Reduction of scales and head canals in Pomato

Verhandlungen der Gesellschaft für Ichthyologie, Band 5, 71-77
Reduction of scales and head canals in Pomatoschistus canestrinii (Ninni, 1883) (Teleostei, Gobiidae)
Reduktion von Schuppen und Kopfkanälen bei Pomatoschistus
canestrinii (Ninni, 1883) (Teleostei, Gobiidae)
Björn Stelbrink and Jörg Freyhof
Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Department of Biology
and Ecology of Fishes, Müggelseedamm 310, D-12587 Berlin, Germany;
[email protected]
Summary: Pomatoschistus canestrinii from freshwater Lake Skadar (Montenegro) have reduced squamation and head canals, while the brackish water population from the River Krka (Croatia) and two
´
additional freshwater populations from the River Ricica (Croatia) and the Bacinska
Lake system
(Croatia) show a complete or almost complete squamation and head canal system. In regard to the
distribution patterns of the head canals as well as head pores, partial reductions could be pointed
´
out for Bacinska
as well as Ricica individuals, while the largest reductive range of variation up to the
complete loss of the canal system could be noticed within the Lake Skadar population. The ecological factors, which lead to these reductions, remain unresolved.
Key words: Adriatic Sea, scale reduction, head canal reduction, Gobiidae, Pomatoschistus
Zusammenfassung: Pomatoschistus canestrinii aus dem Skutarisee (Montenegro) haben eine reduzierte Beschuppung sowie reduzierte Kopfkanäle, während die Brackwasser-Population aus dem
Fluss Krka (Kroatien) sowie zwei zusätzliche Süßwasser-Populationen aus dem Fluss Ricica (Kro´
atien) und dem Bacinska
Seensystem (Kroatien) eine komplette Beschuppung bzw. ein komplettes
oder nahezu komplettes Kopfkanalsystem aufweisen. In Bezug auf das Verteilungsmuster der Kopfkanäle und -poren können teilweise Reduktionen bei den Bacinskasowie Ricica-Individuen aufge´
zeigt werden, während die größte Bandbreite an Reduktionen, bis hin zum vollständigen Verlust
des Kanalsystems, innerhalb der Skutariesee-Population beobachtet werden kann. Die ökologischen Faktoren, die zu diesen Reduktionen führen, bleiben allerdings ungeklärt.
Schlüsselwörter: Adria, Schuppenreduktion, Kopfkanalreduktion, Gobiidae, Pomatoschistus
1. Introduction
European freshwater sand-gobies are traditionally subdivided into the genera Economidichthys, Knipowitschia and Pomatoschistus
(Economidis and Miller 1990). The phylogeny of sand-gobies is considered to be
poorly understood and traditional genera
might form paraphyletic assemblages, originating from multiple independent origins
by marine ancestors (Penzo et al. 1998).
While Economidichthys is distinguished from
the other two genera by an unique perianal
organ and transverse supraorbital papillae
rows (Miller 2004), Knipowitschia and Pomatoschistus are delimited from each other by
the length of the anterior oculoscapular
canal, which is extending to the snout, ending at pore σ in Pomatoschistus (vs. ending
before pore σ in Knipowitschia) (fig. 1). The
posterior oculoscapular canal is present in
Pomatoschistus, whereas in other sand gobies
Verh. Ges. Ichthyol. Bd. 5, 2006
71
Figs. 1a, b: Head lateral-line
canal pores (Greek letters) and
sensory papillae in dorsal view
(from Miller 2004) of a Pomatoschistus canestrinii and b Knipowitschia caucasica. AN, PN, anterior and posterior nostrils.
Abb. 1a, b: Kopfkanalporen
(griechische Buchstaben) und
sensorische Papillen in Dorsalansicht (aus Miller 2004)
von a Pomatoschistus canestrinii
und b Knipowitschia caucasica.
AN, PN, vordere und hintere
Nasenöffnungen.
it is usually absent (Miller 2004). However,
it is well known that sand gobies of the
genus Knipowitschia might reduce their head
canals what makes their generic identification impossible by the characters listed
above. Because no alternative generic concept is available, freshwater species with reduced head canals are generally placed in
the genus Knipowitschia (Economidis and
Miller 1990, Ahnelt 1991).
Fourteen species of estuarine and freshwater
gobies from the Caspian, Black and Mediterranean Sea basins are included in the genus
Knipowitschia. Within Knipowitschia, there is a
group of species with complete squamation
along lateral series until the caudal fin base
and presence of complete or almost complete
cephalic lateral line canals (K. bergi, K. cameliae,
K. caucasica, K. goerneri, K. iljini, K. longecaudata,
and K. panizzae) (Miller 2004). All these species are euryhaline inhabitants of coastal
lagoons and river estuaries.
A second group of species is characterized
by incomplete or absent squamation along
lateral series and/or incomplete or absent
cephalic lateral line canals (K. croatica, K. ephesi, K. mermere, K. milleri, K. punctatissima, K.
thessala) (Miller 2004). All these species are
restricted to freshwater habitats.
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While both species of Economidichthys exhibit a reduced squamation and no head canals, all species of Pomatoschistus have a complete squamation and complete cephalic
lateral-line canals (Miller 2004). Whereas
Economidichthys inhabit freshwaters only
(Miller 2004), P. microps is the only amphidromous species entering freshwaters during seasonal migrations (Miller 2004, Riede
2004). All other Pomatoschistus are resident
inhabitants of marine or at least brackish
waters (Miller 2004).
Miller (2004) already speculated that reduction of squamation and head canals could
be correlated with the invasion of sand
gobies into freshwater. To test this hypothesis, a sand goby should be studied, which
represents a resident inhabitant of estuarine and freshwater habitats.
In Europe two gobies come into question:
Knipowitschia caucasica and Pomatoschistus canestrinii. Knipowitschia caucasica individuals
seem to be monomorphic – or at least less
variable than the other species – in freshand brackish waters, representing the complete pattern of squamation and head
canals (Miller 2004).
Pomatoschistus canestrinii is a euryhaline goby,
well known from estuaries and lagoons in
^ ^
^
All fish were caught using a fine mesh beach seine or a DEKA 3000 portable electroshocker and preserved directly in 5 %
formaldehyde, and later transferred to 70 %
ethanol for storage. Abbreviation FSJF used
denotes the fish collection of Jörg Freyhof
(Fischsammlung Jörg Freyhof). River Krka
individuals (FSJF 1090) represent the brackish water reference population for the estuarine type; the other locations represent
freshwater populations.
Material examined: P. canestrinii. – FSJF
1090, n = 20; 10 males, 10 females, 27.3934.55 mm SL; Croatia: River Krka at uppermost part of Prokljansko Jezero at Skradin; Nina Bogutskaya & Jörg Freyhof. –
FSJF 1074, n = 13; 2 males, 11 females,
20.05-30.08 mm SL; Croatia: reservoir at
River Ricica at village Stikada, 44°19.228’N
15°46.940’E; Nina Bogutskaya & Jörg Freyhof. – FSJF 1088, 1 male, 34.41 mm SL;
´
Croatia: Lake Bacinska
at village Bacina;
Nina Bogutskaya & Jörg Freyhof. – FSJF
^
2. Material and methods
1048, n = 5; 1 male, 4 females, 26.10-30.18
mm SL; Montenegro: Lake Malo Blato at
Begova Glavica; Primoz Zupancic & Jörg
Freyhof. – FSJF 1096, n = 40; 20 males, 20
females, 23.44-31.95 mm SL; Montenegro:
backwater of River Moraèa, west of bridge
between Golubovci and Vukovici, right
river side; Primoz Zupancic & Jörg Freyhof.
Pomatoschistus canestrinii (fig. 2) is distinguished from other Adriatic goby species
in morphological and coloration characters,
using the presence or reduction and loss,
respectively, of head canals and squamation as well as the body coloration, e.g. numbers of vertical bars.
Males and females on their part are distinguished in body coloration. Whereas males
show a prominent black head with yellowwhitish neck blotches as well as a dark grey
pelvic disc, 5-6 dark vertical bars and spots,
the females are characterized by the absence
of bars, a whitish head and pelvic disc as
well as fewer spots (Miller 2004).
The body squamation as well as the head
canal and pore systems were compared with
the species habitus shown by Miller (2004)
and cephalic lateral-line canal description
and canal and pore definition, both using a
binocular microscope.
Within the head canal system three major
structures are crucial for the taxonomic
discrimination of sand-gobies: the anterior
oculoscapular canal, including pores σ, λ,
κ, α, ω and ρ, furthermore the posterior
oculoscapular canal, including the two
pores ρ1 and ρ2 and finally the preopercular
canal with pores γ, δ and ε (for better understanding see fig. 4).
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the northern Adriatic as well as along the
Croatian coast (Miller 2004). While only
brackish and marine populations were
known, an introduced freshwater population was first recorded by Freyhof (1998)
from Italian Lake Trasimeno, demonstrating that this species is able to live in pure
freshwater. Well known, but misidentified
(Ivanovic 1973), freshwater gobies from
Lake Skadar basin were recently identified
as freshwater population of P. canestrinii by
Bohlen et al. (2003). During an expedition
to Croatia and Montenegro this species
could be collected in one estuarine and three
freshwater habitats.
Brackish and freshwater populations of the
goby P. canestrinii were examined to verify
possible reductions in this species and to
evaluate the potential correlation between
this process of reduction and the invasion
into freshwater habitats.
3. Results
The population from brackish waters of
lower River Krka displays full body squamation and a lack of scales on the predorsal body (fig. 3). The same squamation type
could be noticed within the River Ricica
Verh. Ges. Ichthyol. Bd. 5, 2006
73
Fig. 2: Pomatoschistus canestrinii, male, Montenegro, River Moraca.
Abb. 2: Pomatoschistus canestrinii, Männchen, Montenegro, Fluss Moraca.
Fig. 3: Populations of P. canestrinii examined. Red dots denote study sites. Red marks on fish drawings show dominant squamation type. Circular charts show the head canal type distribution pattern within study sites. Outline map shows distribution of P. canestrinii, following Miller (2004).
Abb. 3: Untersuchte Populationen von P. canestrinii. Rote Kreise zeigen Lage der Fundorte. Die rote
Markierung auf den Fischzeichnungen zeigt das dominante Ausmaß der Beschuppung der Populationen. Die Kreisdiagramme zeigen die in der jeweiligen Population dominante Ausprägung der
Kopfkanäle. Die Übersichtskarte zeigt die Verbreitung von P. canestrinii nach Miller (2004).
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and Lake Bacinska
´
freshwater individuals.
Lake Skadar population is distinguished
from the estuarine type by a reduction of
the scales up to a small region underneath
the pectoral fins (fig. 3).
Within the P. canestrinii populations 36 head
canal types could be observed. Similar
forms were summarized into five arbitrary types (fig. 4) to get better information
about the distribution pattern. Type I represents the estuarine type with a complete
or almost complete anterior oculoscapular canal, types II-V represents the arbitrarily defined gradual reduction of the
anterior oculoscapular canal and preopercular canals and pores. The posterior ocu-
loscapular canal is absent in all specimens
examined.
Type I can be noticed within the estuarine
population and the single Lake Bacinska
´
individual. The Ricica individuals are almost
homogenous and possess the type I (n = 4;
4 females) as well as type II (n = 9; 2 males,
7 females). The Lake Skadar population is
represented by type II (n = 6; 5 males, 1
female), type III (n = 15; 9 males, 6 females), type IV (n = 7; 3 males, 4 females) and
type V (n = 17; 4 males, 13 females).
Thus, the largest variation can be observed
within the Lake Skadar population, while
the other populations more or less belong
to one head canal system type (fig. 4).
Fig. 4: Head canal types. Greek letterings denote pores, dashed lines denote canals, solid lines
denote open canals (furrows). Denotation of pores and canals after Miller (2004). AN, PN, anterior
and posterior nostrils. Undefined pores could not be classified into the intraspecific distribution
pattern.
Abb. 4: Kopfkanaltypen. Griechische Buchstaben bezeichnen Poren, gestrichelte Linien den Kanalverlauf, durchgezogene Linien offene Kanäle (Furchen). Bezeichnung der Poren und Kanäle
nach Miller (2004). AN, PN, vordere und hintere Nasenöffnungen. Unbeschriftete Poren konnten
nicht in das intraspezifische Verteilungsmuster eingeordnet werden.
Verh. Ges. Ichthyol. Bd. 5, 2006
75
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The scale and head canal reduction in P.
canestrinii from Lake Skadar is remarkable,
not only being the single examined population with this trait, but also being a homogenous, monomorphic population, regarding this character.
First, one can ask why the other freshwater
populations from the northern regions do
not display these scale reductions, but look
like the brackish water populations. And
secondly, is this reduction of scales due to
the Lake Skadar abiotic and biotic factors?
If the reduction of squamation and head
canals is related to the invasion of freshwater habitiats, the time passed since the
colonization of the freshwater habitats
might be crucial for the understanding of
this process, which might be speculated to
be an adaptive one. In this case, it could be
suspected that Lake Skadar P. canestrinii are
remarkable longer isolated from the coast
than the other examined populations.
The situation in P. canestrinii is somehow
similar to the reduction of lateral plates in
sticklebacks, Gasterosteus aculeatus. There is a
wide range of studies, dealing with plate
reduction in G. aculeatus with different points
of view, whose results and consequential
discussions could be compared with the
results from the present study. For sticklebacks it is supposed that lateral plates mainly
acting as armors against toothed fishes and
increasing the predator´s handling time.
Vice versa, the reduction of plates is therefore due to a lower predatory pressure (e.g.
Fernandez et al. 2000, Reimchen 2000). The
same might be also suspected for P. canestrinii. Further limiting factors, which are mentioned by these and other authors (salinity,
temperature and calcium concentration),
may also be important for the magnitude
of plates in sticklebacks and scales in P. canestrinii, respectively.
The function of the cephalic lateral-line
system can be devided into “prey detection
[…], rheotaxis […], schooling […], intraspecific communication […] and identification and localization of wave sources
[…]” (reviewed by Engelmann et al.
2002).
Ahnelt (2001) presumes that the varied
course of the head canals in Gobius ater and
G. paganellus may due to the different habitats they are living in. Therefore, the reductions in the lateral head canal system in the
Lake Skadar population could display also
a habitat-specific adaptation – possibly supported by the recently described speciesspecific distribution pattern of P. canestrinii
in the Venice Lagoon (Malavasi et al. 2005)
–, conversely, a complete lateral head canal
system may be more advantageous in brackish or marine ecosystems for P. canestrinii. It
could be supposed that a lower predation
pressure might also force the reduction of
head canals as gobies may detect a predator
also by wave sources identification and localization.
Kovacic´ (2005) also reveals reduction patterns of the head canal system as well as
the squamation among P. canestrinii populations from several places along the Croatian coast.
His findings in reductions of the cephalic
lateral-line system are quite similar to those
of our study, even though the specimens
examined by Kovacic´ (2005) show a lower
variability as well as a lower degree of reduction. Also, the pore ω, which was not
found by Kovacic´ (2005), could be recorded in specimens from Lake Skadar and in
some Ricica individuals. Hence, by the hypothesized transformation series in fig. 4
we assume that a canal reduction begins
with a shortening/contraction of the mentioned canal and thus with an adjacent displacement as well as a new development of
pores (e.g. pore ω in this case), finishing with
the loss of the last parts of the canals and
the pores themselves, respectively. By this,
a doubled interorbital canal could be noticed
in some specimens.
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4. Discussion
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Acknowledgements
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We are thankful to Primoz Zupancic
(Ljubljana) for his help during field work.
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Another morphological trait, considered by
Kovacic´ (2005), is the development of the
squamation. Among the study sites two character states were noticed by Kovacic´ (2005),
a continuous squamation along the lateral
midline and a squamation reduced to axillar and caudal areas. Whereas the complete
squamation type is also observed within the
present study, the reduced squamation type
with two scaled areas was not observed. In
Lake Skadar, an axillar scale patch occurred,
but scales were always absent from the caudal peduncle.
Future investigations are necessary to clarify the biogeography of P. canestrinii and the
timing of the invasion of different freshwater bodies. The questions, which ecological factors lead to the observed reductions, remain unresolved.
Laboratory experiments with naked and
scaled P. canestrinii could be performed to
test if scaled P. canestrinii with a full set of
head canals are less vulnerable to predator
pressure than naked P. canestrinii or if predators need a longer handling time preying
on scaled P. canestrinii.
Verh. Ges. Ichthyol. Bd. 5, 2006
77
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