Plastic Hatching Timing by Red-Eyed Treefrog Embryos Interacts with Larval Predator Identity and Sublethal Predation to Affect Prey Morphology but Not Performance

Abstract

Many animals respond to predation risk by altering their morphology, behavior, or life-history. We know a great deal about the cues prey respond to and the changes to prey that can be induced by predation risk, but less is known about how plastic responses to predators may be affected by separate plastic responses occurring earlier in life, particularly during the embryonic period. Embryos of a broad array of taxa can respond to egg- or larval-stage risks by altering hatching timing, which may alter the way organisms respond to future predators. Using the red-eyed treefrog (Agalychnis callidryas), a model for understanding the effects of plasticity across life-stages, we assessed how the combined effects of induced variation in the timing of embryo hatching and variation in the larval predator community impacted tadpole morphology, pigmentation and swimming performance. We found that A. callidryas tadpoles developed deeper tail muscles and fins and darker pigmentation in response to fish predators, either when alone or in diverse community with other predators. Tadpoles altered morphology much less so to dragonfly naiads or water bugs. Interestingly, morphological responses to predators were also affected by induced differences in hatching age, with early and late-hatched tadpoles exhibiting different allometric relationships between tail height and body length in different predator environments. Beyond induced morphological changes, fish predators often damaged tadpoles’ tails without killing them (i.e., sublethal predation), but these tadpoles swam equally quickly to those with fully intact tails. This was due to the fact that tadpoles with more damaged tails increased tail beats to achieve equal swimming speed. This study demonstrates that plastic phenotypic responses to predation risk can be influenced by a complex combination of responses to both the embryo and larval environments, but also that prey performance can be highly resilient to sublethal predation.

Genetic correlations and little genetic variance for reaction norms may limit potential for adaptation to pollution by ionic and nanoparticulate silver in a whitefish (Salmonidae)

“…Hatching, which is the first important niche switch for many species, is a plastic trait, and the timing of this event can be accelerated or delayed to cope with stage‐specific risks such as pathogens and predators in the environment in a wide range of taxa (e.g., Christy ; Doody ; Warkentin ; Pompini et al. ; Touchon and Wojdak ). Whitefish specifically have previously been shown to induce hatching to escape pathogens in their immediate environment (Wedekind ) or to avoid desiccation (Wedekind and Müller ).…”

Vulnerability and behavioral responses of South Chinese anuran tadpoles to native dragonfly (Pantala flavescens) naiads and introduced western mosquitofish (Gambusia affinis)

“…Naiads of the dragonfly Pantala flavescens (Fabricius) have been recognized as voracious native predators of anuran larvae and are widely abundant in lentic water bodies (Caldwell et al 1980;Touchon and Wojdak 2014). The two predators have qualitatively different foraging styles.…”

“…The two predators have qualitatively different foraging styles. P. flavescens naiads are typical ambush predator invertebrates, resting at the bottom of the body of water or perching on the grass nearby, and directly ambushing the head and abdomen of prey with their piercing-sucking mouthpart after slowly approaching prey through the water column (Touchon and Wojdak 2014). Mosquitofish are usually actively swimming and foraging predators (Komak and Crossland 2000;Touchon and Wojdak 2014).…”

“…P. flavescens naiads are typical ambush predator invertebrates, resting at the bottom of the body of water or perching on the grass nearby, and directly ambushing the head and abdomen of prey with their piercing-sucking mouthpart after slowly approaching prey through the water column (Touchon and Wojdak 2014). Mosquitofish are usually actively swimming and foraging predators (Komak and Crossland 2000;Touchon and Wojdak 2014). Because of limited gape, mosquitofish often maim individual tadpoles by biting the tail fin; therefore, this species is considered a sublethal predator, but it can kill prey through multiple injuries (Walls et al 2002;Shulse and Semlitsch 2014;Touchon and Wojdak 2014).…”

“…Mosquitofish are usually actively swimming and foraging predators (Komak and Crossland 2000;Touchon and Wojdak 2014). Because of limited gape, mosquitofish often maim individual tadpoles by biting the tail fin; therefore, this species is considered a sublethal predator, but it can kill prey through multiple injuries (Walls et al 2002;Shulse and Semlitsch 2014;Touchon and Wojdak 2014).…”