The scent of predation: amphibian embryos respond to predator cues
Parental care is relatively rare within amphibians with documented cases only occurring within 20% of salamanders and 6% of anurans. Those that do provide parental care usually lay small clutches of relatively large eggs and one or more of the parents provide protection from potential predators in the form of egg attendance and transport. The vast majority of amphibian species lay their eggs providing little protection from predators. However, the developing embryos and newly emerged larvae may respond to changing environmental conditions including temperature and light. There is increasing evidence that developing embryos can respond to the presence of predators in a variety of ways such as altering hatching rate and size or stage of development.
The streamside salamander Ambystoma barbouri from the United States lays its eggs on the underside of rocks at the bottom of fast flowing streams (Figure 1). The newly emerged larvae are highly vulnerable to predation from flatworms and rates of larval mortality are high. However, when the salamander embryos come close to hatching they are able to detect the presence of the flatworms through chemical cues emitted by the predator. If the embryos detect that flatworms are nearby, they postpone hatching, resulting in the salamander larvae emerging at a larger size and a later stage of development. This results in faster swimming speeds and an increased ability to evade the flatworms. This plasticity in development relative to the presence of predators is a highly adaptive response, allowing greater survival of this species.
Figure 1: The streamside salamander Ambystoma barbouri from the United States. (Insert: the eggs which are laid on the underside of rocks at the bottom of fast flowing streams)
When eggs are prone to predation, the responses of the developing embryos may be different. The southern leopard frog Lithobates sphenocephalus from the United States breeds in ponds and other freshwater habitats and the eggs are vulnerable to attack from crayfish (Figure 2). When in the presence of these predators, eggs of the leopard frog increase their rate of development, resulting in a faster hatching time and larvae are able to escape at a smaller stage of development. In addition, if egg masses are being attacked, the mechanical stimulation, along with chemical cues from conspecific larvae, triggers hatching of the remaining embryos. Stress chemicals released by conspecifics who are being attacked has been documented in other amphibian species. If embryos of the common frog Rana temporaria are under attack, they release chemical alarm signals which trigger the hatching of nearby embryos. Although these may not be at their full stage of development, it allows these newly hatched larvae to move away from the point of attack.
Figure 2: A southern leopard frog Lithobates sphenocephalus from the United States laying her eggs in a pond.
Although the responses of embryos and larvae are usually adaptive, on occasion, non-adaptive responses to the presence of predators may occur. Predator-induced stress has been documented in a number of amphibian species and may occur in synergy with other stressors such as pollutants, UV radiation and temperature changes. For example, newly hatched gray treefrog tadpoles Dryophytes versicolor developing in the ponds of south-eastern Canada which had been contaminated with the pesticide carbaryl, exhibit a stress response, resulting in mortality. This mortality is further increased when in the presence of the predatory salamander Ambystoma maculatum. A similar predator-induced stress response has been documented in the great crested newt Triturus cristatus in the UK. Under laboratory conditions embryos of this species exhibit significantly higher mortality when in the presence of the chemical cues from predatory three-spined sticklebacks. This increase in mortality may have impacts on larval recruitment and subsequent population dynamics.
Both adaptive and non-adaptive responses to predators in the early stages of development are increasingly being documented in amphibian species. In general we know very little about how widespread these occur and the potential positive or negative impacts at the population level. In particular, further research examining the synergies between various stressors such as UV or chemical contaminants with predator chemical cues is required and may increase our understanding of how amphibian species will respond in a changing environment.
References
Crump, M. L. (1995) Parental Care. In: H. Heatwold (ed) Amphibian Biology Volume 2: Social Behaviour. Pp: 518-567. Surrey Beatty & Sons, Australia.
Jarvis, L. E. (2010) Non-consumptive effects of three-spined stickleback (Gasterosteus aculeatus) on great crested newt embryos (Triturus cristatus). Herpetological Journal, 20 (4): 271-275.
Mandrillon, A. L. & Saglio, P. (2007) Effects of embryonic exposure to conspecific chemical cues on hatching and larval traits in the common frog (Rana temporaria). Chemoecology, 17: 169-175.
Relyea, R. A. & Mills, N. (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences of the USA, 98 (5): 2491-2496.
Saenz, D., Johnson, J. B., Adams, C. K. & Jaylon, G. H. (2003) Accelerated hatching of Southern Leopard Frog (Rana sphenocephala) eggs in response to the presence of a crayfish (Procambarus nigrocinctus) Copeia, 2003 (3): 446-649.
Sih, A. & Moore, R. D. (1993) Delayed hatching of salamander eggs in response to enhanced larval predation risk. American Naturalist, 142: 947-960.