Context-dependent interactive effects of non-lethal predation on larvae impact adult longevity and body composition

Abstract

Predation impacts development, behavior and morphology of prey species thereby shaping their abundances, distribution and community structure. Non-lethal threat of predation, specifically, can have a strong influence on prey lifehistory characteristics. While investigations often focus on the impact of predation threat on prey in isolation, tests of its interactive effects with food availability and resource competition on prey survival and fitness can improve understanding of costs, benefits and trade-offs of anti-predator strategies. This study, involving Aedes aegypti mosquitoes as a model organism, investigates both simple and interactive effects of predation threat during the larval stage on survival, size at and time to maturity, stored teneral reserves of glycogen, protein and lipid in adults, and adult longevity. Our results show that development times of mosquito larvae were increased (by 14.84% in males and by 97.63% in females), and size of eclosing adults decreased (by 62.30% in males and by 58.33% in females) when exposed to lowered nutrition and elevated intraspecific competition, but that predation had no detectable effect on these simple traits. Teneral reserves of glycogen, protein and lipid and adult longevity were positively correlated with adult body size. Non-lethal predation threat had significant interactive effects with nutrition and larval competition on teneral reserves in males and adult longevity in males and females. The sexes responded differently to conditions encountered as larvae, with the larval environment affecting development and adult characteristics more acutely for females than for males. The outcome of this study shows how threat of predation on juveniles can have long-lasting effects on adults that are likely to impact mosquito population dynamics and that may impact disease transmission.

Simulated climate change, but not predation risk, accelerates Aedes aegypti emergence in a microcosm experiment in western Amazonia

“…aegypti females exposed to predator risk during the larval stage [23]. Similarly, Chandrasegaran et al [35] found https://doi.org/10.1371/journal.pone.0241070.g004…”

The demographic and life‐history costs of fear: Trait‐mediated effects of threat of predation onAedes triseriatus

“…Although female larvae may not change behavior as strongly as do males in response to predator cues (Wormington & Juliano, ), females still may face significant life‐history costs from any reduction in foraging due to their higher demand for resources to produce greater adult body size. Other studies on trait‐mediated effects of predation or predation cues on mosquitoes have found retarded larval growth and development, reduced adult size, shortened adult longevity, and reduced teneral reserves of lipid, protein, and carbohydrate ( Culex pipiens : Beketov & Liess, ; Aedes notoscriptus : van Uitregt et al, ; Aedes aegypti : Bellamy & Alto, ; Chandrasegaran et al, ), and females are usually more strongly affected than males due to greater reproductive costs (Chandrasegaran et al, ; Wormington & Juliano, ). These nonlethal effects of predators are more likely to be important and detectable when food availability to larvae is limited.…”

“…We found no effects of predator cues on males, but significant life-history costs of predator cue exposure for females (decrease in survivorship, significantly faster emergence times when given higher resource levels, significantly reduced adult longevity when given lower resource levels). Male A. triseriatus exhibit a more extreme shift in behavior in response to predator cues than do females-particularly when they are well-fed-increasing their resting behavior at the surface which reduces their predation risk (Wormington & Juliano, 2014 Chandrasegaran et al, 2018), and females are usually more strongly affected than males due to greater reproductive costs (Chandrasegaran et al, 2018;Wormington & Juliano, 2014). These nonlethal effects of predators are more likely to be important and detectable when food availability to larvae is limited.…”

“…Because the indirect effects of threat of predation are likely mediated through modifications of the energy budget, we expect that the effects of threat of predation should be more severe when resources for larvae are scarce and should impact females, which are more sensitive to reduced resource acquisition (Chandrasegaran et al, ). To understand the consequences of threat of predation at the population level, comprehensive investigation of context‐dependent impacts on life‐table variables (survivorship, age at reproduction, adult feeding success, and fecundity) is necessary (Chandrasegaran et al, ). Because A. triseriatus exhibits greater behavioral responses to predation threat than other container Aedes (Costanzo et al, ; Grill & Juliano, ; Kesavaraju & Juliano, ), A. triseriatus is the ideal focal species for investigating potential life‐history responses in fecundity, longevity, biting rates, and population dynamics.…”

“…Larval mosquitoes are a good system for experimental studies of the trade-offs associated with antipredator defenses. Although intensity of predation is strongest for mosquito larvae that develop in permanent bodies of water (Juliano, 2007;Washburn, 1995), larval mosquitoes that develop in ephemeral water-filled natural and manmade containers also are frequently exposed to predators that specialize on those habitats, and may show strong traitbased responses to those predators (e.g., Bellamy & Alto, 2018;Chandrasegaran, Kandregula, Quader, & Juliano, 2018;Costanzo, Muturi, & Alto, 2011;Kesavaraju & Juliano, 2004;van Uitregt, Hurst, & Wilson, 2012). Small containers and short generation times make it possible to run replicated experiments of generationlength duration.…”