Herpetology Notes, volume 12: 1073-1076 (2019) (published online on 29 October 2019)

The freshwater crab Liberonautes latidactylus (de Man, 1903) preys on adult Allen’s Giant , Conraua alleni (Barbour and Loveridge, 1927)

Marvin Schäfer1,*, Joseph Doumbia2, and Mark-Oliver Rödel1

Post-metamorphic anuran are preyed therein), the role of freshwater crabs as predators is upon by many vertebrates (reviewed by Toledo et less well documented, but particularly for , might al., 2007) and invertebrate predators (Toledo, 2005; be underrated. Freshwater crabs are known to feed on Wells, 2007). Amongst invertebrates, spiders are eggs (Hayes, 1983), tadpoles (Gray and Christy, 2000), most frequently listed (for a recent review concerning juvenile (Affonso and Signorelli, 2011) and adult African examples, see Babangenge et al., 2019), but frogs (Tsuji, 2005; Rosa et al., 2014; Wehrtmann et al., unusual anuran specialists like the carabid beetles 2019). Hence, all anuran life stages are potential prey Epomis have become known as well (Wizen and Gasith, of freshwater crabs. Interestingly, the ability to hunt 2011). Although Diesel (1989) reports an example seems to decrease in freshwater crabs exceeding 25 mm of a tree-hole breeding crab, occasionally preying on of carapace width. Large individuals are supposed to be anuran eggs and tadpoles, crustaceans are only rarely less agile, and hence less effective in capturing elusive mentioned as predators. Toledo (2005) only prey (Williams, 1962; Williams, 1965; Dobson, 2004). lists one of decapod crab as a predator of post- Consequently, one might assume that larger and agile metamorphic anurans. More recently, Pyke et al. (2013) frog species are an unlikely prey of crabs. Herein, we report the predation of an adult frog by a marine crab. present a contradicting observation. Rosa et al. (2014) and Wehrtmann et al. (2019) give On the river Veblo (7.68936° N, 8.35516° W, 875 m evidence for predation of adult frogs by freshwater a.s.l.), Mount Nimba Strict Nature Reserve, Guinea, we crabs in Madagascar and Costa Rica, respectively. observed at 9 pm on 18 June 2019, a large freshwater Freshwater crabs are usually herbivorous scavengers, crab (carapace width approx. 80 mm), with an adult feeding on plant material, or shredding other organic Conraua alleni in its right pincer (Fig. 1). The frog was materials (Williner et al., 2014). Therefore, and because grabbed right behind its head (Fig. 1b) with the tip of of their consumption by many other predators, they are the crab’s pincer possibly piercing the spinal column. considered to play an important role in trophic cascades The frog did not show any movements beyond the head. of tropical freshwater systems (Wehrtmann et al., Usually, this aquatic frog species, maximum size about 2019). Although it is known that most freshwater crabs 70 mm snout-vent-length (Channing and Rödel, 2019), will readily enrich their plant diet with protein, such tries to free itself by forceful pushes with their hind as dead and living invertebrates as well as vertebrates legs when caught. Although we could not observe the (Dobson, 2004; Wehrtmann et al., 2019; and references hunting, it was clear that the catch must have happened when the frog was alive, as the frog was still alive and sometimes gasping (see Supplementary video, DOI: 10.7479/mjv0-wa89). When encountered, the crab was sitting with its prey on a small rock on the riverbanks. The crab initially was tearing flesh from the frog’s legs, but then stopped when getting too irritated by us, i.e. when 1 Museum für Naturkunde Berlin, Leibniz Institute for placing a pencil for size comparison beside it (Fig. 1c, Evolution and Biodiversity Science, Invalidenstraße 43, supplementary video). It then slowly orientated towards 10115 Berlin. 2 ONG EnviSud Guinée, Quartier Kipé T2 Commune de a small crevice between the rocks and disappeared, not Ratoma, 530 BP 558 Conakry. allowing further observations. In total, we observed the * Corresponding author. E-mail: [email protected] scene for 50 seconds. 1074 Marvin Schäfer et al.

Figure 1. The crab Liberonautes latidactylus preying on the frog Conraua alleni; a) the crab tearing flesh from the frog’s leg; b) note the depression on the frog’s head where the pincers are placed; c) the pencil’s maximal horizontal height is 9.8 mm (c extracted from video sequence).

Figure 2. Injuries in three individuals of Odontobatrachus arndti from the Nimba Mountains. a) Partial amputation of the hind limb tarsus (calcaneum missing); b) complete amputation of hind limb tarsus (and subsequent structures); c) complete amputation of the forelimb metatarsus.

Based on morphological features recognisable in the Cumberlidge, 1999). A recent study, including data from photographic and video material, as well as observed on Veblo River, found only one decapod species in the area similar specimens from the same river, we could identify that matches the observed size of our crab (Daniels et the crab’s as Liberonautes Bott, 1955 (compare al., 2016). We thus conclude that our observation was The freshwater crab Liberonautes latidactylus preys on adult Allen’s Giant Frog 1075 based on Liberonautes latidactylus. This species has References lately become known to be an important food source for Affonso, I.D.P., Signorelli, L. (2011): Predation on frogs by the local chimpanzee population (Koops et al., 2019). the introduced crab Dilocarcinus pagei (Stimpson, 1861) Beside an undetailed, casual note on predation of the (Decapoda, Trichodactylidae) on a neotropical floodplain. Puddlefrog krefftii Boulenger, 1909 Crustaceana 84: 1653–1657. by an unidentified crab species in Tanzania (Hirschmann Babangenge, G.B., Jocqué, R., Masudi, F.M., Rödel, M.-O., Burger, and Hödl, 2006), this is the first report of an African M., Gvoždík, V., Pauwels, O.S.G. (2019): Frog-eating spiders in the Afrotropics: an analysis of published and new cases. Bulletin freshwater crab feeding on a life adult frog. However, of the Chicago Herpetological Society 54(3): 57–63. more interesting is the frog species that fell prey to Channing, A., Rödel, M.-O. (2019): Field guide to the frogs and the crab. Conraua alleni is a very skittish, shy and other amphibians of Africa. Struik Nature, Cape Town. fast frog, and at least for humans is the most difficult Cumberlidge, N. (1999): The freshwater crabs of West Africa: anuran species to catch on the Nimba Mountains (pers. Family Potamonautidae. Éditions de l’Institut de Recherche experience of the authors). The crab’s victim was an pour le Développement, Collection Faune et Flore Tropicale No. 236, Paris. adult, well-nourished individual with an approximate Daniels, S.R., McLeod, C., Carveth, C., Mexim, K.K., Cumberlidge, snout-vent length of 70 mm not showing any obvious N. (2016): Examining the evolutionary relationships amongst sign of pre-existing disease or injury. three species of West African freshwater Crabs Liberonautes This observation was the first of its kind in many years Bott, 1955 (Brachyura, Potamonautidae) using mtDNA sequence of riparian surveys in the region. Likewise, literature data. Journal of Crustacean Biology 36: 731–739. research revealed that predation on vertebrates (frogs) Diesel, R. (1989): Parental care in an unusual environment: Metopaulias depressus (Decapoda, Grapsidae), a crab that lives by freshwater crabs is rather the exception than the in epiphytic bromeliads. Behavior 38: 561–572. rule. However, tropical freshwater crabs prey on small Dobson, M. (2004): Freshwater crabs in Africa. Freshwater vertebrates (Maitland, 2003; Tsuji, 2005; Affonso and Biological Association 2004, Freshwater Forum 21: 3–26. Signorelli, 2011; Wehrtmann et al., 2019; Rosa et al., Gray, H.M., Christy, J.H. (2000): Predation by the grapsid crab, 2014) and other aquatic or riparian frogs, living in Armases angustum Smith, 1870, on tadpoles of the green poison sympatry with C. alleni, like Astylosternus occidentalis frog, Dendrobates auratus Girard, 1855. Crustaceana 73: 1023– 1025. Parker, 1931 and Odontobatrachus arndti Barej et al., Hayes, M.P. (1983): Predation on the adults and pre-hatching stages 2015, might even be at higher risk of being preyed by of glass frogs (Centrolenidae). Biotropica 15: 74–76. large freshwater crabs. In fact, injuries like amputations, Hirschamnn, W., Hödl, W. (2006): Visual signaling in occasionally recorded on the latter species (Fig. 2), Phrynobatrachus krefftii Boulenger, 1909 (Anura: Ranidae). resemble crab related injuries described by Rosa et Herpetologica 62(1): 18–27. al. (2014). Based on the reported observations, the Koops, K., Wrangham, R.W., Cumberlidge, N., Fitzgerald, M.A., van Leeuwen, K., Rothman, J.M., Matsuzawa, T. (2019): Crab- hypothesis of stolid, slowly scavenging freshwater fishing by chimpanzees in the Nimba Mountains, Guinea. crabs should be re-evaluated. Journal of Human Evolution 133: 230–241. Maitland, D.P. (2003): Predation on snakes by the freshwater land Acknowledgements. The observation was made during an annual crab Euaniela garmani. Journal of Crustacean Biology 23: amphibian monitoring conducted for the Société des Mines de Fer 241–246. de Guinée (SMFG). The fieldwork was surveyed by an official Pyke, G.H., Ahyong, S.T., Fuessel, A., Callaghan, S. (2013): Marine of the Centre for the Management of the Environment of Mount crabs eating freshwater frogs: Why are such observations so Nimba-Simandou (CEGENS) under the responsibility of the rare? Herpetology Notes 6: 195–199. Ministry of Environment, Water and Forests and Sustainable Rosa, G.M., Sabino-Pinto, J., Noël, J., Andreone, F. (2014): Development. Research permit N° 006/MESRS/DGERIST/2019 Predation on the treefrog Boophis rufioculis (Anura, ) had been granted by the Ministère de l’Enseignement Supérieur by the freshwater crab Hydrothelphusa sp. (Decapoda, et de la Recherche Scientifique (MESRS). We thank SMFG Potamonautidae) in Madagascar. Crustaceana 87: 890–894. for providing organisational as well as financial support. The Toledo, L.F. (2005): Predation of juvenile and adult anurans work of our long-term field-assistants, Mr. Kaman Camara, Mr. by invertebrates: current knowledge and perspectives. François Gbêmou, and Mr. Blaise Pivi is highly valued. Likewise, Herpetological Review 36: 395–400. the helpful assistance of Mr. Famé Koulémou (SMFG) and Mr. Toledo, L.F., Ribeiro, R.S., Haddad, C.F.B. (2007): Anurans as Celestin Iromou (CEGENS) is thankfully accredited! We greatly prey: an exploratory analysis and size relationships between acknowledge the conscientious, thorough work of the reviewers. predators and their prey. Journal of Zoology 271: 170–177. Tsuji, H. (2005): Predation on a fanged frog (Limonectes kuhlii) by a freshwater crab (Candidiopotamon rathbuni). Herpetological Review 36: 125–127. 1076 Marvin Schäfer et al.

Wells, K.D. (2007): The ecology and behavior of amphibians. University of Chicago Press, Chicago. Wehrtmann, I.S., Hernández-Díaz, D., Cumberlidge, N. (2019): Freshwater crabs as predators and prey: the case of Ptychophallus uncinatus Campos and Lemaitre, 1999 (Brachyura, Pseudothelphusidae) from Costa Rica, Central America. Latin American Journal of Aquatic Research 47: 18–26. Williams, T.R. (1962): The diet of freshwater crabs associated with Simulium neavei in East Africa II.: The diet of Potamon berardi from Mount Elgon, Uganda. Annals of Tropical Medicine and Parasitology 56: 362–367. Williams, T.R. (1965): The diet of freshwater crabs associated with Simulium neavei in East Africa. III.: The diet of Potamonautes niloticus and of an unidentified crab species from Mount Elgon, Uganda. Annals of Tropical Medicine and Parasitology 59: 47–50. Williner, V., Carvalho, D.A., Collins, P.A. (2014): Feeding spectra and activity of the freshwater crab Trichodactylus kensleyi (Decapoda: Brachyura: Trichodactylidae) at La Plata basin. Zoological Studies 53: 71. Wizen, G., Gasith, A. (2011): Predation of amphibians by carabid beetles of the genus Epomis found in the central coastal plain of Israel. ZooKeys 100: 181–191.

Accepted by Werner Conradie