Cleaning symbiosis and the disease triangle

Pauline Narvaez found that the dedicated cleaner fish, Labroides dimidiatus, is susceptible to a diversity of parasites and can potentially transmit them to their fish clients. Her work presents a paradigm shift in the prevailing theory that cleaning symbiosis has predominantly positive impacts on coral reef fish communities

Interacções mutualísticas envolvendo os peixes limpadores facultativos Coris julis e Thalassoma pavo

Tese de mestrado. Biologia (Ecologia Marinha). Universidade de Lisboa, Faculdade de Ciências, 2013O comportamento das espécies de peixes limpadores facultativos de águas temperadas, só recentemente começou a ser estudado ao contrário do que sucede em águas tropicais. Duas espécies de labrídeos, Coris julis e Thalassoma pavo, são caracterizadas como limpadoras nas águas costeiras dos Açores, mas pouco se sabe sobre as suas interacções mutualísticas. Com vista a colmatar esta lacuna, este trabalho analisa o comportamento destas duas espécies de peixes limpadores e dos seus peixes visitantes (referidos como “clientes”) aos seus territórios fixos (referidos como “estações de limpeza”), comparando a frequência das suas interacções com aquelas observadas em locais não fixos e no sentido de determinar: a) qual a dependência dos limpadores relativamente às suas actividades mutualísticas, e b) o impacto do seu comportamento nos níveis de infestação da sua “clientela”. Depois de se ter confirmado a existência de “estações de limpeza” nas costas da Ilha de São Miguel, dez estações de limpeza envolvendo C. julis e dez envolvendo T. pavo foram definidas, contabilizando-se um total de 600 min de observações. Para além disso, fora das “estações de limpeza”, 13 observações foram feitas para C. julis e cinco para T. pavo num total de 540 min de observações. Todas as observações foram feitas durante 30 min. Foram capturados aleatoriamente (fora do contexto de limpeza) trinta C. julis e trinta T. pavo, assim como três C. julis e dois T. pavo considerados como limpadores (no contexto de limpeza) presentes nas suas “estações de limpeza”, para posterior análise dos seus conteúdos estomacais. No sentido de determinar o nível de infestação parasitária foram capturados um total de 77 indivíduos pertencentes a oito espécies diferentes de “clientes” e “controlos” (Symphodus caeruleus, Sparisoma cretense, Abudefduf luridus, Sarpa salpa, Labrus bergylta, Mullus surmuletus, Serranus atricauda e Diplodus sargus) que se encontravam nas imediações das “estações de limpeza”. Dentro das estações de limpeza, foram observadas mais interacções entre T. pavo e os seus “clientes” (12, 4 ± 2,3) do que C. julis (10, 7 ± 1,3), enquanto fora das “estações de limpezas” ocorreu o inverso (C. julis: 3 ± 1,8; T. pavo: 1,75 ± 0,8). No conjunto de todas as observações comportamentais das duas espécies de limpadores, não foram encontradas diferenças significativas na diversidade específica dos seus “clientes”, contabilizando um total de sete espécies, seis destas observadas como “clientes” de C. julis (S. caeruleus, S. cretense, A. luridus, L. bergylta, M. surmuletus e C. julis) e quatro de T. pavo (S. caeruleus, S. cretense, S. salpa, L. bergylta), sendo a espécie S. caeruleus o “cliente” dominante no total das interacções de limpeza. Maior parte dos “clientes” foram observados a iniciar as interacções de limpeza adoptando uma postura específica (78,9 %), sendo estas interacções normalmente terminadas pelos limpadores (81,9 %). Uma correlação significativamente positiva foi encontrada entre o número de toques e a área dos peixes “clientes” para ambas as espécie de limpadores, mas a espécie T. pavo passou significativamente mais tempo com os “clientes” maiores, enquanto para C. julis nenhuma relação foi encontrada. Para além disso, T. pavo fez esperar os seus “clientes” significativamente mais tempo do que C. julis e no que toca aos seus níveis de cooperação com a espécie “cliente” S. caeruleus, o limpador C. julis provocou significativamente mais “jolts” (medida comportamental de desonestidade por parte do limpador) em comparação a T. pavo. Foram encontradas diferenças significativas na dieta geral entre C. julis e T. pavo capturados aleatoriamente. O item crustáceos dominou a dieta de ambas as espécies mas demonstrou-se mais importante para a espécie T. pavo, enquanto ectoparasitas (larvas de gnatídeos) foram exclusivamente encontrados na dieta de C. julis. Comparando a dieta de C. julis e T. pavo capturados aleatoriamente com os limpadores, observou-se diferenças onde os limpadores alimentam-se quase exclusivamente de ectoparasitas e apresentaram muco (dois C. julis), enquanto as semelhanças se centralizaram na presença de escamas nos seus conteúdos estomacais. Foram também encontradas diferenças significativas na carga parasitária de todas espécies caracterizadas como “clientes” (S. caeruleus, S. cretense, A. luridus, S. salpa, L. bergylta, M. surmuletus) e “controlos” (S. atricauda, D. sargus), revelando uma dominância de ectoparasitas da família Caligidae em comparação a Gnathiidae. Ainda esta carga parasitária não se mostrou positivamente relacionada com as respectivas áreas corporais dos “clientes” e “controlos”. Num conjunto de todas as interacções de limpeza (dentro e fora de “estações de limpeza”), o limpador C. julis parece ser a espécie mais especializada nesta actividade apresentando um maior número de interacções e um maior leque de espécies “clientes”. Para além disso, esta espécie parece dirigir a sua procura alimentar em torno dos ectoparasitas de forma mais específica e eficaz no corpo dos seus “clientes”, reduzindo o tempo de interacção e a espera dos mesmos, em comparação com T. pavo. A existência de muco (item mais nutritivo e calórico) nos conteúdos estomacais dos C. julis é indicadora de maior batota nesta espécie. A espécie de “cliente” S. caeruleus domina as interacções de limpeza para ambos os limpadores provavelmente devido à sua grande abundância na comunidade costeira dos Açores e à sua maior carga parasitária em gnatídeos (o que aumenta a sua necessidade em ser limpo). No global, em “estações de limpeza” foram os “clientes” que iniciaram com mais frequência as interacções, o que acentua as suas necessidades em serem limpos, enquanto os limpadores terminaram com mais frequência as interacções, o que provavelmente estará relacionado com o esgotamento da fonte principal de alimento (ectoparasitas) na superfície do corpo dos “clientes”. Apesar do número de toques de ambas as espécies de limpadores estar positivamente relacionado com áreas do corpo dos seus “clientes”, o facto de não se ter encontrado uma relação positiva entre o número de ectoparasitas por “cliente” e as suas áreas poderá estar associado ao facto de “clientes” de maiores dimensões poderem apresentar uma distribuição mais difusa de ectoparasitas na superficie dos seus corpos. Os peixes limpadores que limpam em “estações de limpeza” parecem ser mais dependentes de interacções comparado com os peixes aleatórios, embora destes alguns C. julis tenham sido encontrados com ectoparasitas o que reflecte uma maior dependência desta espécie por esta actividade. A dominância de caligídeos como parasitas dos “clientes” pode estar relacionada com a grande selectividade e preferência por parte dos limpadores por gnatídeos. Este exemplo de interacções mutualísticas permitem elevar o papel ecológico das espécies C. julis e T. pavo que, para além de lhes proporcionar uma fonte de alimentação adicional ou mesmo essencial, provavelmente terão um impacto positivo nas comunidades de peixes costeiros dos Açores.The behavior of the cleaning facultative fish species in temperate waters was studied only recently unlike the species in tropical waters. Two species of Labridae, Coris julis and Thalassoma pavo are characterized as cleaner fishes in the waters of the Azorian coastline but there is still little knowledge about their mutualistic interactions. To fill this gap, this paper analyses the behavior of these two species of cleaner fishes and their visitors (called “clients”) in their fixed territory (called “cleaning stations”), comparing the frequency of their interactions with the one observed in non-permanent territories to determine: a) the dependency of the cleaners fishes related to their mutualistic interactions and b) the impact of their behavior concerning the level of infestation of their “clients”. After being confirmed the existence of the “cleaning stations” at the coastline of the island of São Miguel, ten “cleaning stations” of C. julis and ten of T. pavo were defined, counting a total of 600 min of observation. In addition to these “cleaning stations”, 13 other observations were made for C. julis and five for T. pavo in a total of 540 min of observation. All observations were made in a time scale of 30 minutes. There were captured randomly (outside the context of the cleaning) thirty C. julis and thirty T. pavo, as well as tree C. julis and two T. pavo considered as cleaners (in the context of cleaning) present in their “cleaning stations” for posterior analysis of the content of their stomachs. To determine the level of parasitic infestation there were captured a total of 77 individuals belonging to eight different species of “clients” and “controls” (Symphodus caeruleus, Sparisoma cretense, Abudefduf luridus, Sarpa salpa, Labrus bergylta, Mullus surmuletus, Serranus atricauda e Diplodus sargus), which were found near the “cleaning stations”. More interactions between T. pavo and their clients (12,4 ± 2,3) have been observed than with C. julis (10, 7 ± 1,3), while outside the “cleaning stations” the opposite was being observed (C. julis: 3 ± 1,8; T. pavo: 1,75 ± 0,8). No significant differences were found in the total of the observation in the behavior of the two cleaners species concerning the specific diversity of their “clients”, counting a total of seven species, six of them were observed as “clients” of C. julis (S. caeruleus, S. cretense, A. luridus, L. bergylta, M. surmuletus e C. julis) and four of T. pavo (S. caeruleus, S. cretense, S. salpa, L. bergylta), being the specie S. caerulues the dominant “client” in the total of the cleaning interactions. The most part of the “clients” were observed initiating the cleaning interactions adopting a special position (78,9 %), when normally these interactions are finished by the cleaners (81,9 %). It was found a significantly positive correlation between the number of touches and the area of the “client” fishes for both cleaner species, but the specie T. pavo spent significantly more time with bigger “clients” while there was no such relationship found for the C. julis. Beside, T. pavo made their “clients” wait more time than C. julis and concerning the level of cooperation with the “client” species S. caeruleus, the cleaner C. julis provoked significantly more jolts comparing to T. pavo. Significant differences were found in the general diet between C. julis and T. pavo, which were captured randomly. The crustacean item dominated the diet of both species but was more important to the T. pavo, while ectoparasites (gnathiid larvae) were exclusively found in the diet of C. julis. Comparing the diets of C. julis and T. pavo captured randomly with the cleaners, differences were observed where the cleaners fed themselves almost exclusively of ectoparasites and presented mucos (two C. julis), while a similarity was found in the presence of scales in the content of their stomachs. There were found major differences in the parasitic load of all species characterized as “clients” (S. caeruleus, S. cretense, A. luridus, S. salpa, L. bergylta, M. surmuletus) and “controllers” (S. atricauda, D. sargus), revealing a dominance of the ectoparasites of the Caligidae family in comparison to the Gnathiidae. Even this parasitic load didn´t show itself related to the respective area of the body of the “clients” and “controls”. In all cleaning interactions (inside and outside the “cleaning stations”), the cleaner C. julis seems to be the species more specialized in this activity, presenting a major number of interactions and a major variety of “clients” species. Beside this, this specie seems to search their food of ectoparasites in a more specific and effective way on the bodies of their “clients”, reducing the time of interaction and waiting comparing to T. pavo. The existence of mucos (a more nutritious and caloric item) in the content of the stomachs of C. julis is an indicator of cheating. The specie of the “client” S. caeruleus dominates the cleaning interactions for both cleaners, probably due to their abundance in the community of the Azorean coastline and their bigger parasitic load of gnathiid (which increases their need for being cleaned). In a global perspective, the “clients” of the “cleaning stations” initiated with more frequency the interactions, which show their need for being cleaned, while the cleaners stopped the interactions with more frequency, probably due to the lack of the main source of food (ectoparasites) on the surface of the bodies of the “clients”. Even though the number of touches of both cleaning species was positively related to the body areas of their “clients”, the fact that there wasn´t found any positive relation between the number of ectoparasites per “client” and their areas, could be due to the fact that the “clients” which presents bigger dimension could present a more diffused distribution of ectoparasites on the surface of their bodies. The cleaner fishes which were cleaning in the “cleaning stations” seem to be more dependent on the interactions than the random fishes, even though some of the C. julis have been found with ectoparasites, which reflect a bigger dependency of this species in this activity. A dominance of the caligid as a parasite of the “clients” could be related to a bigger selectivity and preference by the cleaners of the gnathiid. This example of mutual interactions allows to give the species C. julis and T. pavo a bigger ecological function which has a positive impact on the communities of fishes on the Azorean coastline, besides giving them an additional source of food

Le parasite isopode, Anilocra physodes, nouvelle source de nourriture pour le poisson lézard Synodus saurus (Synodontidae)

Copyright © 2015 Société Française d'Ichtyologie.During a wide project carried out on the behavior and reproduction of the Atlantic lizardfish Synodus saurus in the Azores (NE Atlantic), specimens of the ectoparasitic isopod Anilocra physodes were discovered in various stomachs contents of these piscivorous predatory fish. This intriguing result allowed us to conclude for the first time that fish species can ingest their own parasites, which becomes doubly beneficial, since it releases them from para- sites but it is also a new food source.RÉSUMÉ: Au cours de différents travaux menés sur le comportement et la reproduction du poisson lézard de l’Atlantique, Synodus saurus, aux Açores (Atlantique NE), des ectoparasites isopodes, Anilocra physodes, ont été découverts dans divers contenus stomacaux de ces prédateurs piscivores. Ce résultat intriguant nous a permis de conclure pour la première fois que des espèces de poissons peuvent ingérer leurs propres parasites, ce qui peut être doublement bénéfi- que pour eux, qui, tout en s’en libérant, disposent d’une nouvelle source de nourriture

Not so monochromatic: Size-dependency of both sex and color in the cleaner wrasse Labroides dimidiatus

In marine interspecific cleaning mutualisms, small fish known as “cleaners” inspect the surface, gills and sometimes the mouth of “client” reef fish, eating ectoparasites, mucus, scales and dead or infected tissue. These cleaner fish species share similar vivid coloration that makes them recognizable by clients. To gain insight on additional communication roles of cleaner fish color, we tested if differences in color among cleaner wrasse Labroides dimidiatus individuals captured from the wild are explained by sex, body size or parasite loads. We found that males were larger, heavier and tended to have more saturated blue tails than females. We also found blue color saturation to be positively correlated with size, and that this size-dependence explains the trend for the sexes to differ in color. Parasite loads did not predict individual differences in color, but fish in our sample were not heavily parasitized. Other color traits (including yellow color saturation and black color brightness) did not differ between the sexes and were associated with morphological differences. Size-dependence of blue color may thus suggest that it is a condition-dependent signal that could be used in various types of inter- and intraspecific social interactions

Temperate facultative cleaner wrasses selectively remove ectoparasites from their client-fish in the Azores

Cleaner fishes are key contributors to the health of fish communities. However, much of the information in the literature refers to tropical systems, while fewer studies have examined the activity of cleaner fish inhabiting temperate ecosystems. Facultative cleaner fish are assumed to clean only during their juvenile phase, and have a broader diet than obligatory cleaner fish. Here, we focused on 2 facultative cleaner fish species, Coris julis and Thalassoma pavo, that live along the temperate coasts of the Azorean island of São Miguel. We found that these species focused their cleaning activities on relatively few species of clients, which supports the general idea that facultative cleaner fishes in temperate waters are less dependent on cleaning interactions than obligatory cleaner fishes in tropical waters. Both cleaner species were found to give more bites per host when inspecting larger clients, likely because the latter typically host more parasites. We found that C. julis consumed a greater diversity of food items, which included gnathiid larvae and fewer caligid copepods, compared to T. pavo where no ectoparasites were found. All cleaner fish that we collected after observations of cleaning had eaten gnathiid isopod larvae but not caligid copepods, even though caligid copepods were the most abundant ectoparasite found on the body of 7 selected fish species (including both client and non-client species), suggesting that both species selectively feed on gnathiid isopods. This study is the first to demonstrate that temperate facultative cleaner fish species actively and selectively inspect and remove ectoparasites from their client-fish species.Fundação para a Ciência e Tecnologia (FCT, grant PTDC/MAR/105276/2008. European Regional Development Fund (ERDF) COMPETE - Operational Competitiveness Programme. FCT - Foundation for Science and Techno - project PEst-C/MAR/LA0015/2011.info:eu-repo/semantics/publishedVersio

New perspectives on the role of cleaning symbiosis in the possible transmission of fish diseases

For the last seven decades, cleaning symbiosis in the marine environment has been a research field of intrigue. There is substantial evidence that, by removing undesired items from their client fishes, cleaner organisms have positive ecosystem effects. These include increased fish recruitment, abundance and enhanced fish growth. However, the intimate association and high frequency of interactions between cleaners and clients potentially facilitates pathogen transmission and disease spread. In this review, we identify knowledge gaps and develop novel hypotheses on the interrelationship between parasites, hosts and the environment (disease triangle concept), with a particular emphasis on the potential role of cleaner organisms as hosts and/or transmitters of parasites. Despite evidence supporting the positive effects of cleaner organisms, we propose the cleaners as transmitters hypothesis; that some parasites may benefit from facilitated transmission to cleaners during cleaning interactions, or may use cleaner organisms as transmitters to infect a wider diversity and number of hosts. This cost of cleaning interactions has not been previously accounted for in cleaning theory. We also propose the parasite hotspot hypothesis; that parasite infection pressure may be higher around cleaning stations, thus presenting a conundrum for the infected client with respect to cleaning frequency and duration. The impact of a changing environment, particularly climate stressors on cleaners’ performance and clients’ cleaning demand are only beginning to be explored. It can be expected that cleaners, hosts/clients, and parasites will be impacted in different ways by anthropogenic changes which may disrupt the long-term stability of cleaning symbiosis

Are cleaner fish clean?

Cleaner fish remove parasites from other organisms, called clients. While there is an extensive body of work on the positive role of cleaners for their clients and reef communities, remarkably, potential parasites hosted by specialised cleaner fishes themselves have not been explored. In this study, we surveyed the parasite community of the Indo-Pacific cleaner wrasse Labroides dimidiatus, and compared it to other wrasses from the same region. L. dimidiatus was found to be infected by eight parasite groups including ectoparasites (copepods, isopods, trichodinids, monogeneans and turbellarians) and endoparasites (myxozoans, trematodes and cestodes) representing at least 12 species. The abundance and prevalence of most parasite groups was comparable to other wrasses, with the exception of bucephalid trematodes, which are not known to infect any other tropical wrasses except for Labroides species. This adds to mounting evidence that some parasite species exhibit atypical life cycles that exploit cleaning symbiosis. Particularly noteworthy was the discovery of gnathiid isopods on L. dimidiatus, which are generally considered the cleaner’s primary food item. Our findings provide new evidence for a potential role of wild cleaner fish as vectors of parasites to new clients, which highlights potential costs associated with cleaning symbiosis

Habitat degradation drives increased gnathiid isopod ectoparasite infection rate on juvenile but not adult fish

Widespread coral mortality is leading to coral reef degradation worldwide. Many juvenile reef fishes settle on live coral, and their predator-avoidance behaviour is disrupted in seawater exposed to dead corals, ultimately increasing predation risk. Gnathiid isopods are micropredatory fish ectoparasites that occur in higher abundances in dead coral. However, the effect of seawater associated with dead coral on the susceptibility of fish to micropredators has never been investigated. We tested whether the infection rate of cultured gnathiid ectoparasites on individual damselfish, Pomacentrus amboinensis Bleeker 1868, from two different ontogenetic stages (juveniles and adults) was influenced by seawater exposed to three different treatments: dead coral, live coral, or no coral. Seawater treatments were presumed to contain different chemical properties and are meant to represent environmental changes associated with habitat degradation on coral reefs. Gnathiid infection of juvenile fish in seawater exposed to dead coral was twice as high as that of fish in live coral or no coral. Infection rates did not significantly differ between live coral and no coral treatments. In contrast to juveniles, the susceptibility of adults to gnathiids was not affected by seawater treatment. During experiments, juvenile fish mortality was relatively low, but was higher for infected fish (9.7%), compared to fish held without exposure to gnathiids (1.7%). No mortality occurred in adult fish that became infected with gnathiids. Our results suggest that chemical cues released from dead corals and/or dead coral colonisers affect the ability of juvenile, but not adult fish to avoid parasite infection. Considering increased habitat degradation on coral reefs and that gnathiids are more abundant in dead coral substrate, it is possible that wild juvenile fish may experience increased susceptibility to parasitic infection and reduced survival rate. This highlights the importance of including parasitism in ecological studies of global environmental change

Cleaner fish are potential super-spreaders

Cleaning symbiosis is critical for maintaining healthy biological communities in tropical marine ecosystems. However, potential negative impacts of mutualism, such as the transmission of pathogens and parasites during cleaning interactions, have rarely been evaluated. Here, we investigated whether the dedicated bluestreak cleaner wrasse, Labroides dimidiatus, is susceptible to and can transmit generalist ectoparasites between client fish. In laboratory experiments, L. dimidiatus were exposed to infective stages of three generalist ectoparasite species with contrasting life histories. Labroides dimidiatus were susceptible to infection by the gnathiid isopod Gnathia aureamaculosa, but were significantly less susceptible to the ciliate protozoan Cryptocaryon irritans and the monogenean flatworm Neobenedenia girellae, compared with control host species (Coris batuensis or Lates calcarifer). The potential for parasite transmission from a client fish to the cleaner fish was simulated using experimentally transplanted mobile adult (i.e. egg-producing) monogenean flatworms on L. dimidiatus. Parasites remained attached to cleaners for an average of 2 days, during which parasite egg production continued, but was reduced compared with that on control fish. Over this timespan, a wild cleaner may engage in several thousand cleaning interactions, providing numerous opportunities for mobile parasites to exploit cleaners as vectors. Our study provides the first experimental evidence that L. dimidiatus exhibits resistance to infective stages of some parasites yet has the potential to temporarily transport adult parasites. We propose that some parasites that evade being eaten by cleaner fish could exploit cleaning interactions as a mechanism for transmission and spread