Targeted census of lionfishes (Scorpaenidae) reveals high densities in their native range.

Indo-Pacific lionfishes generally exhibit cryptic behaviours and so can be missed when conducting non-targeted surveys. Here, the authors report the results from targeted surveys of lionfish at Moorea, French Polynesia. Lionfish from three species (Pterois antennata, Pterois radiata, Dendrochirus biocellatus) were observed at a mean density of 267 individuals ha-1 . This is substantially higher than previous estimates from the same area (Moorea) and represents the highest reported density of lionfishes from their Pacific range. Overall, this study highlights the importance of targeted survey techniques for detecting cryptic species on coral reefs.

Predation drives recurrent convergence of an interspecies mutualism.

Mutualisms are important ecological interactions that underpin much of the world's biodiversity. Predation risk has been shown to regulate mutualism dynamics in species-specific case studies; however, we lack studies which investigate whether predation can also explain broader patterns of mutualism evolution. We report that fish-anemone mutualisms have evolved on at least 55 occasions across 16 fish families over the past 60 million years and that adult body size is associated with the ontogenetic stage of anemone mutualisms: larger-bodied species partner with anemones as juveniles, while smaller-bodied species partner with anemones throughout their lives. Field and laboratory studies show that predators target smaller prey, that smaller fishes associate more with anemones, and that these relationships confer protection to small fishes. Our results indicate that predation is likely driving the recurrent convergent evolution of fish-anemone mutualisms and suggest that similar ecological processes may have selected convergence in interspecies interactions in other animal clades.

Chemically cued suppression of coral reef resilience: Where is the tipping point?

Coral reefs worldwide are shifting from high-diversity, coral-dominated communities to low-diversity systems dominated by seaweeds. This shift can impact essential recovery processes such as larval recruitment and ecosystem resilience. Recent evidence suggests that chemical cues from certain corals attract, and from certain seaweeds suppress, recruitment of juvenile fishes, with loss of coral cover and increases in seaweed cover creating negative feedbacks that prevent reef recovery and sustain seaweed dominance. Unfortunately, the level of seaweed increase and coral decline that creates this chemically cued tipping point remains unknown, depriving managers of data-based targets to prevent damaging feedbacks. We conducted flume and field assays that suggest juvenile fishes sense and respond to cues produced by low levels of seaweed cover. However, the herbivore species we tested was more tolerant of degraded reef cues than non-herbivores, possibly providing some degree of resilience if these fishes recruit, consume macroalgae, and diminish negative cues.

You are what you eat: diet-induced chemical crypsis in a coral-feeding reef fish.

The vast majority of research into the mechanisms of camouflage has focused on forms that confound visual perception. However, many organisms primarily interact with their surroundings using chemosensory systems and may have evolved mechanisms to 'blend in' with chemical components of their habitat. One potential mechanism is 'chemical crypsis' via the sequestration of dietary elements, causing a consumer's odour to chemically match that of its prey. Here, we test the potential for chemical crypsis in the coral-feeding filefish, Oxymonacanthus longirostris, by examining olfactory discrimination in obligate coral-dwelling crabs and a predatory cod. The crabs, which inhabit the corals consumed by O. longirostris, were used as a bioassay to determine the effect of coral diet on fish odour. Crabs preferred the odour of filefish fed their preferred coral over the odour of filefish fed a non-preferred coral, suggesting coral-specific dietary elements that influence odour are sequestered. Crabs also exhibited a similar preference for the odour of filefish fed their preferred coral and odour directly from that coral, suggesting a close chemical match. In behavioural trials, predatory cod were less attracted to filefish odour when presented alongside the coral it had been fed on, suggesting diet can reduce detectability. This is, we believe, the first evidence of diet-induced chemical crypsis in a vertebrate.

Prey selectivity affects reproductive success of a corallivorous reef fish.

Most animals consume a narrower range of food resources than is potentially available in the environment, but the underlying basis for these preferences is often poorly understood. Foraging theory predicts that prey selection should represent a trade-off between prey preferences based on nutritional value and prey availability. That is, species should consume preferred prey when available, but select less preferred prey when preferred prey is rare. We employed both field observation and laboratory experiments to examine the relationship between prey selection and preferences in the obligate coral-feeding filefish, Oxymonacanthus longirostris. To determine the drivers of prey selection, we experimentally established prey preferences in choice arenas and tested the consequences of prey preferences for key fitness-related parameters. Field studies showed that individuals fed almost exclusively on live corals from the genus Acropora. While diet was dominated by the most abundant species, Acropora nobilis, fish appeared to preferentially select rarer acroporids, such as A. millepora and A. hyacinthus. Prey choice experiments confirmed strong preferences for these corals, suggesting that field consumption is constrained by availability. In a longer-term feeding experiment, reproductive pairs fed on non-preferred corals exhibited dramatic reductions to body weight, and in hepatic and gonad condition, compared with those fed preferred corals. The majority of pairs fed preferred corals spawned frequently, while no spawning was observed for any pairs fed a non-preferred species of coral. These experiments suggest that fish distinguish between available corals based on their intrinsic value as prey, that reproductive success is dependent on the presence of particular coral species, and that differential loss of preferred corals could have serious consequences for the population success of these dietary specialists.

COVID-19 lockdown highlights impact of recreational activities on the behaviour of coral reef fishes.

In 2020, the COVID-19 pandemic led to a reduction in human activities and restriction of all but essential movement for much of the world's population. A large, but temporary, increase in air and water quality followed, and there have been several reports of animal populations moving into new areas. Extending on long-term monitoring efforts, we examined how coral reef fish populations were affected by the government-mandated lockdown across a series of Marine Protected Area (MPA) and non-Marine Protected Area (nMPA) sites around Moorea, French Polynesia. During the first six-week lockdown that Moorea experienced between March and May 2020, increases (approx. two-fold) in both harvested and non-harvested fishes were observed across the MPA and nMPA inner barrier reef sites, while no differences were observed across the outer barrier sites. Interviews with local amateur and professional fishers indicated that while rules regarding MPA boundaries were generally followed, some subsistence fishing continued in spite of the lockdown, including within MPAs. As most recreational activities occur along the inner reef, our data suggest that the lockdown-induced reduction in recreational activities resulted in the recolonization of these areas by fishes, highlighting how fish behaviour and space use can rapidly change in our absence.

Changes to an urban marina soundscape associated with COVID-19 lockdown in Guadeloupe.

In 2020, the COVID-19 pandemic led to government-enforced limits on activities worldwide, causing a marked reduction of human presence in outdoors environments, including in coastal areas that normally support substantial levels of boat traffic. These restrictions provided a unique opportunity to quantify the degree to which anthropogenic noise contributes to and impacts underwater soundscapes. In Guadeloupe, French West Indies, a significantly lower number of motor boats were recorded in the vicinity of the major urban marina during the peak of the first COVID-19 lockdown (April-May 2020), compared with the number recorded post-lockdown. The resumption of human activities at the end of May was correlated with a maximum increase of 6 decibels in the ambient noise level underwater. The change in noise level did not impact daily sound production patterns of vocal fishes, with increased activity at dusk seen both during and after the lockdown period. However, during the lockdown vocal activity was comprised of a reduced number of sounds, suggesting that anthropogenic noise has the potential to interfere with vocalization behaviours in fishes.

Effects of COVID-19 pandemic restrictions on coral reef fishes at eco-tourism sites in Bora-Bora, French Polynesia.

The COVID-19 pandemic led to a global lockdown in mid-2020, leading to a rapid decline in international travel and tourism. In French Polynesia, marine-based tourism activities ceased in March 2020 with the suspension of international flights (i.e., 45 days - between 20th March and 04th May 2020), slowly restarting between May-July as domestic and international visitors returned. The impacts of this rapid change in human activity at reef tourism sites on associated reef fishes was examined at Bora-Bora Island through underwater surveys of five control and nine eco-tourism sites. Our results showed that fish density significantly increased from March to May (i.e., the overall density of fishes increased by 143% and harvested species by 215%), but returned to pre-lockdown levels by August 2020. At the usually busy eco-tourism sites, fish diversity, notably of piscivores, omnivores, and benthic feeders, was higher in the absence of tourists. The impact observed is almost certainly related to short term changes in fish behavior, as any density fluctuations at the population level are unlikely to have happened over such a short time frame. Overall, these findings highlight the influence of human activities on fish communities and underline the need for further research to evaluate the environmental impacts of eco-tourism.

Non-visual camouflage.

Rohan Brooker and Bob Wong introduce the ways animals conceal themselves using non-visual sensory stimuli.

Human proximity suppresses fish recruitment by altering mangrove-associated odour cues.

Human-driven threats to coastal marine communities could potentially affect chemically mediated behaviours that have evolved to facilitate crucial ecological processes. Chemical cues and their importance remain inadequately understood in marine systems, but cues from coastal vegetation can provide sensory information guiding aquatic animals to key resources or habitats. In the tropics, mangroves are a ubiquitous component of healthy coastal ecosystems, associated with a range of habitats from river mouths to coral reefs. Because mangrove leaf litter is a predictable cue to coastal habitats, chemical information from mangrove leaves could provide a source of settlement cues for coastal fishes, drawing larvae towards shallow benthic habitats or inducing settlement. In choice assays, juvenile fishes from the Caribbean (Belize) and Indo-Pacific (Fiji) were attracted to cues from mangroves leaves and were more attracted to cues from mangroves distant from human settlement. In the field, experimental reefs supplemented with mangrove leaves grown away from humans attracted more fish recruits from a greater diversity of species than reefs supplemented with leaves grown near humans. Together, this suggests that human use of coastal areas alters natural chemical cues, negatively affecting the behavioural responses of larval fishes and potentially suppressing recruitment. Overall, our findings highlight the critical links that exist between marine and terrestrial habitats, and the importance of considering these in the broader conservation and management of coastal ecosystems.

Domestication via the commensal pathway in a fish-invertebrate mutualism.

Domesticator-domesticate relationships are specialized mutualisms where one species provides multigenerational support to another in exchange for a resource or service, and through which both partners gain an advantage over individuals outside the relationship. While this ecological innovation has profoundly reshaped the world's landscapes and biodiversity, the ecological circumstances that facilitate domestication remain uncertain. Here, we show that longfin damselfish (Stegastes diencaeus) aggressively defend algae farms on which they feed, and this protective refuge selects a domesticator-domesticate relationship with planktonic mysid shrimps (Mysidium integrum). Mysids passively excrete nutrients onto farms, which is associated with enriched algal composition, and damselfish that host mysids exhibit better body condition compared to those without. Our results suggest that the refuge damselfish create as a byproduct of algal tending and the mutual habituation that damselfish and mysids exhibit towards one another were instrumental in subsequent mysid domestication. These results are consistent with domestication via the commensal pathway, by which many common examples of animal domestication are hypothesized to have evolved.

Anthropogenic stressors impact fish sensory development and survival via thyroid disruption.

Larval metamorphosis and recruitment represent critical life-history transitions for most teleost fishes. While the detrimental effects of anthropogenic stressors on the behavior and survival of recruiting fishes are well-documented, the physiological mechanisms that underpin these patterns remain unclear. Here, we use pharmacological treatments to highlight the role that thyroid hormones (TH) play in sensory development and determining anti-predator responses in metamorphosing convict surgeonfish, Acanthurus triostegus. We then show that high doses of a physical stressor (increased temperature of +3 °C) and a chemical stressor (the pesticide chlorpyrifos at 30 µg L-1) induced similar defects by decreasing fish TH levels and affecting their sensory development. Stressor-exposed fish experienced higher predation; however, their ability to avoid predation improved when they received supplemental TH. Our results highlight that two different anthropogenic stressors can affect critical developmental and ecological transitions via the same physiological pathway. This finding provides a unifying mechanism to explain past results and underlines the profound threat anthropogenic stressors pose to fish communities.

Animal domesticators.

Humans have been domesticating plants, animals and microbes for centuries. But are we alone in doing so? Brooker and Feeney explain how domestication by animals of other species goes back even farther.

Boat noise prevents soundscape-based habitat selection by coral planulae.

Understanding the relationship between coral reef condition and recruitment potential is vital for the development of effective management strategies that maintain coral cover and biodiversity. Coral larvae (planulae) have been shown to use certain sensory cues to orient towards settlement habitats (e.g. the odour of live crustose coralline algae - CCA). However, the influence of auditory cues on coral recruitment, and any effect of anthropogenic noise on this process, remain largely unknown. Here, we determined the effect of protected reef (MPA), exploited reef (non-MPA) soundscapes, and a source of anthropogenic noise (boat) on the habitat preference for live CCA over dead CCA in the planula of two common Indo-Pacific coral species (Pocillopora damicornis and Acropora cytherea). Soundscapes from protected reefs significantly increased the phonotaxis of planulae of both species towards live CCA, especially when compared to boat noise. Boat noise playback prevented this preferential selection of live CCA as a settlement substrate. These results suggest that sources of anthropogenic noise such as motor boat can disrupt the settlement behaviours of coral planulae. Acoustic cues should be accounted for when developing management strategies aimed at maximizing larval recruitment to coral reefs.

Anemonefishes.

Feeney and Brooker introduce sea-anemone associated fish.

Exposure to agricultural pesticide impairs visual lateralization in a larval coral reef fish.

Lateralization, i.e. the preferential use of one side of the body, may convey fitness benefits for organisms within rapidly-changing environments, by optimizing separate and parallel processing of different information between the two brain hemispheres. In coral reef-fishes, the movement of larvae from planktonic to reef environments (recruitment) represents a major life-history transition. This transition requires larvae to rapidly identify and respond to sensory cues to select a suitable habitat that facilitates survival and growth. This 'recruitment' is critical for population persistence and resilience. In aquarium experiments, larval Acanthurus triostegus preferentially used their right-eye to investigate a variety of visual stimuli. Despite this, when held in in situ cages with predators, those larvae that previously favored their left-eye exhibited higher survival. These results support the "brain's right-hemisphere" theory, which predicts that the right-eye (i.e. left-hemisphere) is used to categorize stimuli while the left-eye (i.e. right-hemisphere) is used to inspect novel items and initiate rapid behavioral-responses. While these experiments confirm that being highly lateralized is ecologically advantageous, exposure to chlorpyrifos, a pesticide often inadvertently added to coral-reef waters, impaired visual-lateralization. This suggests that chemical pollutants could impair the brain function of larval fishes during a critical life-history transition, potentially impacting recruitment success.

Consistency in the supply of larval fishes among coral reefs in French Polynesia.

For marine fishes with a bipartite life cycle, pelagic larval dispersal can shape the distribution, connectivity, composition and resilience of adult populations. Numerous studies of larval dispersal, and associated settlement and recruitment processes, have examined the relationship between population connectivity and oceanographic features. However, relatively little is known about spatial and temporal variation in the abundance of larvae settling among different reefs and the extent to which the species assemblage of larvae settling at one location is reflective of the assemblage in neighbouring areas. Here, using crest nets, which provide a non-selective measure of the total abundance and assemblage of larvae settling to a reef (i.e. larval supply), we collected larval coral reef fishes at five locations surrounding two spatially disparate French Polynesian islands: Moorea and Nengo-Nengo. Overall, larval settlement patterns were correlated with the lunar cycle, with larval abundance peaking during the new moon. Although there were some spatial differences in larval supply among the five monitored sites, settlement patterns were largely consistent, even at the species level, irrespective of factors such as coastline orientation or distance between sites. This study provides further insights into the mechanisms driving patterns of dispersal and settlement of larval fishes over large spatial scales.

Cryptic effects of habitat declines: coral-associated fishes avoid coral-seaweed interactions due to visual and chemical cues.

Seaweed-dominated coral reefs are becoming increasingly common as environmental conditions shift away from those required by corals and toward those ideal for rampant seaweed growth. How coral-associated organisms respond to seaweed will not only impact their fate following environmental change but potentially also the trajectories of the coral communities on which they rely. However, behavioral responses by coral-associated organisms to seaweeds are poorly understood. This study examined interactions between a guild of obligate and opportunistic coral-feeding butterflyfishes (Chaetodontidae) and scleractinian corals to determine whether fishes continue to interact with corals in contact with seaweed or if they are avoided. Under natural conditions, all species interacted almost exclusively with seaweed-free corals. In a controlled patch reef experiment, fishes avoided corals in physical contact with seaweed, irrespective of dietary preferences. When visual seaweed cues were removed, butterflyfish continued to avoid corals that had been in contact with the allelopathic Galaxaura filamentosa, suggesting that chemical cues produced by coral-seaweed interactions are repellent. These findings suggest that, due to deleterious visual and chemical cues produced by coral-seaweed interactions, coral-associated organisms may struggle to locate resources as seaweed-free corals decline in abundance.

Whole gut microbiome composition of damselfish and cardinalfish before and after reef settlement.

The Pomacentridae (damselfish) and Apogonidae (cardinalfish) are among the most common fish families on coral reefs and in the aquarium trade. Members of both families undergo a pelagic larvae phase prior to settlement on the reef, where adults play key roles in benthic habitat structuring and trophic interactions. Fish-associated microbial communities (microbiomes) significantly influence fish health and ecology, yet little is known of how microbiomes change with life stage. We quantified the taxonomic (16S rRNA gene) composition of whole gut microbiomes from ten species of damselfish and two species of cardinalfish from Lizard Island, Australia, focusing specifically on comparisons between pelagic larvae prior to settlement on the reef versus post-settlement juvenile and adult individuals. On average, microbiome phylogenetic diversity increased from pre- to post-settlement, and was unrelated to the microbial composition in the surrounding water column. However, this trend varied among species, suggesting stochasticity in fish microbiome assembly. Pre-settlement fish were enriched with bacteria of the Endozoicomonaceae, Shewanellaceae, and Fusobacteriaceae, whereas settled fish harbored higher abundances of Vibrionaceae and Pasteurellaceae. Several individual operational taxonomic units, including ones related to Vibrio harveyi, Shewanella sp., and uncultured Endozoicomonas bacteria, were shared between both pre and post-settlement stages and may be of central importance in the intestinal niche across development. Richness of the core microbiome shared among pre-settlement fish was comparable to that of settled individuals, suggesting that changes in diversity with adulthood are due to the acquisition or loss of host-specific microbes. These results identify a key transition in microbiome structure across host life stage, suggesting changes in the functional contribution of microbiomes over development in two ecologically dominant reef fish families.

Using insights from animal behaviour and behavioural ecology to inform marine conservation initiatives.

The impacts of human activities on the natural world are becoming increasingly apparent, with rapid development and exploitation occurring at the expense of habitat quality and biodiversity. Declines are especially concerning in the oceans, which hold intrinsic value due to their biological uniqueness as well as their substantial sociological and economic importance. Here, we review the literature and investigate whether incorporation of knowledge from the fields of animal behaviour and behavioural ecology may improve the effectiveness of conservation initiatives in marine systems. In particular, we consider (1) how knowledge of larval behaviour and ecology may be used to inform the design of marine protected areas, (2) how protecting species that hold specific ecological niches may be of particular importance for maximizing the preservation of biodiversity, (3) how current harvesting techniques may be inadvertently skewing the behavioural phenotypes of stock populations and whether changes to current practices may lessen this skew and reinforce population persistence, and (4) how understanding the behavioural and physiological responses of species to a changing environment may provide essential insights into areas of particular vulnerability for prioritized conservation attention. The complex nature of conservation programmes inherently results in interdisciplinary responses, and the incorporation of knowledge from the fields of animal behaviour and behavioural ecology may increase our ability to stem the loss of biodiversity in marine environments.