Spacing pattern and body size composition of the protandrous anemonefish Amphiprion frenatus inhabiting colonial host anemones

The protandrous anemonefish Amphiprion frenatus often forms a group consisting of a large female, a small male, and a smaller nonbreeder at an isolated single host anemone, where home ranges of subordinates were covered with the female's home range. Within the group, the dominant individuals suppress the growth of subordinates, resulting in large size differences. The spacing pattern and body size composition of A. frenatus on colonial hosts were investigated in Ishigaki Island, Okinawa, Japan. Six breeding pairs and 14 nonbreeders inhabited a colony of 157 anemones. Each pair maintained a territory in which pair members used different hosts. Nonbreeders had unstable home ranges on the outskirts of or in the pairs' territories. Body size differences between males and females in pairs and between males and nonbreeders were small. The small size differences in the colony of hosts are caused by reduced suppression of growth of subordinates by the dominant individuals. The total area of host anemones largely affects spacing pattern and social suppression of the anemonefish.     

Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish

The ecological performance of the sea anemone Heteractis magnifica was examined during a 36-month experiment with respect to season and the presence and numbers of a mutualist (orange-fin anemonefish Amphiprion chrysopterus). Anemones primarily grew during the autumn, with most asexual reproduction occurring in winter; mortality was not strongly seasonal. Individual growth rates did not differ between anemones harboring one or two anemonefish, but these rates were three times faster than for anemones lacking Amphiprion. Anemones with two anemonefish had the highest fission rate, whereas those without anemonefish had the lowest. By contrast, anemones that were not defended by anemonefish suffered higher-than-expected mortality. As a consequence, anemones with two Amphiprion had the greatest net increase in surface area, and those lacking anemonefish had a negligible gain that was statistically indistinguishable from zero after three years. Anemonefish not only enhanced anemone survivorship as previously believed, they also fostered faster growth and more frequent asexual reproduction.     

Ammonia flux,physiological parameters,and <Emphasis Type="Italic">Symbiodinium</Emphasis> diversity in the anemonefish symbiosis on Red Sea coral reefs

Despite the ecological importance of anemonefish symbioses, little is known about how nutritional contributions from anemonefish interact with sea anemone physiology and Symbiodinium (endosymbiotic dinoflagellate) genetic identity under field conditions. On Red Sea coral reefs, we measured variation in ammonia concentrations near anemones, excretion rates of anemonefish, physiological parameters of anemones and Symbiodinium, and genetic identity of Symbiodinium within anemones. Ammonia concentrations among anemone tentacles were up to 49% above background levels, and anemonefish excreted ammonia significantly more rapidly after diurnal feeding than they did after nocturnal rest, similar to their excretion patterns under laboratory conditions. Levels of 4 physiological parameters (anemone protein content, and Symbiodinium abundance, chlorophyll a concentration, and division rate) were similar to those known for laboratory-cultured anemones, and in the field did not depend on the number of anemonefish per anemone or depth below sea surface. Symbiodinium abundance varied significantly with irradiance in the shaded reef microhabitats occupied by anemones. Most anemones at all depths harbored a novel Symbiodinium 18S rDNA variant within internal transcribed spacer region 2 (ITS2) type C1, while the rest hosted known ITS2 type C1. Association with Symbiodinium Clade C is consistent with the symbiotic pattern of these anemones on other Indo-Pacific reefs, but the C1 variant of Symbiodinium identified here has not been described previously. We conclude that in the field, anemonefish excrete ammonia at rapid rates that correlate with elevated concentrations among host anemone tentacles. Limited natural variation in anemonefish abundance may contribute to consistently high levels of physiological parameters in both anemones and Symbiodinium, in contrast to laboratory manipulations where removal of fish causes anemones to shrink and Symbiodinium to become less abundant.     

Anemonefish depletion reduces survival,growth, reproduction and fishery productivity of mutualistic anemone–anemonefish colonies

Intimate knowledge of both partners in a mutualism is necessary to understand the ecology and evolution of each partner, and to manage human impacts that asymmetrically affect one of the partners. Although anemonefishes and their host anemones are iconic mutualists and widely sought by ornamental fisheries, the degree to which anemones depend on anemonefishes, and thus the colony-level effects of collecting anemonefishes, is not well understood. We tracked the size and abundance of anemone Entacmaea quadricolor and anemonefish Amphiprion melanopus colonies for 3 yr after none, some, or all of the resident anemonefish were experimentally removed. Total and partial removal of anemonefish had rapid and sustained negative effects on growth, reproduction and survival of anemones, as well as cascading effects on recruitment and productivity of anemonefish in the remaining colony. As predicted, total removal of anemonefish caused acute declines in size and abundance of anemones, although most anemone colonies (76 %) slowly resumed growth and reproduction after the arrival of anemonefish recruits, which subsequently grew and defended the hosts. Partial removal of anemonefish had similar but typically less severe effects on anemones. Remarkably, the colony-level effects on anemones and anemonefish were proportional to the size and number of anemonefish that were experimentally removed. In particular, anemone survival and anemonefish productivity were highest when one or more adult anemonefish remained in the colony, suggesting that adult fish not only enhanced the protection of anemones, but also increased the recruitment and/or survival of conspecifics. We conclude that the relationship between E. quadricolor and A. melanopus is not only obligate, but also demographically rigid and easily perturbed by anemonefish fisheries. Clearly, these two species must be managed together as a unit and with utmost precaution. To this end, we propose several tangible management actions that will help to minimize fishing effects.     

Effects of anemonefish on giant sea anemones: expansion behavior,growth, and survival

The symbiosis between giant sea anemones and anemonefish on coral reefs is well known, but little information exists on impacts of this interaction on the sea anemone host. On a coral reef at Eilat, northern Red Sea, individuals of the sea anemone Entacmaea quadricolor that possessed endemic anemonefish Amphiprion bicinctus expanded their tentacles significantly more frequently than did those lacking anemonefish. When anemonefish were experimentally removed, sea anemone hosts contracted partially. Within 1–4 h in most cases, individuals of the butterflyfish Chaetodon fasciatus arrived and attacked the sea anemones, causing them to contract completely into reef holes. Upon the experimental return of anemonefish, the anemone hosts re-expanded. The long-term growth rate and survival of the sea anemones depended on the size and number of their anemonefish. Over several years, sea anemones possessing small or no fish exhibited negative growth (shrinkage) and eventually disappeared, while those with at least one large fish survived and grew. We conclude that host sea anemones sense the presence of symbiotic anemonefish via chemical and/or mechanical cues, and react by altering their expansion behavior. Host sea anemones that lack anemonefish large enough to defend them against predation may remain contracted in reef holes, unable to feed or expose their tentacles for photosynthesis, resulting in their shrinkage and eventual death.     

Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines

Tropical marine ornamentals comprise an increasingly important fishery worldwide. Although the potential for overexploitation of marine ornamentals is great, few studies have addressed the population-level impacts of ornamental exploitation and few ornamental fisheries are managed. Analysis of catch records obtained from collectors over a four-month period in the vicinity of Cebu, Philippines, showed that anemonefish and anemones comprised close to 60% of the total catch. Underwater visual census surveys revealed that both anemone and anemonefish densities were significantly lower in exploited areas than in protected areas. The low density of anemones on exploited reefs accounted for over 80% of the reduced density of anemonefish at those sites. There were similar numbers of anemonefish per unit area of anemone in protected and exploited sites; however, biomass of anemonefish per unit area of anemone was lower in exploited areas. Reduction of anemone removals is recommended to support the sustainable harvest of anemonefish from this region.     

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.     

Vertical and horizontal distribution patterns of the giant sea anemone Heteractis crispa with symbiotic anemonefish on a fringing coral reef

The distribution patterns of the leathery sea anemone, Heteractis crispa, which contains an algal endosymbiont (zooxanthellae) and anemonefish, were investigated in relation to size distribution on a shallow fringing reef (3.2 ha, 0–4 m depth) in Okinawa, Japan. Individual growth and movements were also examined. Large individuals (>1,000 cm²) inhabited reef edges up to a depth of 4 m, while small anemone (<500 cm²) inhabited shallow reefs including inner reef flats. Individuals rarely moved, and their sizes were significantly correlated with their water depths. Growth of small anemones was negatively correlated with their distance from the reef edge, suggesting that reef edges provide more prey and lower levels of physiological stress. This study suggested that deep reef edges are suitable habitats for H. crispa. Large anemones were inhabited by large Amphiprion perideraion or large Amphiprion clarkii, both of which are effective defenders against anemone predators. Anemones that settle in deep reef edges may enjoy a higher survival rate and attain a large size because of their symbiotic relationship with anemonefish. However, early settlers do not harbor anemonefish. Their mortality rate would be higher in the deep edges than in shallow edges, the complicated topography of which provides refuge.     

Detrimental effects of host anemone bleaching on anemonefish populations

Coral bleaching and related reef degradation have caused significant declines in the abundance of reef-associated fishes. Most attention on the effects of bleaching has focused on corals, but bleaching is also prevalent in other cnidarians, including sea anemones. The consequences of anemone bleaching are unknown, and the demographic effects of bleaching on associated fish recruitment, survival, and reproduction are poorly understood. We examined the effect of habitat degradation including host anemone bleaching on fish abundance, egg production, and recruitment of the panda anemonefish (Amphiprion polymnus) near Port Moresby, Papua New Guinea. Following a high-temperature anomaly in shallow waters of the region, most shallow anemones to a depth of 6 m (approximately 35% of all the anemones in this area) were severely bleached. Anemone mortality was low but bleached anemones underwent a ~34% reduction in body size. Total numbers of A. polymnus were not affected by bleaching and reduction in shelter area. While egg production of females living in bleached anemones was reduced by ~38% in 2009 compared to 2008, egg production of females on unbleached anemones did not differ significantly between years. Total recruitment in 2009 was much lower than in 2008. However, we found no evidence of recruiting larvae avoiding bleached anemones at settlement suggesting that other factors or different chemical cues were more important in determining recruitment than habitat quality. These results provide the first field evidence of detrimental effects of climate-induced bleaching and habitat degradation on reproduction and recruitment of anemonefish.     

Mobility of Stichodactyla Gigantea Sea Anemones and Implications for Resident False Clown Anemonefish, Amphiprion Ocellaris

For reef fishes that do not move between habitat patches following settlement, habitat selection is expected during settlement. Although false clown anemonefish, Amphiprion ocellaris, are sedentary following settlement, they are not especially discriminating during settlement, and are commonly found occupying anemones at which no apparent nest site exists. In this study I report on mobility of Stichodactyla gigantea sea anemones, including anemones with resident false clowns. I argue that anemone mobility can help explain why settling false clowns are not more discriminating: although the per annum probability of an anemone moving is low, the probability of that anemone moving over the course of a resident's life is considerably higher. Therefore, an anemone's current microhabitat may not be a good predictor of its microhabitat and suitability as a host in the future.     

Assemblage and interaction structure of the anemonefish-anemone mutualism across the Manado region of Sulawesi,Indonesia

The Manado area (Indonesia–North Sulawesi), a marine high diversity hot-spot, hosts 7 species of anemonefish (family Pomacentridae, subfamily Amphiprioniae) living in symbiosis with 9 species of sea anemones (family Stichodactylidae and Actiniidae). This high biological diversity −27% and 80%, respectively, of the total known diversity of anemonefish and sea anemones—allows us to test different hypotheses focused on the obligate mutualism between anemonefish and sea anemones. In the Manado area, species richness of anemones and anemonefish across several sites was not correlated, but all anemones contained at least one fish individual, and there was a strong positive correlation between the numbers of individual anemonefish and anemones. As expected, each fish species had a preferred anemone host; also a partial niche overlap (Pianka’s Index) was often detected. The analysis of unique species composition suggests that competition is not an important factor determining the presence or absence of particular combinations of either anemonefish or host anemones (no evidence of competitive exclusion). The NODF algorithm showed that, at both a regional and local scale, the interaction between anemonefish and host anemones is not significantly nested, as a result of a combination of local conditions with competition, forcing species that regionally are more generalist to become more specialist.     

Benefits to host sea anemones from ammonia contributions of resident anemonefish

Large ectosymbionts (especially fishes and crustaceans) may have major impacts on the physiology of host cnidarians (sea anemones and corals), but these effects have not been well quantified. Here we describe impacts on giant sea anemone hosts (Entacmaea quadricolor) and their endosymbiotic zooxanthellae (Symbiodinium spp.) from the excretion products of anemonefish guests (Amphiprion bicinctus) under laboratory conditions. Starved host anemones were maintained with anemonefish, ammonia supplements (= NH₃ gas and NH₄⁺ ion), or neither for 2 mo. In the presence of external ammonia supplements or resident anemonefish, the zooxanthellae within host anemones increased in abundance (173% and 139% respectively), and provided the hosts with energy that minimized host body size loss. In contrast, anemones cultured with neither ammonia nor anemonefish harbored significantly lower abundances of zooxanthellae (84% of initial abundance) and decreased > 60% in body size. Although they maintained higher zooxanthella abundances, anemones cultured with either ammonia supplements or resident anemonefish exhibited significantly lower ammonia uptake rates (0.065 ± 0.005 µmol g^- 1 h^- 1, and 0.052 ± 0.018 µmol g^- 1 h^- 1 respectively) than did control anemones (0.119 ± 0.009 µmol g^- 1 h^- 1), indicating that their zooxanthellae were more nitrogen sufficient. We conclude that, in this multi-level mutualism, ammonia supplements provide essentially the same level of physiological contribution to host anemones and zooxanthellae as do live resident fish. This nutrient supplement reduces the dependence of the zooxanthellae on host feeding, and allows them to provide abundant photosynthetically-produced energy to the host.     

Cophylogenetic analysis of the relationship between anemonefish Amphiprion (Perciformes: Pomacentridae) and their symbiotic host anemones (Anthozoa: Actiniaria)

ABSTRACT

The association between anemonefish and anemone is a classical example of mutualism in coral reefs. Although mutualism is probably the key innovation that triggered the adaptive radiation of anemonefish into a wide range of habitats, the coevolutionary history between the groups has not been thoroughly tested in a phylogenetic framework. We examined the evolutionary history of the association via distance-based (Parafit and PACo) and event-based methods (Core-PA, Jane). Mitochondrial DNA sequences (COI mtDNA, Cytb, 16S rDNA and 12S rDNA) were used to reconstruct the phylogenies of tropical Amphiprion species and their host anemones by using maximum likelihood with best-fit models selected. Neither distance-based analyses nor event-based analyses revealed global significant congruence between the phylogenies of the hosts and the symbionts, and thus no evidence for coevolution between anemone-anemonefish. However, at the individual pair level, the fish showed some dependence on anemone hosts. Even though living in close association and benefiting from each other, the change of genetic composition of one species (anemonefish) does not always evolve in response to changes in the other (anemones). These findings expand our understanding of the pattern and the role of evolutionary events to allow a better prediction of the future of the anemonefish-anemone relationship.     

Mutualism can mediate competition and promote coexistence

Mutualistic interactions are not believed to promote coexistence of competitors because mutualisms produce positive feedbacks on abundances whereas coexistence requires negative feedbacks. Here we show that a mutualism between an anemonefish (Amphiprion) and its sea anemone host mediates the effect of asymmetrical competition for space between the anemonefish and another damselfish (Dascyllus) in a manner that fosters their coexistence. Amphiprion stimulates increases in host area, the shared resource, but social interactions cap the number of anemonefish to two adults per host. Space generated by the mutualism becomes differentially available to Dascyllus because the effectiveness of an anemonefish in excluding its competitor declines with increases in the area it defends. This alters Amphiprion's ratio of per capita intra‐ to interspecific effects and thus facilitates coexistence of the fishes. This mechanism may be prevalent in nature, adding another major pathway by which mutualism can enhance diversity.     

Why do anemonefishes inhabit only some host actinians?

Synopsis The 25 species ofAmphiprion and one ofPremnas (family Pomacentridae) are obligate symbionts of 10 species of facultatively symbiotic sea anemones. Throughout the tropical Indo-West Pacific range of the relationship, a fish species inhabits only certain of the hosts potentially available to it. This specificity is due to the fishes. Five fishes occupy six sea anemone species at Lizard Island, Great Barrier Reef, Australia.Entacmaea quadricolor harborsP. biaculeatus, A. melanopus andA. akindynos. Adults ofPremnas occur deeper than about 3 m in large, primarily solitary actinians; juveniles may occupy peripheral members ofEntacmaea clones in shallow water. Specimens ofA. melanopus live exclusively in clonal anemones, which are found no deeper than 3 m. Most individuals ofA. akindynos inEntacmaea are juveniles, occurring shallow and deep, in solitary anemones or at the margins of clones. Interspecific as well as intraspecific social control of growth may be responsible for keeping fish small at clone fringes. Conspicuous specimens ofE. quadricolor depend upon their anemonefish to survive. Actinians cleared of symbionts disappeared within 24 h, probably having been eaten by reef fishes.Entacmaea, the most abundant and widespread host actinian at Lizard Island and throughout the range of the association, is also arguably the most attractive to anemonefishes. I believe its vulnerability to predation was a factor in its evolving whatever makes it desirable to fishes. Experimental transfers pitted fish of one species against those of another, controlling for ecophenotype of host, and sex, size and number of fish. Competitive superiority was in the same order as abundance and over-all host specificity:P. biaculeatus, A. melanopus, A. akindynos. At least three factors are necessary to explain patterns of species specificity - innate or learned host preference, competition, and stochastic processes.     

Factors affecting the local abundance of two anemonefishes (Amphiprion frenatus and A. perideraion) around a semi-closed bay in Puerto Galera,the Philippines

Many marine organisms disperse or migrate among habitats, which affects their abundance patterns at individual local habitats. To clarify the factors affecting the distribution patterns of two anemonefishes (Amphiprion frenatus and A. perideraion), we measured the habitat patch size (anemone size), patch isolation (mean distance from other anemones), presence/absence of other anemonefish species, depth, and abundance of the two anemonefishes at each anemone around a semi-closed bay (up to 3.7 km) in Puerto Galera, the Philippines. We assumed that local abundance increases with habitat size and decreases with patch isolation because of greater resource availability and reduced rates of recruitment from other patches. Local abundance of A. frenatus was related to habitat size and the presence of other anemonefish species, whereas that of A. perideraion was affected by the presence of other anemonefish species and water depth. Interspecific competition and/or niche differentiation of habitat can explain the negative relationship between the local abundance of the target species and other anemonefish. Patch isolation was not significant for both species probably because the dispersal rate was not directly proportional to the geographic distance between patches at our study site.     

Aerial exposure and body temperature of the intertidal sea anemone Anthopleura elegantissima

The sea anemone Anthopleura elegantissima is a common member of intertidal communities along the west coast of North America, and can experience extended periods of increased temperature during summertime low tides. Internal body temperatures of emersed individuals of A. elegantissima were monitored in a laboratory wind tunnel and in the field, and factors influencing the anemones’ thermal experience were examined. Larger body size and aggregation with conspecifics slowed body temperature increases in controlled wind tunnel conditions. In the field, anemones in the interior of an aggregation stayed cooler than those on the edges, and microhabitat features related to light exposure and surface orientation overshadowed any direct effects of body size. In the warmest month only (July), aggregations of A. elegantissima were significantly larger at the upper limit of their distribution than they were at the mid and lower limits, suggesting aggregation in high intertidal zones may be a behavioral response to desiccation and temperature stress. As this sea anemone can host multiple species of symbiotic algae with different thermal tolerances, the ability to slow body heating may affect the type of algae hosted and thus the potential contribution of this abundant anemone to primary production in the intertidal zone.     

Forcible eviction and prevention of recruitment in the clown anemonefish

How big an animal group will be depends on how the group's sizeis regulated and on the costs and benefits of living in thegroup. To determine which individuals regulate group size ofthe clown anemonefish, Amphiprion percula, I investigated thestrategies involved in the formation, maintenance, and dissolutionof its groups. Groups composed of a single breeding pair andof zero to four nonbreeding subordinates occupied individualsea anemones (Heteractis magnifica), which provided the fishwith oviposition sites and protection from predators. Groupsize increased linearly with anemone size. I used the residualsof this relationship as a measure of the degree of saturationof each anemone. Residents evicted low-rank subordinates andprevented the recruitment of additional subordinates at anemoneswith a high degree of saturation, but not at anemones with alow degree of saturation. These strategies indicate that residentscontrol group membership of their subordinates, and suggestthat residents might incur costs from the presence of subordinatesin more saturated anemones. In general, whenever residents cancontrol group membership, the prevention of recruitment andthe eviction of subordinates will set an upper limit on groupsize.     

Predation risk assessment by larval reef fishes during settlement-site selection

Predation rates of marine species are often highest during the transition from the pelagic to the benthic life stage. Consequently, the ability to assess predation risk when selecting a settlement site can be critical to survival. In this study, pairwise choice trials were used to determine whether larvae of three species of anemonefish (Amphiprion melanopus, A. percula and Premnas biaculeatus) are able to (1) assess the predation risk of potential anemone settlement sites through olfactory cues alone and (2) alter their settlement choices depending on the options available (host or non-host anemone). When predation risk was assessed with host and non-host anemone species independently, all species of anemonefish significantly chose the odor associated with the low-risk settlement option over the high-risk site. Most importantly, all species of anemonefish selected water with olfactory cues from their host anemone regardless of predation risk when paired against non-host anemone odor. These results demonstrate that larval reef fishes can use olfactory cues for complex risk assessment during settlement-site selection; however, locating the correct habitat is the most important factor when selecting a settlement site.     

The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish

Entacmaea quadricolor is a geographically widespread species of sea anemone that forms a three-way symbiosis with anemonefish and Symbiodinium. This species dominates the reef substrata at North Solitary Island, Australia, which is located in a region identified as a climate change hot spot. Their geographic location places these anemones under significant threat from rising ocean temperatures, although their upper thermal limit and risk of bleaching are unknown. To address this knowledge gap, anemones were exposed to one of four temperatures (23, 25, 27, or 29°C) and one of two irradiance treatments (high or low light) over 6 days. At moderate temperatures (27°C, 1°C above summer average), anemone bleaching was characterised by symbiont expulsion, while extreme temperatures (29°C) resulted in an additional loss of photosynthetic pigments from within symbionts, and in some cases, host mortality. Irradiance influenced the susceptibility to thermal stress with high light promoting the bleaching response, along with significant reductions in the effective quantum yield of anemone symbionts. The long-term loss of photosystem II photochemical efficiency within in hospite symbionts was observed during exposure to temperatures exceeding the summer average, indicating photosynthetic damage. The resident Symbiodinium, identified as clade C using 28S rRNA gene sequences, therefore represents the partner within the symbiosis that is likely to be most vulnerable to rising seawater temperatures. Results suggest that E. quadricolor is living within approximately 1°C of the upper thermal maximum at the Solitary Islands, and given the predictions for rising seawater temperature on Australia’s east coast, the thermal threshold at which bleaching will occur is expected to be reached and exceeded more frequently in the future.