Disturbance cue communication is shaped by emitter diet and receiver background risk in Trinidadian guppies

In animal communication systems, individuals that detect a cue (i.e., ‘receivers’) are often influenced by characteristics of the cue emitter. For instance, in many species, receivers avoid chemical cues that are released by emitters experiencing disturbance. These chemical ‘disturbance cues’ appear to benefit receivers by warning them about nearby danger, such as a predator’s approach. While the active ingredients in disturbance cues have been largely unexplored, by-products of metabolized protein are thought to play a role for some species. If so, the content (quality) and volume (quantity) of the emitter’s diet should affect their disturbance cues, thus altering how receivers perceive the cues and respond. Guppies Poecilia reticulata are a species known to discriminate among disturbance cues from different types of donors, but dietary variation has yet to be explored. In this study, we found evidence that diet quality and quantity can affect disturbance cues released by guppy emitters (i.e., experimental ‘donors’). Receivers discriminated between donor cue treatments, responding more strongly to cues from donors fed a protein-rich bloodworm diet (experiment 1), as well as an overall larger diet (experiment 2). We also found that receivers exposed to higher background risk were more sensitive to disturbance cue variation, with the strongest avoidance responses displayed by high-risk receivers toward disturbance cues from donors fed the high-quality diet. Therefore, diet, and perhaps protein specifically, affects either the concentration or composition of disturbance cues released by guppies. Such variation may be important in information signalling in social species like the guppy.

Multimodal mechanosensing enables treefrog embryos to escape egg-predators

ABSTRACTMechanosensory-cued hatching (MCH) is widespread, diverse and important for survival in many animals. From flatworms and insects to frogs and turtles, embryos use mechanosensory cues and signals to inform hatching timing, yet mechanisms mediating mechanosensing in ovo are largely unknown. The arboreal embryos of red-eyed treefrogs, Agalychnis callidryas, hatch prematurely to escape predation, cued by physical disturbance in snake attacks. When otoconial organs in the developing vestibular system become functional, this response strengthens, but its earlier occurrence indicates another sensor must contribute. Post-hatching, tadpoles use lateral line neuromasts to detect water motion. We ablated neuromast function with gentamicin to assess their role in A. callidryas’ hatching response to disturbance. Prior to vestibular function, this nearly eliminated the hatching response to a complex simulated attack cue, egg jiggling, revealing that neuromasts mediate early MCH. Vestibular function onset increased hatching, independent of neuromast function, indicating young embryos use multiple mechanosensory systems. MCH increased developmentally. All older embryos hatched in response to egg jiggling, but neuromast function reduced response latency. In contrast, neuromast ablation had no effect on the timing or level of hatching in motion-only vibration playbacks. It appears only a subset of egg-disturbance cues stimulate neuromasts; thus, embryos in attacked clutches may receive unimodal or multimodal stimuli. Agalychnis callidryas embryos have more neuromasts than described for any other species at hatching, suggesting precocious sensory development may facilitate MCH. Our findings provide insight into the behavioral roles of two mechanosensory systems in ovo and open possibilities for exploring sensory perception across taxa in early life stages.

Multimodal mechanosensing enables treefrog embryos to escape egg-predators

ABSTRACTMechanosensory-cued hatching (MCH) is widespread, diverse, and improves survival in many animals. From flatworms and insects to frogs and turtles, embryos use mechanosensory cues and signals to inform hatching timing, yet mechanisms mediating mechanosensing in ovo are largely unknown. The arboreal embryos of red-eyed treefrogs, Agalychnis callidryas, hatch prematurely to escape predation, cued by physical disturbance in snake attacks. When otoconial organs in the developing vestibular system become functional, this response strengthens, but its earlier occurrence indicates another sensor must contribute. Post-hatching, tadpoles use lateral line neuromasts to detect water motion. We ablated neuromast function with gentamicin to assess their role in A. callidryas’ hatching response to disturbance. Prior to vestibular function, this nearly eliminated the hatching response to a complex simulated attack cue, egg-jiggling, revealing that neuromasts mediate early MCH. Vestibular function onset increased hatching, independent of neuromast function, indicating young embryos use multiple mechanosensory systems. MCH increased developmentally. All older embryos hatched in response to egg-jiggling, but neuromast function reduced response latency. In contrast, neuromast ablation had no effect on timing or level of hatching in motion-only vibration playbacks. It appears only a subset of egg-disturbance cues stimulate neuromasts; thus embryos in attacked clutches may receive uni- or multimodal stimuli. A. callidryas embryos have more neuromasts than described for any other species at hatching, suggesting precocious sensory development may facilitate MCH. Our findings provide insight into the behavioral roles of two mechanosensory systems in ovo and open possibilities for exploring sensory perception across taxa in early life stages.SUMMARYRed-eyed treefrog embryos use both their lateral line and vestibular systems to sense the disturbance cues in egg-predator attacks that inform escape-hatching decisions.

Sender and receiver experience alters the response of fish to disturbance cues

Predation is a pervasive selection pressure, shaping morphological, physiological, and behavioral phenotypes of prey species. Recent studies have begun to examine how the effects of individual experience with predation risk shapes the use of publicly available risk assessment cues. Here, we investigated the effects of prior predation risk experience on disturbance cue production and use by Trinidadian guppies Poecilia reticulata under laboratory conditions. In our first experiment, we demonstrate that the response of guppies from a high predation population (Lopinot River) was dependent upon the source of disturbance cue senders (high vs. low predation populations). However, guppies collected from a low predation site (Upper Aripo River) exhibited similar responses to disturbance cues, regardless of the sender population. In our second experiment, we used laboratory strain guppies exposed to high versus low background risk conditions. Our results show an analogous response patterns as shown for our first experiment. Guppies exposed to high background risk conditions exhibited stronger responses to the disturbance cues collected from senders exposed to high (vs. low) risk conditions and guppies exposed to low risk conditions were not influenced by sender experience. Combined, our results suggest that experience with background predation risk significantly impacts both the production of and response to disturbance cues in guppies.

Does donor group size matter? The response of guppies (Poecilia reticulata) and convict cichlids (Amatitlania nigrofasciata) to disturbance cues from conspecific and heterospecific donors

Prey are under immense pressure to make context-specific, behavioural decisions. Prey use public information to reduce the costs associated with making inappropriate decisions. Chemical cues are commonly used by aquatic vertebrates to assess local threats and facilitate behavioural decision making. Previous studies on chemosensory assessment of risk have largely focused on damage-released alarm cues, with the cues released by disturbed or stressed prey (i.e., disturbance cues) receiving less attention. Disturbance cues are “early-warning signals” common among aquatic vertebrates that may warn conspecific and heterospecific prey guild members of potential risk. Initially, we conducted a series of laboratory studies to determine (i) if guppies (Poecilia reticulata Peters, 1859) produce and respond to disturbance cues and (ii) if relative concentration (donor group size) determines response intensity. Secondly, we examined if guppies and convict cichlids (Amatitlania nigrofasciata (Günther, 1867)) show similar response patterns to their own vs. heterospecific disturbance cues. Our results suggest that guppies exhibit increased predator avoidance behaviour to conspecific disturbance cues (relative to water from undisturbed conspecifics) and increased donor group size lead to stronger antipredator responses. However, although guppies and cichlids respond to each other’s disturbance cues, we found no effect of donor group size towards heterospecific disturbance cues. Our results suggest that disturbance cues are not generalized cues and present a degree of species-specificity.