Predator-induced maternal effects determine adaptive antipredator behaviors via egg composition

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or “C-start reflexes,” are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes.

Predators affect a plant virus through direct and trait-mediated indirect effects on vectors

Arthropods that vector plant pathogens often interact with predators within food webs. Predators affect vectors by eating them (consumptive effects) and by inducing antipredator behaviors (non-consumptive effects), and these interactions may affect transmission of vector-borne pathogens. However, it has proven difficult to experimentally tease apart the effects of predators on vector fitness and behavior as they are often correlated. We addressed this problem by assessing how both aphids and an aphid-borne pathogen were affected by variable predation risk. Specifically, we experimentally manipulated ladybeetle predators’ mouthparts to isolate consumptive, and non-consumptive, effects of predators on aphid fitness, movement, and virus transmission. We show that although lethal predators decreased aphid vector abundance, they increased pathogen transmission by increasing aphid movement among hosts. Moreover, aphids responded to risk of predation by moving to younger plant tissue that was more susceptible to the pathogen. Aphids also responded to predator risk through compensatory reproduction, which offset direct consumptive effects. Our results support predictions of disease models showing alterations of vector movement due to predators can have greater effects on transmission of pathogens than vector consumption. Broadly, our study shows isolating direct and indirect predation effects can reveal novel pathways by which predators affect vector-borne pathogens.

Experimental predator intrusions in a cooperative breeder reveal threat-dependent task partitioning

In cooperatively breeding species, nonbreeding individuals provide alloparental care and help in territory maintenance and defense. Antipredator behaviors of subordinates can enhance offspring survival, which may provide direct and indirect fitness benefits to all group members. Helping abilities and involved costs and benefits, risks, and outside options (e.g., breeding independently) usually diverge between group members, which calls for status-specific differentiated behavioral responses. Such role differentiation within groups may generate task-specific division of labor, as exemplified by eusocial animals. In vertebrates, little is known about such task differentiation among group members. We show how breeders and helpers of the cooperatively breeding cichlid Neolamprologus savoryi partition predator defense depending on intruder type and the presence of dependent young. In the field, we experimentally simulated intrusions by different fish species posing a risk either specifically to eggs, young, or adults. We used intrusions by harmless algae eaters as a control. Breeders defended most when dependent young were present, while helper investment hinged mainly on their body size and on the potential threat posed by the respective intruders. Breeders and helpers partitioned defense tasks primarily when dependent young were exposed to immediate risk, with breeders investing most in antipredator defense, while helpers increased guarding and care in the breeding chamber. Breeders’ defense likely benefits helpers as well, as it was especially enhanced in the treatment where helpers were also at risk. These findings illustrate that in a highly social fish different group members exhibit fine-tuned behavioral responses in dependence of ecological and reproductive parameter variation.

Maternal predation risk increases offspring’s exploration but does not affect schooling behavior

The environment that parents experience can influence their reproductive output and their offspring’s fitness via parental effects. Perceived predation risk can affect both parent and offspring phenotype, but it remains unclear to what extent offspring behavioral traits are affected when the mother is exposed to predation risk. This is particularly unclear in live-bearing species where maternal effects could occur during embryogenesis. Here, using a half-sib design to control for paternal effects, we experimentally exposed females of a live-bearing fish, the guppy (Poecilia reticulata), to visual predator cues and conspecific alarm cues during their gestation. Females exposed to predation risk cues increased their antipredator behaviors throughout the entire treatment. Offspring of mothers exposed to the predation stimuli exhibited more pronounced exploratory behavior, but did not show any significant differences in their schooling behavior, compared to controls. Thus, while maternally perceived risk affected offspring’s exploration during early stages of life, offspring’s schooling behavior could be influenced more by direct environmental experience rather than via maternal cues. Our results suggest a rather limited role in predator-induced maternal effects on the behavior of juvenile guppies.

Training fails to elicit behavioral change in a marsupial suffering evolutionary loss of antipredator behaviors

Attempts to reintroduce threatened species from ex situ populations (zoos or predator-free sanctuaries) regularly fail because of predation. When removed from their natural predators, animals may lose their ability to recognize predators and thus fail to adopt appropriate antipredator behaviors. Recently, northern quolls (Dasyurus hallucatus; Dasyuromorpha: Dasyuridae) conserved on a predator-free “island ark” for 13 generations were found to have no recognition of dingoes, a natural predator with which they had coevolved on mainland Australia for about 8,000 years. A subsequent reintroduction attempt using quolls acquired from this island ark failed due to predation by dingoes. In this study, we tested whether instrumental conditioning could be used to improve predator recognition in captive quolls sourced from a predator-free “island ark.” We used a previously successful scent-recognition assay (a giving-up density experiment) to compare predator-scent recognition of captive-born island animals before and after antipredator training. Our training was delivered by pairing live predators (dingo and domestic dog) with an electrified cage floor in repeat trials such that, when the predators were present, foraging animals would receive a shock. Our training methodology did not result in any discernible change in the ability of quolls to recognize and avoid dingo scent after training. We conclude either that our particular training method was ineffective (though ethically permissible); or that because these quolls appear unable to recognize natural predators, predator recognition may be extremely difficult to impart in a captive setting given ethical constraints. Our results point to the difficulty of reinstating lost behaviors, and to the value of maintaining antipredator behaviors in conservation populations before they are lost.

The specificity of sperm-mediated paternal effects in threespined sticklebacks

Parental effects can help offspring cope with challenging environments, but whether these effects are unique to specific environmental conditions is largely unknown. Parental effects may evolve via a core pathway that generally prepares offspring for risky environments or could be stimuli-specific, with offspring developing phenotypes that are tailored to specific environmental challenges. We exposed threespined sticklebacks (Gasterosteus aculeatus) fathers to a potentially threatening stimulus (net) versus native predator (sculpin). Offspring of sculpin-exposed fathers were more responsive (greater change in activity) to a simulated predator attack, while offspring of net-exposed fathers were less responsive (lower plasma cortisol and fewer antipredator behaviors). To evaluate offspring response to native and non-native stimuli, we sequentially exposed offspring of net-exposed, sculpin-exposed or control fathers to a net, native sculpin model, or non-native trout model. Paternal treatment did not influence offspring response to stimuli; instead, offspring were more responsive to the native sculpin predator compared to nets or non-native trout predator. Collectively, we demonstrate that sperm-mediated paternal effects in response to different, potentially stressful stimuli result in distinct offspring phenotypes. This specificity may be key to understanding the evolution of adaptive parental effects and how parents prime offspring for encountering both evolved and novel environmental stimuli.

Stress responses to conspecific visual cues of predation risk in zebrafish

Chemical communication relating to predation risk is a trait common among fish species. Prey fish under threat of predation can signal risk to conspecific fish, which then exhibit defensive responses. Fish also assess predation risk by visual cues and change their behavior accordingly. Here, we explored whether these behavioral changes act as visual alarm signals to conspecific fish that are not initially under risk. We show that shoals of zebrafish (Danio rerio) visually exposed to a predator display antipredator behaviors. In addition, these defensive maneuvers trigger antipredator reactions in conspecifics and, concomitantly, stimulate the hypothalamus-pituitary-interrenal axis, leading to cortisol increase. Thus, we conclude that zebrafish defensive behaviors act as visual alarm cues that induce antipredator and stress response in conspecific fish.

Does riparian disturbance alter stream amphibian antipredator behaviors?

Ecological traps occur when a species makes maladaptive habitat-selection decisions. Human-modified environments including deforested riparian habitats can change how organisms respond to environmental cues. Stream amphibians alter their habitat selection in response to abiotic cues associated with riparian clearing, but little research exists to determine if behavioral shifts to abiotic cues may make them more susceptible to predation. To evaluate if deforested habitats create ecological traps, we studied habitat-selection behavior of larval Black-bellied Salamander (Desmognathus quadramaculatus (Holbrook, 1840)) when given conflicting environmental cues. We also evaluated the potential for learning or adaptation to cues in deforested reaches by evaluating individuals from forested and deforested reaches. We anticipated that individuals from deforested reaches would make adaptive antipredator choices when presented with well-lit habitat, whereas individuals from forested reaches would select shaded habitat closer to a predator. We found that habitat origin, light, and predator presence all interacted to influence habitat selection. Although individuals from forested habitats selected shaded environments, all observed individuals adaptively avoided a predator. Individuals from deforested reaches were more willing to enter well-lit habitat to avoid the predator. Despite documented declines of salamanders associated with forest removal, it appears that individuals are capable of making adaptive antipredator decisions in degraded habitats.