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    Body size affects the evolution of eyespots in caterpillars
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    Abstract:
    Significance Eyespots are a widespread form of antipredator defense that have long captured the imagination of evolutionary biologists, geneticists, psychologists, and artists. These markings are particularly common within Lepidoptera, and eyespots on caterpillars have been shown to deter avian predators; however, why eyespots have evolved in particular caterpillar species, and why they are not even more widespread, remain unclear. Here we answer this question using a powerful three-pronged approach. Our phylogenetically controlled analysis of hawkmoths demonstrates that eyespots are typically restricted to large caterpillars, and our field and laboratory experiments provide an explanation for this. Eyespots are costly to small caterpillars because they enhance detectability without providing a protective advantage, but they are beneficial to large caterpillars because they deter predators.
    Keywords:
    Eyespot
    Prey evolve anti-predator strategies against multiple enemies in nature. We examined how a prey species adopts different predation avoidance tactics against pursuit or sit-and-wait predators. As prey, we used two strains of Tribolium beetles artificially selected for short or long duration of death feigning. The results showed that, as prey, the short strains displayed the same behavior, escaping, against the two types of predators. On the other hand, death feigning is known to be effective for evading a jumping spider in the case of the long strains, while the present study showed that the long strain beetles used freezing behavior against a sit-and-wait type predator A. venator in this study. The short strain beetles were more easily orientated by predators and suffered a higher rate of predation than the long strains. The time to predation was also shorter in the short strains compared to the long strains. When the predator was starved, even the long strains were preyed upon when the predator was orientated toward the prey, suggesting the starvation period, i.e., prey density, is an important factor for antipredator behavior. Traditionally, death feigning has been thought to be the last resort in a series of anti-predator avoidance behaviors. However, our results showed that freezing and death feigning were not parts of a series of behavior, but independent behaviors against different predators, at least for these beetles. The results also suggest that the differences in feeding rates between the strains could be explained by differences in activity among the strains.
    We consider the optimal behavior of a cryptic prey individual as it is approached by a predator searching for prey. Although the predator has not yet discovered the prey, it has an increasing likelihood of doing so as it gets closer to the prey. Further, the closer the predator is to the prey when it discovers it, the more likely the predator will be to capture the prey. These arguments suggest that the prey should flee before the predator discovers it. However, the act of fleeing will alert the predator to the presence of the prey and trigger an attack that might not have occurred otherwise. We capture these conflicting outcomes in a mathematical model, which we then use to predict the optimal behavior of the prey and predator. We argue that the optimal strategy for the prey is either to run as soon as they detect a predator approaching or to only flee in response to having been detected by the predator. Running as soon as the predator is detected is associated with low predator search speeds, a low nonpredation cost to running, a large advantage to the prey in initiating chases rather than reacting, limited ability to spot the predator at distance, a high ability to spot prey by the predator, and a high probability that chases will be successful. The optimal strategy for the predator depends on whether its current trajectory is taking it closer to or further from the prey. In the latter case, the predator should attack immediately on discovering the prey; in the former case, it should delay its attack until it reaches the point on its current trajectory where distance to the prey is minimized.
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    In aquatic systems, prey animals associate predation risk with cues that originate either from the predator or from injured conspecifics. Sources and benefits of these cues have received considerable attention in river, lake, and pond ecosystems but are less well understood in small container ecosystems that can hold less than a liter of water. Mosquitoes Aedes triseriatus (Say) and Aedes albopictus (Skuse) encounter predatory Corethrella appendiculata (Grabham) and Toxorhynchites rutilus (Coquillett) in small containers and show antipredatory behavioral responses. We investigated the sources of the predation cues to which these prey larvae respond. We tested whether Ae. albopictus larvae show behavioral responses to cues emanating from the predator or from damage to prey caused by the act of predation. We also tested whether Ae. triseriatus respond to cues present in fluid or solid residues from predator activity. Ae. albopictus showed behavioral modifications only in response to waterborne cues from a feeding predator and not to cues from a starving predator, indicating that Ae. albopictus respond to cues created by the act of predation, which could include substances derived from damaged prey or substances in predator feces. Ae. triseriatus showed behavioral responses to solid residues from predation but not to fluid without those solids, indicating that the cues to which they respond originate in predator feces or uneaten prey body parts. Our results suggest that cues in this system may be primarily chemicals that are detected upon contact with solid residues that are products of the feeding processes of these predators.
    Aedes albopictus
    Kairomone
    Aposematism
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    Organisms are adept at altering behaviors to balance the tradeoff between foraging and predation risk in spatially and temporally shifting predator environments. In order to optimize this tradeoff, prey need to be able to display an appropriate response based on degree of predation risk. To be most beneficial in the earliest life stages in which many prey are vulnerable to predation, innate anti-predator responses should scale to match the risk imposed by predators until learned anti-predator responses can occur. We conducted an experiment that examined whether tadpoles with no previous exposure to predators (i.e., predator-naive) exhibit innate antipredator behavioral responses (e.g., via refuge use and spatial avoidance) that match the actual risk posed by each predator. Using 7 treatments (6 free-roaming, lethal predators plus no-predator control), we determined the predation rates of each predator on Lithobates sphenocephalus tadpoles. We recorded behavioral observations on an additional 7 nonlethal treatments (6 caged predators plus no-predator control). Tadpoles exhibited innate responses to fish predators, but not non-fish predators, even though two non-fish predators (newt and crayfish) consumed the most tadpoles. Due to a mismatch between innate response and predator consumption, tadpoles may be vulnerable to greater rates of predation at the earliest life stages before learning can occur. Thus, naïve tadpoles in nature may be at a high risk to predation in the presence of a novel predator until learned anti-predator responses provide additional defenses to the surviving tadpoles.
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    Studies of phenotypic plasticity frequently ask how organisms respond to a change in their environment, but most organisms do not experience single environmental changes. Therefore, we need to move to the next step and understand how organisms respond to combinations of environmental changes. Recent studies of predator-induced plasticity have addressed how prey respond to different combinations of predators. I briefly review 22 studies of combined predator effects on prey phenotypes and identify four factors that make it difficult to interpret the results of these studies: (1) uncontrolled prey consumption, (2) a low number of prey traits, (3) a low number of predator combinations, and (4) confounded predator composition and total predator density. I address these challenges in an experiment that examined how wood frog tadpoles (Rana sylvatica) altered 12 behavioral, morphological, and life historical traits in response to four different caged predators (Erythemis, Belostoma, Dytiscus, and Anax). The predators were present alone at low density, alone at high density (2×), or combined into six pairwise combinations. When each predator was alone (at either low or high density), tadpoles discriminated among different predators and produced predator-specific phenotypes. The doubling of predator density rarely induced more extreme prey phenotypes. When predators were combined, the tadpoles generally developed phenotypes that were similar to those induced by the more risky predator alone (90% of all traits examined, at either low or high density). These results suggest that tadpoles perceive the risk of combined predators as being similar to the risk of the most dangerous predator in the pair, and not as a summed or averaged predation risk. The actual risk from these predator combinations remains to be tested. This appears to be the first study to take a comprehensive approach that controls prey consumption, examines a large number of prey traits, uses a large number of predator combinations, and separates the effects of predator composition and predator density. There is a clear need for more such studies to determine whether these results can be generalized to other taxa.