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.

Ingestion and Depuration of Microplastics by a Planktivorous Coral Reef Fish, Pomacentrus amboinensis

Microplastics are ubiquitous contaminants in marine environments and organisms. Concerns about potential impacts on marine organisms are usually associated with uptake of microplastics, especially via ingestion. This study used environmentally relevant exposure conditions to investigate microplastic ingestion and depuration kinetics of the planktivorous damselfish, Pomacentrus amboinensis. Irregular shaped blue polypropylene (PP) particles (longest length 125–250 μm), and regular shaped blue polyester (PET) fibers (length 600–700 μm) were selected based on physical and chemical characteristics of microplastics commonly reported in the marine environment, including in coral reef ecosystems. Individual adult damselfish were exposed to a single dose of PP particles and PET fibers at concentrations reported for waters of the Great Barrier Reef (i.e., environmentally relevant concentrations, ERC), or future projected higher concentrations (10x ERC, 100x ERC). Measured microplastic concentrations were similar to their nominal values, confirming that PP particles and PET fibers were present at the desired concentrations and available for ingestion by individual damselfish. Throughout the 128-h depuration period, the 88 experimental fish were sampled 2, 4, 8, 16, 32, 64, and 128-h post microplastic exposure and their gastrointestinal tracts (GIT) analyzed for ingested microplastics. While damselfish ingested both experimental microplastics at all concentrations, body burden, and depuration rates of PET fibers were significantly larger and longer, respectively, compared to PP particles. For both microplastic types, exposure to higher concentrations led to an increase in body burden and lower depuration rates. These findings confirm ingestion of PP particles and PET fibers by P. amboinensis and demonstrate for the first time the influence of microplastic characteristics and concentrations on body burden and depuration rates. Finally, despite measures put in place to prevent contamination, extraneous microplastics were recovered from experimental fish, highlighting the challenge to completely eliminate contamination in microplastic exposure studies. These results are critical to inform and continuously improve protocols for future microplastics research, and to elucidate patterns of microplastic contamination and associated risks in marine organisms.

The impact of long-term reduced access to cleaner fish on health indicators of resident client fish

ABSTRACTIn many mutualisms, benefits in the form of food are exchanged for services such as transport or protection. In the marine cleaning mutualism, a variety of ‘client’ reef fishes offer ‘cleaner’ fish Labroides dimidiatus access to food in the form of their ectoparasites, where parasite removal supposedly protects the clients. Yet, the health benefits individual clients obtain in the long term from repeated ectoparasite removal remain relatively unknown. Here, we tested whether long-term reduced access to cleaning services alters indicators of health status such as body condition, immunity and the steroids cortisol and testosterone in four client damselfish species Pomacentrus amboinensis, Amblyglyphidodon curacao, Acanthochromis polyacanthus and Dischistodus perspicillatus. To do so, we took advantage of a long-term experimental project in which several small reefs around Lizard Island (Great Barrier Reef, Australia) have been maintained cleaner-free since the year 2000, while control reefs had their cleaner presence continuously monitored. We found that the four damselfish species from reef sites without cleaners for 13 years had lower body condition than fish from reefs with cleaners. However, immunity measurements and cortisol and testosterone levels did not differ between experimental groups. Our findings suggest that clients use the energetic benefits derived from long-term access to cleaning services to selectively increase body condition, rather than altering hormonal or immune system functions.

Planetary Health: Are We Part of the Problem or Part of the Solution?

Planetary health, formally defined as the interdependent vitality of all natural and anthropogenic ecosystems—social, political, and otherwise—is a vast concept that has now entered the scientific lexicon. The problems associated with planetary ill-health—biodiversity losses, climate change, environmental degradation, and other problems of so-called “anthropocene syndrome”—are considered so enormous that they can immobilize us; we may feel environmental guilt, but that alone cannot save us or the planet. What is missing is environmental empathy, the nurturance of our capacity to recognize the planet and its many life forms as more than elusive entities to be objectified. Although experts in planetary health have called for a more sophisticated understanding of the psychological connections between humans and the natural world, these appeals are almost exclusively cordoned off from the taboos of science; applying concepts of “self” to non-human animals, and especially non-mammals, are generally proscribed. Here, I will personalize the planetary health concept by describing my research-based endeavors on the Great Barrier Reef—experiences that would change my scientific career and personal life forever. The small damselfish, Pomacentrus amboinensis, became the teacher; the student-in-me departed the reef with an education in environmental empathy, and a greater understanding of the urgency with which we must alter our teaching in ecology and other branches of science. Planetary health as a unifying, multidisciplinary effort generally lacks a narrative perspective in academia; I am hopeful that others will share their narrative perspectives and, in doing so, foster the growth of environmental empathy.

Cleaner wrasse indirectly affect the cognitive performance of a damselfish through ectoparasite removal

Cleaning organisms play a fundamental ecological role by removing ectoparasites and infected tissue from client surfaces. We used the well-studied cleaning mutualisms involving the cleaner wrasse, Labroides dimidiatus, to test how client cognition is affected by ectoparasites and whether these effects are mitigated by cleaners. Ambon damselfish ( Pomacentrus amboinensis) collected from experimental reef patches without cleaner wrasse performed worse in a visual discrimination test than conspecifics from patches with cleaners. Endoparasite abundance also negatively influenced success in this test. Visual discrimination performance was also impaired in damselfish experimentally infected with gnathiid (Crustacea: Isopoda) ectoparasites. Neither cleaner absence nor gnathiid infection affected performance in spatial recognition or reversal learning tests. Injection with immune-stimulating lipopolysaccharide did not affect visual discrimination performance relative to saline-injected controls, suggesting that cognitive impairments are not due to an innate immune response. Our results highlight the complex, indirect role of cleaning organisms in promoting the health of their clients via ectoparasite removal and emphasize the negative impact of parasites on host's cognitive abilities.

Extended exposure to elevated temperature affects escape response behaviour in coral reef fishes

The threat of predation, and the prey’s response, are important drivers of community dynamics. Yet environmental temperature can have a significant effect on predation avoidance techniques such as fast-start performance observed in marine fishes. While it is known that temperature increases can influence performance and behaviour in the short-term, little is known about how species respond to extended exposure during development. We produced a startle response in two species of damselfish, the lemon damselPomacentrus moluccensis,and the Ambon damselfishPomacentrus amboinensis,by the repeated use of a drop stimulus. We show that the length of thermal exposure of juveniles to elevated temperature significantly affects this escape responses.Short-term (4d) exposure to warmer temperature affected directionality and responsiveness for both species. After long-term (90d) exposure, onlyP. moluccensisshowed beneficial plasticity, with directionality returning to control levels. Responsiveness also decreased in both species, possibly to compensate for higher temperatures. There was no effect of temperature or length of exposure on latency to react, maximum swimming speed, or escape distance suggesting that the physical ability to escape was maintained. Evidence suggests that elevated temperature may impact some fish species through its effect on the behavioural responses while under threat rather than having a direct influence on their physical ability to perform an effective escape response.

Protogyny in a tropical damselfish: females queue for future benefit

Membership of the group is a balance between the benefits associated with group living and the cost of socially constrained growth and breeding opportunities, but the costs and benefits are seldom examined. The goal of the present study was to explore the trade-offs associated with group living for a sex-changing, potentially protogynous coral reef fish, the Ambon damselfish,Pomacentrus amboinensis. Extensive sampling showed that the species exhibits resource defence polygyny, where dominant males guard a nest site that is visited by females.P. amboinensishave a longevity of about 6.5 years on the northern Great Barrier Reef. While the species can change sex consistent with being a protogynous hermaphrodite, it is unclear the extent to which the species uses this capability. Social groups are comprised of one reproductive male, 1–7 females and a number of juveniles. Females live in a linear dominance hierarchy, with the male being more aggressive to the beta-female than the alpha-female, who exhibits lower levels of ovarian cortisol. Surveys and a tagging study indicated that groups were stable for at least three months. A passive integrated transponder tag study showed that males spawn with females from their own group, but also females from neighbouring groups.In situbehavioural observations found that alpha-females have priority of access to the nest site that the male guarded, and access to higher quality foraging areas. Male removal studies suggest that the alpha-females can change sex to take over from the male when the position becomes available. Examination of otolith microstructure showed that those individuals which change sex to males have different embryonic characteristics at hatching, suggesting that success may involve a component that is parentally endowed. The relative importance of parental effects and social organisation in affecting the importance of female queuing is yet to be studied, but will likely depend on the strength of social control by the dominant members of the group.

Disrupted learning: habitat degradation impairs crucial antipredator responses in naive prey

Habitat degradation is a global problem and one of the main causes of biodiversity loss. Though widespread, the mechanisms that underlie faunal changes are poorly understood. In tropical marine systems, corals play a crucial role in forming habitat, but coral cover on many reefs is declining sharply. Coral degradation affects the olfactory cues that provide reliable information on the presence and intensity of threat. Here, we show for the first time that the ability of a habitat generalist to learn predators using an efficient and widespread method of predator learning is compromised in degraded coral habitats. Results indicate that chemical alarm cues are no longer indicative of a local threat for the habitat generalist (the damselfish, Pomacentrus amboinensis ), and these cues can no longer be used to learn the identity of novel predators in degraded habitats. By contrast, a rubble specialist and congeneric ( Pomacentrus coelestis ) responded to olfactory threat cues regardless of background environment and could learn the identity of a novel predator using chemical alarm cues. Understanding how some species can cope with or acclimate to the detrimental impacts of habitat degradation on risk assessment abilities will be crucial to defining the scope of resilience in threatened communities.