Host Anemone Species Research Articles

Sea anemone-anemonefish symbiosis: Behavior and mucous protein profiling.

Fish species of the genus Amphiprion (Perciformes: Pomacentridae) seek protection from predators among the tentacles of sea anemones as their natural habitat, where they live essentially unharmed from stinging by the host's nematocysts. The skin mucus of these anemonefish has been suggested as a protective mechanism that prevents the discharge of the nematocysts upon contact. Whereas some anemonefish species seem to produce their own protective mucous coating, others may acquire mucus (or biomolecules within) from the sea anemone during an acclimation period. In controlled experiments, we show that Amphiprion ocellaris acclimated successfully to their natural host anemone species Stichodactyla gigantea, and also to Stichodactyla haddoni, and in some cases Heteractis crispa, neither of which are natural host species. No symbiosis was observed for three other anemone species tested, Entacmaea quadricolor, Macrodactyla doreensis, and Heteractis malu. We explored the skin mucous protein profile from naive and experienced A. ocellaris during their acclimation to natural and unnatural host anemones. We confidently report the presence of metabolic and structural proteins in the skin mucus of all samples, likely involved in immunological defense, molecular transport, stress response, and signal transduction. For those anemonefish that established symbiosis, there was a clear increase in ribosomal-type proteins. We additionally provide evidence for the presence of anemone proteins only in the skin mucus of individuals that established symbiosis. Our results support previous speculation of the role of skin mucous-associated proteins in anemonefish-anemone symbiosis. Further exploration of these mucosal proteins could reveal the mechanism of anemonefish acclimation to host anemones.

Clownfish hosting anemones (Anthozoa, Actiniaria) of the Red Sea: new associations and distributions, historical misidentifications, and morphological variability

BackgroundThe Red Sea contains thousands of kilometers of fringing reef systems inhabited by clownfish and sea anemones, yet there is no consensus regarding the diversity of host anemone species that inhabit this region. We sought to clarify a historical record and recent literature sources that disagree on the diversity of host anemone species in the Red Sea, which contains one endemic anemonefish, Amphiprion bicinctus Rüppell 1830.ResultsWe conducted 73 surveys spanning ~ 1600 km of coastline from the northern Saudi Arabian Red Sea to the Gulf of Aden and encountered seven species of host anemones, six of which hosted A. bicinctus. We revise the list of symbionts for A. bicinctus to include Stichodactyla haddoni (Saville-Kent, 1893) and Stichodactyla mertensii Brandt, 1835 which were both observed in multiple regions. We describe Red Sea phenotypic variability in Heteractis crispa (Hemprich & Ehrenberg in Ehrenberg, 1834) and Heteractis aurora (Quoy & Gaimard, 1833), which may indicate that these species hybridize in this region. We did not encounter Stichodactyla gigantea (Forsskål, 1775), although the Red Sea is the type locality for this species. Further, a thorough review of peer-reviewed literature, occurrence records, and misidentified basis of record reports dating back to the early twentieth century indicate that it is unlikely that S. gigantea occurs in the Red Sea.ConclusionsIn sum, we present a new guide for the host anemones of the Red Sea, revise the host specificity of A. bicinctus, and question whether S. gigantea occurs in the central and western Indian Ocean.

Comparative phylogeography of three host sea anemones in the Indo‐Pacific

AbstractAimThe mutualistic relationship between anemones and anemonefishes is one of the most iconic examples of symbiosis. However, while anemonefishes have been extensively studied in terms of genetic connectivity, such information is lacking entirely for host sea anemones. Here, we provide the first information on the broad‐scale population structure and phylogeographical patterns of three species of host sea anemone, Heteractis magnifica, Stichodactyla mertensii and Entacmaea quadricolor. We evaluate if there is concordance in genetic structure across several distinct biogeographical areas within the Indo‐Pacific region and to what extent the observed patterns may concur with those found for anemonefishes.LocationIndo‐Pacific, including the Red Sea.TaxonHeteractis magnifica, S. mertensii and E. quadricolorMethodsMicrosatellite markers and a combination of statistical methods including Bayesian clustering, isolation by distance (IBD), analysis of molecular variance (AMOVA) and principal components analysis (PCA) were used to determine population structure. The congruence among distance matrices (CADM) method was used to assess similarity in spatial genetic patterns among species.ResultsSignificant population structure was identified in the three host anemone species. Each species is likely composed of at least two genetic clusters corresponding to two biogeographical regions, the Red Sea and the rest of the Indo‐Pacific. Two of the three anemone species seem to be experiencing admixture where the two main clusters overlap (the Maldives). IBD analyses in the Red Sea revealed differences in gene flow among species, suggesting more limited dispersal potential for E. quadricolor than for S. mertensii and H. magnifica. Clonality is documented in S. mertensii for the first time.Main conclusionsThis research documents the genetic population structure for three ecologically important host sea anemones across the Indo‐Pacific and provides valuable insights regarding their biogeography and evolution. Specifically, we found high levels of genetic divergence between populations across different biogeographical regions, suggesting different evolutionary lineages within species. At the same time, common geographical overlap of population structures suggests similar evolutionary histories among all three species. Interestingly, the observed patterns are congruent to some extent with structure reported for several anemonefish species, reflecting their close ecological association.

Phylogenetic relationships among the clownfish-hosting sea anemones

The clownfish-sea anemone symbiosis has been a model system for understanding fundamental evolutionary and ecological processes. However, our evolutionary understanding of this symbiosis comes entirely from studies of clownfishes. A holistic understanding of a model mutualism requires systematic, biogeographic, and phylogenetic insight into both partners. Here, we conduct the largest phylogenetic analysis of sea anemones (Order Actiniaria) to date, with a focus on expanding the biogeographic and taxonomic sampling of the 10 nominal clownfish-hosting species. Using a combination of mtDNA and nuDNA loci we test (1) the monophyly of each clownfish-hosting family and genus, (2) the current anemone taxonomy that suggests symbioses with clownfishes evolved multiple times within Actiniaria, and (3) whether, like the clownfishes, there is evidence that host anemones have a Coral Triangle biogeographic origin. Our phylogenetic reconstruction demonstrates widespread poly- and para-phyly at the family and genus level, particularly within the family Stichodactylidae and genus Stichodactyla, and suggests that symbioses with clownfishes evolved minimally three times within sea anemones. We further recover evidence for a Tethyan biogeographic origin for some clades. Our data provide the first evidence that clownfish and some sea anemone hosts have different biogeographic origins, and that there may be cryptic species of host anemones. Finally, our findings reflect the need for a major taxonomic revision of the clownfish-hosting sea anemones.

Is ancestral hybridization fuelling adaptive radiation in clownfishes?

Event Abstract Back to Event Is ancestral hybridization fuelling adaptive radiation in clownfishes? Sarah Schmid1*, Baptiste Micheli1, Anna Marcionetti1, Joris Bertrand2 and Nicolas Salamin1 1 Université de Lausanne, Switzerland 2 Université de Perpignan Via Domitia, France The contribution of hybridization in the generation of global species diversity has long been a subject of controversy among evolutionary biologists. However it is now increasingly accepted that hybridization has many impacts on the process of speciation. Especially, it is an important mechanism fostering adaptive radiation, because it can generate new phenotypic combinations enabling the occupancy of new niches. Here, we focused on clownfish (Pomacentridae), a clade of 28 coral reef fishes displaying a mutualistic interaction with sea anemones. This behavior is the key innovation that triggered adaptive radiation of clownfishes, as each species is able to occupy a different combination of host anemone species and habitat. Previous work suggested that hybridization might be responsible for the extant diversity of clownfish species. To test this hypothesis, we analyzed whole-genome datasets for each clownfish species. First, we reconstructed the phylogeny of the clade based on topology weighting method, which enables the visualization of the relationships between taxa across the genome. Then, we highlighted possible ancient hybridization events based on comparative genomic framework for detecting introgression in genomes. We highlighted a large amount of significant hybridization between the different clades, which suggests that hybridization occurred between the ancestors of the current species. Moreover, patterns of high heterogeneity in the phylogenetic relationships across the genome might be a consequence of the combined effect of extensive hybridization and polygenic barrier loci. Taken together, these results support the hypothesis of ancestral hybridization occurring during the evolutionary history of clownfishes. Keywords: hybridization, speciation, adaptive radiation, Clownfish, Genomics Conference: XVI European Congress of Ichthyology, Lausanne, Switzerland, 2 Sep - 6 Sep, 2019. Presentation Type: Oral Topic: EVOLUTIONARY GENOMICS OF FISHES Citation: Schmid S, Micheli B, Marcionetti A, Bertrand J and Salamin N (2019). Is ancestral hybridization fuelling adaptive radiation in clownfishes?. Front. Mar. Sci. Conference Abstract: XVI European Congress of Ichthyology. doi: 10.3389/conf.fmars.2019.07.00043 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 29 May 2019; Published Online: 14 Aug 2019. * Correspondence: Mx. Sarah Schmid, Université de Lausanne, Lausanne, Switzerland, sarah.schmid@unil.ch Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Sarah Schmid Baptiste Micheli Anna Marcionetti Joris Bertrand Nicolas Salamin Google Sarah Schmid Baptiste Micheli Anna Marcionetti Joris Bertrand Nicolas Salamin Google Scholar Sarah Schmid Baptiste Micheli Anna Marcionetti Joris Bertrand Nicolas Salamin PubMed Sarah Schmid Baptiste Micheli Anna Marcionetti Joris Bertrand Nicolas Salamin Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Patterns of coexistence of six anemonefish species around subtropical Okinawa-jima Island, Japan

The species diversity of anemonefish in tropical regions has been explained by the niche differentiation hypothesis or cohabitation hypothesis. However, anemonefish community structure has seldom been investigated in high-latitude areas. To understand the mechanism underlying species diversity of anemonefish in the northern limits of their distribution and to compare with previous results from tropical and other areas, we investigated the community structure of anemonefish around the western coast of Okinawa-jima Island, Japan. Seven species of host anemones and six species of anemonefish were distributed across the 12 study sites. The diversity index of anemonefish and the host anemone varied among sites; anemonefish diversity increased with diversity of host anemones, which was associated with the ratio of sandy areas and distance from shore. The density of each species of anemonefish increased with the density of the primary host anemone, which suggests that niche differentiation may be occurring. However, results of two species of host anemone (Stichodactyla mertensii, Heteractis magnifica) associated each with two species of anemonefish did not support the niche differentiation hypothesis. Forty-seven percent of S. mertensii were shared by Amphiprion clarkii and A. sandaracinos simultaneously, supporting the cohabitation hypothesis. Amphiprion ocellaris and A. perideraion used the same host H. magnifica, but never shared a host simultaneously. Moreover, anemone size and water depth did not differ between the two anemonefish species, suggesting the possibility of the lottery model. In subtropical Okinawa, 86.7% of species interactions supported the niche differentiation hypothesis, 6.7% supported the cohabitation hypothesis, and 6.7% supported the lottery hypothesis. The mechanisms of coexistence of anemonefish in subtropical regions include not only niche differentiation and cohabitation but also the lottery hypothesis, which has not been reported in tropical regions.

Range extensions in anemonefishes and host sea anemones in eastern Australia: potential constraints to tropicalisation

Species distributions at range edges show complex shifts with climate change. The present study examined anemonefish and host sea anemone abundance at their southern distribution limits on the eastern coast of Australia, to identify factors influencing the geographic responses of the symbiosis. Roaming surveys (30min) were conducted at 21 sites (~30.01–30.95°S) on rocky reefs in a tropical–temperate transition zone. Two species of host anemones (Entacmaea quadricolor and Heteractis crispa) and anemonefishes (Amphiprion akindynos and A. latezonatus) were found, along with Dascyllus trimaculatus. Nearly all anemones and anemonefishes (>99.5%) were associated with vegetated islands and rocky islets, and abundance was influenced by seawater temperature. Greater numbers of H. crispa and A. akindynos than E. quadricolor and A. latezonatus were found; however, most A. akindynos were juveniles. H. crispa provided nursery habitat for both fishes, whereas adult fishes utilised only E. quadricolor. A southern range extension was found for E. quadricolor, and overwintering of A. latezonatus had extended poleward since the mid-1990s. The paucity of islands and rocky islets south of our surveys, and host-usage patterns, could constrain future range extensions. These findings showed climate-driven latitudinal shifts are complex and are likely to be variably constrained for different species.

Frequency and distribution of melanistic morphs in coexisting population of nine clownfish species in Papua New Guinea

Coral reef fishes exhibit extreme diversity in colouration, with many species being recognised as having colour polymorphism. While melanin-based colouration is known to occur in clownfishes (Pomacentridae), little is known about the frequency at which melanistic morphs occur in natural populations. The aim of this study was to assess the frequency of melanistic morphs in a coexisting population of nine clownfishes and to identify ecological covariates associated with morph distribution. In the Kavieng lagoonal system of Papua New Guinea (2°36ʹS, 150°46ʹE), melanistic morphs were found in Amphiprion chrysopterus (56 % of individuals), A. clarkii (29 %), A. percula (20 %), and A. polymnus (25 %) populations. A. leucokranos, A. melanopus, A. perideraion, A. sandaracinos, and Premnas biaculeatus populations were also surveyed, but were found to be without melanistic morphs. Unbiased recursive partitioning analyses identified a suite of interacting and conditional ecological factors encompassing social rank, host anemone species, and location effects as the primary factors predicting the distribution of melanistic morphs. Melanistic morphs were generally associated with host anemones from the genus Stichodactyla and with fish having a high social rank. The lack of a distinct melanistic morph locational ‘hot spot’ common to all species, despite locational coexistence, suggests that causative factors of location effects were different among species. Our results highlight the complexity of clownfish polymorphism associated with melanism, with multiple non-exclusive potential explanations identified for future investigation.

Genetic tools link long-term demographic and life-history traits of anemonefish to their anemone hosts

The life-history traits and population dynamics of species are increasingly being attributed to the characteristics of their preferred habitats. While coral reef fish are often strongly associated with particular habitats, long-term studies establishing the demographic and life-history consequences of occupying different reef substrata are rare and no studies have monitored individuals in situ over their lifetime and determined the fate of their offspring. Here, we documented a quasi-turnover and local reproductive success for an entire population of orange clownfish (Amphiprion percula) from Kimbe Island, Papua New Guinea, by taking bi-annual samples of DNA over a 10-yr period (2003–2013). We compared demographic and life-history traits of individuals living on two host anemone species, Heteractis magnifica and Stichodactyla gigantea, including female size, adult continued presence (a proxy for relative longevity range), early post-settlement growth, the number of eggs per clutch and ‘local’ reproductive success (defined for each adult as the number of offspring returning to the natal population). Our results indicate that while the relative longevity of adults was similar on both host anemone species, females living in H. magnifica were larger than females in S. gigantea. However, despite females growing larger and producing more eggs on H. magnifica, we found that local reproductive success was significantly higher for clownfish living in S. gigantea. Life-history traits also exhibited local spatial variation, with higher local reproductive success recorded for adults living on S. gigantea on the eastern side of the island. Our findings support a ‘silver-spoon’ hypothesis that predicts individuals that are fortunate enough to recruit into good habitat and location will be rewarded with higher long-term reproductive success and will make a disproportionate contribution to population renewal.

Cohabitation promotes high diversity of clownfishes in the Coral Triangle.

Global marine biodiversity peaks within the Coral Triangle, and understanding how such high diversity is maintained is a central question in marine ecology. We investigated broad-scale patterns in the diversity of clownfishes and their host sea anemones by conducting 981 belt-transects at 20 locations throughout the Indo-Pacific. Of the 1508 clownfishes encountered, 377 fish occurred in interspecific cohabiting groups and cohabitation was almost entirely restricted to the Coral Triangle. Neither the diversity nor density of host anemone or clownfish species alone influenced rates of interspecific cohabitation. Rather cohabitation occurred in areas where the number of clownfish species exceeds the number of host anemone species. In the Coral Triangle, cohabiting individuals were observed to finely partition their host anemone, with the subordinate species inhabiting the periphery. Furthermore, aggression did not increase in interspecific cohabiting groups, instead dominant species were accepting of subordinate species. Various combinations of clownfish species were observed cohabiting (independent of body size, phylogenetic relatedness, evolutionary age, dentition, level of specialization) in a range of anemone species, thereby ensuring that each clownfish species had dominant reproductive individuals in some cohabiting groups. Clownfishes are obligate commensals, thus cohabitation is an important process in maintaining biodiversity in high diversity systems because it supports the persistence of many species when host availability is limiting. Cohabitation is a likely explanation for high species richness in other obligate commensals within the Coral Triangle, and highlights the importance of protecting these habitats in order to conserve unique marine biodiversity.

Searching for a toxic key to unlock the mystery of anemonefish and anemone symbiosis.

Twenty-six species of anemonefish of the genera Amphiprion and monospecific Premnas, use only 10 species of anemones as hosts in the wild (Families: Actiniidae, Stichodactylidae and Thalassianthidae). Of these 10 anemone species some are used by multiple species of anemonefish while others have only a single anemonefish symbiont. Past studies have explored the different patterns of usage between anemonefish species and anemone species; however the evolution of this relationship remains unknown and has been little studied over the past decade. Here we reopen the case, comparing the toxicity of crude venoms obtained from anemones that host anemonefish as a way to investigate why some anemone species are used as a host more than others. Specifically, for each anemone species we investigated acute toxicity using Artemia francisca (LC50), haemolytic toxicity using ovine erythrocytes (EC50) and neurotoxicity using shore crabs (Ozius truncatus). We found that haemolytic and neurotoxic activity varied among host anemone species. Generally anemone species that displayed greater haemolytic activity also displayed high neurotoxic activity and tend to be more toxic on average as indicated by acute lethality analysis. An overall venom toxicity ranking for each anemone species was compared with the number of anemonefish species that are known to associate with each anemone species in the wild. Interestingly, anemones with intermediate toxicity had the highest number of anemonefish associates, whereas anemones with either very low or very high toxicity had the fewest anemonefish associates. These data demonstrate that variation in toxicity among host anemone species may be important in the establishment and maintenance of anemonefish anemone symbiosis.

North-eastern range extension of the anemone Stichodactyla haddoni to the Marshall Islands represents a new record of host use by the endemic anemonefish Amphiprion tricinctus

Amphiprion tricinctus is an anemonefish endemic to the Marshall Islands that was previously reported to inhabit four species of sea anemone. Underwater visual surveys in 2009 and 2010 located five individuals of the anemone Stichodactyla haddoni in the shallow lagoon of Majuro Atoll. This is the first record of S. haddoni in the Marshall Islands and a significant north-eastern range extension by 2200 km from its nearest record in Chuuk State, Federated States of Micronesia. Stichodactyla haddoni was inhabited by juvenile and adult A. tricinctus. This report is the first to describe a symbiotic relationship between A tricinctus and S. haddoni. The number of host anemone species inhabited by A. tricinctus now extends to five.

Ecological Studies on Two Amphiprion Species in Maldivian Coral Reefs

Amphiprion clarkii and A. nigripes were found in coral reefs of three different atolls in the Maldives. A. clarkii was associated with five species of host anemones, but A. nigripes was only found in Heteractis magnifica. In few cases, both anemonefishes have utilized the same individual of H. magnifica. There was no significant correlation between the size of the anemones and the number of the inside living Amphiprion.

Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis crispa, that host anemonefish

Summary As the sea anemones, Entacmaea quadricolor and Heteractis crispa, provide essential habitat for obligate symbiotic anemonefish, knowledge of their reproductive biology is crucial to their effective management and conservation. This paper provides the first detailed information on the spawning times, behaviour and mode of gamete release for these host anemone species. Anemones were collected from subtropical reefs in the Solitary Islands Marine Park, eastern Australia, and monitored in outdoor flow-through seawater tanks from 2003 to 2005. Sexually reproductive anemones were either male or female, releasing their gametes into the water column for external fertilisation and development. Spawning of both sexes was predominately synchronous and was restricted to a few nights each year during the austral summer and autumn. Males generally began to release gametes prior to females, suggesting that sperm or some associated product may trigger the females to spawn. Sperm were commonly released in milky white streams or clouds, whereas eggs were released singly or in large masses. Reproductive seasonality and synchrony of gamete release suggests that spawning in both species is coordinated by similar responses of individuals to a range of environmental factors such as seawater temperature, photoperiod and lunar cycles. Incorporating knowledge of the sexual reproductive biology of host sea anemones into management and conservation programs could help ensure the viability of their populations and their resident anemonefish.

Abundance of giant sea anemones and patterns of association with anemonefishin the northern red sea

patterns of distribution and abundance of giant sea anemones and anemonefish were compared among coral reefs along the coastline of sinai in the northern red sea. the sea anemones varied widely in abundance between reef areas containing different habitat types. they were rare on steep reef slopes with abundant coral cover (=low-density anemone sites, 0.09–0.68 anemones per 1000 m2 of reef area), but were common at a site containing patch reefs interspersed with sand (=high-density anemone site, 6.00–8.11 anemones per 1000 m2). distributions of the endemic two-band anemonefish (amphiprion bicinctus) varied significantly between the two main host anemone species. at the high-density site, individuals of the sea anemone heteractis crispa either did not contain anemonefish, or were occupied by single juvenile fish as shown in previous studies. at low-density sites h. crispa usually hosted clusters of juvenile anemonefish. in contrast, individuals of the sea anemone entacmaea quadricolor hosted either single adult fish (high-density site) or pairs of breeding adults (low-density sites), frequently in addition to some juvenile fish. mechanisms that prevent anemonefish from reaching adult size and forming breeding pairs in h. crispa may include high fish mortality above a size threshold because this host cannot adequately protect them from predation when they become large, active emigration of fish to e. quadricolor as described in previous reports, and/or environmentally-controlled cessation of fish growth. we conclude that in the northern red sea, individuals of h. crispa potentially serve as nurseries for anemonefish.

Acclimation or Innate Protection of Anemonefishes from Sea Anemones?

Studies have shown that anemonefishes can acquire protection from the stinging tentacles of their host anemones through a behavioral process called acclimation. However, some investigators have suggested that anemonefishes are innately protected from all species of host anemones. To definitively test whether anemonefishes are innately protected from anemones, we forced naive anemonefishes, bred and raised in complete isolation from anemones, to contact the tentacles of Macrodactyla doreensis, Heteractis crispa, and Stichodactyla haddoni. Individuals of Amphiprion clarkii were protected when forced to contact the tentacles of all three anemone species. However, individuals of A. ocellaris and A. perideraion were stung by some anemones. All fishes went through acclimation behavior after the initial forced contact with anemones. Thus, anemonefishes are innately protected from some anemone species but must acclimate to live with others.

Host selection, location, and association behaviors of anemonefishes in field settlement experiments

Nine anemonefish species were reared in the laboratory, and individuals were released in the field (Lizard Island, Australia and Madang, Papua New Guinea) at different distances and orientations away from natural (anemone species the fishes are found with in nature) and unnatural species of host anemones. Experiments were conducted to examine factors that could affect the settlement behaviors of the fishes: current velocity, distance and orientation of the fishes to the anemones, chemical vs visual cues, and presence of conspecific or heterospecific fishes. The fishes were usually attracted toward natural host species of anemones but not towards unnatural host anemone species nor to pieces of dead coral. Host selection during settlement provided the best explanation for the host specificity patterns displayed by anemonefishes in nature. The fishes used chemical cues released from the anemones to identify and locate the appropriate host species and could effectively locate the anemones from a maximum distance of 8 m downstream. Fishes released upstream or to the side of anemones (where anemone chemicals were assumed to be reduced or absent) were much less successful in locating anemones. The ability of the fishes to locate natural host anemones was strongly reduced when there was no water current. The presence of resident anemonefishes on host species of anemones did not influence the attraction behavior of anemonefishes released downstream from the anemones. Once the released fishes got close to or entered the anemones, the resident fishes would generally bite and chase them until the recruits left the anemones. Most fishes were not stung upon initial contact with the anemones.