Behavioural responses to con- and heterospecific alarm cues by an alien and a coexisting native fish

The monkey goby Neogobius fluviatilis is an invasive Ponto-Caspian fish that enters habitats of the native gudgeon Gobio gobio in European freshwaters, likely belonging to the same prey guild. Their abilities to detect and avoid predation have been poorly understood, although these traits may contribute to the competitive advantage and drive the invasion success of the goby. We tested intra- and interspecific responses of fish from sympatric populations to damage-released alarm cues (skin extract) in laboratory. Both species of fish responded to conspecific and heterospecific cues, but their responses to conspecifics were more diverse (changed social distancing among individuals, reduced vertical and horizontal movement) than those elicited by heterospecifics (changed social distancing only). Moreover, the fish differed in their anti-predation behaviour: the gudgeon increased whilst the monkey goby decreased inter-individual distances and only the gudgeon exhibited thigmotaxis and reduced mobility in response to the conspecific cues. Interspecific differences show that the species exhibit distant anti-predation strategies. This might be associated with their phylogenetic distance and/or higher differentiation of their ecological niches than commonly assumed. Besides, our results suggest that alien species be included in the interspecific exchange of information in local fish assemblages.

Signals from predators, injured conspecifics, and pesticide modify the swimming behavior of the gregarious tadpole Rhinella dorbignyi (Anura: Bufonidae)

Tadpoles detect chemical signals released from predators and conspecifics, and those present in the environment, and adjust their behavioral responses. This study evaluated the swimming activity of Rhinella dorbignyi (Duméril and Bibron, 1941) tadpoles exposed to chemical signals, including cues from a predator fish Synbranchus marmoratus Bloch, 1975 and an injured conspecific; sublethal concentration of insecticide cypermethrin; and their combination. Swimming behavior (total distance moved, average speed, global activity, number of contacts between tadpoles) was evaluated in an individual (1) and groups of different size (3, 5, 7 and 10 tadpoles) using a video-tracking software tool. Predator exposure modified behavioral parameters, reducing encounters with predators and, therefore, mortality. Total distance moved and average speed increased in trials involving 1 tadpole and 3 interacting tadpoles exposed to injured conspecifics, whereas global activity increased in all group sizes, showing that gregarious tadpoles may be affected by alarm cues and their behavior may be disrupted. The insecticide treatments (alone and combined) increased parameters in all group sizes, causing hyperactivity due to its neurotoxic effect. The different responses observed after exposure to alarm cues and environmental signals in the different group sizes modified the normal behavior and the ecological dynamics of gregarious tadpoles.

Living in mixed species groups promotes predator learning in degraded habitats

Living in mix-species aggregations provides animals with substantive anti-predator, foraging and locomotory advantages while simultaneously exposing them to costs, including increased competition and pathogen exposure. Given each species possess unique morphology, competitive ability, parasite vulnerability and predator defences, we can surmise that each species in mixed groups will experience a unique set of trade-offs. In addition to this unique balance, each species must also contend with anthropogenic changes, a relatively new, and rapidly increasing phenomenon, that adds further complexity to any system. This complex balance of biotic and abiotic factors is on full display in the exceptionally diverse, yet anthropogenically degraded, Great Barrier Reef of Australia. One such example within this intricate ecosystem is the inability of some damselfish to utilize their own chemical alarm cues within degraded habitats, leaving them exposed to increased predation risk. These cues, which are released when the skin is damaged, warn nearby individuals of increased predation risk and act as a crucial associative learning tool. Normally, a single exposure of alarm cues paired with an unknown predator odour facilitates learning of that new odour as dangerous. Here, we show that Ambon damselfish, Pomacentrus amboinensis, a species with impaired alarm responses in degraded habitats, failed to learn a novel predator odour as risky when associated with chemical alarm cues. However, in the same degraded habitats, the same species learned to recognize a novel predator as risky when the predator odour was paired with alarm cues of the closely related, and co-occurring, whitetail damselfish, Pomacentrus chrysurus. The importance of this learning opportunity was underscored in a survival experiment which demonstrated that fish in degraded habitats trained with heterospecific alarm cues, had higher survival than those we tried to train with conspecific alarm cues. From these data, we conclude that redundancy in learning mechanisms among prey guild members may lead to increased stability in rapidly changing environments.

Running away or running to? Do prey make decisions solely based on the landscape of fear or do they also include stimuli from a landscape of safety?

Predator prey interactions are a key part of ecosystem function, and non-consumptive effects fall under the landscape of fear theory. Under the landscape of fear, the antipredator responses of prey are based on the spatial and temporal distribution of predatory cues in the environment. However, the aversive stimuli (fear) are not the only stimuli prey can utilize when making behavioral decisions. Prey might also be using attractive stimuli that represent safety to guide decision making. Using a novel, orthogonal design, we were able to spatially separate aversive and attractive stimuli to determine if prey are utilizing safety cues to navigate their environment. Crayfish Faxonius rusticus were placed in the center of a behavioral arena. Aversive stimuli of either predatory bass Micropterus salmoides cues or conspecific alarm cues increased along the x-axis of the behavioral arena. Safety cues (shelters) increased along the y-axis by decreasing the number of shelter openings in this direction. Crayfish were allowed two phases to explore the arena: one without the fearful stimuli and one with the stimuli. Linear mixed models were conducted to determine if movement behaviors and habitat utilization were affected by the phase of the trial and the type of aversive stimuli. Crayfish responded more strongly to alarm cues than fear cues, with only alarm cues significantly impacting habitat utilization. When responding to alarm cues, crayfish used safety cues as well as fear cues to relocate themselves within the arena. Based on these results, we argue that crayfish are utilizing a landscape of safety in conjunction with a landscape of fear when navigating their environment.

Embryonic exposure to predation risk and hatch time variation in fathead minnows

Organisms are exposed to a wealth of chemical information during their development. Some of these chemical cues indicate present or future dangers, such as the presence of predators that feed on either the developing embryos or their nearby parents. Organisms may use this information to modify their morphology or life-history, including hatching timing, or may retain information about risk until it gains relevance. Previous research has shown predation-induced alterations in hatching among embryonic minnows that were exposed to mechanical-injury-released alarm cues from conspecific embryos. Here, we test whether minnows likewise hatch early in response to alarm cues from injured adult conspecifics. We know that embryonic minnows can detect adult alarm cues and use them to facilitate learned recognition of predators; however, it is unknown whether these adult alarm cues will also induce a change in hatching time. Early hatching may allow animals to rapidly disperse away from potential predators, but late hatching may allow animals to grow and develop structures that allow them to effectively escape when they do hatch. Here, we found here that unlike embryonic fathead minnows (Pimephales promelas) exposed to embryonic cues, embryonic minnows exposed to adult alarm cues do not exhibit early hatching. The ability of embryos to recognize adult alarm cues as a future threat, but not a current one, demonstrates sophisticated ontogenetic specificity in the hatching response of embryonic minnows.

Foraging behavior of the sea urchin Mesocentrotus nudus exposed to conspecific alarm cues in various conditions

Conspecific alarm cues crushed from Mesocentrotus nudus prevent sea urchins from foraging the kelp, but do not repel them far away from the kelp. However, it remains largely unknown of whether this phenomenon was affected by conspecific alarm cues or by the attraction of the kelp. The present study found no significant difference in the duration in the danger area with or without the kelp around conspecific alarm cues. This suggests that the phenomenon is the strategy of sea urchins but not by the attraction of kelp. We found that conspecific alarm cues appearing between the kelp and sea urchins significantly affected foraging behavior of sea urchins fasted for 21 days. This indicates that conspecific alarm cues can effectively prevent fasted sea urchins from foraging the kelp. Further, there was no correlation between foraging velocity and the duration in the danger area. Pearson correlation analysis revealed no significant correlation between foraging velocity and the duration in the safety area close to different amounts of conspecific alarm cues, suggesting that conspecific alarm cues prevent sea urchins with strong foraging ability to forage. Collectively, the present results indicate that conspecific alarm cues as highly available biological barriers are cost-effective approaches to preventing overgrazing of sea urchins in the protection of kelp beds ecosystems. Notably, the present study is a short-term laboratory investigation that does not consider the complexity of natural conditions. Future studies are essential to test the present findings in the field.

Intergenerational effects of manipulating DNA methylation in the early life of an iconic invader

In response to novel environments, invasive populations often evolve rapidly. Standing genetic variation is an important predictor of evolutionary response but epigenetic variation may also play a role. Here, we use an iconic invader, the cane toad (Rhinella marina), to investigate how manipulating epigenetic status affects phenotypic traits. We collected wild toads from across Australia, bred them, and experimentally manipulated DNA methylation of the subsequent two generations (G1, G2) through exposure to the DNA methylation inhibitor zebularine and/or conspecific tadpole alarm cues. Direct exposure to alarm cues (an indicator of predation risk) increased the potency of G2 tadpole chemical cues, but this was accompanied by reductions in survival. Exposure to alarm cues during G1 also increased the potency of G2 tadpole cues, indicating intergenerational plasticity in this inducible defence. In addition, the negative effects of alarm cues on tadpole viability (i.e. the costs of producing the inducible defence) were minimized in the second generation. Exposure to zebularine during G1 induced similar intergenerational effects, suggesting a role for alteration in DNA methylation. Accordingly, we identified intergenerational shifts in DNA methylation at some loci in response to alarm cue exposure. Substantial demethylation occurred within thesodium channel epithelial 1 subunit gammagene (SCNN1G) in alarm cue exposed individuals and their offspring. This gene is a key to the regulation of sodium in epithelial cells and may help to maintain the protective epidermal barrier. These data suggest that early life experiences of tadpoles induce intergenerational effects through epigenetic mechanisms, which enhance larval fitness.This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

Effect of Potential Sea Lamprey (Petromyzon marinus) Repellents on the Distribution of Juvenile Rainbow Trout (Oncorhynchus mykiss) in a Laboratory Environment

Recent studies have begun to consider the use of chemosensory alarm cues as potential repellents of invasive Sea Lamprey (Petromyzon marinus Linnaeus, 1758) in the Great Lakes Basin. An important factor in determining the efficacy of potential P. marinus repellents is whether they are species-specific. To that end, using laboratory stream channels, this study investigated whether a non-target species, the Rainbow Trout (Oncorhynchus mykiss Walbaum, 1792), would change their distribution in response to damage-released P. marinus alarm cues, potential mammalian predator cues, and damage-released conspecific cues. In groups of 10 individuals per replicate, with 10 replicates per stimulus type, subjects were exposed to one of the following treatment types: deionized water (control), P. marinus extract (heterospecific alarm cue), O. mykiss extract (conspecific alarm cue), 2-phenylethylamine hydrochloride (potential predator cue), and human saliva (potential predator cue). None of the stimuli induced a significant avoidance response during the stimulus observation period as compared to the control. These findings provide preliminary support for the species-specific nature of these proposed alternative P. marinus control measures.