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.

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.

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.

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.

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.

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.

Non-visual camouflage.

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

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.

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.

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.

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.

Anemonefishes.

Feeney and Brooker introduce sea-anemone associated fish.

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.

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.

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.

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.

Temporal and Spatial Comparisons of Underwater Sound Signatures of Different Reef Habitats in Moorea Island, French Polynesia.

As environmental sounds are used by larval fish and crustaceans to locate and orientate towards habitat during settlement, variations in the acoustic signature produced by habitats could provide valuable information about habitat quality, helping larvae to differentiate between potential settlement sites. However, very little is known about how acoustic signatures differ between proximate habitats. This study described within- and between-site differences in the sound spectra of five contiguous habitats at Moorea Island, French Polynesia: the inner reef crest, the barrier reef, the fringing reef, a pass and a coastal mangrove forest. Habitats with coral (inner, barrier and fringing reefs) were characterized by a similar sound spectrum with average intensities ranging from 70 to 78 dB re 1 µPa.Hz(-1). The mangrove forest had a lower sound intensity of 70 dB re 1 µPa.Hz(-1) while the pass was characterized by a higher sound level with an average intensity of 91 dB re 1 µPa.Hz(-1). Habitats showed significantly different intensities for most frequencies, and a decreasing intensity gradient was observed from the reef to the shore. While habitats close to the shore showed no significant diel variation in sound intensities, sound levels increased at the pass during the night and barrier reef during the day. These two habitats also appeared to be louder in the North than in the West. These findings suggest that daily variations in sound intensity and across-reef sound gradients could be a valuable source of information for settling larvae. They also provide further evidence that closely related habitats, separated by less than 1 km, can differ significantly in their spectral composition and that these signatures might be typical and conserved along the coast of Moorea.

Chemical spying in coral reef fish larvae at recruitment.

When fish larvae recruit back to a reef, chemical cues are often used to find suitable habitat or to find juvenile or adult conspecifics. We tested if the chemical information used by larvae was intentionally produced by juvenile and adult conspecifics already on the reef (communication process) or whether the cues used result from normal biochemical processes with no active involvement by conspecifics ("spying" behavior by larvae). Conspecific chemical cues attracted the majority of larvae (four out of the seven species tested); although while some species were equally attracted to cues from adults and juveniles (Chromis viridis, Apogon novemfasciatus), two exhibited greater sensitivity to adult cues (Pomacentrus pavo, Dascyllus aruanus). Our results indicate also that spying cues are those most commonly used by settling fishes (C. viridis, P. pavo, A. novemfasciatus). Only one species (D. aruanus) preferred the odour of conspecifics that had had visual contact with larvae (communication).