Top-down effects on antagonistic inducible defense and offense

• Published in: Ecology (Durham) Vol. 90; no. 5; pp. 1217 - 1226
• Main Authors: Kishida, Osamu, Nishimura, Kinya
• Format: Journal Article
• Language: English
• Published: Washington, DC Ecological Society of America 01-05-2009
• Subjects: Aeshna; Aeshna nigroflava; Animal and plant ecology; Animal cognition; Animal, plant and microbial ecology; Animals; Anura - physiology; arms race; Biological and medical sciences; Caudata; coevolution; Community ecology; defensive behavior; Ecological genetics; Ecology; Evolution; Food Chain; Freshwater; Fundamental and applied biological sciences. Psychology; gape-limited predation; General aspects; Hynobius retardatus; Insecta - physiology; intraguild predation; Larva - physiology; larvae; Marine ecology; morphological change; Mortality; multiple predators; Odonata; phenotype; Phenotypes; phenotypic plasticity; Phenotypic traits; Predation; predation risk; predator-prey relationships; Predators; Predatory Behavior; Rana; Rana pirica; Reptiles & amphibians; Salamanders; salamanders and newts; Synecology; Tadpoles; top predator; trait-mediated indirect interactions; traits; trophic polyphenism; Urodela - physiology; Japan; Interaction; Polyphenism; Phenotypic plasticity; top predator; Trophic relation; arms race; Coevolution; Guild; Induced defense; multiple predators; Top down control; gape-limited predation; intraguild predation; Morphological change; Predator; Predation; Predation risk; trait-mediated indirect interactions; trophic polyphenism
• ISSN: 0012-9658; 1939-9170
• DOI: 10.1890/08-0238.1

Antagonistic phenotypic plasticity may strongly influence trait evolution in tightly interacting predator-prey pairs as well as the role that trait plasticity plays in community dynamics. Most work on trait plasticity has focused on single predator-prey pairs, but prey must often contend with multiple predators in natural environments. Hence, a better understanding of the evolutionary and ecological significance of phenotypic plasticity requires experiments that examine how multiple predators shape prey trait plasticity. Here, using a simple food chain consisting of a top predator (dragonfly larvae, Aeshna nigroflava), an intermediate predator (salamander larvae, Hynobius retardatus), and frog (Rana pirica) tadpoles as prey, we show that the presence of dragonfly risk cues substantially modifies the intensity of antagonistic morphological plasticity in both amphibians. In the absence of dragonflies, tadpoles produced bulgier bodies in response to salamanders, and salamanders responded to this defense by enlarging their gape size. However, in the presence of dragonfly risk cues, the expression of both antagonistic traits was significantly reduced because tadpoles and salamanders produced phenotypes that are more effective against dragonfly predators. Thus, the reduced antagonism likely emerged, in part, because the benefits of antagonistic trait expression were outweighed by the potential cost of increased vulnerability to dragonfly predation. In addition, our results suggest that when all three species were present, salamander activity levels, which influence the amount of signals required to induce antagonistic traits, were more strongly affected by dragonfly risk cues than were tadpole activity levels. This species-specific difference in activity levels was likely responsible for the reduced tadpole mortality caused by salamanders in the presence vs. absence of dragonfly risk cues. Hence, dragonflies had a positive trait-mediated indirect effect on tadpoles by modifying both the morphological and behavioral traits of salamanders.