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.

Predation Cues Lead to Reduced Foraging of Invasive Siganus rivulatus in the Mediterranean

Invasive species are one of many anthropogenic challenges to maintaining a healthy marine ecosystem. Two rabbitfish species (Siganus rivulatus and Siganus luridus) are among the more successful migrants from the Red Sea to the Mediterranean, where their intense foraging has caused damage to the algae community, thus reducing primary production and habitat complexity, and impacting nurseries for early life stages. Anecdotal evidence suggests that the impact of rabbitfish on algae is lower in Marine Protected Areas (MPAs) although rabbitfish densities are similar in protected and fished areas. One explanation could be that fear of predators, more often present inside MPAs and an important component of a healthy marine ecosystem, reduces the ecological impacts of rabbitfish. This research aimed to test if such fear effects do occur in rabbitfish. Using controlled mesocosm experiments, we tested S. rivulatus reactions to two chemical predation cues: chemical alarm cues released from a recently killed conspecific fish, and water-borne cues from a tank with a live grouper predator, Epinephelus marginatus. We found that rabbitfish significantly reduce their overall food consumption as well as their bites per minute when exposed to the alarm cue, but not when exposed to the grouper water cue. These results support the idea that MPAs, which effectively increase the density of large piscivores and hence predation, can mitigate the impact of invasive herbivorous species. If the mesocosm results can scale up to natural systems, predation cues may be artificially introduced to other target areas in order to reduce rabbitfish grazing outside reserves. Thus, this study provides information that can be used to manage the ecological impacts caused by invasive rabbitfish, both inside and outside of marine reserves.

Epidermal Club Cells in Fishes: A Case for Ecoimmunological Analysis

Epidermal club cells (ECCs), along with mucus cells, are present in the skin of many fishes, particularly in the well-studied Ostariophysan family Cyprinidae. Most ECC-associated literature has focused on the potential role of ECCs as a component of chemical alarm cues released passively when a predator damages the skin of its prey, alerting nearby prey to the presence of an active predator. Because this warning system is maintained by receiver-side selection (senders are eaten), there is want of a mechanism to confer fitness benefits to the individual that invests in ECCs to explain their evolutionary origin and maintenance in this speciose group of fishes. In an attempt to understand the fitness benefits that accrue from investment in ECCs, we reviewed the phylogenetic distribution of ECCs and their histochemical properties. ECCs are found in various forms in all teleost superorders and in the chondrostei inferring either early or multiple independent origins over evolutionary time. We noted that ECCs respond to several environmental stressors/immunomodulators including parasites and pathogens, are suppressed by immunomodulators such as testosterone and cortisol, and their density covaries with food ration, demonstrating a dynamic metabolic cost to maintaining these cells. ECC density varies widely among and within fish populations, suggesting that ECCs may be a convenient tool with which to assay ecoimmunological tradeoffs between immune stress and foraging activity, reproductive state, and predator–prey interactions. Here, we review the case for ECC immune function, immune functions in fishes generally, and encourage future work describing the precise role of ECCs in the immune system and life history evolution in fishes.

Proteomic responses to ocean acidification in the brain of juvenile coral reef fish

Elevated CO2 levels predicted to occur by the end of the century can affect the physiology and behaviour of marine fishes. For one important survival mechanism, the response to chemical alarm cues from conspecifics, substantial among-individual variation in the extent of behavioural impairment when exposed to elevated CO2 has been observed in previous studies. Whole brain transcriptomic data has further emphasized the importance of parental phenotypic variation in the response of juvenile fish to elevated CO2. In this study, we investigate the genome-wide proteomic responses of this variation in the brain of 5-week old spiny damselfish, Acanthochromis polyacanthus. We compared the expression of proteins in the brains of juvenile A. polyacanthus from two different parental behavioural phenotypes (sensitive and tolerant) that had been experimentally exposed to short-term, long-term and inter-generational elevated CO2. Our results show differential expression of key proteins related to stress response and epigenetic markers with elevated CO2 exposure. Proteins related to neurological development were also differentially expressed particularly in the long-term developmental treatment, which might be critical for juvenile development. By contrast, exposure to elevated CO2 in the parental generation resulted in only three differentially expressed proteins in the offspring, revealing potential for inter-generational acclimation. Lastly, we found a distinct proteomic pattern in juveniles due to the behavioural sensitivity of parents to elevated CO2, even though the behaviour of the juvenile fish was impaired regardless of parental phenotype. Our data shows that developing juveniles are affected in their brain protein expression by elevated CO2, but the effect varies with the length of exposure as well as due to variation of parental phenotypes in the population.

Microhabitat complexity influences fear acquisition in fathead minnows

Habitat varies in structure, with animals often preferring a certain degree of microhabitat complexity that facilitates fitness-related activities such as predator avoidance. Environments with high predation risk can induce elevated baseline fear and neophobia in prey, but whether microhabitat complexity influences the acquisition of neophobia has yet to be reported. Here, we tested whether exposure to predation risk induces different levels of fear in microhabitats that differed in complexity. We exposed fathead minnows, Pimephales promelas, to predation risk repeatedly (12 times over 4 days) in the form of damage-released chemical alarm cues (compared to water control) in tanks with vertical plant structure distributed either throughout the tank (complex habitat) or clumped together (simple habitat). Then, we tested minnows before and after exposure to a novel odor in tanks with either the same microhabitat complexity (i.e., familiar habitats) or in tanks with novel habitat that had different substrate structure and no vertical structure. Minnows in the complex habitat showed less overall movement one day after the background risk period, whereas individuals in the simple habitat showed reduced movement regardless of prior risk exposure. We observed stronger effects in the novel habitat, where background risk in both simple and complex habitats caused neophobia. However, individuals from the simple background habitat showed higher baseline fear behaviors. Hence, for minnows, low microhabitat complexity appears to lead to elevated fear, which remains even after a habitat change.