Mutualism: novel interactions between amphibians and other species
Mutualism is widespread within the animal kingdom and involves the close association between two organisms of different species in which both benefit. Within the Amphibia, there are a number of interesting and novel mutualistic interactions. These range from symbiosis with algae to interactions with predatory spiders and living with water buffalo. Our understanding of the range and extent of mutualistic interactions within amphibians remains relatively poorly understood and here we review some recent discoveries.
The mutualistic symbiosis between algae and embryos of the Spotted Salamander (Ambystoma maculatum) from North America was first reported more than 120 years ago (Figure 1). In this relationship, algae live inside the developing embryos and appear to provide many benefits to the salamanders including: earlier hatching, decreased mortality and reaching a larger size at hatching (Kerney et al., 2011). The algae are thought to gain through feeding on the nitrogenous wastes released by the embryos. Research by Kerney et al. (2011) found that this relationship is closer than originally thought. Through imaging and genetic experimentation, the researchers found that the algae actually invade the salamander tissues during embryo development and live inside the cells of the salamanders for a period of several weeks. At the end of larval development algal cell death occurrs in the majority of salamander cells. However, the researchers found genetic material of the algae in the reproductive tracts of adults, suggesting that the algae remains present and is transferred from one generation to another through the reproductive tract of the adults. This research raises the possibility of transfer of DNA between species and provides evidence of highly close relationships between two very different organisms.
Mutualism between larval amphibians and algae has been reported from other species. The tadpoles of the Dwarf American Toad (Bufo americanus charlesmithi) live in warm, shallow and temporary ponds which receive extended periods of sunlight (Figure 2). It has previously been observed that the tadpoles develop a bright green colouration during their development in these conditions. Tumlison & Trauth (2006) conducted a series of experiments and found that the green glow was the result of a symbiotic algae (Chlorogonium) living on the skin of the tadpoles. The tadpoles benefit through receiving oxygen from the algae who photosynthesise in the sunlight. Shallow, temporary ponds experience severe oxygen depletion during periods of high sunlight and warmth so as a result of obtaining oxygen from the algae, the tadpoles are able to survive longer in the ponds and reach a larger size before metamorphosis. In return, the algae received carbon dioxide from the tadpoles during respiration which aids in their growth.
The family of microhylid frogs from Sri Lanka comprises four genera and 10 species. Several of these species have restricted distributions and occur only in the Kanneliya Forest Reserve. The ecology of many of these microhylid frogs is poorly understood but adults appear to breed in tree holes. Karunarathna & Amarasinghe (2009) found a novel mutualistic interaction between the microhylid frog Uperodon nagaoi and two species of tarantula spider (Poecilotheria species). Both amphibian and tarantula species have been observed to share tree holes and it appears that both species protect each other’s eggs. The eggs of both the amphibian and tarantula are attacked by species of ants, mantids and other spider species. On several occasions Karunarathna & Amarasinghe (2009) recorded the tarantula attacking mantids that were feeding on U. nagaoi eggs. Similarly, individual U. nagaoi were observed predating ants that were feeding on the eggs of the tarantula. In addition, the tadpoles of U. nagaoi appeared to benefit from the remains of predated insects falling into water where they were developing.
Many species of herbivorous vertebrate harbour large populations of nematode worms in their guts. Herbivorous tadpoles are no exception with several thousand species of nematode being recorded from larvae. Several researchers have proposed that some species of nematodes may be mutualistic and provide benefits to their host. This appears to be the case with American Bullfrog (Lithobates catesbeiana) tadpoles which harbours the nematode (Gyrinicola batrachiensis) during its larval stage. Research by Pryor & Bjorndal (2005) found that America Bullfrog tadpoles infected with this nematode increased their rate of development by approximately 16 days, allowing the tadpoles to metamorphose earlier than tadpoles without the nematodes. This has many benefits as this promotes higher survival and subsequent reproductive success of the newly metamorphosed froglets. There could be two main reasons to explain this increase in development. First, the increase in gut size to allow the nematode to live may result in increased food intake and absorption by the tadpole. Second, the nematode increases rate of food fermentation in the gut, which allows the tadpole to absorb more food. The results of this study highlights that some gastrointestinal nematodes inhabiting the gut regions of other herbivores may have a beneficial effect on digestion and nutrition in those hosts.
A final form of novel mutualism has been observed between Marsh Frogs (Pelophylax ridibundus) and the Anatolian Water Buffaloes (Bubalus bubalis) in Turkey (Figure 3). Zduniak et al. (2017) reported a unique behaviour in the frogs where individuals climbed up the fur and onto the backs and heads of the buffaloes where they appeared to be predating flies. Up to 31 frogs were observed feeding on a single buffalo at any one time (Zduniak et al., 2017). It appears that both species benefit from this interaction since the frogs gain food and the buffalo has flies removed which may cause irritation. This appears to be the first record of such interaction between these two species and highlights that novel mutualistic interactions may occur more widely between amphibians and other species.
Tumlison, R. & Trauth, S.E. (2006) A novel facultative mutualistic relationship between bufonid tadpoles and flagellated green algae. Herpetological Conservation and Biology, 1 (1): 51-55.
Karunarathna, D.M.S.S. & Amarasinghe, A.A.T. (2009) Mutualism in Ramanella nagaoi Manamendra-Arachchi & Pethiyagoda, 2001 (Amphibia: Microhylidae) and Poecilotheriam species (Arachnida: Thereposidae) from Sri Lanka. Taprobanica, 1 (1): 16-19.
Kerney, R., Kim, E., Hangarter, R.P., Heiss, A.A., Bishop, C.D. & Hall, B.K. (2011) Intracellular invasion of green algae in a salamander host. PNAS, 108 (16): 6497-6502.
Pryor, G.S. & Bjorndal, K.A. (2005) Effects of the nematode Gyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism. Journal of Experimental Biology, 303A: 704–712.
Zduniak, P., Erciyas-Yavuz, K. & Tryjanowski, P. (2017) A possible mutualistic interaction between vertebrates: frogs use water buffaloes as a foraging place. Acta Herpetologica, 12 (1): 113-11.