Download Marine crabs eating freshwater frogs

Herpetology Notes, volume 6: 195-199 (2013) (published online on 26 April 2013)
Marine crabs eating freshwater frogs:
Why are such observations so rare?
Graham H. Pyke1,2,3,*,Shane T. Ahyong2,4, Adriana Fuessel5 and Susanne Callaghan6
Abstract. We present the first records of predation by a marine crab (Leptograpsus variegatus) on a freshwater frog (Litoria
aurea), and consider why such observations are so rare. We have studied two frog species on an island where breeding occurs
in ponds near the ocean, and often observed marine crabs at these ponds. Given the broad diet and speed of these crabs, they
would be expected to prey on various life-stages of these frogs. However, despite spending much time, both during the day
and at night, surveying tadpoles and frogs, we have observed crabs attempting to prey on tadpoles on only a few occasions and
on an adult frog just once. Possible reasons for the rarity of these observations include the crabs finding the tadpoles and frogs
distasteful and hence avoiding them, and the rapidity with which crabs can capture and consume prey or move out-of-sight
immediately after prey capture.
Keywords. Amphibia, Anura, Crustacea, Decapoda, foraging, diet.
Given that aquatic frogs generally inhabit freshwaters,
while crabs are mostly marine creatures, it seems hardly
surprising that these two kinds of animal rarely prey
on one another. There are, however, some situations
where crabs occur in freshwater and are preyed on by
frogs (Church, 1960; Premo and Atmowidjojo, 1987;
Barrios Quiroz and Casas-Andreu, 2003). In addition,
the Crab-eating Frog (Fejervarya cancrivora), which
is well known for its ability to live under conditions
of relatively high salinity (Gordon and Tucker, 1965;
Uchiyama et al., 1990; Ultsch et al., 1999), may include
marine crabs in its diet when foraging in brackish water
(Elliott and Karunakaran, 1974). Other frogs, such as
the Paradoxical Frog (Pseudis paradoxa) of Trinidad,
may similarly prey on marine crabs in situations where
the water is brackish (Downie et al., 2010).
There are fewer reports of crabs preying on various
life-stages of frogs (Hayes, 1983; Gray and Christy,
2000; Tsuji, 2005; Affonso and Signorelli, 2011), all
1 School of the Environment, University of Technology Sydney,
Broadway NSW 2007, Australia
2 Australian Museum, Sydney, NSW 2010, Australia
3 Department of Biological Sciences, Macquarie University,
Ryde NSW 2109, Australia
4 School of Biological, Earth & Environmental Sciences,
University of New South Wales, Kensington NSW 2052,
Australia
5 School of Environmental and Life Sciences, University of
Newcastle, Callaghan NSW 2308, Australia
6 Hunter Area, NSW National Parks and Wildlife Service,
Nelson Bay NSW 2315, Australia
* Corresponding author; e-mail: [email protected]
of which involve freshwater crabs. Predation on an
adult Fanged Frog (Limonectes kuhlii) by the crab
(Candidiopotamon rathbuni) was observed in Taiwan
(Tsuji, 2005). The crab Dilocarcinus pagei preys on
the frog Leptodactylus latrans in Brazil, as one was
observed feeding on an immature frog in the wild, adult
frogs have been observed with injuries attributable to
attempted predation by crabs, and these crabs have been
recorded killing and eating immature frogs when crabs
and frogs are housed together in captivity (Affonso
and Signorelli, 2011). The sesarmid crab Armases
angustum probably eats tadpoles of the Green Poison
Frog (Dendrobates auratus) because one of these crabs
was repeatedly observed in a tree-hollow containing
tadpoles of this frog species, and readily ate the
tadpoles, which lack the toxins found in adults, when
offered them in captivity (Gray and Christy, 2000). A
similar crab Armases roberti has been observed feeding
on eggs of the Glass Frog Centrolenella granulosa (see
Hayes, 1983).
Here we report our own extremely infrequent
observations of crabs feeding on tadpoles and attacking
an adult frog, and discuss possible reasons for such low
frequencies of such observations. Apparently, ours is the
first report of a marine crab preying, or attempting to
prey, on frog tadpoles and adults.
Broughton Island (latitude: 32°36΄58΄΄S; longitude:
152°19΄01΄΄E), which lies about 3 km off the eastern
coast of Australia and about 200 km north of Sydney,
is home to two species of aquatic frogs, the Green and
Golden Bell Frog Litoria aurea Lesson, 1829 and the
Striped Marsh Frog Limnodynastes peronii Duméril
196
and Bibron, 1841 (Pyke, 1999; Pyke and Miehs, 2001;
Pyke and Miehs, 2004; Pyke, 2005). On the mainland,
L. aurea is relatively rare and considered endangered,
while L. peronii is common, widespread and not
considered threatened with extinction (Pyke and White,
1999; Pyke and White, 2001). Here, both frog species
breed in ponds; there is no moving water suitable for
frog breeding.
For both frog species, most breeding ponds are close
to the ocean (i.e., 5−20 m from high tide line, about 1−3
m vertically above intertidal zone) and hence subject
to occasional large influxes of seawater when storm
conditions result in waves crashing over the rocks along
the shore (Pyke et al., 2002). Pond salinity may then
increase suddenly from a low level (i.e., <5 ppt) to a
level approaching that of sea water (i.e., ~34 ppt) (Pyke
et al., 2002). Tadpoles of both frog species are killed
when salinity exceeds about 8 ppt (Pyke et al., 2002)
and when the ponds occasionally dry out (Pyke et al.,
2002). Sometimes large numbers of dead and dying
tadpoles are observed (GHP, pers. obs.).
On the island, frogs of L. aurea and tadpoles of both
species are abundant (Pyke and White, 2001; Pyke
and Miehs, 2004; Pyke, 2005), conspicuous and easy
to capture, and so should be relatively vulnerable to
predation. During night-time frog surveys, totalling
about 900 person-hours, we have encountered about
9,500 L. aurea, commonly sitting on the ground
adjacent to a pond and occasionally floating in the
water, capturing almost all of them (i.e., 96%). During
the same surveys, we have encountered fewer L. peronii,
but been reasonably successful at capturing them (
i.e., about recorded 1,000 frogs, of which 73% were
captured). Tadpole densities sometimes reach about
10−15 per litre (Pyke and Rowley, 2008) and low water
turbidity (i.e., <50 nts), combined with relatively slow
tadpole movement, makes it easy to see and capture
them. The general ease with which we have been able
to observe and capture both frogs and tadpoles suggests
that potential predators could do likewise.
However, tadpole predators and predation have rarely
been observed. Wading birds, such as herons, that
could prey on tadpoles, have rarely been sighted on
the island. During about 900 person-hours of daytime
surveys, we have recorded White-faced Herons (Ardea
novaehollandiae) in the vicinity of frog ponds on just
two occasions, amounting to three birds in total. On
another occasion we witnessed a Silver Gull (Larus
novaehollandiae) catch and eat 2−3 tadpoles before
flying off. We have not observed any other potential
Graham H. Pyke et al.
avian predators. In addition, aquatic invertebrates, such
as dragonfly larvae, that may also be tadpole predators,
have been seldom encountered. Out of 700 occasions
when we recorded tadpoles in a pond, we simultaneously
recorded dragonfly larvae on just 18 occasions. We have
occasionally recorded adult L. aurea and Water Skinks
(Eulamprus quoyii) preying on tadpoles of L. peronii
and L. aurea, but only when the tadpoles have been
large and relatively abundant (Miehs and Pyke, 2001).
Similarly absent have been potential predators and
evidence of predation regarding adult frogs. Rats have
been frequently observed during night-time surveys
and they have elsewhere been observed to occasionally
prey on L. aurea (Pyke and White, 2001). However, on
Broughton Island, we have never observed an attack on
a frog by a rat. Furthermore, out of about 9,000 adult L.
aurea and 700 adult L. peronii that we have examined,
we have observed tooth marks, indicating attempted
predation, just once. We have not observed any other
signs of attempted predation on adult frogs.
On Broughton Island, predation on L. aurea appears
to be concentrated on the metamorph stage (i.e.,
metamorphosing frogs with both front and hind limbs,
but still having a noticeable tail). At times when
metamorphs have been observed emerging from ponds
in large numbers, Water Skinks (Eulamprus quoyii)
and adult L. aurea have been observed to congregate
at these ponds and prey on the metamorphs (Miehs and
Pyke, 2001; Pyke and Miehs, 2001). At the same times
we have heard the characteristic distress call emitted by
immature frogs when captured and held by a predator
(Miehs and Pyke, 2001).
Another potentially significant predator of tadpoles
and frogs is the Swift-footed Shore Crab Leptograpsus
variegatus (Fabricius, 1793). Though not previously a
focus of our studies, we have made and recorded a small
number of relevant observations described below.
On Broughton Island, this crab is common within the
intertidal zone and just above it, and 5−10 have often
been simultaneously observed in water near the edge
of the ocean, in pools of water near the ocean, or on
nearby rocks (GHP, pers. obs.). On six occasions we
have recorded the crab under the water in ponds that are
also used for breeding by frogs, with water salinity on
these occasions ranging widely from 1 to 30 ppt. Live
tadpoles were also present on two of these occasions;
dead tadpoles were present on one of them.
Despite spending much time observing frogs, tadpoles
and the places in which they live, we have rarely observed
foraging by crabs on them. We have so far spent about
Marine Crabs eating freshwater frogs: Why are such observatons so rare?
197
Figure 1. View from the side and above of a marine crab (Leptograpsus variegatus) observed holding an adult frog (Litoria aurea)
in its claws on Broughton Island. The abdomen and hind limbs of the frog can be seen. The frog had a SVL of 6.8cm and the crab
was similarly sized across its carapace. Photograph was taken by AF.
900 person-hours during daytime surveying ponds for
tadpoles and about the same amount of person-time
during night surveying for frogs. During the daytime
surveys we have recorded crabs eating both dead and
live tadpoles, on one occasion each. We assumed that
the crabs were eating or about to eat the tadpoles as they
were observed holding the tadpoles with their claws in
front of their mouths. On one occasion we watched a
crab stalk, capture and swallow a number of tadpoles.
The tadpoles were relatively small in comparison to
the size of the crabs. During the night-time surveys
we have, as described below, recorded crab attempted
predation on an adult frog just once.
An attack by a crab on an adult frog was observed
during a three-day visit to the island in October 2011.
At about 2100h one night, during frog surveys, we
encountered a crab that was holding an adult L. aurea
with its claws (fig 1). The crab was sitting on rock about
1m from a small pond (i.e., roughly 1 m long, 50 cm
wide and 25 cm deep) where L. aurea has often been
recorded breeding and about 18 m from the intertidal
zone. Upon encounter, we observed that there was
bubbling froth in front of the crab’s mouth and that the
frog was motionless. It was clear that the frog could not
possibly escape. We photographed the duo and then
put both in a small plastic bag, whereupon the crab
Graham H. Pyke et al.
198
released the frog. We found that the frog was alive, so
we processed it as per our normal routine (i.e., identify,
sex, weigh, measure snout-vent length [SVL]) and then
released it close to where we found the crab and frog.
The frog was a normal-sized male in breeding condition
(i.e., SVL = 6.8 cm; body weight = 22 g; nuptial pads
present and dark-coloured), that had been initially
captured and individually identified (through insertion
of a passive integrated transponder under the skin) on
the previous night. It showed no apparent signs of illhealth. We released the crab without measurement or
close examination. We noticed, however, that this crab
was about as large as any other observed individuals of
this species and that its carapace width was similar to
the SVL of the frog (fig. 1). We therefore estimate that
the carapace width of the crab was about 7 cm which
is close to the maximum carapace width that has been
recorded for this species (McLay, 1988).
On the one hand, it is hardly surprising that we have
observed predation, or attempted predation, by crabs
on both living tadpoles and frogs. The Swift-footed
Shore Crab can move rapidly and has been observed
capturing and overcoming a variety of active prey
including smaller crabs of the same or of other species
(STA, pers. obs.). Hence, it should have little difficulty
in catching tadpoles or frogs. Given the generally high
abundances of tadpoles, frogs and crabs, encounters
between crabs and both tadpoles and frogs should be
frequent, with ample opportunity for predation by crabs
to occur and to be observed.
However, considerably less congruent with what we
know about the frogs and the crabs is that we have so
seldom observed predation on tadpoles and frogs by
crabs. One possible explanation is that the tadpoles,
frogs or both are distasteful to the crabs, as secretion
from the skin of L. aurea is highly unpleasant to human
taste and quite painful when it gets into one’s eyes
(GHP, pers. obs.). However, secretion from the skin of
L. peronii has little or no such effect on humans (GHP,
pers. obs.) and some animals are able to eat various
amphibian species and life-stages that other animals
find toxic (Gunzburger and Travis, 2005).
It is possible that the crabs on Broughton Island are
foraging optimally and prefer to prey on alternate food
types because of a higher resulting net rate of energy
gain. Gastropods and barnacles, which generally
constitute most of the live animal material that they eat
(Skilleter and Anderson, 1986), are relatively small and
may require significant ‘handling time’. When feeding
on limpets, for example, a crab must attack individuals
that are in motion so that it can position its claws under
the rim of the limpet shell in order to dislodge the animal
and extract the tissue. The tissue yield from limpets
captured by a foraging crab would typically be no more
than 1 g (STA, pers. obs.), which is small in comparison
with an adult L. aurea, which generally weigh at least
15 g (GHP, pers. obs). Hence the net rate of energy
gain for a crab feeding on a limpet seems likely to be
relatively low. However, the handling time for a crab
to capture and consume a frog may be sufficiently high
that the resulting net rate of energy gain is lower than
it would be for crabs foraging on other potential prey
such as limpets.
However, it is also possible that our observations
have significantly underestimated the frequency of crab
predation on L. aurea as the crabs are generally easily
disturbed and, upon detecting our approach, could
move quickly, frog in claw, to a place where they would
be relatively hidden from view.
Future research might therefore focus on crabs as
well as frogs and tadpoles, evaluating whether Optimal
Foraging Theory provides a satisfactory explanation
for the apparent rarity of frogs and tadpoles in the diets
of the crabs on Broughton Island. Observing foraging
by crabs while minimising any disturbance to them
would provide a general understanding of how, where
and when they forage. In addition, observations and
experiments could lead to estimates of energy yields,
energy costs, handling times and encounter rates
associated with alternative prey for the crabs, which are
all typical ingredients in the optimal foraging approach
(Pyke, 2010).
Acknowledgements. This research was supported by the
Australian Museum and NSW National Parks & Wildlife Service.
It was carried out under Research Authority #09-04 as approved
by the Australian Museum Animal Care & Ethics Committee.
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Accepted by Philip de Pous