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

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

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

1 School of the Environment, University of Technology Sydney, Broadway NSW 2007, Australia

2 Australian Museum, Sydney, NSW 2010, Australia3 Department of Biological Sciences, Macquarie University,

Ryde NSW 2109, Australia4 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: Graham.Pyke@uts.edu.au

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.

Graham H. Pyke et al.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

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

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

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.

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 ill-health. 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.

References

Affonso, I.d.P., Signorelli, L. (2011): Predation on frogs by the introduced crab Dilocarcinus pagei Stimpson, 1861 (Decapoda, Trichodactylidae) on a neotropical floodplain. Crustaceana 84: 1653-1657.

Barrios Quiroz, G., Casas-Andreu, G. (2003): Rana zweifeli (Zweifel’s frog). Herpetological Review 34: 361.

Church, G. (1960): The effects of seasonal and lunar changes on the breeding pattern of the edible Javanese frog, Rana cancrivora Gravenhorst. Treubia 25: 215-233.

Downie, J.R., Hancock, E.G., Muir, A.P. (2010): The diet of the paradoxical frog Pseudis paradoxa in Trinidad, West Indies. Herpetological Journal 20: 111-114.

Graham H. Pyke et al.198

Accepted by Philip de Pous

Elliott, A.B., Karunakaran, L. (1974): Diet of Rana cancrivora in fresh water and brackish water environments. Journal of Zoology 174: 203-216.

Gordon, M.S., Tucker, V.A. (1965): Osmotic regulation in the tadpoles of the crab-eating frog (Rana cancrivora). Journal of Experimental Biology 42: 437-445.

Gray, H.M., Christy, J.H. (2000): Predation by the grapsid crab, Armases angustum (Smith, 1870), on tadpoles of the green poison frog, Dendrobates auratus Girard, 1855. Crustaceana 73: 1023-1025.

Gunzburger, M., Travis, J. (2005): Critical literature review of the evidence for unpalatability of amphibian eggs and larvae. Journal of Herpetology 39: 547-571.

Hayes, M.P. (1983): Predation on the adults and prehatching stages of glass frogs (Centrolenidae). Biotropica 15: 74-76.

McLay, C.L. (1988): Brachyura and crab-like Anomura of New Zealand. Leigh Laboratory Bulletin 22: 1-463.

Miehs, A., Pyke, G.H. (2001): Observations of the foraging behaviour of adult Green and Golden Bell Frogs (Litoria aurea). Herpetofauna 31: 94-96.

Premo, D.B., Atmowidjojo, A.H. (1987): Dietary patterns of the ‘crab-eating frog’, Rana cancrivora, in west Java. Herpetologica 43: 1-6.

Pyke, G.H. (1999): Green and golden bell frog. Nature Australia 26: 50-59.

Pyke, G.H., White, A.W. (1999): Population dynamics amongst frog species occurring in ponds occupied by the endangered Green and Golden Bell Frog Litoria aurea. Australian Zoologist 31: 230-239.

Pyke, G.H., Miehs, A. (2001): Predation by water skinks (Eulamprus quoyii) on tadpoles and metamorphs of the Green and Golden Bell Frog (Litoria aurea). Herpetofauna 31: 99-101.

Pyke, G.H., White, A.W. (2001): A Review of the Biology of the Green and Golden Bell Frog (Litoria aurea). Australian Zoologist 31: 563-598.

Pyke, G.H., White, A.W., Bishop, P.J., Waldman, B. (2002): Habitat-use by the Green and Golden Bell Frog Litoria aurea in Australia and New Zealand. Australian Zoologist 32: 12-31.

Pyke, G.H., Miehs, A. (2004): Effects of stomach flushing on recapture rates for Litoria aurea and Limnodynastes peronii. Herpetofauna 34: 81-83.

Pyke, G.H. (2005): The use of PIT tags in capture-recapture studies of frogs: A field evaluation. Herpetological Review 36: 281-285.

Pyke, G.H., Rowley, J.J.L. (2008): Interactions between tadpoles of Green and Golden Bell Frog Litoria aurea and Striped Marsh Frog Limnodynastes peronii. Australian Zoologist 34: 570-576.

Pyke, G.H. (2010): Optimal foraging theory - Introduction. In: Encyclopedia of Animal Behavior, p. 596-600. Breed, M.D., Moore, J., Eds., Oxford, Academic Press.

Skilleter, G.A., Anderson, D.T. (1986): Functional morphology of the chelipeds, mouthparts and gastric mill of Ozius truncatus (Milne Edwards) (Xanthidae) and Leptograpsus variegatus (Fabricius) (Grapsidae) (Brachyura). Australian Journal of Marine and Freshwater Research 37: 67-79.

Tsuji, H. (2005): Predation on a fanged frog (Limonectes kuhlii) by a Freshwater Crab (Candidiopotamon rathbuni). Herpetological Review 36: 125-127.

Uchiyama, M., Murakami, T., Yoshizawa, H. (1990): Notes on the development of the Crab-Eating Frog (Rana cancrivora). Zoological Science 7: 73-78.

Ultsch, G.R., Bradford, D.F., Freda, J. (1999): Physiology: Coping with the environment. In: Tadpoles. The Biology of Anuran Larvae, p. 189-214. McDiarmid, R.W., Altig, R., Eds., Chicago, University of Chicago Press.

Marine Crabs eating freshwater frogs:Why are such observatons so rare? 199