Cleaner wrasse influence habitat selection of young damselfish

The presence of bluestreak cleaner wrasse, Labroides dimidiatus, on coral reefs increases total abundance and biodiversity of reef fishes. The mechanism(s) that cause such shifts in population structure are unclear, but it is possible that young fish preferentially settle into microhabitats where cleaner wrasse are present. As a first step to investigate this possibility, we conducted aquarium experiments to examine whether settlement-stage and young juveniles of ambon damselfish, Pomacentrus amboinensis, selected a microhabitat near a cleaner wrasse (adult or juvenile). Both settlement-stage (0 d post-settlement) and juvenile (~5 weeks post-settlement) fish spent a greater proportion of time in a microhabitat adjacent to L. dimidiatus than in one next to a control fish (a non-cleaner wrasse, Halichoeres melanurus) or one where no fish was present. This suggests that cleaner wrasse may serve as a positive cue during microhabitat selection. We also conducted focal observations of cleaner wrasse and counts of nearby damselfishes (1 m radius) to examine whether newly settled fish obtained direct benefits, in the form of cleaning services, from being near a cleaner wrasse. Although abundant, newly settled recruits (<20 mm total length) were rarely (2 %) observed being cleaned in 20 min observations compared with larger damselfishes (58 %). Individual damselfish that were cleaned were significantly larger than the median size of the surrounding nearby non-cleaned conspecifics; this was consistent across four species. The selection by settlement-stage fish of a microhabitat adjacent to cleaner wrasse in the laboratory, despite only being rarely cleaned in the natural environment, suggests that even rare cleaning events and/or indirect benefits may drive their settlement choices. This behaviour may also explain the decreased abundance of young fishes on reefs from which cleaner wrasse had been experimentally removed. This study reinforces the potentially important role of mutualism during the processes of settlement and recruitment of young reef fishes.     

Courtship and spawning sounds in bird wrasse Gomphosus varius and saddle wrasse Thalassoma duperrey

Acoustic signals from the bird wrasse Gomphosus varius and saddle wrasse Thalassoma duperrey were recorded on coral reefs in Hawaii. Terminal phase males in both species emit two types of pulse trains (type I and type II). Type I pulses were produced during spawning and courtship, while type II pulses were associated only with courtship behaviours. Gomphosus varius type I pulses were of lower frequency than T. duperrey type I pulses (271 v. 840 Hz) and were of narrower band. Discriminant function analyses revealed interspecific differences between type I pulse trains and individual pulses of both types. This study is the first documentation of courtship and spawning sounds in sympatric labrids and shows divergence in acoustic signals.     

Association of the whale shark Rhincodon typus with the cannonball jellyfish Stomolophus meleagris

This study describes the first record of the whale shark Rhincodon typus association with the cannonball jellyfish Stomolophus meleagris in the Gulf of California, Mexico. Whale sharks were observed swimming and feeding among swarms of jellyfish, suggesting competition and predatory behaviour given the overlap in food preferences between both species. This finding is relevant because of the species‐wide distribution and the importance of these interactions, which should be considered in conservation strategies of R. typus and management of cannonball jellyfish fisheries.     

Habitat suitability of Rhincodon typus in three localities of the Gulf of California: Environmental drivers of seasonal aggregations

The whale shark is an endangered species that usually feeds in coastal areas of highly productive seas such as the Gulf of California, Mexico. This study aims to describe the effect of sea surface temperature, chlorophyll a, bathymetry and slope on the habitat suitability of whale sharks in three important aggregation sites of the Gulf of California. A total of 2396 records of occurrence of whale sharks were obtained from international databases and scientific literature between 1996 and 2018. These records were used for the creation of a species distribution model using MaxEnt for each of the three aggregation sites. The concentration of chlorophyll a explained 71% of the habitat suitability, followed by bathymetry and slope with a combined 17%, and sea surface temperature constituting 10% of the model. Habitat suitability was related to areas where nontargeted fisheries may impact whale sharks through bycatch, entanglement and ship strikes. The implications for the conservation of whale sharks should be considered for management decisions in terms of marine protected areas, fishing refugees or bans, and other regulations regarding fisheries activities.     

Cleaning by the wrasse Thalassoma noronhanum, with two records of predation by its grouper client Cephalopholis fulva

The Noronha wrasse Thalassoma noronhanum was recorded cleaning 19 client fish species at Fernando de Noronha Archipelago, o. north–eastern Brazil. The preferred clients were non–dangerous, mostly planktivorous species, whereas the potentially dangerous, predatory species were rarely cleaned. T. noronhanum acts as a cleaner in two distinct ecological situations, at and outside the cleaning stations, and attends different client species in each of them. Potentially dangerous clients were mostly attended outside the cleaning stations. Many attacks and two instances of predation on the cleaner wrasse by the grouper client Cephalopholis fulva were recorded. The attacks occurred on individual wrasses foraging near the bottom outside the cleaning stations.     

A continuous genome assembly of the corkwing wrasse (Symphodus melops)

The wrasses (Labridae) are one of the most successful and species-rich families of the Perciformes order of teleost fish. Its members display great morphological diversity, and occupy distinct trophic levels in coastal waters and coral reefs. The cleaning behaviour displayed by some wrasses, such as corkwing wrasse (Symphodus melops), is of particular interest for the salmon aquaculture industry to combat and control sea lice infestation as an alternative to chemicals and pharmaceuticals. There are still few genome assemblies available within this fish family for comparative and functional studies, despite the rapid increase in genome resources generated during the past years. Here, we present a highly continuous genome assembly of the corkwing wrasse using PacBio SMRT sequencing (x28.8) followed by error correction with paired-end Illumina data (x132.9). The present genome assembly consists of 5040 contigs (N50?=?461,652?bp) and a total size of 614 Mbp, of which 8.5% of the genome sequence encode known repeated elements. The genome assembly covers 94.21% of highly conserved genes across ray-finned fish species. We find evidence for increased copy numbers specific for corkwing wrasse possibly highlighting diversification and adaptive processes in gene families including N-linked glycosylation (ST8SIA6) and stress response kinases (HIPK1). By comparative analyses, we discover that de novo repeats, often not properly investigated during genome annotation, encode hundreds of immune-related genes. This new genomic resource, together with the ballan wrasse (Labrus bergylta), will allow for in-depth comparative genomics as well as population genetic analyses for the understudied wrasses.     

Roving and Service Quality in the Cleaner Wrasse Labroides bicolor

The cleaner wrasse Labroides dimidiatus occupies fixed ‘cleaning stations’ on coral reefs, which ‘client’ reef fish visit repeatedly to have parasites removed. Conflict arises because cleaners prefer to cheat by feeding on client mucus instead of parasites. Clients can prevent L. dimidiatus from always cheating using control mechanisms such as chasing and partner switching, which depend on repeated interactions. These control mechanisms would be undermined in the absence of frequent repeated interactions, if cleaners roved over large areas. Roving behaviour has been anecdotally described for the closely related cleaner wrasse Labroides bicolor. Here we report field data comparing these two species in Moorea, French Polynesia. Our results confirmed that L. bicolor home ranges are much larger than L. dimidiatus home ranges, and showed that cleaning interactions occurred all over the L. bicolor home range: home range of cleaning interactions increased with total home range size. Moreover, we found that cleaner initiation of interactions increased with home range size in L. bicolor, which would give L. bicolor with large home ranges additional leverage to increase cheating. In line with these results, we found that client jolt rate (used as a measure of cheating) was higher among clients of cleaners with large home ranges. Our results emphasise the importance of game structure and control over initiating interactions as parameters in determining the nature of interactions in mutualisms.     

Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo‐Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea‐level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial‐scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo‐Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales.     

Importance of sandy bottoms in coral reefs to the oscillation of daily rhythms in the tropical wrasse Halichoeres trimaculatus

Most wrasse species swim during the day and bury themselves in the sandy bottoms of shallow reefs at night. This study aimed to evaluate the importance of sandy bottoms to the day-active/night-inactive rhythmicity of the tropical wrasse Halichoeres trimaculatus. Actogram analysis revealed that fish were active during the photophase and inactive during the scotophase in aquariums with both sandy and bare bottoms. When fish were kept in aquariums with bare bottoms, rhythmicity was maintained under constant dark conditions (DD) but became obscured under constant light conditions (LL), suggesting that a day-active/night-inactive rhythmicity is regulated by the circadian system. Robust fluctuations in Period1 (wPer1) and Period2 (wPer2) expression were observed in the pectoral fin tissue under light–dark conditions (LD). Similar fluctuations in wPer1 expression persisted under DD. When fish were kept under LD conditions for 7 days and then DD for 20 days, the emergence of fish from the sandy bottom was delayed gradually. At the same time, the peak time of wPer1 expression under DD was retarded from 06:00 to 10:00. Although wPer2 expression was dampened under DD, it increased after exposing fish to light. These results suggest that wPer1 and wPer2 are differentially involved in the day-active/night-inactive rhythmicity, and that blocking light with a sandy bed at night and exposing fish to light during emergence in the morning play important roles in maintaining consistent activities in wrasse species.     

Acquisition of a defended resource: a benefit of group foraging for the neotropical wrasse,Thalassoma lucasanum

Synopsis The neotropical Pacific wrasse, Thalassoma lucasanum, forms groups of 30 to 300 individuals that overwhelm the defense of embryos by the Pacific sergeant major, Abudefduf troschelii, and thereby gain access to a food resource from which solitary individuals are effectively excluded by paternal defense. The duration of feeding by the wrasse groups and the fraction of embryos eaten in a nest are positively correlated with group size. The benefit of group foraging is probably derived from a reduction in the frequency with which group members experience attack by defending sergeant majors, as reflected in the positive correlation of group size with feeding duration. Large foraging groups only form when sergeant major embryos are present in nests, indicating that this is a primary benefit of participation in these groups for this wrasse. In contrast, in the Caribbean large foraging groups of the congeneric bluehead wrasse, T. bifasciatum, fail to form despite the presence of defended embryos of the Caribbean sergeant major, A. saxatilis. This might be due to the relatively low population densities of the Caribbean wrasse in comparison to those of the Pacific wrasse or to the relatively low densities of Caribbean sergeant major nests containing embryos at any time.     

A comparative study of cleaning activity of two reef fishes at Fernando de Noronha Archipelago,tropical West Atlantic

Cleaner fishes are usually classified as obligate or facultative cleaners according to their diet and the extent to which their nutritional requirements in the different ontogenetic stages are gained from cleaning. While obligate cleaners clean throughout their lives and ingest mainly food taken from the clients’ body surface, facultative cleaners clean only as juveniles and have a broader diet. In addition, some facultative cleaners may experience a relatively higher predation risk, and thus rarely interact with piscivorous fishes. Despite these acknowledged differences, there are very few studies that compare cleaning activity of obligate and facultative cleaners within the same area. Cleaning activity of the obligate cleaner goby Elacatinus cf. randalli and the facultative cleaner wrasse Thalassoma noronhanum were comparatively examined at Fernando de Noronha Archipelago, tropical West Atlantic. The client assemblage attended by the two cleaners differed, as the goby attended a slightly greater diversity of species (22), mostly piscivores and zoobenthivores, and the wrasse attended fewer species (19), mostly planktivores. Chromis multilineata was the most common client species of both cleaners, although body size (which is expected to be positively correlated to clients’ ectoparasite load) of C. multilineata individuals attended by the goby was larger than that of the individuals attended by the wrasse. Despite such differences, T. noronhanum showed a surprisingly species-rich client assemblage when compared with other cleaners of the genus Thalassoma. In addition, the frequency and time spent on cleaning interactions, as well as the number of client species attended per 10-min period, was similar for both cleaner species, which indicate that they have important yet complimentary ecological roles in the reef community at Fernando de Noronha Archipelago.     

Ensemble modeling of the potential distribution of the whale shark in the Atlantic Ocean

The whale shark (Rhincodon typus) is an endangered marine fish species which can be adversely affected by the fishing activities of the industrial purse seine fleet targeting tropical tuna. Tuna tend to aggregate around all types of floating objects, including whale sharks. We analyzed and modeled the spatial distribution and environmental preferences of whale sharks based on the presence and absence data from fishing observations in the Atlantic Ocean. We used a thorough multialgorithm analysis, based on a new presence–absence dataset, and endeavored to follow the most recent recommendations on best practices in species distribution modeling. First, we selected a subset of relevant variables using a generalized linear model that addressed multicollinearity, statistical errors, and information criteria. We then used the selected variables to build a model ensemble including 19 different algorithms. After eliminating models with insufficient performance, we assessed the potential distribution of whale sharks using the mean of the predictions of the selected models. We also assessed the variance among the predictions of different algorithms, in order to identify areas with the highest model consensus. The results show that several coastal regions and warm shallow currents, such as the Gulf Stream and the Canary and Benguela currents, are the most suitable areas for whale sharks under current environmental conditions. Future environmental projections for the Atlantic Ocean suggest that some of the suitable regions will shift northward, but current concentration areas will continue to be suitable for whale shark, although with less productivity, which could have negative consequences for conservation of the species. We discuss the implications of these predictions for the conservation and management of this charismatic marine species.     

Evidence of continued hunting of whale sharks <Emphasis Type="Italic">Rhincodon typus</Emphasis> in the Maldives

Superficial dermal wounds in whale sharks are reported to heal rapidly as with many other elasmobranchs. Here observations of two wounded whale sharks (Rhincodon typus) in Maldivian waters suggest that free ranging sharks are able to recover and rapidly heal from the effects of deeper wounding on internal organs or amputations. One specimen observed impaled by a wooden harpoon shaft, was subsequently re-encountered nearly a year later. The other suffered a near severed first dorsal fin but showed signs of rapid healing. These observations illustrate that despite national bans in whale sharks fishing, the practise persists in the Maldives. Further research to increase understanding of the demography of aggregations of this species is necessary before the impact of illegal exploitation on regional population trends can be determined. National governments are encouraged to enhance marine conservation outreach and education programmes throughout their territories.     

Cleaner wrasse mimics inflict higher costs on their models when they are more aggressive towards signal receivers

Aggressive mimics are predatory species that resemble a 'model' species to gain access to food, mating opportunities or transportation at the expense of a signal receiver. Costs to the model may be variable, depending on the strength of the interaction between mimics and signal receivers. In the Indopacific, the bluestriped fangblenny Plagiotremus rhinorhynchos mimics juvenile cleaner wrasse Labroides dimidiatus. Instead of removing ectoparasites from larger coral reef fish, fangblennies attack fish to feed on scales and body tissue. In this study, juvenile cleaner wrasse suffered significant costs when associated with P. rhinorhynchos mimics in terms of reduced cleaning activity. Furthermore, the costs incurred by the model increased with heightened aggression by mimics towards signal receivers. This was apparently because of behavioural changes in signal receivers, as cleaning stations with mimics that attacked frequently were visited less. Variation in the costs incurred by the model may influence mimicry accuracy and avoidance learning by the signal receiver and thus affect the overall success and maintenance of the mimicry system.     

A missing piece in the Arctic food web puzzle? Stomach contents of Greenland sharks sampled in Svalbard, Norway

Harbour seals in Svalbard have short longevity, despite being protected from human hunting and having limited terrestrial predation at their haulout sites, low contaminant burdens and no fishery by-catch issues. This led us to explore the diet of Greenland sharks (Somniosus microcephalus) in this region as a potential seal predator. We examined gastrointestinal tracts (GITs) from 45 Greenland sharks in this study. These sharks ranged from 229 to 381?cm in fork length and 136–700?kg in body mass; all were sexually immature. Seal and whale tissues were found in 36.4 and 18.2%, respectively, of the GITs that had contents (n?=?33). Based on genetic analyses, the dominant seal prey species was the ringed seal (Pusa hispida); bearded seal (Erignathus barbatus) and hooded seal (Cystophora cristata) tissues were each found in a single shark. The sharks had eaten ringed seal pups and adults based on the presence of lanugo-covered prey (pups) and age determinations based on growth rings on claws (≤1?year and adults). All of the whale tissue was from minke whale (Balenoptera acutorostrata) offal, from animals that had been harvested in the whale fishery near Svalbard. Fish dominated the sharks’ diet, with Atlantic cod (Gadus morhua), Atlantic wolffish (Anarhichas lupus) and haddock (Melanogrammus aeglefinus) being the most important fish species. Circumstantial evidence suggests that these sharks actively prey on seals and fishes, in addition to eating carrion such as the whale tissue. Our study suggests that Greenland sharks may play a significant predatory role in Arctic food webs.     

Aggressive mimicry of the cleaner wrasse by Aspidontus taeniatus functions mainly for small blennies

The mimic blenny Aspidontus taeniatus Quoy & Gaimard is well known for its resemblance to the juvenile and adult cleaner wrasse Labroides dimidiatus (Valenciennes) in colour and shape. As various reef fishes including piscivores actively approach the cleaner wrasse to solicit cleaning by posing, two types of benefits have been suggested for this resemblance, that is, protective mimicry and aggressive mimicry. In aggressive mimicry, the mimic blenny is supposed to have considerable opportunities to bite the fin of deceived fishes when they pose, but some studies have confirmed that fin biting does not seem to be the main feeding tactic in the blenny in nature. Here, we examined the feeding tactics including fin biting by the mimic blenny in relation to its body size in a field observational survey in the coral reefs of Sesoko Island, Okinawa, Japan. The blenny was observed feeding mainly on four food items: the tentacles of Christmas tree worms, the mantle edges of boring clams, the demersal eggs in damselfishes’ nests and the fins of fishes. The feeding frequency by fin biting significantly decreased with body size, while that by egg predation significantly increased with body size of the blenny. When predating on eggs, the blenny was vigorously attacked by egg‐guarding fish, but often succeeded in raiding their nests by forming a feeding group. When feeding by fin biting, the blenny attacked prey fish without performing any cleaning. The ratio of fin biting was considerably higher in small‐sized blennies, suggesting reliance on this feeding tactic because of a difficulty in conducting a risky egg predation. Thus, our results suggest that the mimic blenny utilizes aggressive mimicry only when it is small as an alternative feeding tactic.     

Scarring patterns and relative mortality rates of Indian Ocean whale sharks

This study recorded the scarring rate and severity for whale sharks Rhincodon typus from three Indian Ocean aggregations (Australia, Seychelles and Mozambique), and examined whether scarring (mostly attributed to boat strikes and predator attacks) influences apparent survival rates using photo‐identification libraries. Identifications were based on spot‐and‐stripe patterns that are unique to individual whale sharks. Scarring was most prevalent in the Seychelles aggregation (67% of individuals). Predator bites were the most frequent source of scarring (aside from minor nicks and abrasions) and 27% of individuals had scars consistent with predator attacks. A similar proportion of whale sharks had blunt trauma, laceration and amputation scars, the majority of which appeared to be caused by ship collisions. Predator bites were more common (44% of individuals) and scars from ship collisions were less common at Ningaloo Reef than at the other two locations (probability of among‐site differences occurring randomly = 0·0007 based on a randomized multinomial contingency analysis). In all aggregations, scars occurred most often on the caudal fin, which may result from the fin being the body part closest to the surface when boats pass over, or they may provide a large target for predator attack. No evidence was found for an effect of scarring on apparent survival (φ; mean ±s .e .) for the Ningaloo (not scarred φ= 0·858 ± 0·033; scarred φ= 0·929 ± 0·033) or Seychelles populations (not scarred φ= 0·502 ± 0·060; scarred φ= 0·538 ± 0·070). The lower apparent survival of the Seychelles population may be attributed to a high number of transient whale sharks in this aggregation that might bias estimates. This study indicates that while scarring from natural predators and smaller vessels appears to be unrelated to whale shark survival, the effect of deaths related to ship strike need to be quantified to assist in future management of this species.     

Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs

Mutualisms affect the biodiversity, distribution and abundance of biological communities. However, ecological processes that drive mutualism-related shifts in population structure are often unclear and must be examined to elucidate how complex, multi-species mutualistic networks are formed and structured. In this study, we investigated how the presence of key marine mutualistic partners can drive the organisation of local communities on coral reefs. The cleaner wrasse, Labroides dimidiatus, removes ectoparasites and reduces stress hormones for multiple reef fish species, and their presence on coral reefs increases fish abundance and diversity. Such changes in population structure could be driven by increased recruitment of larval fish at settlement, or by post-settlement processes such as modified levels of migration or predation. We conducted a controlled field experiment to examine the effect of cleaners on recruitment processes of a common group of reef fishes, and showed that small patch reefs (61–285 m²) with cleaner wrasse had higher abundances of damselfish recruits than reefs from which cleaner wrasse had been removed over a 12-year period. However, the presence of cleaner wrasse did not affect species diversity of damselfish recruits. Our study provides evidence of the ecological processes that underpin changes in local population structure in the presence of a key mutualistic partner.     

Isolation,identification and characterisation of ballan wrasse Labrus bergylta plasma pigment

This study confirmed that observations of blue‐green colouration in plasma fractions of the ballan wrasse Labrus bergylta were caused by the linear tetra‐pyrrole biliverdin and that the molecule was of the physiologically relevant IXα isomer. Accumulation appears driven by chromogenic association with an unknown protein moiety which precludes enzymatic reduction and would suggest active management. It was demonstrated that the pigment did not fluctuate relative to ontogeny, or indeed binary gender in the species of interest, but mobilisation and depletion in the subset of individuals undergoing sex change at the time of study supports a potential association with gender inversion processes. It is of note that although biliverdin does have some effect on external colouration, the evidence is indicative that crypsis is a supplementary function thus other factors must be considered.