturale del Monte Rufeno, Acquapendente (VT), Italy
April, 20–23 2016
The Monte Rufeno Natural Reserve, at Acquapendente
(Viterbo), will host the Tenth National Theriological Congress, from 20 to 23 April 2016. The Congress is organised
by Associazione Teriologica Italiana (ATIt), in collaboration
with Agenzia Regionale dei Parchi del Lazio (ARP), Riserva
Naturale di Monte Rufeno and Società Italiana di Ecopatologia della Fauna (SIEF).
According to tradition, the Congress will be an opportunity to see where we’re up to in the field of mammal research,
and will also be a venue useful to promote partnerships and
synergies at all levels: students, professionals and researchers.
The Congress will provide for 4 thematic sessions:
• Mammmals, ecology and behaviour;
• Mammmals, ecopathological and anthropic impacts
and management (in parthership with SIEF)
• Alien mammals: impacts, control and mitigation (in
partnership with U-SAVEREDS LIFE Project,
usavereds.eu);
• Taxonomy, monitoring and conservation of Mammals.
Sessions will be followed by two workshops (“Wildlife
and communication: how to cope with hoaxes” and “Mammals and Natura 2000 Network”), by a laboratory on alien
Sciurids identification and by a round table during which will
be presented the Atlas of Italian Mammals project (therio.it).
Besides the customary Members Assembly and election
of the statutory bodies, other events will facilitate discussions
and the exchange of ideas: “ProiettATIt”, a film exhibition
with documentary films on mammals and camera-trap sequence edits, and “AffamATIt. . . anche di scienza”, a cocktail
party where the posters presented at the Congress will be
commented and discussed informally.
The Congress will close with the traditional social dinner
and ATIt blind auction, after whom the evening will culminate, following the enthusiastic appreciation of the last Congress held in Civitella Alfedena, with the “Forno in piazza”
street show. As in the former Congress event, a team of master potters will prepare and fire in a temporary kiln prepared
in Acquapendente main square a statue representing two roe
deers, that will be donated to the hosting authorities.
During the Congress will be delivered the Best Paper
Award 2016, a 500 Euro prize for the best paper p[ublished
by a young theriologist on Hystrix, the Italian Journal of
Mammalogy.
Further information, as well as the application form, on
the ATIt web site: biocenosi.dipbsf.uninsubria.it/congressi/
The Monte Rufeno Natural Reserve, established in 1983, belongs to the
Latium protected areas network, and covers about 3000 hectares in the town
of Acquapendente, in the province of Viterbo, at the border with Umbria
and Tuscany. Landscpe is characterised by gentle and smooth landforms,
typical of northern Latium and southern Tuscany. Acquapendente is crossed
by the ancient Via Francigena, the historical route still bringing thousand of
pilgrims to Rome each year, here through a perspective of old Etruscan areas
of great importance for their history, wildlife, food and wine.
Avrà luogo presso la Riserva Naturale del Monte Rufeno,
nel comune di Acquapendente (VT), tra il 20 e il 23 Aprile
2016, il decimo Congresso Nazionale di Teriologia, organizzato
dall’Associazione Teriologica Italiana (ATIt), in collaborazione
con l’Agenzia Regionale dei Parchi del Lazio (ARP), la Riserva
Naturale di Monte Rufeno e la Società Italiana di Ecopatologia della Fauna (SIEF).
Come da tradizione, il Congresso sarà l’occasione per
fare il punto a livello nazionale sulle ricerche in atto riguardanti i mammiferi e costituirà un momento di incontro per
promuovere collaborazioni e sinergie a tutti i livelli: studenti,
liberi professionisti e ricercatori.
Il Congresso sarà articolato in 4 sessioni tematiche:
• Mammiferi, ecologia, evoluzione e comportamento;
• Mammiferi impatti ecopatologici, antropici e gestione
(in collaborazione con SIEF)
• Mammiferi alloctoni: impatti, controllo e mitigazioni
(in collaborazione con il Progetto LIFE U-SAVEREDS,
usavereds.eu);
• Tassonomia, monitoraggio e conservazione dei Mammiferi.
Le sessioni saranno affiancate da due workshop (“Fauna e
comunicazione: come fronteggiare le bufale in campo faunistico” e “Mammiferi e Rete Natura 2000”), da un laboratorio
sul riconoscimento degli Sciuridi alloctoni e da una tavola
rotonda durante la quale sarà presentato il Progetto Atlante
Italiano dei Mammiferi (therio.it).
Accanto alla consueta assemblea dei Soci ed elezione
delle cariche statutarie, altri eventi agevoleranno lo scambio
di idee e discussioni: “ProiettATIt”, una rassegna di cortometraggi, video montati da fototrappole e documentari a tema
teriologico, e “AffamATIt. . . anche di scienza”, un aperitivo
durante il quale saranno commentati i poster esposti.
L’evento si concluderà con la tradizionale cena sociale e
con l’asta dell’ATIt. Successivamente, sulla base dell’ottimo
riscontro di quanto organizzato durante lo scorso congresso
svoltosi a Civitella Alfedena, la serata continuerà con il Forno
in piazza, durante il quale si assisterà alla parte finale della
forgiatura di una statua con due caprioli, un maschio e una
femmina, che sarà donata dall’associazione all’Ente ospitante.
Durante il Congresso sarà assegnato il Best Paper Award
2016, un premio di 500 Euro per il miglior articolo pubblicato
da un giovane teriologo su Hystrix, the Italian Journal of
Mammalogy.
Maggiori informazioni, insieme alla scheda per iscriversi
sul sito dell’ATIt: biocenosi.dipbsf.uninsubria.it/congressi/
La Riserva Naturale Monte Rufeno, istituita nel 1983, fa parte del
sistema delle aree protette del Lazio e si estende per circa 3000 ettari nel
territorio del comune di Acquapendente, in provincia di Viterbo, al confine
con l’Umbria e la Toscana. Il territorio è caratterizzato da una morfologia
dolce che si inserisce nel tipico paesaggio collinare dell’Alto Lazio e della
Toscana meridionale. Acquapendente è caratterizzato anche dalla presenza
della Via Francigena, l’antico percorso che porta a Roma migliaia di pellegrini ogni anno, attraversando questo importante scorcio di aree etrusche
di grande interesse storico, naturalistico ed enograstronomico.
7
Published by Associazione Teriologica Italiana
Volume 26 (1): 9–12, 2015
Available online at:
doi:10.4404/hystrix-26.1-11264
http://www.italian-journal-of-mammalogy.it/article/view/11264/pdf
Commentary
The tps series of software
F. James Rohlfa,∗
a
Department of Anthropology, Stony Brook University, Stony Brook, NY 11794-4364, USA
Keywords:
Geometric morphometrics
landmarks
software
thin-plate spline
relative warps
Abstract
The development and the present state of the “tps” series of software for use in geometric morphometrics on Windows-based computers are described. These programs have been used in hundreds
of studies in mammals and other organisms.
Article history:
Received: 20 April 2015
Accepted: 19 May 2015
Acknowledgements
The encouragement by Andrea Cardini for me to prepare this paper and
his comments on the ms. are much appreciated. I am very grateful
also to Anna Loy for her helpful comments on an earlier version of the
manuscript: she greatly helped to improve the article.
Some history
Work on the tps series of programs was begun by me in late 1990. At
that time the only software specifically designed for the new field of
geometric morphometrics was that developed by Fred Bookstein and
Bill Green for the mainframe computer running the MTS operating
system at the University of Michigan. As that operating system was
only available at about a dozen computing centers around the world,
the need for new and easy to use software was quite apparent. This
was quite striking at the NSF-sponsored workshop on morphometrics
held at Stony Brook University in the summer of 1990. New methods
were described by Bookstein but participants were not able to actually
try them on their own data. At the same time, the microcomputer revolution had started and it was clear that the new software should be
developed for these new devices. It was also clear that the new software should include highly interactive graphics because it is easier to
understand shape differences visually than numerically.
The first programs developed in the series were the MS-DOS programs TPSPLINE and TPSRW. The TPSPLINE software smoothly transforms the positions of landmarks and an overlaying grid for one specimen so that its landmark positions would map exactly onto another set.
The grid was then subjected to the same transformation. The thin-plate
spline function was used to provide this maximally smooth transformation, Bookstein (1989). The transformed grid produces a graphic in
the spirit of the D’Arcy Thompson transformation grids, Thompson
(1917). However, these transformed grids represent the actual differences in the location of landmarks rather than intuitive sketches, Klingenberg (2013). The GRF software of Rohlf and Slice (1991) was available at the time of the morphometrics workshop at the University of
Michigan, Rohlf and Bookstein (1990). It was not made part of the
series because the generalized Procrustes computation was to be made
part of most of the programs in the series.
∗
Corresponding author
Email address: [email protected] (F. James Rohlf)
Hystrix, the Italian Journal of Mammalogy ISSN 1825-5272
©cbe2015 Associazione Teriologica Italiana
doi:10.4404/hystrix-26.1-11264
The use of “tps” in the names of these and later software was because
they made use of the thin-plate spline function. At the time the software was first written, the use of the thin-plate spline function and its
decomposition by spatial scale into principal and partial warps seemed
to be an essential component of the new statistical methods. Later,
e.g., Rohlf (1999), it became clear that the computation of partial warp
and uniform scores could be eliminated because a PCA of these scores
differed from that of Procrustes coordinates (after their projection onto
the multivariate space tangent to Kendall’s shape space) by only a multiplication by an orthonormal matrix i.e., a rotation. This is important
because test statistics for standard multivariate statistical methods are
invariant to such transformations. For example, they yield the same
plots of PCA scores. However, this relationship is only exact if the
shape coordinates have been projected onto the space tangent to Kendall’s shape space, see Rohlf (1999). Unfortunately, not all morphometric software performs this projection so that the PCA is performed in a
space that is curved. The amount of curvature depends on the amount
of shape variation, see Slice (2001). Of course with very similar shapes
the curvature will be very small. The decomposition of shape differences at different spatial scales (as captured by the partial warps) is
mathematically elegant but these individual components are unlikely to
be directly interpretable biologically for reasons such as those presented in Rohlf (1998). However, Bookstein (2015) shows that they can
be very important for the study of integration because they allow one
to take variation at different spatial scales into account.
The TPSRW software, described in Rohlf (1993), performed an analysis of relative warps as defined by Bookstein (1989, 1991). The
TPSPLINE and TPSRW programs were available by the time of the 1991
morphometrics workshop in Valsain, Spain, Marcus et al. (1993). By
the time of the 1992 morphometrics workshop in Paris, France, the
TPSREG software was also available. It performed a multivariate multiple regression of partial warp scores onto one or more independent
variables. It is “multivariate” because there will always be more than
one shape variable and “multiple” because the software allows more
than one independent variable.
19th May 2015
Hystrix, It. J. Mamm. (2015)
26(1): 9–12
The programs use the .tps file format designed for holding the 2D
and 3D coordinates of landmark points and, optionally, the name of
the image file corresponding to the landmarks for each specimen. It
was later generalized to also hold coordinates of points along curves
and entire outlines. The landmark coordinates can also be saved as
matrices using the .nts (NTSYSpc) file format. Both formats are described in the help files included with each program. Numerical results
such as matrices of principal warps and partial warp scores, relative
warp scores, etc. can be saved using the .nts (NTSYSpc), .m (Matlab),
and .csv file formats. These are all plain ASCII text files than can
be viewed and modified for use with other software by using a text
editor such as the Windows Notepad (although more powerful editors
are more convenient when more extensive changes are needed). The
decision to develop a series of specialized programs rather than one
comprehensive program was made to enable at least some software for
geometric morphometrics to be available as soon as possible.
Towards the end of the 1990s development was switched from MSDOS to the Windows 3.1 operating system and by the time of the 1997
morphometrics workshop in Rome, Italy, the software had been rewritten and new software developed for use with MS-Windows 95. It was
soon migrated to Windows NT. This change made the analysis of larger
datasets possible as well as better graphics. This also meant that only
minimal changes to the software would then be needed for compatibility with the new versions of Windows. The present suite of programs
in this series were written in a standard way for Windows 7, 8, and 8.1
but should run on future versions of Windows as well as emulators on
Linux (e.g., WINE, http://www.winehq.org/) and MacOS computers. It
should be noted that the software all have help files that provide both
technical information about what the programs do, notes on how to use
each program, and usually examples. The programs are listed below in
alphabetical order.
The present programs in the TPS series
TpsDig2. This software is used to capture the coordinates of landmarks
for a wide variety of 2D image formats. The intended usage of the
software is to start with a .tps file that contains lines with “LM=0” and
“IMAGE=xxx” (where “xxx” is the name of an image file) for all the
specimens in a study. This initial .tps file can be created automatically using one of the options in the tpsUtil program. One can then
move through the images by pressing the red left and right arrow buttons. The images can also be transformed in order to enhance them
so that the landmarks are easier to see. Coordinates of points along
outlines and curves can also be captured. For high-contrast images,
complete outlines can be captured automatically, Souto-Lima and Millien (2014) is an example using molars of voles. TpsDig2 is an update
of TpsDig. The update was needed for compatibility with high resolution image files that are now used. The program can also be used to
measure distances, angles, and areas.
TpsPLS. A program to perform a two-block partial least-squares analysis, 2BPLS, as described by Rohlf and Corti (2000). The software can
be used to analyze and visualize patterns of covariation, if any, between
a set of variables and a sample of shapes from the same set of specimens. An early example of this is given in Adams and Rohlf (2000). A
recent example relating fractures of different teeth to mandible shape in
carnivores is given in Meloro (2012). The software can also be used to
study the covariation between the shapes of two structures for the same
set of specimens. An example of this is given in Pizzo et al. (2009).
Configurations of landmarks corresponding to various positions in the
space of the singular warps can be displayed.
TpsRegr. This performs a multivariate multiple regression of shape
(using warp and the uniform component scores as the dependent variables) regressed on one or more independent variables. The independent variables can be observed variables such as temperature or elevation or they can be dummy variables that code various experimental
designs using the method usually called “fitting constant”, e.g., Sokal
and Rohlf (2012). This allows one to perform MANOVAs and ANCOVAs of shape variation. Choizzi et al. (2014) is a recent example
for Soemmerring’s Gazelle. Cardini and O’Higgins (2004) also used it
10
to test for differences in cranial shape in Marmots. Paired comparison
designs are often useful. Visualizations are provided to show the effects of variation in each independent variable. The results are given in
terms of both Procrustes statistics and conventional multivariate tests.
Permutation test statistics are also provided. The permutations can be
constrained to be either within or among blocks of specimens so as to
conform to certain experimental designs. Configurations of landmarks
predicted by the regression can be displayed. The shape changes associated with each independent variable can be explored by simply moving
a slider back and forth. This software has been used in many studies.
For example, Bastir and Rosas (2004) regressed mandible shape on size
to study allometry in humans, Slater and Van Valkenburgh (2008) regressed cranial shape on tooth length for sabretooth cats. An estimated
image corresponding to a predicted configuration of landmarks can be
created using the TpsSuper software but that does not seem to have
been done often. In addition to the usual interactive mode, the program can also be completely controlled using batch mode commands.
This is very useful when the software is used in simulation studies.
TpsRelw. This is the most used program in the series. Examples are
too numerous to list here. The program computes the average shape
and then aligns all specimens to this average shape using a Generalized Procrustes analysis, Rohlf and Slice (1990). The average shape,
aligned specimens, and centroid sizes can be saved to files. It then performs an analysis of relative warps, i.e., a principal components analysis of shape variation relative to spatial scale, Bookstein (1989, 1991)
and Rohlf (1993). Its α parameter allows weights to be given to differences in landmarks at different spatial scales in the average shape
estimated using generalized Procrustes analysis (often called the reference or the consensus configuration). However, α is now usually
set to zero so that analysis is then simply a principal components analysis of shape variation (as captured by the set of partial warp scores)
and no longer relative to spatial scale. It produces the same results as
a PCA of the Procrustes shape coordinates if they are projected onto
the tangent space. In the plot of the relative warp scores, shapes can
be displayed corresponding to arbitrary positions in the ordination by
moving a small red circle with the mouse. Plots for positions at the extremes along each axis are often published along with the ordination.
Animations corresponding to arbitrary sequences of positions in space
can also be constructed. Another important feature of this software is
that it can slide semilandmarks along curves as described by Bookstein
(1997). While this is the only software in the tps series that provides
this operation, that is not a limitation to the use of this method because
the resulting landmark and semilandmark configuration for each specimen can be output and used as input to the other programs in this series.
The tpsUtil software can be used to create the file that defines the points
that are to be used as semilandmarks rather than the usual fixed landmarks. Because the ordination plots do not provide many options for
customization, the scores are often entered into other software. Unfortunately, such software often does not preserve the relative scales of
the axes. The plots can be very misleading unless the axes are to the
same scale. Figure 3 in Cardini et al. (2015) is a good example of the
correct scaling. The ordination plot is elongated along the first axes
because the first eigenvalue is so much larger than the second. It also
shows shapes corresponding to different locations in the plot. The plot
proposed by Bookstein (2015) can also be produced.
TpsSmall. This is a simple program designed to help a user assess
whether the amount of shape variation in a dataset is small enough to
justify the use of standard multivariate statistical methods in the tangent
space. Fortunately, this is almost always true in studies of mammals.
A possible exception due to the breadth of shapes included is given in
Marcus et al. (2000), a study of variation in the skulls representing the
orders of living mammals. The program plots a matrix of Procrustes
distances element by element against a matrix of Euclidean distances
in the tangent space and reports their uncentered regression slope and
correlation. It also reports on the largest Procrustes distance relative
to the largest possible Procrustes distance, π2 . The distance matrices
can also be saved to a file for use in other software (such as to cluster
The tps series of software
specimens based on their Procrustes distances). This software can also
use 3-dimensional coordinates.
TpsSplin. This software does not perform any statistical analyses. It
simply displays a grid overlaying one specimen transformed using the
thin-plate spline so that the positions of its landmarks coincide with
those of another specimen. It also allows this transformation to be decomposed by spatial scale. Plots can be displayed showing the overall
transformation as well as for just the affine part, the non-affine part
or the latter’s decomposition into the contribution of individual partial
warps. As mentioned above, these decompositions seemed more interesting when the software was first developed than they do now for the
reasons given in Rohlf (1998). The software is still useful for displaying the shape differences between two specimens or two group means.
TpsSuper. This software has several options for the unwarping of
images. An unwarped image is an image that has been transformed
so that its landmarks match those of a specified target configuration of
landmarks. The operation is called “unwarping” rather than “warping”
because, instead of mapping each pixel in the original image to its position in the transformed image, each pixel in the transformed image
is looked-up in the original image. This prevents gaps in the transformed image in regions that are expanded relative to the first image.
See Bookstein (1991) for more discussion and an example. The target
configuration is often an average of all the specimens but it can also be
a configuration of landmarks predicted by regression using tpsRegr, a
point in a PCA plot using tpsRelw, or an estimate of a node in a phylogenetic tree using TpsTree, see Rohlf (2002) for an example of the latter.
It can also compute an average of a sample of images that have been
unwarped to match a specified configuration. Examples are given in
Gharaibeh et al. (2000) for mid-sagittal MRI images of human brains
and in Bookstein et al. (2007) to show the effects of prenatal alcohol
on the brains of children. While most geometric morphometric studies display statistical results as landmark configurations, the addition
of unwarped images can be very helpful for biological interpretation.
I believe that unwarped images should be used more often as they are
more informative than just positions of landmarks and wireframes.
TpsTree. Given a phylogenetic tree or a dendrogram from a cluster
analysis, the program provides visualizations of estimated configuration of landmarks corresponding to the nodes or to arbitrary locations
along the branches. Estimates are computed using the squared-change
parsimony model as described in Maddison (1991). In conjunction
with the TpsSuper software, predicted images can be displayed for the
nodes on the tree. Rohlf (2002) is an example. The software can also
output a phylogenetic covariance matrix — useful in comparative studies that use the phylogenetic generalized least-squares method to analyze their data. See Rohlf (2001) for a discussion. A matrix of independent contrasts, Felsenstein (1985), can also be produced.
TpsTri. This software was designed to display various properties of
shape spaces when there are just 3 landmarks. It does not provide any
statistical analyses of shape variation. It can plot samples of shapes
(user provided or from built-in simulations) on the various shape or
form spaces that have been proposed for use in morphometrics. It can
show, for example, why the reference shape should be at least close to
the mean shape of a sample of shapes. It can also display some of the
properties of the various shape spaces that have been proposed. This
software was used to prepare the plots of shape spaces in Rohlf (2000a);
Slice (2001), and in many other papers describing properties of some
of shape spaces.
TpsUtil. This software resulted from a wide variety requests for
special operations needed when carrying out a morphometric studies. Rather than providing many specialized utility programs, the operations were combined into a single program. It can, for example,
change file formats, delete or reorder landmarks, delete or reorder specimens, split or combine files, and change file formats. The software
can also compute areas, prepare input files for sliding of semilandmarks
in tpsRelw. It includes an option to “unbend” the positions of landmarks
in an attempt to undo distortions in preserved fish. A common use of
tpsUtil is to build the initial .tps file that is used as input to the TpsDig2
software. I am still open to suggestions for additional operations.
Other, more specialized programs
The following programs were written because they were needed for particular papers I wrote. However, the programs were generalized somewhat so that they might also be of use to others — either to duplicate
my simulations or to perform additional experiments.
TpsBias. This software was used for the computations and illustrations in Rohlf (2003). That study examined the patterns of error and
bias for several methods for estimating of the mean shape for a sample.
While that study only simulated isotropic variation at each landmark,
the software can also be used to investigate more general models (different amounts of variation at each landmark and with correlated variation within and between landmarks). The results for these latter models have not yet been published but the conclusions are very similar
— Procrustes methods have much better statistical properties (less bias
and smaller mean square error) than other morphometric methods that
have been proposed – even though these models violate the assumptions
of the Procrustes-based methods. The program can also be completely
controlled using batch mode commands for use in simulation studies.
TpsPower. This software was used for the computations and illustrations in Rohlf (2000b). It allows one to determine the probability of
correctly deciding that two samples of shapes were drawn from populations with different mean shapes. The results are given for several
test statistics. The original version of the software was constrained to
the isotropic model but more general models can also be investigated.
In addition to the usual interactive mode, the program can also be completely controlled using batch mode commands for when the software
is used in simulation studies.
Future development?
It was originally expected that the programs would eventually be combined into a single comprehensive package. That development now
seems less important because there are now several such general programs available. It is a sign of the growing maturity of the field. There
are stand-alone programs such as MorphoJ (http://www.flywings.org.
uk/morphoj_page.htm), Morpheus et al (http://morphlab.sc.fsu.edu/
software.html), NTSYSpc (http://www.exetersoftware.com), IMP (http:
//www3.canisius.edu/~sheets/IMP%208.htm), or the EVAN Toolbox (for
members of the European Virtual Anthropology Network). There are
also collections of procedures for R such as the geomorph package
(http://www.geomorph.net). It is tempting to generalize the tps series
to allow for 3-dimensional coordinates but no firm decision has been
made.
References
Adams D.C., Rohlf F.J., 2000. Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. Proceedings of the National Academy of Sciences, USA 97: 4106–4111.
Bastir M., Rosas A., 2004. Geometric morphometrics in paleoanthropology: Mandibular shape variation, allometry, and the Evolution of modern human skull morphology.
In: Elewa A.M.T. (Ed.) Morphometrics: Applications in Biology and Paleontology.
Springer, Berlin - Wien. 231–241.
Bookstein F.L., 1989. Principal warps: thin-plate splines and the decomposition of deformations. Institute of Electrical and Electronics Engineers, Transactions on Pattern
Analysis and Machine Intelligence 11: 567–585.
Bookstein F.L., 1991. Morphometric tools for landmark data: Geometry and Biology. Cambridge Univ. Press, New York.
Bookstein F.L., 1997. Landmark methods for forms without landmarks: morphometrics of
group differences in outline shape. Medical Image Analysis 1: 225–243.
Bookstein F.L., 2015. Integration, Disintegration, and Self-Similarity: Characterizing the
Scales of Shape Variation in Landmark Data. Evolutionary Biology (online first). doi:
10.1007/s11692-015-9317-8
Bookstein F.L., Connor P.D., Huggins J.E., Barr H.M., Pimentel K.D., Streissguth A.P.,
2007. Many infants prenatally exposed to high levels of alcohol show one particular
anomaly of the corpus callosum. Alcoholism-Clinical and Experimental Research 31:
868–879.
Cardini A., O’Higgins P., 2004. Patterns of morphological evolution in Marmota (Rodentia,
Sciuridae): geometric morphometrics of the cranium in the context of marmot phylogeny, ecology and conservation. Biological Journal of the Linnean Society 82: 385–407.
Cardini A., Polly D., Dawson R., Milne N., 2015. Why the Long Face? Kangaroos and
Wallabies Follow the Same “Rule” of Cranial Evolutionary Allometry (CREA) as Placentals. Evolutionary Biology 42(2): 169-176. doi:10.1007/s11692-015-9308-9
Chiozzi G., Bardelli G., Ricci M., De Marchi G., Cardini A., 2014. Just another island
dwarf? Phenotypic distinctiveness in the poorly known Soemmerring’s Gazelle, Nanger
soemmerringii (Cetartiodactyla: Bovidae), of Dahlak Kebir Island. Biological Journal
of the Linnean Society 111: 603–620.
11
26(1): 9–12
Felsenstein J., 1985. Phylogenies and the comparative method. American Naturalist 125:
1–15.
Gharaibeh W.S., Rohlf F.J., Slice D.E., DeLisi L.E., 2000. A geometric morphometric assessment of change in midline brain structural shape following a first episode of schizophrenia. Biological Psychiatry 48: 398–405.
Klingenberg C.P., 2013. Visualizations in geometric morphometrics: how to read and how
to make graphs showing shape changes Hystrix 24(1): 15-–24. doi:10.4404/hystrix-24.17691
Maddison W.P., 1991. Squared-change parsimony reconstructions of ancestral states for
continuous-valued characters on a phylogenetic tree. Systematic Zoology 40: 304–314.
Marcus L., Hingst-Zaher E., Zaher H., 2000. Application of landmark morphometrics to
skulls representing the orders of living mammals. Hystrix 11(1): 27-47. doi:10.4404/
hystrix-11.1-4135
Marcus L.F., Bello E., Garcia-Valdecasas A. (Eds.), 1993. Contributions to morphometrics.
Monografias, 8. Museo Nacional de Ciencias Naturales, Madrid.
Meloro C., 2012. Mandibular shape correlates of tooth fracture in extant Carnivora: implications to inferring feeding behaviour of Pleistocene predators. Biological Journal of
the Linnean Society 106: 70–80.
Pizzo A., Macagno A.L.M., Roggero A., Rolando A., Palestrini C., 2009. Epipharynx shape
as a tool to reveal differentiation patterns between insect sister species: insights from
Onthophagus taurus and O. illyricus (Insecta: Coleoptera: Scarabaeidae). Organisms
Diversity & Evolution 9: 189–200.
Rohlf F.J., 1993. Relative warp analysis and an example of its application to mosquito
wings. In: Marcus L.F., Bello E., Garcia-Valdecasas A. (Eds.) Contributions to morphometrics. Monografias, 8. Museo Nacional de Ciencias Naturales, Madrid. 131–159.
Rohlf F.J., 1998. On applications of geometric morphometrics to studies of ontogeny and
phylogeny. Systematic Biology 47: 147–158.
Rohlf F.J., 1999. Shape statistics: Procrustes superimpositions and tangent spaces. Journal
of Classification 16: 197–223.
Rohlf F.J., 2000a. On the use of shape spaces to compare morphometric methods. Hystrix
11(1): 9–25. doi:10.4404/hystrix-11.1-4134
12
Rohlf F.J., 2000b. Statistical power comparisons among alternative morphometric methods.
American Journal of Physical Anthropology 111: 463–478.
Rohlf F.J., 2001. Comparative methods for the analysis of continuous variables: geometric
interpretations. Evolution 55: 2143–2160.
Rohlf F.J., 2002. Geometric morphometrics and phylogeny. In: MacLeod N., Forey P.L.
(Eds.) Morphology, shape and phylogenetics. Taylor & Francis, London. 175–193.
Rohlf F.J., 2003. Bias and error in estimates of mean shape in morphometrics. Journal of
Human Evolution 44: 665–683.
Rohlf F.J., Bookstein F.L., (Eds), 1990. Proceedings of the Michigan Morphometrics Workshop. Museum of Zoology special publication no. 2, University of Michigan, Ann Arbor.
Rohlf F.J., Corti M., 2000. Use of two-block partial least-squares to study covariation in
shape. Systematic Biology 49: 740–753.
Rohlf F.J., Slice D.E., 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39: 40–59.
Rohlf F.J., Slice D.E., 1991. GRF – Generalized rotational fit methods, version 1. Department of Ecology and Evolution, State University of New York.
Slater G.J., Van Valkenburgh B., 2008. Long in the tooth: evolution of sabertooth cat cranial
shape. Paleobiology 34: 403–419.
Slice D.E., 2001. Landmarks aligned by Procrustes analysis do not lie in Kendall’s shape
space. Systematic Biology 50: 141–149.
Sokal R.R., Rohlf F.J., 2012. Biometry. The Principles and Practice of Statistics in Biological Research. 4th Edition. W. H. Freeman, San Francisco.
Souto-Lima R.B., Millien V., 2014. The influence of environmental factors on the morphology of red-backed voles Myodes gapperi (Rodentia, Arvicolinae) in Québec and
western Labrador. Biological Journal of the Linnean Society 112: 204–218.
Thompson D.A.W., 1917. On Growth and Form. Cambridge, London.
Associate Editor: A. Cardini
Volume 26 (1): 13–24, 2015
doi:10.4404/hystrix-26.1-11347
Commentary
DNA barcoding in mammals: what’s new and where next?
Andrea Galimbertia , Anna Sandionigia , Antonia Brunoa , Adriana Bellatib , Maurizio Casiraghia,∗
a
ZooPlantLab, Dipartimento di Biotecnologie e Bioscienze, Università degli Studi di Milano-Bicocca,Piazza della Scienza 2, 20126 Milano, Italy.
b
Dipartimento di Scienze della Terra e dell’Ambiente, Università degli Studi di Pavia, Via Ferrata 1, 27100 Pavia, Italy
Keywords:
Biological databases
integrative taxonomy
molecular identification
theriology
wildlife forensics
Article history:
Received: 4 June 2015
Accepted: 25 June 2015
Acknowledgements
The authors are indebted with Monica Pozzi for the linguistic revision
of the manuscript. The authors are also grateful to the anonymous
referees for their useful comments that substantially improved the final
version of this work.
Abstract
DNA barcoding is a universal molecular identification system of living beings for which efficacy
and universality have been largely demonstrated in the last decade in many contexts. It is common
to link DNA barcoding to phylogenetic reconstruction, and there is indeed an overlap, but identification and phylogenetic positioning/classification are two different processes. In mammals, a better
phylogenetic reconstruction, able to dig in fine details the relationships among biological entities,
is really welcomed, but do we need DNA barcoding too? In our opinion, the answer is positive,
but not only for the identification power, nor for the supposed ability of DNA barcoding to discover
new species. We do need DNA barcoding because it is a modern tool, able to create an integrated
system, in which it is possible to link the many aspects of the biology of living beings starting from
their identification. With 7000 species estimated and a growing interest in knowledge, exploitation
and conservation, mammals are one of the best animal groups to achieve this goal.
We organised our review to show how an integrative approach to taxonomy, leaded by DNA
barcoding, can be effective in the twenty-first century identification and/or description of species.
Introduction
Mammals represent a relatively small animal group, with 5564 species listed in the Catalogue of Life (ITIS database, http://www.
catalogueoflife.org). Being our own class, it is thought that these species are among the most known animals, especially regarding taxonomic aspects (Wilson and Reeder, 2006).
Generally speaking this is correct, but there are relevant exceptions,
even on (presumably) well-established species. The case of African
bush and forest elephants is emblematic. In 2001 the populations of
bush and forest elephants were split in two distinct species, Loxodonta
africana (Blumenbach, 1797) and L. cyclotis (Matschie, 1900), using
molecular data to support this separation (Roca et al., 2001). It is clear
that there is a hidden biodiversity within the mammal record, the extent
of which is still under discussion, but surely in some groups like chiroptera, it has a deep impact on the taxonomy (see for example Galimberti
et al., 2012b and Bogdanowicz et al., 2015). On the whole, the estimation of the unknown biodiversity in mammals is not so trivial, but there
is an agreement on the number of about 7000 species (Reeder et al.,
2007). The question is now simple: how to discover them?
Since 2003, DNA barcoding has been claimed to be an innovative
and revolutionary approach to identify living beings, and a way to speed
up the writing of “the encyclopedia of life” (Savolainen et al., 2005). In
other words, the technique would be a system to increase the efficiency
in species discovery. DNA barcoding has many advantages, but criticisms raised against the ability to discover new species (see for a review
Casiraghi et al., 2010). The signature of the success of DNA barcoding is evident from the many group-specific or environment-specific
campaigns launched in the past years (see an updated list of them at
the international Barcode of Life initiative, www.ibol.org). Figure 1
shows a simplistic analysis of the publications on DNA barcoding in
vertebrates since the seminal paper by Paul Hebert was issued in 2003
∗
Email address: [email protected] (Maurizio Casiraghi)
doi:10.4404/hystrix-26.1-11347
(Hebert et al., 2003). The figure has to be carefully taken into consideration because it does not represent a full bibliometric analysis as many
articles do not include barcoding keywords in their title or abstracts
(see Fig. 1 caption for more details), making this schematization certainly incomplete. However, Fig. 1 clearly shows that DNA barcoding
in vertebrates is still largely diffused among fishes (probably for their
importance in the global food market and for the frequent occurrence
of frodes, mislabelling, species substitution to which they are subjected, see for instance Barbuto et al., 2010), whereas this tendency is not
found in other vertebrates.
The DNA barcoding of mammals is ongoing under the auspices of
the iBOL. According to the BOLD System (http://www.boldsystems.
org) at the end of May 2015 about 2850 mammal species have been barcoded, and at least 300 unnamed clusters (i.e. not assigned taxonomic
rank) are recognised on MammaliaBoL. In Fig. 2, the DNA barcoding coverage in mammal known species is plotted. As a consequence,
given the 7000 presumed mammal species, there are DNA barcodes
for about 45% of them. This also means that even if we believe in the
species discovery power of DNA barcoding, it is difficult to think that
this would be the main support for the mammal initiative. It could be
a relevant drive in other animals, but not in mammals. In the modern
taxonomy, identification and classification are two different processes
(Casiraghi et al., 2010) and in mammals the main problem is related
to the phylogenetic reconstruction, that is not, in a strict sense, DNA
barcoding (Rodrigues et al., 2011; Huang et al., 2012).
DNA barcoding is more than a simple identification system and its
major strength is beyond the discrimination power. In this context,
DNA barcoding in mammals moved forward from the identification,
becoming a “service system” useful for several aspects originating from
taxonomy, but being relevant in other areas of the biology of mammals,
ranging from distribution to behaviour and conservation.
So, the time is ripe to ask a fundamental question: do we still need
DNA barcoding in mammals? We wrote our essay to solve this ques27th June 2015
26(1): 13–24
Figure 1 – A schematic overview of the tendencies in published papers on DNA barcoding in vertebrates from the beginning of the initiative (2003) to the end of 2014. Please note that
the graphic is not exhaustive and it has been generated interlinking different keywords searches on ISI WEB of Science. Mammalia: barcode mammals; barcoding mammals; barcode
mammal; barcoding mammal; barcoding mammalia; barcode mammalia. Aves: barcode bird; barcoding bird; barcode birds; barcoding birds; barcoding aves; barcode aves. Amphibia:
barcode amphibian; barcoding amphibian; barcode amphibians; barcoding amphibians; barcoding amphibia; barcode Amphibia. Reptilia: barcode reptiles; barcoding reptile; barcode
reptiles; barcoding reptiles; barcoding reptilia; barcode reptilia. Fish: barcoding fishes; barcode fishes; barcoding cartilaginous fish; barcode cartilaginous fish; barcoding fish; barcode
fish; barcoding Agnatha; barcode Agnatha; barcoding Osteichthyes; barcode Osteichthyes; barcoding bony fishes; barcode bony fishes.
tion, and the different sections listed below are the different answers we
can give.
The importance of reference databases
In DNA barcoding, the identification procedure involves the assignment of taxonomic names to unknown specimens using a DNA reference library of vouchers, previously identified trough different criteria.
Such reference accessions and the international platforms in which they
are organized, constitute the scaffold of the DNA barcoding initiative. Reference DNA barcodes often derive from natural history museums or private collections (Puillandre et al., 2012) as the role of these
institutions has always been that of storing, univocally labelling and
sharing the reference biological material for taxonomists. In the notmolecularized biology, most of the work of taxonomists was entirely
based on the comparison between newly collected or already archived
material and the one of other collections. In the case of mammals,
one of the main challenges for a taxonomist relies on the fact that the
largest reference collections are scattered among museums. This generated some paradoxes with researchers working in tropical biodiversity
hotspots that have to move to North America and Europe to examine
the largest collections of mammals inhabiting their own species-rich
areas (Francis et al., 2010).
The advent of DNA barcoding moved forward allowing contemporary taxonomists to make comparisons with other taxonomic material,
even at a distance with consequent benefits in terms of time and resources saved. In addition, ongoing improvements in molecular technology permit to cheaply obtain high quality sequences from very small
and long-time preserved tissue samples like those stored in museums
(Mitchell, 2015). These advances boosted the researches in mammalogy for several reasons. First, the possibility of confirming the identification of specimens through DNA barcodes allows museums to establish reference collections that can serve as a basis for future research including the description of new biological entities (Puillandre
et al., 2012). Second, the standardized molecular reexamination of
museum-deposited voucher specimens and the comparison with other
reference data permits to rapidly “flag” the identification mistakes typ14
ically occurring during field surveys. As pointed out by Francis and
co-workers 2010, field determinations for many mammal species are
difficult, because they require the analysis of internal morphology (e.g.,
skull or dentition) and are often biased by age/sex variations, undescribed/extralimital species and lack of comparative material. Finally,
the digital nature of genetic information (the so-called “computerization” sensu Casiraghi et al., 2010) makes DNA barcoding data readily
comparable through publicly accessible online databases thus providing a wide panel of potential applications ranging from progresses in
taxonomy to the fields of forensics and food traceability (see dedicated
paragraphs of this review).
Concerning this last point, in the framework of the International Barcode of Life (iBOL) initiative, the building of a comprehensive public
library of DNA barcodes, the Barcode of Life Data System (BOLD),
was launched to provide a global identification system freely accessible
(Ratnasingham and Hebert, 2007, 2013). This platform consists of several components, among which the Identification Engine tool (BOLDIDS) is one of the most useful. BOLD-IDS provides a species identification tool that accepts DNA barcode sequences and returns a taxonomic
assignment at the species level whenever possible.
Unlike other international sequence databases (such as EMBL and
GenBank), BOLD has a quality control system built in, and specific information is required to store and publish a specimen or barcode. To
be included in BOLD, specimens have to be properly vouchered following the protocol specified by the Global Registry of Biodiversity
Repositories (http://grbio.org), and the data standards for BARCODE
Records (Hanner, 2009). Moreover, required details on the sample include the collection date and location with GPS coordinates, and the
PCR primers used to generate the sequences. Finally, submission of
the original trace files is also needed. Noteworthy, barcode sequences
in BOLD are associated with specimen records linked to institutional
(e.g., museum) material making them the most valuable among putative reference accessions.
The accuracy of DNA barcoding species assignment relies upon the
level of taxonomic representation for each group of metazoans and the
amount of intraspecific genetic diversity represented in the databases
(Gaubert et al., 2014).
DNA barcoding of mammals
In the case of mammals, assembling a reference database of DNA
barcode sequences is fundamental for the goals of the iBOL initiative,
also considering that the rate of species discovery within this class has
recently accelerated due to the growing use of molecular techniques
(Reeder et al., 2007).
Differently from larger DNA barcoding campaigns focusing on
fishes (i.e., FISH-BOL, Becker et al., 2011), birds (i.e., ABBI, Hebert et
al., 2004), insects (Jinbo et al., 2011) and others, there have only been a
few references on mammals, generally focusing on a limited number of
taxa or geographic areas. As of 2015, more than 69000 barcode mammalian sequences from over 2800 species have been archived in BOLD
with more than 50% assembled at the Biodiversity Institute of Ontario
in collaboration with the Royal Ontario Museum (ROM) and other institutions. The most part of these data belong to bats, rodents and primates from the Neotropical Region and other tropical biodiversity hotspots (Lim, 2012 and Fig. 2).
To date, the largest published studies on mammals DNA barcoding
are those by Francis et al. (2010) and Clare et al. (2011), where the
authors examined 1896 specimens belonging to 157 species from the
South East Asia and 9076 specimens belonging to 163 species from the
Neotropics respectively. Table 1 provides an updated list of the major
studies that contributed to populate the current reference DNA barcoding database for mammals. Although most of these are limited to a reduced number of species or geographical extent, they are important in
Figure 2 – Overview of the Mammalian DNA barcoding initiative showing the distribution of barcoded species in the different orders. Data on described species is derived from Integrated
Taxonomic Information System (ITIS, http://www.itis.gov). Data on barcoded species is derived from the Barcode of Life Data Systems (BOLD System, http://www.boldsystems.org). In a)
the number of species described and barcoded is plotted in the various mammal orders. In b) the percentage of species described and barcoded is plotted in the various mammal
orders. Dotted line: described species (number or percentage). Continuous line: species with a DNA barcode.
15
26(1): 13–24
filling the gaps of knowledge for many taxonomic groups, discovering
new species or lineages and enabling potential effective conservation
planning. The availability of a public database of reference specimens
and related genetic data of mammal species is also at the base of wildlife forensics as for example recommended by the International Society
for Forensic Genetics Commission (Linacre et al., 2011; Johnson et al.,
2014).
Increasing knowledge on biology, distribution
and conservation
As a matter of fact, the primary role of DNA barcoding in mammals has
been so far, and will long remain, the identification of known species
and one of the most rapid approaches to detect new ones, the so-called
“DNA barcoding sensu stricto”. Table 1 provides a list of case studies where DNA barcoding was successfully used in many application
contexts to identify mammal species.
However, the “sensu lato” face of the approach (see Casiraghi et al.,
2010), is even more interesting as it provides new information on the
biology, distribution and conservation of mammals.
First of all, DNA-based techniques and consequently DNA barcoding are valid data generators to increase the existing knowledge on rare
or poorly investigated taxa. In most cases, the analysis of barcode sequences allowed to confirm the occurrence of certain species in areas
out of their known distributional range such as bats (e.g., De Pasquale
and Galimberti, 2014) and Artiodactyla (e.g., Wilsonet al., 2014). The
implications in a context of conservation are numerous and many studies supported the use of DNA barcoding in recognizing rare or elusive mammal species traditionally monitored with expensive field techniques (i.e., direct observations, captures and camera traps). DNA barcoding proved to be more effective in discriminating morphologically
similar species, such as small ungulates and carnivores, which were
difficult to recognize using camera traps (Inoue and Akomo-Okoue,
2015). In these cases, great advantage was provided by the possibility
of identifying species from a part of the animal (i.e., hair/fur, claws, or
skin) or its droppings as well described in recent case studies conducted in Amazonian and other unexplored areas of the planet (Michalski
et al., 2011; De Matteo et al., 2014; Stanton et al., 2014; Inoue and
Akomo-Okoue, 2015).
In other situations, the DNA barcoding approach could flag the occurrence of newly undescribed lineages that are confined to a certain
geographic area or could represent a new taxa. Apart from the light
and shadows of the method in a pure taxonomic context, an aspect of
primary importance is the possibility of rapidly detecting putative units
deserving further investigations to characterize their ecology, distribution and conservation status. Such kind of approach is fundamental to
plan early and effective conservation strategies. Several studies proved
the role of DNA barcoding in this framework such as in the case of
Italian echolocating bats (Galimberti et al., 2012b) where the authors
found, starting from DNA barcoding, a new well diverged lineage of
Myotis nattereri in Southern Italy and several less divergent lineages
within M. bechsteinii and Plecotus auritus from different areas of the
Peninsula. A greater diversity was also found within neotropical bats
in which Clare and colleagues 2011 found supported evidence of the
existence of previously undescribed lineages for at least 44 species out
of the 163 examined by DNA barcoding.
Invaluable data on mammal ecology and their conservation also derive from the characterization of their diets which has been conducted in many cases with a DNA barcoding approach. Understanding
trophic interactions is fundamental also to assess the importance of certain species for ecosystems functioning and how they respond to variation (Clare et al., 2014a). The recent exploitation of High Throughput
DNA Sequencing techniques (see below) allowed to characterize mixed
DNA samples (e.g., stomach contents or faecal samples) and to identify
the preys consumed by a given predator (Boyer et al., 2015). Such analyses revealed for example temporal and spatial variation patterns in the
use of arthropod resources by different bat species (Clare et al., 2014b;
Rasgour et al., 2011; Alberdi et al., 2012; Vesterinen et al., 2013; Hope
et al., 2014) or diet differentiation between species and/or during dif16
ferent phenological periods (Bohmann et al., 2011; Burgar et al., 2014;
Krüger et al., 2014a,b; Sedlock et al., 2014).
In conclusion, we are now aware that in mammals, even more than
in other animals, we need to collect complementary data to better understand their biology. The system generated by DNA barcoding has
the possibility to rapidly increase these knowledge.
Forensic applications
Given its peculiarities as a universal identification tool, DNA barcoding
naturally acquired a role of primary importance in forensic (Dawnay
et al., 2007; Iyengar, 2014), including case studies on animal derived
foodstuff (e.g., Barbuto et al., 2010; Galimberti et al., 2013). In particular, wildlife forensic is a wide-ranging discipline covering more
forms of crimes compared to human forensic. Concerning mammals,
typical investigations include: trafficking in live specimens or parts of
them, poaching or hunting out of season, cruelty to animals, habitat
destruction and species substitution of food products (e.g., the bushmeat). These phenomena are of major concern also considering their
economic impact at the global scale. For instance, recent estimates
highlighted that a significant portion of the international trade of wildlife and wildlife products is illegal (i.e., 5–8 billion US $ of the total
6-20 billion US $, Baker, 2008) and includes species that are protected by national laws and international conventions (Eaton et al., 2010).
Given the illicit nature of these activities, it is almost impossible to
monitor and quantify the exact volumes and species involved as well
as the real impact on wildlife populations (Gavin et al., 2010; Conteh
et al., 2015). However, in the last century, the tremendous global collapse of some species that are object of illegal trade confirms the emerging problem of wildlife crimes (see for example the cases of Panthera
tigris and Diceros bicornis which populations have decreased of 90%
and 96% respectively in few decades; Linacre and Tobe, 2011). The
biological material that is traded and analyzed in wildlife forensic is
vast, ranging from whole animals (live, hunted or inadvertently killed)
to skins, skeletons or animal body parts (e.g., meat, horns and teeth)
(Huffman and Wallace, 2012; Johnson et al., 2014). In other cases,
the only available material is blood, hairs and trace DNA or mixtures
of genetic material (Johnson et al., 2014). Apart from clearly unmistakable species (e.g., an elephant tusk or a skin of a big carnivore), the
morphological approach used for identification has usually to be undertaken by an expert mammalogist (Huffman and Wallace, 2012). Also
microscopy of hairs or the analysis of bones require high-skilled experience to achieve a reliable identification, and even so, in some cases
they failed to go further from a general group of putative species (see
examples in Moore, 1988). Indeed, the strong processing of the wildlife raw material that can be finally traded as fillets, powders, potions or
oils, often impedes unequivocal identification with morphology. In addition, both general operators and specialists are sometimes required to
investigate on species that have not previously been studied in a forensic
context and therefore lacks of accurate morphological reference data.
Given these premises, it is clear that universal, fast and accurate
methods of species identification are necessary to improve the ability of
detecting, monitoring and controlling the trade in mammals and other
groups of animals (and their processed products).
In the last decades, the advent of DNA-based technologies revolutionized the field of wildlife forensic as DNA tools offered the possibility of overcoming the limits described above. Concerning species
identification, several approaches and loci were selected, but in the last
10 years, DNA barcoding and the use of the mitochondrial cytochromec-oxidase subunit (i.e. mt-coxI) rapidly affirmed their utility in those
cases involving crimes against mammals. Literature and examples are
numerous, and three main categories of wildlife forensic investigations
where DNA barcoding is successfully adopted can be identified:
Illegal hunting and traceability of wild game
The unregulated hunting of wildlife is an emerging issue as it involves
the harvesting of millions of tons of wild game -– mostly mammals -–
per year (Eaton et al., 2010; Gaubert et al., 2014). Conservation problems are typically referred to the “bushmeat” hunting which includes
Table 1 – Updated list of case studies dealing with mammals DNA barcoding. For each study, the context of application, the taxonomic order of target mammals, the aim of the work and
the number of species involved are reported .
Context
Order
DNA taxonomy
DNA taxonomy
DNA taxonomy
Chiroptera
Chiroptera
various
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
DNA taxonomy
Forensic
Forensic
Forensic
Aim
Characterization of Guyana bat species
Identification of a new species of Malaysian bat
Characterization of small mammal communities of
Suriname
Didelphimorphia Identification of cryptic species of opossum
Primates
Characterization of primates species
Chiroptera
Characterization of Malaysian wolly bats
Chiroptera
Characterization of Southeast Asian bats
Soricomorpha
Characterization of white-toothed shrews from Vietnam
Artiodactyla
Characterization of Tanzanian antelopes
Artiodactyla
Characterization of Chinese bovidae
Chiroptera
Characterization of Neotropical bats
Chiroptera
Characterization of Ecuadorian bats
Soricomorpha
Characterization of shrews from Guinea
Didelphimorphia Characterization of opossum species in Brazilian
Atlantic Rainforest
Cetacea
Characterization of Cetacean species
Rodentia
Characterization of Chinese small mammals
Rodentia
Characterization of species in the Praomyini tribe
Chiroptera
Characterization of Neotropical Myotis bats
Chiroptera
Characterization of Italian echolocating bats
Chiroptera
Charachterization of the Mexican funnel-eared bats
Chiroptera
Characterization of Yucatan phyllostomid bats
Didelphimorphia Characterization of atlantic forest didelphid marsupials
Rodentia
Characterization of minibarcode regions for rodents
identification
Chiroptera
Characterization of genetic diversity of northeastern
Palearctic bats
Rodentia
Characterization of Brazilian Sigmodontine Rodents
various
Identification of marine mammals along the French
Atlantic coast
Chiroptera
Identification of cryptic species in the New World
bat Pteronotus parnellii
Chiroptera
Identification of a new bat species in Vietnam
various
Identification of Brazilian forest mammals
Chiroptera
Identification of cryptic bat species in French
Guiana and Brazil
Primates
Characterization of Peruvian primate species
Chiroptera
Characterization of Kerivoula bats in Thailand
Chiroptera
Identification of Malaysian bat species
Rodentia
Identification of alien Callosciurus squirrels in Argentina
Rodentia
Characterization of Chinese species of Murinae and
Arvicolinae
Artiodactyla
Characterization of Chinese Cervidae
Chiroptera
Characterization of two Southeast Asian Miniopterus species
Rodentia
Characterization of Eurasian Ground Squirrels
various
Traceability of bushmeat origin from Central
African and South American countries
Artiodactyla
Identification of wildlife crime cases in South Africa
various
Investigation of illegal hunting cases of Brazilian
wildlife
N°species
References
87
1
74
Clare et al., 2007
Francis et al., 2007
Borisenko et al., 2008
2
50
6
165
6
Cervantes et al., 2010
Nijman and Aliabadian, 2010
Khan et al., 2010
Francis et al., 2010
Bannikova et al., 2011
20
18
163
45
10
2
Bitanyi et al., 2011
Cai et al., 2011
Clare, 2011
McDonough et al., 2011
Jacquet et al., 2012
Sousa et al., 2012
61
11
40
18
31
2
20
11
Viricel and Rosel, 2012
Lu et al., 2012
Nicolas et al., 2012
Larsen et al., 2012
Galimberti et al., 2012b
López-Wilchis et al., 2012
Hernández-Dávila et al., 2012
Agrizzi et al., 2012
103
Galan et al., 2012
38
Kruskop et al., 2012
45
Müller et al., 2013
15
Alfonsi et al., 2013
1
Clare et al., 2013
1
7
2
Kruskop and Borisenko, 2013
Cerboncini et al., 2014
Thoisy et al., 2014
2
7
9
5
Ruiz-García et al., 2014
Douangboubpha et al., 2015
Wilsonet al., 2014
Gabrielli et al., 2014
54
Li et al., 2015b
21
2
Cai et al., 2015
Li et al., 2015a
16
12
Ermakov et al., 2015
Eaton et al., 2010
2
2
Dalton and Kotze, 2011
Sanches et al., 2012
17
26(1): 13–24
Table 1 – Updated list of case studies dealing with mammals DNA barcoding. For each study, the context of application, the taxonomic order of target mammals, the aim of the work and
the number of species involved are reported (continued).
Context
Order
Aim
Forensic
Forensic
Forensic
Artiodactyla
various
Primates
Forensic
Forensic
Forensic
Artiodactyla
various
Artiodactyla
Forensic
various
Non-invasive
sampling
Non-invasive
sampling
Non-invasive
sampling
Non-invasive
sampling
Non-invasive
sampling
Parasitology investigation
Artiodactyla
Carnivora
Identification of African bushmeat items
Identification of organs of threatened species
Identification of primate bushmeat in GuineaBissau markets
Traceability of animal horn products in China
Authentication of South African wild meat products
Identification of ungulates used in traditional
chinese medicine
Development of a traceability system for African
forest bushmeat
etection of Kenyan mountain bongo from faecal
samples
Identification of Carnivore species from faecal
samples
Identification of felid species from scat samples
various
References
15
10
6
Bitanyi et al., 2013
Luo et al., 2013
Minhós et al., 2013
10
10
8
Yan et al., 2013
D’Amato et al., 2013
Chen et al., 2015
59
Gaubert et al., 2014
1
Faria et al., 2011
33
Chaves et al., 2012
4
De Matteo et al., 2014
Species identification from faeces
14
Inoue and Akomo-Okoue, 2015
various
Species identification from blowfly guts content
40
Lee et al., 2015
various
Identification of bloodmeal hosts of ectoparasite
species
Identification of bloodmeal African hosts of tsetse
flies
Identification of bloodmeal hosts of biting midges
16
Alcaide et al., 2009
7
Muturi et al., 2011
3
Lassen et al., 2011
Development of a rapid diagnostic approach to
identify bloodmeal hosts of mosquitoes
Identification of bloodmeal hosts of ticks
5
Thiemann et al., 2012
10
Gariepy et al., 2012
Carnivora
various
various
various
various
most mammals. Although considered illegal, the bushmeat hunting is
an increasing economic activity in many countries among which Western and central Africa and other tropical regions (Nasi et al., 2008). In
these countries the practice has historically been conducted for subsistence consumption or for local trade and now has reached unsustainable
levels (Jenkins et al., 2011; Harrison et al., 2013; Borgerson, 2015).
Several studies, recently examined the utility of DNA barcoding as
a standard tool to monitor the traffic of mammals (i.e., whole animals,
meat, and other products), with particular emphasis on species commonly traded in bushmeat markets or to determine the species of unknown samples deriving from local cases of poaching or species substitution (see for example Eaton et al., 2010; Dalton and Kotze, 2011;
Gaubert et al., 2014). These studies encompassed different groups of
mammals such as: bovids (Bitanyi et al., 2011; Cai et al., 2011), suids
(Eaton et al., 2010) and primates (Minhós et al., 2013) or covered a
wider panel of taxa in an attempt to generate reference datasets for
future applications. Concerning this last category, a clear example
is given by the DNABUSHMEAT dataset developed by Gaubert and
colleagues (2014). Four mitochondrial gene fragments (including the
barcode coxI), were sequenced in more than 300 African bushmeat
samples belonging to nine orders and 59 species. Sequences were then
included as references in a query database, called DNABUSHMEAT,
which provides an efficient DNA typing decision pipeline to trace the
origin of bushmeat items. The DNABUSHMEAT project also contributed in filling the existing gap of African mammals representations in
the international archives (i.e., NCBI and BOLD). The availability of a
well populated reference dataset is a necessary condition for a successful application of DNA-based identification techniques. The relevance
of reference databases has been underlined in recent studies, where a
18
N°species
DNA barcoding survey on bushmeat food items traded in Tanzania (Bitanyi et al., 2013) and South Africa (D’Amato et al., 2013) revealed a
low correctness of species identification by consumers (i.e., 59% of
124 analysed samples, Bitanyi et al., 2013) and a high rate of species
substitution in local markets (i.e., 76.5% of 146 samples, D’Amato et
al., 2013). Such problem is not uncommon in the context of the global
food market and many published works highlighted the suitability of
DNA barcoding in monitoring and hopefully reducing the overexploitation of wildlife species (see for example, Barbuto et al., 2010; Ardura
et al., 2013).
Use of animal parts in traditional medicine
The use of animal organs or parts in traditional medicine involves many
mammalian species that are currently known for their threatened or endangered conservation status. Among the most frequent cases there is
the illegal hunting and trading of rhinoceros horn, saiga antelope horn,
bear bile crystals and many others which are commonly used as ingredients in traditional Asian medicine (Luo et al., 2013; Yan et al., 2013).
Despite the existing international legislation for the safeguard of these
species (i.e., the CITES and the IUCN Red List), the trade of organs
still remains an issue of major concern for wildlife conservation and is
accelerating the extinction of many species.
As reported in several studies, animal organs/parts are usually processed to obtain powder, tablets, capsules and oils (Coghlan et al.,
2012; Cao et al., 2014). Such processes impede any kind of morphological identification and therefore it is almost impossible to set up a
suitable traceability pipeline along the supply chain. A method to characterize the biological origin of processed materials is thus mandatory
to overcome the limits of morphological-based approaches. In recent
years, some studies highlighted the efficacy of DNA barcoding in authenticating mammal traded organs/parts or their occurrence in traditional medicine products (Luo et al., 2013; Yan et al., 2013). Most of
these studies focused on the identification of horns and horn powder,
mainly belonging to Cervidae and Bovidae such as the Saiga antelope
(Saiga tatarica), a protected migratory ungulate living in central Asia
and south-eastern Europe, whose horns are one of the main ingredients of the “Lingyangjiao”, a traditional Chinese remedy (Chen et al.,
2015).
Also in this case, DNA barcoding shows great potentials and should
be considered as a valid tool for enforcing local and international legislation and to prosecute cases of illegal trade of mammal organs/parts.
Pet trade and monitoring of alien species
Another issue of major concern involving wildlife conservation and in
particular mammals is the trade of organisms as pets. Nowadays, the
pet trade is a common pathway of species introduction at the global
scale (Bertolino, 2009; Bomford et al., 2009; Genovesi et al., 2012).
Frequently, traded individuals are able to establish wild populations
as a consequence of either accidental escapes or deliberate releases
thus provoking severe problems to the indigenous communities. As
a matter of fact, the introduction of alien species is one of the most
important causes of biodiversity loss and represents a long-term threat
to ecosystem functioning (Mack et al., 2000; Ehrenfeld, 2010; Strayer,
2012). When monitoring or preventive actions are required to control
the spread of invasive species, as well as tracking their potential pathways of introduction, the first step is the correct identification of the
invasive taxon (Boykin et al., 2012; Pisanu et al., 2013).
In this context, DNA barcoding showed great potential, for instance
in the case of squirrels. Many squirrel species belonging to different
continents have been introduced through the international pet trade for
aesthetic reasons, or to increase hunting opportunities (Long, 2003),
and in most cases they established as successful invaders (Bertolino,
2009; Martinoli et al., 2010). Some studies also suggested a lack
of taxonomic knowledge within this well studied groups of mammals
(Gabrielli et al., 2014; Ermakov et al., 2015). coxI barcode sequences
were used to investigate the taxonomic status of a group of invasive
tree squirrels belonging to the genus Callosciurus introduced in Argentina. Unexpectedly, the captured animals were found to be grouped in
a previously uncharacterized molecular lineage closer to C. finlaysonii
rather than to C. erythraeus as initially expected from morphological
comparisons (Gabrielli et al., 2014). Ermakov and co-workers (2015)
used DNA barcoding to characterize the whole diversity of Eurasian
ground squirrels. They found unexpected levels of coxI divergence in
four species out of the 16 investigated, suggesting the occurrence of
undescribed cryptic species.
In conclusion, the system generated from DNA barcoding is really
useful in the forensic field, and mammals indeed represent a group of
organisms in which this application is really welcomed.
Parasitological analyses
Mammals are the natural hosts for a wide panel of parasites. In a
broader vision, the parasites typically harbored by mammals could be
grouped in macroparasites (e.g., helminths and arthropods) and microbial pathogens (e.g., viruses and bacteria) (Price, 1980; Pedersen et al.,
2007; Hatcher and Dunn, 2011). The attack by one or more group of
parasites can negatively affect the fitness of the host and even cause
significant population declines or boost the extinction risk in already
threatened species (Pedersen et al., 2007). In addition, it has been estimated that since the end of 20th century, at least 75% of the emerging infection diseases for humans were zoonotic (Taylor et al., 2001).
For this reason, the monitoring and control of zoonotic diseases is
nowadays one of the most important concerns in global economies and
human health (Daszak et al., 2000; Chomel et al., 2007; Thompson et
al., 2009; Rhyan and Spraker, 2010). Another factor influencing the
spread of parasites and therefore affecting the conservation status of
mammal species is the interaction of indigenous populations with alien
taxa. Alien species can indeed carry along with them non-indigenous
parasites and these may be transmitted to native species usually lacking
an appropriate defense mechanism (Dunn and Hatcher, 2015; Romeo
et al., 2015).
Knowledge of the exact species of parasite and/or of the mammal
that is carrying harmful pathogens is fundamental to shed light on
the factors influencing the occurrence, proliferation, and transmission
mediated by animal vectors of such agents (Besansky et al., 2003;
Criscione et al., 2005; Kent, 2009). In this framework, molecular methods and in the last decade the DNA barcoding approach, have been playing a key role to understand the complex relationships occurring among
mammal hosts, parasites and their intermediate vectors. Most parasites
are indeed difficult to discriminate based on morphology, for different
reasons (lack of discriminating features, very different life stages, recovery of damaged or partial specimens, see for instance Ferri et al.,
2009). For example in the case of endoparasites, their identification
is often based on post-mortem examination of the hosts, because lessinvasive approaches (e.g., the collection of eggs, larvae or pieces in host
blood, tissue samples or faeces) cannot permit an easier identification
owing to the loss of many diagnostic tracts (Ondrejicka et al., 2014).
DNA barcoding approach contributed to overcome these limits and successful protocols have been developed to identify the principal classes
of parasites affecting mammals such as filarioid nematodes (Ferri et
al., 2009), cestodes (Galimberti et al., 2012a), ticks (Zhang and Zhang,
2014) and mosquitoes (Cywinska et al., 2006). In other cases, DNA
barcoding has been largely applied to identify the mammal hosts of important parasites / pathogens. These case studies especially involved rodent species complexes characterized by a high number of cryptic taxa
inhabiting poorly studied areas of the planet. Specifically, in 2012, Lu
and co-workers, studied the relationships between Rickettsia bacteria
(i.e., the agent responsible for the spotted fever) and ten rodent hosts of
China (Lu et al., 2012). DNA barcoding was used to differentiate host
species and the values of molecular divergence highlighted the need for
further taxonomic investigations on some species groups. Similarly, in
2013, Müller and co-workers used coxI barcode sequences to recognize members of Sigmodontinae subfamily in Brazil which are reservoirs of zoonoses including arenaviruses, hantaviruses, Chagas disease
and leishmaniasis (Müller et al., 2013).
One of the most innovative applications of DNA barcoding in the
study of host-parasite interactions is the characterization of insect
bloodmeals. As a matter of fact, most zoonoses are likely to be vectorborne by blood-feeding arthropods (Jones et al., 2008) which dictate the
relationship between host and pathogen (Thiemann et al., 2012). Blood
feeding vectors may transmit agents responsible for emerging diseases
such as malaria, viral encephalitis, West Nile virus, Chagas disease,
Lyme disease or African sleeping sickness (Kent, 2009). By studying
arthropods behaviour, it has been possible to understand the evolution
of host specificity between vertebrates and their ectoparasites, how the
host choice drives pathogen transmission, and the economic and demographic impacts of ectoparasite infestations on wildlife and domestic
livestock (Kent, 2009). A deep knowledge of these factors can help
improving reliable disease risk models to be used in veterinary and
public health contingency plans (Kent, 2009; Gomez-Diaz and Figuerola, 2010; Collini et al., 2015). Several DNA barcoding-based surveys
have been conducted in the last years to fill the gaps in the comprehension of such dynamics. Published studies involved a specific group of
blood-feeding arthropods such as Culex spp. mosquitoes (Muños et al.,
2012; Thiemann et al., 2012), ticks (Gariepy et al., 2012; Collini et al.,
2015), biting midges (Lassen et al., 2011), tsetse flies (Muturi et al.,
2011) as well as the simultaneous analysis of a wide range of vectors
(Alcaide et al., 2009).
In all of these case studies, the analysis of coxI barcode sequences
obtained from the bloodmeal consumed by hematophagous vectors allowed to trace the identity of the “last supper” (i.e., the vertebrate host
– often a mammal) on which the vector fed before being collected. Finally, in a recent study conducted in Peninsular Malaysia, a biodiversity
hotspot, Lee and colleagues (2015) proposed the DNA barcoding analysis of the stomach content of the saprophagous / coprophagous blow19
26(1): 13–24
flies (Calliphoridae) as a suitable, fast and economic tool to characterize the mammal biodiversity of a study area.
In conclusion, the analysis of parasites is a complex matter and molecular tools, like DNA barcoding, are really welcomed.
Massive DNA sequencing
In the last decade, there has been a great revolution in DNA sequencing technologies. The introduction of the so-called “Next Generation
Sequencing”, NGS, also better defined as “High Throughput DNA Sequencing”, HTS, expanded the universe of DNA sequencing. The rise
of DNA barcoding took place in the same years and it was only a matter of time to assist to the encounter of these two worlds. The DNA
metabarcoding is the result of this marriage (Taberlet et al., 2012). HTS
has revolutionized DNA-based research, especially biodiversity assessment in complex biological matrix (i.e. comprising many species contemporaneously) (Shokralla et al., 2012). In HTS, DNA sequences are
accumulated at an unprecedented rate and it is now possible to analyze simultaneously several samples (through multiplexing) identified
by custom-designed oligonucleotide tags.
The idea is simple: DNA is everywhere, and this molecule is relatively stable and durable in dry, but even wet conditions (Dejean et
al., 2012; Yoccoz et al., 2012). This DNA represents the so-called
“environmental DNA” or eDNA (Shokralla et al., 2012; Thomsen and
Willerslev, 2015). eDNA is formed by short DNA molecules (i.e., free,
cellular debris or particle-bound), which are released by living or dead
organisms. eDNA is typically defined by the process used to collect it,
and this makes its definition in a some way foggy. Much more clear is
the use of eDNA: the living beings present in the environmental sample
are not known and HTS allows to identify them. In addition, even if
DNA in the environment is relatively stable, it is also usually degraded.
In such a condition the classic DNA barcoding approach is often useless, conversely to metabarcoding, due to the possibility of generating
a huge amount of data. The first application in mammals was aimed at
uncovering the diets composition of elusive animals (Valentini et al.,
2009). This approach was successfully adopted in the last 5 years with
some group being very well represented, such as Chiroptera (Bohmann
et al., 2011; Alberdi et al., 2012; Vesterinen et al., 2013; Krüger et al.,
2014a,b; Burgar et al., 2014; Clare et al., 2014a,b; Hope et al., 2014;
Sedlock et al., 2014).
Although it is now relatively simple to characterize the diets of herbivorous and insectivorous mammals, the analysis of diets of carnivores
is really challenging because predator DNA can be simultaneously
amplified with prey DNA (Symondson, 2002; King et al., 2008; Symondson and Harwood, 2014; Boyer et al., 2015). To avoid this problem an interesting approach was the introduction of blocking primers
in the analysis of snow leopard (Panthera uncia) diet (Shehzad et al.,
2012). This molecular approach prevents the amplification of predator
DNA allowing the amplification of the other vertebrate groups.
HTS techniques can also be used to identify elusive mammal species
from the faeces found on the ground (Michalski et al., 2011; Chaves et
al., 2012; Rodgers and Janecka, 2013) or as a general method to identify
mammals in complex mixtures (Foote et al., 2012; Galan et al., 2012;
Deagle et al., 2013; Tillmar et al., 2013). Noteworthy, the possibility of
better defining the areas of distribution of some species with such noninvasive sampling is of particular interest to increase the knowledge of
mammals biology and conservation.
In spite of these practical approaches, HTS techniques in mammals
have also been used to characterize population structure (Rasgour et
al., 2011; Botero-Castro et al., 2013). The rapid developments of these
technologies have created new possibilities to build quickly and costefficiently reference libraries for whole mitochondrial genomes in a
wide range of animal lineages. The accumulation of whole mitogenomes in the public domain covering the Tree of Animal Life will improve our knowledge on evolutionary history of animals and global patterns in genomic features of mitochondria as a sort of future next comprehensive barcode marker.
In conclusion, HTS and the DNA metabarcoding approaches are expanding fields of research that will likely be very fertile for several years
20
to come, particularly considering the rapid increase of reference databases that allows a better characterization of complex cases.
The integrative role of DNA barcoding
As described in the previous sections, DNA barcoding can be successfully involved as a supporting tool for both theoretical and applicative
necessities. The presented case studies highlighted the versatility of
the approach, and the aptitude of being integrated with other sources
of taxonomic information in a highly interconnected environment.
As a matter of fact, species are not unequivocally defined and their
designations based on a single category of taxonomic features (morphological, ecological, molecular, or biogeographic) is questionable.
In this context, molecular techniques and more recently the DNA barcoding, triggered a small revolution inside taxonomy: the process of
identifying biological entities opened the doors to a real integration of
knowledge to improve practical purposes (Unit of Conservation sensu
Dodson et al., 1998) or theoretical approaches (Unit of Evolution or
Evolutionarily Significant Unit, ESU, sensu Ryder, 1986).
In a framework of integration, divergent molecular lineages do not
necessarily reflect distinct species but, in many cases, molecular data
remains at the core of current taxonomic approaches. However, the
future of taxonomy cannot rely only on molecular markers. Rather, it
is more and more oriented towards the definition of the best way to
integrate molecular data into multidisciplinary taxonomic approaches.
In an attempt of providing a better understanding of the possible
taxonomic outcomes deriving from an integrative DNA barcodingbased approach, Galimberti and colleagues recently proposed a schematization using echolocating bats as a model (Galimberti et al., 2012b).
In this schematic view, the taxonomic ranks are grouped based on their
information content: from individuals (i.e., the less informative level),
to species (i.e., the more informative level), passing through intermediate categories defined by the adoption of a single (i.e., morphotype,
Molecular Operational Taxonomic Unit - MOTU and unconfirmed candidate species) or an integrative approach (i.e., Integrative Operational
Taxonomic Units - IOTU, deep conspecific lineage and confirmed candidate species).
Such schematization, tested on Italian bats species, confirmed the
risk of erroneous taxonomic interpretations when molecular entities
(MOTUs) are used as the only criterion (see the case of Eptesicus species in Galimberti et al., 2012b). The authors also proposed a new entity, the IOTU, defined by molecular lineages that have further support
from at least one additional line of evidence. This concept links different data sources in taxonomy, allowing morphological, ecological,
geographical and other characteristics of living beings to be better combined with molecular data. The application of IOTU concept to the
study of echolocating bats showed for example the occurrence a new
undescribed species of Myotis nattereri inhabiting the southern part of
the Italian peninsula.
Known problems of DNA barcoding of mammals
DNA barcoding generated huge controversies, but like any other diagnostic technique it has pros and cons. Since its launch, the practicalities of a universal barcode for all the living beings showed pitfalls,
as firstly dependent on the group of organisms under examination (see
Casiraghi et al., 2010 and Collins and Cruicsshank, 2013 and references therein). Concerning mammals, three main categories of problems should be taken into account when DNA barcoding is applied to
their study. The first concerns the availability of public and well populated reference archives of DNA barcodes and related specimens (see
the dedicated paragraph above). Reference sequences constitute the
main core of the DNA barcoding initiative and their absence or the
lack of control of the correct identification of the source specimens by
expert taxonomists, can irremediably affect the assignment of newly
generated query sequences. The second problem category is directly
related to the processes of molecular evolution, such as the occurrence
of NUMTs (i.e., nuclear copies of mitochondrial DNA). NUMTs are
usually considered a challenge in those case studies based on mtDNA
due to the fact that they can be inadvertently amplified, thus causing
bias in the barcode dataset and in the accuracy of subsequent analyses
(e.g., overestimating intra and interspecific variability levels) (Bensasson et al., 2001; Song et al., 2008; Ermakov et al., 2015). Recently, Ermakov and co-workers (2015), described the amplification of NUMTs
in a species of Eurasian ground squirrel. This is only one of the multiple documented examples of this problem. NUMTs have been found
in over 20 mammalian species belonging to seven different orders (see
(Triant and DeWoody, 2007) for more details). To overcome the risk
of NUMTs interference, Song et al. (2008) and Buhay (2009) suggested step-by-step procedures in order to identify possible pseudogenes.
BOLD itself provides a quality control tool to check sequences for
the presence of stop codons and verify that they derive from coxI by
comparing them against a Hidden Markov Model (Ratnasingham and
Hebert, 2007). To avoid NUMTs interference, Triant and DeWoody
(2007) suggested three alternative strategies: i) the isolation of the
entire mtDNA genome, ii) the use of tissue sources naturally rich in
mtDNA (e.g., liver and muscle), and iii) the use of PCR primers that
amplify substantial portions of the mtDNA molecule (i.e., > 1 kb). In
other cases, the re-extraction of gDNA and the reamplification of the
barcode region can help resolving the matter (Ermakov et al., 2015).
The last group of issues causing failure of DNA barcoding identification are mainly due to the essence of biological species, rather than
in the method, and relies on the criteria adopted to discriminate species. As well as in many other cases, species delimitation in mammals
is based almost completely on two strategies: the genetic distance and
the reciprocal monophyly (Dávalos and Russell, 2014). However, when
dealing with mtDNA, attention is needed when automatically associating divergence values (which are often useful “hypothesis generator”)
with the extent of gene flow. As discussed by Dávalos and co-workers
(2014), such way of thinking can lead to false-positive errors in which
distances or monophyly diagnose species despite ongoing gene flow,
and false-negative errors when gene flow is taken into account despite
its absence. Mitochondrial DNA barcode markers, are indeed prone to
problems such as introgression, incomplete lineage sorting and hybridization and this may generate misleading results particularly in mammals (Heckman et al., 2007; Godinho et al., 2011; Melo-Ferreira et al.,
2012).
In a DNA barcoding study conducted on the whole panel of species
of Eurasian ground squirrels, Ermakov and colleagues (2015), documented the occurrence of mtDNA introgression in four cases due to
ancient hybridization events followed by divergence. Similar conditions have been also detected in other groups of mammals such as bears
(Hailer et al., 2012), marmots (Brandler et al., 2010) and bats (Berthier
et al., 2006; Artyushin et al., 2009).
Moreover, mammals are often characterized by sex-biased gene flow
in which males disperse widely and females exhibit natal philopatry
(Greenwood, 1980). Such condition also shape the genetic structure
of species and populations when maternally-inherited mitochondrial
markers are analysed (Clare, 2011; Dávalos and Russell, 2014). To
overcome this limit of mtDNA, the selection of complementary loci
with independent evolutionary histories can help depicting a more realistic schematization of the divergences at both the intra and interspecific
level. For example, in 2011, Clare published a study in which she successfully compared the phylogeographic patterns revealed through the
maternally inherited mitochondrial coxI and the paternally inherited 7th
intron region of the Dby gene on the Y-chromosome in eight common
Neotropical bat species (Clare, 2011). The combined approach proposed by Clare allowed the author to validate patterns of gene flow and
also to find previously unrecognized species.
Similarly, Silva and coauthors (2014) developed a method based on
polymorphism of the mitochondrial cytb and the nuclear KCAS gene to
identify nine ungulate species occurring in North Africa.
As a final consideration, it is important to underline that when DNA
barcoding investigations reveal the occurrence of new intraspecific lineages, they should be integrated with alternate lines of evidence such
as ecological data, morphology and geography to avoid misinterpretation of genetic variability (Galimberti et al., 2012b). DNA barcoding
problems are well known, but as underlined above, we do not have to
stop at them, and consider the whole system created by this technique.
The future of DNA barcoding of mammals
In spite of an apparent decreasing trend in the rate of publication on the
topic “mammals DNA barcoding” (see Fig. 1), this molecular approach
is still alive and healthy. Probably, this apparent reduction is due to the
fact that the modern taxonomic system is now a matter of fact, and
the DNA barcoding approach is often integrated even without naming
it. Indeed, DNA barcoding does not rely on the use of a monospecific
marker only, as often stated, but is currently referred to as a way of
thinking rather than a name of a technique.
In the case of mammals, DNA barcoding is alive and proactive, because these animals represent the principal group in which the scientific
community moved from a sensu stricto approach to broader applications. Indeed, DNA barcoding sensu stricto is designed for not specialized operators in a certain taxonomic field. Generally speaking,
the specialist does not have real problems to discriminate among the
living beings he/she is studying, because in most cases, he/she himself/herself is the one who created the classification system (hopefully
using a robust integrated approach). Consequently, the specialist is the
principal actor who has to work to create a solid DNA barcoding system to help other users in achieving a correct identification for purposes
ranging from wildlife management, to conservation, eco-ethological
studies and so on.
As we underlined in our essay, in many cases DNA barcoding in
mammals has already reached this level and we foresee that in the next
future this approach will move towards two main branches of application. The first branch (the molecular one) is that of taxonomic studies to
fully uncover the hidden biodiversity within this animal group. On the
other side, even if strictly connected, there will be the branch of “taxonomic services” in which DNA barcoding is one of the more correct,
easier and more sparing (both in terms of money and time) solutions.
References
Agrizzi J., Loss A.C., Farro A.P.C., Duda R., Costa L.P., Leite Y.L. 2012. Molecular diagnosis of Atlantic forest mammals using mitochondrial DNA sequences: didelphid marsupials. Open Zool. J. 5: 2–9.
Alberdi A., Garin I., Aizpurua O., Aihartza J., 2012. The foraging ecology of the mountain
long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes. PLoS One
7(4): e35692.
Alcaide M., Rico C., Ruiz S., Soriguer R., Muñoz J., Figuerola J., 2009. Disentangling
vector-borne transmission networks: a universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals. PLoS One 4(9): e7092.
Alfonsi E., Méheust E., Fuchs S., Carpentier F.G., Quillivic Y., Viricel A., Hassani S., Jung
J.L., 2013. The use of DNA barcoding to monitor the marine mammal biodiversity along
the French Atlantic coast. Zookeys 365: 5–24.
Ardura A., Planes S., Garcia-Vazquez E., 2013. Applications of DNA barcoding to fish
landings: authentication and diversity assessment. ZooKeys 365: 49–65.
Artyushin I.V., Bannikova A.A., Lebedev V.S., Kruskop S.V., 2009. Mitochondrial DNA
relationships among North Palaearctic Eptesicus (Vespertilionidae, Chiroptera) and past
hybridization between Common Serotine and Northern Bat. Zootaxa 2262: 40–52.
Baker C.S., 2008. A truer measure of the market: the molecular ecology of fisheries and
wildlife trade. Mol. Ecol. 17(18): 3985–3998.
Baker R.J., Bradley R.D., 2006. Speciation in mammals and the genetic species concept. J
Mammal. 87: 643–662.
Bannikova A.A., Abramov A.V., Borisenko A.V., Lebedev V.S., Rozhnov V.V., 2011. Mitochondrial diversity of the white-toothed shrews (Mammalia, Eulipotyphla, Crocidura)
in Vietnam. Zootaxa 2812: 1–20.
Barbuto M., Galimberti A., Ferri E., Labra M., Malandra R., Galli P., Casiraghi M., 2010.
DNA barcoding reveals fraudulent substitutions in shark seafood products: the Italian
case of “palombo” (Mustelus spp.). Food Res. Int. 43(1): 376–381.
Becker S., Hanner R., Steinke D. 2011., Five years of FISH-BOL: Brief status report. Mitochondr. DNA 22(S1): 3–9.
Bensasson D., Zhang D.X., Hartl D.L., Hewitt G.M., 2001. Mitochondrial pseudogenes:
evolution’s misplaced witnesses. Trends Ecol. Evol. 16: 314–321.
Berthier P., Excoffier L., Ruedi M., 2006. Recurrent replacement of mtDNA and cryptic
hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proc. R.
Soc. Lond. [Biol] 273: 3101–3109.
Bertolino S., 2009. Animal trade and non-indigenous species introduction: the world-wide
spread of squirrels. Diversity and Distributions 15(4): 701–708.
Besansky N.J., Severson D.W., Ferdig M.T., 2003. DNA barcoding of parasites and invertebrate disease vectors: what you don’t know can hurt you. Trends Parasitol. 19(12):
545–546.
Bitanyi S., Bjørnstad G., Ernest E.M., Nesje M., Kusiluka L.J., Keyyu J.D., Mdegela R.H.,
Røed K.H., 2011. Species identification of Tanzanian antelopes using DNA barcoding.
Mol. Ecol. Resour. 11(3): 442–449.
21
26(1): 13–24
Bitanyi S., Bjørnstad G., Nesje M., Ernest E.M., Mdegela R.H., Røed K.H., 2013. Molecular identification versus local people’s information for accurate estimates of bushmeat
utilization from the Serengeti ecosystem, Tanzania. Afr. J. Biotechnol. 11(1): 243–252.
Bogdanowicz W., Hulva P., Cerná Bolfíková B., Bus M.M., Rychlicka E., Sztencel-Jablonka
A., Cistrone L., Russo D., 2015. Cryptic diversity of Italian bats and the role of the
Apennine refugium in the phylogeography of the western Palaearctic. Zool. J. Linnean
Soc. (Early View) doi:10.1111/zoj.12248
Bohmann K., Monadjem A., Noer C.L., Rasmussen M., Zeale M.R., Clare E., Jones G.,
Willerslev E., Gilbert M.T.P., 2011. Molecular diet analysis of two African free-tailed
bats (Molossidae) using high throughput sequencing. PLoS One 6(6): e21441.
Bomford M., Kraus F., Barry S.C., Lawrence E., 2009. Predicting establishment success
for alien reptiles and amphibians: a role for climate matching. Biol. Invasions 11(3):
713–724.
Borgerson C., 2015. The Effects of Illegal Hunting and Habitat on Two Sympatric Endangered Primates. Int. J. Primatol. 36(1): 74–93.
Borisenko A.V., Lim B.K., Ivanova N.V., Hanner R.H., Hebert P.D., 2008. DNA barcoding
in surveys of small mammal communities: a field study in Suriname. Mol. Ecol. Resour.
8(3): 471–479.
Botero-Castro F., Tilak M.K., Justy F., Catzeflis F., Delsuc F., Douzery E.J., 2013. Nextgeneration sequencing and phylogenetic signal of complete mitochondrial genomes for
resolving the evolutionary history of leaf-nosed bats (Phyllostomidae). Mol. Phylogenet.
Evol. 69(3): 728–739.
Boyer S., Cruickshank R.H., Wratten S.D., 2015. Faeces of generalist predators as “biodiversity capsules”: A new tool for biodiversity assessment in remote and inaccessible
habitats. Food Webs 3: 1–6.
Boykin L.M., Armstrong K.F., Kubatko L., De Barro P., 2012. Species delimitation and
global biosecurity. Evol. bioinform. Online 8: 1–37.
Brandler O.V., Lyapunova E.A., Bannikova A.A., Kramerov D.A., 2010. Phylogeny and
systematics of marmots (Marmota, Sciuridae, Rodentia) inferred from inter-SINE PCR
data. Russ. J. Genet. 46: 283–292.
Buhay J.E., 2009. “COI-like” sequences are becoming problematic in molecular systematic
and DNA barcoding studies. J. Crust. Biol. 29(1): 96–110.
Burgar J.M., Murray D.C., Craig M.D., Haile J., Houston J., Stokes V., Bunce M., 2014.
Who’s for dinner? High-throughput sequencing reveals bat dietary differentiation in a
biodiversity hotspot where prey taxonomy is largely undescribed. Mol. Ecol. 23(15):
3605–3617.
Cai Y., Zhang L., Shen F., Zhang W., Hou R., Yue B., Li J., Zhang Z., 2011. DNA barcoding
of 18 species of Bovidae. Chin. Sci. Bull. 56(2): 164–168.
Cai Y., Zhang L., Wang Y., Liu Q., Shui Q., Yue B., Zhang Z., Li J., 2015. Identification
of deer species (Cervidae, Cetartiodactyla) in China using mitochondrial cytochrome c
oxidase subunit I (mtDNA COI). Mitochondr. DNA 12: 1–4.
Cao M., Wang J., Yao L., Xie S., Du J., Zhao X., 2014. Authentication of animal signatures in traditional Chinese medicine of Lingyang Qingfei Wan using routine molecular
diagnostic assays. Mol. Biol. Rep. 41(4): 2485–2491.
Casiraghi M., Labra M., Ferri E., Galimberti A., De Mattia F., 2010. DNA barcoding: a sixquestion tour to improve users’ awareness about the method. Brief. Bioinform. 11(4):
440–453.
Cerboncini R.A.S., Rubio M.B.G., Bernardi I.P., Braga T.V., Roper J.J., Passos F.C.,
2014. Small mammal community structure and vertical space use preferences in nonfragmented Atlantic Forest. Mammalia 78(4): 429–436.
Cervantes F.A., Arcangeli J., Hortelano-Moncada Y., Borisenko A.V., 2010. DNA barcodes effectively identify the morphologically similar Common Opossum (Didelphis
marsupialis) and Virginia Opossum (Didelphis virginiana) from areas of sympatry in
Mexico. Mitochondr. DNA 21(S1): 44–50.
Chaves P.B., Graeff V.G., Lion M.B., Oliveira L.R., Eizirik E., 2012. DNA barcoding meets
molecular scatology: short mtDNA sequences for standardized species assignment of
carnivore noninvasive samples. Mol. Ecol. Res. 12(1): 18–35.
Chen J., Jiang Z., Li C., Ping X., Cui S., Tang S., Chu H., Liu B., 2015. Identification of
ungulates used in a traditional Chinese medicine with DNA barcoding technology. Ecol.
Evol. 5(9): 1818–1825.
Chomel B.B., Belotto A., Meslin F.X., 2007. Wildlife, exotic pets, and emerging zoonoses.
Emerg. Infect. Diseases 13(1): 6–11.
Clare E.L., 2011. Cryptic species? Patterns of maternal and paternal gene flow in eight
Neotropical bats. PLoS One 6(7): e21460.
Clare E.L., Adams A.M., Maya-Simões A.Z., Eger J.L., Hebert P.D.N., Fenton M.B., 2013.
Diversification and reproductive isolation: cryptic species in the only New World highduty cycle bat, Pteronotus parnellii. BMC Evol. Biol. 13(1): 26.
Clare E.L., Lim B.K., Engstrom M.D., Eger J.L., Hebert P.D., 2007. DNA barcoding of
Neotropical bats: species identification and discovery within Guyana. Mol. Ecol. Notes
7(2): 184–190.
Clare E.L., Lim B.K., Fenton M.B., Hebert P.D., 2011. Neotropical bats: estimating species
diversity with DNA barcodes. PLoS One 6(7): e22648.
Clare E.L., Symondson W.O., Broders H., Fabianek F., Fraser E.E., MacKenzie A.,
Boughen A., Hamilton R., Willis C.K.R., Martinez-Nuñez F., Menzies A.K., Norquay
K.J.O., Brigham M., Poissant J., Rintoul J., Barclay R.M.R., Reimer, J.P., 2014a. The
diet of Myotis lucifugus across Canada: assessing foraging quality and diet variability.
Mol. Ecol. 23(15): 3618–3632.
Clare E.L., Symondson W.O., Fenton M.B., 2014b. An inordinate fondness for beetles?
Variation in seasonal dietary preferences of night-roosting big brown bats (Eptesicus
fuscus). Mol. Ecol. 23(15): 3633–3647.
Coghlan M.L., Haile J., Houston J., Murray D.C., White N.E., Moolhuijzen P., Bellgard
M.B., Bunce M., 2012. Deep sequencing of plant and animal DNA contained within
traditional Chinese medicines reveals legality issues and health safety concerns. PLoS
Genet 8(4): e1002657.
Collini M., Albonico F., Hauffe H.C., Mortarino M., 2015. Identifying the last bloodmeal
of questing sheep tick nymphs (Ixodes ricinus L.) using high resolution melting analysis.
Vet. Parasitol. 210(3–4): 194–205.
Collins R.A., Cruickshank R.H., 2013. The seven deadly sins if DNA barcoding. Mol. Ecol.
Resour. 13(6): 969–975.
Comtet T., Sandionigi A., Viard F., Casiraghi M., 2015. DNA (meta) barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing
aliens. Biol. Invasions 17(3): 905–922.
22
Conteh A., Gavin M.C., Solomon J., 2015. Quantifying illegal hunting: A novel application of the quantitative randomised response technique. Biol. Cons. In press doi:
10.1016/j.biocon.2015.02.002
Criscione C.D., Poulin R., Blouin M.S., 2005. Molecular ecology of parasites: elucidating
ecological and microevolutionary processes. Mol. Ecol. 14(8): 2247–2257.
Cywinska A., Hunter F.F., Hebert P.D., 2006. Identifying Canadian mosquito species
through DNA barcodes. Med. Vet. Entomol. 20(4): 413–424.
D’Amato M.E., Alechine E., Cloete K.W., Davison S., Corach D., 2013. Where is the game?
Wild meat products authentication in South Africa: a case study. Investig. Genet. 4(1):
6.
Dalton D.L., Kotze A., 2011. DNA barcoding as a tool for species identification in three
forensic wildlife cases in South Africa. Forensic Sci. Int. 207(1): e51–e54.
Daszak P., Cunningham A.A., Hyatt A.D., 2000. Emerging infectious diseases of wildlifethreats to biodiversity and human health. Science 287(5452): 443–449.
Dávalos L.M., Russell A.L., 2014. Sex-biased dispersal produces high error rates in mitochondrial distance-based and tree-based species delimitation. J. Mammal. 95(4): 781–
791.
Dawnay N., Ogden R., McEwing R., Carvalho G.R., Thorpe R.S., 2007. Validation of the
barcoding gene COI for use in forensic genetic species identification. Forensic Sci. Int.
173(1): 1–6.
De Matteo K.E., Rinas M.A., Argueelles C.F., Holman B.E., Di Bitetti M.S., Davenport
B., Parker P.G., Eggert L.S., 2014. Using detection dogs and genetic analyses of scat
to expand knowledge and assist felid conservation in Misiones, Argentina. Integr. Zool.
9(5): 623–639.
Deagle B.E., Thomas A.C., Shaffer A.K., Trites A.W., Jarman, S.N., 2013. Quantifying
sequence proportions in a DNA-based diet study using Ion Torrent amplicon sequencing:
which counts count?. Mol. Ecol. Resour. 13(4): 620–633.
Dejean T., Valentini A., Miquel C., Taberlet P., Bellemain E., Miaud C., 2012. Improved detection of an alien invasive species through environmental DNA barcoding: the example
of the American bullfrog Lithobates catesbeianus. J. Appl. Ecol. 49: 953–959.
De Pasquale P.P., Galimberti A., 2014. New records of the Alcathoe bat, Myotis alcathoe
(Vespertilionidae) for Italy. Barbastella 7: 1.
Dodson J.J., Gibson R.J., Cunjak R.A., Friedland K.D., de Leaniz C.G., Gross M.R., Newbury R., Nielsen J.L., Power M.E., Roy S., 1998. Elements in the development of conservation plans for Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 55(Suppl.
1): 312–323.
Douangboubpha B., Bumrungsri S., Satasook C., Wanna W., Soisook P., Bates P.J.,
2015. Morphology, genetics and echolocation calls of the genus Kerivoula (Chiroptera: Vespertilionidae: Kerivoulinae) in Thailand. Mammalia (Ahead of Print)
10.1515/mammalia-2014-0004
Dunn A.M., Hatcher M.J., 2015. Parasites and biological invasions: parallels, interactions,
and control. Trends Parasitol. 31(5): 189–199.
Eaton M.J., Meyers G.L., Kolokotronis S.O., Leslie M.S., Martin A.P., Amato G., 2010.
Barcoding bushmeat: molecular identification of Central African and South American
harvested vertebrates. Conserv. Genet. 11(4): 1389–1404.
Ehrenfeld J.G., 2010. Ecosystem consequences of biological invasions. Annu. Rev. Ecol.
Evol. Syst. 41: 59–80.
Ermakov O.A., Simonov E., Surin V.L., Titov S.V., Brandler O.V., Ivanova N.V., Borisenko,
A.V., 2015. Implications of Hybridization, NUMTs, and Overlooked Diversity for DNA
Barcoding of Eurasian Ground Squirrels. PLoS One 10(1): e0117201.
Faria P.J., Kavembe G.D., Jung’a J.O., Kimwele C.N., Estes L.D., Reillo P.R., Mwangi
A.G., Bruford M.W., 2011. The use of non-invasive molecular techniques to confirm
the presence of mountain bongo Tragelaphus eurycerus isaaci populations in Kenya and
preliminary inference of their mitochondrial genetic variation. Conserv. Genet. 12(3):
745–751.
Ferri E., Barbuto M., Bain O., Galimberti A., Uni S., Guerrero R., Ferté H., Bandi C.,
Martin C., Casiraghi M., 2009. Integrated taxonomy: traditional approach and DNA
barcoding for the identification of filarioid worms and related parasites (Nematoda).
Front. Zool. 6(1): 1–12.
Foote A.D., Thomsen P.F., Sveegaard S., Wahlberg M., Kielgast J., Kyhn L.A., Salling
A.B., Galatius A., Orlando L., Gilbert M.T.P., 2012. Investigating the potential use of
environmental DNA (eDNA) for genetic monitoring of marine mammals. PLoS One
7(8): e41781.
Francis C.M., Kingston T., Zubaid A., 2007. A new species of Kerivoula (Chiroptera: Vespertilionidae) from peninsular Malaysia. Acta Chiropterologica 9(1): 1–12.
Francis C.M., Borisenko A.V., Ivanova N.V., Eger J.L., Lim B.K., Guillén-Servent A.,
Kruskop S.V., Mackie I., Hebert P.D.N., 2010. The role of DNA barcodes in understanding and conservation of mammal diversity in Southeast Asia. PLoS One 5(9): e12575.
Gabrielli M., Cardoso Y.P., Benitez V., Gozzi A.C., Guichón M.L., Lizarralde M.S., 2014.
Genetic characterization of Callosciurus (Rodentia: Sciuridae) Asiatic squirrels introduced in Argentina. Ital. J. Zool. 81(3): 328–343.
Galan M., Pagès M., Cosson J.F., 2012. Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. PLoS One
7(11): e48374.
Galimberti A., De Mattia F., Losa A., Bruni I., Federici S., Casiraghi M., Martellos S.,
Labra M., 2013. DNA barcoding as a new tool for food traceability. Food Res. Int. 50(1):
55–63.
Galimberti A., Romano D.F., Genchi M., Paoloni D., Vercillo F., Bizzarri L., Sassera D.,
Bandi C., Genchi C., Ragni B., Casiraghi M., 2012. Integrative taxonomy at work: DNA
barcoding of taeniids harboured by wild and domestic cats. Mol. Ecol. Resour. 12(3):
403–413.
Galimberti A., Spada M., Russo D., Mucedda M., Agnelli P., Crottini A., Ferri E., Martinoli
A., Casiraghi M., 2012. Integrated operational taxonomic units (IOTUs) in echolocating
bats: a bridge between molecular and traditional taxonomy. PLoS One 7(6): e40122.
Gariepy T.D., Lindsay R., Ogden N., Gregory T.R., 2012. Identifying the last supper: utility
of the DNA barcode library for bloodmeal identification in ticks. Mol. Ecol. Resour.
12(4): 646–652.
Gaubert P., Njiokou F., Olayemi A., Pagani P., Dufour S., Danquah E., Nutsuakor M.E.K.,
Ngua G., Missoup A.D., Tedesco P., Dernat R., Antunes A., 2014. Bushmeat genetics:
setting up a reference framework for the DNA typing of African forest bushmeat. Mol.
Ecol. Resour. 15(3): 633–651.
Gavin M.C., Solomon J.N., Blank S.G., 2010. Measuring and monitoring illegal use of
natural resources. Conserv. Biol. 24(1): 89–100.
Genovesi P., Carnevali L., Alonzi A., Scalera R., 2012. Alien mammals in Europe: updated
numbers and trends, and assessment of the effects on biodiversity. Integr. Zool. 7(3):
247–253.
Godinho R., Llaneza L., Blanco J.C., 2011. Genetic evidence for multiple events of hybridization between wolves and domestic dogs in the Iberian Peninsula. Mol. Ecol. 20(24):
5154–5166.
Gomez-Diaz E., Figuerola J., 2010. New perspectives in tracing vector-borne interaction
networks. Trends Parasitol. 26(10): 470–476.
Greenwood P.J., 1980. Mating systems, philopatry and dispersal in birds and mammals.
Anim. Behav. 28(4): 1140–1162.
Hailer F.V., Kutschera E., Hallstrom B.M., Klassert D., Fain S.R., Leonard J.A., Arnason
U., Janke A., 2012. Nuclear genomic sequences reveal that polar bears are an old and
distinct bear lineage. Science 336: 344–347.
Hajibabaei M., Singer G.A., Hickey D.A., 2006. Benchmarking DNA barcodes: An assessment using available primate sequences. Genome 49: 851–854.
Hanner R., 2009. Data Standards for BARCODE Records in INSDC (BRIs). Available from
http://barcoding.si.edu/PDF/DWG_data_standards-Final.pdf Accessed 15.05.15.
Harrison R.D., Tan S., Plotkin J.B., Slik F., Detto M., Brenes T., Itoh A., Davies S.J., 2013.
Consequences of defaunation for a tropical tree community. Ecol. Lett. 16(5): 687–694.
Hatcher M.J., Dunn A.M., 2011. Parasites in ecological communities: from interactions to
ecosystems. Cambridge University Press, Cambridge.
Hebert P.D.N., Cywinska A., Ball S.L., deWaard J.R., 2003. Biological identifications
through DNA barcodes. Proc. R. Soc. Lond. [Biol] 270(1512): 313–321.
Hebert P.D.N., Stoeckle M.Y., Zemlak T.S., Francis C.M., 2004. Identification of birds
through DNA barcodes. PLoS Biol. 2(10): e312. 10.1371/journal.pbio.0020312
Heckman K.L., Mariani C.L., Rasoloarison R., Yoder A.D., 2007. Multiple nuclear loci
reveal patterns of incomplete lineage sorting and complex species history within western
mouse lemurs (Microcebus). Mol. Phylogenet. Evol. 43(2): 353-–367.
Hernández-Dávila A., Vargas J.A., Martínez-Méndez N., Lim B.K., Engstrom M.D., Ortega J., 2012. DNA barcoding and genetic diversity of phyllostomid bats from the Yucatán Peninsula with comparisons to Central America. Mol. Ecol. Resour. 12(4): 590–
597.
Hope P.R., Bohmann K., Gilbert M.T.P., Zepeda-Mendoza M.L., Razgour O., Jones G.,
2014. Second generation sequencing and morphological faecal analysis reveal unexpected foraging behaviour by Myotis nattereri (Chiroptera, Vespertilionidae) in winter.
Front. Zool. 11(1): 39.
Huang S., Stephens P.R., Gittleman J.L., 2012. Traits, trees and taxa: global dimensions of
biodiversity in mammals. Proc. R. Soc. Lond. [Biol] 279(1749): 4997–5003.
Huffman J.E., Wallace J.R. 2012. Wildlife forensics: methods and applications (Vol. 6).
John Wiley & Sons.
Inoue E., Akomo-Okoue E.F., 2015. Application of DNA barcoding techniques to mammal
inventories in the African rain forest: droppings may inform us of the owners. Tropics
23(4): 137–150.
Iyengar A., 2014. Forensic DNA analysis for animal protection and biodiversity conservation: A review. J. Nat. Conserv. 22(3): 195–205.
Jacquet F., Nicolas V., Bonillo C., Cruaud C., Denys C., 2012. Barcoding, molecular taxonomy, and exploration of the diversity of shrews (Soricomorpha: Soricidae) on Mount
Nimba (Guinea). Zool. J. Linnean Soc. 166(3): 672–687.
Jenkins R.K., Keane A., Rakotoarivelo A.R., Rakotomboavonjy V., Randrianandrianina F.
H., Razafimanahaka H.J., Ralaiarimalala S.R., Jones J.P., 2011. Analysis of patterns
of bushmeat consumption reveals extensive exploitation of protected species in eastern
Madagascar. PLoS ONE 6(12): e27570. 10.1371/journal.pone.0027570
Jinbo U., Kato T., Ito M., 2011. Current progress in DNA barcoding and future implications
for entomology. Entomol. Sci. 14(2): 107–124.
Jones K.E., Patel N.G., Levy M.A., Storeyard A., Balk D., Gittleman J.L., Daszak P., 2008.
Global trends in emerging infectious diseases. Nature 451: 990–994.
Johnson R.N., Wilson-Wilde L., Linacre A., 2014. Current and future directions of DNA
in wildlife forensic science. Forensic Sci. Int-Gen 10: 1–11.
Kent R.J., 2009. Molecular methods for arthropod bloodmeal identification and applications
to ecological and vector-borne disease studies. Mol. Ecol. Resour. 9(1): 4–18.
Khan F.A.A., Solari S., Swier V.J., Larsen P.A., Abdullah M.T., Baker R.J., 2010. Systematics of Malaysian woolly bats (Vespertilionidae: Kerivoula) inferred from mitochondrial,
nuclear, karyotypic, and morphological data. J. Mammal. 91(5): 1058–1072.
King R.A., Read D.S., Traugott M., Symondson W.O.C., 2008. Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol. Ecol. 17(4): 947–963.
Krüger F., Clare E.L., Greif S., Siemers B.M., Symondson W.O.C., Sommer R.S., 2014a.
An integrative approach to detect subtle trophic niche differentiation in the sympatric
trawling bat species Myotis dasycneme and Myotis daubentonii. Mol. Ecol. 23(15):
3657–3671.
Krüger F., Clare E.L., Symondson W.O., Keišs O., Petersons G., 2014b. Diet of the insectivorous bat Pipistrellus nathusii during autumn migration and summer residence. Mol.
Ecol. 23(15): 3672–3683.
Kruskop S.V., Borisenko A.V., 2013. A new species of South-East Asian Myotis (Chiroptera: Vespertilionidae), with comments on Vietnamese “whiskered bats”. Acta Chiropterologica 15(2): 293–305.
Kruskop S.V., Borisenko A.V., Ivanova N.V., Lim B.K., Eger J.L., 2012. Genetic diversity
of northeastern Palaearctic bats as revealed by DNA barcodes. Acta Chiropterologica
14(1): 1–14.
Kvist S., 2013. Barcoding in the dark? A critical view of the sufficiency of zoological DNA
barcoding databases and a plea for broader integration of taxonomic knowledge. Mol.
Phylogenet. Evol. 69(1): 39–45.
Larsen R.J., Knapp M.C., Genoways H.H., Khan F.A.A., Larsen P.A., Wilson D.E., Baker
R.J., 2012. Genetic diversity of Neotropical Myotis (Chiroptera: Vespertilionidae) with
an emphasis on South American species. PLoS One 7(10): e46578. doi:10.1371/journal.
pone.0046578
Lassen S.B., Nielsen S.A., Skovgård H., Kristensen M., 2011. Molecular identification of
bloodmeals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in
Denmark. Parasitol. Res. 108(4): 823–829.
Lee P.S., Sing K.W., Wilson J.J., 2015. Reading Mammal Diversity from Flies: The Persistence Period of Amplifiable Mammal mtDNA in Blowfly Guts (Chrysomya megacephala) and a New DNA Mini-Barcode Target. PLoS One 10(4): e0123871. doi:
10.1371/journal.pone.0123871
Li S., Sun K., Lu G., Lin A., Jiang T., Jin L., Hoyt J.R., Feng J., 2015. Mitochondrial genetic
differentiation and morphological difference of Miniopterus fuliginosus and Miniopterus
magnater in China and Vietnam. Ecol. Evol. 5(6): 1214–1223.
Li J., Zheng X., Cai Y., Zhang X., Yang M., Yue B., 2015. DNA barcoding of Murinae
(Rodentia: Muridae) and Arvicolinae (Rodentia: Cricetidae) distributed in China. Mol.
Ecol. Resour. 15(1): 153–167.
Lim B.K., 2012. Preliminary assessment of Neotropical mammal DNA barcodes: an underestimation of biodiversity. Open Zool. J. 5: 10–17.
Linacre A., Tobe S.S., 2011. An overview to the investigative approach to species testing
in wildlife forensic science. Investig. Genet. 2: 2.
Linacre A., Gusmao L., Hecht W., Hellmann A.P., Mayr W.R., Parson W., Prinz M.,
Schneider P.M., Morling N., 2011. ISFG: recommendations regarding the use of nonhuman (animal) DNA in forensic genetic investigations. Forensic Sci. Int-Genet. 5(5):
501–505.
Long J.L., 2003. Introduced mammals of the world. Their History, Distribution and Influence. Wallingford, United Kingdom.
López-Wilchis R., Guevara-Chumacero L.M., Pérez N.Á., Juste J., Ibáñez C., Barriga-Sosa
I.D., 2012. Taxonomic status assessment of the Mexican populations of funnel-eared
bats, genus Natalus (Chiroptera: Natalidae). Acta Chiropterologica 14(2): 305–316.
Lorenz J.G., Jackson W.E., Beck J.C., Hanner R., 2005. The problems and promise of
DNA barcodes for species diagnosis of primate biomaterials. Philos. T. Roy. Soc. B
360: 1869–1878.
Lu L., Chesters D., Zhang W., Li G., Ma Y., Ma H., Song X., Wu H., Meng F., Zhu C.,
Liu, Q., 2012. Small mammal investigation in spotted fever focus with DNA-barcoding
and taxonomic implications on rodents species from Hainan of China. PLoS One 7(8):
e43479. doi:10.1371/journal.pone.0043479
Luo J.Y., Yan D., Song J.Y., Zhang D., Xing X.Y., Han Y.M., Yang M.H., Dong X.P., Peng
C., Chen S.L., Xiao X.H., 2013. A strategy for trade monitoring and substitution of the
organs of threatened animals. Sci. Rep. 3: 3108.
Mack R.N., Simberloff D., Lonsdale M.W., Evans H., Clout M., Bazzaz F.A., 2000. Biotic
invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10(3):
689–710.
Martinoli A., Bertolino S., Preatoni D.G., Balduzzi A., Marsan A., Genovesi P., Tosi G.,
Wauters L.A., 2010. Headcount 2010: the multiplication of the grey squirrel populations
introduced to Italy. Hystrix 21(2): 127-136. doi:10.4404/hystrix-21.2-4463
McDonough M.M., Ferguson A.W., Ammerman L.K., Granja-Vizcaino C., Burneo S.F.,
Baker R.J., 2011. Molecular verification of bat species collected in Ecuador: Results of
a country-wide survey. Occ. Pap. The Museum of Texas Tech University 301: 1–28.
Melo-Ferreira J., Boursot P., Carneiro M., Esteves P.J., Farelo L., Alves P.C., 2012. Recurrent introgression of mitochondrial DNA among Hares (Lepus spp.) revealed by speciestree inference and coalescent simulation. Syst. Biol. 61: 367–381.
Michalski F., Valdez F.P., Norris D., Zieminski C., Kashivakura C.K., Trinca C.S., Smith
H.B., Vynne C., Wasser S.K., Metzger S.P., Eizirik E., 2011. Successful carnivore identification with faecal DNA across a fragmented Amazonian landscape. Mol. Ecol. Resour. 11(5): 862–871.
Minhós T., Wallace E., Da Silva M.J.F., Sá R.M., Carmo M., Barata A., Bruford M.W.,
2013. DNA identification of primate bushmeat from urban markets in Guinea-Bissau
and its implications for conservation. Biol. Conserv. 167: 43–49.
Mitchell A., 2015. Collecting in collections: a PCR strategy and primer set for DNA
barcoding of decades-old dried museum specimens. Mol Ecol. Resour. (Early View)
doi:10.1111/1755-0998.12380
Moore J.E., 1988. A key for the identification of animal hairs. Sci. Justice 28(5): 335–339.
Müller L., Gonçalves G.L., Cordeiro-Estrela P., Marinho J.R., Althoff S.L., Testoni A.F.,
González E.M., Freitas T.R., 2013. DNA barcoding of sigmodontine rodents: identifying wildlife reservoirs of zoonoses. PLoS One 8(11): e80282. doi:10.1371/journal.pone.
0080282
Muñoz J., Ruiz S., Soriguer R., Alcaide M., Viana D.S., Roiz D., Vázquez A., Figuerola J.,
2012. Feeding patterns of potential West Nile virus vectors in South-West Spain. PLoS
One 7(6): e39549. doi:10.1371/journal.pone.0039549
Muturi C.N., Ouma J.O., Malele I.I., Ngure R.M., Rutto J.J., Mithöfer K.M., Enyaru J.,
Masiga D.K., 2011. Tracking the feeding patterns of tsetse flies (Glossina genus) by analysis of bloodmeals using mitochondrial cytochromes genes. PLoS One 6(2): e17284.
doi:10.1371/journal.pone.0017284
Nasi R., Brown D., Wilkie D., Bennett E., Tutin C., van Tol G., Christophersen T., 2008.
Conservation and use of wildlife based resources: the bushmeat crisis. In: Technical
Series no. 33. Secretariat de la Convention sur la diversite biologique, Montreal et Centre
pour la recherche forestiere (CIFOR), Bogor, Indonesia. 50.
Nicolas V., Schaeffer B., Missoup A.D., Kennis J., Colyn M., Denys C., Tatard C., Cruaud
C., Laredo C., 2012. Assessment of three mitochondrial genes (16S, Cytb, CO1) for
identifying species in the Praomyini tribe (Rodentia: Muridae). PLoS One 7(5): e36586.
doi:10.1371/journal.pone.0036586
Nijman V., Aliabadian M., 2010. Performance of distance-based DNA barcoding in the
molecular identification of Primates. C. R. Biol. 333(1): 11–16.
Ondrejicka D.A., Locke S.A., Morey K., Borisenko A.V., Hanner R.H., 2014. Status and
prospects of DNA barcoding in medically important parasites and vectors. Trends Parasitol. 30(12): 582–591.
Pedersen A.B., Jones K.E., Nunn C.L., Altizer S., 2007. Infectious diseases and extinction
risk in wild mammals. Conserv. Biol. 21(5): 1269–1279.
Pisanu B., Obolenskaya E.V., Baudry E., Lissovsky A.A., Chapuis J.-L., 2013. Narrow
phylogeographic origin of five introduced populations of the Siberian chipmunk Tamias
(Eutamias) sibiricus (Laxmann, 1769)(Rodentia: Sciuridae) established in France. Biol.
Invasions 15(6): 1201–1207.
Price P.W. 1980. Evolutionary biology of parasites. Princeton University Press, Princeton,
New Jersey.
Puillandre N., Bouchet P., Boisselier-Dubale M.C., Brisset J., Buge B., Castelin M.,
Chagnoux S., Corbari T.C.L., Lambourdière J., Louzet P., Marani G., Rivasseau A.,
Silva N., Terryn Y., Tillier S., Utge J., Samadi S., 2012. New taxonomy and old collections: integrating DNA barcoding into the collection curation process. Mol. Ecol.
Resour. 12(3): 396–402.
Ratnasingham S., Hebert P.D.N., 2007. BOLD: The Barcode of Life Data System (www.
barcodinglife.org). Mol. Ecol. Notes 7: 355–364.
Ratnasingham S., Hebert P.D.N., 2013 A DNA-Based Registry for All Animal Species:
The Barcode Index Number (BIN) System. PLoS ONE 8(8): e66213. doi10.1371/journal.
pone.0066213
23
26(1): 13–24
Razgour O., Clare E.L., Zeale M.R., Hanmer J., Schnell I.B., Rasmussen M., Gilbert T.P.,
Jones G., 2011. High-throughput sequencing offers insight into mechanisms of resource
partitioning in cryptic bat species. Ecol. Evol. 1(4): 556–570.
Reeder D.M., Helgen K.M., Wilson D.E., 2007. Global trends and biases in new mammal
species discoveries. Occ. Pap. The Museum of Texas Tech University 269: 1–35.
Rhyan J.C., Spraker T.R., 2010. Emergence of diseases from wildlife reservoirs. Vet. Pathol.
47(1): 34–39.
Roca A.L., Georgiadis N., Pecon-Slattery J., O’Brien S.J., 2001. Genetic Evidence for Two
Species of Elephant in Africa. Science 293: 1473–1477.
Rodgers T.W., Janecka J.E. 2013. Applications and techniques for non-invasive faecal genetics research in felid conservation. Eur. J. Wildl. Res. 59(1): 1–16.
Rodrigues A.S., Grenyer R., Baillie J.E., Bininda-Emonds O.R., Gittlemann J.L., Hoffmann
M., Safi K., Schipper J., Stuart S.N., Brooks T., 2011. Complete, accurate, mammalian
phylogenies aid conservation planning, but not much. Philos. Trans. R. Soc. London
[Biol] 366(1578): 2652–2660.
Romeo C., Ferrari N., Lanfranchi P., Saino N., Santicchia F., Martinoli A., Wauters L.A.,
2015. Biodiversity threats from outside to inside: effects of alien grey squirrel (Sciurus
carolinensis) on helminth community of native red squirrel (Sciurus vulgaris). Parasitol.
Res. 114(7): 2621-2628. doi:10.1007/s00436-015-4466-3
Ruiz-García M., Pinedo-Castro M., Shostell J.M., 2014. How many genera and species of
woolly monkeys (Atelidae, Platyrrhine, Primates) are there? The first molecular analysis
of Lagothrix flavicauda, an endemic Peruvian primate species. Mol. Phylogenet. Evol.
79: 179–198.
Ryder O.A., 1986. Species conservation and systematics: the dilemma of subspecies.
Trends Ecol. Evol. 1: 9–10.
Sanches A., Tokumoto P.M., Peres W.A., Nunes F.L., Gotardi M.S., Carvalho C.S., Pelizzon
C., Godoi T.G., Galetti M., 2012. Illegal hunting cases detected with molecular forensics
in Brazil. Investig. Genet. 3(1): 1–5.
Sedlock J.L., Krüger F., Clare E.L., 2014. Island bat diets: does it matter more who you are
or where you live?. Mol. Ecol. 23(15): 3684–3694.
Shokralla S., Spall J.L., Gibson J.F., Hajibabaei M., 2012. Next generation sequencing technologies for environmental DNA research. Mol. Ecol. 21:1794–1805.
Savolainen V., Cowan R.S., Vogler A.P., Roderick G.K., Lane R. 2005. Towards writing the
encyclopedia of life: an introduction to DNA barcoding. Philos. Trans. R. Soc. Lond. B
Biol. Sci. 360(1462): 1805–1811.
Shehzad W., Riaz T., Nawaz M.A., Miquel C., Poillot C., Shah S.A., Pompanon F., Coissac E., Taberlet P., 2012. Carnivore diet analysis based on next-generation sequencing:
application to the leopard cat (Prionailurus bengalensis) in Pakistan. Mol. Ecol. 21(8):
1951–1965.
Silva T.L., Godinho R., Castro D., Abáigar T., Brito J.C., Alves P.C., 2014. Genetic identification of endangered North African ungulates using noninvasive sampling. Mol. Ecol.
Resour. 15(3): 652–661.
Song H., Buhay J.E., Whiting M.F., Crandall K.A., 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes
are coamplified. Proc. Natl. Acad. Sci. USA 105: 13486–13491.
Sousa L.C.C., Gontijo C.M.F., Lacorte G.A., Meireles S.N., Silva A.P., Fonseca C.G.,
2012. Molecular characterization of an opossum Didelphis albiventris (Marsupialia,
Didelphidae) population in an urban fragment of Brazilian Atlantic Rain Forest and
support to species barcode identification. Genet. Mol. Res. 11(3): 2497–2496.
Stanton D.W., Hart J., Vosper A., Kumpel N.F., Wang J., Ewen J.G., Bruford M.W.,
2014. Non-invarive generic identification confirms the presence of the endangered
okapi Okapia johnstoni south-west of the Congo River. Oryx (First View). doi:10.1017/
S0030605314000593
Strayer D.L., 2012. Eight questions about invasions and ecosystem functioning. Ecol. Lett.
15(10): 1199–1210.
24
Symondson W.O.C., 2002. Molecular identification of prey in predator diets. Mol. Ecol.
11(4): 627—641.
Symondson W.O.C., Harwood J.D., 2014. Special issue on molecular detection of trophic
interactions: unpicking the tangled bank. Introduction. Mol. Ecol. 23(15): 3601–3604.
Taberlet P., Coissac E., Pompanon F., Brochmann C., Willerslev E., 2012. Towards
next-generation biodiversity assessment using DNA metabarcoding. Mol. Ecol. 21(8):
2045—2050.
Taylor L.H., Latham S.M., Mark E.J., 2001. Risk factors for human disease emergence.
Philos. Trans. R. Soc. B 356(1411): 983–989.
Thiemann T.C., Brault A.C., Ernest H.B., Reisen W.K., 2012. Development of a highthroughput microsphere-based molecular assay to identify 15 common bloodmeal hosts
of Culex mosquitoes. Mol. Ecol. Resour. 12(2): 238–246.
Thoisy B.D., Pavan A.C., Delaval M., Lavergne A., Luglia T., Pineau K., Ruedi M., Rufray
V., Catzeflis F., 2014. Cryptic diversity in common mustached bats Pteronotus cf. parnellii (Mormoopidae) in French Guiana and Brazilian Amapa. Acta Chiropterologica
16(1): 1–13.
Thompson R.C., Kutz S.J., Smith A., 2009. Parasite zoonoses and wildlife: emerging issues. Int. J. Environ. Res. Public Health 6(2): 678–693.
Thomsen P.F., Willerslev E., 2015. Environmental DNA -– An emerging tool in conservation for monitoring past and present biodiversity. Biol. Conserv. 183: 4–18.
Tillmar A.O., Dell’Amico B., Welander J., Holmlund G., 2013. A universal method for
species identification of mammals utilizing next generation sequencing for the analysis
of DNA mixtures. PLoS One 8(12): e83761. doi:10.1371/journal.pone.0083761
Triant D.A., DeWoody J.A., 2007. The occurrence, detection, and avoidance of mitochondrial DNA translocations in mammalian systematics and phylogeography. J. Mammal.
88(4): 908–920.
Valentini A., Miquel C., Nawaz M.A., Bellemain E., Coissac E., Pompanon F., Gielly L.,
Cruaud C., Nascetti G., Wincker P., Swenson J.E., Taberlet P., 2009. New perspectives in
diet analysis based on DNA barcoding and parallel pyrosequencing: the trnL approach.
Mol. Ecol. Resour. 9(1): 51-–60.
Vesterinen E.J., Lilley T., Laine V.N., Wahlberg N., 2013. Next generation sequencing
of fecal DNA reveals the dietary diversity of the widespread insectivorous predator
Daubenton’s Bat (Myotis daubentonii) in Southwestern Finland. PLoS One 8(11):
e82168. doi:10.1371/journal.pone.0082168
Viricel A., Rosel P.E., 2012. Evaluating the utility of cox1 for cetacean species identification. Mar. Mam. Sci. 28(1): 37–62.
Wilson D.E., Reeder D.M., 2005. Mammal species of the world: a taxonomic and geographic reference. Baltimore, Maryland: Johns Hopkins University Press.
Wilson J.J., Sing K.W., Halim M.R.A., Ramli R., Hashim R., Sofian-Azirun M., 2014.
Utility of DNA barcoding for rapid and accurate assessment of bat diversity in Malaysia
in the absence of formally described species. Genet. Mol. Res. 13(1): 920–925.
Yan D., Luo J.Y., Han Y.M., Peng C., Dong X.P., Chen S.L., Sun L.G., Xiao X.H., 2013.
Forensic DNA barcoding and bio-response studies of animal horn products used in traditional medicine. PLoS One 8(2): e55854. doi:10.1371/journal.pone.0055854
Yoccoz N.G., Brathen K.A., Gielly L., Haile J., Edwards M.E., Goslar T., Von Stedingk
H., Brysting A.K., Coissac E., Pompanon F., Sønstebø J.H., Miquel C., Valentini A.,
De Bello F., Chave J., Thuiller W., Wincker P., Cruaud C., Gavory F., Rasmussen M.,
Gilbert M.T.P., Orlando L., Brochmann C., Willerslev E., Taberlet P., 2012. DNA from
soil mirrors plant taxonomic and growth form diversity. Mol. Ecol. 21(15): 3647–3655.
Zhang R.L., Zhang B., 2014. Prospects of using DNA barcoding for species identification
and evaluation of the accuracy of sequence databases for ticks (Acari: Ixodida). Ticks
Tick Borne Dis. 5(3): 352–358.
Associate Editor: D.G. Preatoni
Volume 26 (1): 25–35, 2015
doi:10.4404/hystrix-26.1-10263
Research Article
Good for management, not for conservation: an overview of research, conservation and management
of Italian small mammals
Sandro Bertolinoa,∗, Paolo Colangelob , Emiliano Moria , Dario Capizzic
a
Department of Agriculture, Forest and Food Sciences, Largo Paolo Braccini 2, 10095 Grugliasco (TO), Italy
b
National Research Council, Institute of Ecosystem Study, Verbania-Pallanza, Italy
c
Regional Park Agency, Latium Region, Via del Pescaccio 96, 00166 Rome, Italy
Keywords:
Biodiversity
Rodentia
Soricomorpha
Erinaceomorpha
legal protection
conservation priorities
impacts
alien species
Article history:
Received: 08 August 2014
Accepted: 10 March 2015
Abstract
Small mammals (Rodentia, Soricomorpha and Erinaceomorpha) play a crucial ecological role for
their distribution and importance in food chains, as well as for being considered environmental
bioindicators. Thus, they represent excellent models for understanding the evolutionary processes
of ecosystems, population dynamics under changing environmental conditions, and habitat vulnerabilities. However, some rodents may help the spread of human diseases and are responsible for
impacts on agriculture, forestry, and ecosystems. Consequently, small mammal species are often
neglected in conservation biology, and only a few of them are protected according to national and
European laws and directives. In this work, we summarize open questions related to Italian small
mammals and analyze conservation issues linked to these species. We address research, management and conservation priorities by considering ongoing activities and the novelties as regards the
taxonomy and zoogeography. In Italy, 39 native species, including four out of six Italian endemic
mammal species and one questioned as native, and 10 alien species are currently included within the
category “small mammals”. Although several studies revealed that small mammals may be heavily
impacted by habitat loss and fragmentation as well as forest management, only three rodents are listed in IUCN red list as “Near Threatened”, the remaining being “Least Concern”. We suggest that
this may be due to the fact that pertinent information, is not translated in assessments in line with
those of other taxonomic groups (e.g. bats). Conservation strategies are still inadequate, impacts
of alien species still partly unknown or neglected. Thus, wide monitoring projects, ecological studies and general public involvement in conservation effort should be implemented, with the aim to
amend national legislation, thus providing native small mammals with adequate protection status.
Introduction
Small mammals represent a polyphyletic assemblage which typically
applies to any non-flying mammal weighing less than a threshold value
(e.g. <1 kg). However, the presence of some rodent species heavier
than 1 kg (e.g. Marmota marmota, Hystrix cristata, Myocastor coypus)
would make it difficult to establish a weight limit. Here, we consider as
“small mammals” all the Soricomorpha, Erinaceomorpha and Rodentia
species present in Italy, regardless of their weight.
Small mammals constitute a key component of ecosystems, contributing to many functions: they can act as seed (Steele et al., 2005) and
fungal spores dispersers (Janos et al., 1995; Bertolino et al., 2004) and
help pollination (Dickman, 1999). Furthermore, most of them are important prey for a wide range of predators and many species are efficient predators themselves (Capizzi and Luiselli, 1996a; Dickman,
1999). Small mammals are also considered as bioindicators of sustainable forest management, as they respond to habitat disturbance (Capizzi
and Luiselli, 1996b; Pearce and Venier, 2005; Leis et al., 2008; Mortelliti et al., 2010, 2011) and to environmental contaminants (Talmage
and Walton, 1991; Shore and Douben, 1994), thus enabling the detection of environmental trends. The interactions between rodents and the
environment are sometimes so deep that these species are considered
as ecosystem engineers for their ability to change the physical states
of the areas where they inhabit (e.g. by burrowing activities of fossor-
∗
Email address: [email protected] (Sandro Bertolino)
doi:10.4404/hystrix-26.1-10263
ial rodents, Meadows and Meadows, 1991, changes in water flow by
beaver dams, Naiman et al., 1986).
On the other hand, some rodent species may have an impact in the
spread of zoonotic diseases and on agriculture production, forestry and
other human activities (e.g. food industries). Furthermore, they may
also negatively affect other species and/or ecosystems (Capizzi et al.,
2014). Therefore, the role of small mammals in providing ecosystem
services is overwhelmed by the fact that few species are regarded as
pests and targeted for control throughout the world, both in native and
introduced ranges (Sieg, 1987; Delibes-Mateos et al., 2011; Capizzi et
al., 2014). This is perhaps the foundation of the perception that most,
if not all, rodent species are pests and do not need any protection. For
this reason, small mammals are often neglected in conservation planning (Amori and Gippoliti, 2000). Among other mammals, carnivores
and artiodactyls receive much more attention than rodents, despite the
latter account for nearly 40% of the world mammal species (Amori and
Gippoliti, 2000). In such a situation, the conservation of these species
is far from being an easy issue, given also that they are rarely taken
into account by the legislation: only very few small mammal species
are currently protected according to national and European laws and
directives.
Within this general framework, aims of our review were to: 1) summarize open issues related to Italian small mammals; 2) analyze conservation issues concerning small mammals to better address conservation priorities; 3) review currently ongoing management activities,
stating whether they are based on documented and/or assumed impacts
19th May 2015
26(1): 25–35
Table 1 – Native Italian small mammals: * endemic species; ** species with a range centred in Italy and extended for a small part to neighbouring countries; *** considered as introduced.
National red list reports the IUCN categories for Italy: LC = Least Concern; NT = Near Threatened; DD = Data Deficient.
Family
Erinaceidae
Talpidae
Soricidae
Sciuridae
Gliridae
Cricetidae
Muridae
Hystricidae
Species
Erinaceus europaeus
Erinaceus roumanicus
Talpa europaea
Talpa romana *
Talpa caeca **
Sorex alpinus
Sorex antinorii **
Sorex minutus
Sorex samniticus *
Suncus etruscus
Neomys anomalus
Neomys fodiens
Crocidura leucodon
Crocidura pachyura
Crocidura sicula *
Crocidura suaveolens
Sciurus vulgaris
Marmota marmota
Dryomys nitedula
Eliomys quercinus
Glis glis
Muscardinus avellanarius
Arvicola amphibius
Arvicola scherman
Chionomys nivalis
Microtus agrestis
Microtus arvalis
Microtus brachycercus *
Microtus liechtensteini
Microtus multiplex **
Microtus savii **
Microtus subterraneus
Myodes glareolus
Apodemus agrarius
Apodemus alpicola
Apodemus flavicollis
Apodemus sylvaticus
Micromys minutus
Hystrix cristata ***
Vernacular name
European hedgehog
White-breasted hedgehog
European mole
Roman mole
Blind mole
Alpine shrew
Valais shrew
Eurasian pigmy shrew
Apennine shrew
White-toothed pygmy shrew
Southern water shrew
Eurasian water shrew
Bicolored shrew
North African white-toothed shrew
Sicilian shrew
Lesser white-toothed shrew
Eurasian red squirrel
Alpine marmot
Forest dormouse
Garden dormouse
Edible dormouse
Hazel dormouse
European water vole
Fossorial water vole
European snow vole
Field vole
Common vole
Calabria pine vole
Liechtenstein’s pine vole
Alpine pine vole
Savi’s pine vole
European pine vole
Bank vole
Striped field mouse
Alpine field mouse
Yellow-necked field mouse
Long-tailed field mouse
Eurasian harvest mouse
Crested porcupine
and identifying future intervention priorities; 4) examine the recent acquisitions in taxonomical and zoogeographical terms; 5) propose legislative measures to promote conservation and management of Italian
small mammals.
1. Are conservation priorities properly set?
More endemic species than all mammals
The list of Italian small mammals was compiled using Amori et al.
(2008) and Rondinini et al. (2013) as references. Currently, 39 native species grouped in seven families are included within the category
“small mammals” in Italy (Tab. 1): Erinaceidae (n=2), Talpidae (n=3),
Soricidae (n=11), Sciuridae (n=2), Gliridae (n=4), Cricetidae (n=11),
Muridae (n=5), and Hystricidae (n=1). According to genetic, archeozoological, and paleontological evidences the crested porcupine Hystrix
cristata could be considered as introduced from North Africa, maybe
as a game species during the Middle ages (Trucchi and Sbordoni, 2009;
Masseti et al., 2010; for a review, see Mori et al., 2013; but see Angelici
et al., 2003 for an alternative hypothesis). The Udine shrew Sorex arunchi is not recognized anymore as a valid species, as morphological
(Wilson and Reeder, 2005) and genetic (Yannic et al., 2012) differences
between this species and the Valais shrew S. antinori are weak. Accordingly, the validity of Arvicola scherman as a proper species is currently
debated, but we retained it in our screening, as no definitive explana26
National Red List
LC
LC
LC
LC
DD
LC
DD
LC
LC
LC
DD
DD
LC
DD
LC
LC
LC
LC
LC
NT
LC
LC
NT
DD
NT
LC
LC
LC
LC
LC
LC
LC
LC
LC
LC
LC
LC
LC
LC
tion has been claimed yet (Kryštufek et al., 2014). Recently, Gippoliti
(2013), in a thoughtful and provocative paper, based on a screening of
the published literature, proposed to increase to 131 species the list of
the Italian mammals, with 20 introduced, and 15 possible endemic species. According to this paper, Italian small mammals would arise to 56
species. Although some of the putative species identified by Gippoliti
(2013) are likely to represent only isolated populations and not good
species, there is no doubt that the current taxonomic knowledge of the
Italian small mammals needs a thorough revision.
Rodents and Soricomorpha include four out of six Italian endemic
mammal species (Tab. 1); the others are the Apennine hare Lepus corsicanus and the Sardinian long-eared bat Plecotus sardus. Three rodents (Eliomys quercinus, Arvicola amphibius, Chionomys nivalis) are
included in the category Near Threatened in the Italian red list (Tab. 1);
however, for five Soricomorpha (Crocidura pachyura, Talpa caeca,
Neomys anomalus, N. fodiens, Sorex antinorii) and one rodent (Apodemus alpicola), the knowledge on abundance and distribution was
considered as being too limited to assess their conservation status and
thus they were included in the category Data Deficient (Fig. 1a). The
Eurasian red squirrel Sciurus vulgaris is still included in the category
Least Concern in the Italian red list, although it is currently threatened
in at least five Italian regions (Piedmont, Liguria, Lombardy, Veneto
and Umbria), where introduced populations of the competitive grey
Small mammals: good for management, not for conservation
duced species (e.g. S. carolinensis) are more safeguarded than native
ones. Only in 2014 the law was amended indicating that introduced
species should be managed toward eradication or control, also removing legal protection to coypu. Indeed, the near endemic blind mole T.
caeca and the rarest (or at least poorly known) Italian voles (A. amphibius, A. scherman and C. nivalis) are excluded from any form of
legal protection, and no permission is required for their numerical control.
Similar gaps, different concerns: the case study of small
mammals and bats
Figure 1 – IUCN Red List categories for a) Italian native small mammals; b) Italian native
small mammals and Chiroptera (in percentages). Number in parentheses are referred to
the number of species with each threat category in each mammal group. LC = Least
Concern; NT = Near Threatened; VU = Vulnerable; EN = Endangered; CR = Critically
Endangered; RE = Regionally Extinct; DD = Data Deficient.
squirrel Sciurus carolinensis are expanding (Martinoli et al., 2010; Bertolino et al., 2014a); therefore, its IUCN status may change in the next
future in the absence of an effective management strategy of the grey
squirrel.
Listing species as “threatened” in the IUCN Red List requires to evaluate the reduction in the geographic range and population size of the
species. These data are in many cases not available for small mammals.
Even the knowledge on the ecology and biology of these species is still
scanty (Amori et al., 2008). Many species are extremely elusive (e.g.
Neomys spp.; Churchfield et al., 2000; Čepelka et al., 2011), hard to
be trapped (e.g. Talpa caeca; Di Febbraro and Loy, 2014), occurring
at low densities (e.g. E. quercinus, Bertolino et al., 2001; S. vulgaris,
Wauters et al., 2008), and/or have nocturnal habits (E. quercinus, Bertolino, 2007; H. cristata:, Mori et al., 2014a), all aspects which make field
studies challenging. This lack of data makes it difficult any quantitative
assessment of populations and geographical ranges; thus, conservation
ranking for this group of species is mainly based on expert judgement
(Temple and Terry, 2007). Bertolino et al. (2014b) proposed a new
ranking system for small mammals, based on their degree of vulnerability and their conservation value, which could be used when species
needs to be evaluated for further investigation or conservation actions.
A legal perspective
From a legal perspective, the currently available tools for species conservation are largely unsatisfactory. For small mammals, Italian national law N. 157/1992 recorded as especially protected (Art. 2.4)
only the species listed in the Bern Convention (Annex II, H. cristata)
and in the Habitat Directive 92/43/CEE (All. IV: Crocidura sicula,
Muscardinus avellanarius, Dryomys nitedula and H. cristata), as well
as those identified as endangered by possible special decrees by the
President of the Council of Ministers. The same Italian law declares
as “protected” all mammals and birds living in Italy. However, these
standards explicitly exclude from the legal protection moles, rats, mice
and, voles (Art. 2.2). Accordingly, the Near Threatened E. quercinus
is excluded from the “especially protected” species, and many intro-
In spite of the same knowledge gaps shared with small mammals, Chiroptera, including 33 species distributed throughout Italy, are especially
protected. All species are listed in both the Bern Convention (Annex
II, with the exception of Pipistrellus pipistrellus) and in the Habitats
Directive (Annexes II and IV), being also especially protected by the
National Law 157/1992. Moreover, Italy adhered to the European Bat
Agreement for the conservation of European bats population, through
the National Law 104/2005. An analytical comparison of Red List Categories assessed for Italian Chiroptera and small mammals (Rodentia,
Soricomorpha and Erinaceomorpha) (Fig. 1b) revealed that: 1) the
relative proportion of Data Deficient species is very similar between
Chiroptera and small mammals (15.1% and 18.4% respectively), and
did not differ statistically (Yates corrected χ2(1) =0.09, p=0.76); 2) The
number of RE (Regionally Extinct) species is only slightly higher for
Chiroptera (1 and 0 respectively); it is noteworthy that the only RE
species is Rhinolophus blasii, a Balcanic species, with only a marginal
occurrence in Italy (Jacobs et al., 2008); 3) building a 2×2 contingency
table with the frequencies of Chiroptera and small mammals species in
the LC (Least Concern) category against those in the remaining threat
categories (i.e. Near Threatened, Vulnerable, Endangered, and Critically Endangered), revealed the presence of statistically significant differences (Yates corrected χ2 =33.5, p<0.0001). Therefore, in spite of
similar knowledge gaps and extinction rates, the allocation of the threat
categories was significantly skewed in favour of bats.
2. A conservation perspective
According to the IUCN assessment, the most important threat to
European terrestrial mammals is habitat loss and degradation, followed
by pollution and human disturbance (Temple and Terry, 2007); habitat
loss is the most severe threat also at the global level followed by human
environmental exploitation (Viè et al., 2009). To evaluate the main
pressure that may affect the Italian small mammals, we checked both
national and global IUCN red lists reporting threat factors identified by
experts for each species.
In detail, Italian threats have been reported only when different from
the global ones (Tab. 2). We also checked the last Italian report
(2013), produced within the framework of the Habitat Directive, which
includes three rodents and one Soricomorpha. Threats are listed for
8 (20.5%) out of 39 species according to the global red list, for 26
(66.7%) according to the Italian red list; respectively, 23 (59.0%) and
10 (25.6%) species are considered not affected by serious threats, and
8 (20.5%) and 3 (7.75%) are listed as data deficient. For two species
(Apodemus alpicola and Arvicola scherman), data are lacking both at
the global and Italian scale.
The main threat is represented by habitat alteration, affecting 18 species (46.2%), immediately followed by environmental pollution, affecting the survival of 14 species (35.9%). The first category includes both
habitat loss and fragmentation, in terrestrial and freshwater environments. For instance, deforestation mainly threaten arboreal species,
such as the red squirrel, edible and hazel dormice (Capizzi et al., 2002,
2003; Mortelliti et al., 2009, 2014; for a review see Mortelliti et al.,
2010), while spatial and temporal allocation of logging may affect the
survival of forest shrews, mice and voles (Capizzi and Luiselli, 1996b;
Mortelliti and Boitani, 2009). Species typical of meadows and prairies (e.g. wild mice, harvest mice and blind moles) are impacted by
mowing and/or cattle grazing or, conversely, by the disappearance of
the pastures because of the re-colonization of the forest. On the other
27
26(1): 25–35
Table 2 – Threat factors listed in the Italian (IT) and global (GL) IUCN red lists and in the last Habitat Directive Assessment (Hab). Threats in the Italian red list are reported only when
different from the global red list. Question marks underline potential threats.
Species
Habitat loss/
fragmentation
Environmental
pollution
Population
control
Threats
Alien
species
Notes
Poaching
IT
Erinaceus europaeus
Erinaceus roumanicus
Talpa europaea
Talpa romana
Talpa caeca
Sorex alpinus
Sorex antinorii
Sorex minutus
Sorex samniticus
IT
IT
IT ?
Suncus etruscus
Roadkilling
No serious
threat
IT ?
GL
IT ?
GL
IT
GL
IT ?
GL
IT
IT ?
GL
No data
Use of biocides and
chemical products in
agriculture (locally)
Use of biocides and
Use of biocides and
GL
Use of biocides
GL
IT
GL
GL
IT
GL
Neomys anomalus
IT ?
IT ?
GL
Neomys fodiens
IT ?
IT ?
GL
Crocidura leucodon
Crocidura pachyura
Crocidura sicula
Crocidura suaveolens
Sciurus vulgaris
GL
IT
IT
IT ?
IT/Hab
IT/Hab
IT
IT
GL
GL
GL
GL/IT
IT
GL/IT
Marmota marmota
Dryomys nitedula
GL/IT
Eliomys quercinus
GL/IT
Glis glis
GL/IT
Muscardinus
avellanarius
Arvicola amphibius
Arvicola scherman
Chionomys nivalis
Microtus agrestis
Microtus arvalis
Microtus brachycercus
Microtus leichtensteini
Microtus multiplex
Microtus savii
Microtus subterraneus
Myodes glareolus
Apodemus agrarius
Apodemus alpicola
Apodemus flavicollis
Hab
GL/IT/Hab
GL/IT
GL
Deforestation and
forest burning
Particularly for
populations in islands
Unknown status for
Sardinian population
Deforestation and
forest burning
Water pollution
GL/IT
IT
GL
GL/IT
GL/IT
IT
GL/IT
GL/IT
GL
GL/IT
Crop damages
GL/IT
GL/IT
GL
IT
GL/IT
GL/IT
Apodemus sylvaticus
IT
Micromys minutus
IT
IT ?
Hystrix cristata
hand, water quality affects the survival of the sensitive water shrews
(Greenwood et al., 2002) and water voles (Barreto et al., 1998; Rushton
et al., 2000), although data for these species from Italy are still lacking. Alien species may also play an important role for the conservation of some small mammal species. Grey squirrels Sciurus carolinensis are replacing the native red squirrel Sciurus vulgaris (Bertolino
et al., 2014a)), while interaction with rats may threaten the survival of
Mediterranean shrew Crocidura pachyura in Pantelleria and possibly
in Sardinia (http://www.iucn.it/scheda.php?id=-344640608). Introduced
28
Use of biocides and
Use of biocides and
water pollution
Use of biocides and
water pollution
Use of biocides
Interaction with rats
Use of biocides
in smaller islands
around Sicily
Use of biocides
Competition with
Sciurus carolinensis
GL
GL
IT
IT
Habitat loss by
cattle grazing
Habitat loss by
mowing
GL
American minks Neovison vison exert a strong predation upon water
voles Arvicola amphibius in Great Britain (Woodroffe et al., 1990;
Rushton et al., 2000); this alien carnivore is also present in at least four
Italian regions (Iordan et al., 2012) where it may affect the local populations of the water vole. Population control regards only the Savi’s
pine vole (Caroli et al., 2000), which exerts damages in orchards and is
not protected by any law. Although legally protected, the crested porcupine is still subjected to a strong local poaching pressure, for both its
meat and damages to crops (Mori et al., 2014b).
Table 3 – Divergent lineages of Italian small mammals.
Species
Localization of divergent lineage
Justification
Erinaceous europaeaus
Restricted to Sicily
Allozimic and molecular data
Talpa caeca
Talpa europaea
Sorex minutus
Neomys fodiens
Sciurus vulgaris
Myodex glareolus
Microtus arvalis
Microtus savii
Arvicola amphibius
Apodemus sylvaticus
Eliomys quercinus
Italian peninsula
Italian peninsula
Italian peninsula
Restricted to Calabria
Northern Italy and Switzerland
Monophyletic lineage restricted to Sicily
Italian peninsula
Monophyletic lineage restricted to Sicily
Italian peninsula, Sicily, Sardinia and Corsica
Chromosome and molecular data
Molecular and morphological data
Molecular and morphological data
Molecular data
Molecular data
Molecular data
Molecular data
Molecular data
Molecular data
Molecular data
Chromosome and molecular data
IUCN red lists are endorsed by the Ministry of Environment and they
are therefore the main reference to evaluate the status of the species.
The lack of data on the population trends prevents a thoughtful assessment for many species. When data are scanty, species may be wrongly
considered safe because there is no indication of decline; nation-wide
monitoring programs on small mammals are still lacking in Italy.
Increasing urbanization, large infrastructure construction, agricultural intensification and widespread habitat erosion in the last decades
have produced a wide-scale land use change to Italian landscape whose
potential effects on local fauna should be investigated. A number of recent studies focused on the effects of forest fragmentation on rodents
(Capizzi et al., 2002, 2003; Mortelliti et al., 2009, 2011, 2014) and
shrews (Mortelliti et al., 2007; Mortelliti and Boitani, 2009) pointing
out that habitat loss negatively affects many species that probably need
protection and management interventions.
3. New discoveries and long-standing issues:
know we do not know?
The contribution of molecular biology to the assessment of diversity of
animal species gave a new boost to different disciplines from taxonomy
and systematics to ecology, biogeography and evolutionary biology.
The increase of genetic studies on mammals has provided a most accurate information on the genetic structure of populations and on evolutionary relationships among taxa. Such information has been used for
the reconstruction of the phylogeographic history of many taxa, as well
as for the identification of cryptic species (Ferguson, 2002).
Molecular techniques proved to be especially useful in the study of
small mammals diversity. Small mammals, representing most of the
total mammalian species described till now (Reeder et al., 2007), still
harbour an undisclosed diversity for the presence of subspecies or populations that will likely be considered as valid species in the future.
Within rodents it has been estimated that many species have still to be
described in the next years (Reeder et al., 2007) and genetics and molecular biology, including the new genomic approaches, will probably
play a fundamental role.
Many recent studies focused on the assessment of genetic diversity
in the South European areas, which played a central role in the colonization and diversification of mammals in Europe (Randi, 2007). In spite
of this, few studies focused on the description of genetic diversity in
Italy, and most studies performed at an European scale took into consideration Italy only marginally (often a few localities in the northern
or central Italy: e.g. Berggren et al., 2005; Ruiz-Gonzalez et al., 2013).
By contrast, a number of recent works raised up the importance of the
genetic study for a better knowledge of taxonomic and genetic diversity
of Italian small mammals (Castiglia et al., 2008; Grill et al., 2009; Vega
et al., 2010; Colangelo et al., 2012; Mouton et al., 2012). The case of
Microtus savii which, as currently defined, is a paraphyletic taxon on
the basis of mtDNA and may include more than one species, is emblematic (Castiglia et al., 2008). The presence of divergent lineages in
Calabria (Southern Italy) was identified both for S. vulgaris (Grill et
Bibliography
Filippucci and Simson, 1996 ; Santucci et al.,
1998; Seddon et al., 2001
Meylan, 1966; Colangelo et al., 2010
Corti and Loy, 1987; Feuda et al., 2015
Vega et al., 2010
Castiglia et al., 2007
Grill et al., 2009
Colangelo et al., 2012
Tougard et al., 2008
Castiglia et al., 2008
Taberlet et al., 1998
Michaux et al., 2005
Gornung et al., 2010
al., 2009) and Myodes glareolus (Colangelo et al., 2012). In particular, the latter species shows a high level of genetic divergence (based on
mtDNA) from other Italian bank voles, hard to be considered only as
intraspecific variability and comparable to levels of genetic divergence
observed among good species within the genus Myodes (Colangelo et
al., 2012). Recent genetic analyses seem to confirm the evidence that
M. glareolus from Calabria should be considered as a distinct species
(Markovà et al., 2014). For many other small mammals, genetic analyses highlighted the distinctiveness of the Italian populations (Taberlet
et al., 1998; Feuda et al., 2015) reinforcing the view of the Italian peninsula as one of the hot-spot of diversity and an endemism-rich area
(Randi, 2007).
More recently, the use of multidisciplinary approaches which combine mitochondrial DNA phylogeography, ecological niche modelling
and morphometrics (Vega et al., 2010) proved to be very useful to give
an insight in mechanisms which originated the diversity of Italian small
mammals. Furthermore, the combination of genetic and morphometrics gives also the opportunity to fill the gaps between the new DNA
taxonomy and the “old” taxonomy, thus potentially allowing the use of
collections available in the Italian and European natural history museums (Gippoliti et al., 2014) which, if possible, should be used as
reference points for the assessment of small mammal diversity. The
description of new species poses also a conservation issue related to
the need to protect those taxa which are restricted endemism, declining, or of an uncertain status and not yet taken into account by national
laws and international directives. The importance of species recognition for conservation purposes is well reflected in recent debates on
the implications of different species concepts for the identification of
conservation units (Gippoliti and Groves, 2013; Gippoliti et al., 2013;
Zachos et al., 2013; Zachos and Lovari, 2013).
Despite the definition of a clear, unambiguous and operatively valid
species concept, remains a central issue in evolutionary biology and
taxonomy, from a conservation perspective, the use of genetic tools to
identify “units of diversity” irrespectively of the taxonomic level (at
species level or below it) for which it is necessary to define conservation actions is more interesting. For this reason, in the last two decades
the concept of Evolutionary Significant Unit (ESU) become central in
conservation biology (Moritz, 1994). The purpose of defining ESUs is
to ensure that evolutionary heritage is recognized and protected (Moritz, 1994) by posing the attention on genetically distinct lineages. By
preserving isolated and diversified lineages, conservation actions can
ensure that the evolutionary potential of a species is preserved. From
this perspective, genetic analyses highlighted how several small mammals lineages from Italy represent distinct lineages (see Tab. 3 and Gippoliti, 2013). Also in absence of a clear taxonomic revision, in many
cases the Italian divergent lineages may represent ESUs of high interest
for the definition of management units for conservation.
29
26(1): 25–35
Table 4 – Small mammals introduced and naturalized in Italy.
Family
Sciuridae
Hystricidae
Cricetidae
Muridae
Myocastoridae
*
Species
Sciurus carolinensis
Callosciurus finlaysonii
Callosciurus erythraeus
Tamias sibiricus
Hystrix cristata*
Ondatra zibethicus
Mus musculus
Rattus norvegicus
Rattus rattus
Myocastor coypus
English name
Eastern grey squirrel
Finlayson’s squirrel
Pallas’s squirrel
Siberian chipmunk
Crested porcupine
Muskrat
House Mouse
Brown rat
Black rat
Coypu
First introduction
1948
1980s
2000s
1980s
Middle Ages
1990s
-6000
1700
-200/-400
1928
Pathways
Pet trade
Pet trade
Pet trade
Pet trade
Game species
Fur farming
Transported by humans
Fur farming
The origin of this species is still debated.
4. Unwanted guests
Rodent invaders: alien species introduction in Italy
Overall, at least 10 rodent species are introduced to Italy, six of them in
the last century (Tab. 4). They represent nearly one third (31%) of the
rodents present in Italy. Ancient introductions are the now ubiquitous
R. rattus and Mus musculus, while R. norvegicus was transported by
humans more recently; Ondatra zibeticus and M. coypus were imported in Europe for fur farming (Amori et al., 2008). The presence of the
coypu in Italy originated from individuals escaped or released from
fur farms, while O. zibeticus spontaneously colonized north-eastern
Italy from Slovenia (Lapini and Scaravelli, 1993). The populations
of three squirrel species originated from animals imported as pets and
then intentionally released or escaped (Bertolino, 2009; Martinoli et al.,
2010). A fourth squirrel species, Callosciurus erythraeus, has been recently discovered in Lombardy (A. Martinoli and L. Wauters personal
communication 2014).
Molecular data may play a pivotal role in integrating ecological
data in the context of biological invasions (Dlugosch and Parker, 2008;
Fitzpatrick et al., 2011; Handley et al., 2011) and in the identification of
introduction dynamics of alien species. Multiple introductions of alien
species pose a major obstacle to eradication programs, by promoting
an increase of genetic diversity and thus of the adaptive potential of
alien species to the newly invaded environment (Alda et al., 2013); this
may represent a crucial issue for species with high reproductive rates,
as small mammals, and particularly for their management as pests. Genetics may reveal the exact geographical origin of alien populations
(Ficetola et al., 2008; Forcina et al., 2012), or specific attribution where
morphology by itself is not enough (Moralee et al., 2000; Allendorf et
al., 2012). For instance, according to genetics, population of grey squirrel in Umbria was founded by translocations of animals from Piedmont,
where the species has been established since 1940s (Signorile et al.,
2014). The anthropogenic origin of the Molara island reinvasion by
R. rattus was established by comparing the DNA of invading with that
of eradicated population (Ragionieri et al., 2013). The historical introduction of R. rattus, which presence was recorded since 3000 b.p.
in the western Mediterranean (Kotsakis and Ruschioni, 1984; Ruffino
and Vidal, 2010), was also investigated by means of mtDNA markers.
Despite the potential multiple introduction expected for this commensal
species, the observed genetic diversity unexpectedly fits with a pattern
of single introduction (Colangelo et al., 2015) opening interesting perspectives in understanding the ecology and ethology of this species.
Knowing the invaders
The impacts the ten rodent species introduced to Italy may exert to ecosystems and human activities are reported with relative references in
Tab. 5. These were divided into five broad categories, considering impacts to (i) native species, (ii) natural vegetation, (iii) agriculture (including arable crops and orchards), (iv) animal husbandry and (v) other
impacts. Finally, the potential for a species to be (vi) vector of parasites and diseases was also considered. Impacts confirmed for Italy are
highlighted in bold. R. rattus, R. norvegicus and M. musculus are characterized by widespread impacts which cover all categories, followed
30
Origin
North America
Asia
Asia
Asia
Africa
North America
Asia
Asia
Indian Peninsula
South America
by S. carolinensis and M. coypus, which may have negative effects on
other animal species, natural vegetation, agriculture, and may also be
reservoir of parasites and pathogens. Myocastor coypus and Ondatra
zibethicus could weaken riverbanks with their burrowing activities; this
impact is especially important for the first species (Panzacchi et al.,
2007). Introduced squirrels may affect forestry and orchards, as well
as other animal species, mainly birds and mammals (Bertolino, 2009;
Bertolino and Lurz, 2013), even replacing native species (i.e. the competition between S. carolinensis and S. vulgaris, Gurnell et al., 2004;
Wauters et al., 2005). For three species, C. erythraeus, Tamias sibiricus, O. zibethicus, no information on the impacts produced in Italy is
available; however, it should be stressed that these species still have a
restricted distribution in the country.
Facing the invader
A national or European strategy aiming at reducing the risks posed by
introduced species should be based on a three-stage hierarchical approach which includes prevention of new introductions, early detection
and rapid response when prevention failed, and a mitigation of impacts
with the eradication, containment or control of populations (Genovesi
and Shine, 2004).
Prevention
Prevention against new introductions should be based on the identification of the pathways of entry (e.g. pet trade, fur farming, escapes from
zoos) and the implementation of effective measures to avoid or reduce
arrivals. For instance the importation of pets followed by either a deliberate release or the escape from captivity is the main source of squirrel
introductions (Bertolino, 2009; Martinoli et al., 2010). A regulation of
the pet trade should thus be considered to avoid a further proliferation
of new species and populations. This has been already done but only
for few species.
The importation of three squirrel species (S. carolinensis, Sciurus
niger, C. erythraeus) in the European Union is suspended since 2012,
after having listed them within the Annex B of the EU Regulation
338/1997 (the European Union Wildlife Trade Regulation that enforces
CITES within the European Union). It is now forbidden to import live
specimens of these species in the EU, even though there are no restrictions to their movement within the boundaries of EU. A further request
aiming to establish restrictions to possession and movement of live specimens within the European countries was denied. A more stringent
regulation has been recently adopted by Italy. A decree signed by the
Ministers of the Environment, Agriculture and Economic Development
and published on 2nd February 2013 in the Official Journal of Italian Republic forbids trading, raising and keeping the three squirrel species.
It should be stressed that the inclusion of few species in these lists
is a reactive approach: species are proposed for trade restriction when
are already established and proven to be invasive. An alternative option is to encourage a voluntary ban of the trade of high-risk species
or to evaluate a complete trade restriction except for authorized species
(Davenport and Collins, 2011; Takahashi, 2006).
Table 5 – Species introduced to Italy and their impacts. References in bold refers to Italian studies; other references are from the international literature.
Species
Native species
Natural
vegetation
(Mayle, 2005)
Agriculture
Sciurus
carolinensis
S. vulgaris
(Gurnell et al.,
2004; Wauters
et al., 2005);
Birds
Callosciurus
finlaysonii
Birds (Bertolino
and Lurz, 2013)
(Bertolino et al.,
2004; Aloise and
Bertolino, 2005)
(Bertolino et al.,
2004; Aloise and
Bertolino, 2005)
Callosciurus
erythraeus
Birds (Bertolino
and Lurz, 2013)
(Bertolino and
Lurz, 2013)
Tamias
sibiricus
Birds?
Ondatra
zibethicus
Invertebrates,
Vertebrates
(Nummi et al.,
2006; Hulme
et al., 2010)
(Skyrienė and
Paulauskas, 2012)
Mus musculus
Invertebrates,
Vertebrates
(Wanless et al.,
2007; Angel
et al., 2009)
(Jones et al.,
2003)
(Brown and
Singleton,1998;
Capizzi and
Santini, 2007)
(Leirs et al., 2004;
Capizzi and
Santini, 2007)
Reservoir of diseases
and parasites infectious
to humans
(Meerburg et al., 2009)
Damage to manufactures
and stored food;
commensal populations
need to be controlled by
rodenticides toxic to non
target species (Capizzi et
al., 2014)
Rattus
norvegicus
Invertebrates,
Vertebrates
(Atkinson, 1985;
Long, 2003)
(Towns et al.,
2006; Harris,
2009)
(Capizzi and
Santini, 2007;
Lambert et al.,
2008)
Capizzi and
Santini, 2007)
to humans
Damage to manufactures
and stored food;
al., 2014)
Rattus rattus
Invertebrates,
Vertebrates
(Baccetti et al.,
2009; Capizzi
et al., 2010;
Long, 2003)
(Towns et al.,
2006; Harris,
2009)
(Horskins et al.,
1998; Capizzi
and Santini,
2007)
Capizzi and
Santini, 2007)
to humans
Damage to electric cable
and other manufactures;
damage to stored food;
al., 2014)
(Santini, 1980)
(Tweheyo et al.,
2005; Capizzi
and Santini,
2007; Mori et
al., 2014b)
(D’Antoni et al.,
2002; Bertolino
et al., 2005)
(Panzacchi et al.,
2007; Bertolino
and Viterbi,
2010)
Reservoir of
Leptospira
(Arcangeli, 2002;
Bollo et al., 2003)
Burrowing can weaken
riverbanks (Panzacchi
et al., 2007)
Hystrix
cristata
Myocastor
coypus
Birds
(Bertolino et al.,
2011; Angelici
et al. 2012)
Animal
husbandry
(Currado, 1993;
Currado et al.,
1997)
Vector of parasites
and diseases
Reservoir of squirrel
poxvirus
(Sainsbury et al., 2000)
Tompkins et al., 2002)
Other impacts
and other manufactures
(Bertolino and Genovesi,
2005)
(Bertolino and Genovesi,
2005)
Vector of parasites
(Bertolino and Lurz,
2013)
(Bertolino and Lurz, 2013)
Reservoir of Borrelia
spp., vector of Lyme
disease (Vourch et al.,
2007)
Reservoir of
Leptospira interrogans,
Francisella tularensis,
Echinococcus
multilocularis
Early detection and rapid response
Early detection of introduced animals is essential to start a rapid action
before significant populations are established. Italy does not have an
early warning system and reaction of authorities is limited, often starting with a large delay. A call for the eradication of the grey squirrel
was published in 1987, the first action plan was prepared in 1997 but it
was stopped by a recourse to the court from animal right groups; a new
management project started only in 2010, 62 year after the first introduction of the species in Italy (Bertolino and Genovesi, 2003; Bertolino
et al., 2014a). The Finlayson’s squirrel was introduced in urban areas
of Acqui Terme and Maratea in the 1980s but the presence of the animals in these two areas was reported to local authorities with a delay
of 18-20 years (Bertolino et al., 1999; Aloise and Bertolino, 2005).
Eradication and control
The only successful removals of mammals in Italy have been rat eradications from small islands. Since the late 90s, many islands have been
released by rats, with the goal of protecting target species (i.e. nesting seabirds, mainly shearwaters) and, more generally, island ecosystems. Although two rat species are present on Italian islands, R. rattus
is largely the most widespread on Mediterranean islands (Baccetti et al.,
2009). Islands were selected according to their importance in terms of
seabird nesting pairs as well as the monetary cost for the implementation of the eradication (Capizzi et al., 2010). Furthermore, the risk
of rat reinvasion was also taken into account. On the whole, between
1999 and 2014, rats were eradicated from 11 islands, in areas ranging
between 1 ha and 1000 ha (Montecristo), but 6 of them were reinvaded
(see Ragionieri et al., 2013 for the case of Molara island). Monitor31
26(1): 25–35
ing of seabird reproductive success confirmed the positive effect of rat
removal on target species (Baccetti et al., 2009).
As previously mentioned, an early attempt to eradicate the grey
squirrel was halted at the stage of a first trial when radical animal rights
groups took the responsibles for the project to the court (Bertolino and
Genovesi, 2003). The two officers involved were acquitted by the Appeal Court, but no other action was implemented till a recent new attempt started in 2010 which is still ongoing (Bertolino et al., 2014a).
The only introduced rodent species widely controlled in Italy is the
coypu. The management of the species is a current practice in many
regions of north-central Italy, though control activities seem to be ineffective at a large scale. During a six-years period (1995-2000), despite
the removal of 220,688 coypu with a cost of € 2,614,408, the damage
produced to agriculture and riverbanks increased to € 11,631,721 (Panzacchi et al., 2007). However, coypu populations were locally managed
in an effective way, with reduction of economic losses (Bertolino and
Viterbi, 2010) and preservation of biodiversity (Bertolino et al., 2005).
An important feature of these projects was an adequate level of trapping effort, which was maintained constant or even increased after first
results were achieved (Bertolino and Viterbi, 2010). It should also be
stressed that the cost for a successful 11-years eradication project in
England was largely exceeded by the cost related to few years of permanent control campaign in Italy, demonstrating that a timely eradication could be cost-effective in respect to a long-term control campaign
(Panzacchi et al., 2007).
The future
The Council of the European Union adopted on 29 September 2014 the
regulation on the prevention and management of the introduction and
spread of invasive alien species. The regulation establishes a framework for tackling invasive species at the European level with the aim to
protect biodiversity and ecosystem services, as well as to mitigate the
economic and sanitary impacts that these species can have (Genovesi et
al., 2014). This will be achieved by focusing resources on priority species and on preventive measures. The proposal is based on a black list
of invasive alien species of Union Concern, which will be developed
and updated through risk assessment and scientific evidence. Criteria
that will be considered are the following: non-native in EU territory,
ability to establish and spread, causing such damage so as to deserve
EU action. Selected species will be banned from the EU, meaning it
will not be possible to import, use, release or sell them.
5. Scattershot, the homemade management of
small mammals
Italian law does not protect a number of rodent and mole species (i.e.
rats, mice, voles and moles), the main reason being that most of them
are regarded as pest species of economic and public health importance.
This is of course an opportunity for pest control operators (PCO companies), which can eliminate pest species in many sensitive contexts,
food industries, urban areas, agricultural premises and sewers without
any legal problem. However, most of the pest control operations are
usually carried out in contexts where non-target small mammal species
may live (i.e. peripheral or green urban areas, or in rural contexts),
thus setting them at risk of primary poisoning and, as consequence,
their main predators (e.g diurnal and nocturnal raptors, carnivores, etc)
of secondary poisoning.
Main target species are invariably synanthropic rats and mice (R.
rattus, R. norvegicus and M. musculus, Capizzi and Santini, 2007).
Most pest control operations are carried out largely relying on nonselective anticoagulant rodenticides (Capizzi et al., 2014). The use
of trap devices is usually deserved inside buildings or food industries.
Toxic baits are placed inside bait stations, distributed without worrying about the possible presence of other non-target species, either nonprotected (wood mice, voles) or protected (dormice), which may have
access to them.
Contrary to what happens in other European countries, where the
most powerful active ingredients are prohibited in outdoor areas (e.g.
32
brodifacoum and flocoumafen in United Kingdom), in Italy there are
no restrictions on the active ingredients. Rodent control activities are
routinely performed by PCO companies in buildings, food industries,
municipalities and green areas. Furthermore, all rodenticides are commonly sold in stores, and anyone can buy them. This implies that rodent control activities can be carried out by anyone without checking
out if they are actually managing harmful species or, more likely, hitting anyone walking there (in fact, scattershot). In fact, the impact of
rodenticides on non-target small mammals has been well documented
(Brakes and Smith, 2005).
Another relevant issue is the risk of secondary poisoning for predators and scavengers (Berny et al., 1997; Fournier-Chambrillon et al.,
2004). The risk is strictly depending on the active ingredient used,
low (although not irrelevant, O’Connor et al., 2003) for first generation
anticoagulants (e.g. warfarin, clorophacinone), high for second generation ones (bromadiolone and difenacoum, Berny et al., 1997), and
even higher for the most potent ones (brodifacoum and flocoumafen,
Alterio, 1996; Hoare and Hare, 2006). However, as no restriction in
outdoor areas exists, the risk is out of control, and no published account
is available for Italy. A study performed in Latium on roadkilled birds
revealed the presence of anticoagulant residues in about 40% diurnal
and nocturnal raptors (Capizzi et al., unpublished data). It is worth
noting that the baits are often consumed by invertebrates (snails, ants,
cockroaches, grasshoppers), thus endangering other predators.
Rodent control inside buildings is often performed relying on trap
devices, either mechanic or glue boards. In both cases, these devices
are not fully selective towards synanthropic rats and mice, but may also
catch non-target small mammals, such as shrews and dormice (Capizzi
and Santini, 2007). The scale of operations is usually very small (group
of buildings, small parts of urban areas). When rodent control is applied on a larger scale (municipalities, large urban areas), no attempt of
forecasting and modeling rodent presence (e.g. Langton et al., 2001;
Traweger and Slotta-Bachmayr, 2005), which may significantly reduce
the distribution of rodenticide baits, is planned.
A first attempt to tackle the problem of rodent resistance to anticoagulants is in place (Capizzi et al., 2013). Nowadays, the phenomenon
can be localized on a genetic basis (Pelz et al., 2005), and a first monitoring was launched at a national level, in the wake of similar studies at a
more advanced stage in other European countries (Pelz, 2007; Buckle,
2011).
6. Not only criticisms and self-pity: an operational proposal for the future
Italian small mammal fauna is composed by species which apparently
do not require conservation attention. According to the IUCN red list,
only three rodents are Near Threatened. This situation, however, is related more to the absence of adequate information than to a thoughtful
evaluation of the species status, based on population and range trends.
Six species were classified as Data Deficient, as knowledge about their
abundance and distribution is still too limited; the elusiveness of many
species and the need to trap them to collect data on their ecology and
population dynamics or even on their presence, make it difficult and
expensive to start long term studies. In such a situation, the lack of
information implies the risk of considering most species as safe, because there is no indication of decline. Furthermore, small mammals
are r-strategist and with wide distributions, therefore they end up being
considered as Least Concern.
Recent studies highlighted the need of a stronger effort on genetic
analyses of small mammals. Almost all the species surveyed till now
showed genetic peculiarity respect to the conspecific populations from
the rest of Europe (e.g. divergent lineages, cryptic diversity, large genetic diversity) suggesting that some of the divergent lineages found in
Italy may represent valid species, thus endemic to Italy and with a conservation status to evaluate. Moreover, any research focusing on conservation of small mammals should take into account that maintaining
high genetic diversity (i.e preserving Italian species and divergent genetic lineages) helps to preserve the evolutionary potential of the whole
species.
Table 6 – Species of conservation concern currently not protected by Italian law (DD, Data
Deficient; NT, Near Threatened).
Species
Talpa romana
Talpa caeca
Arvicola amphibius
Chionomys nivalis
Microtus brachycercus
Apodemus alpicola
Endemic
Limited
distribution
range
Threatened
(Italian
IUCN category)
X
DD
NT
NT
X
DD
X
X
Although Rodents and Soricomorpha include most of the Italian endemic mammal species, their protection is in most cases inadequate.
Species which would need conservation attention, such as A. amphibius
or C. nivalis, are not protected at all and can be controlled without any
permission. This is a great difference with respect to bats, which are
“particularly protected” according to the national law and European
Directive. The Habitats Directive, in particular, requires a monitoring
scheme for protected species and the evaluation of possible effects of
activities that could affect habitat and species in or close to the Nature
2000 network or in breeding sites. Only four small mammal species,
one of which, H. cristata, is now considered as introduced, benefit of
such a high level of protection. Furthermore, not including small mammals in European Directives has important implications also on the allocation of funds devoted to conservation projects. For instance, almost
70% of the funds allocated until 2010 to LIFE projects on mammals in
Italy involved only three species (brown bear, wolf, Apennine chamois),
while no project on small mammals has been funded (Silva et al., 2011).
The protection of Italian small mammals is far from being adequate.
The National Law 157/1992 on Wildlife protects all free-living species
of mammals and birds, with the only exceptions of moles, rats, mice
and voles. Therefore, according to this law, while introduced mammal
species are protected, despite their impacts, and their control is strictly
regulated, many native small mammals are not protected at all. This
implies that no conservation strategy is currently applied to these species, notwithstanding some of them are endemic or considered nearly
threatened by the Italian IUCN red list (Tab. 6). We agree that there
should be the possibility to better control the two rat species and the
house mouse, or some vole species, such as Microtus savii, where they
produce damage or pose at risk public health and human activities.
However, it is time to amend the present law, including moles, mice
and voles in the protection and allowing in derogation the numerical
control only of those species actually impacting on human activities.
Invasive alien species may affect ecosystems and human well being
in different ways (Vilà et al., 2010). In Italy, introduced rodents may
produce a variety of impacts that, however, are rarely quantified. If
we consider M. coypus, a species which is widely distributed and controlled in the country (Panzacchi et al., 2007), quantitative information
on its damage to natural vegetation are reported only in two studies
based on comparison before and after the colonization of some wetlands by the aquatic rodent and after its control (Bertolino et al., 2005)
and comparing plots where the species was excluded with control areas
(D’Antoni et al., 2002). Management activities of introduced species
including long-term control plans offer good opportunities for applied
research, which are seldom exploited. For instance, different authors
have hypothesized that M. coypus could affect waterbirds preying on
eggs and nestling (Scaravelli, 2002; Tinarelli, 2002). However, only recently with the use of photo-cameras it has been shown that coypu did
not eat eggs, but rather use the nests as resting platforms, thus destroying or sinking the eggs (Bertolino et al., 2011; Angelici et al., 2012).
Even when data are collected the authors are in most cases likely to
present the results in national conferences, without subsequently producing a full paper. For instance, very few data are available on the
damage produced by H. cristata despite some studies were presented
in conferences.
In conclusion, Italian small mammals are largely neglected and even
not protected in the case of many rodents. Efforts are mostly directed toward the management of those species whose impact on human
activity and wellbeing is documented, while conservation activity is
very limited. There is an urgent need to reconsider the status of these
species by increasing our knowledge on their ecology, distribution and
populations trends. Monitoring projects for single species or groups
of them should start with an effective coordination between different
areas. National laws should be amended providing protection for native rodents. At the end, there is the need to involve the general public
to get more support in the conservation effort. This should be achieved
primarily by raising the image of these specie through the production
of impacting publications and starting projects of citizen science, as
done for decades by The Mammal Society in Great Britain.
References
Alda F., Ruiz-López M.J., García F.J., Gompper M.E., Eggert L.S., García J.T., 2013. Genetic evidence for multiple introduction events of raccoons (Procyon lotor) in Spain.
Biol. Inv. 15: 687–698.
Allendorf F.W., Luikart G.H., Aitken S.N., 2012. Conservation and the genetics of populations. John Wiley & Sons, Chirchester, West Sussex, UK.
Aloise G., Bertolino S., 2005. Free-ranging population of the Finlayson’s squirrel Callosciurus finlaysonii (Horsfield, 1824) (Rodentia, Sciuridae) in South Italy. Hystrix 16:
70–74.
Alterio N., 1996. Secondary poisoning of stoat (Mustela erminea), feral ferrets (Mustela
furo), and feral house cats (Felis catus) by the anticoagulant poison, brodifacoum. N.
Zeal. J. Zool. 23: 331–338.
Amori G, Gippoliti S., 2000. What do mammalogists want to save? Ten years of mammalian
conservation biology. Biodiv. Cons. 9: 785–793.
Amori G., Contoli L., Nappi A., 2008. Fauna d’Italia, Mammalia II: Erinaceomorpha,
Soricomorpha, Lagomorpha, Rodentia. Edizioni Calderini, Bologna, Italia.
Angel A., Wanless R.M., Cooper J., 2009. Review of impacts of the introduced house mouse
on islands in the Southern Ocean: are mice equivalent to rats? Biol. Inv. 11: 1743–1754.
Angelici C., Marini F., Battisti C., Bertolino S., Capizzi D., Monaco A., 2012. Cumulative
impact of rats and coypu on nesting waterbirds: first evidences from a small Mediterranean wetland (Central Italy). Vie et Milieu – Life and Environment 62: 137–141.
Angelici F.M., Capizzi D., Amori G., Luiselli L., 2003. Morphometric variation in the
skulls of the crested porcupine Hystrix cristata from mainland Italy, Sicily, and northern
Africa. Mammal. Biol. 68: 165–173.
Arcangeli G., 2002. La nutria selvatica quale potenziale “reservoir” di agenti trasmissibili all’uomo: situazione in Italia e nel mondo. In: Petrini R., Venturato E. (Eds.). La
gestione delle specie alloctone in Italia: il caso della nutria e del gambero rosso della
Louisiana. Quaderni del Padule di Fucecchio n.2, Centro di Ricerca, Documentazione e
Promozione del Padule di Fucecchio, pp. 31.
Atkinson I.A.E., 1985. The spread of commensal species of Rattus to oceanic islands and
their effects on island avifaunas. In Moors P.J. (Ed.). Conservation of Island Birds. ICBP
Technical Publication No.3: 35–81.
Baccetti N., Capizzi D., Corbi F., Massa B., Nissardi S., Spano G., Sposimo P., 2009. Breeding shearwater on Italian islands: population size, island selection and co-existence with
their main alien predator. Riv. Ital. Ornit. 78: 83–99.
Barreto G.R., Rushton S.P., Strachan R., Macdonald D.W., 1998. The role of habitat and
mink predation in determining the status and distribution of water voles in England.
Anim. Cons. 1: 129–137.
Berggren K.T., Ellegren H., Hewitt G.M., Seddon J.M., 2005. Understanding the phylogeographic patterns of European hedgehogs, Erinaceus concolor and E. europaeus using
the MHC. Heredity 95: 84–90.
Berny P.J., Buronfosse T., Buronfosse F., Lamarque F., Lorgue G., 1997. Field evidence of
secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo) by bromadiolone, a 4-year survey. Chemosph. 35: 1817–1829.
Bertolino S., 2007. Microhabitat use by garden dormice (Eliomys quercinus) during nocturnal activity. J. Zool. London 272: 176–182.
Bertolino S., 2009. Animal trade and non-indigenous species introduction: the world-wide
spread of squirrels. Divers. Distrib. 15: 701–708.
Bertolino S., Genovesi P., 2003. Spread and attempted eradication of the grey squirrel
(Sciurus carolinensis) in Italy, and consequences for the red squirrel (Sciurus vulgaris)
in Eurasia. Biol. Conserv.109: 351–358.
Bertolino S., Genovesi P., 2005. The application of the European strategy on invasive alien
species: an example with introduced squirrels. Hystrix 16: 59–69.
Bertolino S., Lurz P.W.W., 2013. Callosciurus squirrels: worldwide introductions, ecological impacts and recommendations to prevent the establishment of new invasive populations. Mammal Rev. 43: 22–33.
Bertolino S., Viterbi R., 2010. Long-term cost-effectiveness of coypu (Myocastor coypus)
control in Piedmont (Italy). Biol. Inv. 12: 2549–2558.
Bertolino S., Angelici C., Monaco E., Monaco A., Capizzi D., 2011. Is the coypu
(Myocastor coypus) a nest predator or a nest destroyer? Hystrix 22: 333–339.
Bertolino S., Cordero di Montezemolo N., Preatoni D.G., Wauters L.A., Martinoli A.,
2014a. A grey future for Europe: Sciurus carolinensis is replacing native red squirrels
in Italy. Biol. Inv. 16: 53–62.
Bertolino S., Currado I., Mazzoglio P.J., 1999. Finlayson’s (Variable) Squirrel Callosciurus
finlaysoni in Italy. Mammalia 63: 522–525.
Bertolino S., Girardello M., Amori G., 2014b. Identifying conservation priorities when data
are scanty: a case study with small mammals in Italy. Mammal. Biol. 79: 349–356.
Bertolino S., Perrone A., Gola L., 2005. Effectiveness of coypu control in small Italian
wetland areas. Wildl. Soc. Bull. 33: 714–720.
Bertolino S., Viano C., Currado I., 2001. Population dynamics, breeding patterns and spatial utilisation of the garden dormouse Eliomys quercinus in an Alpine habitat. J. Zool.
London 253: 513–521.
33
26(1): 25–35
Bertolino S., Vizzini A., Wauters L.A., Tosi G., 2004. Consumption of hypogeous and
epigeous fungi by the red squirrel (Sciurus vulgaris) in subalpine conifer forests. Forest
Ecol. Manag. 202: 227–233.
Bollo E., Pregel P., Gennero S., Pizzoni E., Rosati S., Nebbia P., Biolatti B., 2003. Health
status of a population of nutria (Myocastor coypus) living in a protected area in Italy.
Res. Vet. Sci. 75: 21–25.
Brakes C.R., Smith R.H., 2005. Exposure of non-target small mammals to rodenticides:
short-term effects, recovery and implications for secondary poisoning. J. Appl. Ecol.
42: 118–128.
Brown P.R., Singleton G.R., 1998. Efficacy of brodifacoum to control house mice, Mus
domesticus, in wheat crops in Southern Australia. Crop Prot. 17: 345–352.
Buckle A., 2011. Anticoagulant resistance in the UK and a new guideline for the management of resistant infestations of Norway rats (Rattus norvegicus Berk.). Julius-KühnArchiv 432: 61–62.
Capizzi D., Luiselli L., 1996a. Feeding relationships and competitive interactions between
phylogenetically unrelated predators (owls and snakes). Acta Oecol. 17: 265–284.
Capizzi D., Luiselli L., 1996b. Ecological relationships between small mammals and age
of coppice in an oak-mixed forest in central Italy. Rev. Ecol. 51: 277–291.
Capizzi D., Battistini M., Amori G., 2002. Analysis of the Hazel dormouse, Muscardinus
avellanarius, distribution in a Mediterranean fragmented woodland. Ital. J. Zool. 69:
25–31.
Capizzi D., Battistini M., Amori G., 2003. Effects of habitat fragmentation and forest management on the distribution of the edible dormouse Glis glis. Acta Theriol. 48: 359–371.
Capizzi D., Santini L., 2007. I Roditori italiani. Ecologia, impatto sulle attività umane e
sugli ecosistemi, gestione delle popolazioni. Antonio Delfino Editore, Rome, Italy.
Capizzi D., Baccetti N., Sposimo P., 2010. Prioritizing rat eradication on islands by cost
and effectiveness to protect nesting seabirds. Biol. Cons. 14: 1716–1727.
Capizzi D., Castiglia R., Colangelo P., 2013. Monitoring rodent resistance to anticoagulants
in Italy. In: Bertolino S., Capizzi D., Colangelo P., Mori E., Scaravelli D. (Eds.). I Piccoli
Mammiferi in un mondo che cambia. Atti del II Convegno sui Piccoli Mammiferi, 24-25
Novembre 2013, Ercolano (Naples), Italy, p. 13.
Capizzi D., Bertolino S., Mortelliti A., 2014. Rating the rat: global patterns and research
priorities in impacts and management of rodent pests. Mammal Rev. 44: 148–162.
Caroli L., Capizzi D., Luiselli L., 2000. Reproductive strategies and life-history traits of the
Savi’s pine vole, Microtus savii. Zool. Sci. 17: 209–216.
Castiglia R., Annesi F., Aloise G., Amori G., 2007. Mitochondrial DNA reveals different
phylogeographic structures in the water shrews Neomys anomalus and N. fodiens (Insectivora: Soricidae) in Europe. J. Zool. Syst. Evol. Res. 45: 255–262.
Castiglia R., Annesi F., Aloise G., Amori G., 2008. Systematics of the Microtus savii complex (Rodentia, Cricetidae) via mitochondrial DNA analyses: paraphyly and pattern of
sex chromosome evolution, Mol. Phyl. Evol. 46: 1157–1164.
Čepelka L., Suchomel J., Purchart L., Heroldovà M., 2011. Small mammals diversity in the
Beskydy Mts. forest ecosystems subject to different forms of management. Beskydy 4:
101–108.
Churchfield S., Barber J., Quinn C., 2000. A new survey method for water shrews (Neomys
fodiens) using baited tubes. Mammal Rev. 30: 249–254.
Colangelo P., Bannikova A.A., Kryštufek B., Lebedev V.S., Annesi F., Capanna E., Loy A.,
2010. Molecular systematics and evolutionary biogeography of the genus Talpa (Soricomorpha: Talpidae). Mol. Phyl. Evol. 55: 372–380.
Colangelo P., Aloise G., Franchini P., Annesi F., Amori G., 2012. Mitochondrial DNA
reveals hidden diversity and an ancestral lineage of the bank vole in the Italian peninsula.
J. Zool. London 287: 41–52.
Colangelo P., Abiadh A., Aloise G., Amori G., Capizzi D., Vasa E., Annesi F., Castiglia R.,
2015. Mitochondrial phylogeography of the black rat supports a single invasion of the
western Mediterranean basin. Biol. Inv. 17: 1859–1868. doi:10.1007/s10530-015-0842-2
Corti M., Loy A., 1987. Morphometric divergence in Southern European moles (Insectivora, Talpidae). Bollettino di Zoologia 54: 187–191.
Currado I., 1993. Lo scoiattolo grigio americano (Sciurus carolinensis Gmelin), nuovo
nemico per l’arboricoltura da legno in Italia (Rodentia: Sciuridae). Convegno Arboricoltura da Legno e politiche comunitarie, Tempio Pausania (OT), Italy: 85–94.
Currado I., Mazzoglio P.J., Amori G., Wauters L. 1997. Rischi biologici delle introduzioni:
il caso dello Scoiattolo grigio in Italia (Sciurus carolinensis Gmelin, 1788). In: Spagnesi
M., Toso S. Genovesi P. (Eds). Atti del III Convegno dei Biologi della Selvaggina, Suppl.
Ric. Biol. Selvaggina 27: 277–284.
D’Antoni S., Pacini A., Cocchieri G., Pittiglio C., Reggiani G., 2002. L’impatto della nutria
(Myocastor coypus) nella Riserva Naturale Tevere-Farfa (RM). In: Petrini R., Venturato
E. (Eds.). La gestione delle specie alloctone in Italia: il caso della nutria e del gambero rosso della Louisiana. Quaderni del Padule di Fucecchio n.2, Centro di Ricerca,
Documentazione e Promozione del Padule di Fucecchio, pp. 41–50.
Davenport K., Collins J., 2011. European code of conduct on pets and invasive alien
species. T-PVS/Inf (2011) 1 rev, Strasbourg, France. Available from http://www.
nonnativespecies.org/downloadDocument.cfm?id=946[3 July 2015].
Delibes-Mateos M., Smith A.T., Slobodchikoff C.N., Swenson J.E., 2011. The paradox
of keystone species persecuted as pests: a call for the conservation of abundant small
mammals in their native range. Biol. Cons. 144: 1335–1346.
Dickman C.R., 1999. Rodent-ecosystem relationships: a review. In: Singleton G.R., Hinds
L., Leirs H., Zhang Z. (Eds.). Ecologically Based Rodent Management., Australian
Centre for International Agricultural Research, Canberra, pp. 113–133.
Di Febbraro M., Loy A., 2014. A new method based on indirect evidences to infer activity
pattern in moles. A test on the blind mole in Central Apennines. Folia Zool. 63: 116–
121.
Dlugosch K.M., Parker I.M., 2008. Founding events in species invasions: genetic variation,
adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17: 431–449.
Ferguson J.W.H., 2002. On the use of genetic divergence for identifying species. Biol. J.
Linn. Soc. 75: 509–516.
Feuda R., Bannikova A.A., Zemlemerova E.D., Di Febbraro M., Loy A., Hutterer R., Aloise
G., Zykov A.E., Annesi F., Colangelo P., 2015. Tracing the evolutionary history of Talpa
europaea through mtDNA phylogeography and species distribution modelling. Biol. J.
Linn. Soc. 114: 495–512.
Ficetola G.F., Bonin A., Miaud C., 2008. Population genetics reveals origin and number of
founders in a biological invasion. Mol. Ecol. 17: 773–782.
Filippucci M.G., Simson S., 1996. Allozyme variation and divergence in Erinaceidae
(Mammalia: Insectivora). Israel J. Zool. 42: 335–345.
34
Fitzpatrick B.M., Fordyce J.A., Niemiller M.L., Reynolds R.G., 2011. What can DNA tell
us about biological invasions? Biol. Inv. 14: 245–253.
Forcina G., Panayides P., Guerrini M., Mori E., Gupta B.K., Al-Sheikhly O.F., Mansoori
J., Khaliq I., Rank D.N., Parasharya B.M., Khan A.A., Hadjigerou P., Barbanera F.,
2012. Molecular evolution of the Asian francolins (Francolinus, Galliformes): a modern
reappraisal of a classic study in speciation. Mol. Phyl. Evol. 65: 523–534.
Fournier-Chambrillon C., Berny P.J., Coiffier O., Barbedienne P., Dassé B., Delas G., Galineau H., Mazet A., Pouzenc P., Rosoux R., Fournier P., 2004. Evidence of secondary
poisoning of free-ranging riparian mustelids by anticoagulant rodenticides in France:
implications for conservation of European mink (Mustela lutreola). J. Wildl. Dis. 40:
688–695.
Genovesi P., Shine C., 2004. European Strategy on Invasive Alien Species. Nature and
Environment, n. 137. Council of Europe publishing, Strasbourg, 67 pp.
Genovesi P., Carboneras C., Vilà M., Walton P., 2014. EU adopts innovative legislation on
invasive species: a step towards a global response to biological invasions? Biol. Inv.
17(5): 1307–1311. doi:10.1007/s10530-014-0817-8
Gippoliti S., 2013. Checklist sulle specie di mammiferi italiani (esclusi Mysticeti e Odontoceti): un contributo per la conservazione della biodiversità. Boll. Mus. Civ. St. Nat.
Verona 37: 1–23.
Gippoliti S., Groves C.P., 2013. “Taxonomic inflation” in the historical context of mammalogy and conservation. Hystrix 24: 8–11.
Gippoliti S, Cotterill F.P.D., Groves C.P., 2013. Mammal taxonomy without taxonomists: a
reply to Zachos and Lovari. Hystrix 24: 145–147.
Gippoliti S., Amori G., Castiglia R., Colangelo P., Capanna E., 2014. The relevance of
Italian museum collections for research and conservation: the case of mammals. Rend.
Fis. Acc. Lincei, 25: 351–357.
Gornung E., Bizzoco D., Castiglia R., Colangelo P., 2010. Comparative cytogenetic and genetic study of two Italian populations of the garden dormouse Elyomys quercinus (Sciuromorpha: Gliridae). Ital. J. Zool. 77: 137–143.
Greenwood A., Churchfield S., Hickey C., 2002. Geographical distribution and habitat occurrence of the water shrew (Neomys fodiens) in the Weald of South-East England. Mammal Rev. 32: 40–50.
Grill A., Amori G., Aloise G., Lisi I., Tosi G., Wauters L.A., Randi E., 2009. Molecular
phylogeography of European Sciurus vulgaris: refuge within refugia? Mol. Ecol. 18:
2687–2699.
Gurnell J., Wauters L.A., Lurz P.W., Tosi G., 2004. Alien species and interspecific competition: effects of introduced eastern grey squirrels on red squirrel population dynamics.
J. Anim. Ecol. 73: 26–35.
Handley L.J.L., Estoup A., Evans D.M., Thomas C.E., Lombaert E., Facon B., Aebi A.,
Roy H.E., 2011. Ecological genetics of invasive alien species. BioControl 56: 409–428.
Harris D.B., 2009. Review of negative effects of introduced rodents on small mammals on
islands. Biol. Inv. 11: 1611–1630.
Hewitt G.M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Phil.
Trans. R. Soc. London 359: 183–195.
Hoare J.M., Hare K.M., 2006. The impact of brodifacoum on non-target wildlife: gaps in
knowledge. N. Zeal. J. Zool. 30: 157–167.
Horskins K., White J., Wilson J., 1998. Habitat usage of Rattus rattus in Australian macadamia orchard systems: Implications for management. Crop Prot. 17: 359–364.
Hulme P.E., Vilà M., Nentwig W., Pyšek P., 2010. Are the aliens taking over? Invasive
species and their increasing impact on biodiversity. Atlas of Biodiversity Risk. Pensoft,
Sofia and Moscow: 132–133.
Iordan F., Rushton S.P., Macdonald D.W., Bonesi L., 2012. Predicting the spread of feral
populations of the American mink in Italy: is it too late for eradication? Biol. Inv. 14:
1895–1908.
Jacobs D., Cotterill F.P.D., Taylor P.J., Aulagnier S., Nagy Z., Karataş A., 2008. Rhinolophus blasii. In: IUCN, 2013. IUCN Red List of Threatened Species. Version 2013.2.
Available from www.iucnredlist.org [25 November 2013].
Janos D.P., Sahley C.T., Emmons L.H., 1995. Rodents dispersal of vescicular–arbuscular
mycorrhizal fungi in Amazonian Peru. Ecology 76: 1852–1858.
Jones A.G., Chown S.L., Gaston K.J., 2003. Introduced house mouse as a conservation
concern on Gough Island. Biol. Cons. 12: 2107–2119.
Kotsakis T., Ruschioni E., 1984. I microvertebrati di un insediamento dell’Età del Ferro
presso Tortoreto (Teramo, Italia centrale). Atti della Accademia nazionale dei Lincei.
Rendiconti. Classe di scienze fisiche, matematiche e naturali, 76: 295–304.
Kryštufek B., Koren T., Engelberger S., Horvàth G.F., Purger J.J., Arslan A., Chişamera
G., Murariu D., 2014. Fossorial morphotype does not make a species in water voles.
Mammalia, doi:10.1515/mammalia-2014-0059.
Lambert M., Quy R., Smith R., Cowan D., 2008. The effect of habitat management on
home-range size and survival of rural Norway rat populations. J. Appl. Ecol. 45: 1753–
1761.
Langton S.D., Cowan D.P., Meyer A.N., 2001. The occurrence of commensal rodents in
dwellings as revealed by the 1996 English House Condition Survey. J. Appl. Ecol. 38:
699–709.
Lapini L., Scaravelli D., 1993. Preliminary data on the muskrat Ondatra zibeticus (Linneo, 1766) in North-eastern Italy (Mammalia, Rodentia, Arvicolidae). In: Spagnesi M.,
Randi E. (Eds.). Proceedings of the VII Congress of the Association A. Ghigi for the
Biology and Conservation of Vertebrates. Supplemento Ricerche della Biologia della
Selvaggina 21, Bologna, Italy, pp. 249–252.
Leirs H., Lodal J., Knorr M., 2004. Factors correlated with the presence of rodents on
outdoor pig farms in Denmark and suggestions for management strategies. NJAS - Wageningen J. Life Sci. 52: 145–159.
Leis S.A., Leslie D.M., Engle D.M., Fehmi J.S., 2008. Small mammals as indicators of
short-term and long-term disturbance in mixed prairie. Environm. Monitor. Ass. 137:
75–84.
Long J.L., 2003. Introduced mammals of the world: their history, distribution and influence.
CSIRO Publishing: Melbourne, Australia.
Markovà S., Searle J.B., Kotlìk P., 2014. Relaxed functional constraints on triplicate αglobin gene in the bank vole suggest a different evolutionary history from other rodents.
Heredity 113: 64–73.
Martinoli A., Bertolino S., Preatoni D.G., Balduzzi A., Marsan A., Genovesi P., Tosi G.,
Wauters L.A., 2010. Headcount 2010: the multiplication of the grey squirrel population
introduced to Italy. Hystrix, Ital. J. Mamm. 21: 127–136.
Masseti M., Albarella U., De Grossi Mazzorin J., 2010. The crested porcupine, Hystrix
cristata L., 1758, in Italy. Anthropozool. 45: 27–42.
Mayle B.A. 2005. Britain’s woodlands under threat. Grey squirrels and the risk they pose
to European woodlands. Trees, Journal of the International Tree Foundation 65: 9–11.
Meadows P.S., Meadows A., 1991. The environmental impact of burrowing animals and
animal burrows. Clarendon Press Oxford, U.K.
Meerburg B.G., Singleton G.R., Kijlstra A., 2009. Rodent-borne diseases and their risks for
public health. Critical Rev. Microbiol. 35: 221–270.
Meylan A., 1966. Données nouvelles sur le chromosomes des Insectivores européens
(Mamm.). Rev. suisse Zool. 73: 548–588.
Michaux J.R., Libois R., Fillippucci M.-G., 2005. So close and so different: comparative phylogeography of two small mammal species, the Yellow-necked fieldmouse (Apodemus flavicollis) and the Woodmouse (Apodemus sylvaticus) in the Western Palearctic
region. Heredity 94: 52–63.
Moralee R.D., Van der Bank F.H., Van der Waal B.C.W., 2000. Biochemical genetic markers to identify hybrids between the endemic Oreochromis mossambicus and the alien
species, O. niloticus (Pisces: Cichlidae). Water Sa-Pretoria 26: 263–268.
Mori E., Sforzi A., Di Febbraro M., 2013. From the Apennines to the Alps: recent range
expansion of the crested porcupine Hystrix cristata L., 1758 (Mammalia: Rodentia:
Hystricidae) in Italy. Ital. J. Zool. 80: 469–480.
Mori E., Nourisson D.H., Lovari S., Romeo G., Sforzi A., 2014a. Self-defence may not be
enough: moonlight avoidance in a large, spiny rodent. J. Zool. London, 294: 31–34.
Mori E., Lovari S., Sforzi A., Romeo G., Pisani C., Massolo A., Fattorini L., 2014b. Patterns
of spatial overlap in a monogamous large rodent, the crested porcupine. Behav. Proc.
107: 112–118.
Moritz C., 1994. Defining “Evolutionary Significant Units” for conservation. Trends Ecol.
Evol. 9: 373–375.
Mortelliti A., Amori G., Sammuri G., Boitani L., 2007. Factors affecting the distribution
of Sorex samniticus, and endemic Italian shrew, in an heterogeneous landscape. Acta
Theriol. 52: 75–84.
Mortelliti A., Boitani L., 2009. Distribution and coexistence of shrews in patchy landscapes:
a field test of multiple hypotheses. Acta Oecol. 35: 797–804.
Mortelliti A., Santulli Sanzo G., Boitani L., 2009. Species’ surrogacy for conservation planning: caveats from comparing the response of three arboreal rodents to habitat loss and
fragmentation. Biodiv. Conserv. 8: 1131–1145.
Mortelliti A., Amori G., Capizzi D., Rondinini C., Boitani L., 2010. Experimental design
and taxonomic scope of fragmentation studies on European mammals: current status
and future priorities. Mammal Rev. 40: 125–154.
Mortelliti A., Amori G., Capizzi D., Cervone C., Fagiani S., Pollini B., Boitani L., 2011.
Independent effects of habitat loss, habitat fragmentation and structural connectivity on
the distribution of two arboreal rodents. J. Appl. Ecol. 48: 163–172.
Mortelliti A., Sozio G., Driscoll D.A, Bani L., Boitani L., Lindenmayer D.B. 2014. Population and individual-scale responses to patch size, isolation and quality in the hazel
dormouse. Ecosphere 5(9): art107. doi:10.1890/ES14-00115.1
Mouton A., Grill A., Sarà M., Kryštufek B., Randi E., Amori G., Juškaitis R., Aloise G.,
Mortelliti A., Panchetti F., Michaux J., 2012. Evidence of a complex phylogeographic
structure in the common dormouse, Muscardinus avellanarius (Rodentia: Gliridae).
Biol. J. Linn. Soc.105: 648–664.
Naiman R.J., Melillo J.M., Hobbie J.E., 1986. Ecosystem alteration of boreal forest streams
by beaver (Castor canadensis). Ecology 67: 1254–1269.
Nummi P., Väänänen V.M., Malinen J., 2006. Alien grazing: indirect effects of muskrats
on invertebrates. Biol. Invas. 8: 993–999.
O’Connor C.E., Eason C.T., Endepols S., 2003. Evaluation of secondary poisoning hazards
to ferrets and weka from the rodenticide coumatetralyl. Wildl. Res. 30: 143–146.
Panzacchi M., Bertolino S., Cocchi R., Genovesi P., 2007. Cost/benefit analysis of two opposite approaches to pest species management: permanent control of Myocastor coypus
in Italy versus eradication in East Anglia (UK). Wildl. Biol. 13: 159–171.
Pearce J., Venier L., 2005. Small mammals as bioindicators of sustainable boreal forest
management. Forest Ecol. Manag. 208: 153–175.
Pelz H.J., 2007. Spread of resistance to anticoagulant rodenticides in Germany. Int. J. Pest
Manag. 53: 299–302.
Pelz H.J., Rost S., Hünerberg M., Fregin A., Heiberg A.C., Baert K. MacNicoll A.D.,
Prescott C.V., Walker A.S., Oldenburg J., Müller C.R., 2005. The genetic basis of resistance to anticoagulants in rodents. Genetics 170: 1839–1847.
Ragionieri L., Cutuli G., Sposimo P., Spano G., Navone A., Capizzi D., Baccetti N., Fratini S., 2013. Establishing the eradication unit of Molara Island: a case of study from
Sardinia, Italy. Biol. Inv. 15: 2731–2742.
Randi E., 2007. Phylogeography of south European mammals. In: Weiss S., Ferrand N.
(Eds.). Phylogeography of southern European refugia. Springer Editions, Dordrecht
(Netherlands), pp. 101–126.
Reeder D.M., Helgen K.M., Wilson D.E., 2007. Global trends and biases in new Mammal
species discoveries. Occasional Papers, Museum of Texas Tech University 269: 1–36.
Rondinini C., Battistoni A., Peronace V., Teofili C., 2013. Lista Rossa dei Vertebrati Italiani.
MATTM, Federparchi, IUCN.
Ruffino L., Vidal E., 2010. Early colonization of the Mediterranean Basin by the ship rat
Rattus rattus: a review of zooarcheological data. Biol. Invas. 12: 2389–2394.
Ruiz-Gonzalez A., Madeira M.J., Randi E., Abramov A.V., Davoli F., Gòmez-Moliner B.J.,
2013. Phylogeography of the forest-dwelling European pine marten (Martes martes):
new insights into cryptic northern glacial refugia. Biol. J. Linn. Soc. 109: 1–18.
Rushton S.P., Barreto G.W., Cormack R.M., Macdonald D.W., Fuller R., 2000. Modelling
the effects of mink and habitat fragmentation on the water vole. J. Appl. Ecol. 37: 475–
490.
Sainsbury A.W., Nettleton P., Gilray J., Gurnell J., 2000. Grey squirrels have a high seroprevalence to a parapoxvirus associated with deaths in red squirrels. Anim Conserv 3:
229–233.
Santini L., 1980. The habits and influence on the environment of the old world porcupine
Hystrix cristata L. in the northernmost part of its range. In: Clark J.P. (Eds.). Proc. of
9th Vert. Pest Conf., Fresno, California, USA, pp. 149–153.
Santucci F., Emerson B.C., Hewitt G.M., 1998. Mitochondrial DNA phylogeography of
European hedgehogs. Mol. Ecol. 7: 1163–1172.
Scaravelli D., 2002. Myocastor problem: some considerations from the experience in the
province of Ravenna. In: Petrini R., Venturato E. (Eds.). The management of alien species in Italy; the case of the coypu and the red swamp crayfish. Centro di Ricerca, documentazione e Promozione del Palude di Fucecchio, Larciano, Pistoia, Italy, pp. 25–29.
Seddon J.M., Santucci F., Reeve N.J., Hewitt G.M., 2001. DNA footprints of European
hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene refugia, postglacial expansion and colonization routes. Mol. Ecol. 10: 2187–2198.
Shore R.F., Douben P.E., 1994. Predicting ecotoxicological impacts of environmental contaminants on terrestrial small mammals. Reviews of environmental contamination and
toxicology. Springer, New York, USA, pp. 44–89.
Sieg C.H., 1987. Small mammals: pests or vital components of the ecosystem. Great Plains
Wildlife Damage Control Workshop Proceedings, p. 97.
Signorile A.L., Paoloni D., Reuman D.C., 2014. Grey squirrels in central Italy: a new threat
for endemic red squirrel subspecies. Biol. Inv. 16: 2339-2350.
Silva J.P., Demeter A., Toland J., Jones W., Eldridge J., Hudson T., O’Hara E., Thévignot C.,
2011. LIFE and European Mammals. Improving their conservation status. Publications
Office of the European Union.
Skyrienė G., Paulauskas A., 2012. Distribution of invasive muskrats (Ondatra zibethicus)
and impact on ecosystem. Ekologija 58: 357–367.
Steele M., Wauters L.A., Larsen K.W., 2005. Selection, predation and dispersal of seeds by
tree squirrels in temperate and boreal forests: are tree squirrels keystone granivores? In:
Lambert J.E., Hulme P.E., Vander Wall S.B. (Eds.). Seed fate: predation, dispersal, and
seedling establishment. CABI International, pp. 205–221.
Taberlet P., Fumagalli L., West-Saucy A.-G., Cosson J.-F., 1998. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7: 453–464.
Takahashi M.A., 2006. A comparison of legal policy against alien species in New Zealand,
the United States and Japan - can a better regulatory system be developed? In: Koike F.,
Clout M.N., Kawamichi M., De Poorter M., Iwatsuki K., (Eds.). Assessment and Control
of Biological Invasion Risks. Shoukadoh Book Sellers, Kyoto, Japan and IUCN, Gland,
Switzerland, pp. 45–55.
Talmage S.S., Walton B.T., 1991. Small mammals as monitors of environmental contaminants. Springer, New York, USA, pp. 47–145.
Temple H.J., Terry A., 2007. The status and distribution of European mammals. Luxembourg, Office for Official Publications of the European Communities.
Tinarelli R., 2002. L’impatto della nutria sulle zone umide dell’Emilia Romagna e considerazioni sulle misure di controllo. In: Petrini R., Venturato E. (Eds.). La gestione
delle specie alloctone in Italia: il caso della nutria e del gambero rosso della Louisiana. Quaderni del Padule di Fucecchio n.2, Centro di Ricerca, Documentazione e Promozione del Padule di Fucecchio, pp. 39–40.
Tompkins D.M., Sainsbury A.W., Nettleton P., Buxton D., Gurnell J., 2002. Parapoxvirus
causes a deleterious disease in red squirrels associated with UK population declines.
Proc. R. Soc. London B Biol. Sci. 269: 529–533.
Tougard C., Renvoisé E., Petitjean A., Quéré J.P., 2008. New insight into the colonization
processes of common voles: inferences from molecular and fossil evidence. PLoS One
3: e3532.
Towns D.R., Atkinson I.A., Daugherty C.H., 2006. Have the harmful effects of introduced
rats on islands been exaggerated? Biol. Inv. 8: 863–891.
Traweger D., Slotta-Bachmayr L., 2005. Introducing GIS-modelling into the management
of a brown rat (Rattus norvegicus Berk.) (Mamm. Rodentia Muridae) population in an
urban habitat. J. Pest Sci. 78: 17–24.
Trucchi E., Sbordoni V., 2009. Unveiling an ancient biological invasion: molecular analysis
of an old European alien, the crested porcupine (Hystrix cristata). BMC Evol. Biol. 9:
109. doi:10.1186/1471-2148-9-109
Tweheyo M., Hill C.M., Obua J., 2005. Patterns of crop raiding by primates around the
Budongo Forest Reserve, Uganda. Wildl. Biol. 11: 237–247.
Vega R., Amori G., Aloise G., Cellini S., Loy A., Searle J.B., 2010. Genetic and morphological variation in a Mediterranean glacial refugium: evidence from Italian pygmy shrew
(Sorex minutus Mammalia, Soricomorpha). Biol. J. Linn. Soc. 100: 774–787.
Viè J.C., Hilton-Taylor C., Stuart S.N., 2009. Wildlife in a changing world—an analysis of
the 2008 IUCN red list of threatened species. IUCN, Gland, Switzerland.
Vilà M., Basnou C., Pyšek P., Josefsson M., Genovesi P., Gollasch S., Nentwig W., Olenin
S., Roques A., Roy D., Hulme P.E., DAISIE partners, 2010. How well do we understand the impacts of alien species on ecosystem services? A pan European cross taxa
assessment. Front. Ecol. Envir. 8: 135–144.
Vourch, G., Marmet, J., Chassagn, M., Bord, S., Chapuis, J.L., 2007. Borrelia burgdorferi
sensu lato in Siberian chipmunks (Tamias sibiricus) introduced in suburban forests in
France. Vector-Borne and Zoonotic Diseases 7: 637–642.
Wanless R.M., Angel A., Cuthbert R.J., Hilton G., Ryan P.G., 2007. Can predation by invasive mice drive seabird extinctions? Biol. Lett. 3: 241–244.
Wauters L.A., Tosi G., Gurnell J., 2005. A review of competitive effects of alien grey squirrels on behaviour, activity and habitat use of red squirrels in mixed, deciduous woodland
in Italy. Hystrix 16: 27–40.
Wauters L.A., Githiru M., Bertolino S., Molinari A., Tosi G., Lens L., 2008. Demography
of alpine red squirrel populations in relation to fluctuations in seed crop size. Ecography
31: 104–114.
Wilson D.E., Reeder D.M., 2005. Mammal Species of the World. Johns Hopkins University
Press, Baltimore, MD, USA.
Woodroffe G.L., Lawton J.H., Davidson W.L., 1990. The impact of feral mink Mustela
vison on water voles Arvicola terrestris in the North Yorkshire Moors National Park.
Biol. Cons. 51: 49–62.
Yannic C., Pellissier L., Dubey S., Vega R., Basset P., Mazzotti S., Pecchioli E., Vernesi
C., Hauffe H.C., Searle J.B., Hausser J., 2012. Multiple refugia and barriers explain the
phylogeography of the Valais shrew, Sorex antinorii (Mammalia: Soricomorpha). Biol.
J. Linn. Soc. 4: 864–880.
Zachos F.E., Apollonio M., Bärmann E.V., Festa-Bianchet M., Göhlich U., Habel J.C., Haring E., Kruckenhauser L., Lovari S., McDevitt A.D., Pertoldi C., Rössner G.E., SánchezVillagra M.R., Scandura M., Suchentrunk F., 2013. Species inflation and taxonomic artefacts – A critical comment on recent trends in mammalian classification. Mammal. Biol.
78: 1–6.
Zachos F.E., Lovari S., 2013. Taxonomic inflation and the poverty of the Phylogenetic Species Concept - a reply to Gippoliti and Groves. Hystrix 24: 142–144.
Associate Editor: L. Wauters
35
Volume 26 (1): 37–40, 2015
doi:10.4404/hystrix-26.1-10981
Research Article
A five-year cycle of coypu abundance in a remnant wetland: a case of sink population collapse?
Corrado Battistia,∗, Frencesca Marinia , Leonardo Vignolib
a
“Torre Flavia” LTER (Long Term Ecological Research) Station, Provincia di Roma - Servizio Aree protette – Parchi regionali, via Tiburtina 691, Rome, Italy
b
Dipartimento di Scienze, Università degli Studi di Roma Tre, Viale Marconi 446, 00146 Rome, Italy
Keywords:
peripheral population
explosion
establishment
collapse
cold winter
minimum temperatures
Article history:
Received: 9 November 2014
Acknowledgements
We thank Susanna D’Antoni (ISPRA, Rome), the Assistant Editor (Lucas
Wauters) and an anonymous reviewer for useful comments and suggestions that allow us to largely improve a first draft of the manuscript.
Simona Petruzzi deeply reviewed the English translation.
Abstract
In this work, we report a five-year study (2008–2013) of a coypu sub-population in a Mediterranean remnant wetland. Using a standardized transect, irregular inter-annual and seasonal patterns
in mean abundance were observed over the five year period. A first phase of demographic explosion
in autumn-winter 2008 was followed from 2009 to 2011 by a yearly-based hump-shaped pattern,
with a progressive increase from winter to summer and a decline in abundance from late summer to
winter. In 2013, a population crash was observed, with individuals being detected only occasionally. In 2010–2011, pattern in mean abundance was significantly correlated to pattern in minimum
daily temperatures. Finally, in February 2012 a single event of snow with low temperatures probably contribute to the local population collapse. The correspondence between a strong isolated
meteorological event (snow and sleet) and the disappearance of clear seasonal hump-shaped patterns followed by a population collapse suggests that this single climatic phenomenon played a role
in strongly reducing coypu numbers. Our data may corroborate the hypothesis that extrinsic environmental stochasticity and intrinsic physiological sensitivity to cold weather may be important
factors affecting coypu population dynamics. We hypothesize that this peripheral population may
be a sink of a larger meta-population at regional scale. Our data may also have implications for wildlife management. In fact, at least for peripheral sub-populations, control/eradication plans should
also take into consideration uncertainty deriving from stochastic events, which, disrupting local
demography, may affect control success. In this regard, knowledge of spatial structure of coypu
sub-populations may be important to devise appropriate strategies of population control.
Introduction
Coypu (Myocastor coypus Molina, 1782), an invasive semi-aquatic rodent introduced to North America as well as in several European countries as a domestic furbearer, is now widely diffused also in Italy (Bertolino and Genovesi, 2007). This species occurs mainly in plain landscapes with the presence of wet habitats. Since generally these habitat
types have a patchy distribution in Mediterranean landscapes, coypu
is usually spatially distributed with a meta-population structure (sensu
Hanski, 1998). In this sense, an effective migration among coypu subpopulations with colonization dynamics and local extinctions, have
already been documented (e.g. Callahan et al., 2005) and modelled
(Reeves and Usher, 1989; Schippers at al., 1996).
In meta-population systems, the most important factors explaining
the animal density in a single habitat patch are resource availability,
extrinsic environmental factors (e.g., local climate), and extinctioncolonization patterns among subpopulations. All these factors are capable of inducing change in demographic parameters (Hanski, 1998).
Despite in the Mediterranean region coypu became invasive since its
first introduction during the first half of 20th century (Reggiani et al.,
1995; Cocchi and Riga, 2008), data on coypu seasonal and annual density and dynamics of subpopulations in this area are rare, covering a
small time span (1-3 years: e.g. Doncaster and Micol, 1989; Guichón
and Cassini, 2005), and are not carried out following a meta-population
approach.
Along the Tyrrhenian coast of central Italy, coypu distribution is
patchy at regional scale with large populations in wide land reclaimed
∗
Email address: [email protected] (Corrado
Battisti)
doi:10.4404/hystrix-26.1-10981
plains (e.g. Tiber valley) and peripheral populations (sensu Rapoport,
1982; Hanski, 1982) inhabiting smaller river basins (for the area surrounding Rome, see Amori et al., 2009).
In a protected remnant wetland of Tyrrhenian Central Italy, the Local
Administration (Province of Rome) has developed a pilot study (sensu
Sutherland, 2004) since 2008 focused on the coypu population status
and trend aimed to develop a control program in this area of conservation concern (Marini et al., 2011). The project is still ongoing and
the continuous data collection on coypu density allows analysing multiyear patterns, also in relation to a set of meteorological variables. This
data sampling allowed us to estimate coypu density over a relatively
long time span.
In this work we reported the pattern of population abundance of a
coypu sub-population on a 5-year time span that shown an apparent
cycle of demographic explosion, stabilization and collapse. We tested
the effects of a set of weather parameters on coypu abundance and
discussed our results in relation to a spatial population approach (e.g.
Bjørnstad et al., 1999).
Materials and methods
The study area is located inside the “Palude di Torre Flavia” Natural Monument (hereafter named, TFNM), in Central Italy (41°58′ N;
12°3′ E).This is a protected wetland on the Tyrrhenian coast (size-area:
40 ha), designated as a Special Protection Area, according to the EU
Directive 79/409 (Code IT6030020). TFNM is the remnant of a larger wetland which, in the second half of the 20th century, was drained
and converted into an agricultural and urbanized landscape. It shows
semi-natural patchiness with ponds and channels (28 channel traits for
approximately 2055 m/10 ha), reed beds (Phragmites australis with
18th May 2015
26(1): 37–40
Figure 1 – Five-year pattern (October 2008-December 2013) in MAB (monthly mean coypu abundance and their standard deviation, s.d.: histograms) and in minimum temperatures (min
T; continuous line). Black arrow corresponds to the single meteorological event.
rare occurrences of Calystegia sepium and Sambucus nigra), flooded
meadows, dune and backdune areas, patches of Carex hirta, Juncus
acutus, Bolboschoenus maritimus and Cyperaceae (Juncetalia maritime, 1410 EU Directive habitat type), Mediterranean salt meadows
(Sarcocornetea fruticosi 1420 EU Directive habitat type), environment
back dunes (embryonic shifting dunes, 2110 EU Directive habitat type)
and annual vegetation of drift lines (1210 EU Directive habitat type).
TFNM is intensely managed for fish farming in a network of channels
(approximately 2000 m long, see above) developing mainly in a Phragmites reed bed core area. These channels have been artificially built in
the first half of the 20th century for fish farming activity. The water
supply comes largely from rainfall (meso-mediterranean xeric region
characterized by hot summer with an aridity period and cold winter;
Blasi, 1994), while flow from surrounding areas is scarce.
Water level is variable according to location and time of year, with an
evident water stress induced by fishery farm activity in late spring–late
summer (Causarano and Battisti, 2009; Battisti et al., 2008).
Coypu presence has been documented in this area since 2004 (Battisti, 2006) and some studies have been carried out on seasonal abundance (Marini et al., 2011), diet (Marini et al., 2013) and coypu impact
on biodiversity (Amori and Battisti, 2008; Battisti et al., 2008; Angelici
et al., 2012).
To estimate coypu relative abundance, individual coypu were counted directly along a standardized perimeter transect. This transect is
representative of the whole study area, extending for about 2000 m
from the southern (Ladispoli) to the northern side (Campo di mare -–
Cerveteri), and encompassing all habitat types. From October 2008 to
December 2013, a large number of replicated sessions along the transect were carried out (1140 sampling sessions; 18.1 sessions/month;
range: 5–24). In each session, we sampled the total number of individual sighted by means of a 10×50 binocular inside a 100 m wide
main belt, along a single side of the transect.
The maximum number of individual coypu observed along the transect were then grouped in monthly periods and an average monthly index of local abundance (MAB: mean abundance) was calculate, obtaining a multi-annual pattern of abundance.
From the meteorological station very close to the study site (Cerveteri, Ladispoli), we obtained the local values of minimum, medium and
higher daily temperatures, humidity and rainy (in mm, Ufficio Idrografico e Mareografico della Regione Lazio; http://www.idrografico.
roma.it/default.aspx). Since the minimum temperature (min T) was
38
highly correlated to mean and maximum temperatures (both rs =1,
p=0), we used only min T, averaging their values monthly, and correlating them to monthly MAB.
The patterns of MAB (mean monthly coypu abundance) was modelled using Generalized Linear Models (McCullagh and Nelder, 1989).
We built one model selecting as dependent variables the logarithm of
MAB recorded in the years 2009–2013 (normal distribution and identity function; we excluded year 2008 – consisting in observation ranging from October to December – from the analysis in order to allow
a whole inter-season comparison) as dependent variable. The season
(nominal variable) and the year (ordinal variable) were included in
the model as factors (categorical predictors), and min T, air humidity, and rainfall as covariates (continuous predictors); the model design
included the main effects for each variable, and the 2-way interaction
between the factors (fractional factorial design, McCullagh and Nelder,
1989). We also used univariate tests for comparing MAB values among
months by performing the non parametric Kruskal-Wallis test (Dytham,
2010).
We set alpha level to 0.05, using the SPSS 13.0 software for Windows
(SPSS, 2003). We followed the requisites requested for reliable data
reported in Battisti et al. (2014).
Results
Overall, we obtained 2272 records of coypu during 1140 sampling sessions.
On a larger time scale (2008–2013) we observed a first phase of
demographic explosion (higher MAB: autumn-winter 2008), followed
by two years of stabilization (2009–2011) and a consequent collapse
(2012–2013; see Fig. 1). In detail, from February 2009, we observed a
yearly based hump-shaped pattern, with a progressive increase in MAB
from winter to summer, and a decline from late summer to winter with
significant changes among months (2009: χ2 =55.9; 2010: χ2 =156.2;
2011: χ2 =132.9, p<0.01, Kruskal Wallis test).
The MAB significantly varied among seasons and along the years
with a clear effect of the interaction term YEAR*SEASON on the considered variable (Tab. 1 and Fig. 2). MAB showed a minimum in
winter with a gradual increase through spring until reaching a peak in
summer (Fig. 2a). During the five years of observations, coypu MAB
showed an abrupt decrease after 2010 (Fig. 2b). The interaction term
showed that coypu abundance started to collapse at the end of 2012
(winter) when no coypu was observed in the study site. The minimum
Coypu sink population collapse
temperature (average monthly values) strongly influenced MAB with a
positive relationship (Tab. 1). Air humidity and rainfall did not show
any effect on coypu abundance. As for the seasonal distribution of the
monthly MAB within a given year, a hump-shaped pattern is evident in
2009 (excluding January), 2010 and 2011. From 2010 to 2011, MAB
patterns showed a progressive decline in their modal values until 2012
and 2013, when we documented a collapse by observing few individuals occasionally.
Discussion
During the five-year period, irregular inter- and intra-annual MAB
patterns of coypu subpopulation were observed. Following a phase
of occasional presence documented in local literature (first individuals observed in 2004; Battisti, 2006), from autumn 2008, a colonization phase, characterized by a sudden increase in abundance, was
observed. Then, starting from spring 2009 until 2011, three periodic hump-shaped yearly patterns of coypu abundance were registered,
likely corresponding to the phase of stabilization. This phase was characterized by strong inter-and intra-annual oscillations (higher MAB
values in 2010, lower in 2011 and higher values in summer when compared to winter). Finally, in 2012 and 2013, only a few coypu were
occasionally observed, no longer distributed in a clear seasonal pattern.
We found an overall and significant correlation between MAB and
min T. The lowest min T (<5 ◦C) was recorded in February 2012. In this
month, presence of unbroken ice sheets on water surface, which prevent
coypus from getting into the water, and the lack of thick vegetative cover
above ground, contributed to exacerbate the impact of cold events on
the species.
Our findings on this issue are consistent with the relationship
between temperature and coypu abundance reported in literature (Doncaster and Micol, 1990). Other factors, such as humidity and rain, apparently did not affect MAB.
Moreover, the correspondence between a strong isolated meteorological event (wetland waters froze during a snowing event in February
2012: local min T about 0 ◦C; personal observation) and the disappearance of a clear hump-shaped patterns due to a consequent collapse
suggests that this stochastic event could, at least partially, have played a
role in the observed demographic variation. Probably this factor acted
on a population yet declining for other undetected causes. However,
while in the years before 2012 (2008–2010), the population showed a
yearly decline in winter followed by a recovery from spring to summer,
after the winter 2012 no population recovery was observed.
Density-independent environmental stochasticity (e.g. weather
factors) may be an important factor affecting population dynamics in
mammals (e.g. Post and Stenseth, 1998; Sibly et al., 2005; Saether,
1997), changing their dispersal and population growth (Usher, 1986),
especially in small populations (Caughley, 1994). As for coypu, it
has been suggested that its density is strictly related to the absence of
severe winters as well as to resource availability (Reggiani et al., 1995;
Carter and Leonard, 2002). Therefore, physiological sensitivity to cold
weather could act as a strong selective factor, since in cold winter climate, when temperatures are below freezing for several days, coypu
density decreases by increasing reproductive failure, abortion, and juvenile mortality (Doncaster and Micol, 1989, 1990; for Mediterranean
region: Velatta and Ragni, 1991; Reggiani et al., 1995; Bertolino et al.,
2005).
This response to climatic conditions (and to other stochastic events)
may not be universal. For example, when a population is organized as
meta-population, the effects of a cold winter may be limited or absent,
at least in central sub-populations where the effects of local meteorological events may be counterbalanced by a higher birth rate and dispersal
from other sub-populations (Doncaster and Micol, 1990; Bertolino et
Table 1 – Synopsis of the Generalized Linear Model (fractional factorial design) results,
showing which parameter (including the between effects) significantly influence the MAB
in the study species at the study area. MIN T: mean minimum monthly air temperature.
Significant effects are in bold.
Figure 2 – Significant effects of SEASON (A), YEAR (B), and the interaction term SEASON*YEAR (C) on MAB (log transformed). For Wald statistics and statistical significance of
each effect refer to the Generalized Linear Model results shown in Tab. 1.
Variables
Intercept
MIN T
HUMIDITY
RAINFALL
SEASON
YEAR
SEASON*YEAR
Degrees of freedom
1
1
1
1
3
4
12
Wald statistic
0.923
7.956
0.712
0.866
22.303
183.067
80.869
p
0.337
0.005
0.399
0.352
0.00006
0
0
39
26(1): 37–40
al., 2005; Panzacchi et al., 2007; Cocchi and Riga, 2008). Since we observed an evident demographic collapse after the cold event in winter
2012 not followed by a prompt population recovery, we hypothesize
that our peripheral population may be a sink (Pulliam, 1988; Gosselin,
1996; Dias, 1996) of a larger meta-population diffused on regional scale
(i.e., corresponding to the large Tiber river valley). This sink may be
only occasionally interested by the occurrence of immigrant individuals that use this habitat patch more as a temporary trophic area (due
the great cover of Juncetalia maritimi rush-beds and others palatable
plants; Marini et al., 2013), than as a reproductive site (Aliev, 1973).
The interpretation of our data based on a multi-annual cycle of a
coypu subpopulation inhabiting a remnant wetland allowed us to postulate an a posteriori hypothesis that should be tested in further research (inductive approach; Romesburg, 1981; Guthery, 2007), that
is: single winter meteorological events (i.e. severe temperature, snow
cover, frozen water surface) may contribute to induce collapses of peripheral sub-populations on a large temporal scale.
Although the long-term analysis conducted on a Mediterranean
coypu population represents a key factor of our study, our data were
based on observational data and the only demographic parameter used
was a population trend index. Although this index may be useful to
detect demographic patterns at coarse-grain temporal scale, we think
that its predictive power to detect more fine-grained patterns, e.g. seasonally referred, may be very limited since the monthly variation could
reflect more the activity of the animals (or their detectability across
vegetation) then real variation in population density at monthly scale.
Therefore, since in this case data on population dynamics may be biased
(Gibbs, 2000; Meier and Fagan, 2000), and other more fine-grained
parameters at single and regional population level (for example, juvenile individual density, reproductive failure, mortality rates, and adult
survival) are needed to support our hypothesis.
Implications for management
At least for peripheral sub-populations, management plans should also
take into consideration the uncertainty deriving from stochastic events.
Indeed, such events, given their disruptive effects on local demography,
may facilitate control and eradication actions Therefore, assessing the
status of a coypu sub-population following a dynamic meta-population
approach and checking the role of stochastic events is determinant to
define the type and regime of actions in an eradication program and to
determine the priority of sub-populations on which control should be
concentrated.
References
Aliev F.F., 1973. Cases of mass mortality of nutria in the wetlands of Azerbaidzhan in
winter 1971-1972. Mammalia 36: 539–540.
Amori G., Battisti C., 2008. An invaded wet ecosystem in central Italy: an arrangement and
evidence for an alien food chain. Rend. Fis. Acc. Lincei 19: 161–171.
Amori G., Battisti C., De Felici S., 2009. I Mammiferi della Provincia di Roma. Dallo
stato delle conoscenze alla gestione e conservazione delle specie. Provincia di Roma,
Assessorato alle politiche dell’agricoltura, Stilgrafica, Roma. [in Italian]
Angelici C., Marini F., Battisti C., Bertolino S., Capizzi D., Monaco A., 2012. Cumulative
impact of rats and coypu on nesting waterbirds: first evidences from a small Mediterranean wetland (central Italy). Vie et Milieu — Life and Environment 62: 137–141.
Battisti C. (Ed.), 2006. Biodiversità, gestione, conservazione di un’area umida del litorale
tirrenico. Gangemi editore – Provincia di Roma, Assessorato alle politiche agricole e
dell’ambiente, Roma. [in Italian]
Battisti C., Luiselli L., Pantano D., Teofili C., 2008. On threats analysis approach applied to
a Mediterranean remnant wetland: is the assessment of human-induced threats related
into different level of expertise of respondents? Biodiv. Conserv. 16: 1529-–1542.
Battisti C., Dodaro G., Franco D., 2014. The data reliability in ecological research: a proposal for a quick self-assessment tool. Natural History Science 1: 75–79.
Bertolino S., Genovesi P., 2007. Semiaquatic mammals introduced into Italy: Case studies
in biological invasion. In: Gherardi F. (Ed.) Biological invaders in inland water. Profiles,
distribution and threats. Springer, Netherlands. 175-–191.
Bertolino S., Perrone A., Gola L., 2005. Effectiveness of coypu control in small Italian
wetland areas. Wildlife Society Bulletin 33: 714–720.
Bjørnstad O.N., Ims R.A., Lambin X., 1999. Spatial population dynamics: analyzing patterns and processes of population synchrony. Trends Ecol. Evol. 14: 427-432.
Blasi C., 1994. Fitoclimatologia del Lazio. Carta del fitoclima del Lazio. Università La
Sapienza, Roma. [in Italian]
Callahan C.R., Henderson A.P., Eackles M.S., King T.L., 2005. Microsatellite DNA markers for the study of population structure and dynamics in nutria (Myocastor coypus).
Molecular Ecology Notes 5: 124–126.
Caughley G., 1994. Directions in conservation biology. J. Appl. Ecol. 63: 215–244.
Causarano F., Battisti C., 2009. Effect of seasonal water level decrease on a sensitive bird
assemblage in a Mediterranean wetland. Rend. Fis. Acc. Lincei 20: 211–218.
Carter J., Leonard B.P., 2002. A review of the literature on the worldwide distribution,
spread of, and efforts to eradicate the coypu (Myocastor coypus). Wildl. Soc. Bull. 30:
162–175.
Cocchi R., Riga F., 2008. Control of a coypu Myocastor coypus population in northern Italy
and management implications. Ital. J. Zool. 75: 37–42.
Dias P.C., 1996. Sources and sinks in population biology. Trends Ecol. Evol. 11: 326–330.
Doncaster C.P., Micol T., 1989. Annual cycle of a coypu (Myocastor coypus) population:
male and female strategies. J. Zool., London 217: 227–240.
Doncaster C.P., Micol T., 1990. Response by coypus to catastrophic events of cold and
flooding. Ecography 13: 98–104.
Dytham C., 2010. Choosing and using statistics. A biologist’s guide. Third Edition.
Cheichester Wiley Blackwell, UK.
Gibbs J.P., 2000. Monitoring populations. In: Boitani L., Fuller T.K. (Eds.) Research techniques in animal ecology: controversies and consequences. Columbia University, New
York, USA. 213–252.
Gosselin F., 1996. Extinction in a simple source/sink system: application of new mathematical results. Acta Oecologica 17: 563–584.
Guichón M.L., Cassini M.H., 1999. Local determinants of coypu distribution along the
Luján River, East-central Argentina. J. Wildl. Manag. 63: 895–900.
Guichón M.L., Cassini M.H., 2005. Population parameters of indigenous populations of
Myocastor coypus: the effect of hunting pressure. Acta Theriologica 50: 125–132.
Guthery F.S., 2007. Deductive and inductive methods of accumulating reliable knowledge
in wildlife science. J. Wildl. Manag. 71: 222–225.
Hanski I., 1982. Dynamics of regional population distribution: the core and satellite hypothesis. Oikos 38: 210–221.
Hanski I., 1998. Metapopulation dynamics. Nature 396: 41-–49.
Marini F., Ceccobelli S., Battisti C., 2011. Coypu (Myocastor coypus) in a Mediterranean
remnant wetland: a pilot study of a yearly cycle with management implications. Wetl.
Ecol. Manag. 19: 159–164.
Marini F., Gabrielli E., Montaudo L., Vecchi M., Santoro R., Battisti C., Carpaneto G.M.,
2013. Diet of Coypu (Myocastor coypus) in a Mediterranean coastal wetland: a possible
impact on threatened rushbeds? Vie et Milieu -– Life and Environment 63: 97–103.
McCullagh P., Nelder J., 1989. Generalized Linear Models. Chapman and Hall, London.
Meier E., Fagan W.F., 2000. Will observation error and biases run the use of simple extinction models? Conserv. Biol. 14: 148–154.
Panzacchi M., Cocchi R., Genovesi P., Bertolino S., 2007. Population control of coypu
Myocastor coypus in Italy compared to eradication in UK: a cost-benefit analysis. Wildlife Biol. 13: 59–171.
Post E., Stenseth N., 1998. Large-scale climatic fluctuation and population dynamics of
moose and white-tailed deer. J Anim Ecol. 67: 537–543.
Pulliam H.R., 1988. Sources, sinks, and population regulation. Am. Nat. 132: 652–661.
Rapoport E., 1982. Areography – Geographical strategies of species. Pergamon, New York.
Reeves S.A., Usher M.B., 1989. Application of a diffusion model to the spread of an invasive
species: the Coypu in Great Britain. Ecol. Modell. 47: 217–232.
Reggiani G., Boitani L., De Stefano R., 1995. Population dynamics and regulation in the
coypu Myocastor coypus in central Italy. Ecography 18: 138–146.
Romesburg H.C., 1981. Wildlife science: gaining reliable knowledge. Journal of Wildlife
Management 45: 293–313.
Saether B.E., 1997. Environmental stochasticity and population dynamics of large herbivores: a search for mechanisms. Trends Ecol. Evol. 12: 143–149.
Schippers P., Verboom J., Knaapen J.P., van Apeldoorn R.C., 1996. Dispersal and habitat connectivity in complex heterogeneous landscapes: an analysis with a GIS-based
random walk model. Ecography 19: 97–106.
Sibly R.M., Baker A.D., Dehman M.C., Hone J., Pagel M., 2005. On the regulation of
populations of mammals, birds, fish, and insects. Science 309: 607–610.
SPSS Inc., 2003. SPSS for Windows — Release 13.0 (1 Sept. 2004). Leadtools ©. Lead
Technologies Inc.
Sutherland W.J., 2004. Ecological census techniques. Blackwell Science, Massachussets.
Usher M.B., 1986 Invasibility and wildlife conservation: invasive species on nature reserves. Philosoph. Trans. Royal Soc., London B 314: 695–710.
Velatta F., Ragni B., 1991. The coypu population in Lake Trasimeno. Population parameters
and numerical control. In: Spagnesi M., Toso S. (Eds.), II Congresso Nazionale dei
Biologi della Selvaggina, Abstracts, Suppl. Ric. Biol. Selvaggina 19. 311-–326.
Associate Editor: L.A. Wauters
40
Volume 26 (1): 41–45, 2015
doi:10.4404/hystrix-26.1-9946
Research Article
Tusker’s social bonds in Rajaji
Ritesh Joshia,1,∗
a
Conservation & Survey Division, Ministry of Environment, Forest & Climate Change, Indira Paryavaran Bhawan, Jor Bagh Road, New Delhi 110003, India
Keywords:
Asian elephant
male social behaviour
long-term association
conservation
Rajaji National Park
Article history:
Received: 5 March 2014
Acknowledgements
Author would like to acknowledge the anonymous reviewers and the
Associate Editor who have provided valuable inputs and comments on
the previous versions of the manuscript and contributed significantly to
improve the manuscript to its present form. Author would also like to
acknowledge G.B. Pant Institute of Himalayan Environment & Development, and Doon Institute of Engineering and Technology for infrastructure support, and to the Uttarakhand Forest Department, especially the
administration of the Rajaji National Park and Haridwar forest division
for providing permission to conduct research on elephant behaviour.
Thanks are due to Mr. Somnath and Mr.Umed Singh, Haridwar Forest
Division, Mr. Shanti Prasad, Field Assistant and Mr. Sunil Pal and Mr.
Swarup Puri for their valuable help in collection of the field data. Finally, I would like to thank Dr. Kamal Kant Joshi, Assistant Professor,
Graphic Era Hill University for assisting in data analyses.
Abstract
Male elephants are known to live a solitary life after attaining the pubertal stage which is considered at the age of about 15 years. However, observations of single young males (about 10 years
old) have also been reported. In contrast, few studies have explored that male elephants do have
associations; however these associations are occasional and temporary. In Rajaji National Park,
north-western Shivalik landscape of India, bull elephants were observed to have a year round association, mainly to perform movements outside the boundaries of protected habitats and to enjoy
palatable crops. A recognised group of bull elephants (c. 2–8) was recorded between 2006–2010,
performing movements in parts of Rajaji National Park, Haridwar forest division and agriculture
fields nearby the protected habitats. Bull elephant interactions and social bond are illustrated. Since
a long continuous chain of forests, which existed in the Rajaji–Corbett wildlife corridor, has been
disrupted mainly because of habitat fragmentation, and since man-elephant conflict is increasing
rapidly, regular monitoring of elephant habitat and population dynamics is of paramount importance. This is the first time that male-male interactions/male elephant behaviour in groups has been
recorded from north-west India and possible explanations for the behaviour are discussed.
Introduction
Elephants live in a matriarchal society, where the oldest female usually leads the group. In contrast, bull elephants prefers to live solitary
life, especially after attaining the pubertal stage. However, their movements are confined nearer to the groups during mating period in search
of oestrous females. During this period, bull elephants randomly join
and leave the groups. Male elephants leave their families when they are
on the threshold of sexual maturity, usually between the age of ten and
fifteen years, and bulls use to wander on their own or seek the company
of other bulls after leaving their families. Besides, since male elephants
cannot recognize their children, they do not show interest in taking care
of young (Sukumar, 1989, 1994). Various aspects of social organisation have been studied in African Savannah elephants (Loxodonta africana africana) (Vidya and Sukumar, 2006). However, only few studies
have been conducted on this aspect in the range of the Asian elephant
(Elephas maximus) and more information on their complex social organization is yet to be documented.
In a long-term study carried out on the behaviour and movement of
adolescent male African elephant in the Okavango Delta, Botswana, it
was revealed that adolescence in male African elephants is an important social period, reflecting in higher levels of social interactions and a
preference for being in larger social groups than older males (Evans and
Harris, 2008). This study also revealed that adolescent males can gather
∗
1
Email address: [email protected] (Ritesh Joshi)
During the study period the author was associated with the G.B. Pant Institute of Himalayan Environment & Development, Garhwal Unit, Srinagar-Garhwal, Uttarakhand,
India, and Doon Institute of Engineering & Technology, Rishikesh, Uttarakhand, India.
doi:10.4404/hystrix-26.1-9946
information about new areas and learn about the new social system they
have entered into, using the mature bulls as social and ecological repositories of knowledge and therefore, post-prime bulls still have an
important role to play in the social system of male elephants. Bradshaw and Schore (2007) based on their review on relationship between
developmental context and behaviour outcome, have exposed that ethological, psychological and neurobiological models are needed to gain
deeper insights into the relationships between developmental contexts
and behaviour outcomes. In another similar study carried out on elephant’s association network, it was argued that male social clusters have
a heterogeneous age distribution and most of the males prefer to associate with age peers and some prefer to associate with individuals
younger or older than them (Chiyo et al., 2012). This study suggested
that raiding is acquired through social learning from older males which
are raiders. The tendency of individual elephants to associate with one
another to form transient or stable same-sex or mixed-sex groups, or
to remain solitary may be an important component of their life-history
strategies (Srinivasaiah et al., 2012).
The above referred studies are examples that illustrate new dimensions in conservation based research, showing that elephant complex
social behaviour should be studied in the context of changing environment. The factors motivating individual Asian elephants to form specific associations in different socio-ecological environments needs to
be thoroughly investigated (Srinivasaiah et al., 2012).
Here, I present a study of the social bonds and long-term association
among male Asian elephants in eastern part of the Rajaji National Park
and north-eastern part of the Haridwar forest division, India, in relation
to the social behaviour of bull elephants and strategies to raid crops. By
25th April 2015
26(1): 41–45
my knowledge, this is the first study of this type of behaviour among
male Asian elephants.
graphic evidence. Geographical coordinates of each observation were
taken (Garmin GPS 72).
Study Area
Results and Discussion
′
Rajaji National Park (RNP) is located in north–west India at 29°15 –
30°31′ N 77°52′ –78°22′ E, falls under the Gangetic plains biogeographic zone and upper Gangetic plains province (Fig. 1). Maximum
portion of the park lies under Shivalik’s biogeographic sub-division.
RNP was established in 1983 with the aim of maintaining a viable
Asian elephant (Elephas maximus) population and is designated a reserved area for “Project Elephant” by the Ministry of Environment,
Forest & Climate Change, Government of India. The total size of
the park is 820.21 km2 . The dominant vegetation of the area comprises Sal Shorea robusta, Kamala Mallotus phillipinensis, Cutch Acacia catechu, Kadam Adina cordifolia, Bahera Terminalia bellirica, Indian Banayan Ficus bengalensis and Indian Rosewood Dalbergia sissoo. The dominant fauna of the park consists of tiger Panthera tigris,
leopard Panthera pardus, Himalayan black bear Ursus thibetanus, sloth
bear Melursus ursinus, Striped Hyaena Hyaena hyaena, barking deer
Muntiacus muntjak, goral Nemorhaedus goral, spotted deer Axis axis,
sambar Cervus unicolor and wild boar Sus scrofa, and among reptiles the mugger crocodile Crocodylus palustris and king cobra Ophiophagus hannah. Haridwar Forest Division (HFD) is located adjacent
to the RNP (in the north) at 29°58′ 6.02′′ N, 78°13′ 9.82′′ E and well
connected with the Lansdowne Forest Division. The dominant fauna
in HFD is the same as in RNP.
A year round association of a recognized group of eight adult/sub-adult
bull elephants was observed in RNP and in part of HFD from 2006 to
2010. A total of 521 random observations, made between January 2006
and December 2010 revealed that this recognized group of eight bulls
performed co-movements in outskirts of RNP and HFD and outside
of the protected areas, in the agriculture fields. However, movements
of single bull elephants from this group were also recorded at several
occasions. Elephant group formation was analysed between two major seasons (summer and winter) over the entire study period. Results
revealed that groups were seen more often than expected in summer
season (mean number of observations per year±SD=40±13) as compared to winter season (mean value±SD=6±2; One-sample goodnessof-fit test χ2 =263.5; df=1; p<0.0001). There was no difference between
years (year-effect χ2 = 4.29; df=4; p=0.37) These recognized bull elephants were found moving in a stable group on 284 occasions (55%) i.e.
they moved in a close group composed of all individuals, whereas on
173 occasions (33%), loose group movements were recorded i.e. only
some individual of the recognized group were found moving together
(2–5 bulls). However, solitary movement of some bull elephants of the
group was recorded on 64 occasions (12%).
Comparison between the recognized group movement and solitary movement of individual bull elephants from the group in summer and winter seasons respectively revealed that movement of bull
elephants in group was significantly higher as compared to solitary
movement of the bulls in summer season as compared to winter (Onesample goodness-of-fit test on solitary movements between seasons
χ2 =10.6; df=1; p=0.0012) However, at the onset of summer, elephant
movement outside from the protected area was observed rarely (mean
Figure 1 – Location map of the Rajaji national Park.
(a)
Methods
This paper is part of my long-term study on elephants in RNP and HFD.
Field data was collected randomly between 2006 to 2010 from Chilla
and Gohri forests of the RNP and Shyampur and Chiriapur forests of
the HFD. Since all these forest ranges exists in a same biological area
and movements of various groups and bull elephants can be defined on
a seasonal basis, I was able to identify all those bull elephants whose
movements were confined within these forest ranges. Male elephants
were identified on the basis of their tusk shape and size (tusk length and
thickness, pointed or curved shape, upward or downward tilt, broken
signs, if having only one tusk, left or right tusk, etc.), tail shape and
size (full or cut tail, bunch of hairs at tip etc.), ear forms (ear fold,
pigmentation, scars, holes, etc.), and pigmentation on trunk base.
Movements of single bulls and bull groups in buffer zones and crop
fields were also recorded on a seasonal basis. In addition, information
on the movement of bull elephants was also collected from the forest
officials, Gujjars residing in HFD and local people. Field binocular
(Nikon Action Series, 10×50 CF) was used to observe the elephants in
forests and Nikon Coolpix 8700 Camera was used to produce photo42
(b)
Figure 2 – a) Number of observations of group movement of recognized bull elephants
(with standard error); b) Solitary movement of individuals from the recognised group of
bull elephants (with standard error), during summer and winter seasons respectively from
2006 to 2010.
Male elephant social behaviour
(a)
(b)
(c)
(d)
(e)
(f)
Figure 3 – a, b, c) A group of male elephants on Haridwar–Bijnor national highway existing across Haridwar forest division, while moving towards Ganges; d, e) Made for each other:
bull elephants are playing in Haridwar forest division; f) Bull elephant swimming in Ganges.
value=5.5±1.2), and in smaller groups (c. 2–4) or solitary (Fig. 2ab). Usually, bull elephants used to form such groupings in evening
hours, when they start moving towards agriculture fields to enjoy palatable crops, especially from early evening hours to dawn (for nearly 14
hours). However, from early morning hours to evening hours, generally
they used to perform solo movements, which include hovering nearer to
the groups, which had receptive females. Sometimes they spent whole
day in a female group as well.
Joining of new bull in the group and separation of one or two bull
from the group was recorded randomly, which influenced the size of the
recognised bull group (sometimes to 6, 7 or 8 elephants). Largest association of the recognised bull elephant group was observed in May 2006
and June 2007 consisting of seven individuals and in December 2008
and June 2009 consisting of eight individuals. In contrast, in 2010 the
largest association of the group was recorded in November and December consisting of six individuals.
43
26(1): 41–45
Observations on co-movements and social behaviour of these bulls
revealed that they had a strong social bond and well developed
strategies to move across the buffer areas (outskirt areas) of the protected habitats. An adult bull elephant aged more than 50 years was observed leading the group especially when they were performing movements across the populated areas and agriculture fields. On several
occasion especially during summer, they were found standing under
cool shaded trees like Ficus bengalensis and Adina cordifolia to take
rest. Several times they were found playing together, by pushing each
other with trunk and placing trunk over to back of others and enjoying
swimming in Ganges (Fig. 3a-f). Play fighting is important in developing male social organisation and new hierarchies and helps in avoiding
serious conflict when there is competition for resources (Desai, 1997).
On occasions, when any one of them remained behind, they were observed waiting for the companion. Some bull fights were observed during the course, however, any conflict for courtship preferences was not
observed.
Unfortunately in the night of 15th July 2008, the oldest bull elephant
died due to electrocution in Shyampur forest. This master bull ruled
over to the eastern part of the RNP for more than a decade. The magnificent bull elephant had assisted other bull elephants especially juveniles in learning about the traditional journeys and feeding grounds.
Since this oldest bull was leading and educating other bulls about itinerant in traditional grounds, after its death changes in the behaviour
of other bulls were observed (movement of remaining bulls was observed isolated or in small group of 2–3 animals, they faced problems
in crossing the highway especially in evening hours, their movements
across the Ganges was restricted to night hours etc.).
Factors that influence learning and the spread of behaviour in wild
animal populations are important for understanding species responses
to changing environments and for species conservation (Chiyo et al.,
2012). An important, often neglected aspect of behavioural ecology
concerns the ability of animal populations and individuals to respond
to changes in their immediate environment, both in the long and short
term (Srinivasaiah et al., 2012).
In 2009-2010 temporary co-movements of remaining six bull elephants were observed randomly and recorded. They were found performing solo movements during day hours, however used to assemble
at a place in evening hours, particularly to move in a group towards crop
fields. Since bull elephants are known to live solitary life and used to
raid crops in groups, this association might be a strategy for enjoying
palatable crops. Such strategies of bull elephants however are temporary and for achieving some particular object, but can affect their social
behaviour especially in context of ranging pattern. This could also enhance the rate of man-elephant conflict. Adult and sub-adult male elephants represent a higher propensity of occurrence in high-disturbance
areas when associated in a group, while solitary elephants exhibit the
least propensity to occur in such areas (Srinivasaiah et al., 2012). A
study carried out on the influence of life history milestones among male
African elephants revealed that older males are more likely to be raiders than younger males, that males are more likely to be raiders when
their closest associates are also raiders, and when their second closest
associates are raiders older than them (Chiyo et al., 2012).
Studies carried out on male-male interactions and bonds in parts of
Asia recorded that bull elephants do have associations, though temporary, ranging from 2–6 individuals (recorded in Ceylon), 2–3 individuals
(recorded in southern India) and up to 5 individuals (recorded in northwest India) (McKay, 1973; Sukumar, 1994; Joshi and Singh, 2008).
For male African elephants, it was shown that younger male elephants
seek out older males and learn social behaviour from them and that larger groups of bull elephants (up to 15 individuals) of mixed age groups
can persist for many years (O’Connell-Rodwell, 2010).
Since most of the associations among bull elephants have been observed in parts of RNP and HFD for raiding crops, some of the cultivators of affected villages, situated along the Ganges were consulted
and the datasets were compared with elephant movement. Elephant
group (c. 4–18) which includes adult males and females, sub-adult
males and females and juveniles were observed frequently before 200144
2002 in eastern part of RNP, visiting Ganges, flowing across the HFD,
and crop fields through crossing the Haridwar-Bijnor national highway. However, movement of groups with calves (infants less than 6
months) was only observed up to Ganges and not in the agriculture
fields. In HFD, the tracks from where elephants are known to perform
movements towards Ganges are adjoined to the central part of RNP,
which holds Motichur-Chilla wildlife corridor as well. Soon after the
establishment of Uttarakhand state in late 2000, group movements were
bunged mainly because of increasing rate of development activities, including expansion of road network, construction of six bridges over to
various annual rivers (that served as passage for elephants), establishment of human settlements, etc. Thereafter, solo movement of some
recognised bulls (≈2)continued for nearly two years (2003–2004) and
slowly other bull elephants, especially sub-adults and juveniles started
to follow some older bulls, which finally converted to a big group (c.
2–9) (Fig. 2a-b).
Based on the field observations, it seems that crop raiding by elephants will continue in various parts of north-western Shivalik landscape. Does these aberrant behaviour among male elephants is a
strategy to raid crop? Are these male-male aggregations the result of
habitat isolation? To address all these issues, long-term monitoring
studies are needed, which can then serve to propose possible conservation actions.
Finally, it needs to be mentioned that in 1970s, after the establishment of Chilla hydro-electric power plant/channel, RNP was divided
into two major parts -– the eastern and western part. Later on, after
the establishment of Uttarakhand state in 2000, increased rate of traffic
pressure in Haridwar–Dehradun national highway and railway track,
which exist across RNP, had restricted elephant movement in between
these forests, as a result of which larger population of elephants were
pocketed into smaller ones. This had disrupted the connecting corridor
for elephant movement in between Rajaji and Corbett National Park
as well and escalated man-elephant conflict in north-western Shivalik
landscape.
Conclusions and management guidelines
The eastern part of RNP and north-eastern part of HFD are one of the
crucial elephant habitats in north-western Shivalik landscape. However, isolation of large migratory corridors, increasing rate of anthropogenic activities and unnatural deaths of tuskers are growing problems threatening long-term survival of the elephant population (see
also Joshi and Singh, 2010). Generally, elephants used to migrate towards parts of Corbett Tiger Reserve (in Lansdowne forest division and
Sonanadi Wildlife Sanctuary) at the onset of monsoon and return back
to the RNP and HFD, in the upper Gangetic plains at the onset of summer. However, it is uncertain whether some of the bulls are still following these traditional journeys.
For sustainable management of the elephants in this region, the following recommendations can be made: 1) Shyampur and Chiriapur
forest ranges of HFD should be merged in RNP to strengthen conservation approaches. 2) Three to four large underpasses (siphons) should
be constructed in Haridwar-Bijnor national highway at the points where
elephants are known to cross. They need to be kept clean, since debris
and stones are deposited rapidly through annual streams especially
in monsoon. 3) Few small islands situated in Ganges and riparian
corridors should be restored and freed from anthropogenic activities.
4) Gujjars (a nomadic pastoral community) who are residing in the
Shyampur and Chiriapur forest ranges of the HFD, need to be rehabilitated, to restore the ecosystem. 5) Within the recognised bull group,
one of the older bull should be radio-collared to monitor their movements and facilitate studies on social behaviour. 6) Chilla-Motichur
(c. 3.5 kilometer long and 1.0 kilometer wide) and Rawasan-Sonanadi
(c. 10.0 kilometer long and 5.0 kilometer wide) wildlife corridors
should be restored avoiding anthropogenic and developmental activities. 7) Bridges, which are located over to Chilla power channel, one
at Soni shroath and another at Kunao shroath (water streams), should
be widened. These bridges are ≈3.5 meter wide. Two more bridges
could be constructed over to the power channel, one at Ram shroath, in
Male elephant social behaviour
between Chilla power house and Kaudia village and another at Kunao,
in between Binj river and Kunao bridge. These possible approaches
can give elephants a larger number of corridors to move across Ganges,
which lies in Chilla-Motichur corridor as well.
References
Bradshaw G.A., Schore A.N., 2007. How elephants are opening doors: developmental neuroethology, attachment and social context. Ethology 113: 426–436.
Chiyo P.I., Moss C.J., Alberts S.C., 2012. The influence of life history milestones and association networks on crop-raiding behaviour in male African elephants. PLoS ONE 7(2):
e31382.
Desai A., 1997. The Indian elephant. Vigyan Prasar, New Delhi and Sanctuary Magazine
(NCSTC-Hornbill Natural History Series), Mumbai joint Publication, India.
Evans K.E., Harris S., 2008. Adolescence in male African elephants, Loxodonta africana,
and the importance of sociality. Animal Behaviour 76: 779–787.
Joshi R., Singh R., 2008. Unusual behaviour of Asian elephants in the Rajaji National Park,
North-west India. Gajah 29: 32–34.
Joshi R., Singh R., 2010. Does wide ranging tuskers survive in north-west India? National
Academy Science Letters 33(7–8): 205–215.
O’Connell-Rodwell C., 2010. How male elephants bond. Article published in the Smithsonian Magazine, November 2010. Available from http://www.smithsonianmag.com/
science-nature/how-male-elephants-bond-64316480/
McKay G.M., 1973. Behavior and ecology of the Asiatic elephant in southeastern Ceylon.
Smithsonian Contributions to Zoology 125, Smithsonian Institution Scholarly Press,
Washington, D.C.
Srinivasaiah N.M., Anand V.D., Vaidyanathan S., Sinha A., 2012. Usual populations, unusual individuals: insights into the behaviour and management of Asian elephants in
fragmented landscapes. PLoS ONE 7(8): e42571.
Sukumar R., 1989. The Asian Elephant: Ecology and Management. Cambridge Studies in
Applied Ecology and Resource Management, Cambridge University Press, Cambridge.
Sukumar R., 1994.Elephant Days and Nights: Ten Years with the Indian Elephant. Oxford
University Press, New Delhi, India.
Vidya T.N.C., Sukumar R., 2005. Social and reproductive behaviour in elephants. Current
Science 89(7): 1200–1207.
45
Volume 26 (1): 47–51, 2015
doi:10.4404/hystrix-26.1-11035
Research Article
The masked invader strikes again: the conquest of Italy by the Northern raccoon
Emiliano Moria,∗, Giuseppe Mazzab,c , Mattia Menchettib , Mattia Panzerid , Yann Gagere , Sandro Bertolinoa , Mirko Di Febbrarof
a
c
University of Turin, Department of Agronomy, Forestry and Food Sciences, Entomology and Zoology, Largo Paolo Braccini 2, 10095 Grugliasco (Turin), Italy
b
University of Florence, Department of Biology, Via Romana 17, 50125 Florence, Italy
Council for Agricultural Research and Economics - Agrobiology and Pedology Research Centre (CRA-ABP), via di Lanciola 12/a, 50125 Cascine del Riccio, Florence, Italy
d
Università degli Studi dell’Insubria, Dipartimento di Scienze Teoriche e Applicate, Unità di Analisi e Gestione delle Risorse Ambientali
– Guido Tosi Research Group, Via J.H. Dunant 3, 21100 Varese, Italy
e
Max Planck Institute for Ornithology, Dept. of Migration and Immuno-Ecology, Am Obstberg 1, 78315 Radolfzell, Germany
f
University of Molise, Department of Biosciences and Territory, C.da Fonte Lappone, 86090 Pesche (Isernia), Italy
Keywords:
Procyon lotor
invasive alien species
range expansion
potential distribution
Article history:
Received: 18 December 2014
Accepted: 17 April 2015
Acknowledgements
Authors thank F.M. Angelici, M. Ferri, D. Righetti, P. Genovesi, P. Debernardi, S. Capt, T. Duscher, I. Ungari, L. Ravizza, L. Rossetti, J. Kotnik, D.
Sonzogni, G. Jiraux, F. Koike, M. Ishiguro, H. Keiser and A. Pegoiani for
helping in data collection. G. Petri and P. Jennings revised the English
grammar and syntax of the manuscript. Marten Winter kindly took the
time to improve the first draft of this manuscript.
Abstract
The Northern raccoon Procyon lotor is a species native to North and Central America, but alien
populations have established in Europe, several Caribbean islands, Azerbaijan, Uzbekistan and Japan, being introduced for fur farming, hunting, or as pets/attraction in animal parks. In the introduced range, raccoons may impact on breeding birds and amphibians, exert crop damages and
transmit pathologies to wild species and humans. The species has been introduced also in Italy,
where the only known reproductive population is observed since 2004 in Lombardy, along the
Adda river. We reconstructed the current distribution range of the Northern raccoon in Italy, collecting information from scientific papers, articles in newspapers and books, as well from experts
and local reporters. A total of 53 occurrence points were collected from observation sites. Since
2008, records from Lombardy increased, and sporadic observations were reported from seven other
regions. A complete lack of records from the Northernmost provinces of Lombardy (Varese, Como
and Sondrio) suggests that the only Italian population does not derive from a range expansion from
Switzerland, but it should be considered as an independent, new introduction. Accidental observations of single individuals possibly escaped from captivity are often ignored, and only few animals
were removed from the wild. An analysis of the potential distribution of the species was performed
in a species distribution modeling framework (MaxEnt). A global model was built up considering
the occurrences of reproductive populations from the native range and introduced areas in Europe
and Japan and then projected to Italy. The model suggested a good suitability for the plains in
Central-Northern Italy and a very low suitability of the Alpine region, thus providing support to the
hypothesis that the Italian population did not derive from dispersal from Switzerland. If escapes or
releases of raccoons will continue, there is a risk that the species could colonize other areas, making
its containment more difficult.
Introduction
A growing global evidence identifies the impact of alien species as one
of the main cause of the current biodiversity crisis (Wonham, 2006). In
Europe, more than 12000 alien species have been recorded to be present
(DAISIE; www.europe-aliens.org/aboutDAISIE.do); many of them may
exert a negative impact on biodiversity, environment, human health and
economics (Vilà et al., 2010; Scalera et al., 2012; Mazza et al., 2014).
About 10-15% of these species exert damages for about 12 billion Euro
per year (Kettunen et al., 2008).
The Northern raccoon Procyon lotor is listed within the 100 of the
worst invasive alien species in Europe (DAISIE, 2009). The species is
a medium-sized carnivore, naturally distributed from Southern Canada
to Central America (Timm et al., 2008). Introduced populations
have been established in Japan, several Caribbean islands, Azerbaijan,
Uzbekistan, as well as in many European countries (Lorvelec et al.,
2001; Ikeda et al., 2004; Timm et al., 2008; Beltràn-Beck et al., 2012;
Garcia et al., 2012). Diet spectrum of the Northern raccoon is very wide
as it may feed on a huge variety of invertebrates, fishes, amphibians,
birds and small mammals (Hayama et al., 2006; Bartoszewicz et al.,
2008; Garcia et al., 2012). Seasonally, vegetables and cultivated fruits
∗
Email address: [email protected] (Emiliano Mori)
doi:10.4404/hystrix-26.1-11035
are an important part of the diet, as well as carrion and garbage in urban
and suburban areas (Hayama et al., 2006; Bartoszewicz et al., 2008).
Growing evidence also suggests a role of raccoons as disease vectors
(e.g. rabies, nematode-mediated pathologies) with possible transmission to the native fauna, domestic animals and even humans (Arjo et al.,
2005; Bartoszewicz et al., 2008; Puskas et al., 2010; Vos et al., 2012;
Beltràn-Beck et al., 2012; Hulme, 2014).
In Europe, raccoons were imported for fur farming, hunting or as
pets/attraction in animal parks. They were observed in the wild for
the first time in Germany (Hessen) in 1927 (Hohmann and Bartussek,
2001). In 30 years, the German population of raccoons doubled
(Hohmann and Bartussek, 2001), conquering and invading neighboring countries. Signs of presence of the raccoon in Switzerland date
back to the 1970s, when the first individuals appeared near the German border. Thenceforth, recordings of raccoons have been reported
from all regions of Switzerland except for the Southern and Southeastern part. The current distribution pattern found in Switzerland could be
explained by erratic expansion of individuals combined with the presence of escaped or released animals (S. Capt, Centre Suisse de Cartographie de la Faune, personal communication, 2014). A similar story
occurred in Austria, where first raccoons were seen in 1980s (Aubrecht,
1985). In the second half of the 1990s, Austrian population expanded
mainly northward and reached Bohemia, Czech Republic (Mlíkovsky
3rd June 2015
26(1): 47–51
and Styblo, 2006). Currently, breeding populations are known to occur in 18 European countries (Beltràn-Beck et al., 2012; Alda et al.,
2013). Single individuals were sporadically observed in Great Britain,
Denmark, Norway and Sweden (Beltràn-Beck et al., 2012), while the
current status in Slovenia is unknown (Kryštufek, 2011). Despite this
wide distribution range of introduction, a huge gap in knowledge still
occur, as no study has been assessed yet to quantify the impact of the
raccoon on native biodiversity and environment, e.g. very few research
on diet (cf. Garcia et al., 2012). By contrast, sanitary impacts have
been more deeply described (Michler and Michler, 2012; Vos et al.,
2012).
As for Italy, the first reproductive population of Northern raccoon
has been established since 2004 in Lombardy (Northern Italy), along
the Adda river and its tributary canals (Canova and Rossi, 2008)). It
has been hypothesized that this species colonized Italy through a dispersal route, which links Switzerland to the Adda river basin (Canova
and Rossi, 2008). With an expanding range and a large array of potential impacts on native ecosystems, a synthesis of the distribution of the
Northern raccoon in Italy is required. Thus, aims of our work were (i)
to update the current distribution of this species in Italy ten years after
the first observation and (ii) to determine its potential range expansion
through a Species Distribution Model based on climatic variables.
Materials and Methods
Species data
Published and unpublished data on the presence and distribution of the
Northern raccoon in Italy were collected. The main source of information were: (i) scientific papers on raccoon distribution; (ii) generic articles reporting the presence and distribution of this species; (iii) data
collected through citizen science and (iv) direct observations carried
out by experts in several Italian regions.
Occurrences from the native area and from the introduced part of
the range were also collected. In detail, data from Switzerland were
provided by Centre Suisse de Cartographie de la Faune, those from
Japan were provided by M. Ishiguro, those from native range, France,
Luxembourg, Poland and Germany were taken from iNaturalist (http:
//www.inaturalist.org), VertNet (http://portal.vertnet.org), Arctos (http:
//arctos.database.museum) and GBIF Database (http://www.gbif.org).
Species Distribution Model
Species distribution models represent a reliable and widely used tool to
evaluate risks and sites of future invasions by alien species (Beaumont
et al., 2009; Ficetola et al., 2007; Di Febbraro et al., 2013). The model
for the raccoon was calibrated using Maxent (Phillips et al., 2006; Phillips and Dudìk, 2008), a machine-learning method that estimates species distributions using environmental predictors together with species
occurrences. This algorithm, based on an application of the maximum
entropy principle in an ecological context (Jaynes, 1957), calculates the
distribution probability in order to satisfy a set of constraints derived
from environmental conditions at presence sites. These constraints impose that the expected value of each environmental predictor falls as
close as possible to the empirical mean of that predictor measured over
the presence records. Among all the possible distributions satisfying
these constraints, the algorithm chooses the closest to the uniform, thus
maximizing the entropy. Maxent has generally shown to perform better
than other similar techniques, especially in predicting invasive species
distributions outside their native ranges (Elith et al., 2006; Heikkinen
et al., 2006; Ficetola et al., 2007; Di Febbraro et al., 2013).
Recent studies have shown that including records from native and invasive ranges in model building increase its performance in respect to
considering only records from the native range (Beaumont et al., 2009;
Di Febbraro et al., 2013). Therefore, we included in our model a total
of 1403 occurrences from the native range (N=1119) and from naturalized reproductive populations in Germany, Poland, Luxembourg,
France, Switzerland, Northern Italy and Japan (N=294: Fig. S1). Isolated occurrences in Italy, Austria and Slovenia were not included in the
analysis to avoid incorrect estimates.
48
From the ecological point of view, the Northern raccoon has a high
water requirement, thus occurring in a low number in arid environment (Stuewer, 1943; Hoffmann and Gottschang, 1977; Rosatte, 2000).
Moreover, trunk cavities, badger and fox burrows are often used for
reproductive purposes, emphasizing the importance of forests for this
species (Kamler and Gipson, 2003; Henner et al., 2004; Beasley et al.,
2007; Bartoszewicz et al., 2008; Hermes et al., 2011). Notwithstanding
this, raccoons also explore suboptimal habitat types, although possibly
at lower population densities (Hermes et al., 2011).
High altitudes may represent a limit for the range expansion of the
Northern raccoon in Europe, because it reduces its activity during snow
cover and winter survival is strictly linked to the amount of fat deposited during the previous autumn (Folk et al., 1968; Mugaas and Seidensticker, 1993). The altitudinal range of Northern raccoon in the native
range starts from the sea level up to a maximum of 1520 meters a.s.l.
in the USA and 2743 meters a.s.l. in Southern Mexico (Goldman,
1950). Raccoons do not hibernate and select preferentially areas not
covered by snow (Lotze and Anderson, 1979; Zeveloff, 2002; Kamler
and Gipson, 2003; Beasley et al., 2007). Although they are not impenetrable barriers, ridges represent an important hindrance to raccoon
movements (Puskas et al., 2010), and valleys represent the preferred
dispersal way.
No published data are available yet for the introduced range, with the
only exception of Germany (Tomaschek, 2008), but we know from the
occurrences that raccoon may reach over 1000 meters a.s.l. in Switzerland, Japan and in Germany as well.
According to these biological requirements, we chose the following
six climatic predictors, derived from the WORLDCLIM dataset, at a
resolution of 2.5 arc-minutes (≈ 5 km) (Hijmans et al., 2005): mean
temperature of the warmest quarter, mean temperature of the coldest
quarter, annual precipitation, precipitation of the driest month, precipitation of the warmest quarter and precipitation of the coldest quarter.
The collinearity between the predictors was assessed with a VIF (Variance Inflation Factor) analysis, setting a maximum VIF value of 10 (see
Zuur et al., 2010 for further details). The VIF analysis resulted in the
exclusion of annual precipitation from the initial set of environmental
variables.
We randomly split the occurrence data into two subsets to obtain
a reliable evaluation of the model, using 70% of records to calibrate
the model and the remaining 30% to evaluate it. This procedure was
replicated 10 times, each time randomly selecting different 70–30%
portions of occurrence data. The final model was obtained by averaging
the 10 runs. We evaluated predictive performance of the model for each
replicate by calculating the Area Under the Curve (AUC) of a receiver
operating characteristic plot (ROC; Fielding and Bell, 1997), the True
Skill Statistic (TSS; Allouche et al., 2006), and the related standard
deviations (SD). The evaluation scores were then averaged.
The final model was projected in a geographic area encompassing
Italy and borders with neighboring countries.
Results
A total of 38 sites of observation of Northern raccoon has been collected for Italy between 1987 and 2014, corresponding to 53 occurrences.
Among those, 25 sites were located in Southern Lombardy and referred
to the only known reproductive Italian population (Fig. 1). All the other
occurrences represented accidental individuals possibly escaped from
captivity or from wildlife recovery centres. Three of them were found
dead and only three other individuals were captured and removed from
the wild (Fig. 1).
The Species Distribution Model reached a good predictive performance with an AUC of 0.812 (SD=0.001) and a TSS of 0.478
(SD=0.019). Main suitable areas in Italy are represented by the Po
plain, the North-Eastern coastline, the internal plain areas of Central
Italy and the foothills of the Alps in Lombardy, characterized by dense
river networks. By contrast, the Alps and the main Apennine peaks
represented areas with low climatic suitability for raccoons, as well as
the xeric areas of Southern Italy (Fig. 1).
The conquest of Italy by the Northern raccoon
Figure 1 – Current distribution and climatic suitability for Northern raccoon in Italy.
Population of Lombardy markedly increased its range since the first
assessment of 2008 (Canova and Rossi, 2008: Fig. 2), and now the animals are observed in the Adda basin, as well as in the Southern floodplains of Lambro and Oglio rivers, and up to the North of the Po river
(provinces of Bergamo, Monza-Brianza, Milan, Cremona and Lodi).
The current distribution of the species in this region, calculated on the
two minimum convex polygon (2008 and 2014) encompassing all the
occurrences, is now 138% wider than it was in 2008.
Discussion
Our work provided new evidence on the current status and invasion
risk of Northern raccoon in Italy. Although records of this carnivore
have been reported from eight Italian regions, evidence of reproduction
are currently available only for Southern Lombardy. With respect to
the first assessment (Canova and Rossi, 2008), the area with records is
more than doubled.
In detail, we suggest that the hypothesis that the Italian population
derive from individuals in natural dispersal from Switzerland (Canova
and Rossi, 2008) should be discarded. The aspect of the raccoon is
unmistakable and well-known by the general public; we suggest that the
absence of data in the intermediate area between Switzerland and the
Adda river basin might be due to a real discontinuity in the distribution
range rather than to a lack of reports; records from Southern and SouthEastern part of Switzerland, near the border with Italy, are few too and
in an early phase of colonization (S. Capt, personal communication,
2014).
The linear distance between these two populations of raccoons is
about 270 km. Although in Germany a marked individual was caught
285 km straight line from its release point (Michler and Köhnemann,
2010), dispersal distances reported for the species are on average of
lesser extent (Lynch, 1967; Puskas et al., 2010). Even if Puskas et al.
(2010) claimed that dispersal of raccoon is mainly associated with valleys and that ridges are basically not selected, the complete absence
of records from climatically suitable areas (e.g. Province of Varese,
Northern Lombardy) bring us further support to the hypothesis that
different introduction events may have occurred in Switzerland and in
Italy. A different hypothesis would be that no signs/citizen science data
do not necessarily mean absence and some individuals may be present
at low densities between Italian and Swiss populations. Genetic analyses of both the Swiss and the Italian population would be useful to
clarify this issue.
Although being ecologically generalist, according to habitat types
and food selection, the Northern raccoon has specific requirements in
terms of climate, preferring the immediate surroundings of rivers or
water courses, possibly because of food requirements, and avoiding the
49
26(1): 47–51
Figure 2 – Current distribution of Northern raccoon in Lombardy (red triangles), with respect to the first detection (yellow circles: Canova and Rossi, 2008). The hydrographic map of
Lombardy is available at http://idro.arpalombardia.it/pmapper-4.0/map.phtml (Accessed on 30th November 2014..
coldest areas (Stuewer, 1943; Folk et al., 1968; Mugaas and Seidensticker, 1993; Hermes et al., 2011). According to our model, the Alps
does not constitute a climatically suitable environment for the presence
of raccoons, representing a potential barrier between the Italian and
the Swiss populations. In addition, the Po plain and the Italian coastline may constitute a preferential way for the conquest of Central and
Southern regions, where other sporadic observations of Northern raccoon have been reported.
An optimal strategy aiming at reducing the risks posed by introduced
species should consider a three-stage hierarchical approach, which includes i) prevention of new introductions, ii) early detection when prevention failed, and iii) a mitigation of impacts with the eradication,
containment or control of populations (Genovesi and Shine, 2004; Bertolino et al., 2015). Despite being considered an invasive species in
Europe, prevention is failing: the trade of the Northern raccoon is not
controlled yet and enclosures do not avoid risk of escapes. If a species
is present in a country and occurs free in the wild with some frequency,
early detection and rapid response should be adopted. Conversely, only
3 individuals out of 14 recorded outside Lombardy were captured and
removed, in addition to other three found road-killed (see Fig. 1). This
species easily gains emotional affiliation from the general public (Gilbert, 1982), thus possibly limiting management actions as control and
eradication, as it happened for other “attractive” alien species (e.g. grey
squirrel Sciurus carolinensis: Bertolino and Genovesi, 2003; Bertolino
50
et al., 2014; rose-ringed parakeet Psittacula krameri: Menchetti and
Mori, 2014). Alien populations of Northern raccoon may be funded
by a small number of individuals (Alda et al., 2013; Biedrzycka et al.,
2008); if sporadic escapes or releases by private owners or zoo parks
will continue, they form new propagule that could establish reproductive populations, leading to greater difficulties in management activity.
The invasive potential of the Northern raccoon, also helped by a wide
ecological plasticity and by multiple introductions (Alda et al., 2013;
Biedrzycka et al., 2008), has been widely observed in its introduced
range, both in Europe and in Japan (Bartoszewicz et al., 2008; Hayama
et al., 2006; Beltràn-Beck et al., 2012). Our study shows a rapid expansion of the species in Lombardy, suggesting the potential for raccoon
invasion in Northern Italy. Considering the experiences from other
European countries and Japan (Ikeda et al., 2004; Beltràn-Beck et al.,
2012; Garcia et al., 2012), this population should be rapidly removed to
avoid further expansion and consequent impacts to biodiversity. At the
same time, it is important to activate a response system with the rapid
removal of new animals found free in the environment.
The conquest of Italy by the Northern raccoon
References
Alda F., Ruiz-López M.J., García F.J., Gompper M.E., Eggert L.S., García J.T., 2013. Genetic evidence for multiple introduction events of raccoons (Procyon lotor) in Spain.
Biol. Invasions 15: 687–698.
Allouche O., Tsoar A., Kadmon R., 2006. Assessing the accuracy of species distribution
models: prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43: 1223–
1232.
Arjo W., Fisher C., Armstrong J., Johnson D., Boyd F., 2005. Monitoring raccoon rabies in
Alabama: the potential effects of habitat and demographics. Wildlife Damage Management Conferences Proceedings: 96.
Aubrecht G., 1985. Der Waschbär, Procyon lotor (Linnè, 1758), in Österreich (Mammalia
Austriaca 11). Jahrbuch des Oberösterreichischen Musealvereins 130: 243–257. [In German]
Bartoszewicz M., Okarma H., Zalewski A., Szczesna J., 2008. Ecology of the raccoon
(Procyon lotor) from Western Poland. Ann. Zool. Fenn. 45: 291–298.
Beasley J.C., DeVault T.L., Retamosa M.I., Rhodes O.E., 2007. A hierarchical analysis of
habitat selection by raccoons in northern Indiana. J. Wildl. Manage. 71: 1125–1133.
Beaumont L.J., Gallagher R.V., Thuiller W., Downey P.O., Leishman M.R., Hughes L.,
2009. Different climatic envelopes among invasive populations may lead to underestimations of current and future biological invasions. Divers. Distrib. 15: 409–420.
Bertolino S., Genovesi P., 2003. Spread and attempted eradication of the grey squirrel
(Sciurus carolinensis) in Italy, and consequences for the red squirrel (Sciurus vulgaris)
in Eurasia. Biol. Cons. 109: 351–358.
Bertolino S., Colangelo P., Mori E., Capizzi D., 2015. Good for management, not for conservation: an overview of research, conservation and management of Italian small mammals. Hystrix 26(1) (online first) doi:10.4404/hystrix-26.1-10263
Bertolino S., Cordero di Montezemolo N., Preatoni D.G., Wauters L.A., Martinoli A., 2014.
A grey future for Europe: Sciurus carolinensis is replacing native red squirrels in Italy.
Biol. Invasions 16: 53–62.
Beltràn-Beck B., Garcìa F.J., Gortàzar C., 2012. Raccoons in Europe: disease hazard due
to the establishment of an invasive species. Eur. J. Wildl. Res. 58: 5–15.
Biedrzycka A., Zalewski A., Bartoszewicz M., Okarma H., Jędrzejewska E., 2013. The genetic structure of raccoon introduced in Central Europe reflects multiple invasion pathways. Biol. Invasions 16: 1611–1625.
Canova L., Rossi S., 2008. First records of the northern raccoon Procyon lotor in Italy.
Hystrix 19(2): 179-182. doi:10.4404/hystrix-19.2-4428
DAISIE, 2009. Handbook of alien species in Europe. Springer, Dordrecht, Germany.
Di Febbraro M., Lurz P.W.W., Maiorano L., Girardello M., Bertolino S., 2013. The use
of climatic niches in screening procedures for introduced species to evaluate risk of
spread: the case of the American Eastern grey squirrel. PLoS ONE 8(7): e66559. doi:
10.1371/journal.pone.0066559
Elith J., Graham C.H., Anderson R.P., Dudik M., Ferrier S., Guisan A., Hijmans R.J.,
Huettman F., Leathwick J.R., Lehmann A., Li J., Lohmann L., Loiselle B.A., Manion G., Moritz C., Nakamura M., Nakazawa Y., Overton J.M., Peterson A.T., Phillips
S., Richardson K., Schachetti Pereira R., Schapire R.E., Soberòn J., Williams S.E., Wisz
M., Zimmermann N.E., 2006. Novel methods improve predictions of species’ distributions from occurrence data. Ecography 29: 129–151.
Ficetola G.F, Thuiller W., Miaud C., 2007. Prediction and validation of the potential global
distribution of a problematic alien invasive species – the American bullfrog. Divers.
Distrib. 13: 476–485.
Fielding A.H., Bell J., 1997. A review of methods for the assessment of prediction errors
in conservation presence/absence models. Environ. Conserv. 24: 38–49.
Folk G.E. Jr, Coady K.B., Folk M.A., 1968. Physiological observations on raccoons in
winter. Proc. J. Iowa Acad. Sci. 75: 301–305.
Garcia J.T., Garcia F.J., Alda F., Gonzàlez J.L., Aramburu M.J., Cortes Y., Prieto B., Pliego
B., Perez M., Herrera J., Garcıa-Roman L., 2012. Recent invasion and status of the
raccoon (Procyon lotor) in Spain. Biol. Invasions 14: 1305–1310.
Genovesi P., Shine C., 2004. European Strategy on Invasive Alien Species, final version.
Convention on the Conservation of European Wildlife and Natural Habitats. Council of
Europe, Strasbourg.
Gilbert F.F., 1982. Public attitudes toward urban wildlife: A pilot study in Guelph, Ontario.
Wildlife Soc. B. 10: 245–253.
Goldman E.A., 1950. Raccoons of North and Middle America. Washington: U.S. Government Printing Office.
Hayama H., Kaneda M., Tabata M., 2006. Rapid range expansion of the feral raccoon in
Kanagawa Prefecture, Japan, and its impact on native organisms. In: Koike F., Clout
M.N., Kawamichi M., De Poorter M., Iwatsuki K. (Eds.). Assessment and Control of
Biological Invasion Risks. Shoukadoh Book Sellers, Kyoto, Japan and IUCN, Gland,
Switzerland. 196–199.
Heikkinen R.K., Luoto M., Araujo M.B., Virkkala R., Thuiller W., Stykes M.T., 2006.
335 Methods and uncertainties in bioclimatic envelope modelling under climate change.
Prog. Phys. Geogr. 30: 751–777.
Henner C.M., Chamberlain M.J., Leopold B.D., Burger L.W. Jr., 2004. A multi-resolution
assessment of raccoon den selection. J. Wildl. Manage. 68: 179–187.
Hermes N., Köhnemann B.A., Michler F.U., Roth M., 2011. Radiotelemetrische Untersuchungen zur Habitatnutzung des Waschbären (Procyon lotor L., 1758) im MüritzNationalpark. Beiträge zur Jagd & Wildtierforschung 36: 557–572. [In German]
Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A., 2005. Very high resolution
interpolated climate surfaces for global land areas. International Journal of Climatology
25: 1965–1978.
Hijmans R.J., Graham C.H., 2006. The ability of climate envelope models to predict the
effect of climate on species distributions. Glob. Change Biol. 12: 2272–2281.
Hoffmann C.O., Gottschang J.L., 1977. Numbers, distribution, and movements of a raccoon
population in a suburban residential community. J. Mammal. 58: 623–636.
Hohmann U., Bartussek I., 2001. Der Waschbär. Oertel and Spörer. Reutlingen, Germany.
[In German]
Hulme P.E., 2014. Invasive species challenge the global response to emerging diseases.
Trends Parasitol. 30: 267–270.
Ikeda T., Asano M., Matoba Y., Abe G., 2004. Present status of invasive alien raccoons and
its impact in Japan. Glob. Environm. Res. 8: 125–131.
Jaynes E.T., 1957. Information Theory and Statistical Mechanics. II. Physical Review 108:
171–190.
Kamler J.F., Gipson P.S., 2003. Space and habitat use by male and female raccoons, Procyon lotor, in Kansas. Can. Field Nat. 117: 218–223.
Kettunen M., Genovesi P., Gollasch S., Pagad S., Starfinger U., Ten Brink P., Shine C.,
2008. Technical support to EU strategy on invasive species (IAS) – Assessment of the
impacts of IAS in Europe and the EU (final module report for the European Commission). Institute for European Environmental Policy (IEEP), Brussels, Belgium.
Kryštufek B., 2011. Rakun pri Trebnjem. Lovec 94: 409-410. [In Slovenian]
Lorvelec O., Pascal M., Pavis C. 2001. Inventaire et statut des Mammifères des Antilles
françaises (hors Chiroptères et Cétacés). In Rapport n° 27 de l’Association pour l’Etude
et la Protection des Vertébrés et Végétaux des Petites Antilles, Petit-Bourg, Guadeloupe.
[In French]
Lotze J.H., Anderson S., 1979. Procyon lotor. Mamm. species. 1–8.
Lynch G.M., 1967. Long-range movement of a raccoon in Manitoba. J. Mammal. 48: 659–
660.
Mazza G., Tricarico E., Genovesi P., Gherardi F., 2014. Biological invaders are threats to
human health: an overview. Ethol. Ecol. Evol. 26: 112–129.
Menchetti M., Mori E., 2014. Worldwide impact of alien parrots (Aves Psittaciformes) on
native biodiversity and environment: a review. Ethol. Ecol. Evol. 26: 172-194.
Michler F.U., Köhnemann B.A., 2010. Tierische Spitzenleistung – Abwanderungsverhalten
von Waschbären (Procyon lotor L., 1758) in Norddeutschland. Labus 31: 52–59. [In
German]
Michler F.U.F., Michler B.A., 2012: Ökologische, ökonomische und epidemiologische
Bedeutung des Waschbären (Procyon lotor) in Deutschland – eine aktuelle Übersicht.
Beiträge zur Jagd & Wildtierforschung 37: 389–397. [In German]
Mlíkovsky J., Styblo P., 2006. Nepůvodní druhy fauny a flóry České Republiky. Český svaz
ochránců přírody, Praha, Czech Republic. [In Czech]
Mugaas J.N., Seidensticker J., 1993. Geographic variation of lean body mass and a model
of its effect on the capacity of the raccoon to fatten and fast. Bull. Fla Mus. Nat. Hist.
36: 85–107.
Phillips S.J., Anderson R.P., Schapire R.E., 2006. Maximum entropy modeling of species
geographic distributions. Ecol. Model. 190: 231–259.
Phillips S.J., Dudìk M., 2008. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31: 2005–2010.
Puskas R.B., Fischer J.W., Swope C.B., Dunbar M.R., McLean R.G., Root J.J., 2010. Raccoon (Procyon lotor) movements and dispersal associated with ridges and valleys of
Pennsylvania: implications for rabies Management. Vector Borne Zoonotic Dis. 10:
1043–1048.
Rosatte R.C., 2000. Management of raccoons (Procyon lotor) in Ontario, Canada: do human intervention and disease have significant impact on raccoon populations? Mammalia 64: 369–390.
Scalera R., Genovesi P., Essl F., Rabitsch W., 2012. The impacts of invasive alien species
in Europe. EEA Technical report no. 16/2012.
Stuewer F.W., 1943. Raccoons: their habits and management in Michigan. Ecol. Monograph. 13: 203–257.
Timm R., Cuarón A.D., Reid F., Helgen K., 2008. Procyon lotor. The IUCN Red List of
Threatened Species. Version 2014.3. Available ftom www.iucnredlist.org. Downloaded
on 30 November 2014.
Tomaschek K., 2008. Current distribution of the Raccoon (Procyon lotor L., 1758) in Germany (hunting bag data) and Europe (single record data). Masterarbeit Fachhochschule
Eberswalde.
Vilà M., Basnou C., Pyšek P., Josefsson M., Genovesi, P., Gollasch S., Nentwig W., Olenin
S., Roques A., Roy D., Hulme P.E., DAISIE partners, 2010. How well do we understand the impacts of alien species on ecosystem services? A pan-European cross-taxa
assessment. Front. Ecol. Environ. 8: 135–144.
Vos A., Ortmann S., Kretzschmar A.S., Köhnemann B., Michler F.U., 2012. The raccoon
(Procyon lotor) as potential rabies reservoir species in Germany: a risk assessment.
BMTW 125: 228–235.
Wonham M., 2006. Species invasions. In: Groom M.J. Meffe G.K., Carroll C.R. (Eds).
Principles of conservation biology. Sunderland, Massachussets. Sinauer Associates,
Inc., USA. 209-227.
Zeveloff S.I., 2002. Raccoons: a natural history. UBC Press, New York, USA.
Zuur A., Ieno E., Elphick C., 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1: 3–14.
Supplemental information
Additional Supplemental Information may be found in the online version of this article:
Figure S1 Localization of the occurrences used for the model.
51
Volume 26 (1): 53–57, 2015
doi:10.4404/hystrix-26.1-11304
Research Article
Macro-ecological patterns of the endemic Afrosoricida and Rodentia of Madagascar
Giovanni Amoria,∗, Giuliano Milanaa , Chiara Rotondoa , Luca Luisellib,c
a
CNR – Institute for Ecosystem Study, Rome, Italy
Centre of Environmental Studies Demetra, Rome, Italy
c
Niger Delta Ecology and Biodiversity Conservation Unit, Department of Applied and Environmental Biology,
Rivers State University of Science and Technology, PMB 5080, Port Harcourt, Rivers State, Nigeria
b
Keywords:
Mammalia
Madagascar
macro-ecology
mid-domain effect
Article history:
Received: 14 May 2015
Accepted: 1 June 2015
Abstract
We examined the macro-ecological and species richness correlates of the endemic mammal fauna
(Afrosoricida and Rodentia) of Madagascar. We divided the whole of Madagascar into 307, 50×50
km cells, and showed that there was a significantly uneven distribution of species across cells in
both Afrosoricida and Rodentia, with a higher number of species per cell in the former taxon (peaks
at around 19–21 species per cell in Afrosoricida versus 11–12 species in Rodentia). In each cell,
the number of Afrosoricida species was positively correlated with the number of Rodentia species.
Cell vegetation category affected species richness per cell in both Afrosoricida and Rodentia (evergreen forest cells had higher species richness than cells of any other type of vegetation). There was
a significant effect of altitude category on species richness per cell in both Afrosoricida and Rodentia, with a confirmed Mid Domain Effect in both groups. Heterogeneity of habitat also influenced
significantly and positively the species richness per cell in either Afrosoricida or Rodentia. About
15% of Afrosoricida and 28% of Rodentia are threatened according to IUCN. The distribution of
threatened species of the two groups per cell showed (i) a low density of threatened species (just
one species per cell in most cases) and (ii) distinct patterns for the two studied groups. Afrosoricida
had two main regions where threatened species are concentrated (the evergreen forest belt in Eastern Madagascar and the deciduous broad-leaf forest in Central-Western Madagascar). Threatened
Rodentia occur only in the portion of cells covered by evergreen forest, thus overlapping with part
of the region where also threatened Afrosoricida occur.
Introduction
Madagascar is a unique geographical region in terms of endemism (e.g.,
Pearson and Raxworthy, 2009; Vences et al., 2009), and also one of the
most important biodiversity hotspots because of the actual threatened
status of most of its natural habitats (Myers et al., 2000). For instance,
the whole Malagasy subcontinent has undergone large-scale deforestation during the last 50 years (e.g., Green and Sussman, 1009; Harper
et al., 2007), and as a consequence heavy conservation threats have
emerged towards its species-rich endemic fauna (e.g., Smoth et al.,
1997; Andreone and Luiselli, 2003; Bollen and Donati, 2006).
Concerning mammals, the great majority of species is endemic (Garbutt, 1999, 2007), but studies exploring the macro-ecological correlates
and the conservation implications of their distribution have been focusing mainly on lemurs and on other large-sized species (e.g., Smoth et
al., 1997; Mittermeier and Nash, 2006; Mittermeyer et al., 2008; Gerber et al., 2010; but see also Lees et al., 1999). Studies of the same type
concerning the endemic Afrosoricida and Rodentia of Madagascar are
few (Lees et al., 1999). In this paper, we explore the geographical patterns of distribution of these two mammal groups. We emphasize on
testing whether there are any specific nonrandom patterns explaining
the current distribution of Afrosoricida and Rodentia, and on the conservation implications of the patterns observed. More specifically, we
explore the habitat-related and altitude-related patterns of distribution
of the various species, with an emphasis on the eventual differences
between the two groups. In addition, we also offer the same type of ana∗
Email address: [email protected] (Giovanni Amori)
doi:10.4404/hystrix-26.1-11304
lysis for the species which are currently listed as threatened by IUCN
(2014.3; available at www.iucnredlist.org), in order to highlight whether
there is any identifiable pattern that can have conservation and/or management implications.
Materials and methods
The geographical territory of Madagascar was divided into 307 cells
of 50×50 km area, using Quantum GIS (Quantum GIS Development
Team, 2015; freely available at http://www.qgis.org; Fig. 1). In each
cell, the vegetation type was assigned by using the map available at
http://www.wildmadagascar.org/maps/land_cover.html, and then transforming it to a raster and geo-referencing it. Although blocks of a given
habitat were not so large than a 50×50 cell (and hence most of the cells
included more than one habitat type), we assigned each cell to the vegetation type that was the most represented in the given cell. Habitat
categories were categorized as follows: (1) savannah, (2) deciduous
broad-leaf forest, (3) mixed forest, and (4) evergreen forest. Savannah
was essentially grassy vegetation derived from pristine habitat alteration, including deforestation. Deciduous broad-leaf forest is a tropical
dry forest ecoregion that is situated in the western part of Madagascar.
This type of forest is characterized by high numbers of endemic plant
and animal species; however it has suffered large-scale devastation due
to clearance for agriculture. Mixed forests include divergent types of
habitats such as spiny thickets, shrublands, and dry forests. Evergreen
forests, widely distributed in the eastern side of Madagascar, consist of
both broad-left and needle-leaf forest, which do not lose their leaves
during the cold season.
3rd June 2015
26(1): 53–57
Figure 1 – Map of Madagascar showing the cells used for our analyses, and the number of species present in each cell (A = Afrosoricida; B = Rodentia).
For each cell, we also assigned the most representative category
of altitude by using GIS vector data available at http://www.diva-gis.
org/gdata. The categories (m a.s.l) were as follows: (1) -8–548,
(2) 549–1105, (3) 1106–1660, and (4) 1661–2218. These categories were derived after exploring the frequency distribution of the various elevational zones, and considering the discontinuities as the various thresholds. Habitat heterogeneity was determined by calculating the number of habitat types within each cell, using the habitat
types available in the FAO map of Madagascar available at http://www.
wildmadagascar.org/maps/land_cover.html.
The list and distribution of species was compiled using Garbutt
(2007) and IUCN red list maps (www.iucnredlist.org), and using also
Wilson and Reeder (2005) as an integration. A few other recently
described species (Microgale grandidieri, M. jenkinsae, M. jobihely,
Macrotarsomys petteri, and Vohalavo anthsabensis) were omitted from
our calculations because they are presently known from less than 5 specimens, and therefore their distribution range is not known. Also, we
did not include in calculations the introduced species (e.g., Rattus rattus, Rattus norvegicus, Mus musculus, and Suncus murinus).
Figure 2 – Relationship between the number of Afrosoricida per cell and number of
Rodentia species per cell. For statistical details, see the text.
54
Inter-cell differences in the species richness for the two studied taxa
were assessed by a Monte Carlo procedure of χ2 test, with 9999 iterations. Differences inside each cell in the species richness of the two
groups were assessed by Wilcoxon paired test. Correlations between
number of Afrosoricida species per cell and number of Rodentia species per cell were assessed by Pearson’s correlation coefficient. The
Distribution patterns of Afrosoricida and Rodentia in Madagascar
Figure 3 – Mean (and dispersion measures) of species richness per cell in relation to vegetation category in Madagascar. (A) Afrosoricida; (B) Rodentia.
effect of cell vegetation and altitude categories on species richness per
cell were assessed by GLM with Poisson error structure, since counts
for species richness were used, and this variable was not continuous.
The correlations between heterogeneity of habitat and species richness
per cell were assessed by Spearman’s rank correlation coefficient. In
all cases, alpha was set at 5%, and the tests were two-tailed. Analyses
were performed with Statistica version 10.0 version and PAST 3 softwares.
Results
Overall, our analyses are based on a total of 27 species of Afrosoricida,
1 of Soricomorpha (Suncus madagascariensis) and 25 of Rodentia. As
expected, there was a significantly uneven distribution of species across
cells in both Afrosoricida (Monte Carlo χ2 =563.9, p<0.0001) and Rodentia (Monte Carlo χ2 =405.3, p<0.001). The number of species per
cell was generally higher for Afrosoricida than for Rodentia, with peaks
at around 19–21 species per cell in Afrosoricida versus 11–12 species
per cell in Rodentia (Fig. 2). Indeed, deeper inspection of data revealed that, in each cell, there was a significant difference in species
richness of the two groups (Wilcoxon paired test: Z=14.6, p<0.0001).
The number of Afrosoricida and Rodentia species per cell were positively correlated (r=0.91, p<0.0001; Fig. 2).
Species richness per cell in Afrosoricida (Fig. 3A) was higher in
evergreen forest cells than in cells with any other type of vegetation.
Mixed forest cells had higher species richness than cells with savannah
and deciduous broad-leaf forests. A GLM model revealed that vegetation type significantly affected species richness (mean square=677.06,
df=3, F=9.081, p<0.005), as well as the interaction term vegetation
type × altitude (mean square=134.66, df=11, F=10.284, p<0.0001),
whereas elevation alone did not influence species richness (mean
square=235.49, df=5, F=2.84, p=0.062). Concerning Rodentia, a similar pattern was also observed (Fig. 3B). In this case, only evergreen
forest cells had higher species richness than cells of any other type of
vegetation, whereas all other vegetation types were similar in terms of
their species richness per cell. A GLM model revealed that vegetation
type significantly affected species richness (mean square=233.12, df=3,
F=39.206, p<0.001), as well as the interaction term vegetation type ×
altitude (mean square=47.45, df=11, F=7.767, p<0.0001), whereas elevation alone did not influence species richness (mean square=71.55,
df=5, F=2.396, p=0.094).
For Afrosoricida, the species richness per cell was significantly
higher at 549–1105 and 1106–1660 m a.s.l. than all other categories
(Tukey test, all p<0.0001; Fig. 4A), and that the 1661–2218 m altitude
category cells contained significantly less species than all other elevation categories (Tukey test, all p<0.001). For rodents, the same trend
was confirmed: species richness per cell was significantly higher at
549–1105 and 1106–1660 m a.s.l. than at other elevations, and lowest
in cells situated at 1661–2218 m (Tukey test, all p<0.001; Fig. 4B).
Heterogeneity of habitat also influenced significantly and positively
the species richness per cell in either Afrosoricida (Spearman’s r=0.20,
n=308, p<0.001) or Rodentia (Spearman’s r=0.16, n=308, p<0.01).
A relatively low percentage of species is threatened according to
latest IUCN data (about 15% in Afrosoricida and 28% in Rodentia).
The distribution of threatened species of the two groups per cell (Fig.
5) showed (i) a low density of threatened species (just one species per
cell in most cases) and (ii) distinct patterns for the two studied groups.
Indeed, Afrosoricida had two main regions where threatened species
are concentrated, i.e. a large area characterized by evergreen forest,
Figure 4 – Mean (and dispersion measures) of species richness per cell in relation to altitude category in Madagascar. (A) Afrosoricida; (B) Rodentia.
55
26(1): 53–57
Figure 5 – Map of Madagascar showing the number of threatened species present in each cell (A = Afrosoricida; B = Rodentia). Threatened species were counted by following IUCN Red
List www.iucnredlist.org.
and another main area in Central-Western Madagascar with deciduous
broad-leaf forest. Conversely, threatened Rodentia occur only in the
portion of cells covered by evergreen forest, thus overlapping with part
of the region where threatened Afrosoricida occur (Fig. 5).
Discussion
Our study revealed several non-random macro-ecological patterns for
Malagasy Afrosoricida and Rodentia, some of them being expected on
the basis of available literature on other Malagasy vertebrates, but also
being rather unexpected (see below). To begin with, our study showed
that, despite the total species richness of Afrosoricida and Rodentia was
similar at the overall scale of Madagascar (e.g., Garbutt, 1999, 2007),
the number of Afrosoricida was significantly higher in each cell. This
pattern may arise from the remarkable differences in the average range
size of the two groups, with rodents showing significantly narrower
ranges than Afrosoricida species (Amori et al., unpublished data), and,
consequently, with several Afrosoricida being habitat generalists (e.g.,
Tenrec ecaudatus, Setifer setosus, etc). On the contrary, most of the
endemic rodents of Madagascar are specialized forest-dwelling species
(e.g., Nesomys rufus, Brachytarsomys albicauda; see Garbutt, 2007).
Evergreen forest cells clearly showed a higher richness of species
of both orders than cells with any other type of vegetation category.
However, for interpreting the above-mentioned pattern, it should be reminded that in a 50×50 km cell different habitat types can occur, thus
56
the results based on our method to assign habitat type must be considered with some caution. This result is clearly expected on the basis
of the available literature, as tropical evergreen forests are in general
among the most species-rich habitats of the whole world (e.g., Gentry,
1988; Phillips et al., 1994; Barlow et al., 2007 and later literature), and
the same was also true in Madagascar. For instance, Malagasy evergreen forests represented the main species richness hotspots for such
distinct animals as butterflies, frogs, chameleons and lemurs (Lees et
al., 1999).
Concerning distribution along the elevation gradient of the two
mammal groups, we found clear evidence that the peaks of species richness tend to occur in mid-elevation cells, especially in conjunction with
forest ecosystems. We interpret this pattern as a case of mid-domain
effect. According to general theory, a mid-domain effect occurs where
landmass boundaries such as oceans and mountaintops limit species
ranges and the simple overlap of many, variously sized ranges, create
a peak in species richness at mid-elevation (Colwell and Hurtt, 1994;
Colwell and Lees, 2000; McCain, 2004). Similar cases of mid-domain
effect in small mammals were also documented for, e.g., the Philippines
(Heaney, 2001), Borneo (Md. Nor, 2001) and in Taiwan (Yu, 1994).
Heterogeneity of vegetation per cell also affected positively the species richness per cell in both Afrosoricida and Rodentia. Also in this
case, our pattern can be reconducted to an explicit theoretical ecological model that is the edge effect (Lidicker, 1999; Lettinen et al.,
Distribution patterns of Afrosoricida and Rodentia in Madagascar
2003), with the linear trend in high heterogeneity peaks supporting a
hypothesis of a suite of interacting climatic/microhabitat variables influencing the pattern of biodiversity at a larger scale. As alternative
hypothesis, since 2500 km2 is a very large scale compared to small
mammals average range size, it is possible that a cell with two different
habitats should host more species than a cell with a single habitat type
simply because, to the number of species common to both habitats, it
can be summed the number of species living only in the first or in the
second habitat.
This result is somewhat counterintuitive if we think that the evergreen forests are the most species-rich vegetation type in Madagascar, and that, therefore, cells dominated by only (large-sized) evergreen
forest habitat would have been predicted to be more species rich than
those with a suite of habitats (including smaller patches of evergreen
forest). We think that this pattern indirectly shows that forest-specialist
Afrosoricida and Rodentia do not need large forest patches to survive,
but also can occur in small and fragmented patches, thus being found
also in cells with a low percentage of territory being actually covered
by evergreen forest.
The correlation between the number of species of the two groups per
cell was likely dependent on the fact that the same main environmental
variables (and especially the main vegetation zones) drive the species
richness of the two groups. Indeed, evergreen forests contained by far
the higher number of species per cell.
Concerning the threatened taxa, the figures relative to Afrosoricida
and to Rodentia presented opposite patterns. On the one hand, there
was a remarkably lower percentage of threatened taxa among Malagasy
Afrosoricida (about 15% of the species) than among the whole representatives of this order (31.5%, see Amori et al., 2014). On the other
hand, Malagasy rodents were remarkably more threatened in Madagascar (about 28% of the total number of species) than overall (15.9%, see
Amori et al., 2014). We interpret that also these differences may reside
in the higher specialization for forest habitats of Malagasy rodents compared to Afrosoricida, thus resulting in a higher global threatening risk
due to the current alteration status of the Malagasy forests (e.g., Green
and Sussman, 1009; Lowry et al., 1997; Harper et al., 2007). However,
a shared pattern between Afrosoricida and Rodentia resides in that almost invariably only one threatened species of each group occurs in a
single cell, with many cells across Madagascar housing a threatened
species. The consequence of this pattern is that there is no single area
of specially high conservation priority for the two investigated groups.
Nonetheless, there is a need of widespread and de-centered conservation effort in order to maintain and protect the threatened Afrosoricida
and Rodentia of Madagascar. In particular, it would be necessary to
concentrating field efforts in evergreen forests, not only in large but
also in smaller patches, in order to better explore the ecological correlates of richness distribution in these two groups of mammals.
References
Amori G., Gippoliti S., Luiselli L., 2014. A short review of the roles of climate and man in
mammal extinctions during the Anthropocene. Rendiconti Fisica Accademia dei Lincei
25: 95-–99.
Andreone F., Luiselli L., 2003. Conservation priorities and potential threats influencing the
hyper-diverse amphibians of Madagascar. Italian Journal of Zoology 70: 53–63.
Barlow J., Gardner T.A., Araujo I.S., Avila-Pires T.C., Bonaldo A.B., Costa J.E., Esposito M.C., Ferreira L.V., Hawes J., Hernandez M.I.M., Hoogmoed M.S., Leite R.N.,
Lo-Man-Hung N.F., Malcolm J.R., Martins M.B., Mestre L.A.M., Miranda-Santos R.,
Nunes-Gutjahr A.L., Overal W.L., Parry L., Peters S.L., Ribeiro-Junior M.A., da Silva
M.N.F., da Silva Motta C., Peres C.A., 2007. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. PNAS 104: 18555–18560.
Bollen A., Donati G., 2006. Conservation status of the littoral forest of south-eastern Madagascar: a review. Oryx 40: 57-66.
Colwell R.K., Hurtt G.C., 1994. Nonbiological gradients in species richness and a spurious
Rapoport effect. American Naturalist 144: 570–595.
Colwell R.K., Lees D.C., 2000. The mid-domain effect: geometric constraints on the geography of species richness. Trends in Ecology and Evolution 15: 70–76.
Garbutt N., 1999. Mammals of Madagascar. Pica Press, Sussex.
Garbutt N., 2007. Mammals of Madagascar: a complete guide. A & C Black, London.
Gentry A.H., 1988. Tree species richness of upper Amazonian forests. Proceedings of the
National Academy of Sciences of the USA 85: 156–159.
Gerber B., Karpanty S.M., Crawford C., Kotschwar M., Randrianantenaina J., 2010. An assessment of carnivore relative abundance and density in the eastern rainforests of Madagascar using remotely-triggered camera traps. Oryx 44: 219–222.
Goodman S.M., Soarimalala V., 2004. A new species of Microgale (Lipotyphla: Tenrecidae: Oryzorictinae) from the Forêt des Mikea of southwestern Madagascar. Proceedings of the Biological Society of Washington 117: 251–265
Green G.M., Sussman R.W., 1990. Deforestation history of the eastern rain forests of Madagascar from satellite images. Science 248: 212–215.
Harper G.J., Steininger M.K., Tucker C.J., Juhn D., Hawkins F., 2007. Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation 34:
325–333.
Heaney L.R., 2001. Small mammal diversity along elevational gradients in the Philippines:
an assessment of patterns and hypotheses. Global Ecology and Biogeography 10: 15–39.
Lees D.C., Kremen C., Andriamampianina L., 1999. A null model for species richness
gradients: bounded range overlap of butterflies and other rainforest endemics in Madagascar. Biological Journal of the Linnean Society 67: 529–584.
Lethinen R.M., Ramanamanjato J.-B., Raveloarison J.G., 2003. Edge effects and extinction
proneness in a herpetofauna from Madagascar. Biodiversity and Conservation 12: 1357–
1370.
Lidicker W.Z., 1999. Responses of mammals to habitat edges: an overview. Landscape
Ecology 14: 333–343.
Lowry P.P., Schatz G.E., Phillipson P.B., 1997. The classification of natural and anthropogenic vegetation in Madagascar. In: Goodman S.M., Patterson B.D. (Eds.) Natural
change and human impact in Madagascar. Smithsonian Institution Press, Washington,
DC. 93-–123.
McCain C.M., 2004. The mid-domain effect applied to elevational gradients: species richness of small mammals in Costa Rica. Journal of Biogeography 31: 19–31.
Md. Nor S., 2001. Elevational diversity patterns of small mammals on Mount Kinabalu,
Sabah, Malaysia. Global Ecology and Biogeography 10: 41-–62.
Mittermeier R.A., Nash S.D., 2006. Lemurs of Madagascar. Conservation International,
Washington DC.
Mittermeier R.A., Ganzhorn J., Konstant W., Glander K., Tattersall I., Groves C., Rylands
A., Hapke A., Ratsimbazafy J., Mayor M., Louis E., Rumpler Y., Schwitzer C., Rasoloarison R., 2008. Lemur Diversity in Madagascar. International Journal of Primatology
29(6): 1607-–1656.
Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B., Kent J., 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858.
Pearson R.G., Raxworthy C.J., 2009. The evolution of local endemism in Madagascar: watershed versus climatic gradient hypotheses evaluated by null biogeographic models.
Evolution International Journal of Organic Evolution 63: 959–967.
Phillips O.L., Hall P., Gentry A.H., Sawyer S.A., Vasquez R., 1994. Dynamics and species
richness of tropical rain forests. Proceedings of the National Academy of Sciences of
the USA 91: 2805–2809.
Quantum GIS Development Team, 2015. Quantum GIS Geographic Information System.
Open Source Geospatial Foundation Project. Available at http://qgis.osgeo.org
Smith A.P., Horning N., Moore D., 1997. Regional biodiversity planning and lemur conservation with GIS in Western Madagascar. Conservation Biology 11: 498–512.
Vences M., Wollenberg K.C., Vieites D.R., Lees C.D., 2009. Madagascar as a model region
of species diversification. Trends in Ecology and Evolution 24: 456–465.
Wilson D.E., Reeder D.R., 2005. Mammal species of the world: a taxonomic and geographic reference, 3rd Edn. John Hopkins University Press, Baltimore.
Yu H., 1994. Distribution and abundance of small mammals along a subtropical elevational
gradient in central Taiwan. Journal of Zoology, London 234: 577–600.
Associate Editor: D.G. Preatoni
57
Volume 26 (1): 59–60, 2015
doi:10.4404/hystrix-26.1-10624
Short Note
New long-distance recapture of a noctule (Nyctalus noctula) from eastern Europe
Sergey Gashchaka , Anton Vlaschenkob,∗, Péter Estóka , Kseniia Kravchenkoc
a
Chernobyl Centre for Nuclear Safety, Radioactive Waste and Radioecology, P.O. Box 151, 11, 77th Gvardiiska Dyviziya St., Slavutych, Kyiv Region, 07100, Ukraine
b
Bat Rehabilitation Center of Feldman Ecopark, Kharkov region, Dergachevsky district, village Lesnoye, Kiev highway str., 12, Ukraine
c
Eszterházy Károly College, Eszterházy tér 1., H-3300 Eger, Hungary
Keywords:
Nyctalus noctula
migration
Ukraine
Hungary
Article history:
Received: 24 September 2014
Accepted: 19 December 2014
Abstract
Long distance recaptures of banded bats from Eastern European countries (Belarus, Ukraine,
European part of Russia) have been lacking for decades. The last transboundary recapture was
recorded in the late 1960s. We herewith report a new long-distance recapture of a noctule Nyctalus
noctula). The fresh carcass of a ringed adult female noctule was found in South-East Hungary on
22 May 2014. The bat was mist-netted and ringed on 31 May 2011 on the territory of Chernobyl
Exclusion Zone, in North Ukraine. The direct distance between the two locations is 800 km.
Acknowledgements
We thank Lajos Földi (Szeghalom) és László Puskás (Körösladány) for
presenting the ring to the local nature conservation authority, and Péter
Bánfi (Körös-Maros National Park Directorate) for informing us about the
ringed bat. We thank Sara Troxell for language correction. Field research
in Chernobyl Exclusion Zone was implemented with the support of The
Rufford Small Grants for Nature Conservation, project “Fauna of bats as
an indicator of the most valuable natural complexes in Chernobyl Exclusion Zone worthy of legislative protection”. The relevant research
activity of Péter Estók was supported by the European Union and the
State of Hungary, co-financed by the European Social Fund in the framework of TÁMOP-4.2.4.A/2-11/1-2012-0001 ‘National Excellence Program’.
The interest in long-distance bat movement has increased significantly in the last years in Europe. It became clear that large numbers of
bats are killed by wind-power facilities, mostly during autumn migration (Rydell et al., 2010). The bats killed by wind facilities in Germany
possibly originate from territories hundreds of kilometers away, in Russia or Belarus (Voigt et al., 2012; Lehnert et al., 2014). These results
force us to return to the study of bat migration with the new meaning of conservation. Recaptures of banded bats from Eastern European
countries (Belarus, Ukraine, European part of Russia) have been lacking for decades. The last transboundary recapture was recorded in the
late 1960s (Panyutin, 1980). There were only few transboundary recaptures of bats ringed in Ukraine recorded in the data from the territory
of former USSR (Hutterer et al., 2005).
In this note we present information about a new recapture of a ringed
noctule (Nyctalus noctula) from Eastern Europe (Fig. 1).
The fresh carcass of a ringed adult female noctule was found in a
shed of a private home owner in South-East Hungary (47°3′ 44.9′′ N,
21°5′ 31.2′′ E) on 22 May 2014. The ring number was “Kiev
Ukraine DT01528”. The bat was mist-netted and ringed on 31 May
2011 in the territory of Chernobyl Exclusion Zone (51°12′ 17.92′′ N,
30°1′ 11.57′′ E) on the bend of the Uzh river (North Ukraine). The specimen was identified as not more than one year old. The direct distance
between the two locations is 800 km.
Bat ringing was started in Chernobyl Exclusion Zone in 2007 as
a part of overall bat summer assemblage research. In the 2007-2013
period 2842 bats of 14 species were ringed (Gashchak et al., 2013) including 1321 noctules.
∗
In the Chernobyl Zone vast woodlands, various water-bodies,
marshes, and moderate climate with frosty winter represent a typical breeding area for many migrating forest-dwelling bats (Strelkov,
1997a,b). The nearest known winter aggregation of noctules is located in the city of Kiev (80 km to the South) and was formed no more
than 15 years ago (Tyshchenko and Godlevska, 2008). This recapture
confirms the proposed main direction (northeast-southwest) of the migration of noctules in Europe (Petit and Mayer, 2000; Hutterer et al.,
2005). The locality of the Hungarian recapture is on the southern border of the breeding territory of the species (Görföl et al., 2009) and
also falls within the wintering range. In northeast Hungary (ca. 120
km north of the site of the present recapture) characteristic changes
were observed in the sex ratio of noctules, females were absent during
the nursing period, but were present in spring and autumn in significant numbers, which supports the presence of a considerable sex-biased
migration in the area (Estók, 2007). It is not clear why the bat stayed in
this hibernation area for so long (up to the end of May). Migrations of
bats from high radioactive regions to “clear” remote areas should not
be considered sources of pollution in nonradioactive areas. Besides the
relatively low starting level of contamination in their bodies, bats depurate over a rather short period due to natural excretion of radionuclides
(Gashchak et al., 2010).
Email address: [email protected] (Anton Vlaschenko)
doi:10.4404/hystrix-26.1-10624
25th February 2015
26(1): 59–60
Figure 1 – Documented long-distance recapture of a Noctule from Ukraine to Hungary (S:
summer ringed location, W: spring (wintering) recapture location).
References
Estók P., 2007. Seasonal changes in the sex ratio of Nyctalus species in North-East Hungary.
Acta Zool. Acad. Sci. H. 53(1): 89–95.
Gashchak S.P., Beresford N.A., Maksimenko A., Vlaschenko A.S. 2010. Strontium-90 and
caesium-137 activity concentrations in bats in the Chernobyl exclusion zone. Radiat.
Environ. Biophys. 49(4): 635–644.
Gashchak S.P., Vlaschenko A.S., Naglov A.V., Kravchenko K.A., Prylutska A.S., 2013.
Bats fauna of the Exclusion Zone in concern of assessment of environmental value of
its areas. Problems of Chernobyl exclusion zone 11: 56–78. (In Russian with English
summary)
Görföl T., Dombi I., Boldogh S., Estók P., 2009. Going further south: new data on the
breeding area of Nyctalus noctula (Schreber, 1774) in Central Europe. Hystrix 20(1):
37–44.
Hutterer R., Ivanova T., Meyer-Cords C., Rodrigues L., 2005. Bat migration in Europe. A
review of banding data and literature. Federal Agency of Nature Conservation, Bonn.
Lehnert L.S., Kramer-Schadt S., Schönborn S., Lindecke O., Niermann I., Voigt C.C., 2014.
Wind farm facilities in Germany kill Noctule bats from near and far. PloS one 9(8):
e103106.
Panyutin K.K., 1980. Bats. In: Kucheruk V.V. (Ed.). Results of marking mammals. Moskva
pp. 23-46. (in Russian)
Petit E., Mayer F., 2000. A population genetic analysis of migration: the case of the noctule
bat (Nyctalus noctula). Mol. Ecol. 9: 683–690.
Rydell J., Bach L., Dubourg-Savage M-J., Green M., Rodriguez L., Hedenström A. 2010.
Bat mortality at wind turbines in northwestern Europe. Acta Chiropt. 12(2): 261–274.
Strelkov P.P., 1997a. Breeding area and its position in range of migratory bat species (Chiroptera, Vesportilionidae) in East Europe and adjacent territories, communication 1.
Zool. Zhurnal 76: 1073–1082.
Strelkov P.P., 1997b. Breeding area and its position in range of migratory bat species (Chiroptera, Vesportilionidae) in East Europe and adjacent territories, communication 2.
Zool. Zhurnal 76: 1381–1390.
Tyshchenko V.M., Godlevska O.V., 2008. First winter records of Vespertilio murinus and
Nyctalus noctula (Chiroptera) in Kyiv. Vestn. Zool. 42(3): 280. (In Ukrainian)
Voigt C.C., Popa-Lisseanu A., Niermann I., Kramer-Schadt S., 2012. The catchment area
of wind farm for European bats: A plea for international regulations. Biol. Conserv. 153:
80–86.
Voigt C.C., Lehnert L.S., Popa-Lisseanu A.G., Ciechanowski M., Estók P., Gloza-Rausch
F., Görföl T., Göttsche M., Harrje C., Hötzel M., Teige T., Wohlgemuth R., KramerSchadt S., 2014. The trans-boundary importance of artificial bat hibernacula in managed
European forests. Biol. Conserv. 23(3): 617–631.
Associate Editor: D. Russo
60
Volume 26 (1): 61–62, 2015
doi:10.4404/hystrix-26.1-10957
Short Note
Effectiveness of electric fences as a means to prevent Iberian lynx (Lynx pardinus) predation on lambs
Germán Garrotea,∗, Guillermo Lópeza , Manuel Ruiza , Santiago de Lilloa , José F. Buenoa , Miguel Angel Simónb
b
a
Agencia de Medio Ambiente y Agua de Andalucía. c/ Johan Gutenberg s/n, Isla de la Cartuja, 41092, Seville, Spain
Consejería de Medio Ambiente de la Junta de Andalucía. c/ Doctor Eduardo García-Triviño López, 15. 23009, Jaén, Spain
Keywords:
Livestock depredation
Iberian lynx
electric fences
human-wildlife conflict
Article history:
Received: 31 October 2014
Acknowledgements
The study was supported by the LIFE Project 10NAT/ES/570 “Recovery of
the historical distribution of the Iberian lynx (Lynx pardinus) in Spain
and Portugal”.
Abstract
To mitigate the conflict derived from Iberian lynx (Lynx pardinus) predation on livestock, a prevention and compensation program has been implemented to compensate farmers for poultry and
lambs killed by Iberian lynx. Although the majority of the attacks were carried out on poultry,
the predation of lambs in extensive flocks leads to greater economic losses. The effectiveness of
portable electric fences in preventing predation by Iberian lynx on lambs in such flocks was evaluated. Electric fences were installed around two flocks of sheep suffering from attacks by Iberian
lynx. Before the experiment, both flocks grazed without any surveillance during the day. At night,
sheep with a single lamb were left to roam freely or spent the night in a poorly constructed enclosure. Sheep with two lambs remained with their lambs without any type of protection. After
the electrified enclosures were put in place, sheep with lambs were moved inside at night. No attacks were detected inside the electric fences. During the daytime, four attacks on lambs grazing
without surveillance were recorded. Despite the initial success of this experiment, more study is
still needed to test the long-term effectiveness of this preventive tool as a means of minimizing the
conflict between Iberian lynx and humans at a broader scale.
Predation by carnivores on livestock and subsequent retaliatory persecution are conservation concerns the world over (Bagchi and Mishra,
2006), and many carnivore conservation measures target to prevent this
type of conflict (Treves and Karanth, 2003). Compensation schemes
have been established in many wild felid conservation programs that
aim to mitigate the losses suffered by herders (Loveridge et al., 2010).
Although compensation is a necessary and effective measure in the
short term, preventing predation is probably a better strategy in the
long-term (Garrote et al., 2013).
To mitigate the conflict arising from predation by the critically endangered Iberian lynx (Lynx pardinus; IUCN, 2011) on livestock, a
prevention and compensation program was implemented in order to
compensate farmers for the poultry and lambs killed by this felid (Garrote et al., 2013). Although the majority of attacks were carried out on
poultry, greater economic losses were caused by predation on lambs in
extensive flocks. The goal of this study was to evaluate the effectiveness of portable electric fences in avoiding Iberian lynx predation on
lambs in extensive flocks. The work was conducted under the auspices
of the Iberian lynx conservation LIFE project in Andalusia (see Simón
et al., 2012).
The study was conducted on two flocks of sheep whose lambs had
been predated by Iberian lynx since 2011. Both flocks were located on
private estates at the eastern limit of this felid’s known range in the Sierra Morena (SE Spain; Simón et al., 2012). This mountainous area
is covered by well-preserved Mediterranean forests and scrubland and
large game reserves are the main land use. Each flock is composed of
about 500 head of sheep and produces between 420 and 500 lambs per
year. Although both flocks graze in the Iberian lynx distribution area
by day without surveillance, prior to our testing husbandry practices
differed during the night. In flock 1, sheep without lambs and most of
∗
Email address: [email protected] (Germán Garrote)
doi:10.4404/hystrix-26.1-10957
those with just a single lamb were left to graze freely. Occasionally,
ewes with one lamb spent the night in a small enclosure close to the
shepherd’s house. Sheep with two lambs were tied up with their lambs
in an area between 10 and 500 m from the shepherd’s house without any
other type of protection. In flock 2, ewes with a single lamb spent the
night in a small enclosure close to the shepherd’s house, whereas those
with two lambs were tied up with their lambs in the outer part of the enclosure. In both cases, the pens where sheep were enclosed at night had
no more than one meter-high fence and were poorly constructed. The
mating season is controlled in both flocks to obtain two different lambing periods: half of the flock gives birth in December-January (winter
births) and the other half in March-April (spring births), and Iberian
lynx attacks in previous years were concentrated during these two periods.
Between December 2012 and May 2014 (including both lambing
seasons) we registered all attacks on the studied flocks. We considered
only attacks that could be unambiguously attributed to Iberian lynx by
footprints, scats, photographs or by distinctive marks left on uneaten
animals (Garrote et al., 2013). In early March 2013 (before the spring
lambing season), a portable electric enclosure with a total perimeter
of 75 m and 106-cm high fence was placed around each flock. The
fence consisted of a braided plastic rope that was live over its entire
length. In order to increase the height of the fence, two 4-cm wide conductor strips were placed over the mesh giving a total height of 160 cm
(Fig. 1). A generator with a battery recharged by solar panels was included in each enclosure. Enclosures were fixed in position. In flock
1, all sheep with lambs (irrespective of their number) were moved inside the electric enclosure at night. In flock 2, sheep with one lamb
continued using the traditional enclosure, while those with two lambs
were moved inside the electric fence at night. This trial scheme was
maintained for three months until the youngest lamb was 1.5 months
old. During the 2013 winter lambing season, both flocks suffered from
attacks by Iberian lynx. Ten of such events, involving 10 lambs, took
place during the day when sheep were grazing freely, whereas 7 events
13th June 2015
26(1): 61–62
took place at night, both in the free and tied-up flocks, involving 13
lambs. After the installation of the electric fences (spring lambing season in 2013, winter and spring lambing season in 2014), no attacks by
Iberian lynx or other carnivores occurred inside the fences. In flock 2,
one week after the installation of the electric fence we found it partially
broken down with Iberian lynx hairs entangled, a likely indication of a
predation attempt during which the electric discharge might have dissuaded the lynx from killing a lamb. During the daytime, however, we
recorded four attacks on lambs grazing without surveillance.
Despite the impossibility of unambiguously determining the factors
leading to the lack of attacks at night detected during the study, it is
likely that two factors in particular were of importance: flock protection
at night and the dissuasive ability of the electrified enclosure. Local
shepherds participated in the design of the enclosures and the choice of
materials. They believed in the effectiveness of this prevention method
and agreed to enclose their lambs at night. This way of managing livestock is known to reduce felid attacks on livestock (Scognamillo et al.,
2002). Even so, enclosing animals is not always enough to prevent felid predation (see Saenz and Carrillo, 2002), and in the past the owner
of flock 1 lost lambs to predation inside a non-electrified enclosure.
Given that Iberian lynxes have been seen to jump over fences of up to
2-m high, 1.6 m is not by any means an insuperable height for them.
Like other felid species (Schiaffino et al., 2002; Scognamillo et al.,
2002), Iberian lynx frequently pass through mesh fences that control
cattle movements. Lynx can usually penetrate a lightweight mesh and,
given the similarity of the electrified fence to the standard fence, the
lynx may have tried to pass through instead of jumping over, thereby
suffering the electric shock that dissuaded them from entering again.
This would seem to explain why electric fences are effective in avoiding predation on livestock in other felid species (see Scognamillo et al.,
2002).
Electrified fences are easy to set up in the field and are cost-effective
anti-predator deterrents. Despite the initial success we reported in this
preliminary testing, further study on the effectiveness of preventive
tools in minimizing the conflict between Iberian lynx and humans are
clearly needed. Moreover, the problem of daytime predation has still
not been resolved. In these cases, farmers should be encouraged to
become involved in managing human-wildlife conflicts, above all by
improving their own herding and vigilance practices, by building better herding facilities and by adopting more reliable herding procedures
(see Wang and Mcdonald, 2006). Managers, researchers and farmers
must work together in the planning and implementation of appropriate
and effective programs and actions aimed at resolving this conflict, as
this collaboration could further enhance farmers willingness to coexist
with large carnivores.
Figure 1 – Technical drawing of the fence structure.
References
Bagchi S., Mishra C. 2006. Living with large carnivores: predation on livestock by the snow
leopard (Uncia uncia). J. Zool. 268: 217–224.
Garrote G., López G., Gil-Sánchez J.M., Rojas E., Ruiz M., Bueno J.F., de Lillo S.,
Rodríguez-Siles J., Martín J.M., Pérez J., García-Tardío M., Valenzuela G., Simón M.A.
2013. Human–felid conflict as a further handicap to the conservation of the critically endangered Iberian lynx. Eur. J. Wild. Res. 59: 287–290.
IUCN (International Union for Conservation of Nature) 2011. 2011 IUCN red list of
threatened animals. IUCN, Gland, Switzerland and Cambridge, UK.
Loveridge A.J., Wang S.W., Frank L.G., Seidensticker J. 2010. People and wild felids: conservation of cats and management of conflicts. In: McDonald D.W., Loveridge A.J.
(Eds.). Biology and conservation of wild felids, 1st ed. Oxford University Press, London, UK. pp. 161–195
Saenz J.C., Carrillo E. 2002. Jaguares depredadores de ganado en Costa Rica: ¿un problema sin solución?. In: Medellín R.A., Equihua C., Chetkiewic C.L.B., Crawshaw P.G.,
Rabinowitz A., Redford K.H., Robinson J.G., Sanderson E.W., Taber A.B. (Eds.). El jaguar en el nuevo milenio. Fondo de Cultura Económica/Universidad Nacional Autónoma
de México/Wildlife Conservation Society, México City, México. pp. 139–150.
Schiaffino K., Malmirca L., Perovic P. 2002. Depredación de cerdos domésticos por jaguar
en un área rural vecina a un parque nacional en el noreste de Argentina. In: Medellín
R.A., Equihua C.,Chetkiewic C.L.B., Crawshaw P.G., Rabinowitz A., Redford K.H.,
Robinson J.G., Sanderson E.W., Taber A.B. (Eds.). El jaguar en el nuevo milenio. Fondo
de Cultura Económica/Universidad Nacional Autónoma de México/Wildlife Conservation Society, México City, México. pp. 251–264.
Scognamillo D., Maxit I., Sunquist M.E., Farrell L. 2002. Ecología del jaguar y el problema
de la depredación de ganado en un hato de Los Llanos Venezolanos. In: Medellín R.A.,
Equihua C., Chetkiewic C.L.B., Crawshaw P.G., Rabinowitz A., Redford K.H., Robinson J.G., Sanderson E.W., Taber A.B. (Eds.). El jaguar en el nuevo milenio. Fondo de
Cultura Económica/Universidad Nacional Autónoma de México/Wildlife Conservation
Society, México City, México. pp. 139–151.
Simón M.A., Gil-Sánchez J.M., Ruiz G., Garrote G., McCain E., Fernández L., López-Parra
M., Rojas E., Arenas-Rojas R., del Rey T., García-Tardío M., López G. 2012. Reverse
of the decline of the endangered Iberian lynx. Conserv. Biol. 26: 731–736.
Treves A., Karanth K.U. 2003. Human–carnivore conflict and perspectives on carnivore
management worldwide. Conserv. Biol. 17: 1491–1499.
Wang S.W., Mcdonald D.W. 2006. Livestock predation by carnivores in Jigme Singye
Wangchuck National Park, Bhutan. Biol. Conserv. 129: 558–565.
Associate Editor: P. Ciucci
62
HYSTRIX
Volume 26(1) • 2015
Aims and scope
Hystrix, the Italian Journal of Mammalogy accepts papers on original research in basic and applied mammalogy on fossil and
living mammals. The Journal is published both in paper and electronic “online first” format. Manuscripts can be published
as full papers or short notes, as well as reviews on methods or theoretical issues related to mammals. Commentaries can
also be occasionally accepted, under the approval by the Editor in Chief. Investigations of local or regional interest, new data
about species distribution and range extensions or confirmatory research can be considered only when they have significant
implications. Such studies should preferably be submitted as short notes. Manuscripts bearing only a local interest will not be
accepted.
Full papers have no limits in length as well as in figure and table number and are abstracted in English. Authors are
encouraged to add supplemental material in form of colour figures, original datasets and/or computer program source code.
Supplemental material and colour figures will appear only on the electronic edition.
Short notes must be about 16000 characters long (including title, author names and affiliations, abstract and references),
and do not include supplemental material. They are abstracted in English.
Proceedings of symposia, meetings and/or workshops, and technical reports can be published as special supplements to
regular issues, under the approval by the Editor in Chief and the Associate Editors.
There are no page charges.
Manuscript submission
Manuscripts must be submitted electronically registering to the on-line submission system at the Journal web site (http://www.
italian-journal-of-mammalogy.it). A comprehensive Electronic Publication Guide can be downloaded from the Journal web
site: Part II of that document contains a detailed step-by-step description of the electronic submission process. Authors must
submit at least a manuscript file; a cover letter and a copyright transfer form are not necessary since the electronic submission
process provides both for manuscript presentation and copyright transfer acceptance. Tables and figures must be included in
the manuscript file, whilst other supplemental material (if any) must be uploaded separately.
Manuscript structure
Full papers: manuscript must be divided into sections in the following sequence: title page (page 1), abstract and keywords,
(page 2), introduction (from page 3 onwards), materials and methods, results and discussion, acknowledgements, list of symbols
(if any), references. Tables, legends of figures and figures should be on separate pages as specified above. If necessary and
useful to improve manuscript readability, a single section could be divided into subsections or paragraphs. If necessary,
conclusions and/or any final consideration can be stated as a last paragraph of results and discussion.
Short notes do not have Introduction, Material and methods, Results and Discussion, and are organised in a single section.
Authors are advised to structure Short notes without subdivision of the text, with an Abstract in English. The whole length
of the manuscript must not exceed 16000 characters (spaces included), comprehensive of title, author names and affiliations,
abstract, text body and references. In a short note references should be kept to a minimum.
Publication process
The Technical Editor checks all submitted manuscripts for compliance with the Instructions to Authors. The Editor in Chief
then assigns the manuscript to an Associate Editor for the peer-review process. Once accepted, the manuscript will be typeset
and a final galley will be sent to Authors for their approval. Once approved by the Authors, the manuscript will be published
“online first” and will be printed in the next available issue.
Privacy statement
The names and email addresses appearing in this journal will be used exclusively for the stated journal’s purposes and will not be made available for any other
purpose or to any other party, as provided by the Italian Law no. 675, 31/12/1996. No notification to the Warrant is needed, as provided in art. 7, sec. 5ter,
a), f), Italian Law no. 675, 31/12/1996.
Open Access Policy
This journal provides open access to all of its content on the principle that making research freely available to the public supports a greater global exchange
of knowledge. For more information on this approach, see the Public Knowledge Project (http://pkp.sfu.ca), which has designed this system to improve the
scholarly and public quality of research, and which freely distributes the journal system as well as other software to support the open access publishing of
scholarly resources.
HYSTRIX
Volume 26(1) • 2015
Contents
Rohlf F.J. – The tps series of software . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Galimberti A., Sandionigi A., Bruno A., Bellati A., Casiraghi M. – DNA barcoding in
mammals: what’s new and where next? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Bertolino S., Colangelo P., Mori E., Capizzi D. – Good for management, not for
conservation: an overview of research, conservation and management of Italian small
mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Battisti C., Marini F., Vignoli L. – A five-year cycle of coypu abundance in a remnant
wetland: a case of sink population collapse? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
9
13
25
37
Joshi R. – Tusker’s social bonds in Rajaji . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Mori E., Mazza G., Menchetti M., Panzeri M., Gager Y., Bertolino S., Di Febbraro
M. – The masked invader strikes again: the conquest of Italy by the Northern raccoon
41
47
Amori G., Milana G., Rotondo C., Luiselli L. – Macro-ecological patterns of the endemic
Afrosoricida and Rodentia of Madagascar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
53
Gashchak S., Vlaschenko A., Eśtok P., Kravchenko K. – New long-distance recapture
of a Noctule (Nyctalus noctula) from eastern Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
59
Garrote G., López G., Ruiz M., de Lillo S., Bueno J.F., Simon M.A. – Effectiveness of
electric fences as a means to prevent Iberian lynx (Lynx pardinus) predation on lambs
61

- Hystrix, the Italian Journal of Mammalogy

Transcription

Similar documents

EasyPure Genomic DNA Spin Kit

The Masterof

WHY INTERNAL COMMUNICATIONS?

Central Dogma of Biology Nucleic Acids

Presentation - Produce Marketing Association

DNA Structure - hrsbstaff.ednet.ns.ca

Video: The Incredible World Of the Microscope

Cell division

`CSI effect` impacts justice in Tucson