Download Ostracoda and Amphibia in temporary ponds: who is the prey

Aquat Ecol
DOI 10.1007/s10452-010-9323-y
Ostracoda and Amphibia in temporary ponds: who
is the prey? Unexpected trophic relation in a mediterranean
freshwater habitat
Dario Ottonello • Antonio Romano
Received: 8 November 2009 / Accepted: 5 May 2010
Ó Springer Science+Business Media B.V. 2010
Abstract Small and temporary freshwater ecosystems are important biodiversity ‘‘hot spots’’ of the
Mediterranean region, and their food webs are considered as very complex systems. Amphibians and
ostracods are two highly ubiquitous classes of metazoans adapted to live in temporary ponds. Their
trophic interactions are considered unidirectional, the
amphibians acting as predators and the ostracods as
preys. In the field, we observed the opposite interaction in few ponds in Northern Italy. To confirm this
qualitative evidence, we set up laboratory experiments to investigate the predation by the Ostracod
mussel shrimp (Heterocypris incongruens) on eggs
and tadpoles of Common toad (Bufo bufo) and
Stripless tree frog (Hyla meridionalis). Amphibian
eggs of both species were offered to ostracods either
as unique trophic resource or, alternatively, together
with another kind of food. Similarly, tadpoles of both
species were simultaneously offered to ostracods
(with alternative food) to disclose their preferences.
Ostracods preyed mainly on amphibian eggs and no
Handling Editor: Piet Spaak.
D. Ottonello
Via San Domenico 200, 17027 Pietra Ligure (SV), Italy
A. Romano (&)
Dipartimento di Biologia, Università di Roma ‘‘Tor
Vergata’’, Via della Ricerca Scientifica, 00133 Rome,
Italy
e-mail: [email protected]
significant differences in the rate of predation between
toad and treefrog eggs were detected. However,
ostracods preferred Bufo when offered along with
Hyla tadpoles. Toad eggs and larvae are commonly
considered highly unpalatable, but our results contrasted this view. The difference in the predation rate
between the two tadpole species is discussed in the
light of their swimming behaviour. We show that
feeding relationships between Amphibia and Ostracoda are much more complex than expected and
depend on both the ecological context and amphibian
life stage. The knowledge of the trophic connections
among taxa is a fundamental prerequisite to further
and more exhaustive studies on community ecology.
Keywords Amphibia Ostracoda Egg predation Food web Temporary ponds
Introduction
Aquatic habitats may differ in productivity, resource
abundance and community composition (e.g. Polis
et al. 1997). Food webs are particularly complex in
large and permanent aquatic ecosystems (e.g. Belgrano
et al. 2005), although their complexity in small and
temporary ponds has been often underestimated (e.g.
Wilbur 1997; Urban 2007). In the Mediterranean
region, ephemeral aquatic habitats represent the very
large majority of freshwater ecosystems (Blondel and
Aronson 1999) and the temporary ponds (sensu De
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Aquat Ecol
Meester et al. 2005) may be collectively considered as
biodiversity ‘‘hot spots’’ (e.g. Céréghino et al. 2008 and
references therein; Williams et al. 2004). In fact, they
harbour taxa of high conservation interest (Della Bella
et al. 2005; Griffiths 1997).
Ostracoda and Amphibia are two highly ubiquitous
classes of metazoans colonising an extremely wide
variety of freshwater environments (Balian et al. 2008;
Martens et al. 2008), included the temporary ponds
(Eitam et al. 2004; Griffiths 1997; Rossetti et al. 2006).
Ostracods, or mussel shrimps, display a variety of
feeding strategies as they can act as filter-feeders,
detrivores, herbivores and carnivores. Among freshwater ostracods, scavenging is the main form of carnivory,
while parasitism is the least common carnivorous habit.
Several feeding habits may be adopted by the same taxon
as complementary and opportunistic feeding strategies
(Bennett et al. 1997; Vannier et al. 1998; Wilkinson et al.
2007 and references therein). Amphibians are predators
at the adult stage, whereas their larvae may be carnivorous (salamanders, newts and caecilians, see Kupfer
et al. 2005 and references therein; but also some anuran
species: McDiarmid and Altig 1999), herbivorous,
detritivorous or omnivorous (in frogs, toads and treefrogs: McDiarmid and Altig 1999). In many ecosystems,
amphibians are the major predator of invertebrates and
algae consumers (Blaustein and Wake 1990; Wake
1991), representing, in turn, a rich trophic resource for
mammals, birds, fishes, snakes (Blaustein and Wake
1990; Hayes and Jennings 1990) and, at least during their
egg or larval stages, for several invertebrates (Gunzburger and Travis 2005; Romano and Di Cerbo 2007).
In the field, we qualitatively observed an unexpected trophic relation between ostracods and amphibians (eggs and larvae) where the first were the predator
and the second were the prey. These observations
suggested that mussel shrimps might prey on amphibian eggs and tadpoles. To test this hypothesis, we
performed a set of laboratory experiments to attempt to
estimate the rate of predation, the species-specific
preference for eggs, and to assess whether amphibian
eggs were preyed also when predators were provided
with an alternative food.
Study area, materials and methods
The study area includes four temporary ponds located
in an abandoned limestone quarry at 280 m a.s.l near
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Bergeggi (Liguria, North West Italy). The ponds
(30 m2 each, maximum depth: 0.6 m) are artificial
and were created for amphibians conservation purpose. The area is characterised by Mediterranean
climate and the pond hydroperiod may last from
October to June depending on precipitations. Quarrying activities were stopped in 1960 and since then
the area has been naturalised by grass and shrub
vegetation typical of the Mediterranean maquis.
The ostracod Heterocypris incongruens (Ramdohr
1808) is common in the four ponds where the
Balearic green toad Bufo balearicus Boettger 1880,
the Parsley frog Pelodytes punctatus (Daudin 1802)
and the Stripeless treefrog Hyla meridionalis Boettger 1874, also breed. The Common toad Bufo bufo
(Linnaeus 1758) spawns in only one of these ponds
which was our study pond.
Fig. 1 Egg strings of Common toad (Bufo bufo) in a
temporary pond in Northern Italy were hardly attacked by
ostracods (Heterocypris incongruens) which preyed on the
embryos
Aquat Ecol
Fig. 2 A Common toad tadpole (Bufo bufo) preyed upon
ostracods (Heterocypris incongruens) as observed in a temporary ponds in Northern Italy
In March 2009, we observed that ostracod density
was very heterogeneous among different microhabitats of the pond where B. bufo breeds. Swarms of
H. incongruens were concentrated around and on the
eggs strings of the Common toad (Fig. 1) and high
densities were recorded also upon small submerged
sprigs. We also observed that ostracods seemed to
have attacked some tadpoles (Fig. 2). In order to test
the hypothesis that H. incongruens might prey on
amphibian eggs and tadpoles, we set up several
laboratory experiments. Experiment 1 and 3 were
designed to estimate the rate of predation, Experiment
2 and 4 to assess whether amphibian eggs were preyed
also when predators were provided with an alternative
food, Experiment 5 and 6 to assess the species-specific
preference for eggs and tadpoles, respectively, Experiment 7 was design to control for factor other than
predation on the deterioration of eggs.
For each experiment, Ostracods, eggs and larvae of
B. bufo and H. meridionalis, and several sprigs covered
by incrusting algae were collected by hand from the
study pond and carried in laboratory. At the time of
collection, pond water parameters were: temperature = 15°C, pH = 8.91, conductivity = 302 lS/cm,
dissolved oxygen = 152 ppm). In the lab, seven
aquaria (20 9 30 9 20 cm, for a total volume of
12 l) were filled with tap water and kept at constant
temperature (20°C). Tap water was left to stand for
24 h before the experiments began to allow evaporation of the chlorine. In each experiment, we placed
amphibian eggs and ostracods in the same aquarium.
Ostracods were placed in the aquaria 2 h earlier than
amphibian eggs or tadpoles in order to allow for their
acclimatisation to experimental conditions. At the
beginning of the experiment, the tap water parameters
were: temperature = 20°C, pH = 8.44, conductivity =
169 lS/cm, dissolved oxygen = 89 ppm. Aquaria were
not exposed to direct solar radiation. Given that
experiments were performed in April, photoperiod
may be considered homogenous (12 h light vs. 12 h
darkness). The difference between the initial number of
amphibian eggs and the final number of eggs was
considered as the number of preyed eggs. We used the
following combination of ostracods, eggs, larvae and
other vegetable food (i.e. sprigs, which were substituted
every 24 h to provide abundant availability of incrusting
algae).
Experiment 1 (Exp.1): 21 eggs of B. bufo were
placed in an aquarium with 300 ostracods.
Experiment 2 (Exp.2): 21 eggs of B. bufo were
placed in an aquarium with 300 ostracods and sprigs.
Experiment 3 (Exp.3): 20 eggs of H. meridionalis
were placed in an aquarium with 300 ostracods.
Experiment 4 (Exp.4): 20 eggs of H. meridionalis
were placed in an aquarium with 300 ostracods and
sprigs.
Experiment 5 (Exp.5): 21 eggs of B. bufo and 21
eggs of H. meridionalis were placed in the same
aquarium with 300 ostracods.
Experiment 6 (Exp.6): 12 tadpoles of B. bufo and 12
tadpoles of H. meridionalis were placed in the same
aquarium with 300 ostracods and sprigs. All tadpoles
were at Gosner stage 26-30 (sensu Gosner 1960).
Experiment 7 (Exp.7): especially given the amphibian eggs may dissolved quickly under the action of
aquatic fungi (e.g. Kiesecker and Blaustein 1995), 15
toad eggs were placed in a box without ostracods or
sprigs to verify whether other factors could cause the
disappearing of amphibian eggs.
In experiments 1, 2, 3, 4 and 5, we recorded the
number of amphibian eggs every 12 h for a period of
7 days. In experiment 6 and 7, we recorded the number
of amphibian tadpoles or eggs only at the beginning
and at the end of the experiment (i.e. after 7 days).
In order to evaluate whether the difference in the
level of ostracod predation upon eggs or tadpoles in
the different experiments was statistically significant,
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Aquat Ecol
we processed the final results (i.e. the number of egg
remained in a couple of boxes, or in the same box in
the Exp.5 and Exp.6) with the Fisher’s exact test
using StatisticaÒ ver. 5.0 (Statistica package, Statsoft
Inc., USA).
In particular, we tested the results of Exp.1
versus Exp.2 and Exp.3 versus Exp.4 to highlight
the possible preferences between amphibian eggs and
alternative food. We also tested the results of Exp.5
and Exp.6 to disclose preferences showed by ostracods between two sources of amphibian eggs (toad and
treefrog) as food.
fluctuating physical and chemical parameters (Lahr
1997). The mussel shrimp Heterocypris sp., in
particular, is highly tolerant to different environmental conditions, as expected in freshwater species with
a wide geographical distribution (Yılmaz and Külköylüoğlu 2006). Furthermore, dechlorinated tap water
is often used for freshwater crustaceans (De Meester
and Dumont 1989; Hanazato and Ooi 1992; Oda et al.
2007) and tadpoles (e.g. Kiesecker et al. 1996;
Saidapur et al. 2009) in ecotoxicological and ecological laboratory experiments. This suggests that the
use of tap water in our experiment did not alter
significantly the results.
Results
Interactions between ostracods and amphibians
In the control experiment (Exp.7), we did not observe
decreasing of amphibian egg number, as we did not
observe any difference in the number of live eggs
at the beginning and at the end of the treatment.
The rate of predation showed by ostracods versus
amphibian eggs, in different conditions, is reported in
Fig. 3. The number of common toad eggs preyed
upon by ostracods differed significantly if alternative
vegetable food was available (Exp.1 vs. Exp.2, twotailed Fisher’s exact test, P = 0.009). Conversely, no
significant differences were detected when treefrog
eggs and alternative food were provided (Exp.3 vs.
Exp.4, two-tailed Fisher’s exact test, P = 0.096).
Finally, if ostracods could choose between toad
and treefrog eggs, they did not show any feeding
preference (Exp.5, two-tailed Fisher’s exact test,
P = 0.744). However, when they were provided
with tadpoles of B. bufo and H. meridionalis (plus
incrusted sprigs), ostracods preyed significantly more
on toad larvae than on treefrog larvae (Exp.6, twotailed Fisher’s exact test, P = 0.005).
Amphibian eggs and larvae are eaten by a wide range
of specialised and occasional consumers. However,
no literature records include ostracods (Gunzburger
and Travis 2005; Romano and Di Cerbo 2007). Given
that in the control experiment (Exp. 7), the amphibian
eggs were not dissolved by fungi (egg number
remained unvaried), the decrease in amphibian eggs
observed in the experiments was because of predation
by Ostracods, confirming our field observations.
Freshwater ostracods usually prey small invertebrates (Deschiens et al. 1953; Deschiens 1954; Cohen
1982; Cohen and Kornicker 1987; Janz 1992).
Although swarms of freshwater ostracods on larger
animals have been recorded, in these cases, predation
was not observed. In fact, despite the high number of
ostracods observed on a single amphibian reported in
the literature, i.e. on specimens of Yellow bellied
toad (Bombina variegata), Smooth newt (Lissotriton
vulgaris) and Crested newt (Triturus cristatus; Seidel
1989), there was neither evidence that the ostracods
were attacking toads or newts nor evidence that they
could cause them injuries or death. Probably, ostracods were feeding on the amphibian skin secretions,
although the may use amphibians also for dispersion,
as suggested by Seidel (1989). However, in our field
observation, the tadpoles were completely immobilised by ostracods (Fig. 2) and thus they were unable
to act as vector.
Morphological adaptation to scavenging, the most
common feeding strategy in the ostracod order Podocopa, includes the possession of powerful furcal rami
(also called uropod). Although the uropod is used for
locomotion, it may also have several major functions in
Discussion
Experimental conditions
The use of tap water in our experiments could
influence the trophic behaviour of the ostracods.
However, organisms adapted to life in temporary
freshwater ponds, probably suffer in the slightest
degree for artificial changes of their aquatic mean
because they are well adapted to unpredictable and
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Aquat Ecol
Exp. 1 vs Exp. 2
24
Exp.1: toad eggs
22
Exp.2: toad eggs and algae
20
18
16
14
N
12
10
8
6
4
2
0
0
12
24
36
48
60
72
84
96
108
120
132
144
156
168
hours
24
Exp. 3 vs Exp. 4
22
Exp. 3: treefrog eggs
20
Exp. 4: treefrog eggs and algae
18
16
14
N
12
10
8
6
4
2
0
0
12
24
36
48
60
72
84
96
108
120
132
144
156
168
hours
24
Experiment 5
22
Toad eggs
20
Treefrog eggs
18
16
14
N
12
10
8
6
4
2
0
0
12
24
36
48
60
72
84
96
108
120
132
144
156
168
hours
days
I
II
III
IV
V
VI
VII
Fig. 3 Histograms showing the initial number of amphibian eggs (Bufo bufo and Hyla meridionalis) in five experiments and their
decreasing due to predation by ostracods (Heterocypris incongruens). See the text for further details
the feeding process, including holding on carcasses of
large animals and their cutting and dismembering
(Parker 1997). Coherently, H. incongruens often attacks
small invertebrates (Ganning 1971; Meisch 2000) and
feeds on carcasses of water birds (Reichholf 1983) and
amphibians (D. Ottonello unpublished data).
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Aquat Ecol
Palatability of amphibian eggs
The eggs and larvae of the two amphibian species
chosen in our study are considered different in their
palatability. Eggs and tadpoles of Bufo are generally
considered to be unpalatable, in particular to many
vertebrates and invertebrates with chewing mouth
parts (e.g. Henrikson 1990; Licht 1968; but see also
the criticism to this consideration in Gunzburger and
Travis 2005), while eggs and larvae of Hyla are
unanimously considered palatable (e.g. Gunzburger
and Travis 2005; Heuesser 1970; Licht 1969;
McDiarmid and Altig 1999).
Henrikson (1990) found that the eggs of B. bufo
were palatable to invertebrate predators with sucking
mouth parts while tadpoles were attractive to most
predators. Although ostracods may be considered as
possessor of a chewing apparatus (Meisch 2000), our
results show that they were not repulsed by Common
toad eggs, embryos and tadpoles. Thus, early life
stages of Bufo were not found unpalatable at a higher
rate than other taxa, confirming earlier observations
by Gunzburger and Travis (2005).
Ostracods seemed to prefer toad tadpoles to treefrog
larvae. Woodward (1983) found that reduced mobility
of tadpoles lowers mortality risk from invertebrate
predators. However, Bufo and Hyla larvae, at the
development stages included in our study, have similar
mobility (Chovanec 1992). Conversely, locomotor
mode of Bufo tadpoles, which use the whole tail for
locomotion, could makes them easier detectable than
Hyla tadpoles, which move mainly the tail tip and
therefore move less water mass (Heyer et al. 1975;
Chovanec 1992).
Furthermore, there are other factors which may
contribute in determining the different predation level
suffered by tadpoles of these two amphibian species.
First of all, the frontal position of the eyes of Bufo
tadpoles allows a restricted visual field in comparison
with that of Hyla (see Arnold and Ovenden 2002).
Second, the toad tadpoles, in comparison with other
anuran species, exhibit lower manoeuvrability, lower
speed of swimming and lower predator avoiding
movement because they have less axial musculature
(Wassersug and von Seckendorf Hoff 1985; Saidapur
et al. 2009). Third, Bufo tadpoles prefer to swim in the
whole water column in contrast to Hyla larvae which
prefer water surface (see Chovanec 1992). Differently
to other anurans, B. bufo tadpoles lack constitutive
123
morphological defences against invertebrate predators, which are more dissuaded by morphological and
behavioural defences than by chemical deterrents
(Álvarez and Nicieza 2006). Overall, ostracods, as
other aquatic invertebrate predators, seem to prefer
toad tadpoles to other anuran larvae, probably because
they are more easily detectable by mean of visual and
tactile stimuli.
Conclusions
The knowledge, although sometimes anecdotal, of a
trophic connection between two (or more) taxa, i.e.
nodes in the food web, is the fundamental prerequisite for further and more complex studies which
intend to understand community ecology. Recently
redefined food webs invalidated partially some earlier
generalisations showing that long food chain and
omnivory are common in food web structure (e.g.
Martinez 1991; Schmid-Araya et al. 2002).
The consumption of a given prey item depends by
the predator hunger level and by the availability of
alternative food (Gunzburger and Travis 2005).
Amphibian eggs and larvae could be considered an
alternative trophic resource for ostracods, if other type
of food is lacking. Although less amphibian eggs were
consumed when alternative trophic resource was
provided, in all tests that we carried out, a portion of
amphibian eggs was also eaten by ostracods. Presumably, the prey–predator relationship we report here
cannot be merely considered as an occasional behaviour, but it is likely a widespread feeding strategy, at
least when ostracods and amphibians are abundant in
the same aquatic site.
Prey–predator interactions between Ostracoda and
Amphibia were so far considered unidirectional, with
ostracods relegated in the role of preys and amphibians (both at larval and adult stages) in the role of
predators (e.g. Cicort-Lucaciu et al. 2005; Dutra and
Callisto 2005; Spencer and Blaustin 2001). However,
trophic web where ostracods and amphibians are
involved are proved to be more complex, and a
variety of feeding relationships between these taxa is
now reported. Ostracods may pass unharmed through
the amphibian gut (being eliminate in the faeces
and thus potentially colonising new habitats, see
Hartmann 1975; Lopez et al. 2002). Furthermore, we
report for the first time that they are able to behave
as active predators on amphibians. In freshwater
Aquat Ecol
ecosystems, the answer to the question ‘‘who is the
prey, Amphibia or Ostracoda?’’, is not straightforward and unambiguous.
Acknowledgments We would like to thank Fabrizio Oneto for
the help during field survey and Giampaolo Rossetti for the
taxonomic determination of ostracods and suggestions. Federico
Marrone, Antonio Ruggiero and Sebastiano Salvidio provided
useful suggestions and stimulating discussions. We are indebted
to Ylenia Chiari, Filippo Barbanera and Angelo G. Solimini
for the linguistic revision and for the critical reading of the
ms. Finally, we would like to thank two other anonymous
reviewers for their precious suggestions during the revision of
the manuscript.
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