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Pan-American Journal of Aquatic Sciences
Research articles
The egg capsule of Rioraja agassizi (Müller & Henle) (Elasmobranchii, Rajidae), endemic to the
SW Atlantic.
ODDONE, M. C., MESA, A. & AMORIM, A. F..…………..…………………………………………43
Multivariate morphological analyses in continental and island populations of Abudefduf saxatilis
(Linnaeus) (Pomacentridae, Perciformes) of Western Atlantic.
MOLINA, W. F., SHIBATTA, O. A. & GALETTI-JR, P. M.......................................................................49
Impacto potencial de invasión de Ficopomatus enigmaticus (Fauvel) (Polychaeta: Serpulidae) en la
Laguna de Rocha, Uruguay.
BORTHAGARAY, A. I., CLEMENTE, J. M., BOCCARDI, L., BRUGNOLI, E. & MUNIZ, P......…………...57
Record of a pregnant bentfin devilray, Mobula thurstoni (Lloyd) (Elasmobranchii, Mobulidae)
caught in Southwestern Brazil.
CASAS, A. L. S., CUNHA, C. M., INTELIZANO, W. & GONZALEZ, M. M. B.....……….........................66
Intestinal bacterial diversity in live rock lobster Panulirus homarus (Linnaeus) (Decapoda,
Pleocyemata, Palinuridae) during transportation process.
IMMANUEL, G., RAJ, P. I., RAJ, P. E. & PALAVESAM, A......................................................................69
Morphological aspects and seasonal changes of some planktonic ciliates (Protozoa) from a
temporary pond in Buenos Aires Province, Argentina.
KÜPPERS, G. C., LOPRETTO, E. C. & CLAPS M. C…...........................................................................74
Ocupação da praia da Boa Viagem (Recife/PE) ao longo de dois dias de verão: um estudo
preliminar.
SILVA, J. S., BARBOSA, S. C. T., LEAL, M. M. V., LINS, A. R. & COSTA, M. F....................................91
Report on the smallfin catshark Apristurus parvipinnis Springer & Heemstra (Chondrichthyes,
Scyliorhinidae) in Western South Atlantic with notes on its taxonomy.
GOMES, U. L., SIGNORI, C. N. & GADIG, O. B. F.................................................................................99
Benthic macroinvertebrate bycatch in the snail Zidona dufresnei (Donovan) fishery from the
Uruguayan continental shelf.
RIESTRA, G., LOZOYA, J. P., FABIANO, G., SANTANA, O & CARRIZO, D...........................................104
Feeding Ecology of Nereis diversicolor (O.F. Müller) (Annelida, Polychaeta) on Estuarine and
Lagoon Environments in the Southwest Coast of Portugal.
COSTA, P. F., OLIVEIRA, R. F. & FONSECA, L. C...............................................................................114
Pan-American Journal of Aquatic Sciences (2006), 1 (1)
Original scientific photographs
Genidens genidens (Cuvier) (Pisces, Ariidae), oral incubation of eggs.
GARCIA, A. M., VIEIRA, J. P. & BURNS, M. D. M..................................................................................I
Eunectes murinus (Linnaeus) (Serpentes, Boidae), preying activity.
MACEDO-BERNARDE, L. C...................................................................................................................II
Software and Book Review
POSEIDON LINUX – Uma distribuição Linux voltada para público acadêmico e científico.
FERREIRA, C. F., VELASCO, G., ALBERGONE, E. H., HELLEBRANDT, D., VAZ, B. S............................III
Pan-American Journal of Aquatic Sciences (2006), 1 (1)
The egg capsule of Rioraja agassizi (Müller & Henle)
(Elasmobranchii, Rajidae), endemic to the SW Atlantic
MARÍA CRISTINA ODDONE1,3, ALEJO MESA1 & ALBERTO FERREIRA DE AMORIM2
1
Universidade Estadual Paulista, Departamento de Ecologia, Campus Rio Claro Av. 24-A 1515, CP 199, CEP 13506900, Rio Claro, SP, Brazil.
2
Instituto de Pesca, Av. Bartolomeu de Gusmão, 192, Ponta da Praia, CEP: 11030-906, Santos, SP, Brazil.
3
Correspondence to: M. C. Oddone: [email protected]
Abstract. Freshly collected egg capsules of Rioraja agassizi were light and bright brown in colour,
laterally keeled and symmetrically convex with a smooth configuration of the surface. The base of
the horns, the lateral margins and the ventral wall of the egg capsules were covered by sticky, shiny
yellow attaching fibrils. The mean total length of the egg capsules was 47 mm and the mean width
was 31 mm. Microscopically, the dorsal wall of the egg capsules was 0.21 mm thick and consisted
of three layers, being the central one colourless and laminated. The ventral wall was 0.11 mm in
thickness and presented the same layer’s patterns of the dorsal wall. Length of the egg capsules
positively increased with female’s length.
Key words: oviparity, lateral keel, egg-bearing, microscopic structure.
Resumen. La cápsula ovígera de Rioraja agassizi (Müller & Henle, 1841) (Elasmobranchii,
Rajidae), endémica del Atlántico SW. Las cápsulas ovígeras de Rioraja agassizi recientemente
colectadas eran de un color marrón claro brillante, presentaban una quilla lateral, eran
simétricamente convexas y poseían superficies lisas. La base de los cuernos, así como los márgenes
laterales y la pared ventral estaban recubiertos por filamentos pegajosos de adhesión de color
amarillo brillante. La longitud total media de las cápsulas fue 47 mm y el ancho medio 31 mm.
Microscópicamente, la pared dorsal de las cápsulas ovígeras tenía un grosor de 0.21 mm y consistía
en tres capas, siendo la del medio descolorida y laminada. La pared ventral tenía un grosor de 0.11
mm y presentaba el mismo patrón laminar de la fase dorsal. La longitud de las cápsulas ovígeras
aumentó positivamente con la longitud total de las hembras.
Palabras clave: oviparidad, quilla lateral, ovada, estructura microscópica
Introduction
The genus Rioraja is endemic to the austral
region of South America (McEachran & Aschliman
2004) and comprises one single species, R. agassizi
(Müller & Henle 1841), which occurs from
Argentinean waters to Rio de Janeiro in
Brazil and inhabits from coastal waters to
depths of up to 130 m (Figueiredo 1977).
In south Brazil is considered a constantly present
species being found from 15 to 60 m of depth
(Vooren 1997).
In oviparous elasmobranchs the egg is
covered with a thick leathery membrane, the egg
capsule (shell) with features that aid in their
identification
besides
establishing
possible
relationships between genera and even between
species; apart from throwing some light on adaptive
differentiation of various species (Ishiyama 1958).
Apart from providing taxonomic information (Hubbs
& Ishiyama 1968), the morphology and external
features of the skate’s egg capsules can provide data
on the distribution and reproductive biology of
skates (Oddone et al. 2004). Furthermore, Ishiyama
(1958) demonstrated that the microscopic structure
of Japanese skates’ egg capsules is an important
source of systematic information on the different
rajid species.
In this work, the morphological and
microscopical description of the egg capsule of R.
agassizi is presented.
Pan-American Journal of Aquatic Sciences (2006), 1 (2): 43-48
M. C. ODDONE ET AL.
44
Materials and Methods
A number of 119 egg capsules of Rioraja
agassizi were collected by bottom trawler
commercial vessels during March and May 2005, off
Southeast Brazil. The fishing area is presented in
Figure 1. Depth ranged between 13 and 52 m. Egg
capsules were directly extracted from the females’
uteri; fixed in 4% formalin and preserved in 70%
ethanol (Fig. 2). Terminology on the egg capsule
and methods of measurements followed Hubbs &
Ishiyama (1968) Templeman (1982) and Gomes &
Carvalho (1995).
Rio de Janeiro
22°
23°
100
500
São Paulo
24°
25° Paraná
26°
27°
Santa Catarina
28°
100
500
49° 48° 47° 46° 45° 44° 43° 42° 41° 40°
Figure 1. Map of the study area: Southeast Brazil, showing the
trawling stations (dotted circles) from where samples of Rioraja
agassizi came from.
Data recorded from each egg capsule were
classified into measurable variables and features
(Hubbs & Ishiyama 1968). The measurable variables
were: total length; total width; total length of
anterior and posterior horns, height (in the highest
point) and thickness and width of the lateral keel.
Features recorded were: colour; configuration of the
surface or texture; basic morphology, presence of
adhesion fibrils and microscopical structure of both
sides of the capsule’s wall. Horns were measured on
each side, according to Hubbs & Ishiyama (1968).
All measurements were made with Vernier
calipers with 0.1 mm precision. Differences were
tested using a t-test (Sokal & Rohlf 1987) with a
significance
level
of
0.05.
The
terms
‘anterior’/’posterior’ and ‘ventral/’dorsal’ refer to
the position of the egg capsules in the uteri (Clark
1922, Hubbs & Ishiyama 1968).
To examine the microscopical structure of
the egg capsules’ wall, rectangular sections (5x5
mm) of the dorsal and ventral walls were carried out
centrally on the egg capsules using a scalpel
according to Hubbs & Ishiyama (1968). The latter
were submitted to the following inclusion protocol
in historesin to be afterwards cut with the aid of a
microtome: a) sections were dehydrated for half an
hour in alcohol 70%, 80 %, 90 % and finally 95 %;
b) an embedding resin was prepared and reposed for
24 hours refrigerated; c) preparation protocol for
inclusion resin consisted in mixing 15 ml of the
embedding plus 1 ml of the hardener solution,
shaking (in the shaker) for 3 minutes and depositing
in mould, where the egg capsules’ cuts were
incorporated and hold with tweezers until the resin
hardened to keep the vertical position to allow the
transversal cut desired in the microtome; d) the
samples were kept in heater for 24 hours and
immersed in silica to extract humidity; e) moulds
containing the sections were glued to wooden blocks
to be cut in the microtome (LEICA RM 2145,
at Histology Laboratory, Biology Department,
UNESP); f) after discriminating between several
thickness in the microtome and observing in the
microscope, the ideal thickness was found to
be 8 μ and this thickness was kept for all the cuts.
Sections were placed in the slides and deposited
in the heater for 24 hours; g) sections were
embedded in Canadian Balsam, covered with cover
slide, deposited in the heater for 48 hours for
fixation; h) sections were observed under
microscope (at 100X) for black and white
photographing and assessing. Internal layer refers to
the egg capsule’s wall layer oriented to the capsule
interior; external layer refers to the layer in contact
to the exterior.
n.g.
Figure 2. Complete posterior oviducts (uteri) recently extracted
from a female of Rioraja agassizi bearing term egg capsules;
n.g.=nidamental glands. Black bar represents 1 cm.
A linear regression was used to analyse the
relationship between total length of the egg capsule
and total length of the female.
The egg capsule of Rioraja agassizi.
45
Results
In all the analysed females, only one
egg capsule per uterus was found. Freshly collected
and fully formed egg capsules of R. agassizi
were typically rectangular with a horny process
in each corner and bright brown in colour.
The base of the horns, the lateral margins and the
ventral wall of the egg capsules were covered
by sticky, shiny yellow adhesion fibrils.
To the naked eye and touch, both dorsal and
ventral walls were smooth. In lateral view, the
egg capsules were keeled and symmetrically
convex, with the highest point situated
centrally (Fig. 3).
laminated, with a number of 28 superimposed
lamina and 0.182 mm thick and an interior rather
thin layer; dark brown and 0.007 mm thick (Fig. 4a).
The ventral wall presented the same pattern of a
light, middle uncoloured layer between two darker
and rather thinner layers. In transverse section, the
ventral wall of the egg capsule was 0.11 mm in
thickness. The most external layer was dark brown
and 0.022 mm thick, followed by a middle layer,
colourless and laminar (consisting of about
20 lamina) and 0.084 mm thick, and finally, an
interior layer, dark brown and 0.0044 mm wide (Fig.
4b).
a
ext
int
b
ext
The total length of the egg capsules
of R. agassizi ranged from 41 to 56 mm
(mean=47.34) and the width ranged from
22 to 36 mm (mean=30.53). The descriptive
statistics for all the morphological variables
recorded are presented in Table I. The anterior
horns’ length varied from 38 to 53 cm (mean=49.15)
and posterior horns’ length from 35 to 68.
Posterior horns were significantly longer than
anterior horns (t=-15.1, P>0.000, df=95). The ratio
posterior/anterior horns was 1:4. The lateral keel
was in mean 1.16 mm wide and 1.66 mm thick. The
egg capsules had a mean height of 12.08 mm. In
eight egg capsules, anterior velum was absent, and
was variable in length when existing, with a mean
length of 3.34 mm and the posterior velum of 6.33.
Microscopically, the dorsal wall of the egg
capsule of R. agassizi was 0.21 mm thick and
consisted of three layers: an external layer; dark
brown and markedly darker than the rest, 0.023 mm
thick; a middle layer; colourless, luminous and
int
Figure 4. The microscopical structure of the dorsal (a) and
ventral (b) walls of Rioraja agassizi (100X); ext.=external;
int.=internal.
Larger females were found to produce larger
egg
capsules
according
to:
ECL=0.0402*FTL+1.1632
(ECL=egg
capsule
length; FTL=female total length). The total length of
the egg capsule as dependent variable had a positive
and significant (p < 0.000, R=0,61) relationship with
the female’s total length (Fig. 5).
TOTAL LENGTH EGG CAPSULE (cm)
Figure 3. The term egg capsule of Rioraja agassizi in lateral
view (above) and upper view (below). Black bar represents 1
cm.
4.0
3.5
3.0
2.5
2.0
30
35
40
45
50
55
60
65
70
TOTAL LENGTH FEMALE (cm)
Figure 5. The relationship between female’s total length (cm)
and egg capsule’s length (cm) for Rioraja agassizi.
M. C. ODDONE ET AL.
46
Table I. Descriptive statistics for the variables measured (mm) on the egg capsules of Rioraja agassizi; number (n),
mean, range, standard deviation (SD) and standard error (SE) for: total length, total width, height, width and thickness
of the keel, length of anterior and posterior horns (A., P., horns), length of anterior and posterior velum (A., P., velum).
Variable
Total length
Total width
Height
Keel width
Keel thickness
A. horns
P. horns
P. velum
A. velum
n
119
118
79
110
110
112
107
114
55
Mean
47.34
30.53
12.08
1.16
1.66
35.93
49.15
6.33
3.34
Discussion
Single oviparity (one embryo per egg
capsule) is the only type of reproduction in the
family Rajidae, being one egg deposited at a time
from each oviduct usually in pairs during the
spawning season (Musick & Ellis 2005).
The smooth surface of the egg capsule of
R. agassizi distinguishes it from the egg capsules of
the species of genus Atlantoraja, where a marked
(and macroscopical) longitudinal striation exist, with
the exceptional egg capsule of A. castelnaui which
has a rather smooth surface that resemble the egg
capsule’s surface of R. agassizi, even in the
microscopical composition of the egg capsule’s wall
(Oddone, unpublished data). In the Japanese rajids,
there is a notorious difference in the configuration of
the surface of the main portion of the capsules
between the northern and the southern species; being
the capsule somewhat roughened with minute
prickles or tubercles over the entire surface in the
northern forms, but it is, in general, very smooth in
the southern ones (Ishiyama 1958).
Another difference with the genus
Atlantoraja is the equally convex walls of the egg
capsule of R. agassizi, that are also typical of
Sympterygia acuta, S. bonapartii, and Psammobatis
spp. (Oddone & Vooren 2002, Oddone et al. 2004).
The egg capsule of R. agassizi is smaller than the
egg capsules of Atlantoraja spp. (with a mean size
of ~47x30 cm against 68x39 cm in A. cyclophora,
the smallest egg capsule of the genus) and than the
egg capsules of S. bonapartii with mean dimensions
of 77x48 cm (Mabragaña et al. 2002), but somewhat
larger than S. acuta’s, with mean size of ~5x3 cm.
The latter can be easily distinguished because of the
coloration (green olive) and the presence of tendrils
instead of posterior horns as in R. agassizi (Oddone
& Vooren 2002).
The disposition of the adhesion fibrils in R.
agassizi is the same than observed in Atlantoraja
Range
41-56
22-36
7-15
1-2
1-3
15-53
35-68
3-10
1-6
SD
3.09
2.32
1.45
0.33
0.42
1.06
6.54
1.13
1.33
SE
0.28
0.21
0.16
0.03
0.04
0.45
0.45
0.11
0.18
spp. (Oddone et al. 2004, Oddone, unpublished
data). In Callorhynchus milii a convex surface is
covered with sticky fibrils that attach sand thereby
camouflaging the egg capsule, while the opposite
side is smooth and acts as a suction cup to keep the
capsule planted in the sand (Hamlett et al. 2005) that
likely happens in R. agassizi. The degree of
development of the fibrils’ mass in some cases is a
character of value in distinguishing one species from
another (Ishiyama 1958).
Ishiyama (1958) recorded lateral keel in
20 of a total of 21 examined species. Egg capsules of
Rioraja are typically laterally keeled as in
Atlantoraja spp., unlike in genus Symperygia
(at least in S. acuta and S. bonapartii) where
capsules are laterally flanged (Mabragaña et al.
2002, Oddone et al. 2004). A striking external
feature of the egg capsule of R. agassizi was the
variability of the anterior velum length that varied
from absent to 6 mm, in some cases being longer
than the posterior velum.
The length of the horns shows rather large
intraspecific variations and as a rule, the length of
the posterior horns tends to appear a trifle longer
than that of the anterior ones (Ishiyama 1958).
In R. agassizi, the ratio posterior/anterior horns was
1.4. In Atlantoraja cyclophora and A. platana this
ratio was 2.4 and 2.7 respectively (Oddone et al.
2004). In S. acuta the ratio is 15.7, particularly high
because of the presence of tendrils instead of
(posterior) horns (Oddone & Vooren 2002).
As observed by Ishiyama (1958) for
Japanese rajid species, the main portion of the egg
capsule in R. agassizi is made of an internal, ‘pulpy’
layer and an external layer darker than the rest. The
author noted that, in general, the ‘pulpy’, middle
layer (forming the lining of the capsule wall) is
relatively soft and colourless, but the tissue becomes
hard and the colour changes from yellow to brown
in the external layer which covers the surface of the
The egg capsule of Rioraja agassizi.
47
capsule and that the degree of development of this
‘pulpy’ layer seemed to be correlated with the
distribution of the skates. In A. cyclophora, for
instance, the external layer corresponds with about
0.33% of the egg capsule’ wall in both ventral and
dorsal walls (Oddone, 2005). In R. agassizi, this
percentage is ~0.1-0.2. Ishiyama (1958) concluded
that there is a close relationship between the
differentiation of the capsule and the geographical
distribution, as well as the breeding habits of the
adult skates (though there are some examples that do
not fit this conclusion) and the much smoother
surface of an egg capsule’s species, could have
resulted from its adaptation to an environment where
the temperature is relatively high. This can be
related with the different areas inhabited by R.
agassizi and A. cyclophora; while the former prefers
coastal, shallow waters of up to 50 m deep, the latter
is found at deeper shelf waters of up to 300 m deep
(Vooren 1997, Oddone 2003, Oddone 2005).
Positive relationships between egg capsules length
and female’s total length have been observed for
several Rajidae and also Scyliorhinidae (Ishiyama
1958, Templeman 1982, Braccini & Chiaramonte
2002, Iglesias et al. 2002). Such relationship,
however, was not observed in Atlantoraja
cyclophora (Oddone 2003).
Acknowledgments
We are thanked to: P. L. Mancini for collaboration
in the samples’ collection and processing; skippers
of the CVs ‘Antares & Polares’, ‘Cigano do Mar’ I
& II, ‘Dourado & Araguaia’ and ‘Jangadeiro’, G.
M. Souza for histological assistence and three
referees who revised and improved the submitted
manuscript. This study was financed by FAPESP
(Fundação de Amparo à Pesquisa do Estado de São
Paulo).
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Received May 2006
Accepted June 2006
Published online June 2006
Multivariate morphological analyses in continental and
island populations of Abudefduf saxatilis (Linnaeus) (Pomacentridae,
Perciformes) of Western Atlantic
WAGNER F. MOLINA1, OSCAR A. SHIBATTA2 & PEDRO M. GALETTI-JR.3
1
Departamento de Biologia Celular e Genética, Centro de Biociências, Universidade Federal do Rio Grande do Norte,
CEP 59078-970 Natal, RN, Brazil. E-mail: [email protected]
2
Departamento de Biologia Geral, Universidade Estadual de Londrina, CEP 86051-970 Londrina-PR, Brazil.
3
Departamento de Genética e Evolução, Universidade Federal de São Carlos, Caixa Postal 676, CEP 13565-905 São
Carlos-SP, Brazil.
1
Corresponding author
Abstract. The reef species Abudefduf saxatilis (Linnaeus, 1758) is usually considered as a single large
Western Atlantic population distributed in reef habitats from northern United States (Rhode Island) to
Uruguay. However, principal components and canonical variables analyses of samples distributed along
the Brazilian coast (Rio Grande do Norte, Ceará, Bahia, Rio de Janeiro and Santa Catarina states), and
oceanic islands of Atol das Rocas and St. Paul’s Rocks, showed morphological variation, which could
suggest subdivisions among different populations. Clinal variations of meristic traits along the northsouth direction seem to have temperature as their main causative factor. Also, there was a greater
similarity among contiguous populations that become more differentiated with distance. In this context,
the Brazilian Current flowing, in north-south direction, seems to play an important dispersive role. There
were differences between insular and continental populations, which suggest the occurrence of selfrecruitment either by a possible existence of circular currents, an active larval role and/or a possible
selection for an optimal egg-laying period leading to restrictions in their dispersion. Thus, phenetic
divergences seem to suggest restrictions to the genetic flow in the South Atlantic A. saxatilis population.
Key words: morphological analyses; canonical variable; population structure; geographical barriers;
cline.
Resumo. Análises morfológicas multivariadas em populações continentais e insulares de Abudefduf
saxatilis (Linnaeus) (Pomacentridae, Perciformes) do Atlântico Ocidental. A espécie de peixe recifal,
Abudefduf saxatilis, tem sido considerada como uma única grande população Atlântica Ocidental
distribuída em habitats recifais do norte dos Estados Unidos (Rhode Island) ao Uruguai. Contudo,
análises por componentes principais e variáveis canônicas em amostras distribuídas ao longo da costa
Brasileira (Estados do Rio Grande do Norte, Ceará, Bahia, Rio de Janeiro e Santa Catarina), e das ilhas
oceânicas do Atol das Rocas e Rochedos de São Paulo, mostraram modificações morfológicas que podem
sugerir subdivisões entre diferentes populações. Alguns padrões gerais podem ser observados quanto à
distribuição de Abudefduf saxatilis. Variações clinais de características merísticas, na direção norte-sul,
indicam a temperatura como o principal fator causal. Além disso, há uma maior similaridade entre
populações contíguas que se tornam mais diferenciadas com a distância. Neste contexto, a Corrente do
Brasil que flui na direção norte-sul parece desempenhar um importante papel dispersivo. Existem
diferenças entre populações insulares e continentais, que sugerem a ocorrência de auto-recrutamento pela
possível existência de correntes circulares, um papel ativo de larvas e/ou seleção para um período ótimo
de desova levando a restrições a sua dispersão. Tais divergências fenéticas sugerem restrições ao fluxo
genético entre populações de A. saxatilis.
Palavras Chave: análises morfológicas; variáveis canônicas; estrutura populacional; barreiras
geográficas; clina.
W. F. MOLINA ET AL.
50
Introduction
In spite of its physical continuity, the marine
environment shows regional, oceanographic and
ecological peculiarities. Reef fish populations living
in distinct environmental conditions across wide
geographic areas may present subtle color
differentiation (Planes & Doherty 1997) or
significant modifications in their body shape (Bell et
al. 1982).
Pomacentridae family stands out as
important reef fishes because of its abundance in
Western Atlantic reefs. It has great species diversity
but because their morphological similarities (cryptic
species) and pigmentation patterns that vary
ontogenetically (Novelli et al. 2000) it is difficult to
differentiate among species. They are spread over
vast areas (Allen 1975), whereas distribution of
some species is restricted to oceanic islands (Emery
1972, Edwards & Lubbock 1983; Gasparini et al.,
1999). Others are found spread over vast areas
(Allen, 1975, 1991).
Among widely distributed groups, the genus
Abudefduf represents a good example of dispersive
capacity, especially A. saxatilis. This species is
distributed in reef and rocky environments from the
northern USA to the border with Uruguay (Menezes
& Figueiredo 1985). Disagreement about time
period and number of species divergences within
this genus has triggered molecular phylogenetic
studies (Lessios et al. 1995, Bermingham et al.
1997).
Pomacentridae shows great fidelity to their
microhabitats, and can live in certain reefs for
months or years (Reese 1973). This ecological
characteristic indicates little or no influence of
migration in their distribution, suggesting that it is
conditioned basically by larval dispersion. Despite
to its reduced pelagic larval stage (18-27 days), A.
saxatilis shows homogeneous populations through
Caribbean because its post larval, pelagic stage, may
extend up to 55 days (Shulman & Bermingham
1995).
It is known that modifications in body shape
of populations and species usually reflect an
association of environmental conditions and
adaptive genetic changes (Shaklee, 1984; Lessios et
al. 1995). Considering the current assumption of a
single large A. saxatilis population in the Atlantic
Ocean, the present study aimed to compare
geographically distant samples from the Brazilian
coast and oceanic islands. We used principal
components and canonical variables to analyze
meristic and multivariate morphometry data in order
to identify possible morphological variations
suggesting population subdivisions.
Samples of different sizes (juveniles and
adults) of A. saxatilis were collected in reef and
rocky bottoms in the Brazilian offshore Islands - St
Paul’s Rocks (0°55' N; 29°21' W), Atol das Rocas
(3o50' S; 33o49' W), respectively 960 km and 270
km in front to northern coast, and along Brazil coast
- Natal (05°52'43" S; 35°10'23" W) (Rio Grande do
Norte state), Tinharé Island (13º28' S; 39º02' W),
Cairu (Bahia state) and Bombinhas (27º07'54" S;
48º31'40" W), Penha (Santa Catarina state), and
Fortaleza (03º41'15" S; 38º29' W) (Ceará state; only
juveniles) (Fig.1). Samples were fixed in
formaldehyde at 10% and stored in 70% ethyl
alcohol. Body measurements were taken head to tail
using a caliper precision 0.05mm using the truss
networks method (Strauss & Bookstein 1982). The
samples for each geographic area are showed in the
Table I.
Figure 1. Map of the sampling locations. (1) Ceará, (2) Rio
Grande do Norte, (3) Atol das Rocas, (4) St Paul’s Rocks, (5)
Ilha de Tinhare, Bahia, (6) Bombinhas, Santa Catarina.
Twenty-two quantitative traits were
measured for each specimen. The following
morphological measurements of the distances of
landmarks (Fig. 2) in the comparative analysis of
Abudefduf saxatilis populations were used: 1. Predorsal distance, 2. Dorsal pectoral distance,
Multivariate morphological analyses in Abudefduf saxatilis.
51
Table I. Variation in meristic traits among Abudefduf saxatilis populations on the coast and oceanic islands
of Western Atlantic.
Area
N
min/
max
Atol das Rocas
16
14-15
St Paul’s
Rocks
11
13-14
Ceará
09
13
R.io Grande do
Norte
17
13-14
Bahia
13
13-14
Santa Catarina
10
12-13
Dorsal rays
Mode
14
(87%)
13
(63%)
13
(100%)
13
(94%)
13
(92%)
13
(90%)
Mean
14.1
13.4
13.0
13.0
13.1
12.9
Pectoral rays
min/
Mode Mean
max
19
19
19.0
(100%)
19
18-19
18.7
(72%)
19
18-19
18.9
(89%)
18-19
17-19
18.2
(94%)
19
18-19
18.8
(77%)
17
16-18
17.3
(50%)
3. Pectoral ventral distance, 4. Ventral-anal distance,
5. Pectoral anal distance, 6. Diagonal between the 1st
ray on the dorsal fin and 1st ray on the anal fin, 7.
Diagonal between the pectoral fin and the last ray on
the dorsal fin, 8. Diagonal of the 1st ray of the anal
fin to the start of the 3rd lateral bar, 9. Distance
between the 1st ray of the dorsal fin to the start of the
3rd lateral bar, 10. Length of the 1st ray of the anal
fin, 11. Distance between the start of the 3rd lateral
bar and the last dorsal fin ray, 12. Diagonal between
the 1st anal ray to the last dorsal ray, 13. Length from
the base of the dorsal fin, 14. Diagonal between the
1st ray of the dorsal fin to the last anal ray, 15.
Length of the base of the anal fin, 16. Diagonal
between the last ray of the dorsal fin to the last ray
of the anal fin, 17. Diagonal from the last ray of the
dorsal fin to the lower base of the tail, 18. Dorsal fin
Anal rays
min/
max
13-14
12-14
11-13
12
11-13
12-14
Mode
13
(75%)
13
(63%)
12
(66%)
12
(100%)
12
(54%)
12
(60%)
Mean
13.2
12.8
12.1
12.0
12.3
12.5
Lateral line scales
min/
Mode Mean
max
22
21-22
21.6
(56%)
21
21-22
21.4
(63%)
21
21-22
21.4
(55%)
21
21-22
21.4
(58%)
21
21-22
21.2
(77%)
21
21-22
21.5
(50%)
to upper tail base distance, 19. Distance anal fin to
lower base of the tail, 20. Diagonal from the last ray
of the anal fin to the upper base of the tail, 21.
Height of the tail peduncle, 22. Interorbital distance.
Body shapes were studied by morphometric
analysis of the canonical variables independent of
size (Reis et al. 1990). This analysis allows
visualization of morphological similarities among
individuals by projecting individual scores on
canonical axes of a bidimensional graph. It also
allows discrimination of traits obtained for each
group of individuals and related to collection points.
Principal components analysis (PCA) (Morrison
1976) was used to identify shape and size variation
among A. saxatilis individuals (n=76, using the
SAS®-PC (SAS Institute In. 1988) statistical
program. Meristic counts of the soft ray of dorsal,
pectoral and anal fins, and lateral line scales were
obtained for all samples. The geographic sites and
analyzed individuals per sample are showed in the
Table I.
Results
Figure 2. Abudefduf saxatilis (Linnaeus, 1758) specimen.
Landmarks used in this study (1-11 and interorbital distance IOD). (1) snout, (2) anterior base of dorsal fin. (3) anterior base
of pectoral fin (leading edge). (4) anterior base of pelvic fin. (5)
anterior base of anal fin. (6) length of first anal ray. (7) upper
edge of third lateral strip. (8) posterior base of dorsal fin. (9)
posterior base of anal fin. (10) ventral base of caudal fin. (11)
dorsal base of caudal fin. Scale bars = 5 cm.
Meristic characters
There were indications of a clinal reduction
in number of segments across the north-south
direction along the Brazilian coast (Table I). Atol
das Rocas samples showed highest values for almost
all traits analyzed, including samples from St Paul’s
Rocks, located further north. Clinal values were
more evident through analyses of structures means.
The lowest counts were detected at Bombinhas
(Santa Catarina state) in the southern portion of the
Brazilian coast. Number of lateral line scales hardly
varied among samples analyzed. However, a higher
modal value was observed in the Atol das Rocas
samples.
W. F. MOLINA ET AL.
52
Table II. Coefficients of variables on the first (PC1)
and second (PC2) principal component of traits
studied in the Abudefduf saxatilis populations.
Character
L1
L2
L3
L4
L5
L6
L7
L8
L9
L10
L11
L12
L13
L14
L15
L16
L17
L18
L19
L20
L21
L22
% variation
PC1
0.2002
0.2175
0.2404
0.2159
0.2313
0.2285
0.2188
0.2272
0.2259
0.1755
0.2198
0.2147
0.2217
0.2210
0.2128
0.2151
0.2007
0.1833
0.1751
0.1973
0.2159
0.2161
98.78
PC2
-0.0457
0.0898
0.0372
-0.3635
-0.3458
0.0084
-0.1659
0.0380
-0.0229
0.4615
-0.2884
0.0941
-0.0466
-0.0450.
0.1860
0.0039
0.0251
0.1429
-0.2299
-0.0754
0.1085
0.5212
0.2100
Principal Component Analysis (PCA)
Two eigenvectors extracted from the
variance-covariance matrix accounted for 98.78%
and 0.21% of the observed variation, respectively
(Table II). All coefficients of the first eigenvector
were positive, suggesting it may be interpreted as a
multivariate measurement of size. The second
eigenvector had positive and negative values and
could be interpreted as a shape axis.
Individual scores of A. saxatilis populations
plotted in PC1 and PC2 space (Fig. 3) revealed an
extensive overlap among samples distributed on PC2
axis. There were no precise differentiations among
island and continental samples, but samples from
Atol das Rocas and St Paul’s Rocks could be
discriminated from each other. Also, samples from
Atol das Rocas and Santa Catarina differentiated in
form. Individuals from Ceará formed a well defined
group by PC1, possibly reflecting the lower sizes of
these individuals.
Canonical Variables Analysis (CVA)
Canonical variables 1, 2 and 3 explained
51.41%, 25.43% and 11.73% of the observed
variation, respectively. Both axes had positive and
negative values showing interaction between shape
and size. The dispersion scores graphic of canonical
variable CV1, CV2 and CV3, plotted in
bidimensional space, indicate that point distances are
proportional to dissimilarity degree among
populations. The most important morphometric traits
in the discrimination of each variable (p = 0.001)
were the measurements 10, 7, 3 and 21 for the
negative side of the first axis. In contrast, variables
that most influenced the discrimination on the
second axis were 7, 5, 14 and 11 on the positive side
and 22, 12, 2 and 21 on the negative side.
Figure 3. Dispersion diagram of individual scores in different
Abudefduf saxatilis populations in the space defined by PC1 and
PC2. (a) Rio Grande do Norte, (b) Santa Catarina, (c) St Paul’s
Rocks (d) Atol das Rocas, (e) Ceará and (f) Bahia.
Similarly to PCA, the diagram of canonical
variable 1 (CV1) and canonical variable 2 (CV2)
(Fig. 4) showed that A. saxatilis from Ceará state
was different from other samples. Dispersion of
individual scores demonstrated overlapping among
samples of Bahia and Atol das Rocas, forming a
distinct cluster in the second canonical axis
compared to one composed by St Paul’s Rocks,
Santa Catarina and Rio Grande do Norte samples.
This analysis showed that samples from both
oceanic islands were different in shape and size.
Scores plotted in CV1 and CV3 spaces (Fig. 5)
discriminated island samples from those of continent
along CV3 axis. Continental samples showed greater
overlapping, except for Ceará samples, which
formed an isolated cluster along CV1. Specimens
from Atol das Rocas and St Paul’s Rocks were also
discriminated between each other by the size
component.
Figure 4. Dispersion of individual scores of Abudefduf saxatilis
populations in the space defined by CV1 and CV2. (a) Rio
Grande do Norte, (b) Santa Catarina, (c) St Paul’s Rocks, (d)
Atol das Rocas, (e) Ceará and (f) Bahia.
Figure 5. Dispersion of individual scores of Abudefduf saxatilis
populations in the space defined by CV1 and CV3. (a) Rio
Grande do Norte, (b) Santa Catarina, (c) St Paul’s Rocks, (d)
Atol das Rocas, (e) Ceará and (f) Bahia.
53
Discussion
Occurrence of physical barriers among
marine fish populations is not always clear (Joyeux
et al. 2001). However, geographic and/or ecological
subdivisions allow the establishment of population’s
traits
representing
suitable
models
for
biogeographic, taxonomic, ecological and genetic
studies. In such cases, morphometric analyses can
produce valuable information about phenotypic
plasticity of species and possible effects of genetic
changes on morphological variation (Hauser et al.
1995).
Abudefduf saxatilis populations along South
America coast showed a clinal gradient in the northsouth direction in relation to their meristic variables.
Temperature may be a decisive factor explaining
regional differences among these samples and it is
not uncommon for meristic traits to have lower
number of segments in colder waters at the southern
coast, when compared to northern warmer waters.
Usually,
parameters
delaying
ontogenetic
development, such as hypoxia, low temperatures,
high salinity and reduced food sources, favor the
development of greater number of body segments
(Barlow 1961; Shaklee & Tamaru 1981). Notably,
Atol das Rocas population had highest counts even
compared with St Paul’s Rocks located at the limit
of the equatorial line. Higher mean temperatures in
shallower waters of Atol das Rocas than those of St
Paul’s Rocks (environmental factor) or differences
in the genetic pool of these populations (genetic
factor) could account for this discrepancy.
In some cases, although temperature and
salinity influenced some species regarding numbers
of fins’ rays, certain structures are not modified by
different environmental conditions, suggesting a
major genetic control in the establishment of serial
elements (Barlow 1961).
Among various characteristics identified in
species with wide geographic distribution, size is the
most frequently observed. In Pomacentridae, clinal
variations in color have been shown and it is related
to the great variety of pigmentation patterns in this
species (Doherty et al. 1994). Genetic analyses,
carried out in populations with pigment variation,
have shown divergences (Amphiprion clarkii, Bell et
al. 1982, Acanthochromis polyacanthus, Planes &
Doherty 1997) or even the existence of cryptic
species in this group (Chrysiptera cyanea, Lacson
1994, Stegastes nigricans and Chrysiptera glauca,
Lacson & Clark 1995). However, the level of
genetic intraspecific variability is compatible with
the one observed in species with no color variations
(Lacson & Clark 1995). Although data suggesting
W. F. MOLINA ET AL.
54
between-populations, morphological and genetic
differences are not necessarily correlated (Gorman &
Kim 1977, Bell et al. 1982), genetic polymorphisms
detected by RAPD (Random Amplification of
Polymorphic DNA) markers or alozymes are
associated with pronounced among-population
morphometric variations in some marine species
(Dahle et al. 1997; Mamuris et al. 1998). Thus,
morphometric analyses can provide real data on
species plasticity and possible effects of genetic
changes on morphological traits.
Lessios et al. (1995) identified particular
color patterns, in the lower suborbital margin (scale
presence or absence) and in the pre-opercule,
between Abudefduf concolor from eastern Pacific
coast and A. declivifrons from Atlantic Ocean. Body
depth, snout length and caudal peduncle depth play a
discriminatory role among these species. These data,
together with molecular differences in mtDNA and
isoenzymes, confirmed they are distinct species. In
spite of separation estimative of ca. 14 to 15 million
years, they still show similar phenotypic
characteristics. Long periods of time, in some cases,
seem to be insufficient to overcome a conservative
situation in the morphotype of certain species. Thus,
isoenzymatic
markers
and
multivariate
morphometric analyses were able to discriminate
two sympatric and cryptic species of the Albula
genus in Hawaii waters. Even though they diverged
around 20 to 30 million years ago, these two species
seem to have extremely conservative morphology
(Shaklee & Tamaru 1981).
Abudefduf saxatilis populations showed little
morphological discrimination when analyzed by
principal components analysis. This methodology is
appropriated to access the morphological variability
in shape and size in different populations. Much of
the variation observed could be associated to a size
component. However, the analysis showed good
discrimination for shape between Atol das Rocas
(270 km from the coast) and St Paul’s Rocks (960
km from the coast) populations. Atol das Rocas was
also divergent in size and shape from Santa Catarina
coastal sample. These data agree with meristic
values showing that populations of these two
localities were markedly different. Ceará sample,
consisting of juvenile individuals, showed strong
discrimination in size.
Canonical
variable analysis showed
differentiation among populations in distinct
locations. Canonical variables 1 and 2 showed
greater body similarity among samples from Atol
das Rocas, Bahia and Ceará compared to those from
St Paul’s Rocks, Rio Grande do Norte and Santa
Catarina. Canonical variables 2 and 3 showed a
similar tendency, with both clusters being clearly
defined. This pattern could be explained by
dispersive events caused by the Equatorial South
Current that comes from East Atlantic, passes by St
Paul’s Rocks and Atol das Rocas and divides at Rio
Grande do Norte coast, with one branch following
the north coast as the Guyana Current and the other
flowing south as the Brazil Current. The South
Equatorial Current seems to provide a contact zone
among oceanic populations of the Atol das Rocas,
and the populations of Ceará (north coast) and
Bahia. Positioned between these two resulting
currents, Rio Grande do Norte population has lower
contact with these neighboring areas.
Abudefduf saxatilis population at St Paul’s
Rocks, because of its distance from the South
American coast, seems to form an isolated and selfmaintaining population. The discontinuity caused by
oceanic isolation was evident when canonical
variables 1 and 2 were analyzed. Two clusters,
diverging for shape, were discriminated; one oceanic
representing Atol das Rocas and St Paul’s Rocks
populations and another clustering coastal
populations.
Isolated A. saxatilis populations collected on
Ascension Island, southeast of St Paul’s Rocks in the
mid Atlantic, showed mtDNA pattern different from
those of Western Atlantic (Bermingham et al. 1997),
also suggesting a probable genetic component
associated to the morphological differences observed
in the geographical isolated St Paul’s Rocks and
Atol das Rocas populations.
Morphological and genetic differences in
island populations arise from the impediment to
genetic flow, caused by closed circulation currents
in the reproduction areas where eggs and larvae tend
to remain within their area of influence with few
possibilities to disperse and to establish contact with
populations from other areas. Clustering of coastal
populations in one group on PC1 and PC3 seems to
suggest an unidirectional dispersion system among
them, capable of showing shared similarities.
However, they had sufficient peculiar characteristics
to be distinguished by PC1 and PC2 axes.
The analyzed data indicated structuring of
morphologically distinct A. saxatilis populations in
the Brazilian Province, whose effects were attributed
to dispersion by dominant currents (e.g., Briggs
1974, Floeter et al. 2001). St Paul’s Rocks and Atol
das Rocas populations were differentiated
morphologically in all performed analyses.
Our study provided the first investigation
using methods of multivariate morphometry in
Atlantic populations of a reef fishes involving
distances over 5,000 km. Lower morphological
homogeneity than expected, emphasizes the
importance of conservation of these populations,
especially of the St Paul’s Rocks. These results,
complemented by future genetic marker analyses,
could support effective conservation Pomacentridae
species in South Atlantic.
Acknowledgments
The authors are grateful to P.R.A.M. Affonso for
sample collections of Rio de Janeiro and F. Hostim
for collection of individuals in Santa Catarina coast.
This research received funding from CAPES
(fellowship to WFM), CNPq and institutional
support from UFRN and UFSCar.
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Systematic Zoologic, 31: 113-135.
Received March 2006
Accepted June 2006
Published online June 2006
Impacto potencial de invasión de Ficopomatus enigmaticus (Fauvel)
(Polychaeta: Serpulidae) en la Laguna de Rocha, Uruguay
ANA INES BORTHAGARAY1, JUAN M. CLEMENTE1, LUCÍA BOCCARDI1,
ERNESTO BRUGNOLI1 & PABLO MUNIZ1,2
1
2
Departamento de Ecologia, Facultad de Ciencias, Iguá 4225, C.P.11.40, Montevideo, Uruguay.
Autor para correspondencia: Pablo Muniz. E-mail: [email protected]
Abstract. Potential impact of Ficopomatus enigmaticus (Fauvel) (Polychaeta: Serpulidae) invasion
in Laguna de Rocha, Uruguay. The aim of this work is to assess the invasion risk and the potential
impact of the exotic Ficopomatus enigmaticus on the benthic community structure of the northern zone
of Laguna de Rocha. These evaluations were done considering the similar environmental and biological
characteristics of this lagoon and other coastal systems on the Atlantic coast (Laguna Garzón and Arroyo
Valizas) and the Río de la Plata (Bahia de Montevideo and Arroyo Solís Grande) that had been infected
by this species. In Laguna de Mar Chiquita (Argentina), the most well studied ecosystem affected by this
polychaete, the presence of F. enigmaticus has substantially modified the landscape, promoting serious
ecological alterations. The environmental and benthic community characteristics of Laguna de Rocha are
favourable to the settlement of the species; therefore, we can consider this lagoon as a potential reception
ecosystem for the invasive pest F. enigmaticus. Because of the similarity between Rocha and Mar
Chiquita lagoons, it is possible to predict the potential impact that a F. enigmaticus invasion could cause
in Laguna de Rocha. Studies to achieve basic knowledge about the distribution and behaviour of this
species in Laguna de Rocha are important to determine the level of biological contamination in this
aquatic environment. The results of this study are required for the development of management and
control strategies of the invasion process of this species and will contribute to the conservation of the
aquatic biodiversity of Laguna de Rocha.
Key-word: biological contamination, invasive species, benthos, coastal lagoon.
Resumen. El objetivo de este trabajo es evaluar cualitativamente el riesgo de invasión y el impacto
potencial de la especie exótica Ficopomatus enigmaticus en la estructura de la comunidad bentónica en la
zona norte de la Laguna de Rocha. Esto se discute en base a la similitud de condiciones físicas y
biológicas de esta laguna con otros sistemas costeros, sobre la costa atlántica (Laguna Garzón y Arroyo
Valizas) y del Río de la Plata (Bahia de Montevideo, Arroyo Solís Grande) ya infectados por la especie.
En la laguna costera de Mar Chiquita (Argentina) la presencia de Ficopomatus enigmaticus ha
modificado notoriamente el paisaje del área, ocasionando serias alteraciones ecológicas. En un primer
análisis, la Laguna de Rocha puede considerarse un ecosistema potencialmente receptor para el poliqueto
invasor F. enigmaticus. Esta afirmación se sustenta en base a las condiciones físicas y biológicas que
presenta este cuerpo de agua, las cuales son favorables para el asentamiento de la especie. Dada la
similitud de características físicas y biológicas (comunidad bentónica) que presentan la Laguna de Rocha
y la Laguna de Mar Chiquita (Argentina) se podría predecir el impacto esperado sobre la Laguna de
Rocha. El desarrollo de estudios dirigidos a la generación de información básica sobre la distribución y
comportamiento de esta especie en la Laguna de Rocha es importante para determinar el estado de
contaminación biólogica en este sistema. Esto permitirá realizar un plan de manejo y control de este
poliqueto invasor, y contribuir a la conservación de la biodiversidad acuática nativa de la Laguna de
Rocha.
Palabras clave: contaminación biológica, especie invasora, bentos, laguna costera.
A. I. BORTHAGARAY ET AL
58
Introducción
La modificación o destrucción del hábitat a causa de
la introducción de especies exóticas es considerado
una de los principales factores responsable de la
pérdida de biodiversidad de los sistemas naturales
(Bertness 1984, Simberlof 1997). En tal sentido, el
resultado final y más dramático de la interacción
entre una especie nativa y otra exótica (ej.
competencia, depredación) es la extinción de la
primera. Como consecuencia de ello, la distribución
y abundancia de la especie nativa así como su
composición y dinámica se ven modificadas
(Stachowicz et al. 2002).
La gran mayoría de los ecosistemas
terrestres, marinos y continentales han sufrido las
consecuencias de las invasiones biológicas
(Williamson 1996, Parker et al. 1999).
Aproximadamente 102 - 104 especies exóticas han
sido documentadas (Ricciardi & Rasmussen 1998),
pero este número se incrementa con el tiempo como
consecuencia del intenso tráfico de fauna y flora de
una región geográfica a otra. En tal sentido, el agua
de lastre y el transporte de sedimentos son los
principales vectores de dispersión de especies
exóticas acuáticas (Carlton & Geller 1993, Ruiz et
al. 2000).
Una vez que la especie potencialmente
invasora ingresa en la nueva región (área receptora),
la probabilidad de un sistema de ser infectado
dependerá de las condiciones locales físico-químicas
y ecológicas, así como de las características
biológicas de la especie invasora. La invasibilidad
de un sistema, es decir, la susceptibilidad del
ambiente a ser invadido, es una propiedad emergente
de la comunidad receptora. Diferentes hipótesis
asociadas a disturbios (Crawley 1987), diversidad de
especies (Elton 1958, Tilman 1997), productividad
comunitaria (Tilman 1993) y fluctuaciones en la
disponibilidad de recursos (Davis et al. 2000) son
propuestas para explicar la invasibilidad de un nuevo
sistema (Davis & Pelsor 2001). Entre los
ecosistemas acuáticos, y según su estado de impacto,
existen diferentes grados de susceptibilidad a la
llegada de organismos exóticos. Los ambientes
marinos pelágicos presentan una susceptibilidad
menor que ambientes como ríos, lagos y zonas
costeras, que son especialmente vulnerables a este
fenómeno (Perrings 2002).
El impacto provocado será función de la
interacción entre la especie invasora y su nuevo
ambiente (Ricciardi 2003). De este modo, la
identificación de patrones de invasión a partir de
sitios ya infectados permitirán predecir el impacto de
una especie invasora en un nuevo sistema sobre los
diferentes niveles de organización biológica
(individuo, población, comunidad) (Ricciardi 2003).
Por lo tanto, conocida la historia de invasión de una
especie y los sitios ya invadidos, sería posible
identificar un patrón de impacto de la especie
invasora y así predecir el potencial efecto de la
invasión sobre la comunidad receptora. Sin
embargo, se debe tener en cuenta que el
comportamiento de una especie en un sistema dado
no es necesariamente el mismo que en otro sistema.
En Uruguay, hasta la fecha fueron
reportadas 12 especies acuáticas exóticas
introducidas accidentalmente (Brugnoli et al. en
prensa), incrementándose los reportes en los últimos
años. En particular, varias especies bentónicas
introducidas accidentalmente han colonizado
exitosamente
los
ecosistemas
alcanzados,
evidenciándose una rápida expansión de sus áreas
de distribución (Brugnoli et al. 2005). Entre ellas, el
poliqueto Ficopomatus engimaticus (Fauvel 1923)
fue citado por primera vez para Uruguay (y
Atlántico Sudoccidental) en 1938 en el Arroyo Las
Brujas (San José) (Monro 1938). Si bien es aceptado
que esta especie es endémica del Hemisferio Sur
(Eno et al. 1997), existe controversia respecto de su
área de origen. Se encuentra en regiones templadas,
en cuerpos de agua salobres con salinidad variable,
en zonas de escasa profundidad y baja velocidad de
corriente (Obenat 2001). Este poliqueto, considerado
exótico para nuestra región, pertenece a la familia
Serpulidae y es constructor de tubos calcáreos, los
que conforman extensas estructuras arrecifales.
Hasta la fecha, este poliqueto fue observado en
varios sistemas sobre la costa Atlántica y del Río de
la Plata (Monro 1938, Rioja 1943, Scarabino et al.
1975, Nión 1979, Muniz & Venturini 2001,
Orensanz et al. 2002). Sin embargo, el tamaño de las
estructuras arrecifales observadas en Uruguay no
parecerían ser de dimensiones tan importantes como
las encontradas en otras áreas de la región (ej.
Laguna de Mar Chiquita, Argentina; Schwindt
2001). Diversas explicaciones asociadas a
condiciones
físico-químicas
(ej.
salinidad,
temperatura, nutrientes, velocidad de corriente) o
factores ecológicos (ej. competencia, depredación,
disponibilidad de recursos) podrían explicar la no
expansión de este poliqueto en los sistemas de
Uruguay donde ya ha sido identificado. A pesar de
ello, F. enigmaticus permanece latente en estos
sitios, como especie exótica, por lo que podría
presentar una explosión poblacional. Además, las
áreas afectadas serían potenciales donadoras para la
infección de nuevos sistemas. En la región, en
particular en Argentina en la Laguna de Mar
Chiquita, la presencia de F. enigmaticus ha
Impacto potencial de invasión de Ficopomatus enigmaticus
modificado notoriamente el paisaje del área,
ocasionando problemas ecológicos (ej. modificación
de las interacciones intra e interespecíficas) y afecta
la navegación dentro de la laguna (Schwindt &
Iribarne 2000, Schwindt 2001, Schwindt et al. 2001,
Luppi et al. 2002).
Recientemente,
F.
enigmaticus
fue
observado en la zona norte de la Laguna de Rocha.
En particular, se ha registrado la presencia de tubos
calcáreos de este poliqueto, pero no se han
observado estructuras arrecifales (Clemente obs.
per.). Sin embargo, dada la similitud de
características físicas y biológicas (comunidad
bentónica) que presenta la Laguna de Rocha y la
Laguna de Mar Chiquita (Argentina) se podría
predecir el impacto esperado sobre la Laguna de
Rocha. Por tro lado, la presencia de F. enigmaticus
en la laguna representa una señal de alerta para la
conservación de la fauna de este sistema Reserva de
la Biosfera, por lo cual sería de gran relevancia la
identificación de los potenciales ecosistemas
donantes.
El objetivo del presente trabajo es evaluar
cualitativamente el riesgo de invasión y el potencial
impacto de la presencia de Ficopomatus enigmaticus
en la estructura de la comunidad bentónica en la
zona norte de la Laguna de Rocha. Esto se discute en
base a la similitud de condiciones físicas y
biológicas de la Laguna de Rocha con otros
sistemas, potenciales zonas fuentes, ya infectados
por la especie. El conocimiento del estado de
infección de este ecosistema, Reserva de la Biosfera
MaB UNESCO, contribuiría al desarrollo de un plan
de manejo con el fin de amortiguar los efectos ya
observados en otros ecosistemas.
59
nacionales (Decreto 693 de 1987) y por acuerdos
internacionales (Convención de Bonn/Ley 16062 de
1989), albergan comunidades de peces y anfibios
endémicos de la región y una importante riqueza de
flora. Estas lagunas fueron declaradas Áreas
Naturales Protegidas por decretos y leyes nacionales
(Reserva de Fauna Laguna de Castillos - Decreto
266/66 y Parque Nacional Lacustre y Área de Uso
Múltiple Lagunas de Rocha, José Ignacio y Garzón
- Decreto 260/77) y por la suscripción de Uruguay a
convenciones internacionales (sitio Ramsar desde la
Laguna Merín hasta la Laguna de Castillos - Ley
15.337 y Reserva de Biosfera desde la Laguna de
Rocha a la Merín – MaB UNESCO) (Conde et al.
2003).
Entre estas, la Laguna de Rocha (Fig. 1) se
conecta periódicamente con el mar a través de una
barra de arena y alberga una gran diversidad de
invertebrados (Giménez et al. 2006, Pintos et al.
1991), peces (Pintos et al. 1988) y aves (Pintos et al.
1988). Es un sitio clave para el ciclo de vida de
peces costeros (Pogonias chromis, Paralichtys sp.),
crustáceos como el camarón (Farfantepenaeus
paulensis) y el cangrejo azul (Callinectes sapidus).
La laguna ha sido recientemente indicado como un
importante sitio de reproducción para la corvina
blanca (Micropogonias furnieri), el segundo recurso
pesquero del país (Conde et al. 2003).
Materiales y metodos
Arroyo
Valizas
Área de estudio
La costa atlántica uruguaya presenta una
extensión de 220 km a lo largo de la cual se
distribuyen una serie de lagunas costeras. Las
lagunas situadas en esta zona son ecosistemas
salobres que se continúan hacia el norte por la costa
brasilera. Son sistemas someros, ecológicamente
complejos y muy productivos. Sus cuencas cumplen
un importante rol hidrológico, recolectando agua en
las sierras, distribuyéndola a través de un complejo
sistema de cursos de agua y humedales, recargando
acuíferos, abasteciendo de agua durante sequías,
atenuando las inundaciones durante las épocas
lluviosas y manteniendo el funcionamiento de
diversos ecosistemas (Conde & Rodríguez-Gallego
2002). Representan áreas de cría de aves acuáticas
residentes y migratorias protegidas por decretos
Bahia de
Montevideo
Laguna
de Rocha
Laguna
Garzon
Arroyo Solis
Grande
Figura 1. Costa atlántica y del Rio de la Plata de Uruguay
mostrando los potenciales sitios donadores para la Laguna de
Rocha.
Riesgo de invasión e impacto ecológico potencial
Un primer paso en la predicción de
invasiones biológicas es la identificación de
potenciales
regiones
geográficas
donadoras
(Ricciardi & Rasmussen 1998). La mayoría de las
invasiones exitosas provienen de latitudes similares
(Carlton 1985). De este modo, la invasión podrá
iniciarse a partir de áreas donde la especie es nativa
o desde sistemas ya invadidos.
La existencia de corredores de dispersión
60
entre la región donadora y el área receptora podrían
aumentar la probabilidad de futuras invasiones. En
el caso de la Laguna de Rocha, todas las áreas
potenciales donadoras se encuentran en el Río de la
Plata o el Océano Atlántico, incluida la Laguna de
Mar Chiquita. En este sentido, las fluctuaciones de
la salinidad favorecerían la colonización, ya que esta
especie está bien adaptada a la vida en aguas
salobres con salinidad variable aún en su fase
planctónica (Obenat 2001). El vector de dispersión
entre la Laguna de Rocha y los sistemas infectados
estaría asociado principalmente al tráfico de barcos
deportivos, de pesca artesanal u otras estructuras
donde F. enigmaticus podría ser transportado, o
incluso a través de aves, ya que varios de los sitios
donadores son áreas de cría y/o alimentación de aves
que se desplazan localmente entre estos ambientes.
El impacto potencial de F. enigmaticus en la
Laguna de Rocha es evaluado a través de las
similitudes que ésta presenta con la Laguna de Mar
Chiquita. En tal sentido, estos sistemas presentan
ciertas condiciones físicas y biológicas similares, lo
que permite hipotetizar comportamientos similares o
comparables en cuanto a la respuesta del sistema
frente a la invasión del poliqueto Ficopomatus
enigmaticus.
Tabla I. Algunas características abióticas de las
potenciales zonas donadoras. S: rango de salinidad;
T: rango de temperatura; Z: profundidad media.
Bahía de Montevideo
Arroyo Solís Grande 2
Laguna Garzón 3
(verano)
Arroyo Valizas 4
S (ups)
T (°C)
Z (m)
0.5 – 25
12 – 24
3*
2.6 – 32
18 – 23
(nd)
7 - 20
23 - 28
0.5
2.1 – 31.9
8 – 24.3
1.9
1
Muniz et al. 2004; 2 Muniz & Venturini 2001; 3 Conde
(promedio de dos veranos (2004-2005) datos no publicados); 4
Nion 1979. * Muniz com pers. nd (dato no disponible).
Tabla II. Composición de las comunidades
bentónicas en las potenciales zonas donadoras en
relación a los principales representantes del
macrozoobentos de la Laguna de Rocha (zona
norte). Em: Erodona mactroides; Tp: Tagelus
plebeius; Ha: Heleobia australis; Np: Nephtys
fluviatilis;
Lc:
Laeonereis
culvieri;
Hs:
Heteromastus similis; Cg: Chasmagnatus granulata;
Ca: Cyrtograpsus angulatus.
Em Tp Ha Np Lc
Bahía de
Montevideo1
Arroyo Solís
Grande2
Laguna
Garzón3
Arroyo
Valizas4
Laguna
Rocha5
Resultados y discusión
Identificación de potenciales zonas donadoras de
F. enigmaticus para la Laguna de Rocha
Carlton (1996) denomina región donadora (o
fuente) a aquellos sitios donde una especie exótica
tiene contacto con un mecanismo de transporte,
mientras que regiones receptoras son sitios en los
que la especie exótica es inicialmente liberada y
luego se establece. Por otro lado, la similitud en
condiciones físico-químicas y biológicas entre
potenciales zonas donadoras y zonas receptoras
podría incrementar aun más la probabilidad de
contagio entre ambas. En tal sentido, basado en
características físicas (Tabla I) y composición de la
comunidad bentónica (Tabla II), se identificaron
diferentes zonas potencialmente donadoras de F.
enigmaticus en la costa atlántica y Río de la Plata
para la Laguna de Rocha: Bahía de Montevideo
(zona interna), Arroyo Solís Grande y Laguna
Garzón, ubicados a 180, 105 y 30 kilómetros
respectivamente al oeste de Laguna de Rocha, y el
Arroyo Valizas, ubicado a 60 kilómetros al este de la
misma.
La Bahía de Montevideo se encuentra en la
zona fluvio-marina del Río de la Plata, donde se
ubica el frente de turbidez y salino del Río de la
1
1
*
*
*
*
*
*
*
*
*
*
*
*
Hs Cg Ca
*
*
*
*
*
*
*
2
*
*
*
*
*
*
*
*
3
Venturini et al. 2004; Muniz & Venturini 2001; Giménez et
al. 2003; 4 Nion 1978; 5 Pintos et al. 1991.
Plata (isóbata de 5 m, “Barra del Indio”) (Nagy et al.
1987). En la zona interna de la Bahía de
Montevideo, F. enigmaticus fue observada en las
tuberías de enfriamiento de la refinería de ANCAP
(Boccardi & Clemente datos no publicados) y en la
desembocadura del Arroyo Pantanoso (Scarabino et
al. 1975). Cabe destacar que la Bahía de
Montevideo, y en particular su zona interna, donde
fue encontrado F. enigmaticus, es un sitio altamente
contaminado (Muniz et al. 2004), que lo haría más
sensible al establecimiento de especies exóticas. Si
bien nunca fue cuantificado, probablemente las
estructuras arrecifales observadas de ANCAP sean
las de mayor tamaño en Uruguay (Muniz et al.
2005a).
El Arroyo Solís Grande es un sistema
conectado con la zona fluvio-marina del Río de la
Plata a través de una barra arenosa que se abre
periódicamente. Como consecuencia de ello, las
condiciones hidrodinámicas locales generan un
gradiente salino creciente hacia la desembocadura,
que junto con las características granulométricas
(sedimento
areno-fangoso)
determinan
la
composición y distribución de la comunidad
bentónica (Muniz & Venturini 2001) (Tabla II). En
el año 1995, F. enigmaticus fue encontrado a 5 km
de la desembocadura del Arroyo Solís Grande
(Muniz & Venturini 2001). En dicha zona, los
sedimentos predominantes fueron arena gruesa y
fango. Además, se observó gran abundancia de
valvas de moluscos, especialmente de Erodona
mactroides y Tagelus plebeius. Varios trabajos
señalan la importancia de la disponibilidad de estas
conchillas como sustrato para el asentamiento de F.
enigmaticus y la posterior formación de sus
estructuras arrecifales (Schwindt & Iribarne 2000,
Obenat 2001). Sin embargo, valvas de E. mactroides
y T. plebeius también fueron observadas en otras
zonas del Arroyo Solís Grande, próximas a donde
fue hallado F. enigmaticus, aunque en esa zona este
poliqueto no fue encontrado (Muniz & Venturini
2001). Contrariamente a lo observado en la Laguna
de Mar Chiquita, en el Arroyo Solís Grande la
comunidad bentónica asociada a la presencia de este
poliqueto fue sumamente pobre y poco diversa
(Muniz & Venturini 2001, Muniz et al. 2005b).
Recientemente, en 2004, F. enigmaticus fue también
observado aguas arriba a 10 km de la
desembocadura sobre canto rodado en las márgenes
del arroyo (Clemente & Borthagaray obs. per.). La
intrusión del Río de la Plata en el Arroyo Solís
Grande podría haber conducido un pulso de larvas
aguas más arriba, ampliando su rango de
distribución dentro de este sistema. En este caso, si
bien no fue cuantificada su abundancia, se
observaron las estructuras arrecifales mencionadas
por otros autores pero de tamaños menores.
En la Laguna Garzón y en la zona media del
Arroyo Valizas, sistemas someros conectados con el
Océano Atlántico a través de una barra arenosa
también de apertura periódica, fue registrada la
presencia de F. enigmaticus (Nion 1978, Orensanz et
al. 2002). En la zona media del Arroyo Valizas el
sustrato está compuesto por sedimento arenofangoso y conchillas del bivalvo E. mactroides,
mientras que la comunidad bentónica de ambos
sistemas esta formada por los mismos grupos
taxonómicos que la Laguna de Rocha (Tabla II)
(Nión 1979, Giménez et al. 2003).
En síntesis, las características físicas
compartidas por las zonas de los sistemas donadores
infectadas con F. enigmaticus son salinidad
variable, baja o moderada velocidad de corriente y
sedimentos areno-fangosos mezclado con conchillas
61
de bivalvos. Todos los sitios potencialmente
donantes se comportan como sub-estuarios (Bahía
de Montevideo y Arroyo Solís Grande) o estuarios
(Laguna Garzón y Arroyo Valizas) (Giménez et al.
2005), son sistemas poco profundos (Tabla I) y de
aguas salobres, conectados con el Río de la Plata u
el Océano Atlántico. En ninguna de las potenciales
zonas donadoras antes mencionadas se habría
registrado la presencia de importantes estructuras
arrecifales como las observadas en otros sistemas
costeros de la región (ej. Laguna de Mar Chiquita).
Sin embargo cabe destacar la disponibilidad de
valvas de Erodona mactroides y Tagelus plebeius,
sustrato adecuado para el asentamiento de las larvas
de F. enigmaticus, lo que posteriormente permitiría
el desarrollo de las estructuras arrecifales. Estas
valvas también son observadas en la Laguna de
Rocha, aunque su abundancia no ha sido hasta el
momento cuantificada. La composición taxonómica
de la comunidad bentónica indica una importante
similitud entre los diferentes sistemas fuente y la
Laguna de Rocha.
Impacto potencial de la expansión de F. enigmaticus
en la Laguna de Rocha
Dada la similitud entre las características
físicas y ecológicas que presenta la Laguna de Mar
Chiquita (37º32’S–57º19’W), Argentina, con la
Laguna de Rocha (Tabla III), se supone que la
evolución del proceso de invasión en esta laguna
podría ser comparable al ocurrido en aquella. Sin
embargo, hasta la fecha ningún estudio se ha
realizado con el fin de confrontar ambos sistemas.
En Mar Chiquita, el poliqueto invasor F.
enigmaticus fue introducido accidentalmente antes
del año 1964 (Schwindt 2001). La cobertura de
arrecifes aumentó 24 % desde 1975 a 1999. Hasta el
año 1999, estos arrecifes ocupaban 86 % de la
superficie total de la laguna, con una densidad media
de 89 arrecifes por hectárea (Schwindt 2001,
Schwindt et al. 2004a). Estas estructuras son de
forma circular de hasta 7 m de diámetro y 0.5 m de
altura. En los últimos años el incremento del tamaño
de los arrecifes ha llevado a la fusión de varios de
ellos, constituyendo extensas plataformas calcáreas
de varios metros de longitud (Obenat 2001). Las
larvas de F. enigmaticus necesitan de sitios de
asentamiento (núcleo) para comenzar la invasión del
sistema. Luego comienzan a construir los tubos
calcáreos y estos mismos sirven como estructura de
asentamiento para otras larvas, lo que en conjunto
resulta en las estructuras arrecifales (Schwindt &
Iribarne 2000, Obenat 2001).
Las variables ambientales claves en el
control de la expansión de esta especie, al menos en
62
Tabla III. Comparación de las características ecológicas de la Laguna de Rocha (zona norte) y la Laguna de
Mar Chiquita.
Laguna de Mar Chiquita1
Laguna de Rocha
12.6–21.5
13-25 *
Salinidad (ups)
0.3–35
0-30 **
Profundidad (m)
0.2-2
0.6-1 **
0.025-0.4
(nd)
0.0086-3.68
0.030–0.040 ***
7.59-8.96
7.54-8.63 *
1.52-167.32
15-30 ***
0.0034-2.94
(nd)
0.48 conchillas 100 m-2
(nd)
Temperatura (°C)
Velocidad de corriente (m s-1)
Sólidos en suspensión (g l-1)
pH
Clorofila a (mg m-3)
Concentración de detritus (g l-1) (calculado
como la diferencia de peso tras eliminación de
la materia organica por ignición)
Disponibilidad de sustrato 2
1
*
**
Schwindt et al. 2004b; Pintos et al. 1991; Conde et al. 1999;
Conde (datos no publicados) 2sustrato
natural (conchillas de Pachycymbiola brasiliana) en áreas sin arrecifes. nd (dato no disponible).
esta laguna, están asociadas a la salinidad, nutrientes
y velocidad de corriente (Schwindt et al. 2004b). De
este modo, la baja salinidad, la alta concentración de
nutrientes y la baja velocidad de corriente
favorecerían la reproducción y crecimiento de F.
enigmaticus. Otra variable que parece ser clave para
la expansión de la especie en el sistema es la
disponibilidad de núcleos para su asentamiento y
posterior formación de los arrecifes (Schwindt &
Iribarne 2000). Por otro lado, cabe destacar que F.
enigmaticus, al igual que otros poliquetos de la
familia Serpulidae, puede asentarse también sobre
sustratos artificiales como botellas, latas o restos
plásticos (Schwindt et al. 2004b). Esto tiene
importantes implicancias para el manejo de esta
especie, ya que la disponibilidad de sustratos de
origen biológico o antrópico podría asegurar el éxito
de colonización de la especie en un sistema.
Finalmente, existe poca evidencia de que
interacciones biológicas como competencia o
depredación constituyan factores importantes en el
control de esta especie (Schwindt 2001). Dos
especies que podrían ser potenciales competidores,
Balanus improvisus y Brachidontes rodriguezii, se
encuentran en densidades muy bajas. Lo mismo
sucede con el único depredador reportado para esta
especie, el pez Gobiosoma parri (Schwindt 2003).
Si bien la salinidad, velocidad de corriente y
nutrientes podrían ser los factores determinantes en
la expansión de esta especie (Schwindt et al. 2004b),
la disponibilidad de sustratos potenciaría la invasión
de F. enigmaticus al sistema. En la Laguna de Rocha
***
se desconoce la disponibilidad de sustratos
artificiales o naturales en la zona norte para el
asentamiento de F. enigmaticus. Sin embargo,
Sommaruga & Conde (1990), observaron conchillas
de Erodona mactroides en gran parte del fondo de la
laguna, lo que podría favorcer la invasión de este
poliqueto. Por otro lado, es posible que en la Laguna
de Rocha existan otros factores estructuradores que
reduzcan su invasión impidiendo la formación y el
desarrollo de los sistemas arrecifales. De todos
modos, la expansión de F. enigmaticus en este
sistema aún no ha sido observada en la magnitud
encontrada en la Laguna de Mar Chiquita.
Dada la similitud de características físicas
así como también de la comunidad bentónica de la
Laguna de Rocha y la Laguna de Mar Chiquita,
frente a una expansión de F. enigmaticus sería de
esperar cambios similares a los ocurridos en la
segunda, tanto en la comunidad bentónica como en
la hidrodinámica de la laguna. La presencia de los
arrecifes de F. enigmaticus en la Laguna de Mar
Chiquita ocasionó cambios ecológicos y físicos en el
ambiente. Desde el punto de vista ecológico, la
formación de las estructuras arrecifales aumenta la
heterogeneidad espacial, lo que genera nuevos
refugios favoreciendo así la presencia de organismos
epifaunales. Por otro lado, los arrecifes generan un
efecto en cascada sobre la infauna (poliquetos) al
controlar la densidad de otros organismos
(cangrejos). En tal sentido, Cyrtograpsus angulatus
aumenta su densidad en áreas arrecifales (mayor
cantidad de refugios), afectando negativamente, a
través de su actividad excavadora, a los poliquetos
que se encuentran en las camadas sub-superficiales
del sedimento (Schwindt et al. 2001). Las
estructuras arrecifales también afectan la
hidrodinámica de la laguna, al interrumpir el curso
natural del agua proveniente de arroyos y canales
artificiales, que debería descargarse en el mar. En
consecuencia, gran parte del sedimento queda
retenido en la laguna, favoreciendo la deposición de
material fino en el fondo, lo que podría llevar a una
colmatación del ecosistema entero produciendo la
extinción local de todas las especies (Schwindt et al.
2004a).
Conclusiones
En un primer análisis, la Laguna de Rocha
puede
considerarse
como
un
ecosistema
potencialmente receptor del poliqueto invasor F.
enigmaticus. Esta afirmación está sustentada en las
condiciones físicas (salinidad y moderada o baja
velocidad de corriente) y biológicas (comunidad
bentónica) que presenta este cuerpo de agua, las
cuales son favorables para el asentamiento de esta
especie. La disponibilidad de sustratos naturales o
artificiales para el comienzo del proceso de invasión
también sería otra variable a ser considerada. Si bien
esto último no parecería ser un factor fundamental
en el proceso de expansión de F. enigmaticus dentro
de los sistemas, hasta el momento se desconoce la
disponibilidad de sustratos para el proceso inicial de
colonización en la Laguna de Rocha. Además, varios
sitios sobre la costa atlántica y del Río de la Plata
han sido identificados como potenciales zonas
donadoras de este poliqueto.
Dado la similitud de características físicas y
biológicas (comunidad bentónica) que presentan la
Laguna de Rocha y la Laguna de Mar Chiquita se
podría predecir el impacto esperado sobre la Laguna
de Rocha. Para ello, es necesario desarrollar estudios
dirigidos a la generación de información básica para
determinar exactamente el estado de infección de
este sistema, así como su posible avance al resto de
la laguna. Esto permitiría realizar un plan de manejo
y control poblacional para este poliqueto invasor,
contribuyendo a la conservación de la biodiversidad
de la Laguna de Rocha. Los estudios permitirán
desarrollar planes de erradicación de esta especie
previos a su etapa de expansión en el ecosistema,
cuando sus costos suelen ser menores y las
posibilidades de erradicarla mayores.
Agradecimientos
Los autores agradecen a E. Schwindt y A. Carranza
por sus comentarios, los cuales permitieron mejorar
63
el presente documento, asi como también a S.
Obenat y otro revisor anonimo por sus valiosas
correciones.
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Published online August 2006
Record of a pregnant bentfin devilray, Mobula thurstoni (Lloyd)
(Elasmobranchii, Mobulidae) caught in Southwestern Brazil
ANDRÉ L. S. CASAS 1, CARLO M. CUNHA 2, WAGNER
INTELIZANO 3 & MANOEL M. B. GONZALEZ 4
1
Laboratório de Anatomia Veterinária, Instituto de Saúde, Universidade Paulista (UNIP-Campinas). Avenida
Comendador Enzo Ferrari, 280. Swift, Campinas-SP. CEP: 13043-900. E-mail: [email protected]
2
Departamento de Cirurgia da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo.
Avenida Prof. Dr. Orlando Marques de Paiva, 87, São Paulo-SP. CEP: 05508-900. E-mail: [email protected]
3
Laboratório de Anatomia Veterinária, Faculdade de Medicina Veterinária, Universidade Metropolitana de Santos.
Rua da Constituição, 374, Vila Nova, Santos - São Paulo – Brasil. CEP: 11015-904. E-mail:
[email protected]
4
Museu de Arqueologia e Etnologia, Universidade de São Paulo and Núcleo de Pesquisa e Estudo em Chondrichthyes,
Rua Ana Pimentel, 12, Ponta da Praia, Santos - São Paulo - Brasil. CEP: 11030-050. E-mail: [email protected]
Abstract. Registro de uma fêmea grávida de raia diabo, Mobula thurstoni (Lloyd) (Elasmobranchii,
Mobulidae) capturada no Sudeste do Brasil. The present paper reports the first occurrence of a 183 cm
disc width pregnant female of Mobula thurstoni (Lloyd, 1908) in southwest Brazilian coast, caught by a
commercial longline fishing vessel. Morphometrics and a morphological description of the male embryo
are presented.
Key-word: Embryo, reproduction, mobulid, batoid, trophonemata.
Resumo. O presente trabalho reporta a primeira ocorrência de uma fêmea grávida de Mobula thurstoni
(Llyod, 1908), capturada por barco de pesca de espinhel na costa sudeste do Brasil. A morfometria e a
descrição morfológica do embrião macho são apresentadas.
Palavras-clave: Embrião, reprodução, mobulídeo, batóideo, trofonemata.
The family Moubulidae Rafinesque, 1810, includes
species poorly known in many biological aspects,
such as the reproductive pattern. Devilrays, genus
Mobula, comprise nine living species, measuring
from 1 to about 4 m of disc width (DW) and
represented worldwide in warm temperate and
tropical seas (Notarbartolo-di-Scaria, 1987; Last &
Stevens, 1994). Five species of this genus were
reported in the Western Atlantic: Mobula hypostoma
(Bancroft, 1831), Figueiredo (1977); Mobula
tarapacana (Philippi, 1893), Notarbartolo-di-Scaria
& Hillyer (1989); Mobula rochebrunei (Vaillant,
1879), Mobula japanica (Müller and Henle, 1841)
and Mobula thurstoni (Lloyd, 1908), Gadig et al.
(2003). Occurrence of embryos and pregnant
females of Mobula mobular (Bonnaterre, 1788) have
been reported in the region of Palermo, Italy
(Tortonese, 1957) and in the Northern Tyrrhenian
Sea, Southeast of Gorgona Island (Notarbartolo-diScaria & Serena, 1988). Garayzar (1991) reported
the presence of embryos and gravid Mobula
munkiana Notarbartolo-di-Sciara, 1987 specimens in
Bahia de La Paz, Mexico and pregnant M hypostoma
with term embryos were reported in south and
southwestern Brazilian coast (Kotas, et al. 2005),
however no data are available for M. thurstoni
pregnancy. An adult 1830 mm DW female specimen
was accidentally caught at about 50-80 m of depth
with long line and hook and landed to the fishing
wharves on July, 2002 in Santos city, São Paulo
State, Brazil. The specimen was donated by
fishermen of the commercial longline fishing vessel
“Progressão”, (southwestern Brazil) and identified
as M. thurstoni following the identification key
Record of a pregnant bentfin devilray, Mobula thurstoni in Southwestern Brazil
proposed by Notarbartolo-di-Scaria (1987) and it
agrees with specimens previously studied in the
same area by Gadig et al. (2003). These specimens
shared the following characteristics: tail base
dorsally depressed, prominent double curvature of
anterior margin of pectoral fins, a rectangular light
gray area in the nuchal region between the origins of
pectoral fins and a white spot on the tip of the dorsal
fin. In addition, the dorsal coloration presented a
grayish color and a white triangular small area
located about midway between the origin and the
apex of the dorsal fins (fig. 3). The ventral region
presented with coloration. The material was fixed in
10% formalin solution, and deposited in the
ichthyological collection of the Núcleo de Pesquisa e
Estudo em Chondrichthyes (NUPEC) on July, 2002.
The female was 1830 mm DW (NUPEC 1868) and
the male embryo was 340 mm DW (NUPEC1867).
The morphometric protocol followed (Table I)
Notarbartolo-di-Scaria (1987) and the celomatic
cavity was incised by the linea alba to verify the
67
internal organs. The left uterus presented a dilatation
and during its dissection (Figs 1-3), an embryo was
visualized with the pectoral fins overlapping the
dorsal region (Fig.1-2). The trophonemata and its
secretion - the “uterine milk”, which nourishes the
developing embryos - were observed and
characterize the viviparity with matrotrophy (Fig. 2)
(Hamlett & Hysell, 1998; Hamlett, 2005). The male
embryo was 340 mm DW and 190 mm total length
(TL). The presence of uterine trophonemata and
uterine milk in the female uterus, the incomplete
dorsal grayish pigmentation, white marks on its
dorsal side, the small size of the animal, and the fact
that this species is expected to give birth to young at
about 850 mm DW (Notarbartolo-di-Scaria, 1987)
are evidences that the embryo was in mid-term stage
of development. The presence of adult males of M.
thurstoni, with developed claspers and pelvic fins
Table I – Female and embryo measurements of Mobula
thurstoni.
Specimen
Disc width
Disc length
Anterior projection 1
Anterior projection 2
Predorsal lenght
Dorsal fin base length
Dorsal fin height
Precloacal distance
Tail length
1st gill slit opening length
2nd gill slit opening length
3rd gill slit opening length
4th gill slit opening length
5th gill slit opening length
Between first gill slits
Between fifth gill slits
Rostrum to first gill slits
Rostrum to fifth gill slits
Pelvic fin length
Cephalic fin length
Cephalic fin width
Orbit height
Between antorbitals
Preoral length
Head length
Mouth width
Internarial distance
Upper toothband length
Lower toohband length
Measurements (mm)
Female
Embryo
1830
340
1030
190
680
144
1057
195
840
165
110
15
82
14
840
165
1200
415
100
18
105
18
108
17
99
17
62
9
220
46
95
18
197
45
385
90
217
37
221
36
71
23
30
10
240
67
75
15
232
50
215
45
195
39
195
45
163
44
Figures 1-3. Embryo of Mobula thurstoni. 1, during the uterus
dissection a fetus with the pectoral fins overlapping the dorsal
region was observed. 2, the uterine trophonemata 3, embryo
removed from uterus with incomplete dorsal pigmentation.
A. L. S. CASAS
68
congested and swollen may indicate mating activity
in southwest Brazilian coast(Gadig et al. 2003). The
occurrence of a gravid female in the same region
corroborates the assumption that the Brazilian
southwestern coast is an important reproductive site
for the species.
Acknowledgements
The authors wish to thank Giuseppe Notarbartolo-diSciara for the references provided.
References
Figueiredo, J. L. 1977. Manual de Peixes
Marinhos do Sudeste do Brasil, Parte 1.
Introdução. Cações, raias e quimeras.
Museu de Zoologia, Universidade de São
Paulo, São Paulo, 104 p.
Gadig, O.B.F., Namora, R.C. & Motta, F.S. 2003.
Occurrence of the bentfin devil ray, Mobula
thurstoni (Chondrichthyes: Mobulidae), in the
western Atlantic. Journal of the Marine
Biological Association of the United
Kingdon, 83:869-870.
Garayzar, C.J.V. 1991. Observations on Mobula
munkiana (Chondrichthyes: Mobulidae) in the
Bahia de La Paz, B.C.S. Mexico. Revista de
Investigação Científica de la Universidad
Autonoma de Baja California Sur, 2 (2):
78-81.
Hamlett, W. C. & Hysell, M. 1998. Uterine
specialization in Elasmobranches. Journal of
Experimental Zoology, 282: 438-459.
Hamlett, W.C. 2005. Reproductive biology and
phylogeny of Chondrichthyes: sharks,
Enfield, 562 p.
Kotas, J. E., Petrere, M. J., Azevedo, V. G., Santos
S. 2005. A pesca de emalhe e de espinhel de
superfície na Região Sudeste-Sul do Brasil.
Instituto Oceanográfico da USP, São Paulo,
72p.
Last, P.R. & Stevens, J.D. 1994. Sharks and rays of
Australia. CSIRO Austrália. 513p.
Notarbartolo-di-sciara, G., 1987. A revisionary
study of genus Mobula Rafinesque, 1810
(Chondrichthyes: mobulidae) with the
description of a new species). Zoological
Journal of the Linnean Society, 91:1-91.
Notarbartolo di Sciara G. & Serena F., 1988. Term
embryo of Mobula mobular Bonnaterre,
1788) from the Northern Tyrrhenian Sea. Atti
della Società Italiana di Scienze Naturali e
del Museo Cívico di Storia Naturale di
Milano, 129:396-400.
Notarbartolo di Sciara G. & Hillyer E.V., 1989.
Mobulid rays off Eastern Venezuela. Copeia,
(3): 607-614.
Tortonese E., 1957. Studi sui Plagiostomi. XI.
Descrizione di un embrione di Mobula
mobular. Bolletino di Zoologia, 24 (2): 4547.
Received May 2006
Accepted July 2006
Published online August 2006
Intestinal bacterial diversity in live rock lobster Panulirus homarus
(Linnaeus) (Decapoda, Pleocyemata, Palinuridae) during
transportation process
GRASIAN IMMANUEL1, 2, PALANISAMY IYAPPA RAJ1, PALANICHAMY ESAKKI RAJ1
& ARUNACHALAM PALAVESAM1
1
Marine Biotechnology Division, Centre for Marine Science and Technology, M. S. University, Rajakkamangalam629 502, Tamilnadu, India.
2
Corresponding author: Ph.: +91-4652-253078; E-mail: g [email protected]
Abstract. This study investigates the bacterial diversity in the intestine of rock lobster Panulirus
homarus during live transportation process lasting for 14h. The total viable count (TVC) in the intestine
of P. homarus (Linnaeus, 1758) prior to packing (control) was 130.33 x 106 cfu ml-1. In the intestine of
packed lobsters (experimental), the TVC showed an increasing trend and the recorded values were
between 139.0 and 150.0 x 106 cfu ml-1 respectively during 2nd and 14th h. The bacterial species
composition and their percentage occurrence were also varied much between control and experimental
samples (p < 0.05), but the variation in species composition between the incubation period was
statistically non significant (P>0.05). Among the species identified, Pseudomonas aeruginosa (Schroeter,
1872) and Vibrio parahaemolyticus (Fujino et al., 1951) were predominantly seen and seven other less
dominant species were also identified.
Key words: intestine, species composition, time intervals, TVC.
Resumo. Diversidade bacteriana intestinal em vida da Lagosta-das-rochas Panulirus homarus
(Linnaeus, 1758) (Decapoda, Pleocyemata, Palinuridae) durante processo de transporte. Este estudo
investigou a diversidade bacteriana em intestino da Lagosta-das-rochas Panulirus homarus (Linnaeus,
1758) durante o processo de transporte em vida passadas 14 horas. A contagem do total viável de
bactérias (CVT) nos intestinos de P. homarus antes do transporte (grupo controle) foi 130,33 x 106 cfu
ml-1. Nos intestinos de lagostas transportadas (grupo testado), a CVT mostrou uma tendência de aumento
e os valores registrados ficaram entre 139,0 e 150,0 x 106 cfu ml-1 passados 2 e 14 horas,
respectivamente. A composição de espécies de bactérias e suas percentagens de ocorrência também
variaram bastante entre os grupos testados e controle apresentando médias significativamente diferentes
(p < 0,05). Entre as espécies identificadas, Pseudomonas aeruginosa (Schroeter, 1872) e Vibrio
parahaemolyticus (Fujino et al., 1951) foram predominantemente observadas. Outras sete espécies menos
dominantes foram também identificadas.
Palavras Chave: intestino, composição de espécies, intervalos de tempo, CVT.
Introduction
Microbial biomass in aquatic habitat plays
an important role, besides being a subject of delicate
balance between the host and environment
relationship. When such balance is disturbed, it
could result in disease out break, which may affect
adversely the host. In general, pathogenic microbes
usually are anaerobic forms harbored within the
intestinal tract of all animal species, along with a
complex microbial community, known as intestinal
micro flora (Tannock, 1995 & 1997).
In the aquatic environment, the host
intestine access begins with pathogens colonize
multiplication in the gills and its dissemination,
affecting in both beneficial and harmful ways
depending on the prevailing conditions. Separate
G. IMMANUEL ET AL
70
subject about fish from the previous affirmation,
e.g., in fishes, it has been demonstrated that, obligate
anaerobic bacteria are disseminated in the intestinal
tract of many fish species such as grass carp
(Ctenopharingodon idella (Valenciennes, 1844)) and
gold fish (Carassius auratus (Linnaeus, 1758))
(Trust et al., 1979).
Intestinal microflora of penaeid shrimp
species was also studied. The gastrointestinal flora
of fresh water shrimp Palaemon paucidens de Haan,
1844 adapted to seawater was reported (Sujita et al.,
1986a). Farfantepenaeus aztecus (Ives, 1891) from
sea grass meadows of Red Fish Bay near Port
Aransas, Texas, harbors nine bacterial genera
including Flavobacterium, Cytophaga, Alcaligenes,
Pseudomonas,
Xanthamonas,
Alteromonas,
Aeromonas, Vibrio and also Chromobacterium and
Photobacterium (Kitting et al. 1984; Dempsey &
Kitting 1987).
In crustaceans, the intestinal microbial
colonization has great importance in healthy
condition and better growth performance. Oxley et
al. (2002) reported that wild and cultured prawns
(eg. Fenneropenaeus merguiensis (De Man, 1888))
harbor a diverse bacterial flora, which includes the
dominant genera like Aeromonas, Plesiomonas,
Photobacterium, Pseudoalteromonas, Pseudomonas
and Vibrio. The similarity existing in the intestine
bacterial flora of cultured prawns suggests the host
specificity of intestinal microbial colonization. An
understanding of the host intestinal bacterial floral
interactions is of much significance for the
development of a healthy cultivation environment
and also to optimize the potential species growth.
Despite of those reports, there are still lacks
of similar information from other crustacean species.
However, in recent years there has been a growing
interest on the endogenous intestinal micro flora of
commercially important finfish and shellfish species
as a tool for helping fish diseases and pathological
interpretation studies about. Information on the
micro flora of aquatic organisms is especially
available for the lobster Panulirus japonicus (Von
Siebold, 1824) (Sujita et al. 1986 b, 1987). Although
much literature on transportation of live lobsters is
available (Solomon & Hawkins, 1981; Mc Larney,
1984; Homma, 1990; Sujita & Deguchi, 1990), the
changes in the qualitative and quantitative
composition of the intestinal microflora of live
lobsters during transportation process are poorly
known. The present study was carried out to
investigate the changes in intestinal bacterial flora of
lobster Panulirus homarus (Figure 1) during live
transportation process.
Live lobsters were obtained from a local
fish-landing centre at Chinnamuttam, Kanyakumari,
South India and brought to the laboratory
and acclimatized at 28 ± 10C temperature
and a salinity of 35‰ for five days.
During acclimatization period, the lobsters were fed
with mussels (Perna sp. Philipsson, 1788).
Afterwards, lobsters were selected considering
healthy, activity and weight range uniformly
(130 ± 8.0g) for the live transportation assay based
on morphological and behavioral adaptation. The
selected ones have been starved for 12 h before the
experiment starting the procedures.
For the present study, the temperature of the
lobster holding container (1 tone capacity) was
brought down to 12–150C from the initial
temperature of 27± 10C at the rate of 30C per hour
achieving by using bags filled with ice cubes. The
mouth bags were sealing to avoid the melted ice
released into the container. Three to five ice bags
were placed on the surface of water in the container
and were continuously aerated to maintain a uniform
temperature.
Figure 1. Specimen of P. homarus on laboratorial conditions.
Simultaneously, sterilized dry sawdust,
straw and pieces of gunny sacks were aseptically
pre-cooled in a freezer (-200C) along with 0.5 l
capacity plastic bottles filled with water. Seven
thermo cool boxes (40 × 30 × 15 cm) were prepared
with two cooled layers settled on the bottom first
saw dust and the second one straw. Besides, two
frozen ice bottles wrapped with filter paper were
placed at the sides of the box. Then the lobsters were
placed on the straw (10 lobsters each/box) by gently
folding the antennae and abdomen to bring them
close to their body in order to uniformly
accommodate. Finally the lobsters were covered
with a piece of pre-cooled gunny sack and then the
box was closed with lid and sealed with adhesive
tape.
obtained were statistically transformed and analyzed
by one-way ANOVA test. Significant differences
between means (p<0.05) of the TVC due to
incubation time were not detected.
16
Cumulative bacterial load (%)
The intestine was sampled in the beginning
from unpacked lobsters (control) and then, each two
hours; three lobsters were collected from different
boxes, till number seven totaling 14 hours for
bioassay. The lobster intestine was collected
aseptically by cutting the cuticle. The collected
intestinal samples were stored in a refrigerator in
pre-labeled containers for further bacterial
enumeration.
All samples were analyzed about Total
Viable Count (TVC), bacteria diversity and number
using spread plate method and identified according
to Holt et al. (1994). The results were submitted to
parametric statistical tests, using Standard Deviation
(SD) and Analysis of Variance (ANOVA).
If necessary, the data were transformed
(log transformation) as described by Zar (1974).
71
14
12
10
8
6
4
2
0
0
2
4
6
8
10
12
14
Tim e interval (h)
Results and Discussion
Figure 2. Cumulative increasing percentage of TVC in different
hours.
Aquatic organisms often harbor a great
number of bacteria into their intestinal tract, gills
and body surface, which they acquired from water,
sediment and /or food. However, most of these
bacteria are temporary residents, due to (i)
incompatible physical and chemical conditions, (ii)
lethal interaction with resident bacteria and/or (iii)
long term immune response of the host. Qualitative
and quantitative information concerning the micro
flora of aquatic vertebrates including fish and of
crustaceans has been provided by Sujita et al.
(1987); Sujita & Deguchi (1988) and Cahill (1990).
The bacterial load associated with the gill
and intestine of freshly caught Japanese spiny
lobster P. japonicus ranged between 3.2 ×106 to 1.2
× 107 cfu.g-1 (colony forming unit per g tissue) and
9.5 × 107 to 1.3 × 109 cfu.g-1 respectively (Sujita et
al. 1986b, Sujita et al., 1987). The total viable count
(TVC - cfu.ml-1) of both control (unpacked) and
experimental (packed) lobsters at different time
intervals (2nd–14th h) after packing are given in Table
I. The data on TVC was relatively more in the
intestinal samples collected from lobsters during
experimentation process, when compared the value
recorded in the intestinal samples collected from the
unpacked (control) lobsters. The maximum TVC
value of 150.0 ± 2.51 × 106 cfu.ml-1 was noticed
against the minimum value of 130.33 ± 2.51 × 106
cfu.ml-1 in control samples. The cumulative increase
in TVC of 14 h experimental sample was maximum
(15.09%) and it was minimum (6.23%) in 2h
experimental sample (Fig. 2). The percentage
increase in TVC within the experimental samples
during 2 to 14 h was not differed much and it
fluctuated between 0.89 to 2.08%. The TVC data
The bacteria qualitative and quantitative data
from all samples are presented in Table II. In the
control lobsters, 42 suspected isolates were taken
from the intestinal samples. Among these, ten
bacterial species were identified and one
unidentified species was also recorded. Within these,
Pseudomonas aeruginosa (Schroeter, 1872) strain
was dominated with 21.42% occurrence. The next
dominant species was Vibrio parahaemolyticus
(Fujino et al., 1951) (14.28%) and the least
percentage occurrence was Alcaligenes sp.
Castellani & Chalmers, 1919 (2.38%).
In experimental lobsters, the number of
suspected isolates examined was 41, 39, 44, 48, 44,
40 and 47 respectively during 2nd to 14th h of
experimentation. Among these P. aeruginosa, V.
parahaemolyticus, Bacillus circulans Jordan, 1890
and Escherichia coli (Migula, 1895) were recorded
in high numbers and the percentage occurrence
ranged from 10.25 – 20.0% at different time
intervals. Species like Photobacterium damselae
(Love et al., 1982) (6.25–10.25%), Flavobacterium
columnare (Bernardet & Grimont, 1989) (5.00 –
9.09%), Micrococcus luteus (Schroeter, 1872) (5.0 –
10.25%), Enterobacter aerogenes Hormaeche &
Edwards, 1960 (2.56 – 5.00%), Corynebacterium
xerosis (Lehmann & Neumann, 1896) (0 – 4.87%)
and Alcaligens (2.08 – 2.56%) were also recorded.
Two-way ANOVA test indicated that the variation
in bacterial species within the experimental duration
was not statistically significant (p > 0.05).
Sujita et al. (1986b, 1987) reported that, Vibrio and
Pseudomonas spp were dominant in the gut and
gill of Scomber japonicus Houttuyn, 1782.
G. IMMANUEL ET AL
72
Table I. Total Viable Count (TVC - cfu ml-1) of bacterial strains in the intestinal samples of live rock lobster
P. homarus at different time intervals during transportation process.
Time
T V C (cfu ml-1) in the Increasing of TVC in different Cumulative increasing of TVC
intestinal samples
hours (%)
in different hours (%)
interval (h)
0 (Control)
130.33 ± 2.51 x 10 6
2
139.00 ± 1.00 x 10 6
4
140.33 ± 0.57 x 10 6
6
142.33 ± 0.57 x 10 6
8
144.00 ± 1.00 x 10 6
10
145.33 ± 0.57 x 10 6
12
147.66 ± 0.57 x 10 6
14
150.00 ± 2.00 x 10 6
Each value is a mean of three replicates (± SD)
--6.23
0.89
2.08
1.28
1.02
1.79
1.80
--6.23
7.12
9.20
10.48
11.50
13.29
15.09
TVC was statistically non significant (P>0.05)
Table II. Species composition of micro flora (%) isolated from intestinal samples of live
(P. homarus) at different time intervals (0-14h) during transportation process.
Intestinal samples at different time intervals (h)
Bacterial species
0 (C)
2
4
6
8
10
12
9
8
8
7
8
7
7
P. aeruginosa
(21.42)
(19.50) (20.51) (15.90) (16.66) (15.90) (17.5)
6
6
5
7
7
6
6
V. parahaemolyticus
(14.28)
(14.63) (12.82) (15.90) (14.58) (13.63) (15.0)
5
5
6
6
7
8
8
B. circulans
(11.90)
(12.19) (15.38) (13.63) (14.58) (18.18) (20.0)
5
5
4
7
8
7
7
E .coli
(11.90)
(12.19) (10.25) (15.90) (16.66) (15.90) (17.5)
4
4
4
3
3
4
3
P. damselae
(9.52)
(9.75)
(10.25) (6.81)
(6.25)
(9.09)
(7.50)
4
3
3
4
4
3
2
F. columnare
(9.52)
(7.31)
(7.69)
(9.09)
(8.33)
(6.81)
(5.00)
3
3
4
3
4
3
2
M. luteus
(7.14)
(7.31)
(10.25) (6.81)
(8.33)
(6.81)
(5.00)
2
2
1
2
2
2
2
E. aerogens
(4.76)
(4.87)
(2.56)
(4.54)
(4.16)
(4.54)
(5.00)
2
2
1
2
2
1
1
C. xerosis
(4.76)
(4.87)
(2.56)
(4.54)
(4.16)
(2.27)
(2.50)
1
1
1
1
1
1
1
Alcaligenes
(2.38)
(2.43)
(2.56)
(2.27)
(2.08)
(2.27)
(2.50)
1
2
2
2
2
2
1
Unidentified
(2.38)
(4.87)
(5.12)
(4.54)
(4.16)
(4.54)
(2.50)
Total isolates
42
41
39
44
48
44
40
lobsters
14
8
(17.02)
8
(17.02)
7
(14.89)
7
(14.89)
4
(8.50)
4
(8.50)
4
(8.50)
2
(4.25)
--1
(2.12)
2
(4.25)
47
Values in parenthesis denotes percentage of species composition Statistically significant (P<0.05) between the organisms
Statistically non significant (P > 0.05) between the experimental duration
Elston (1989) reported that, out of 518 strains of
Vibrio isolated from the spiny lobster, 69 strains
were identified as Vibrio alginolyticus (Miyamoto et
al., 1961), a causative agent of crustacean vibriosis.
This result suggested the prevalence of pathogenic
bacterial colonies even in the gills and gut of healthy
spiny lobsters which may cause opportunistic
infectious diseases under stress conditions.
In the present study, P. aeruginosa was
recorded as the dominant species, followed by
V. haemolyticus, B. circulans, E. coli, P. damselae,
F. columnare and M. luteus. It was observed Vibrio
sp. was present in 14.28% of the control lobster. In
experimental lobsters packed for live transportation,
the raise in TVC was 17% over the control value
during 10 – 14h. This clearly indicates the processes
of bacterial proliferation during the live
transportation.
Even during processes of live lobster
transportation by using suitable container maintained
at low temperature, the microbes colonized in gill,
mucus and also in intestine may proliferate and
accounts for the increase in bacterial load. This may
be the reason for no significant (P>0.05; One-way
ANOVA) increase of TVC value recorded during
the later hours (10 – 14 h) of experimentation
process in the present study.
This strongly suggests that healthy spiny
lobsters should be starved for 1-2 days before the
transportation so as to minimize the nutrient
availability in the gut for rapid proliferation of
bacterial species. Additionally, the temperature
inside the package should be kept to a minimum
level to reduce the rate of bacterial proliferation and
also to enhance the survival to a maximum extent of
> 80%. Besides these procedures, it is recommended
the use of sterilized seawater and packaging
materials to avoid added microbial contamination
through the process of packing (Sujita & Deguichi,
1990). In the present study care was taken to
sterilize and hence added bacterial proliferation was
avoided. The adoption of discussed precautious
measures, it might reduce the bacterial proliferation
during live lobster transportation process and
prevent the spoilage by indirect mean.
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Dempsey, A .C. & Kitting, C. L. 1987.
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Elston, R. 1989. Bacteriological methods for
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& Austin, D.A. (Eds.). Methods for
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(Ed.). Aquarium systems, Academic Press,
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digestive tract of fresh water shrimp
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water. Nippon Suisan Gakkaishi, 42: 211 –
215.
Sujita, H., Veda, R. & Deguchi, Y. 1986b. An
anaerobic bacterium isolated from Japanese
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reference to tetrodoxin producing bacteria. p.
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advances in Tetrodotoxin research,
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Received June 2006
Accepted August 2006
Published online September 2006
Morphological aspects and seasonal changes of some planktonic
ciliates (Protozoa) from a temporary pond in
Buenos Aires Province, Argentina
GABRIELA C. KÜPPERS 1, ESTELA C. LOPRETTO 1 & MARÍA C. CLAPS 2
1
Cátedra Zoología Invertebrados I, Facultad de Ciencias Naturales y Museo (UNLP), Museo de La Plata, Paseo del
Bosque s/n, 1900 La Plata, Argentina. E-mail: [email protected]; [email protected]
2
Instituto de Limnología 'Dr. R. A. Ringuelet' (CONICET-UNLP), Avenida Calchaquí km 23.5, 1888 Florencio
Varela, Argentina. E-mail: [email protected].
Abstract. The morphology of some planktonic ciliates in a temporary freshwater pond located in Buenos
Aires province, Argentina, is compared and the seasonal variation in their abundances over an annual
cycle is described. Samples were taken from June 2004 to June 2005. Physical and chemical
characteristics of the environment were also recorded. Taxonomic identifications were made in vivo and
after employing the Protargol technique. Five planktonic species were recorded for the first time in South
America.
Key words: Ciliophora, plankton, freshwater pond, morphology, abundances variation.
Resumo. Aspectos morfológicos e mudanças sazonais de alguns ciliados (Protozoa, Ciliophora)
planctônicos de uma poça temporária na província de Buenos Aires, Argentina. Dados morfológicos
de alguns ciliados planctônicos, coletados de uma poça temporária de água doce localizada na província
de Buenos Aires, Argentina, são comparados, assim como também foram descritas as variações sazonais
da densidade ao longo do ciclo anual. Amostras foram obtidas desde junho de 2004 até junho de 2005 em
três locais de coleta. Características físicas e químicas do ambiente foram registradas. As identificações
taxonômicas foram feitas in vivo e depois da utilização da técnica de Protargol. Cinco espécies
planctônicas foram registradas pela primeira vez América do Sul.
Palavras Chave: Ciliophora, plâncton, poça de água doce, morfologia, variação das abundâncias.
Introduction
Taxonomic studies of freshwater ciliates have
been scarcely conducted in Argentina, despite of
their ubiquity in planktonic communities and
their important role as carbon recyclers.
Although ciliates taxonomy has been already
investigated employing silver staining methods and
electron microscopy in other countries, mainly in
Europe, in South America the contribution to
this field is from Paiva & da Silva-Neto
(2003, 2004a, b, c, 2005) in Brazil and
Pettigrosso et al. (1997), Pettigrosso (2001, 2003),
Barría (2002), and Pettigrosso & Barría (2004)
in Argentina. In this country, other researchers
have studied the ciliate fauna of several
temporary ponds in Buenos Aires province
by live observation (Cela 1972, Vucetich 1972,
Vucetich & Escalante 1979, Modenutti &
Claps 1986). At global scale, ciliates in temporary
waters are poorly known (Andrushchyshyn et al.
2003). These habitats, which are frequent in
Buenos Aires province during humid periods, are
populated
by
organisms
with
particular
physiological and behavioral properties and function
as microcosms to study their ecology (Williams
2001).
The aims of this work are to compare
morphological aspects of planktonic ciliate species
from a temporary pond (Buenos Aires province,
Argentina)
with
earlier
descriptions
of
corresponding species from other continents. We
also analyze the variability in the abundance of those
species along a year cycle and their relationship with
physical and chemical changes.
Morphological aspects and seasonal changes of planktonic ciliates
The study was carried out in a freshwater
temporary pond located near the city of La Plata in
Buenos Aires province, Argentina (35° 05’ S, 57°
48’ W) (Fig. 1) that goes through drought
periods, mainly in summer and the beginning of
autumn. During rainy periods, the pond has an
approximate length of 30 m and about
1 m maximum depth. It is located beneath a
cattle field, bounded by Eucalyptus spp. (Myrtaceae)
and the Route 36. The water supply comes
mainly
from
rainfall.
Following
the
summer drought, the macrophytes Alternanthera
philoxeroides (Amaranthaceae) and Ludwigia
peploides (Onagraceae) persist in the pond for a
short period of time and after their decomposition,
the planktonic community dominates the water
body. Samples were taken monthly during the
morning at three sampling stations, with 5 liter
bottles from June 2004 to June 2005, except in
October 2004, summer 2005, and May 2005,
when the pond was dry. Two replicates were
collected at the same time and at each sampling
site, from which two 250 ml sub-samples were
fixed using acid Lugol 2% and other live subsamples were cultured in wheat infusions.
Temperature, pH, and conductivity were recorded
with a multiparameter sensor (®Horiba U21).
Dissolved oxygen was estimated by the
Winkler method (Clesceri et al. 1998). Observations
and measurements were performed in vivo and after
revealing
the
argentophilic
structures
by
the Protargol technique (Wilbert 1975), at
magnifications of 100, 400 and 1000×. Previous to
the silver staining, the ciliates were fixed with
Bouin’s solution. The drawings of impregnated cells
were performed by using a tracing device and the
micrographs were taken with a Leica Wild MPS52.
Cells were counted using an inverted microscope
in 10 ml chambers (Utermöhl 1958), examining the
entire chamber at a magnification of 150×. The
classification proposed by Lynn & Small (2000) was
followed.
Abbreviations used in morphometric tables
are as follow: X, arithmetic mean; Min, minimum
observation; Max, maximum observation; M,
median; SD, standard deviation; N, number of
observations.
Results
Observations on the species
The morphology and infraciliature of
ten planktonic ciliates belonging to the orders
Haptorida (one species), Cyclotrichida (two species),
75
Prostomatida
(one
species),
Choreotrichida
(one species), Halteriida (one species), Strombidiida
(three species), and Stichotrichida (one species)
were considered. Five species were recorded
for the first time in South America, another one in
Argentina, and additionally one in Buenos Aires
province.
Morphology
and
infraciliature
of Askenasia volvox, Coleps hirtus hirtus, and
Halteria grandinella, which were previously
studied in vivo and by supravital staining, were
also considered. Abundances of Teuthophrys
trisulca africana, Rhabdoaskenasia minima,
and Hypotrichidium conicum were not estimated
from field samples as these species were cultured in
the laboratory.
Order Haptorida Corliss
Teuthophrys trisulca africana (Dragesco &
Dragesco-Kernéis) Foissner,
Berger & Schaumburg
(Table I; Figs. 2a and 3a)
Sack-like body shape with three anterior,
spirally curved oral arms. Posterior contractile
vacuole. Macronucleus vermiform and coiled.
Cytoplasm colorless and without endosymbiotic
algae. Oral arms lined by trychocysts. Somatic
ciliature uniform. With rod-shaped somatic
extrusomes (2.8-8 μm long) and dark granules over
the body.
This species was recorded in autumn, when
Alternanthera philoxeroides occurred, and in
cultures of mud samples taken in October 2004,
where the resting cysts developed.
Order Cyclotrichida Jankowski
Askenasia volvox (Eichwald) Kahl
(Table II; Figs. 2b and 3b, c)
Body ovoid to pyriform, widened
posteriorly.
Without
endosymbiotic
algae.
Contractile vacuole sub-equatorial and with
another posterior floating vacuole. Macronucleus
globular to ellipsoidal, sometimes constricted.
Micronucleus indented in the macronucleus.
Somatic kineties arranged in a pre-equatorial
girdle, each row of them with single kinetosomes
with 7 groups of flame like cilia that extend
anteriorly; an equatorial girdle with paired
kinetosomes with posteriorly directed cilia; a subequatorial girdle with flexible bristles, each row with
3 kinetosomes. Oral region surrounded by a
circumoral wreath of granules. Extrusomes were
faintly impregnated.
G. C. KÜPPERS ET AL.
76
Figure 1. Location of the sampling site in Buenos Aires province, Argentina. a. Aerial view. b, c. The pond during a rainy period (b)
and a dry phase (c).
This species occurred in the pond from late
autumn to winter and early spring. It was not
recorded at temperatures over 11 °C. The highest
densities occurred at the lowest conductivity values,
alkaline pH, and over 70 % of dissolved oxygen
saturation (Fig. 4). Cyclidium glaucoma Müller and
Halteria grandinella (Müller) Dujardin were
observed inside the food vacuoles of A. volvox in
Protargol stained preparations.
Rhabdoaskenasia minima Krainer & Foissner
(Table III; Fig. 2c)
Body pyriform, with rounded posterior end.
With a single contractile vacuole. Macronucleus
reniform. Oral dome surrounded by a circumoral
row of dikinetids that give rise to the rhabdos.
Somatic kineties, arranged in a pre-equatorial kinety
girdle with single kinetosomes in each row; an
equatorial girdle also with single kinetosomes; a
sub-equatorial girdle of bristles, with 2 kinetosomes
in each row.
This species occurred in late autumn.
Order Prostomatida Schewiakoff
Coleps hirtus hirtus (Müller)
Foissner, Berger & Schaumburg
(Table IV; Fig. 2d)
Body barrel-shaped. In vivo with pretzel-like
cortical windows and three posterior cortical
spines. Symbiotic algae are absent. Somatic
kineties composed by dikinetids. With single
caudal cilium. Dorsal brush in three groups with
two longitudinal rows of basal bodies each.
First group with four basal bodies in each row
and the other groups with three basal bodies in
each row. External pectinelles with two basal
bodies and internal pectinelles with four basal
bodies.
Coleps hirtus hirtus was only absent in
autumn. The maximum abundance of this species
was observed under the highest temperatures,
intermediate conductivity values (183 µS cm-1), low
dissolved oxygen saturation (49 %) and slightly
acid pH (Fig. 4).
77
Table I. Morphometric data on Teutophrys trisulca africana.
in vivo
Body, length
Body, width
X
261.3
126
Min
238
112
Max
280
140
M
266
126
SD
21.4
14
N
3
3
After Protargol
Body, length
Body, width
X
207.2
98
Min
168
84
Max
252
112
M
210
98
SD
22.7
8.4
N
10
8
Oral arms, length
128.7
112
154
126
10.1
13
Oral extrusomes, length
5.9
5
7
5.6
0.7
13
Somatic extrusomes, length
Somatic extrusomes, width
5.9
0.7
2.8
0.7
8
0.7
6
0.7
1.6
0
13
13
Pigmented granules, width
1.8
0.7
2.8
2.1
0.8
13
Table II. Morphometric data on Askenasia volvox.
in vivo
Body, length
Body, width
X
46.7
38.5
Min
35
35
Max
63
42
M
45.5
38.5
SD
9.5
3.8
N
6
6
Groups of anterior cilia,
number
7
7
7
7
0
3
After Protargol
Body, length
Body, width
X
51.8
46.5
Min
49
42
Max
63
56
M
49
49
SD
4.2
4.7
N
20
20
Somatic kineties, number
Kinetosomes in preequatorial girdle, number
Paired kinetosomes in
equatorial girdle, number
Kinetosomes in subequatorial girdle, number
49.9
46
53
50.5
2.7
20
11
8
14
10
1.9
20
9.5
9
10
9.5
0.7
2
3
3
3
3
0
20
Kinetosomes per circumoral
lobe, number
4.5
3
5
5
0.6
20
Macronucleus, length
Macronucleus, width
18
15.1
11.2
10
25.2
26.6
19.3
14.7
4.4
5.2
10
10
Micronucleus, diameter
3.1
2.8
3.5
2.8
0.4
5
Order Choreotrichida Small & Lynn
Strobilidium caudatum (Fromentel) Foissner
(Table V; Figs. 2e and 3d, e)
Body pyriform, posteriorly pointed and
truncated. Horse shoe-shaped macronucleus.
Contractile vacuole at the posterior end of the body.
Five somatic kineties, three of them form a caudal
spiral and the other two are shorter. Oral apparatus
composed by a closed ring of external
membranelles, some of which enlarge into the oral
cavity, one internal membranelle, and the endoral
kinety. Some specimens had irregularly spaced
extrusomes and pigmented granules in the posterior
half of the body.
78
Table III. Morphometric data on Rhabdoaskenasia minima.
After Protargol
Body, length
Body, width
X
52.5
45.5
Min
42
42
Max
63
49
M
52.5
45.5
SD
14.8
4.9
N
2
2
Kinetosomes in pre-equatorial
girdle, number
Kinetosomes in sub-equatorial
girdle, number
77.5
75
80
77.5
3.5
2
8.5
8
9
8.5
0.6
4
2
2
2
2
0
4
32
32
32
32
0
1
29.4
29.4
29.4
29.4
0
1
Circumoral paired granules,
number
Macronucleus, maximum
length
Table IV. Morphometric data on Coleps hirtus hirtus.
in vivo
Body, length
Body, width
X
Min
Max
M
SD
N
61.5
24.6
61.5
24.6
61.5
24.6
61.5
24.6
0
0
1
1
After Protargol
Body, length
Body, width
X
40
17.9
Min
35
11.2
Max
49
28
M
38.8
17.8
SD
4.9
4.2
N
12
12
Cytopharynx, length
11.4
8.4
14.7
11.2
2.1
7
13
11
15
13
1.2
7
13
12
14
13
0.5
8
10
10
10
10
0
2
2
2
2
2
0
3
10
10
10
10
0
2
4.4
4
5
4
0.5
5
3
3
3
3
0
3
4
4
4
4
0
2
3
3
3
3
0
2
3
3
3
3
0
2
Macronucleus, width
10.1
11.2
7
6.3
16.8
17.5
9.1
10.5
2.8
3.1
10
10
1.4
1.4
1.4
1.4
0
2
Paired kinetosomes per
somatic kinety, number
External pectinelles, number
Kinetosomes per external
pectinelle, number
Internal pectinelles, number
Kinetosomes per internal
pectinelle, number
Paired kineties in dorsal brush,
number
Paired kinetosomes in dorsal
brush kinety 1, number
79
Figure 2. Morphology of the species recorded, composite from protargol impregnation and live observation (a, b, j) and protargol
impregnation only (c-i). a. Teuthophrys trisulca africana. b. Askenasia volvox. c. Rhabdoaskenasia minima, circumoral wreath of
granules (left arrowhead), two sub-equatorial kinetosomes (right arrowhead). d. Coleps hirtus hirtus, cytopharynx (C), dorsal brush
(DB), external pectinelles (EP), internal pectinelles (IP). e. Strobilidium caudatum, ventral view. f. Halteria grandinella, equatorial
somatic kinety (arrowhead). g. Limnostrombidium pelagicum, ventral view. h. Limnostrombidium viride, ventral view, symbiont (S).
i. Pelagostrombidium mirabile, ventral view. j. Hypotrichidium conicum, ventral view, contractile vacuole (arrowhead). (a) scale bar
= 50 µm; (b-f, i) scale bar = 10 µm; (g, h, j) scale bar = 20 µm.
Strobilidium caudatum was only absent in
late winter and late spring. This non
euplanktonic species reached the maximum
densities in coincidence with high conductivity,
low temperatures, and intermediate dissolved
oxygen concentrations. This ciliate was recorded
under acid as well as alkaline pH values (Fig. 4). It
was also observed adhered to artificial substrates. It
could be maintained in wheat cultures for a short
time.
80
Figure 3. Morphology of the species recorded, after protargol impregnation. a. Teuthophrys trisulca africana, aboral view.
b. Askenasia volvox. c. A. volvox, circumoral wreath of granules (left arrowhead) and three subequatorial kinetosomes (right
arrowhead). d. Strobilidium caudatum, dorsal view, extrusomes (arrowhead). e. S. caudatum, oral view, caudal spiral (arrowhead).
f. Limnostrombidium pelagicum, ventral view, ventral kinety (arrowhead). g. L. pelagicum, oral view. h. L. viride, symbionts near
the oral region (arrowhead). i. L. viride, ventro-posterior view, clavate cilia in equatorial girdle (left arrowhead) and neoformation
organelle (right arrowhead). j. Hypotrichidium conicum, ventral view, single frontal cirri (top arrowhead) and posterior rows of cirri
(down arrowhead). k. H. conicum, dorsal view, posterior rows of cirri (arrowhead). (a, f, j, k) scale bar = 20 µm. (b-e, g) scale bar =
10 µm.
Order Halteriida Petz & Foissner
Halteria grandinella (Müller) Dujardin
(Table VI; Fig. 2f)
The most important features to separate this
species from its congeners are the absence of
symbiotic algae and the disposition of basal bodies
in the equatorial somatic kineties in four groups, two
of them with two kinetosomes each and the other
two with four kinetosomes each.
Halteria
grandinella
was
recorded
throughout the studied period. The highest densities
occurred at temperatures below 11°C but under a
wide range of conductivity, pH and dissolved
oxygen concentration (Fig. 4).
Order Strombidiida Petz & Foissner
Limnostrombidium pelagicum (Kahl) Krainer
(Table VII; Figs. 2g and 3f, g)
Body conical-shaped, narrowed posteriorly.
With an equatorial girdle of extrusomes, lined by a
ring of somatic dikinetids with clavate cilia. Ventral
somatic kinety with paired kinetosomes. Oral
apparatus composed by an open ring of collar and
ventral membranelles, and the endoral kinety.
Without endosymbiotic algae. Macronucleus
globular; micronuclei elliptical and indented in the
posterior pole of the macronucleus. With numerous
ovoid pigmented granules, mainly in the posterior
81
half of the body and near equatorial extrusomes.
This species was recorded from winter to late spring.
It was maintained for a few days in wheat infusion
cultures.
Table V. Morphometric data on Strobilidium caudatum.
in vivo
Body, length
Body, width
X
71.4
50.1
Min
42
28
Max
98
68.6
M
84
56
SD
24.4
17.7
N
5
5
After Protargol
Body, length
Body, width
X
72.2
59.1
Min
56
49
Max
84
70
M
70
56
SD
6.6
5.1
N
16
16
Peristome, diameter
45
35
56
42
5.6
17
Apex to end of cytopharyngeal
fibers, distance
42
33.3
50
43.3
5.2
13
Macronucleus, width
7
32.1
5.6
23.1
8.4
39.2
7
39.2
1
4.6
10
9
Micronucleus, length
Micronuclei, number
2.7
1
2.1
1
3.2
1
2.8
1
0.3
0
6
6
5
5
5
5
0
20
External polykineties, number
Enlarged external polykineties,
number
Internal polykineties, number
19
18
21
20
0.8
20
6
4
7
6
0.9
18
1
1
1
1
0
11
Extrusomes, length
Extrusomes, width
3.9
1
3.3
0.7
5
1.4
3.3
1
0.9
0.3
11
11
Table VI. Morphometric data on Halteria grandinella.
After Protargol
Body, length
Body, width
X
24
22.7
Min
21
19.6
Max
28
28
M
23.8
22.4
SD
2.8
2
N
13
13
Equatorial somatic kineties,
number
7
6
7
7
0.4
16
Adoral polykinetids, number
Ventral polykinetids, number
16
7
15
6
17
7
16
7
0.7
0.5
15
4
Macronucleus, width
9.5
16
8.4
9.1
11.2
21
9.1
16.4
1
3.3
10
10
Micronucleus, width
2.5
2.2
2.1
2.1
2.8
2.8
2.8
2.1
0.4
0.3
5
5
82
Table VII. Morphometric data on Limnostrombidium pelagicum.
After Protargol
Body, length
Body, width
X
61.8
46.4
Min
48
35
Max
80
60
M
60
45
SD
9.2
8.4
N
30
30
16
12
16
10
16
14
16
12
0
0.9
22
25
Ventral somatic kinety,
number of basal body pairs
11
8
12
11
1
22
Macronucleus, width
17.3
21
14
14
22
27
17
21
2.6
3.2
25
25
Micronucleus, number
2.7
2
2.1
1
3.5
2
2.8
2
0.4
0.3
15
15
Pigmented granules, diameter
2.3
2.1
2.8
2.1
0.3
25
Table VIII. Morphometric data on Limnostrombidium viride.
After Protargol
Body, length
Body, width
X
56
42.1
Min
40
30
Max
70
55
M
55
40
SD
8.2
5.9
N
30
30
16
13
16
11
16
15
16
13
0
0.9
12
18
Ventral somatic kinety,
number of basal body pairs
15
13
18
15
1.2
20
Macronucleus, width
19.9
24.7
13
20
25
28
21
24
3.6
3
10
10
2.9
1.1
2.1
1
3.5
2
2.8
1
0.4
0.3
9
9
Pigmented granules, diameter
2.2
1.5
2.8
2.1
0.4
20
12
10
14
12
2
3
5.9
5.6
7
5.6
0.5
8
8.9
5.6
10
9.4
1.4
8
Equatorial extrusomes, number
of groups
Equatorial extrusomes,
diameter of groups
Symbionts, diameter
Limnostrombidium viride (Stein) Krainer
(Table VIII; Figs. 2h and 3h, i)
This species is similar to L. pelagicum
but it mainly differs in that it maintains
functional plastids (cleptoplasts) from the algae
it feeds on. The number of paired kinetosomes
(13-18) in ventral kinety and the number of
ventral membranelles (11-15) are also slightly
different.
This species was recorded during
autumn
and
winter,
coexisting
with
L. pelagicum. Both species reached the
maximum abundances at temperatures below
8 °C (Fig. 4).
83
Table IX. Morphometric data on Pelagostrombidium mirabile.
in vivo
Body, length
Body, width
X
40
28.3
Min
40
25
Max
40
30
M
40
30
SD
0
2.8
N
3
3
After Protargol
Body, length
Body, width
X
42.2
32.5
Min
30
25
Max
60
50
M
40
30
SD
7
5.7
N
24
24
15
12
13
10
16
14
15
12
1
1.1
11
17
Macronucleus, width
20.2
18.7
16.8
12.6
28
28
19.8
16.8
2.8
5.1
12
11
4.8
4.2
5.6
4.9
0.5
9
Extrusomes, length
19.6
15.4
25.2
18.2
5
3
Table X. Morphometric data on Hypotrichidium conicum.
in vivo
Body, length
Body, width
X
105
70
Min
98
56
Max
112
84
M
105
70
SD
9.8
19.7
N
2
2
Buccal cavity, depth
56
56
56
56
0
2
After Protargol
Body, length
Body, width
X
128.1
88.2
Min
98
63
Max
168
112
M
126
87.5
SD
17.7
14
N
30
30
Buccal cavity, depth
82.1
70
98
84
9.5
30
Frontal cirri, number
Frontal rows of cirri, number
Number of cirri,
1st frontal row
2nd frontal row
3rd frontal row
4th frontal row
1
4
1
4
1
4
1
4
0
0
20
30
6
6
11
14
4
5
10
11
7
7
13
16
6
6
12
13
0.7
0.5
1.1
1.5
20
20
20
20
Posterior rows of cirri, number
6
6
6
6
0
20
Rows of dorsal bristles, number
3
3
3
3
0
11
Oral polykinetids, number
41
34
49
40
3.7
20
Macronucleus, width
28.7
17.8
21
14
63
21
28
21
9
3.6
20
20
Micronucleus, width
3.2
2.7
2
2.8
2.1
2
4.2
3.5
2
3.5
2.8
2
0.4
0.3
0
20
20
20
84
Table XI. Compared physical and chemical variables (V) under which the species were found. T,
temperature (°C); DO, dissolved oxygen (mg L-1); C, conductivity (µS cm-1).
Species
V
T
pH
DO
C
Our observations
8.6
5.4
6.3
220
Other authors
5.2 - 8.7
8.4
6.7 - 10.2
⎯
Locality
Citation
France,
Germany
Foissner et al.
(1999)
Askenasia volvox
T
pH
DO
C
2.4 - 10.8
4.5 - 8.4
5.5 - 8.8
160 - 220
2.0 - 21.0
5.0 - 9.5
5.1 - 15.9
⎯
Germany
Foissner et al.
(1995)
Rhabdoaskenasia minima
T
pH
DO
C
2.39
4.97
5.47
220
⎯
⎯
⎯
⎯
⎯
⎯
Coleps hirtus hirtus
T
pH
DO
C
2.39-19.17
4.97-8.57
4.53-9.65
145-276
1-30
4.7-9.5
0-38
⎯
Austria,
Bulgaria,
Germany
Bick & Kunze
(1971)
Strobilidium caudatum
T
pH
DO
C
2.4 - 20.8
4.9 - 7.5
5.5 - 8.8
160 - 220
5.3 - 29
4.9 - 9.0
4.0 - 11.0
⎯
Austria,
Bulgaria,
USA
Foissner et al.
(1991)
T
pH
DO
2.39-19.17
4.97-8.57
4.53-9.65
0.8-35
4.2-9.8
0-38
145-276
⎯
Foissner et al.
(1999)
C
Austria,
Bulgaria,
Germany,
Hungary,
USA
Limnostrombidium pelagicum
T
pH
DO
C
9.4 - 24.1
6.3 - 6.8
6.3 - 7.9
120 - 220
10.6 - 21.4
⎯
⎯
⎯
USSR
Belova (1989)
L. viride
T
pH
DO
C
2.4 - 20.8
4.9 - 8.4
5.5 - 8.8
145 - 220
1.4 - 21
6.1 - 9.5
0.2 - 15.9
⎯
Germany,
Hungary,
USA
Foissner et al.
(1991)
Pelagostrombidium mirabile
T
pH
DO
C
6.7 - 10.8
7.8 - 8.4
6.6 - 8.0
145 - 189
⎯
⎯
⎯
⎯
⎯
⎯
Hypotrichidium conicum
T
pH
DO
C
24.7
6.82
⎯
190
3.0 - 27.5
6.4 - 7.2
1.5 - 5.8
⎯
Slovakia
Foissner et al.
(1999)
Teuthophrys trisulca africana
Halteria grandinella
Pelagostrombidium mirabile (Penard) Krainer
(Table IX; Fig. 2i)
Body ellipsoidal, posteriorly narrower than
anteriorly, mostly covered by polygonal cortical
platelets. Cytoplasm yellowish-green due to the
presence of cleptoplasts. Girdle of somatic
extrusomes lined by a non-ciliated ring of
kinetosomes, continuous at the buccal vertex. Adoral
zone of membranelles as an opened ring, composed
of collar and ventral membranelles that end below
mid-body. Endoral kinety at the right margin of the
buccal cavity.
This species was recorded in late winter and
early spring. The density peaks occurred under
alkaline pH, low temperature (11 °C) and low
conductivity values, while the dissolved oxygen
concentration was high (72 % of saturation)
(Fig. 4).
Order Stichotrichida Fauré-Fremiet
Hypotrichidium conicum Ilowaisky
(Table X; Figs. 2j and 3j, k)
85
2005. Pelagostrombidium mirabile appeared for the
first time in July 2004 (2917 ind L-1) and was
present in the pond only until September, when it
reached the highest numbers (8066 ind L-1).
Askenasia volvox was present from June to
September 2004 and in June 2005, mostly in low
numbers (less than 400 ind L-1) except during
September 2004 (1233 ind L-1). Strobilidium
caudatum was not found in the pond only in August
and December 2004, and attained the highest
densities during June 2004 (1000 ind L-1) and April
2005 (2283 ind L-1), when it was the most abundant
species. Limnostrombidium spp. could not be
identified to species level in Lugol preserved
samples and the highest number of individuals was
recorded during June 2004 (2783 ind L-1).
Limnostrombidium spp. were not recorded during
December 2004 and June 2005.
Rhabdoaskenasia minima, Teuthophrys
trisulca africana, and Hypotrichidium conicum were
not detected in Lugol fixed samples.
Discussion
Body pyriform, posteriorly widened and
with a cytoplasmic process. Two macronuclear
nodules, with one indented micronucleus each.
Contractile vacuole on the left, lateral to the
peristome and in the superior third of the body.
Single frontal cirrus in front of the paroral
membrane and four rows of frontal cirri to the right
of the peristome. Six oblique rows of posterior cirri
and 3 dorsal rows of dikinetids. Buccal field
relatively long, extending up to ¾ of body length.
Paroral and endoral kineties cross at the right margin
of the buccal cavity.
This species was recorded in spring and it
also grew from mud samples in summer. It was
maintained in wheat cultures for a short time.
Table XI shows the ranges of the physical
and chemical variables under which this species, as
well as the other ones, were recorded.
Species abundances and variation along an
annual cycle
The most abundant species were Halteria
grandinella,
Coleps
hirtus
hirtus,
and
Pelagostrombidium mirabile. Halteria grandinella
was present in the pond along the whole studied
period, reaching the highest abundances in July 2004
(18916 ind L-1). The greatest densities of C. h. hirtus
were recorded during December 2004 (11366 ind L1
), being relatively scarce in the other months (less
than 600 ind L-1) and was not found during June
Teuthophrys trisulca africana is recorded for
the first time in South America. Our specimens
match better with the African specimens observed
by Dragesco & Dragesco-Kernéis (1986), since it is
apochlorotic, although the macronucleus is not dumb
bell-shaped but vermiform and coiled. Foissner et al.
(1999) also found apochlorotic specimens from mud
samples in Australia. It is considered a rare species,
which prefers the spring (Foissner et al. 1999),
although we found it for the first time in autumn and
late spring.
Askenasia volvox was previously cited in a
water quality paper (Zaleski & Claps 2000) for a
eutrophic shallow lake from Buenos Aires province
but no description is available. The species was
recorded in South America by Pinto (1925) in Brazil
and by Wölfl (1996) in Chile, also without
description. The number of paired kinetosomes in
the equatorial kinety girdle is lower (9-10) than that
found by Packroff & Wilbert (1991) (18-20).
Rhabdoaskenasia minima is a new record
for South America. Morphometric data are
coincident with those of Krainer & Foissner (1990),
although the extrusomes of our specimens were not
well impregnated and this is a key character
according to Foissner et al. (1999). In this study, it
was identified as R. minima due to the presence of a
very conspicuous rhabdos, single kinetosomes in the
equatorial kinety girdle, two basal bodies in the subequatorial kinety girdle, and a single contractile
vacuole. The previously cited authors recorded this
species along the whole year, peaking in autumn
86
Figure 4. Ranges of species densities (ind L-1) related to conductivity and temperature (left column) and to dissolved oxygen and pH
(right column).
(2670 ind L-1 and 1720 ind L-1) and feeding on
Urotricha sp. On the contrary, we only found it once
in winter and coexisting with A. volvox.
Coleps hirtus hirtus was previously cited in
Argentina and South America by other authors (de la
Rua 1911, Cela 1972, Guillén-Aguirre 2002),
although it was only observed in vivo and
after supravital staining. Morphometry is
coincident with the observation of other
authors (Foissner et al. 1994, 1999).
Strobilidium caudatum is a new record for
Argentina. It was previously observed in South
America by Bürger (1909) in Chile, and by GuillénAguirre (2002) in Peru. Most morphometric data are
coincident with those observed by other authors
(Foissner et al. 1991, Petz & Foissner 1992). The
number of external membranelles coincides with the
observations of Petz & Foissner (1992), although
Foissner et al. (1991) mentioned a wider range (1821 vs 22-30, respectively). On the other hand, we
observed cortical extrusomes and pigmented
granules in some individuals, which was not cited by
other authors and would need further investigation.
Halteria grandinella is a cosmopolitan
species, which was previously cited in Argentina
and South America (de la Rua 1911, Cela 1972,
Guillén-Aguirre 2002), although it was only studied
in vivo or by supravital staining. Morphometric
characters are coincident with the observations of
other authors (Fauré-Fremiet 1951, Dragesco 1970,
Foissner et al. 1999) but Song & Wilbert (1989)
observed a higher number of equatorial somatic
kineties (9-10 groups).
Limnostrombidium pelagicum is a new
record for South America. It could have been
mistaken by other Argentinean researchers with L.
viride as was also pointed by Foissner et al. (1999)
for other localities. Morphometric characters
coincide with those stated in Foissner et al. (1999),
although we observed a slightly higher number of
basal body pairs in the ventral kinety (7-10 vs 8-12,
respectively) and numerous ovoid pigmented
extrusomes, mainly in the posterior half of the body
and
near
the
equatorial
extrusomes.
Limnostrombidium pelagicum became very similar
to L. viride after a few days in culture, when it lost
the plastids and presumably began to feed on
bacteria.
Limnostrombidium viride is a new record for
Buenos Aires province. It has been previously found
in Argentina by Seckt (1924), in Córdoba province,
who mentioned it in a checklist, without taxonomic
description, and by Modenutti & Pérez (2001), in an
Andean lake. Morphometric characters are
coincident with those described by other authors
(Kahl 1932, Foissner et al. 1991, 1999), although in
the present study the specimens possessed few
symbionts and of larger size than those described in
Foissner et al. (1999), which were 6 × 3.2 μm and
possibly belonging to genus Kirchneriella.
Pelagostrombidium mirabile is a new record
for South America, while other authors only found it
in Eurasia (Foissner et al. 1999). The morphometric
characters of this species match with the descriptions
of Penard (1922), Krainer (1991), and Foissner et al.
(1999), although the range of ventral membranelles
in our observations is lower than that stated in
Foissner et al. (1999) (10-14 vs 12-17, respectively).
Hypotrichidium conicum is a new record for
the ciliate fauna from South America. This
cosmopolitan and typical euplanktonic species has
been found in other ephemeral and eutrophic
environments (Foissner et al. 1991, 1999). As the
87
species developed from mud samples when the pond
went through a drought period, we assume it is able
to form resting cysts, although they were not
observed. The contractile vacuole was located on the
left side, lateral to the peristome on the superior
third of the body as in H. tisiae, and not near the
cytostome, as stated in Foissner et al. (1991, 1999).
It is different from the previously mentioned species
by having six posterior rows of cirri, and, for this
reason, it was identified in this study as H. conicum.
Concerning the seasonal variation of the
species found, the highest density of Askenasia
vovlox was recorded in early spring, while other
authors found low numbers during the cold half of
the year (Wang 1928, Wilbert 1969, Foissner et al.
1999). Coleps hirtus hirtus was recorded throughout
the year, as found in previous studies, along a
maximum in spring (Foissner et al. 1999). The
highest numbers of Strobilidium caudatum were
observed during autumn, when macrophytes were
present in the pond, while Wilbert (1969) found
60000 ind L-1 during summer in a eutrophic stream
from Germany. Halteria grandinella occurred in
more than 1000 ind L-1, which indicates eutrophic or
highly eutrophic conditions (Foissner et al. 1999).
Limnostrombidium pelagicum could not be
distinguished from L. viride in Lugol fixed samples
but, in coincidence with the findings of Krainer
(1991, 1995) in Austria, we observed higher
numbers of both species in spring and summer.
Limnostrombidium viride was very abundant in
autumn after the summer drought, while other
authors found higher numbers in summer (Foissner
et al. 1999) and summer and autumn (Modenutti &
Pérez 2001). Mixotrophic ciliates are known to be
dominant in oligotrophic environments due to the
accessibility to scarce nutrients (Fenchel 1987),
which along with the bacterivorous feeding regime
allow L. viride to inhabit very different habitats,
such as ultraoligotrophic lakes in Patagonia
(Modenutti & Pérez 2001) and, as in the present
study, a eutrophic shallow pond, being tolerant to a
wide range of environmental characteristics.
Pelagostrombidium mirabile appeared only during
winter and spring, while Krainer (1991) found it
abundantly throughout the year in eutrophic
groundwater ponds in Austria, peaking in autumn.
Most of the ecological characteristics
recorded coincide with other findings (Table XI). In
addition, the physical and chemical variables under
which
Rhabdoaskenasia
minima
and
Pelagostrombidium mirabile were found, were not
mentioned by other authors. Teuthophrys trisulca
africana was recorded under lower pH conditions
than those stated in its ecological summary by
88
Foissner et al. (1999).
The presence of the species dealt within this
study in an unpredictable environment such as this
temporary pond is related to their bacterivorous
regime (Fenchel 1987) as a primary or secondary
option, their tolerance to a wide range of
environmental conditions, when the pond was filled,
and their ability to produce resting cysts (Foissner
1987) to survive during dry periods.
Acknowledgments
Norbert Wilbert from Zoologisches Institut der
Universität
Bonn,
Germany,
is
greatly
acknowledged for his unconditional help. Thanks go
also to C. Ituarte and L. Lunaschi from the División
Zoología Invertebrados, Museo de La Plata, S.
Kleinman for improving the English, and M.
Meléndez for his help with the Portuguese. Support
of the Consejo Nacional de Investigaciones
Científicas y Técnicas (CONICET), Argentina, to
which the authors belong, is gratefully
acknowledged.
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Received July 2006
Accepted August 2006
Published online September 2006
Ocupação da praia da Boa Viagem (Recife/PE) ao longo de dois dias
de verão: um estudo preliminar
JACQUELINE S. DA SILVA 1,2, SCHEYLA C. T. BARBOSA 1, MÔNICA M. V. LEAL,
ANA R. LINS & MONICA F. DA COSTA1.
1
Laboratório de Ecologia e Gerenciamento de Ecossistemas Costeiros e Estuarinos (LEGECE). Departamento de
Oceanografia da UFPE. Av. Arquitetura, s/n°, Cidade Universitária, Recife-PE. CEP: 50740-550. Tel/fax: (81) 2126
8225/7218.
2
E-mail: [email protected]
Abstract. Occupation of a beach in Recife (NE Brazil) during summer days: a preliminary study.
The increase of local population, especially in beaches resorts, changes their carrying capacity leading to
pollution, as well as an uncomfortable feeling of pressure. This work identified the carrying capacity for a
beach area in Boa Viagem, Recife, Brazil. The carrying capacity was determined trough counting of
beach users along crowded days. Transects had 10 m width. Paper cards were handed over to beach users
when they went into the area. The beach area was divided according use, morphological and physical
aspects, in three Zones: active, solarium and open sea. The carrying capacity was measured through
effectively used area per person. The number of beach users varied from 0-1,590 in all Zones. The active
zone was the most used. The area occupied by beach users varied from 2,9 – 40,5 m²/ person. The peak
of beach users was between 10:00 to 13:00 hs. The main arrival time was from 9:00 to 10:00 h and
leaving time was 15:00 h. There were significative differences (p< 0,05) for number of beach users along
the day. The intense use resulted in pollution of the beach area and changed the kind of users along the
time.
Key words: carrying capacity, beach users, tourist beaches, tropical beaches.
Resumo. O aumento da população local, especialmente em cidades de praia traz como conseqüência a
poluição, bem como a situação de desconforto. O presente trabalho identificou a capacidade de carga
para uma faixa de praia em Boa Viagem, Recife, Brasil, determinada através da contagem de usuários da
praia ao longo de dias feriados. Transectos com 10m de extensão foram demarcados e cartões de papel
foram entregues aos usuários quando entravam na faixa de praia estudada. A faixa de praia foi dividida
de acordo com o uso, aspectos físicos e morfológicos, em três Zonas: ativa, sollarium e de mar aberto. A
capacidade de carga foi medida através da área efetivamente utilizada por pessoa. O número de usuários
da praia variou de 0-1590 em todas as Zonas. A zona ativa foi a mais usada. A área ocupada pelos
usuários da praia variou de 2,9 - 40,5 m²/pessoa. O horário de pico de usuários ocorreu entre 10:00 e
13:00 h. O horário de chegada foi 9:00 as10:00 h, e o de saída foi ás 15:00 h. Existiram diferenças
significativas (p< 0,05) no número de usuários da praia ao longo do dia. A intensidade de uso resulta na
poluição da faixa de praia e mudanças no tipo de usuário ao longo do tempo.
Palavras-chave: capacidade de carga, usuários da praia, praias turísticas, praias tropicais.
Introdução
O turismo é atualmente um dos principais
responsáveis pela ocupação do litoral brasileiro, com
importante influência no processo de urbanização. A
expansão da atividade turística ocorre pela
exploração de ambientes litorâneos ensolarados que
reforçam a vocação turística da costa brasileira,
sendo a qualidade ambiental e beleza cênica fontes
diretas de bem-estar (MMA 1998).
A escolha da praia visitada reflete a
J. S. DA SILVA ET AL.
92
expectativa de uma praia ideal que varia de usuário
para usuário. De Ruyk (1997) classificou os usuários
das praias em agregacionistas e individualistas. Os
agregacionistas vão à praia para experiência social,
preferindo praias desenvolvidas, superlotadas e com
abundancia de atividades. Por outro lado, os
individualistas, são aqueles que procuram uma
experiência de contato com a natureza, preferindo
praias pouco desenvolvidas, com beleza natural e
tranqüilidade (De Ruyk 1997, Morgan 1999,
Eugenio-Martins 2004).
A capacidade do recurso base para uso
recreacional pode ser analisada através da ocupação
da praia. Essa ocupação é definida através do
número máximo de pessoas por m2, que podem usar
o ambiente sem declínio na qualidade da experiência
social. Estudos prévios sobre capacidade de carga
determinaram um intervalo de uso no qual o número
de usuários compromete a experiência recreacional
(De Ruyk 1997, Da Silva 2002a, b). É baseada no
conceito
da
manutenção
do
nível
de
desenvolvimento e uso que não resulte na
deterioração sócio-cultural e ambiental, ou na
percepção da degradação do recurso pelos usuários
(De Ruyk 1997, Papageorgiou & Brothereton 1999,
Morgan 1999, Eugenio-Martins 2004).
O Brasil apresenta 8500 km de linha de
costa (Awosika & Marone 2000), o que denota uma
alta
potencialidade
turística,
advinda
das
características ambientais locais. Dentre estas o
clima, vegetação, presença de dunas, recifes de coral
e arenito agregam valor paisagístico as praias,
tornando-as instrumento de apreciação dos usuários.
Alguns dos principais cartões postais
brasileiros são as praias do litoral Pernambucano. O
Estado apresenta uma linha de costa de 187 km, com
praias
que
são
destinos
turísticos
em
desenvolvimento e consolidados, por exemplo,
Maracaípe e Boa Viagem, respectivamente.
Na década de 70, a praia da Boa Viagem foi
palco da exploração turística que acelerou seu
processo de urbanização. Sem planejamento
adequado a orla da Boa Viagem passou a ser
explorada não só pela atividade turística, mas
também pela atividade imobiliária, resultando na
perda das características ambientais. A especulação
imobiliária na área acelerou a verticalização e
aumentou o custo de vida da população local, sendo
o bairro da Boa Viagem um dos bairros com maior
custo de vida da cidade. Devido ao crescimento
desordenado, parte da praia sofreu mudança
paisagista devido aos processos de erosão costeira
(Gregório 2004, Souza 2004, Leal 2006).
A praia da Boa Viagem possui cerca de 8km
de extensão os quais se apresentam em um conjunto
paisagístico composto de sol, areia, mar e recifes de
arenito paralelos a linha de costa (Costa & Kahn
2003, Costa & Souza 2002). A orla da Boa Viagem
pode ser classificada como “exposta com
urbanização consolidada” ou “exposta com
urbanização” (PROJETO ORLA 2001). Seguindo
outra classificação (Smith 1991) ela é considerada
como cidade resort, ou praia altamente desenvolvida
(Morgan 1999). Esta praia apresenta diferentes graus
de conservação em relação ao ambiente praial. Os
recifes de arenito são responsáveis pela formação de
piscinas naturais durante a baixa-mar. A maioria dos
hotéis de luxo construída na orla da Boa Viagem
encontram-se em frente a maior faixa de extensão
desses recifes, explorando a beleza cênica do local.
Por isso, este trabalho teve como objetivo
definir a dinâmica de ocupação e recreação ao longo
do dia no trecho mais ocupado da praia. Um estudo
dessa natureza em uma praia de importância sócioeconômica e ambiental como Boa Viagem é de
grande relevância. A partir dele é possível
determinar os locais mais susceptíveis a impactos
oferecendo base para elaboração de planos de gestão
e ordenamento da orla a fim de mitigar os efeitos
negativos causados pela intensidade de uso.
Material e Métodos
A área de estudo, onde foi estabelecido o
transecto, está localizada na porção central da praia
de Boa Viagem (Figura 1), onde ocorre a formação
das piscinas naturais na maré baixa. A escolha desta
área foi condicionada por três variáveis: a) ser um
dos pontos identificados por Silva et al. (2006) e
Leal (2006) como de maior uso da praia; b) por ter
uma qualidade ambiental considerada intermediária
(Souza 2004) e c) por ser um dos pontos de
concentração de atividades econômicas.
Esta
parte
da
praia
apresenta
aproximadamente 50 metros de mesolitoral os quais
são totalmente tomados pela água na maré alta.
Devido à especulação imobiliária, o supra-litoral foi
quase totalmente transformado na avenida beira-mar,
que é densamente ocupada por edifícios e hotéis
luxuosos.
A metodologia utilizada foi baseada no
trabalho de Polette et al. (2001) e Polette & Raucci
(2003), que sugerem um zoneamento do ambiente
praial a partir das características morfológicas,
hidrodinâmicas e de uso, da seguinte maneira:
1 - Zona solarium (supra e mesolitoral) –
onde são realizadas atividades como tomar banho de
sol, armar barracas e guarda-sóis, etc.
2 - Zona ativa (mesolitoral) - faixa de praia
junto ao mar, altamente influenciada pela oscilação
da maré, utilizada para caminhadas e atividades
Ocupação da praia de Boa Viagem
93
recreativas na areia (jogos, castelos de areia e etc.).
3 - Zona de surf (infralitoral) - faixa onde
ocorre a quebra das ondas, e na qual são realizadas
atividades recreacionais aquáticas que não
necessitam do uso de equipamentos (nado e banho
de mar).
A área estudada apresenta todas as zonas
supracitadas. Para visualização do ponto do
experimento em cada Zona da praia, foi delimitada
uma faixa de 10 m de largura, que se estendia desde
o calçadão à linha d’água. Cordas laterais e
bandeiras foram utilizadas para demarcar os limites.
A área de amostragem correspondeu a 620 m2 e 515
m2 para um feriado e domingo de verão,
respectivamente.
Figura 1. Imagem da faixa de praia estudada na Parte central da
Praia da Boa Viagem, Recife/Brasil (ZS, Zona solarium; ZA,
Zona ativa e ZSURF, Zona de surf). (Foto: Monica F.Costa
2002)
Cartões de papel numerados, contendo o
título da pesquisa, seus objetivos e uma breve
explicação sobre de que forma o usuário poderia
colaborar com o experimento foram confeccionados
(Tabela I). Os cartões tinham diferentes cores para
cada intervalo de hora de chegada, com a finalidade
de identificar a hora de chegada de cada usuário no
momento em que o mesmo o devolvia na saída. Os
cartões devolvidos eram acondicionados em
envelopes com o intervalo de hora de saída
identificada, a fim de calcular o tempo de
permanência na praia.
A equipe no local de amostragens constou
de quatro pesquisadores, os quais ficaram divididos
com as seguintes funções: um para fotografar a cada
intervalo de hora, dois para realizarem a abordagem
dos usuários e um outro para contar o número de
usuários na zona ativa.
À medida que as pessoas entravam na área
delimitada (±100 m2), eram abordadas pelos
pesquisadores, que entregavam o cartão, explanando
brevemente sobre a pesquisa e como o usuário
poderia colaborar com o experimento. Em seguida,
era medida a área no formato de retângulo ocupada
pelo grupo de usuários, o número de usuários e a
atividade realizada por eles no momento da
abordagem.
A cada hora, das 8:00 às 18:00, foram
tiradas fotografias da área delimitada da praia. As
fotografias foram utilizadas para contagem de
usuários na Zona de surf e de mar aberto tomando
como limite as cordas estendidas na Zona do
Solarium. Não foi possível utilizar as fotografias
para a Zona do Solarium, visto que os guarda-sóis
impossibilitavam a visualização correta do número
de pessoas. Nesse mesmo intervalo de tempo, das
8:00 às 18:00, era feita a contagem do número de
usuário que passavam na zona ativa, durante 15
minutos com o auxílio de um contador manual.
A capacidade de carga foi calculada de
acordo com Ruschman (1999) e Eugenio-Martin
(2004), através da densidade de usuários na Zona do
solarium:
C = V/K
Onde, C é a capacidade de carga, V e área
disponível para uso e K é o número de usuários.
Existe uma imprecisão no experimento
devido ao número de usuários que se recusaram a
participar somado aos usuários que esqueceram de
entregar o cartão. Esta recusa pode está associada a
forma de abordagem que pode ter alterado o
comportamento do usuário. Esta imprecisão foi
calculada pelo número de cartões que estavam
faltando ao final do dia somado com o número de
recusas recebidas. Este estudo foi realizado nos dois
dias de maior freqüência de usuário (Silva et al.
94
Tabela I. Modelo dos cartões bilíngües (português e inglês) que eram entregues aos usuários quando eles entravam na
área de estudo.
Esta é uma pesquisa sobre a capacidade de carga This is a research about Beach Carrying Capacity. Beach
recreacional de uma praia. Capacidade de carga carrying capacity is the number of users that an area may
recreacional é o número de visitantes que determinada receive without changing its quality. It helps planning
área pode receber sem alterar sua qualidade. Isso ajuda sustainable tourism.
no planejamento do turismo sustentável.
Objective: To measure Boa Viagem carrying capacity in
Objetivo: Determinar a capacidade de carga order to understand the beach’s dynamics and the
recreacional da praia da Boa Viagem, afim de se interference of users on this environment.
entender a dinâmica da praia bem como a interação dos
visitantes com o meio.
How can you collaborate with our experiment?
Como você pode colaborar para a nossa pesquisa?
• Não retirar as bandeiras que delimitam a área do
experimento;
• Permita a medição da área que você está ocupando e
• Devolva este cartão na saída.
•
Do not remove the flags marking the
experimental area;
•
Allow us to take the measurements around your
area and
•
Hand back the card when you leave the beach.
Thank you!
Obrigado!
2006) da praia de Boa Viagem: um feriado nacional
de 8 de dezembro e o domingo subseqüente, no mês
de dezembro de 2004.
Para avaliar se existe diferença significativa na
quantidade de usuários nos horários amostrados uma
ANOVA foi realizada, utilizando o software
STASTISTICA 5. Onde a ANOVA mostrou-se
significativamente diferente, um teste a posteriori
Tukey’s foi usado para determinar quais médias
foram significativamente diferentes (p<0,05).
Resultados e Discussão
Trabalhos de capacidade de carga
recreacional são amplamente utilizados para avaliar
os impactos dos usuários e a percepção destes em
relação aos problemas por eles gerados. As
metodologias amplamente utilizadas e difundidas
para o cálculo da capacidade de carga recreacional
são o senso visual (De Ruyk 1997, Saveriades 2000,
Polette et al. 2001, Arnberger et al. 2004,
Arnberg & Haider 2005, Silva et al. 2006) e
imagem aérea e digital, (Da Silva 2002a,
Arnberg et al. 2004, Arnberger & Haider 2005).
Muitas vezes a estimativa do número de usuários
presentes está associada as entrevistas que tem
como objetivo relacionar a percepção do usuário à
superlotação e a possibilidade dele vir a repetir a
visita
ao
local.
Todos
esses
métodos
supracitados sozinhos ou em conjunto dão uma boa
estimativa do número total de usuários que
freqüentam o local, sem apresentar diferenças
significativas (Arnberger & Haider 2005).
O somatório do número de usuários nos dois
dias amostrados foi em média de 1590 pessoas/dia
nas três Zonas da praia (Solarium, ativa e surf). A
imprecisão foi em média de 3,7% nos dois dias
amostrados, o que demonstrou uma grande aceitação
do usuário em participar do experimento. O horário
de pico de freqüência dos mesmos esteve entre 10:00
e 13:00 h. O horário de chegada de usuários no
ponto de estudo estava entre 9:00 e 10:00 h, e o de
saída entre 13:00 e 15:00 h (Figuras 2 e 4). Não
houve diferença significativa no comportamento da
freqüência entre os dias amostrados (p > 0,05). A
análise ANOVA demonstrou existir diferenças
significativas (p< 0,05) no número de usuários ao
longo do dia. De acordo com os resultados, os
intervalos definidos como de pico (10:00 ás 13:00 h)
diferem significativamente (p<0,05) daqueles
reconhecidos como de começo de manhã (8:00 9:00 h) e fim de tarde (15:00 - 16:00). A dinâmica
de ocupação da praia ao longo do dia está
diretamente associada as maiores incidências da luz
solar. Diferenças de latitude proporcionam
diferenças no horário de pico e na quantidade de
horários de pico, quando comparados com outros
estudos da mesma natureza (Deacon & Kolstad
2000, Da Silva 2002b, Silva et al. 2006). Da Silva
(2002a, b) observou que o pico de freqüência de
usuários em cinco praias portuguesas estava entre
11:00 e 12:00 h. Deacon & Kolstad (2000)
observaram um pico de freqüência de usuários as
13:30 h durante o final de semana nas praias de
Newport e Huntington (Califórnia, Estados Unidos).
Para Balneário Camburiú (SC) o pico de usuários
ocorreu às 10:00 h durante o verão, com redução
95
Figura 2. Ocupação da Zona do solarium ao longo do dia em frente ao Hotel Recife Palace Lucsim, Praia da Boa Viagem, PE.
(Fotos: Jacqueline S. da Silva 2004).
significativa entre 11:00 e 15:30 h (Polette et al.
2001). Quando comparado com estudo anterior em
Boa Viagem (Silva et al. 2006), os resultados
obtidos nestes estudos corroboram os anteriores com
relação ao horário de pico, intensidade de uso e sua
área disponível.
A dinâmica de ocupação de uma praia é
refletida pela sua densidade de usuários localizados
no supra e meso litoral (Zona do Solarium), onde a
principal atividade realizada é o banho de sol. Nas
horas de maior intensidade solar ocorreu o aumento
de usuários, que proporcionou a diminuição da área
disponível para uso (Figura 3). O tamanho do grupo
influenciou diretamente no valor da área ocupada
(Tabela II). A área disponível para uso é
inversamente proporcional ao número de usuários. A
área disponível para os usuários na faixa de praia
estudada variou de 2,9 a 40,5 m²/pessoa (Figura 3).
O menor valor de área disponível ocorreu no horário
de maior número de usuários (10:00-13:00 hs). De
acordo com Leal (2006), os usuários da praia
habitualmente se reúnem em grupo no mesmo local,
independente do número de visitantes. De Ruyk
(1997) estabeleceu como intervalo de conforto para
os usuários 6.3-25 m²/indivíduos para praias
arenosas da África do Sul. Em Portugal a área
disponível para os usuários variou de 13,5 a 111,7
m²/pessoa (Da Silva 2002a), sendo considerada pelo
autor como intolerável/desconfortável.
O tempo de permanência dos usuários variou
entre 2 a 5 horas. As pessoas que chegaram às 8:00 h
permaneceram em média 2 horas, as que chegaram
no horário de pico (11:00-13:00 h) permaneceram
em média 3 horas e saíram ao final do dia (15 e 17
hs). Dos usuários amostrados na área 88,4% estavam
na praia em grupos que variaram de 2 a 4 pessoas
(Tab. II). Leal (2006) retratou através de
questionário estruturado o perfil do usuário da praia
da Boa Viagem. De acordo com este trabalho, as
pessoas que utilizam a praia permanecem
aproximadamente quatro horas e geralmente vão em
grupo de quatro pessoas, que são comumente seus
parentes.
O número de usuários na zona ativa foi em
média 1391,5 pessoas/dia, com mínimo de 20 e
máximo de 254 pessoas em 15 minutos (Figura 5). O
padrão de uso desta zona foi o mesmo nos dois dias
amostrados. A freqüência total de usuários foi quatro
vezes maior na Zona ativa do que no Solarium para
todos os horários amostrados. De acordo com a
estimativa para uma hora de contagem, os horários
de pico de freqüência estiveram entre 9:00 e 10:00 h,
o que não corresponde aos do Solarium. Ocorre uma
diminuição do número de pessoas caminhando a
partir das 12:00 h.
Nos últimos três anos, o turismo em
Pernambuco vem diminuindo, dando espaço a outros
Estados nordestinos que têm as mesmas
características de litoral ensolarado, como Ceará e
Alagoas. Uma das razões apontadas para essa
diminuição é a falta de investimentos em marketing
turístico, bem como a ocorrência de ataques de
tubarão na Boa Viagem. Em dez anos (1992-2002),
foram registrados trinta e oito ataques nas quatro
praias metropolitanas do estado, sendo vinte e dois
em Boa Viagem (Silva 2002). Já no ano de 2006, 50
ataques foram registrados na Boa Viagem. Segundo
Leal (2006), apenas 39,6% dos freqüentadores da
Boa Viagem afirma ter mudado a forma de uso da
praia, devido aos ataques. Entre as mudanças
96
Tabela II. Comparação do tamanho médio dos
grupos de usuários localizados na zona de Solarium
da praia da Boa Viagem nos dois dias amostrados.
Total de
pessoas
204
Tamanho do grupo no Solarium (%)
1
2
3
≥4
11,6
37,8
20,5
30,1
Tamanho médio da área ocupada pelos
grupos (m²)
1,3
1,6
3,7
≥ 4,6
Figura 3. Área utilizada na Zona de Solarium ao longo do dia.
Figura 4. Número médio de pessoas na Zona de Solarium ao
longo do dia.
em média 96,5 pessoas/dia. Os padrões entre os dois
dias variaram bastante, provavelmente devido à
diferença na amplitude de maré (feriado - cheia e
domingo, minguante). A amplitude de maré em
Recife varia aproximadamente 2,5 m. A falta de
segurança no banho é um dos fatores que
influenciam essa evasão do uso do balneário. Na
praia de Boa Viagem o usuário não entra na água
para tomar banho na maré alta, e quando o faz, fica
restrito à Zona de surf, onde os recifes lhe garantem
alguma proteção (Figura 2). Por essa razão o número
de usuários na Zona de Surf foi baixo em relação às
outras zonas.
O dano ao ambiente recreacional torna-se
perceptível quando a dinâmica de ocupação
diminui. A faixa de areia fica repleta de resíduos
sólidos, geralmente compostos por itens plásticos
descartáveis, como copos, pratos, colheres e
garrafas. Esses resíduos são típicos de usuários da
praia (Silva et al. 2006). O declínio da qualidade
ambiental de Boa Viagem vem sendo documentado
não só pela perda das características paisagísticas
(Souza 2004), qualidade da água (Costa & Barleta
2004), mas também pelos impactos originados pelos
seus usuários (Silva et al. 2006).
A perda das características paisagísticas e a
poluição da água e da areia aparentemente não
cessam a visita dos usuários da praia da Boa
Viagem. Ao longo dos anos esses fatores podem ter
sido responsáveis pela mudança no tipo de usuário.
Os usuários da praia de Boa Viagem que antes
procuravam o contato com a natureza eram
compostos basicamente por turistas interessados na
exploração da beleza natural da praia. Hoje, os
usuários da Boa Viagem são basicamente os
residentes e locais que buscam a praia para
experiência social (Leal 2006).
Considerações Finais
Figura 5. Número de pessoas na Zona Ativa na praia ao longo
do dia.
apontadas por eles as principais foram: não entrar
no mar, mergulhar em águas rasas e entrar receoso
na água (Leal 2006). Por estas razões as Zonas de
surf e mar aberto foram pouco freqüentadas.
O número de usuários na Zona de surf foi
A capacidade de carga recreacional é uma
ferramenta que deverá ser utilizada para elaboração
de planos de gestão e ordenamento da orla de modo
a mitigar os efeitos negativos causados pela
intensidade de uso. Cada Zona da praia apresentou
uma dinâmica de uso que estava diretamente
relacionada com a atividade praticada e a
intensidade solar. Os usuários da Zona Solarium,
cuja principal atividade é o banho de sol, preferem
horários com maior radiação solar. Já a zona ativa é
mais utilizada nos horários de baixa intensidade
solar. A maioria dos usuários vão a praia em grupos
compostos de 2 a 4 indivíduos. A quantidade de
usuários variou significativamente ao longo do dia,
sendo esta variação provocada provavelmente pela
97
intensidade solar e altura da maré. A capacidade de
carga recreacional para o ponto de estudo foi alta
(2,9 m²/pessoa). O horário de pico ocorreu no
intervalo de almoço, coincidindo com a maior
intensidade solar. Fatores como morfologia da praia,
horários de maior incidência solar e amplitude de
maré influenciam na capacidade de carga
recreacional da praia. Devido a isso é essencial para
avaliar se a dinâmica de ocupação varia ao longo da
praia amostras mais freqüentes e em outros setores
da praia da Boa Viagem.
Agradecimentos
Os autores agradecem ao Hotel Recife Palace
Lucsim pela autorização para fotografar em frente a
área de estudo. À Coordenação de Aperfeiçoamento
de Ensino Superior - CAPES, pela bolsa de
Mestrado de Jacqueline Santos da Silva.
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Received July 2006
Accepted October 2006
Published online November 2006
Report on the smallfin catshark Apristurus parvipinnis Springer &
Heemstra (Chondrichthyes, Scyliorhinidae) in Western South
Atlantic with notes on its taxonomy
ULISSES L. GOMES 1, CAMILA N. SIGNORI 2 & OTTO B. F. GADIG 3*
1
Universidade do Estado do Rio de Janeiro, Departamento de Biologia Animal de Vegetal, Rua São Francisco Xavier
524, 20559-900, Rio de Janeiro, Brazil, [email protected], research suported by PROCIÊNCIA/UERJ/FAPERJ.
2
Universidade do Estado do Rio de Janeiro, Departamento de Oceanografia, Rua São Francisco Xavier 524, 20559900, Rio de Janeiro, Brazil, [email protected], research suported by IC-CNPq, process 118048/2004-0.
3
Universidade Estadual Paulista, Campus do Litoral Paulista, Praça Infante Dom Henrique s/n, 11330-900, São
Vicente, SP, Brazil, e.mail: [email protected]., supported by CNPq , process 309740/2003-7; * corresponding
author.
Abstract. This note presents data on the smallfin catshark Apristurus parvipinnis in the Western South
Atlantic, with taxonomic comments on this species. The smallfin catshark was previously reported,
usually from Western North Atlantic, but few recorded specimens are known from Brazilian Western
South Atlantic. This species occurs on the upper and middle continental slopes, usually near the bottom.
This report is based in one 588 mm total length mature male, collected off Rio de Janeiro between depths
of 650-720 meters. Comments on its taxonomy are presented, comparing this species with other Atlantic
Apristurus species.
Keywords: Elasmobranchii, Carcharhiniformes, distribution, Brazil, morphometrics.
Resumo. Registro do tubarão-gato-escuro Apristurus parvipinnis Springer & Heemstra
(Chondrichthyes, Scyliorhinidae) no Atlântico Sul Ocidental, com notas sobre sua taxonomia. Este
trabalho apresenta dados sobre o tubarão-gato-escuro Apristurus parvipinnis no Atlântico Sul Ocidental,
com comentários taxonômicos sobre a espécie, que foi previamente registrada principalmente no
Atlântico Norte Ocidental, mas poucos registros são conhecidos em águas do Brasil, no Atlântico Sul
Ocidental. Esta espécie vive nos taludes superior e médio, normalmente próxima ao fundo. Os dados aqui
apresentados são baseados em um exemplar macho maduro de 588 mm de comprimento total, coletado
em frente ao Rio de Janeiro, entre 650 e 720 m de profundidade. São apresentados comentários sobre sua
taxonomia, comparando a espécie com outros tubarões do gênero Apristurus do Atlântico.
Palavras-chave: Elasmobranchii, Carcharhiniformes, distribuição, Brasil, morfometria.
The catsharks of genus Apristurus Garman, 1913,
are deepwater species from continental slopes,
usually inhabiting at depths up to 2000 m (Nakaya et
al. 1999). The genus is characterized by a fully and
mostly uniformly dark slender body with an
elongated anal fin ending in front of the beginning
of the lower caudal fin, possessing a flatted and
spatulated snout, and presenting upper and lower
labial furrows. The genus is comprised of thirty two
recognized species and at least seven undescribed
species (Compagno 1984, Meng et al. 1985, Nakaya
1975, 1988a, b, 1989, 1991, Nakaya & Séret 1989,
1992, Nakaya & Stehmann 1998, Nakaya & Sato
1998, 1999, Nakaya et al. 1999).
Apristurus
parvipinnis
Springer
&
Heemstra, 1979, has been reported from Gulf of
Mexico, off Pensacola (Florida), Gulf of Campeche
(Mexico), off the Caribbean coast of Panama and
Colombia, and off French Guiana (Uyeno & Sasaki
1983, Compagno 1984). Springer (1966), studying
the Western Atlantic scyliorhinids had erroneously
termed this species as Apristurus indicus Garman,
1913 (recorded for the Western Indian Ocean). This
species occurs near the bottom on the upper and
Apristurus parvipinnis in Western South Atlantic
100
middle continental slopes. The holotype was
captured in the depth of 1115 m and the twelve
paratypes were collected between 676 and 1097 m.
According to Springer (1979) and Compagno
(1984), it is a small shark reaching from 268 up to
521 mm of total length (TL).
A few previous reports on the occurrence of
Apristurus parvipinnis in the Western South Atlantic
are presented by Gadig & Gomes (2003), for Bahia
(central Brazil) and Rincon & Vooren (2006), for
Santa Catarina coast, southern Brazil. Both studies
do not present any aditional data on this species.
The present study reports the occurrence and
taxonomic data of the smallfin catshark, Apristurus
parvipinnis, in the Brazilian Western South Atlantic,
with taxonomic comments on this species,
comparing it with other catsharks genus Apristurus
from Atlantic.
The Brazilian specimen, a 588 mm TL
mature male, was caught by bottom-trawl in 2004,
between 650-720 meters deep off eastern Cabo Frio
(23º50' S e 41º20' W), Rio de Janeiro State. The
specimen was frozen for morphometric and
morphological analysis, and placed at the
Ichthyological Collection of the Universidade do
Estado do Rio de Janeiro - UERJ 2056.
Morphometric and meristic data, visceral disposition
pattern and cephalic sensory canal terminology
followed respectively Springer (1979), Nakaya
(1991) and Nakaya & Sato (1999).
The small catshark Apristurus parvipinnis
(Fig. 1) was identified by the following combination
of features: presence of a long upper labial furrows
reaching midway to the nostril; lengths of the upper
labial furrows are longer than the lower ones;
distance between pectoral and pelvic fin bases long,
from 10.8 to 14.0% of the total length (14.4% in the
Brazilian specimen); anal fin base about 16.0 to
18,0% of the total length (17.3% in the Brazilian
specimen); rear end of the base of second dorsal fin
in advance of rear end of base of anal fin; distance
between dorsal fin bases less than distance from tip
of snout to eye; origin of dorsal fin posterior to rear
end of pelvic fin base; distance between dorsal fin
bases greater than length of base of second dorsal
fin; anal fin long, its rear tip separated from origin of
lower caudal lobe by a distance less than half the
length of the eye. The morphometric description of
the Brazilian A. parvipinnis specimen is presented in
Table 1 in comparison to the holotype.
According to Springer (1979) this species
presents more than 50 rows of teeth in each jaw.
Brazilian specimen showed 89 rows of small teeth in
the upper jaw and 90 rows in lower jaw (89/90) or
44-45/44-46. Symphyseal and commissural teeth of
upper jaw with 4 cusps, while symphyseal and
commissural teeth of lower jaw presented 5 and 6 or
7 cusps, respectively. The 588 mm TL adult male
herein examined represents the greatest total length
up to date recorded for this species.
According to Compagno (1984) a crest of
enlarged denticles along the dorsal margin of the
caudal fin can be variably developed in the
following species: Apristurus canutus Springer &
Heemstra, 1979, Apristurus investigatoris (Misra,
1962), Apristurus manis (Springer, 1979),
Apristurus microps (Gilchrist, 1922), Apristurus
parvipinnis, Apristurus profundorum (Goode &
Bean, 1896), Apristurus stenseni (Springer, 1979) or
even absent in the other species of Apristurus.
Compagno (1984) affirms that A. parvipinnis
presents enlarged denticles along the dorsal margin
of the caudal fin, otherwise, Uyeno & Sakaki (1983)
report that there are no modified denticles in the
caudal fin of this species. Our specimens presented
not a real crest, but enlarged dermal denticles along
the dorsal margin of the caudal fin.
There are 11 described Apristurus species in
the Atlantic Ocean (Compagno et al. 2005).
A. parvipinnis differs from Apristurus aphyodes
Nakaya & Stehmann, 1998, A. manis, A. microps
and Apristurus riveri Bigelow & Schroeder, 1944 in
presenting more spiral valves counts (15-22 versus
8-12), head sensory canal pores discontinued and
upper labial furrow longer than lower. This species
is similar to A. canutus, Apristurus laurussonii
(Saemundsson, 1922) e Apristurus saldanha
(Barnard, 1925) concerning the discontinued head
Figure 1 – Apristurus parvipinnis, adult male 588 mm TL, caught off Rio de Janeiro, southern Brazil (UERJ 2056).
ULISSES L. GOMES ET AL.
101
Table I – Morphometrics expressed as percentage of total length in Apristurus parvipinnis, comparing
specimen from the present study with the holotype and range in 12 paratypes.
Measurements
Tip of snout to:
front of the mouth
Eye
origin pectoral fin
origin 1st dorsal fin
origin pelvic fins
origin 2nd dorsal fin
origin upper caudal lobe
Orbit:
horizontal diameter
vertical diameter
Mouth:
Width
Length
length upper labial furrow
length lower labial furrow
Gill slits:
1st
5th
First dorsal fin:
length base
Height
length anterior margin
Second dorsal fin:
length base
Heigth
Pectoral fin:
width base
greatest width
Pelvic fin:
distance origin to posterior tip
Caudal fin:
upper margin
Distance between fin bases:
First to second dorsals
pectoral to pelvic
holotype♂
476 mm
paratypes
268-521 mm
UERJ 2056♂
588 mm
8.8
10.1
21.4
51.5
42.0
63.0
8.6-9.2
9.6-11.2
20.0-22.5
49.6-52.8
39.0-43.0
60.4-65.0
8.2
9.2
20.9
50.7
42.5
64.1
72.2
69.0-73.8
74.6
3.1
1.2
2.9-3.5
0.7-1.4
3.4
1.4
7.1
3.6
2.9
1.7
7.0-9.2
2.8-3.9
2.6-3.4
1.7-2.2
9.5
2.9
3.2
2.2
1.7
1.5
1.3-2.2
1.0-1.7
1.9
1.4
3.8
3.4
6.1
3.6-4.5
1.3-3.4
5.5-7.6
4.8
1.5
7.3
5.7
2.5
9.2
5.3-7.3
2.0-3.2
8.3-9.7
5.8
2.2
7.8
8.0
11.6
8.2
7.1-9.8
10.1-14.6
7.2-8.5
8.2
11.4
9.2
12.6
10.1-12.6
10.0
27.3
26.0-30.9
28.7
8.0
13.7
6.7-9.4
11.3-13.7
8.8
14.4
sensory canal pores and size but differs in the
number of counts of the intestinal spiral valves.
However, such data must be carefully considered
due to the low number of specimens examined from
other species, as follows: A. canutus (14–17 valves,
11 specimens examined), A. laurussoni (17–20, five
specimens) and A. saldanha (16 valves, one
specimen).
In A. parvipinnis and A. canutus the first
dorsal fin is much smaller than second, and the
surface area equal to or less than the half of the
surface area of the second dorsal fin (in A.
laurussonii and A. saldanha the first dorsal fin
surface is a little smaller than the second dorsal fin
surface area, corresponding to two thirds of the
second dorsal surface area); A. parvipinnis differs
from A. canutus in having the pectoral-pelvic
distance more than half of the anal fin base (less
than half of the anal fin base in A. canutus).
Springer (1979) and Compagno (1984)
affirms that A. parvipinnis is one of the commonest
Apristurus species caught in deep trawls around Gulf
Apristurus parvipinnis in Western South Atlantic
102
of
Mexico-Caribbean
area,
along
with
A. laurussonii. Previous records of this species are
mostly from the Western North Atlantic and
Caribbean (Springer 1979, Nakaya & Stehmann
1998, Nakaya & Sato 1999). A few specimens are
known from Western South Atlantic (Gadig &
Gomes 2003, Rincon & Vooren 2006), but these
studies just cited A. parvipinnis in this area, with no
more additional taxonomic, morphological or
biological data. The specimen herein examined
represents the greatest total length up to date
reported for this species.
Genus Apristurus’ species are known to
occur at deep oceanic waters and its conservative
external morphology can lead, in many cases, to
mistakes in the species identification (Nakaya &
Sato 1999). Just one species was recorded in the
Western South Atlantic, but it is possible that more
species do occur in Brazilian deep waters, since besides the factors above mentioned - the Brazilian
fishery fleet usually does not operate at the deep
waters where this genus usually occurs. Oceanic
deep sharks species comprise about 20 % of the total
shark species recorded in Brazilian waters, and
Scylorhinidae represents about 31 % of these
oceanic deep species (Gadig, 2001). Rincon &
Vooren (2006) also suggest that the increasing
fishing and research efforts in such environment
should provide more data on the poorly known
fishes. Additionally, taxonomic studies on these
Brazilian deep sea elasmobranchs can be considered,
aiming for a more consistent knowledgement on the
Brazilian elasmobranch fauna.
Ackowledgements
To A. Tomás and B. Mourato for the
donation of the specimen; D. Pagnoncelli and
Á. Mendes for taking the photographs; and to
K. Nakaya for sending his papers on Scyliorhinidae.
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Received October 2006
Accepted November 2006
Published online November 2006
Benthic macroinvertebrate bycatch in the snail Zidona dufresnei
(Donovan) fishery from the Uruguayan continental shelf
GUSTAVO RIESTRA1,2, JUAN PABLO LOZOYA1, GRACIELA FABIANO3, ORLANDO
SANTANA3 & DANIEL CARRIZO4
1
Dirección Nacional de Recursos Acuáticos, Montevideo-Uruguay. e-mail: [email protected]
Museo de Historia Natural “Dr. Carlos Torres de la Llosa”, Uruguay.
3
Dirección Nacional de Recursos Acuáticos, La Paloma-Uruguay.
4
Instituto de Investigaciones Químicas y Ambientales de Barcelona, Spain.
2
Abstract. The benthic macroinvertebrate fauna associated with the fishery of “caracol fino” Zidona
dufresnei (Mollusca, Gastropoda) was analysed during three fishery cruises in the Uruguayan continental
shelf. Species composition, richness, diversity and qualitative dominance were estimated from the
examination of the bycatch of 172 fishing hauls using a double bottom otter trawl. In the Uruguayan
Atlantic waters 55 species of macroinvertebrates were associated with Z. dufresnei, being molluscs and
crustaceans the dominant taxa in species number and frequency of occurrence. Two gastropods
(Adelomelon beckii and Tonna galea), two decapod crustaceans (Libinia spinosa and Propagurus
gaudichaudii), one asteroid (Astropecten brasiliensis), and one Actiniaria ind. were the most
representative species in the “caracol fino” bycatch. Further studies considering unexplored bathymetric
gradients are strongly recommended, they will help to fill our current gap in the knowledge of the
macrobenthic diversity in the Uruguayan continental shelf.
Key words: Benthic macrofauna, fauna associated, diversity, qualitative dominance, Uruguay.
Resumen. Captura incidental de macroinvertebrados bentónicos en la pesquería de caracol fino
Zidona dufresnei en la plataforma continental uruguaya. La fauna de macroinvertebrados bentónicos
asociada a la pesquería de “caracol fino” Zidona dufresnei (Mollusca, Gastropoda) en la plataforma
continental uruguaya fue estudiada en base a tres cruceros de pesca. Se determinó la composición y
riqueza específica, diversidad y dominancia cualitativa mediante el análisis de 172 lances efectuados con
red de arrastre de fondo. Se registraron 55 especies de macroinvertebrados asociadas a Z. dufresnei en el
Atlántico uruguayo, resultando los moluscos y los crustáceos los taxa dominantes en número y frecuencia
de ocurrencia. Dos gasterópodos (Adelomelon beckii y Tonna galea), dos crustáceos decápodos (Libinia
spinosa y Propagurus gaudichaudii), un asteroideo (Astropecten brasiliensis), y un Actiniaria ind. fueron
las especies más representativas en el bycatch del “caracol fino”. Se recomienda considerar nuevos
gradientes batimétricos a los efectos de profundizar en el conocimiento de la diversidad macrobentónica
en la plataforma continental uruguaya, en futuros estudios.
Palavras Clave: Macrofauna bentónica, fauna asociada, diversidad, dominancia cualitativa, Uruguay.
Introduction
Bottom trawling and the use of other active fishery
techniques disrupt marine bottoms in the same way
as logging affects forest ecosystems. Although it is
easy to recognize the effects of deforestation on
biological diversity and economic sustainability,
concern for the loss of marine benthic habitats as a
result of fishery is far less common. In fact, it was
not until the middle of 1980’s that marine biologists
started to foresee the potential effects of the
generalized disturbance of the sea floor due to the
growth in number and capacity of the fleet of bottom
trawlers (Watling & Elliot 1998).
Unrestricted fishery has different impacts on
marine ecosystems. Fishery has direct effects on
target species, reducing populations and stocks,
affecting body size composition, and in some cases
spawning biomass. Moreover, it has also indirect
Benthic macroinvertebrate bycatch in Zidona dufresnei Uruguayan fishery.
effects on predator-prey interactions, modifying
community structure, even generating temporal
alternative states. A genetic selection of certain size
classes and reproductive characteristics can also be
promoted, reducing or removing local stocks. Two
additional indirect perturbations associated with the
fishery are the bycatch or mortality of non-target
species, and the reduction of habitat complexity,
particularly by bottom trawling (Kaiser et al. 2001).
Coastal macrobenthic communities are
ecologically and economically important. They
provide a number of ecological services to mankind,
not restricted to their role in the nutrient and organic
matter recycling and as supporting biomass for
fishes (Caddy 1989).
Given their relevance, identification of
priority areas for marine conservation is critical, and
in order to do so, basic knowledge on macrobenthic
diversity is essential (Costello 1998). Exploratory
studies on macrobenthic spatial patterns will
contribute to a more responsible use of the marine
environment (Van Hoey et al. 2004). Unfortunately,
large portions of the coastal sea-bed, particularly in
the Southern Hemisphere, remain poorly described,
even in aspects as basic as species composition and
habitat associations. The knowledge on faunal
composition at the continental shelf will facilitate
the prediction of potential impacts resulting from the
development and growth of demersal fisheries, and
will help to identify species potentially important
from a socio-economic point of view.
Although several studies have described
benthic communities in the South Atlantic region
(Buckup & Thomé 1962, Olivier et al. 1968, Escofet
et al. 1978, Roux et al. 1993, Capitoli 1996, Klein et
al. 2001, Giberto et al. 2004), studies focusing on
the benthic associations in the Uruguayan shelf are
rather scarce (Juanicó & Rodríguez-Moyano 1975,
Milstein et al. 1976, Riestra 2000). Most of these
previous studies focused on specific groups such as
molluscs (Olivier & Scarabino 1972, Scarabino
1973, Layerle & Scarabino 1984), decapod
crustaceans (Itusarry 1984), echinoderms (Barattini
1938, Bernasconi 1966, Lucchi 1985) and
polychaetan annelids (Faget 1983). The focus of this
study encompasses an array of these invertebrates,
analyzing the benthic macroinvertebrates associated
with the marine gastropod Zidona dufresnei
(Donovan, 1823), a volutid snail locally known as
“caracol fino”, an important fishery resource in the
Uruguayan continental shelf.
105
Study Area
The study was carried out in the
north-eastern zone of the Uruguayan continental
shelf, between 34º20' - 35º22' Lat S and
52º47' - 54º53' Long W, which represents the
most important fishing grounds for Zidona dufresnei
in Uruguay (DINARA 1997). The snail’s fishing
area is 30 to 70 m deep (Fig. 1), with sandy, muddy,
and occasionally rocky bottoms. This zone
is influenced by the Malvinas and Brazil currents,
plus a significant flow of fresh water from the Río
de la Plata, which results in a peculiar
hydrographical system (Guerrero & Piola 1997,
Ortega & Martínez ‘in press’).
Figure 1. Portion of the Uruguayan continental shelf where
fishing operations were carried out.
Sampling and laboratory methods
A total of 172 fishing hauls were undertaken
during three commercial fishing trips (September
and November 2000, and May 2001), with scientific
observers from the National Direction of Aquatic
Resources (DINARA) on board (Fig. 1).
Commercial outrigger trawlers, rigged to tow one
bottom otter trawl on each outrigger, were used in
the
three
fishing
trips
where
benthic
macroinvertebrate samples were taken (FAO 2005).
The trawls employed in the Z. dufresnei fishery had
a 100 mm mesh size between opposed knots, a
mouth framed by a headline with floats providing a
maximum vertical opening of 1.5 m and a ground
gear with chains, designed according to the bottom
condition to maximize the catches and protect the
gear from damage.
Samples of the benthic macroinvertebrate
bycatch were taken along each one of the three
G. RIESTRA ET AL.
106
campaigns and from each fishing haul, labelled and
fixed in 10% formaldehyde. Afterwards, in the
laboratory, the organisms collected were identified
to the lowest possible taxonomic level, in most of
the cases to species level. Sampling location (GPS),
depth, speed and tow’s duration were also registered
for each fishing haul. The total swept area (square
nautical miles: nm2) in each campaign was
calculated using the vessel speed, the maximum
horizontal gear opening and the duration of each
trawl.
Data analyses
Mean species richness (Sm) for each
trip was obtained from the species richness of
each haul, based on the number of benthic
macroinvertebrate species obtained. Mean diversity
(Shannon-Weaver 1979: H’m) for each campaign
was also calculated, using the diversity of each haul.
A Chi-square test (χ2) was performed to test for
differences in Sm and H’m between fishing trips
(Zar 1999).
The relative importance of the different
species in the three trips combined was assessed
using Qualitative dominance (Bouderesque 1971)
according to the frequency of occurrence (%).
Five categories were defined by this author:
occasional (0-20%), scarce (21-40%), common (4160%), abundant (61-80%) and very abundant (81100%).
Based on the presence-absence species
matrix, and employing a Similarity Coefficient (Qmode), the similarity between species was calculated
for each trip. An Unweighted Pair Group Method for
Arithmetic averages (UPGMA) (Legendre &
Legendre 1979) was applied as a technique of
average linking.
Results
The mean duration of campaigns was
13 days, with a maximum number of fishing hauls
in September and May (59 hauls) and a minimum in
November (54 hauls). Mean haul duration (± SE)
was shorter in May (3.14 ± 0.12 hours) than in
November (3.38 ± 0.49 hours) and September
(3.45 ± 0.46 hours). The shortest (1.00 hour) and the
longest (4.35 hours) hauls occurred in May.
However, mean haul speed (± SE) was faster
in November (3.1 ± 0.13 knots) than in May
(2.8 ± 0.08 knots) and September (2.8 ± 0.15 knots).
The bottom swept area was larger in November
(6.9 nm2) than in May (5.9 nm2) and September
(5.8 nm2).
Bycatch
The macroinvertebrate bycatch associated
with the snail Zidona dufresnei fishery in the
Uruguayan continental shelf included 55 species
(data of all trips combined). These species belong to
5 phyla (Table I and II): mollusks (45%) and
arthropods (36%) were the most represented,
followed by echinoderms (7%), cnidarians (7%) and
annelids (6%).
Species richness and diversity
The total number of species (S) identified
in September 2000 (S = 33 species) was larger than
in November 2000 (S = 31 species) and May 2001
(S = 25 species). However, the total number of
species, the mean species richness and the mean
diversity did not differ significantly among
campaigns (Table II).
Qualitative dominance
Based on data of the three campaigns
combined, the very abundant category was
composed of the exploited target species
Z. dufresnei (98%), Libinia spinosa Milne-Edwards,
1834 (89%) and Adelomelon beckii (Broderip, 1836)
(87%). Tonna galea (Linnaeus, 1758), Propagurus
gaudichaudii Milne-Edwards, 1836, Actiniaria ind.
and Astropecten brasiliensis Müller & Troschel,
1842, were abundant, 4 species were common,
7 were scarce and 37 were occasional (Table III).
Other species with very low occurrence
(scarcely present in one haul), were not considered
for this analysis: Astrangia rathbuni Vaughan, 1906,
Aequipecten
tehuelchus
d’Orbigny,
1842,
Lithophaga
patagonica
(d’Orbigny,
1842),
Pododesmus rudis (Broderip, 1834), Pteria
hirundo (Linnaeus, 1758), Transenpitar americana
(Doello-Jurado, 1951), Bostrycapulus aculeatus
(Gmelin, 1791), Crepidula sp., Polystira
formosissima (E. A. Smith, 1915), Balanidae ind.,
Heterosquilla platensis (Berg, 1900), Corystoides
chilensis Lucas, 1844, Leucippa pentagona
Milne-Edwards, 1833, Ovalipes trimaculatus
(De Haan, 1933), Pinnotheres sp. and Portunus
spinicarpus (Stimpson, 1871).
Similarity
Based on the cluster analysis, the highest
similarity (> 93%) was found between Z. dufresnei,
L. spinosa and A. beckii for both September (Fig. 2a)
and November (Fig. 2b) campaigns. However, in
May 2001, the highest similarity (90%) was
found between the fishing target species and T.
galea (Fig. 2c). Considering a level of similarity
107
Table I - Species composing of the benthic macroinvertebrate bycatch of the snail Zidona dufresnei fishery
in the Uruguayan continental shelf.
Phylum Cnidaria
Class Anthozoa
Alcyonaria ind.
Antholoba achates (Drayton, 1846)
Astrangia rathbuni Vaughan, 1906
Phlyctenanthus australis Carlgren, 1950
Phylum Annelida
Class Polychaeta
Aphrodita longicornis Kingberg, 1855
Phyllochaetopterus socialis Claparède, 1870
Polychaeta ind.
Phylum Mollusca
Class Polyplacophora
Chaetopleura angulata (Spengeler, 1797)
Class Bivalvia
Aequipecten tehuelchus d’Orbigny, 1842
Corbula patagonica d’Orbigny, 1846
Ennucula uruguayensis (E.A. Smith, 1885)
Lithophaga patagonica (d' Orbigny, 1842)
Mytilus edulis Linnaeus, 1758
Ostrea puelchana d' Orbigny, 1842
Panopea abbreviata Valenciennes, 1839
Pitar rostratus (Koch, 1844)
Pododesmus rudis (Broderip, 1834)
Pteria hirundo (Linnaeus, 1758)
Trachycardium muricatum (Linnaeus, 1758)
Transenpitar americana (Doello-Jurado, 1951)
Class Gastropoda
Adelomelon beckii (Broderip, 1836)
Adelomelon brasiliana (Lamarck, 1811)
Buccinanops cochlidium (Dillwyn, 1817)
Bostrycapulus aculeatus (Gmelin, 1791)
Crepidula sp.
Cymatium parthenopeum (von Salis, 1793)
Polystira formosissima (E.A. Smith, 1915)
Prunum martini (Petit, 1853)
Tonna galea (Linnaeus, 1758)
Zidona dufresnei (Donovan, 1823)
Class Cephalopoda
Loligo sanpaulensis Brakoniecki, 1984
Octopus tehuelchus d’ Orbigny, 1834
Phylum Echinodermata
Class Asteroidea
Asterina stelliffer (Möbius, 1859)
Astropecten brasiliensis Müller & Troschel, 1842
Luidia sp.
Class Ophiuroidea
Ophiuroidea ind.
Phylum Arthropoda
Class Crustacea
Balanidae ind.
Callinectes sapidus Rathbun, 1896
Corystoides chilensis Lucas, 1844
Farfantepenaeus paulensis (Pérez-Farfante, 1967)
Hepatus pudibundus (Herbst, 1785)
Heterosquilla platensis (Berg, 1900)
Leucippa pentagona Milne-Edwards, 1833
Leurocyclus tuberculosus Milne-Edwards & Lucas, 1842
Libinia spinosa Milne-Edwards, 1834
Metanephrops rubellus (Moreira, 1905)
Ovalipes trimaculatus (De Haan, 1933)
Propagurus gaudichaudii Milne-Edwards, 1836
Peltarion spinosulum (White, 1843)
Persephona mediterranea (Herbst, 1794)
Pinnotheres sp.
Platyxanthus crenulatus Milne-Edwards, 1879
Platyxanthus patagonicus Milne-Edwards, 1879
Pleoticus muelleri (Bate, 1888)
Portunus spinicarpus (Stimpson, 1871)
Scyllarides deceptor Holthuis, 1963
of 80%, the Actiniaria ind. and Buccinanops
cochlidium were added to the original group, and an
association between Octopus tehuelchus and A.
brasiliensis appeared in September 2000 (Fig. 2a).
Propagurus gaudichaudii, Pitar rostratus, T. galea,
Ostrea puelchana and A. brasliensis were included
in the initial similarity group in November 2000
(Fig. 2b), and P. gaudichaudii and L. spinosa were
incorporated to the initial group in May 2001
(Fig. 2c). Considering a 60% similarity level,
the same seven species were associated in the
three campaigns: Z. dufresnei, A. beckii, T. galea,
L. spinosa, P. gaudichaudii, A. brasiliensis and
Actiniaria ind. (Figs. 2 a, b and c).
Discussion
Some methodological constraints must be
considered before the discussion of the results. The
objective of the fishing campaigns and mainly the
sampling procedure employed, which only caught
large macroepifauna (> 50 mm), not allow a
comparison with previous studies in the region.
The 55 species of benthic macroinvertebrates that form the bycatch of the snail
Z. dufresnei’s fishery on the Uruguayan
continental shelf represent a lower species richness
than for other areas of the Southeastern
Atlantic region already described, such as the
southern Brazilian Atlantic littoral (Klein et al.
2001), the Rio de la Plata estuary and adjacent shelf
G. RIESTRA ET AL.
108
Table II - Mean species richness (Sm ± SE), mean diversity (H’m ± SE), associated χ2 test statistics, and
phyla composition (%) of the bycatch of the three fishing campaigns.
Mean species richness
Mean diversity
Mollusca
Arthropoda
Phyla
Echinodermata
composition
Annelida
Cnidaria
Sep 2000 Nov 2000 May 2001
12 ± 3.6
11 ± 2.5
9 ± 2.9
χ2 = 1.17; P = 0.56
2.5 ± 0.3 2.3 ± 0.3
2.2 ± 0.3
χ2 = 0.02; P = 0.99
43
46
52
33
32
28
9
13
8
9
6
8
6
3
4
waters (Giberto et al. 2004), and the Mar del Plata
(Argentina) region (Roux et al. 1993). It must be
taken into account that the lack of previous studies
in the region, regarding the macrobenthic bycatch in
the
Z.
dufresnei’s
fishery,
does
not
allow an adequate comparison. Nevertheless, the
Shannon-Weaver diversity index obtained for the
Uruguayan continental shelf was in agreement with
those documented for the Argentinean zone (Roux et
al. 1993, Roux & Bremec 1996).
The macroinvertebrate community defined
as the bycatch of the Z. dufresnei’s fishery showed
faunal components of warm-temperate (e.g.,
H. platensis, L. pentagona and P. muelleri) and
cold-temperate regions (e.g., P. gaudichaudii and P.
spinosulum) (Boschi et al. 1992). This could be
explained by the convergence of different water
masses with contrasting thermohaline that
characterize the Uruguayan continental shelf
(Ortega & Martínez ‘in press’). Tropical Water
carried southward by the Brazil Current
(Sverdrup et al. 1942), Subantarctic Water advected
northwards by the Malvinas Current (Bianchi et al.
1993) and Coastal Waters mainly from the Rio de la
Plata estuary, result in this peculiar hydrographical
system (Guerrero & Piola 1997, Ortega & Martínez
‘in press’).
The highest qualitative dominance values
corresponding to molluscs and crustaceans
are in agreement with those found for the
Argentinean and Brazilian continental shelves
(Bastida et al. 1992, Roux et al. 1993, Roux &
Bremec 1996, Bremec & Roux 1997, Klein et al.
2001), although those authors used different
sampling methods.
To
characterize
the
macrobenthic
invertebrates associated with the snail Z. dufresnei in
the Uruguayan continental shelf, six species with a
coefficient of similarity higher than 60% were
chosen: two gastropod molluscs (A. beckii and
T. galea), two decapod crustaceans (L. spinosa and
P. gaudichaudii), one asteroid echinoderm
(A. brasiliensis) and one Actiniaria ind. These
results agree partially with those of Buckup &
Thomé (1962), who considered Z. dufresnei,
L. spinosa and Adelomelon brasiliana as very
frequent species in the Rio Grande do Sul
continental shelf (Brazil) between 20 and 50 m deep.
In the present study, A. brasiliana did not follow
that association, being classified as an occasional
species.
Despite L. spinosa and the hermit crab
Dardanus arrosor insignis were documented as very
frequent species for that zone by Itusarry (1984),
only the first one was founded in our study. The
unexpected absence of this hermit crab could be
partially ascribed to a potential error in the
identification of the hermit crabs. In the other hand,
the frequent occurrence of A. brasiliensis is in
agreement with the results of Juanicó & RodríguezMoyano (1975) for the south-eastern zone of La
Paloma (Rocha, Uruguay), where it was the second
faunal component, only preceded by Mytilus edulis,
between 35 and 50 m deep. This asteroid was also
very well represented in the Euvola ziczac shell
banks at the Brazilian south coast (20 to 50 m depth)
(Klein et al. 2001). The very low frequency obtained
for Mytilus platensis, Lithophaga patagonica,
Bostrycapulus aculeatus, and Chaetopleura isabellei
could be explained by the fact that these species are
highly associated with hard bottoms (Roux et al.
1993), where the Uruguayan Z. dufresnei fishery
does not operates.
A biological association between the snail
B. cochlidium and the actinian Phlyctenanthus
australis, described by Pastorino (1993) for
Patagonian coastal waters (Argentina), was also
observed in our study. Other associations that were
109
Table III - Qualitative Dominance (%) (Bouderesque, 1971) of each species and their corresponding
phylum: (A) Arthropoda, (An) Annelida, (C) Cnidaria, (E) Echinodermata, (M) Mollusca.
Category
Very Abundant
Abundant
Common
Scarce
Occasional
Species
Zidona dufresnei
Libinia spinosa
Adelomelon beckii
Tonna galea
Propagurus gaudichaudii
Actiniaria ind.
Astropecten brasiliensis
Buccinanops cochlidium
Aphrodita longicornis
Platyxanthus crenulatus
Octopus tehuelchus
Pitar rostratus
Asterina stellifer
Platyxanthus patagonicus
Phyllochaetopterus socialis
Leurocyclus tuberculosus
Ostrea puelchana
Farfantepenaus paulensis
Loligo sanpaulensis
Cymatium parthenopeum
Metanephrops rubellus
Mytilus edulis
Peltariom spinosulum
Chaetopleura angulata
Luidia sp.
Adelomelon brasiliana
Panopea abbreviata
Trachicardium muricatum
Ophiuroidea ind.
Persephona mediterranea
Ennucula uruguayensis
Ovalipes trimaculatus
Pleoticus muelleri
Polychaeta ind.
Alcyonaria ind.
Astrangia rathbuni
Aequipecten tehuelchus
Balanidae ind.
Bostrycapulus aculeatus
Callinectes sapidus
Corbula patagonica
Crepidula sp.
Corystoides chilensis
Hepatus pudibundus
Heterosquilla platensis
Leucippa pentagona
Lithophaga patagonica
Pinnotheres sp.
Pododesmus rudis
Polystira formosissima
Portunus spinicarpus
Prunum martini
Pteria hirundo
Transenpitar americana
Scyllarides deceptor
Phylum
M
A
M
M
A
C
E
M
An
A
M
M
E
A
An
A
M
A
M
M
A
M
A
M
E
M
M
M
E
A
M
A
A
An
C
C
M
C
M
A
M
M
C
A
A
C
M
C
M
M
C
M
M
M
A
Qualitative dominance (%)
98.3
89.2
86.6
74.7
74.0
71.0
68.1
56.3
55.4
48.8
43.1
39.4
35.8
33.5
33.1
31.5
24.6
23.1
17.2
13.6
11.6
10.0
9.6
8.9
6.2
5.5
4.9
4.0
3.1
2.4
1.7
1.7
1.7
1.2
1.1
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
G. RIESTRA ET AL.
110
T .g a le a
A .lo n g ic o rn is
Z .d u fr e s n e i
L .s p in o s a
A .b e c k ii
A c t in ia r ia in d .
B .c o c h lid iu m
O .t e h u e lc h u s
A .b ra s ilie n s is
P .g a u d ic h a u d ii
O .p u e lc h a n a
P .c re n u la tu s
L .s a n p a u le n s is
L .tu b e r c u lo s u s
F .p a u le n s is
P .s o c ia lis
C .p a r th e n o p e u m
A .s te llife r
P .r o s tr a tu s
P .s p in o s u lu m
M .r u b e llu s
M .e d u lis
P .p a ta g o n ic u s
P .a b b re v ia ta
C .a n g u la ta
P .m e d ite rr a n e a
A .b ra s ilia n a
P in n o th e re s s p .
S .d e c e p t o r
O p h iu r o id e a in d .
T .m u r ic a tu m
A lc y o n a r ia in d .
H .p u d ib u n d u s
a
0
20
40
60
80
100
b
0
M .edulis
M .rubellus
T .m uricatum
E .uruguayensis
P .m uelleri
F .paulensis
O .tehuelchus
P .crenulatus
A .longicornis
.m agna
Z .dufresnei
A .beckii
L.spinosa
P .gaudichaudii
.gaudichaudi
P .rostratus
T .galea
O .puelchana
A .brasiliensis
P .patagonicus
A .stellifer
Luidia sp.
C .parthenopeum
C .socialis
P
ephalodiscus sp.
O .trim aculatus
A lcyonaria ind.
C .patagonica
L.sanpaulensis
C .sapidus
O phiuroidea ind.
C .angulata
A .brasiliana
P .m editerranea
20
40
60
80
c
0
100
F.paulensis
F.
C.angulata
C.
C.partenopheum
C.
P.m artini
P.
P.spinosulum
m
artini
P.
M .edulis
M
.
O.tehuelchus
O
.
B.cochlidium
B.
P.crenulatus
P.
A.brasiliensis
A.
A.stellifer
A.
Z.dufresnei
Z.
T.galea
T.
P.gaudichaudii
P.
L.spinosa
L.
Actiniaria
ind.
Anthozoa
A.beckii
A.
L.tuberculosus
L.
A.longicornis
A.
P.socialis
Cephalodisc
O.puelchana
O
.
M .rubellus
M
.
P.abbreviata
P.
A.brasiliana
A.
P.rostratus
P.
20
40
60
80
100
Fig. 2 - Species dendrogram (UPGMA). Dotted vertical line represents the 90% of similarity between species: a) September 2000, b)
November 2000 and c) May 2001.
already observed for Argentinean waters were also
found in the Uruguayan continental shelf:
A. brasiliana and the actinia Antholoba achates
(Luzzatto & Pastorino 2006) and Libinia spinosa
with A. achates (Acuña et al. 2003).
Even if in the last years the number of
vessels in the fishery of “caracol fino” has
substantially diminished, the fishery is still open and
the bottom is still heavily trawled. Fishing gears
alters seafloor habitats and understanding the extent
of these impacts, and the effects on populations of
living marine resources, is needed to properly
manage current and future levels of fishing effort
(Auster et al. 1996). The knowledge of the
macroinvertebrate diversity results essential for a
sustainable fisheries management and the
development of potentially valuable resources.
Because of the lack of pristine sites, where the use of
active fishing is prohibited, no empirical studies that
could demonstrate population level effects of bottom
trawling, have been conducted so far. If marine
fisheries management is to evolve toward an
ecosystem or habitat management approach,
experiments are required on the effects of habitat
change, both anthropogenic and natural (Auster et
al. 1996). According to the current gap in the
knowledge of macrobenthic diversity in the
Uruguayan continental shelf, further investigations
concerning unexplored bathymetric gradients with
systematic samplings and experiments are strongly
recommended.
Acknowledgments
The authors wish to thank the collaboration of the
fishing companies as well as to the captains and
crews of the snail vessels. We also express our
sincere thanks to F. Scarabino for his comments on
the determination of species and for bibliography.
We also gratefully acknowledge Dr. M. Zamponi for
his identification of the actinian. The authors want to
thank Dr. E. Spivak, Dr. P. Quijón, Dr. S. Acevedo
and Dr. McCormark for the critical revision of the
manuscript and especially to Dr. Alexandre García
and Dr. Gonzalo Velasco, Editorial Board of PanAmerican Journal of Aquatic Sciences.
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Received June 2006
Accepted October 2006
Published online December 2006
Feeding Ecology of Nereis diversicolor (O.F. Müller) (Annelida,
Polychaeta) on Estuarine and Lagoon Environments
in the Southwest Coast of Portugal
PEDRO FIDALGO E COSTA 1, 2, RUI F. OLIVEIRA 3 & LUÍS CANCELA DA FONSECA 2, 4
1
Escola Superior de Educação João de Deus, Av. Alvares Cabral, 69, P - 1269-094 Lisboa, Portugal, e-mail:
[email protected]
2
IMAR/Laboratório Marítimo da Guia, Estrada do Guincho, P - 2750-642 Cascais, Portugal.
3
Unidade de Investigação em Eco-Etologia, Instituto Superior de Psicologia Aplicada, R. Jardim do Tabaco 44, P 1149-004 Lisboa, Portugal.
4
FCMA, Universidade do Algarve, Campus de Gambelas, P - 8005-139 Faro, Portugal.
Abstract. The feeding ecology of Nereis diversicolor (O. F. Müller, 1776) (Annelida: Polychaeta) was
studied over 14 months at three estuarine-lagoon systems of the Southwest coast of Portugal (Odeceixe,
Aljezur and Carrapateira). The analyses of digestive tract revealed that diet change according to site,
period of the year and individual sizes. There are no differences in the digestive contents between sexes.
In all sampling stations a total of thirty items were found, but only five shown an occurrence superior to
1%. These were: mucus (56.3%), sand (17.6%), vegetable detritus (10.7%), Nereididae (7.7%) and
Corophium sp. (1.8%). N. diversicolor was detected in all sampling stations with a filter-feeding
behaviour, although in Carrapateira there is evidence of slightly higher carnivore behaviour than in
Odeceixe and Aljezur. Mucus (a food complex including organic matter, bacteria, fungi and
phytoplankton) was the main gut content.
Key words: Seaworms, “common ragworm”, feeding behaviour, diet, brackish environments.
Resumo. Ecologia Alimentar de Nereis diversicolor (O.F. Müller) (Annelida, Polychaeta) em
Ambientes Estuarino-Lagunares da Costa Sudoeste de Portugal. A ecologia alimentar de Nereis
diversicolor (O.F. Müller, 1776) (Annelida: Polychaeta) foi estudada num período de 14 meses em três
sistemas estuarino-lagunares da costa Sudoeste de Portugal (Odeceixe, Aljezur e Carrapateira). A análise
do conteúdo digestivo revelou uma variação da dieta de acordo com os locais estudados, época do ano e
com o tamanho dos indivíduos. Não houve diferenças nos conteúdos de machos e fêmeas. Foram
encontrados em todas as estações amostradas um total de trinta itens, mas apenas cinco revelaram uma
ocorrência superior à 1%. Estes foram: muco (56.3%), areia (17.6%), detritos vegetais (10.7%),
Nereididae (7.7%) e Corophium sp. (1.8%). N. diversicolor evidenciou hábitos filtradores, em todas as
estações amostradas embora na Carrapateira tenham sido detectadas percentagens de carnivoría
ligeiramente superiores às encontradas em Odeceixe e Aljezur. O principal conteúdo do tracto digestivo
foi o muco (complexo alimentar que aglutina matéria orgânica, bactérias, fungos e fitoplâncton).
Palavras-chave: Poliquetas, “minhocas-da-pesca”, comportamento alimentar; dieta, sistemas salobros.
Introduction
The polychaeta Nereis diversicolor (O. F. Müller,
1776) is widely distributed in estuarine and lagoonal
habitats from North Africa to the North of Europe
(Mettam 1979, 1981, Gillet 1993). The species
shows high physiological tolerance to extreme
variations in environmental factors, and can grow
and reproduce in different sediment types and in
stressed environments (Bartels-Hardege & Zeeck
1990, Cheggour et al. 1990, Miron & Kristensen
1993, Zubillaga & Salinas 1997, Scaps 2002).
It not only adapts well to a variety of
environments, but also its feeding habits are quite
generalist. N. diversicolor has a wide capacity
Feeding Ecology of Nereis diversicolor.
115
regarding the size of food it feeds upon, which
ranges from micro and macrozoobenthos, diatoms,
to fragmented organic matter including detritus
(Gorke 1971, Reise 1979, Witte & Wild 1979, Smith
et al. 1996, Lucas & Bertru 1997). This species can
also uses different strategies to capture its food: i)
deposit feeding, capturing its food on the sediment
surface and around the gallery (Esselink & Zwarts
1989, Esnault et al. 1990); ii) suspension feeding,
releasing a web of mucus in the gallery and through
dorsal-ventral movements, it generates a continuous
current capturing the phytoplankton in the web to be
ingested afterward (Harley 1950, Well & Dales
1951, Riisgård 1991, Vedel 1998). It adopts this
feeding strategy when the water column presents a
high concentration of phytoplankton (Vedel &
Riisgård 1993); iii) herbivore, it is able to ingest
parts of algae and aquatic macrophytes (Olivier et al.
1996, Hughes et al. 2000); iv) carnivore, playing an
important role in the structure of brackish water
ecosystems, because it acts as a predator of different
bottom fauna species (Rönn et al. 1988). These
strategies seem to be related to food availability and
quality, presence or absence of predators, tidal
height and season (Esselink & Zwarts 1989, Masson
et al. 1995).
Nereis diversicolor, searched as live food or
bait by aquaculture and sport fishing activities, is
also an important species to the structure of the food
webs of another lagoonal environment of Portuguese
Southwest coast (Cancela da Fonseca 1989,
Bernardo 1990). As a part of a research project
dealing with the biology and ecology of this species
(Fidalgo e Costa et al. 1998, Fidalgo e Costa et al.
2002), the analysis of the monthly variation of its
digestive tract contents was carried out in order to
assess its feeding patterns and so, its trophic position
in the wild. In addition the type of food ingested by
the different size classes, as well as by different
sexes, was also investigated.
estuaries (Figure 1), with water basins of about 250,
200 and 110 km2 respectively, which partially drain
the Western part of Southwest Portugal. According
to Day et al. (1987), these types of brackish
environments, although representing a great
geomorphological diversity are from an ecological
point of view lagoon-estuarine ecosystems.
The sampling stations (two for Odeceixe,
three for Aljezur and for Carrapateira) have the
highest occurrences of N. diversicolor according to
previous studies conducted in those systems
(Magalhães et al. 1987, Magalhães 1988). To
facilitate the statistical work and also to keep the
initial goal of comparing the different brackish
environments, it was decided to combine and
analyse all data per sampling site (ODX, ALZ and
CAR) with no specific reference to the sampling
stations, within each site. These are arranged in a
North-South geographic position in which ODX is
the sampling site located further north and CAR the
sampling site further south. The distance between
these two areas is approximately 35 km.
Field and laboratory work
Monthly data on rainfall, water salinity, near
sediment salinity and temperature, and sediment
organic matter, chlorophyll a and phaeopigments
were obtained to characterize the environmental
conditions of each site. Salinity and temperature
values were measured in situ at each station. Surface
and near sediment salinity values were obtained
in order to evaluate fresh water inputs.
Study Area
The studied sites are located inside a natural
protected area (the Sudoeste Alentejano and Costa
Vicentina Nature Park – PNSACV), in which they
constitute vital habitats for many species, much of
them aquatic birds. It is also one of the best
preserved coastal areas in Europe with high
landscape, geological and biodiversity richness
(Silva e Costa et al. 1983). The sampling stations
were established at the lower part of Odeceixe
(ODX), Aljezur (ALZ) and Carrapateira (CAR)
Figure 1 – Map of Portugal and the soutwestern coast showing
the sampling sites (black dotes).
P. FIDALGO E COSTA ET AL.
116
Rainfall values were obtained from the National
Meteorological Institute and General Administration
of Natural Resources. Organic matter, chlorophyll a
and phaeopigments of sediment were determined on
the top centimetre of sediment samples obtained in
each station with a 5 cm diameter corer and were
frozen until laboratory analysis (Fidalgo e Costa et
al. 2002).
All specimens of N. diversicolor used in this
work were collected between April 1993 and May
1994: i) at low tide in the sublittoral fringe (the
upper subtidal layers in a tidal environment) at the
lower part of ODX and ALZ; ii) in the sublittoral
area (the upper submerged layers in a non-tidal
environment) of CAR, in a small coastal lagoon
formed by the partial closing of a sandy barrier near
the beach. For each station, a total sampling area of
2
0.1m was obtained by five sub-samples of 30 cm
depth, using a 0.02 m2 hand corer. The samples were
then sieved through a 0.5 mm square mesh and the
remaining fraction was kept in 10% formalin
buffered with borax. In the laboratory, samples were
washed in order to extract the excess of formalin and
sediment. The remainder was dipped into a saturated
saccharose solution, which separates the organic
from the inorganic matter by flotation (Cancela da
Fonseca 1989, Caron et al. 1993). All samples were
then kept in 70º alcohol (Möller 1985).
Some of the captured animals were too small
to be dissected while others had no digestive tract
contents due to damages during sampling. Therefore
the guts of 3000 animals were observed but, from
these, 907 (30%) had any content (220 in ODX, 460
in ALZ and 227 in CAR).
All individuals were measured, based on the
length of L3 (length of prostomium, plus
peristomium and 1st chaetiger) according to Gillet
(1990, 1993). This measure presented the best
correlation with the biomass (Fidalgo e Costa et al.
1998) being a good conversion factor (dry weight
(mg) = 1.982 (L3, mm)3.479 , N=259, r2=0.914,
p<0.001). All measurements were performed using a
camera lucida and digitising table (Houston
Instruments HiPad) linked to a PC. For the practical
purposes of this study, and according to the previous
results on cohort analysis (Fidalgo e Costa et al.
1998), three basic sizes were established (small (S1),
medium (S2) and large (S3)), being represented by a
L3 measure, respectively, of [0.3, 1.5 mm [, [1.5, 3.0
mm [ and [3.0, 4.5 mm].
The collection of digestive tract content was
done after opening individuals with iris scissors,
from the first to the last chaetiger. The material was
then placed in a Petri dish and observed with a
binocular stereomicroscope and, when necessary, a
compound microscope. The identification of the
found food items was narrowed down to the lowest
possible taxonomic level. Due to the conditions of
gut material, we chose to represent individual results
as percentage of occurrence. For each month the
data were analysed as frequency of occurrence
according to the following formula:
number of digestive tract with a certain item
× 100
number of digestive tract with the observed content
Sex was determined when the individuals
were opened to extract out the tract contents.
Observation of the oocytes and the sperm plates was
performed using binocular microscopes and the total
sex ratio found in ODX, ALZ and CAR was always
female biased, being, respectively, 1:2.9, 1:3.1 and
1:4.1 (Fidalgo e Costa, 2003).
From sediment samples, pigments were
extracted with 90 % acetone during 24 h in darkness
at 4º C, and subsequently centrifuged. Chlorophyll a
(surface Chl a is generally used as an index of
microphytobenthos biomass) and phaeopigments
were determined spectrophotometrically by the
method of Lorenzen (1967) adapted by Plante-Cuny
(1974) and results expressed as mg m-2.
The organic matter content of the superficial
layer of sediment was estimated through the loss on
ignition, a method that, according to Duck (1986),
provides a close estimate of the total organic matter
expressed in g m-2.
Data analysis
The proportions of different food items
ingested per individual were compared between the
sexes using T-tests and among size classes (large,
medium, small) using one-way ANOVA (each food
item was analysed separately). In both cases the
variables conformed to the assumptions of
parametric statistics of normality and homogeneity
of variances was investigated by normal probability
plots and Levene’s test respectively (Zar 1984,
Underwood 1997).
For the statistical analysis of seasonal effects
and due to the scarcity of gut contents in some
months, the data from the different months were
merged into four seasons: spring (April and May
1993; March, April and May 1994), summer (June,
July and August 1993), autumn (September, October
and November 1993) and winter (December 1993;
January and February 1994).
Spatial (Odeceixe vs. Aljezur vs.
Carrapateira) and seasonal (Spring vs. Summer vs.
Autumn vs. Winter) effects in the proportion of food
117
items ingested were investigated using two-way
ANOVA after transforming the data (arc-sin of the
square root) to match the assumptions of ANOVA
(Underwood 1997), followed by planned
comparisons to identify the significant differences in
the same site along different seasons or among the
three sites in the same season (Zar 1984, Underwood
1997). A similar analysis (i.e. two-way ANOVA
followed by planned comparisons) was performed
for the abiotic factors measured. Of the abiotic
factors, only salinity and temperature values were
log-transformed to meet the assumptions of ANOVA
(Underwood 1997). In order to evaluate which
groups differed significantly from each other posthoc HSD tests for samples with different sizes were
used with a p-level of 0.05 –. All descriptive
statistics were expressed as mean ± standard error of
the mean. All statistical tests were performed using
software package Statistica for Windows v. 5.0,
from Statsoft.
mg.m-2, n = 24) and winter (113±17.6 mg.m-2,
n = 24) (post-hoc HSD test, p<0.05).
The chlorophyll degradation represented
by phaeopigment values (Figure 3B), emphasise
when (months) and where (sites) accumulation of
detritus of plant or microalgae cell occur. The
ANOVA showed only a site effect (F2,100 = 7.97,
p<0.001).
The sediment organic matter (Figure 3C) is
related to grain size composition in the different
sampling sites. The ANOVA showed no significant
differences between sites (F2,100 = 2.19, p = 0.12) and
season of the year (F3,100 = 0.60, p = 0.62).
Results
Abiotic factors and phytopigments
Monthly water temperature values showed
a variation according to the normal annual behaviour
of this parameter (Figure 2). The ANOVA revealed
an effect of the sampling site (F2,99 = 30.76, p<0.001)
and of the season (F3,99 = 77.50, p<0.001).
Significant differences on temperature stress a site
effect with CAR presenting the highest value
and ODX the lowest (ODX:15.6 ± 0.52 ºC, n = 42;
ALZ: 17.5 ± 2.07 ºC, n = 42; CAR: 19.5 ± 0.62 ºC,
n = 28) (post-hoc HSD test, p<0.05). There
is also an effect caused by seasonality (Spring:
21.3 ± 2.1 ºC, n = 40; Summer; 21.6 ± 0.7 ºC,
n = 24; Autumn; 15.7 ± 0.5 ºC, n = 24; Winter:
13.7 ± 0.3 ºC, n = 24 - post-hoc HSD test, p<0.05).
Salinity values reflect tidal influence,
rainfall and river flow, which is observed
through constant stratification throughout the
year (Figure 2), especially in spring and winter
at sites ODX and ALZ. ANOVA undoubtedly shows
an effect of the sampling site (F2,99 = 10.14, p<0.001)
due to differences in bottom salinity between
CAR (15.0 ± 1.2, n = 42) and the other sampling
sites (ODX – 31.8 ± 0.89, n = 28; ALZ – 30.0 ± 2.8,
n = 42) (post-hoc HSD test, p<0.05).
Sediment chlorophyll a reveals temporal
variation (F3,100= 3.46, p = 0.02), associated with
the amount of fresh water brought by rain and
in particular by the continental runoff that
penetrates the system (Figure 3A). Significant
variations occurred between summer (59.8±9.90
Figure 2 – Monthly rainfall on the south-western coast of
Portugal (A). Monthly values of salinity (surface and bottom)
and temperature in ODX (B), ALZ (C) and CAR (D).
118
Spatial and seasonal diet variations
A total of 30 items were found in
gut contents for all sampling sites (Table I).
However, from this total only five showed a
frequency of occurrence higher than 1%. These
items were: mucus (56.3%), sand (17.6%), vegetable
detritus (10.7%), Nereididae (7.7%) and Corophium
sp. (1.8%).
The results for feeding habits of
N. diversicolor in all sampling stations clearly
show the ingestion of various food items, with
differences in occurrence of these items between
sites and during the year (Figure 4).
Figure 4 – Different items ingested by N. diversicolor in all
sampling stations clearly showing the ingestion of various food
items, with differences in occurrence of these items between
sites and during the year.
Figure 3 – Sediment values of chlorophyll a (A),
phaeopigments (B) and organic matter content (C) in ODX,
ALZ and CAR during the sampling period.
ANOVA showed an effect of sampling
site (F2,895 = 4.65, p = 0.001) and of the season
(F3,895 = 3.10, p = 0.03) on the percentage of mucus.
There was also an effect of the interaction between
the two independent variables (F6,895 = 2.33, p =
0.03), showing that mucus seems to be the most
important item during spring/summer periods,
mainly in what concerns ODX and CAR The effect
of sampling site is due to differences between
CAR (50 ± 2.37 %, n = 227), with more lagoonal
characteristics, and the two remaining sampling sites
(ODX: 61.3 ± 2.17 %, n = 220; ALZ: 56.8 ± 1.54 %,
n = 460) (post-hoc HSD test, p<0.05). On the other
hand, the effect of season was determined by the
differences between winter (47.7 ± 3.01 %, n = 156)
and the other three seasons of the year (spring: 58.4
± 1.68 %, n = 383; summer: 59.5 ± 2.0 %, n = 205;
autumn: 58.6 ± 2.84 %, n = 163) (post-hoc HSD test,
p<0.05). The interaction effect was due to
differences between autumn and summer in CAR,
and between CAR and ALZ in winter (post-hoc
HSD test, p<0.05).
There were no significant differences
between sampling sites concerning the amount of
ingested sand (F2,895 = 1.60, p = 0.20). However for
this variable, noteworthy differences related to
season (F3,895 = 5.06, p = 0.002) and interaction
(F6,895 = 4.64, p<0.001) were confirmed by ANOVA.
In summer N. diversicolor ingested a higher
percentage of sand (22.1 ± 1.79 %, n = 205) than in
spring (15.0 ± 1.18 %, n = 383) (post-hoc HSD test,
p<0.05). The effect of the interaction is due to
differences between ODX and ALZ in autumn (p =
0.004), ALZ between spring and autumn (p = 0.004)
and ALZ between winter and autumn (p = 0.002)
(post-hoc HSD test, p<0.05).
ANOVA results showed, for vegetable
detritus, that there were no differences between
sampling sites (F2,895 = 1.95, p = 0.14), seasons
(F3,895 = 0.35, p = 0.79) and also interaction between
them (F6,895 = 1.23, p = 0.27).
Larvae,
parapods
and
bristles
of
N. diversicolor as well as some other Nereididae
were found in the samples suggesting cannibalistic
behaviour. The ANOVA showed a non significant
119
Table I – Gut content of N. diversicolor (%) in the
whole sampling stations (main items in bold).
Gut Contents
%
mucus
Total Sediment
sand
mud
Vegetable detritus
Total Polychaeta
Nereididae
Spionidae
Capitellidae
Polychaeta (unidentified)
Total Crustacea
Cirripedia
Cyprideis sp.
Ostracoda (unidentified)
Copepoda
Cyathura carinata
Sphaeroma hookeri
Anthuridae
Isopoda (unidentified)
Corophium sp.
Gammarus sp.
Amphipoda (unidentified)
Crustacea (unident. remains)
Others
Foraminifera
Hydrobidae
Gastropoda (unidentified)
Bivalvia
Acari
Chironomidae
Insecta (unidentified)
unidentified
56,33
17,64
17,56
0,08
10,68
7,92
7,68
0,07
0,03
0,14
4,64
0,01
0,91
0,19
0,02
0,44
0,33
0,08
0,18
1,76
0,01
0,29
0,44
2,79
0,27
0,71
0,01
0,01
0,01
0,78
0,10
0,91
marginal effect for the sampling sites (F2,894 = 2.70, p
= 0.07) and a non significant effect for the season of
the year (F2,894 = 1.84, p = 0.14). Although, the same
analyses revealed a significant effect of the
interactions between variables (F6,894 = 2.77, p =
0.01), due to differences between CAR in spring and
in winter (post-hoc HSD test, p<0.05).
ANOVA indicates that there was a
significant effect away from the sampling sites
(F2,895 = 20.7, p<0.001) on the percentage of
Corophium sp. found in the digestive tract of N.
diversicolor. This effect is due to the fact that CAR
(5.4 ± 1.19 %, n = 227) is higher than ODX and
ALZ (0.02 ± 0.02 %, n=220; 0.8 ± 0.32 %, n = 460)
(post-hoc HSD test, p<0.05). There was also an
effect of the interaction between the sampling station
and season (F6,895 = 2.23, p = 0.04), due to
differences between CAR and ALZ in winter. (posthoc HSD test, p<0.05).
There was a clear trend for the increment of
the item “other” (other crustaceans, other
polychaetes and different animal groups found in
small quantities - cf. Table I) in the rainy seasons
(autumn, winter and spring – cf. Figure 2A), mainly
at ALZ and CAR (Figure 4). The slight increase in
this item in ODX (November and April 1994 - see
Figure 4) was due to the presence of the ostracod
Cyprideis sp. and the isopod Cyathura carinata.
ALZ showed a little bit higher species richness than
ODX, attributable to the presence of almost
completely digested and unidentifiable crustaceans.
Samples from the family Anthuridae (mainly
Cyathura carinata), Sphaeroma hookeri, and
Chironomidae larvae were also found at this site. In
December 1993, February 1994 and April 1994 (see
Figure 4), and in comparison with other sampling
sites a representative amount of unidentifiable parts
of crustaceans outer Cyprideis sp., Cyathura
carinata and Sphaeroma hookeri, were observed in
CAR. Also remarkable was the wide presence of
Chironomidae larvae in this sampling site.
Figure 5 shows the contents for each site and
also a graph formed by the whole of the sampling
sites. All crustaceans and polychaetes found were
grouped for all sampling sites as well as gastropods
and insects were also grouped for ALZ and CAR,
respectively, to emphasise their consumption by N.
diversicolor. The analysis of this figure makes clear
the main gradients found in the diet of this species
from ODX (the northern sampling site) to CAR (the
southern sampling site): i) sand and mucus decrease
from ODX to CAR; ii) an increased predation on
crustaceans and polychaetes from northern to
southern sampling sites; iii) gastropods and insects
were relevant in the diet respectively, in ALZ and
CAR.
Body size and sex effects on diet
Only mucus (F2,904 = 5.26, p = 0.005) and
sand (F2,904 = 6.37, p = 0.002) showed a significant
difference between the three sizes studied (S1, S2
and S3) (post-hoc HSD test, p<0.05). Smaller
individuals (S1) ingest a higher quantity of sand
(S1<S2=S3) and a lower quantity of mucus
(S1>S2=S3). The feeding strategies have changed
between S1 and S2 / S3 size classes, ingesting the
latter higher quantities of mucus (see Table II).
There were no significant differences in food
contents between males and females (Table III, Ttest for each food item, p>0,05).
120
Table II – Comparison (ANOVA) of gut contents
(S1) small, (S2) medium and (S3) large.
S1
n
avg. ± se.
n
Mucus
344
51.9 ± 1.90
542
Sand
21.2 ± 1.52
Detritus
8.9 ± 1.02
Nereididae
8.15 ± 1.33
Corophium sp.
2.74 ± 0.75
of N. diversicolor (%) separated in different size classes:
S2
avg. ± se.
58.8 ± 1.40
15.5 ± 0.98
11.1 ± 0.80
7.47 ± 0.90
2.17 ± 0.33
Table III – Male and female N. diversicolor gut
contents (%).
♂ (n=62)
♀ (n=159)
avg ± se.
avg ± se.
t
p
Mucus
63.0 ± 4.3
58.5 ± 2.8
0.85
0.40
Sand
11.7 ± 2.6
12.6 ± 1,7
-0.28
0.78
Detritus
9.92 ± 2.4
11.1 ± 1.6
-0.40
0.69
Nereididae
5.9 ± 2.4
7.9 ± 1.9
-0.60
0.55
Corophium sp.
1.4 ± 1.3
2.5 ± 1.1
-0.61
0.54
n
21
S3
avg. ± se.
66.1 ± 7.05
10.7 ± 4.78
10.4 ± 2.57
5.74 ± 3.71
0.71 ± 0.70
F2,904
5.26
6.37
1.48
0.22
2.5
p
0.0053
0.0017
0.23
0.79
0.08
Fidalgo e Costa et al. 2002) was also another
explanation for this result. It is known that N.
diversicolor acts as an active filter-feeder through
the production of a mucus net, when there is a higher
predation risk and/or the amount of suspended
particles is high (Esselink & Zwarts 1989, Vedel &
Riisgård 1993, Masson et al. 1995). When it is
submerged, this feeding strategy may be more
Discussion
Nereis diversicolor worms with the digestive
tract completely empty were found in the study area.
Two main explanations may be used for these
results: i) for southern sites, namely CAR, the
increase of predatory activity showed a large number
of worms with only few unidentifiable remains on
the gut contents, pointing out Gaston (1987)
statement that empty digestive tracts can reveal a
predatory feeding strategy, in which digestion is
completed more quickly, as opposed to digestion of
vegetable matter rich in cellulose; and ii) the
existence of a noticed continuous reproductive
activity throughout the year (Fidalgo e Costa et al.
1998), in which the gut was reabsorbed and feeding
ceased, as observed for this species and other
Nereididae during its sexual maturity period
(Golding 1987, Golding & Yuwono 1994, Last &
Olive 1999).
Mucus, the most frequent item found in
the digestive tracts, is not by itself a food item; it
is
an
aggregation
complex
of
organic
matter, bacteria, fungi, phytoplankton and
microphytobenthos. Differences in the amount of
mucus present in the contents between CAR and the
remaining sample sites was certainly based on its
less eutrophic state (Cancela da Fonseca et al.
2001a). The scarcity of phytoplankton in the bottom
water caused by occasional stratification (Figure 2),
and/or by the insufficient renewal promoted by the
tidal effect, while the connection to the sea in this
site is reduced (Cancela da Fonseca et al. 2001b,
Figure 5 – Main gut contents of N. diversicolor (%) in the
whole sampling stations and in each station separately.
121
effective (Harley, 1950, Wells & Dales, 1951,
Esselink & Zwarts, 1989, Vedel, 1998). In CAR,
with its frequent lack of tidal effect, due to its
lagoonal properties (except in November 1993 when
a rupture of the sand barrier occurred), a higher
quantity of mucus was expected. But in this site N.
diversicolor increases a carnivore strategy, partially
abandoning filtering through the mucus net. This
fact can be explained by i) the reduced quantity of
particulate material in the water column, or ii) a
favorable new feeding option as the capture of
crustaceans and insect larvae.
The fact that the mucus ingestion and the
aggregated food items increases at the time that the
ingestion of sand decreases (Table II), may be due to
an ontogenetic change in feeding habits. Small
individuals,
with
small
burrows,
acquire
detritivorous habits feeding more frequently on the
surface of the sediment. Possibly this strategy is due
to the inability of obtaining enough food through
filtration due to the reduced dimensions of its mucus
net or to difficulties in bringing enough water inside
the gallery through dorsal-ventral pumping
movements. On the other hand, larger individuals
with a better physical condition are capable of
building deeper galleries and pumping higher
quantity of water (Esselink & Zwarts, 1989).
Sand was observed frequently in the
digestive tract contents of Nereis, which swallows
large amounts of sediment in sweep-and-plough
food-searching strategy. This item may also have
been overvalued once it was extremely persistent in
the digestive tract, due to the fact that it is not
attacked by the digestive processes like the other
mentioned items. Like mucus it shows microalgae
glued to its surface (mainly diatoms), but also meio
and microfauna existing in the interstitial space
(Lucas & Bertru, 1997, Tita et al. 2000). For all
sampling sites, the differences found can be
narrowed down to seasonal differences that follow
the torrential character of the southern Portuguese
rivers in which the studied areas are included
(Magalhães et al. 1987, Fidalgo e Costa et al. 2002)
and, consequently, a greater or lower sediment
carriage from terrestrial or marine origins. These
seasonal changes are strongly evident in ODX and
ALZ, and in CAR they present only very low
amplitudes (Fidalgo e Costa et al. 2002). Frequently
that changes include also a seasonal contribution of
particulate organic matter (OM) brought by
continental runoff (Magalhães et al. 1987). So, when
the OM amount is higher one may expect that N.
diversicolor adopt a predominantly filter-feeding
behaviour, reducing the amount of sand ingested. On
the other hand a reduced organic flow may increase
ingested sand as it was found in CAR sampling site.
These statements were supported by the work of
several researchers that have already pointed out the
effect of sediment dynamics, induced by different
degrees of hydrodynamics and even by bioturbation,
on the superficial layers in which N. diversicolor
feeds on (Tamaki 1987, Meadows et al. 1990,
Turner et al. 1995, Mclachlan 1996).
Comparisons of chlorophyll a and
phaeopigment levels (Figure 3 A and B) with the
percentages of sand or mucus ingested (Figure 4) did
not allow the establishment of a comprehensive
pattern. This is possibly due to the fact that the
distribution and abundance of several species of
microalgae are controlled by a number of interdependent factors (Cadée & Hegeman 1974,
Pomeroy et al. 1981, Zedler 1982). In fact values of
ODX, ALZ and CAR sediment chlorophyll a (as an
indicator of microphytobenthos biomass) strongly
correlates to rainfall, indicating a dependence of this
environmental variable (Fidalgo e Costa et al. 2002).
As it was also concluded the variation of the ratio
between chlorophyll a and phaeopigments
emphasize that the chlorophyll a increase was due to
an in situ production of microalgae cells (Fidalgo e
Costa et al. 2002). Nevertheless these details
reinforce the above interpretation about sand
ingestion because it is supposed that a peak in
chlorophyll a (related to runoff) stimulate filtration
instead
of
sediment
ingestion
behaviors.
Nevertheless it was difficult to interpret our feeding
results based only on a phytopigments dataset,
referred only to one sampling day per month.
Detritus has an important role as a food
source both in the freshwater and marine benthic
communities. It is made up of all kinds of biogenic
materials such as bacteria, protozoa, micro and
macroalgae, parts of vascular plants in various
degrees of decomposition, which may contain
energy to be used by the species consumers (Tenore,
1977, Hansen & Kristensen, 1998). In the study
area, N. diversicolor used detritus as a food source in
all sampling stations, especially vegetable detritus
such as algae, roots, and parts of the macrophyte
Ruppia sp. The sampling sites revealed variations in
the percent occurrence of ingested vegetable detritus
which increased with precipitation (Figures 2A and
4), that may be related with the detritus amount
inside a system, with a more torrential character
(Magalhães et al. 1987). In ODX, it was observed
that the occurrence of mucus have decreased with
the augmented ingestion of vegetable detritus
(Figure 4) contrarily to ALZ where this ingestion
have no influence on mucus amounts. In CAR, the
rise in the consumption of vegetable detritus started
122
also with rainfall rise (Figure 4). For this site,
November 1993 was the single month where the
total emptying of the lagoon occurred, remaining
only a few puddles. During the following period
filter-feeding was difficult due to the small amount
of water available and so N. diversicolor fed on
remains and roots of Ruppia sp. as an alternative.
The decomposition of these macrophytes occurred as
a result of their emergence and exposure to the sun.
The increase in the vegetable remains consumed in
the winter and at the beginning of spring seems to be
caused by their transport to the system by the
frequent rains during these seasons (e.g. Figure 2A).
The digestive contents of N. diversicolor in
the present study confirm the results of previous
studies (Mcintosh 1907, Bogucki 1953), which
suggest cannibalistic behavior in this species. It
showed continuous reproduction in the three systems
studied, with a recruitment peak in early autumn,
reaching annual averages of 1126 ind.m-2 in ODX,
957 ind.m-2 in ALZ and 337 ind.m-2 in CAR
(Fidalgo e Costa et al. 1998). For this reason the
presence of larvae and juveniles in the gut contents
was frequent at almost all sites (Figure 4). The
larvae, juveniles and parts of individuals found in
the gut contents suggest that cannibalism follows the
life cycle of this species and showed a slightly
increase after the referred early autumnal peak of
larva with the growth of juveniles and the beginning
of an active free benthic life (Fidalgo e Costa et al.
1998).
Feeding on the surface of the sediment has
been observed in wild and under laboratory
conditions (Fidalgo e Costa et al. 2000) and it varies
according to quantity of food available. This practice
is considered as a complement to filter-feeding due
to the predation risks it involves (Masson et al.
1995). This feeding strategy may also be facilitated
by the absence of predators of N. diversicolor such
as Carcinus maenas. The lack of this active predator
of N. diversicolor (Cancela da Fonseca, 1989) in this
lagoon was mentioned by Magalhães (1988) and
confirmed during the present study. Due to the
apparent lack of predators, N. diversicolor could
promotes prolonged feeding journeys outside of the
burrows, which together with gallery digging, favors
the sediment turnover making it easier to find prey.
Corophium sp. was one of the preys frequently
observed in the intertidal environment of all
sampling stations. In ODX and ALZ with abundant
presence of C. maenas, there was no significant
predation on crustaceans. However in CAR there
was active predation of Corophium sp. during the
study period, which can be confirmed by the pieces
and whole individuals found in the digestive content
(Figure 4). In lagoonal environments such as CAR,
and according to Jensen & André (1993) even the
juvenile N. diversicolor have a negative effect on the
juvenile Corophium volutator, above all in
extraordinarily lentic lagoons, which is the case of
this lagoon.
In the future, it would be interesting to
verify a trade-off between food preferences and
predation risk in the laboratory. It would also be
interesting to determine in the field how predation
affects the population structure of this species.
Acknowledgments
This work was supported by a grant of the
Portuguese National Board of Scientific Research,
JNICT (BD/2265/92-IG) and by the JNICT contract
PBIC/C/MAR/1298/92. The authors are indebted to
all the colleagues from the Guia Marine Laboratory
who assisted in fieldwork. We are also grateful to
Dr. J.-P. Cancela da Fonseca for the revision of the
manuscript and to two anonymous referees for their
valuable criticisms and suggestions and their
significant contributions for its improvement. The
authors would also like to thank Dr. Elza Neto and
Dr.Michael Heasman for improving the English.
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Received September 2006
Accepted November 2006
Published online December 2006
Genidens genidens (Cuvier) (Pisces, Ariidae), oral incubation of eggs
ALEXANDRE M. GARCIA1, JOÃO P. VIEIRA & MARCELO D. M. BURNS
1
Fundação Universidade Federal de Rio Grande (FURG), Laboratório de Ictiologia, Departamento de Oceanografia,
CP 474, Rio Grande, RS, Brasil. *E-mail: [email protected]
Sea catfishes represent a major resource in artisanal fisheries along the East Coast of South America, and several
species, usually males, have been reported incubating eggs or young in areas of low salinity (Gomes & Araújo 2004). In
fact, species of this family produce the largest eggs among teleosts (Wallace & Selman 1981). During the incubation
period, males show an expansion of the hyoid region probably to increase the space available to carry eggs or young.
Size of the oral cavity, therefore, can limit fecundity in this species (Chaves 1994; Gomes & Araújo 2004). The above
specimen was photographed by AMG on November 15th, 2005, at São Gonçalo Channel, a natural channel connecting
Mirim and Patos lagoons in the Rio Grande do Sul state, southern Brazil. The individual (ca. 202 mm) was caught by
bottom trawling below the São Gonçalo’s dam. We observed only two eggs, with a diameter of approx. 15 mm each,
inside the oral cavity. As previously observed by Chaves (1994), eggs and larvae could be expel out of the oral cavity
due to the stress caused during the capture of the individual. He also mentioned that adults engaged in oral incubation
usually show total length from 192 and 270 mm, and have eggs with maximum diameter ranging between 13.1 and 15.5
mm and weight ranging between 1.5 and 1.9 g each. Picture characteristics: Digital Machine model Fujifilm® FinePix
S5100; Resolution of 4.2 megapixels (72 dpi); diaphragm aperture 5.7; time of exposition 1/480; Speed ISO-64.
References
Chaves, P.T.C. 1994. A incubação de ovos e larvas em Genidens genidens (Valenciennes) (Siluriformes, Ariidae) da
Baía de Guaratuba, Paraná, Brasil. Revista Brasileira de Zoologia, 11: 641-648.
Wallace, R.A. & Selman, K. 1981. Cellular and dynamic aspects of oocyte growth in teleosts. American Zoologist, 21:
325-343.
Gomes, I. D. & Araújo, G. F. 2004. Reproductive biology of two marine catfishes (Siluriformes, Ariidae) in the
Sepetiba Bay, Brazil. Revista de Biologia Tropical, 52 (1): 143-156.
This picture may be used for academic or personal purposes but always accompanied by the author's information
(copyright). To obtain permission for commercial use or for any other non-personal, non-academic use, or to inquire
about reprints, fees, and licensing, please contact the author via e-mail.
Pan-American Journal of Aquatic Sciences (2006), 1 (2): I
Eunectes murinus (Linnaeus) (Serpentes, Boidae), preying activity
LÍLIAN CRISTINA MACEDO-BERNARDE
Laboratório de Ecologia Animal, Faculdade de Ciências Biomédicas de Cacoal - FACIMED, Av. Cuiabá No. 3.087,
Jardim Clodoaldo, Cacoal – RO, Brasil. CEP 78.976-005. E-mail [email protected]
A
B
Eunectes murinus (Linnaeus, 1758) (Figure 1 a,b) is a aquatic, nocturnal and euryphagic snake species, feeding on
several vertebrates types (fishes, frogs, turtles, lizards, snakes, caimans, birds and mammals) (Strimple 1993, Martins &
Oliveira 1998). On 03 May 2006 at 13:00 h it was observed a large adult specimen of E. murinus (over 4000 mm
lenght) in the process of constriction killing a domestic pig (Sus scropha Linnaeus, 1758) in the edge of Mequéns river,
municipality of Alto Alegre do Parecis (12º51’03 " S; 61º54’56 " W), Rondônia States, Brazil. Picture Characteristics:
Digital Machine Canon PowerShot A610; Resolution of 5 megapixels (96 dpi); automatic; Speed ISO-50.
References
Martins, M. & Oliveira, M. E. 1998. Natural history of snakes in forests of the Manaus region, Central Amazonia,
Brazil. Herpetological Natural History, 6:78-150.
Strimple, P. 1993. Overview of the natural history of the green anaconda (Eunectes murinus). Herpetological Natural
History, 1:25-35.
This picture may be used for academic or personal purposes but always accompanied by the author's information
(copyright). To obtain permission for commercial use or for any other non-personal, non-academic use, or to inquire
about reprints, fees, and licensing, please contact the author via e-mail.
Pan-American Journal of Aquatic Sciences (2006), 1 (2): II
Software & Book Review Section
Poseidon Linux – uma distribuição Linux voltada para público
acadêmico e científico
CHRISTIAN DOS S. FERREIRA 1, GONZALO VELASCO 1,2, BERNARDO DOS S. VAZ 3,
EDUARDO H. ALBERGONE 1, DENIS HELLEBRANDT 1,4
1
Fundação Universidade do Rio Grande (FURG), Rio Grande, RS, Brasil ([email protected])
Universidade Estadual Paulista (UNESP), Rio Claro, SP, Brasil.
3
Universidade Federal de Pelotas (UFPEL), Pelotas, RS, Brasil.
4
School of Development Studies, University of East Anglia, Norwich, NR4 7TJ, UK.
2
Abstract. This paper introduces Poseidon Linux, a Linux distribution for academic and scientific use.
Poseidon Linux is a remastering from Kurumin Linux, but differs from Kurumin by the addition a large
number of programs applied to GIS/Maps, numerical modelling, 2D/3D/4D visualization, statistics, as
well as tools for creating simple and complex graphics and programming languages. Also, it includes
tools for daily use on a workstation, such as a complete office suite, internet browsers, e-mail client,
instant messaging, chat, and many other tools. Poseidon Linux can run on two modes, as a live-CD or
installed on the hard disk. It has support only for Brazilian Portuguese, but support for English and
Spanish languages is planned.
Resumo. Este artigo introduz o Poseidon Linux, uma distribuição Linux voltada para o uso acadêmico e
científico. Poseidon Linux é um remasterização do Kurumin Linux, mas difere do Kurumin por
apresentar um grande número de ferramentas nas áreas de Sistemas de Informação Georeferenciadas
(SIG), modelagem numérica, visualização 2D/3D/4D, estatística, ferramentas para criação de gráficos
simples e/ou complexos, e linguagens de programação. Também inclui ferramentas para o uso geral em
uma estação de trabalho, como um pacote de escritório completo, navegadores para internet, leitor de email, mensagens instantâneas, chat, e várias outras ferramentas. O Poseidon Linux pode rodar de duas
maneiras, como um “live-CD” ou instalado no disco rígido. Ele tem suporte somente para Português do
Brasil, mas há planos de versões em Inglês e Espanhol.
Introdução
Histórico
Ao longo deste artigo iremos apresentar brevemente
a história do UNIX/Linux e como ela envolveu as
universidades. A partir disso, falaremos sobre o que
motivou a criação do Poseidon Linux, com uma
descrição das ferramentas que nele estão incluídas.
Por último serão abordados planos para o futuro do
Poseidon Linux.
Desde o surgimento do sistema operacional
(SO) UNIX nos anos 70, seguido por sua
popularização nas universidades em meados dos '70,
o ambiente acadêmico foi palco da criação de novas
ferramentas e tendências baseadas no código fonte
do UNIX. Por sua portabilidade e robustez o UNIX
logo ganhou terreno em diversos centros de
C. DOS S. FERREIRA ET AL.
IV
pesquisa, e propiciou também o surgimento da
Internet (Wirzenius 2003). Porém com o aumento da
popularidade do UNIX nos anos 80 e devido aos
grandes interesses econômicos, o sistema começou a
se distanciar da filosofia de colaboração aberta,
comum na comunidade acadêmica e científica.
Com o objetivo de trazer novamente a
abertura, Richard Stallman criou a Free Software
Foundation em 1984. Stallman era um ex-aluno do
Massachusetts Institute of Technology (MIT) que
descontente com a filosofia do software proprietário
iniciou o projeto GNU (que significa “Gnu is Not
Unix”) (Free Software Foundation 2005). O
principal objetivo do projeto era criar um UNIX
aberto e gratuito. Nos anos 90, o SO GNU já estava
com praticamente tudo pronto, mas ainda faltava
uma peça fundamental, o kernel (núcleo) do sistema,
responsável por fazer a comunicação entre o
hardware e o software.
Em 1993, Linus Torvalds, um estudante da
universidade de Helsinki, Finlândia, deu o passo que
faltava ao criar um kernel que, somado aos softwares
do projeto de Stallman, rapidamente ganharam o
mundo através da Internet, dando origem ao SO
GNU/Linux (Wirzenius 2003).
Com o surgimento do GNU/Linux aparece
um novo conceito, o das distribuições ou coloquialmente- “distros” (Linux International
2001). Este termo vem do fato que cada grupo de
usuários ou empresas pode personalizar segundo sua
necessidade particular ou do mercado uma versão do
GNU/Linux e assim distribuí-la. Hoje em dia
existem diversas distribuições de Linux, entre as
mais famosas podemos destacar Debian, RedHat,
SuSE, Mandrake e Slackware. Dentre as
distribuições, a Debian é uma das mais importantes.
É uma das maiores no mundo e conta com milhares
de desenvolvedores que trabalham de forma
voluntária (Lamerte 2002). Como resultado deste
modo de trabalho uma vasta gama de softwares é
mantida pela equipe. O Debian é considerado uma
das melhores distribuições porque prima por
segurança e estabilidade. Porém versões mais atuais
dos programas não são incluídas até que estejam
totalmente testadas quanto à estabilidade, tornando-o
um pouco menos amigável para usuários iniciantes.
Para contornar isso, Klaus Knopper criou o
Knoppix, uma distribuição que é executada de forma
direta a partir de um CD (live-CD), sem necessidade
de instalar o sistema no disco rígido do computador,
e que usa o Debian como base, incluindo também
diversos scripts que permitem a detecção e autoconfiguração do hardware. Isso a tornou famosa já
que permitiu que diversos usuários pudessem
conhecer o GNU/Linux sem ter que instalar e alterar
nada em seus computadores.
Posteriormente, o Knoppix foi usado como
base para o surgimento de diversas derivações. Entre
elas, podemos destacar no Brasil o Kurumin Linux,
que incorpora diversas personalizações que buscam
facilitar ainda mais a utilização do GNU/Linux por
usuários domésticos.
Poseidon Linux
Usando
como
base
o
Kurumin,
pesquisadores da Fundação Universidade Federal do
Rio Grande (FURG) criaram o Poseidon Linux
(http://poseidon.furg.br).
A
finalidade
desta
distribuição é trazer para a comunidade acadêmica e
científica diversas ferramentas fundamentais
baseadas em software livre, visto que estas são
gratuitas,
apresentam
boa
estabilidade,
documentação, e –principalmente- tem o código
aberto, permitindo adaptação e personalização por
parte dos usuários, se desejado (Maliszewskyj &
Dickerson 1998, Laird 2002).
A justificativa para tal deve-se a realidade
atual nestes ambientes de trabalho: a presença de
sistemas e programas caros, que muitas vezes
exigem renovação periódica das licenças, que em
muitos casos são instáveis, ou -no pior dos casos- o
nada desejado uso de cópias não autorizadas de
software sem licença (pirataria). Tal cenário é
incompatível com o desenvolvimento de atividades
de pesquisa e educação, motivo pelo qual a opção
pelo software livre torna-se tão oportuna e
necessária.
Ainda, com a criação de uma plataforma
como o Poseidon Linux, o conceito de colaboração e
integração em ciência pode ser trazido também para
o software, fazendo possível que haja uma interação
entre diversos grupos para fomentar melhorias ou a
criação de novas ferramentas o que pode se reverter
também em aprimoramentos das pesquisas
(Wonnacott & Dougherty 1999).
As ferramentas científicas incluídas no
Poseidon Linux (atualmente na versão 2.0) buscam
abranger diversas áreas, tais como: Sistemas de
Informações Geográficas (SIG), banco de dados,
linguagens de programação, Estatística/Matemática,
modelagem numérica, visualização 2D/3D/4D,
editoração de documentos LATEX e criação de
gráficos científicos. Os programas específicos
incluídos (diferenciais) são apresentados com mais
detalhes na Tabela I.
Na figura 1 mostra-se o resultado de um
trabalho realizado totalmente no Poseidon Linux,
analisando milhares de dados pontuais de
profundidade do oceano na costa brasileira e
Poseidon Linux
V
Tabela I. Lista de software específicos do Poseidon Linux (versão 2.0).
Área
Sistema de Informações
Geográficas e
Geoprocessamento
Estatístico/Matemático
Modelagem numérica
Visualização 2D/3D/4D
Editor TEX
Linguagens de programação
Banco de dados
Gráficos e mapas
Editor Postscript
Editor de diagramas
CAD 2D
Softwares
GRASS 6.0.0
SPRING 4.1
Terraview 3.0+
QGIS 0.6
GMT 3.4.4
PROJ 4.4
R 2.0.1
Scigraphica 0.8
Octave 2.1
OpenDX 4.3
Vis5D 5.2
Lyx 1.3.5
Kile 1.7
C e C++ 3.3.5
G77 3.3.5
Python 2.3
PostgreSQL 7.4
MySQL 4.1
PostGIS 1.0.1
Gri 2.19
XFig 3.2.5
Dia 0.94
QCAD 2.0.4
integrando esses dados em uma figura tridimensional
(extraído de Ferreira et al. 2005).
Além das ferramentas acadêmicas/científicas
estão incluídos vários programas necessários para o
dia-a-dia, como um pacote de escritório completo
(OpenOffice.org),
navegadores
de
internet
(MozillaFirefox e Konqueror), leitores de correio
eletrônico (Thunderbird), programas para mensagens
instantâneas (Kopete), editores de imagens (GIMP e
Kolourpaint), e visualizadores de imagem PS e PDF,
tudo isso num ambiente amigável e visualmente
moderno (Fig. 2).
Figura 1 – Mapa do relevo do fundo da plataforma continental
brasileira e oceano adjacente realizada utilizando as ferramentas
do Poseidon Linux e dados de pesquisa oceanográfica.
URL
http://grass.itc.it/
http://www.dpi.inpe.br/spring/
http://www.dpi.inpe.br/terraview/
http://qgis.sourceforge.net/
http://gmt.soest.hawaii.edu/
http://proj.maptools.org/
http://www.r-project.org/
http://scigraphica.sourceforge.net/
http://www.octave.org/
http://www.opendx.org/
http://www.ssec.wisc.edu/~billh/vis5d.html
http://www.lyx.org/
http://kile.sourceforge.net/
http://gcc.gnu.org/
http://www.gnu.org/software/fortran/fortran.htm
l
http://www.python.org/
http://www.postgresql.org/
http://www.mysql.com/
http://postgis.refractions.net/
http://gri.sourceforge.net/
http://www.xfig.org/
http://www.gnome.org/projects/dia/
http://www.ribbonsoft.com/qcad.html
Por utilizar a tecnologia live-CD torna-se
acessível aos pesquisadores a introdução ou
utilização plena de todas as ferramentas inclusas no
Poseidon Linux e o SO GNU/Linux sem a
necessidade de instalação. Se desejado, existe
também a opção de instalação do Poseidon Linux em
disco rígido como sistema operacional de um
computador pessoal ou portátil, inclusive para o uso
simultâneo de mais de um sistema no mesmo PC.
Isto é, o Poseidon Linux pode estar instalado em
uma máquina que já possua outro(s) sistema(s) e o
usuário escolhe ao ligar o computador qual sistema
vai usar, graças a um administrador de inicialização
(LILO).
O Poseidon Linux já foi apresentado em
diversas palestras em universidades públicas e outras
instituições do Brasil e em diversos eventos
específicos, destacando-se o VI Fórum Internacional
de Software Livre, realizado em Porto Alegre (RS)
em 2005, onde contou com um stand de exposição
especial.
Já há usuários do Poseidon nas seguintes
universidades brasileiras: FURG, UFPEL, UNIVALI
e Instituto Oceanográfico da USP. Algumas
instituições do governo como SIVAM, EMBRAPA,
DAER e IBAMA, já usam o Poseidon Linux ou
estão avaliando sua utilidade. Pesquisadores de
outros países da América Latina também estão
VI
C. DOS S. FERREIRA ET AL.
Figura 2 – Imagem da visualização do Poseidon Linux 2.0 rodando em um computador. Em detalhe o menu expandido mostrando
algumas dos programas instalados.
avaliando e/ou usando o Poseidon. Existe no site da
internet do projeto um guia de instalação em
espanhol, além do guia em português, o qual foi
muito acessado desde sua publicação (Novembro de
2005).
Planos Futuros
A equipe Poseidon Linux já está trabalhando
para desenvolver versões em Espanhol e Inglês do
mesmo, para atender um número maior de
pesquisadores fora do Brasil. Ainda, pretende-se
criar uma versão específica para computação de alto
desempenho (montagem de clusters).
Conclusões
Esta é uma distribuição Linux totalmente
composta por Software Livre (SL), baseado no
Kurumin Linux, e inspirada pelo Quantian Linux. O
Poseidon é e sempre será livre e gratuito. Outro
detalhe importante é que todos os programas podem
rodar a partir do CD (“bootável”), já que o Poseidon
possui tecnologias que permitem isso, sendo
possível utilizar todos os programas sem instalar
absolutamente nada. Existe também a opção de
instalar no computador se o pesquisador ou
estudante assim desejar. Este não é, por tanto, um
produto comercial e/ou que inclui programas
“piratas”.
Considera-se que o Poseidon Linux é uma
alternativa de plataforma de trabalho atraente para
pesquisadores,
professores
e
alunos
das
universidades públicas e privadas, já que inclui uma
enorme gama de ferramentas estáveis e gratuitas que
podem auxiliar-los no desenvolvimento da pesquisa
e na popularização do software livre no meio
acadêmico e científico. Representa um pacote
completo (sistema operacional base e a maioria dos
aplicativos utilizados no dia-a-dia, tanto em um
computador pessoal como uma estação de trabalho
em uma universidade ou instituto de pesquisa). A
Equipe Poseidon Linux atualiza o pacote
periodicamente para incluir as novas versões dos
programas, quando disponíveis, e também para eventualmente- incluir novas ferramentas científicas
que os usuários e colaboradores sugerem num fórum
aberto aos mesmos.
Referências bibliográficas
Ferreira, C., Albergone, E., H., Velasco, G., Vaz, B.,
Hellebrandt, D., 2006, Poseidon Linux, uma
distribuição Linux voltada para público
acadêmico e científico. Resumos do 7o
Fórum Internacional do Software Livre
(FISL7). Porto Alegre.
Free Software Foundation. 2005. The GNU
Operating System. http://www.gnu.org/.
Acessado em abril de 2005
Laird, C. 2002. Open source in the lab (Python,
Poseidon Linux
Perl, and open source toolkits bring
multiple benefits to science). IBM.
http://www128.ibm.com/developerworks/linux/library/loslab/. Acessado em Outubro de 2005
Lamerte, D. 2002. Debian GNU/Linux: The Past,
the
Present
and
the
Future,
http://telemetrybox.org/tokyo/. Acessado em
Outubro de 2005
Linux International. 2001. What is Linux.
http://www.li.org/whatislinux.php
Maliszewskyj, P. & Dickerson, B. 1998. Linux
VII
Journal: Linux in a Scientific Laboratory,
http://noframes.linuxjournal.com/article/2596.
Acessado em Agosto de 2005
Wirzenius, L. 2003. Linux: the big picture,
http://liw.iki.fi/liw/texts/linux-the-bigpicture.
Wonnacott, D. & Dougherty, J. 1999. Linux in the
Lab
http://www.haverford.edu/publications/summe
r99/linuxlab.htm

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