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.

Effects of COVID-19 lockdown on the observed density of coral reef fish along coastal habitats of Moorea, French Polynesia.

During the first COVID-19 lockdown in 2020, levels of coastal activities such as subsistence fishing and marine tourism declined rapidly throughout French Polynesia. Here, we examined whether the reduction in coastal use led to changes in fish density around the island of Moorea. Two natural coastal marine habitats (bare sand and mangrove) and one type of man-made coastal structure (embankment) were monitored on the west coast of the island before and after the first COVID-19 lockdown. At the end of the lockdown (May 2020), significantly higher apparent densities of juvenile and adult fish, including many harvested species, were recorded compared to levels documented in 2019 at the same period (April 2019). Fish densities subsequently declined as coastal activities recovered; however, 2 months after the end of the lockdown (July 2020), densities were still higher than they were in July 2019 with significant family-specific variation across habitats. This study highlights that short-term reductions in human activity can have a positive impact on coastal fish communities and may encourage future management policy that minimizes human impacts on coastline habitats. Supplementary Information: The online version contains supplementary material available at 10.1007/s10113-022-02011-0.

The overlooked complexity of avian brood parasite-host relationships.

The relationships between avian brood parasites and their hosts are widely recognised as model systems for studying coevolution. However, while most brood parasites are known to parasitise multiple species of host and hosts are often subject to parasitism by multiple brood parasite species, the examination of multispecies interactions remains rare. Here, we compile data on all known brood parasite-host relationships and find that complex brood parasite-host systems, where multiple species of brood parasites and hosts coexist and interact, are globally commonplace. By examining patterns of past research, we outline the disparity between patterns of network complexity and past research emphases and discuss factors that may be associated with these patterns. Drawing on insights gained from other systems that have embraced a multispecies framework, we highlight the potential benefits of considering brood parasite-host interactions as ecological networks and brood parasitism as a model system for studying multispecies interactions. Overall, our results provide new insights into the diversity of these relationships, highlight the stark mismatch between past research efforts and global patterns of network complexity, and draw attention to the opportunities that more complex arrangements offer for examining how species interactions shape global patterns of biodiversity.

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.

Social learning of a brood parasite by its host.

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.

Why cuckoos remove host eggs: Biting eggs facilitates faster parasitic egg-laying.

Brood parasitism by cuckoos relies on manipulating hosts to raise their offspring and has evolved stunning adaptations to aid in their deception. The fact that cuckoos usually but not always, remove one or two host eggs while laying their eggs has been a longstanding focus of intensive research. However, the benefit of this behavior remains elusive. Moreover, the recently proposed help delivery hypothesis, predicting that egg removal by cuckoos may decrease the egg-laying duration in the parasitism process caused by biting action, lacks experimental verification. Therefore, in this study, we examined the effects of egg removal/biting on the egg-laying speed in the common cuckoo (Cuculus canorus) to experimentally test this hypothesis. We compared the duration of cuckoo egg-laying in empty nests, nests with host eggs, and nests with artificial blue stick models to test whether cuckoos biting an egg/stick can significantly hasten the egg-laying speed than no biting action. Our results showed that biting an egg or an object is associated with cuckoos laying approximately 37% faster than when they do not bite an egg or an object. This study provides the first experimental evidence for the help delivery hypothesis and demonstrates that when cuckoos bite eggs or other objects in the nest, they lay eggs more quickly and thereby avoid suffering the hosts' injurious attack.

Chase-away evolution maintains imperfect mimicry in a brood parasite-host system despite rapid evolution of mimics.

We studied a brood parasite-host system (the cuckoo finch Anomalospiza imberbis and its host, the tawny-flanked prinia Prinia subflava) to test (1) the fundamental hypothesis that deceptive mimics evolve to resemble models, selecting in turn for models to evolve away from mimics ('chase-away evolution') and (2) whether such reciprocal evolution maintains imperfect mimicry over time. Over only 50 years, parasites evolved towards hosts and hosts evolved away from parasites, resulting in no detectible increase in mimetic fidelity. Our results reflect rapid adaptive evolution in wild populations of models and mimics and show that chase-away evolution in models can counteract even rapid evolution of mimics, resulting in the persistence of imperfect mimicry.

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.

Patterns of genetic divergence and demographic history shed light on island-mainland population dynamics and melanic plumage evolution in the white-winged Fairywren.

The existence of distinct traits in island versus mainland populations offers opportunities to gain insights into how eco-evolutionary processes operate under natural conditions. We used two island colonization events in the white-winged fairywren (Malurus leucopterus) to investigate the genomic and demographic origin of melanic plumage. This avian species is distributed across most of Australia, and males of the mainland subspecies (M. l. leuconotus) exhibit a blue nuptial plumage in contrast to males of two island subspecies - M. l. leucopterus on Dirk Hartog Island and M. l. edouardi on Barrow Island - that exhibit a black nuptial plumage. We used reduced-representation sequencing to explore differentiation and demographic history in this species and found clear patterns of divergence between mainland and island populations, with additional substructuring on the mainland. Divergence between the mainland and Dirk Hartog was approximately 10 times more recent than the split between the mainland and Barrow Island, supporting two independent colonizations. In both cases, estimated gene flow between the mainland and the islands was low, contributing to signals of divergence among subspecies. Our results present demographic reconstructions of mainland-island dynamics and associated plumage variation in white-winged fairywrens, with broader implications regarding our understanding of convergent evolution in insular populations.

Long term relationship between farming damselfish, predators, competitors and benthic habitat on coral reefs of Moorea Island.

Understanding the processes that shape biodiversity is essential for effective environmental management. Across the world's coral reefs, algal farming damselfish (Stegastes sp.) modify the surrounding benthic community through their creation of algae "farms". Using a long-term monitoring dataset (2005-2019) from Moorea Island, French Polynesia, we investigated whether the density of dusky damselfish (Stegastes nigricans) is associated with benthic habitat composition, the density of predators and/or competitors, and whether the survey area was inside or outside of a Marine Protected Area (MPA). We found no evidence that benthic cover or number of competitors were associated with dusky damselfish densities, both inside and outside MPAs. In contrast, fluctuations in dusky damselfish densities were negatively associated with the density of predators (e.g. Serranidae, Muraenidae and Scorpaenidae) in the preceding year in non-MPA areas, and both within and outside of MPAs when predator densities were high (2005-2010). These results suggest that healthy predator populations may be important for regulating the abundances of keystone species, such as algal farming damselfish, especially when predator densities are high.

Sparrows use a medicinal herb to defend against parasites and increase offspring condition.

The incorporation of aromatic plants into nests by birds is suspected to constitute an example of preventative medicine use, whereby the phytochemical compounds within plants reduce infestation by parasites and increase offspring condition [1,2]. In China, russet sparrows (Passer cinnamomeus) incorporate wormwood (Artemisia verlotorum) leaves into their nests around the same time that local people hang wormwood from their doors as a traditional custom during the Dragon Boat Festival. The belief that this behaviour confers protection against ill health [3] is supported by the description of anti-parasite compounds in wormwood [4]. It has been suggested that the incorporation of fresh wormwood leaves into nests may serve a similar function for sparrows. Here we show that sparrows choose nest location and resupply established nests with fresh wormwood leaves using olfactory cues, that nests containing wormwood leaves have lower ectoparasite loads, and that nests with more wormwood leaves produce heavier chicks. Our results indicate that sparrows use wormwood as a preventative medicine to control ectoparasites and improve the body mass of their offspring.

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.

Practical methods for culturing parasitic gnathiid isopods.

The reliance of parasites on their hosts makes host-parasite interactions ideal models for exploring ecological and evolutionary processes. By providing a consistent supply of parasites, in vivo monocultures offer the opportunity to conduct experiments on a scale that is generally not otherwise possible. Gnathiid isopods are common ectoparasites of marine fishes, and are becoming an increasing focus of research attention due to their experimental amenability and ecological importance as ubiquitous, harmful, blood-feeding "mosquito-like" organisms. They feed on hosts once during each of their three juvenile stages, and after each feeding event they return to the benthos to digest and moult to the next stage. Adults do not feed and remain in the benthos, where they reproduce and give birth. Here, we provide methods of culturing gnathiids, and highlight ways in which gnathiids can be used to examine parasite-host-environment interactions. Captive-raised gnathiid juveniles are increasingly being used in parasitological research; however, the methodology for establishing gnathiid monocultures is still not widely known. Information to obtain in vivo monocultures on teleost fish is detailed for a Great Barrier Reef (Australia) and a Caribbean Sea (US Virgin Islands) gnathiid species, and gnathiid information gained over two decades of successfully maintaining continuous cultures is summarised. Providing a suitable benthic habitat for the predominantly benthic free-living stage of this parasite is paramount. Maintenance comprises provision of adequate benthic shelter, managing parasite populations, and sustaining host health. For the first time, we also measured gnathiids' apparent attack speed (maximum 24.5 cm sec-1; 6.9, 4.9/17.0, median, 25th/75th quantiles) and illustrate how to collect such fast moving ectoparasites in captivity for experiments. In addition to providing details pertaining to culture maintenance, we review research using gnathiid cultures that have enabled detailed scientific understanding of host and parasite biology, behaviour and ecology on coral reefs.

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.

Monogamy without parental care? Social and genetic mating systems of avian brood parasites.

Classic evolutionary theory predicts that monogamy should be intimately linked with parental care. It has long been assumed, therefore, that avian brood parasites-which lay their eggs in the nests of 'host' species and provide little, if any, parental care-should be overwhelmingly promiscuous. However, recent studies have revealed that the social mating systems of brood parasites are surprisingly diverse, encompassing lek polygyny, monogamy, polygamy and promiscuity. What ecological or phylogenetic factors explain this variation, and why are some brood parasites apparently monogamous? Here we review the social and genetic mating systems of all 75 brood parasitic species for which data are available and evaluate several hypotheses that may help explain these patterns. We find that social monogamy is widespread, often co-occurring with territoriality and cooperative behaviour by the mated pair. Comparative studies, though preliminary, suggest that in some species, monogamy is associated with low host density and polygamy with higher host density. Interestingly, molecular data show that genetic and social mating systems can be entirely decoupled: genetic monogamy can occur in parasitic species that lack behavioural pair-bonds, possibly as a by-product of territoriality; conversely, social monogamy has been reported in parasites that are genetically polygamous. This synthesis suggests that social and genetic monogamy may result from very different selective pressures, and that male-female cooperative behaviours, population density and territoriality may all interact to favour the evolution of monogamous mating in brood parasites. Given that detailed descriptive data of social, and especially genetic, mating systems are still lacking for the majority of brood parasitic species, definitive tests of these hypotheses await future work. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

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.

Anemonefishes.

Feeney and Brooker introduce sea-anemone associated fish.

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.

Phenotypic plasticity confers multiple fitness benefits to a mimic.

Animal communication is often deceptive; however, such dishonesty can become ineffective if it is used too often, is used out of context, or is too easy to detect [1-3]. Mimicry is a common form of deception, and most mimics gain the greatest fitness benefits when they are rare compared to their models [3, 4]. If mimics are encountered too frequently or if their model is absent, avoidance learning of noxious models is disrupted (Batesian mimicry [3]), or receivers become more vigilant and learn to avoid perilous mimics (aggressive mimicry [4]). Mimics can moderate this selective constraint by imperfectly resembling multiple models [5], through polymorphisms [6], or by opportunistically deploying mimetic signals [1, 7]. Here we uncover a novel mechanism to escape the constraints of deceptive signaling: phenotypic plasticity allows mimics to deceive targets using multiple guises. Using a combination of behavioral, cell histological, and molecular methods, we show that a coral reef fish, the dusky dottyback (Pseudochromis fuscus), flexibly adapts its body coloration to mimic differently colored reef fishes and in doing so gains multiple fitness benefits. We find that by matching the color of other reef fish, dottybacks increase their success of predation upon juvenile fish prey and are therefore able to deceive their victims by resembling multiple models. Furthermore, we demonstrate that changing color also increases habitat-associated crypsis that decreases the risk of being detected by predators. Hence, when mimics and models share common selective pressures, flexible imitation of models might inherently confer secondary benefits to mimics. Our results show that phenotypic plasticity can act as a mechanism to ease constraints that are typically associated with deception. VIDEO ABSTRACT.

Nest destruction elicits indiscriminate con- versus heterospecific brood parasitism in a captive bird.

Following nest destruction, the laying of physiologically committed eggs (eggs that are ovulated, yolked, and making their way through the oviduct) in the nests of other birds is considered a viable pathway for the evolution of obligate interspecific brood parasitism. While intraspecific brood parasitism in response to nest predation has been experimentally demonstrated, this pathway has yet to be evaluated in an interspecific context. We studied patterns of egg laying following experimental nest destruction in captive zebra finches, Taeniopygia guttata, a frequent intraspecific brood parasite. We found that zebra finches laid physiologically committed eggs indiscriminately between nests containing conspecific eggs and nests containing heterospecific eggs (of Bengalese finches, Lonchura striata vars. domestica), despite the con- and heterospecific eggs differing in both size and coloration. This is the first experimental evidence that nest destruction may provide a pathway for the evolution of interspecific brood parasitism in birds.