Patterns of pair formation in protandrous anemonefishes,Amphiprion clarkii,A. frenatus andA. perideraion,on coral reefs of Okinawa,Japan

Synopsis At Sesoko Island, stocks of anemonefishes were observed for 2 years in a 350 m × 150 m area where host sea anemones were sparse. About 40% of the pairs separated, mostly due to typhoon attacks or displacement. Widowed mates remained and acquired new mates on the same sea anemone, except for one case. New mates were immigrant adults inAmphiprion clarkii and A.frenatus, but resident juveniles inA. perideraion. A. clarkii andA. frenatus moved between sea anemones and sometimes displaced smaller consexuals, butA. perideraion rarely moved. The difference in mobility among the 3 species was related to the mean difference in standard length between the largest juveniles in breeding groups and the minimum size of breeding males in each species, and that between breeding males and the minimum size of breeding females. InA. perideraion both of these differences were small, so pairs could be formed quickly by residents after mate loss. On the contrary, inA. clarkii andA. frenatus, either or both differences were large and it would take a longer time to form a pair after mate loss. Differences in mobility affected the patterns of pair formation, and then the size composition of members in breeding groups.     

Social and mating systems of the protandrous anemonefish Amphiprion perideraion under the influence of a larger congener

The effect of a larger anemonefish Amphiprion clarkii (Bennett) on the social and mating system of a smaller congener Amphiprion perideraion (Bleeker) was investigated on a coral reef at Okinawa, Japan, where both species use the same host sea anemone Heteractis crispa (Ehrenberg). The population of A. perideraion consisted of adult, subadult and juvenile groups. Adult groups, which consisted of one or two adults and a varying number of subadults and juveniles, usually did not share the host with A. clarkii. In contrast, subadult and juvenile groups, which included no adults, always cohabited with A. clarkii. In the heterospecific groups, subadult A. perideraion were able to mature histologically, and changed to female when they were the largest among conspecific members, although their reproduction was suppressed by A. clarkii. After all members of A. clarkii emigrated or disappeared from a heterospecific group, adult A. perideraion could begin breeding. I suggest that A. perideraion in both heterospecific and conspecific groups adopt a mating strategy that involves waiting for vacated breeding posts because of their low mobility and a low host density.     

Materials on fauna of anemonefishes (Perciformes, Pomacentridae, Amphiprioninae) and host sea anemones (Cnidaria, Actiniaria) from Con Son Islands (South China Sea, Southern Vietnam)

The species composition of anemonefishes (Amphiprioninae) and host sea anemones (Actiniaria: Actiniidae, Stichodactylidae) from the Con Son Islands is given for the first time. The investigations carried out in archipelago waters revealed four species of the anemonefishes associated with four species of the host sea anemones: Amphiprion freanatus in the symbiosis with sea anemone Entacmaea quadricolor (Actiniidae), A. perideraion with sea anemone Heteractis magnifica (Stichodactylidae), A. sandaracinos with sea anemone Stichodactyla mertensii (Stichodactylidae), and A. polymnus with sea anemone S. haddoni. The possibility of larval carrying in one more species of anemonefishes, i.e., A. clarkii, into the water area of the Con Son Islands from the nearby regions of the South China Sea is discussed. The view on the probable revealing of this species in the investigated region in the future is expressed.     

Mating behavior and sex change of the anemonefish,Amphiprion clarkii,in the temperate waters of southern Japan

Synopsis In the main habitat of the anemonefishes Amphiprion, their movements between host sea anemones are generally restricted because of the low population density of hosts and high predation pressures. On the contrary, movements of A. clarkii between hosts were usual in the present study area (temperate waters of southern Japan), where host anemones are abundant. The general social unit of the anemonefishes is an isolated group consisting of a monogamous breeding pair and a varying number of nonbreeders. In the present study area, however, monogamous pairs established territories almost contiguous to others and nonbreeders had home ranges on the outskirts of the pairs' territories. The high host population density allows A. clarkii to move between hosts for searching for mates and acquiring additional mates. Most pair bonds lasted for more than 6 months, but 13% of the pairs separated because of migration of a mate to another territory. Bigamy occasionally originated from a penetration into a territory of a breeder by a mated neighbor of the opposite sex after the former's mate loss. Among 18 males who had lost their mates, only 3 changed sex and others re-paired with immigrant females, migrated to unmated females' territories or invaded pairs' territories. In the present study area, sex change to female is not the best way for an unmated male to increase his future reproductive success because of a loss of time spent on sex change and an opportunity to re-pair with new mates larger than himself, but is adaptively maintained as the best of a bad situation for the unmated male.     

Fauna of anemonefishes (Pomacentridae,Amphiprioninae) and their host sea anemones (Cnidaria,Actiniaria) on reefs of Phu Quy,Con Son,and An Thoi Islands (South China Sea,South Vietnam,and Gulf of Thailand) and a review of these groups from the coastal waters of Vietnam

A full species composition of anemonefishes (Pomacentridae, Amphiprioninae) and their host sea anemones (Cnidaria, Actiniaria) from reefs of Phu Quy and Con Son Islands (off South Vietnam) and An Thoi Islands (northeastern Gulf of Thailand) is presented for the first time. A comparison of the faunas of anemonefishes and their host sea anemones is conducted in the coastal waters of Vietnam and adjacent waters. The presence of intermittent ranges of the anemonefishes in the coastal waters of Vietnam is demonstrated. For example, the ranges of two species, Amphiprion clarkii and A. frenatus, include the coastal waters of Vietnam, excluding the Gulf of Thailand, where they are not found even at the eastern border of the gulf. A. perideraion is absent in the Gulf of Tonkin, but it is distributed to the south along the entire coastal zone of Vietnam, including the Gulf of Thailand. In the coastal waters of Vietnam, A. sandaracinos is distributed only between the Gulf of Tonkin and Gulf of Thailand. A. polymnus is reliably indicated in the coastal waters of Vietnam between 12°50′ and 9°54′ N, but, most likely, its range is continuous along the entire Vietnamese coast. The richness of species composition of host sea anemones decreases (from nine to three species) in the southern direction, from Central Vietnam to the eastern border of the Gulf of Thailand.     

Do the Anemonefish Amphiprion ocellaris (Pisces: Pomacentridae) Imprint Themselves to Their Host Sea Anemone Heteractis magnifica (Anthozoa: Actinidae)?

Juvenile anemonefishes detect their host sea anemone by olfactory stimuli; in order to investigate whether this behaviour is innate or acquired, the anemonefish species Amphiprion ocellaris was bred in two different ways: 1. With no host sea anemone present at all (–A); and 2. With the specific host sea anemone Heteractis magnifica present in the hatching aquarium, so that these eggs were laid and hatched close to the sea anemone, as in nature (+A). The two different types of juvenile A. ocellaris were presented to the odours of the host sea anemone H. magnifica in two sets of short-term experiments with the host (a) visually hidden in a net cage, and (b) visible but physically separated from the anemonefishes. In both cases, a water flow was established between fishes and host. The +A-fishes found their host by olfactory and not by visual stimuli. In both series, the –A-fishes showed a significantly lower affinity behaviour towards the odour compounds from the host sea anemone than the +A-fishes did. A third type of experiment was a direct confrontation between fishes and host; here, the –A-fishes were indifferent towards the host sea anemone for almost 48 h, while the +A-fishes acclimated to the host sea anemone within the first 5 min of the direct confrontation. The results of this study suggest that Amphiprion ocellaris imprints itself olfactorily to its species-specific host sea anemone Heteractis magnifica, and, furthermore, may be genetically disposed towards olfactory recognition of the host sea anemone.     

Acquisition of Breeding Space by Nonbreeders in the Anemonefish Amphiprion clarkii in Temperate Waters of Southern Japan

Behavior of Amphiprion clarkii, especially of nonbreeders, was investigated at the shore of boulders and rocks in Uwa Sea, southern Japan. All individuals except small ones under one year were tagged. Movements of A. clarkii between host sea anemones were usual in this study area where host anemones were abundant, unlike in the general habitat (coral reefs) of Amphiprion, where movements between hosts are restricted. Monogamous pairs established almost contiguous territories containing all hosts except small ones. Nonbreeders had home ranges on the fringes of the pairs' territories and sheltered in relatively small hosts. Breeding spaces were saturated with breeders and were available for nonbreeders only after disappearance of one or both members of an established breeding pair. Home ranges of nonbreeders of similar body size were spaced out, due perhaps to competition for breeding spaces. It is suggested that large nonbreeders refrained from becoming females to keep their gonads ambosexual, so that they could replace either sex in a territory as breeding space became available, or, in pairing with other nonbreeders, the larger fish of the pair could take the female role.     

Marine protected area restricts demographic connectivity: Dissimilarity in a marine environment can function as a biological barrier

The establishment of marine protected areas (MPAs) can often lead to environmental differences between MPAs and fishing zones. To determine the effects on marine dispersal of environmental dissimilarity between an MPA and fishing zone, we examined the abundance and recruitment patterns of two anemonefishes (Amphiprion frenatus and A. perideraion) that inhabit sea anemones in different management zones (i.e., an MPA and two fishing zones) by performing a field survey and a genetic parentage analysis. We found lower levels of abundance per anemone in the MPA compared to the fishing zones for both species (n = 1,525 anemones, p = .032). The parentage analysis also showed that lower numbers of fishes were recruited from the fishing zones and outside of the study area into each anemone in the MPA than into each anemone in the fishing zones (n = 1,525 anemones, p < .017). However, the number of self‐recruit production per female did not differ between the MPA and fishing zones (n = 384 females, p = .516). Because the ocean currents around the study site were unlikely to cause a lower settlement intensity of larvae in the MPA, the ocean circulation was not considered crucial to the observed abundance and recruitment patterns. Instead, stronger top‐down control and/or a lower density of host anemones in the MPA were potential factors for such patterns. Our results highlight the importance of dissimilarity in a marine environment as a factor that affects connectivity.     

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.     

Larval settlement of the nemertean egg predator Carcinonemertes errans on the Dungeness crab,Metacarcinus magister

Due to their habitat specificity, marine parasites present excellent systems for studying the processes and patterns of larval settlement. Settlement of Carcinonermertes errans, an egg predator of the Dungeness crab, is described here for the first time. Upon contact with a host individual, competent larvae of C. errans settled on the crab's exoskeleton and migrated under the abdominal flap within 24 h. When removed from the host, recently settled worms retained their larval characteristics. After 48 h on the host, however, metamorphosis proceeded and larvae became juvenile worms. Additional field studies showed that competent larvae were present in the waters of the Coos Bay Estuary during the months of August through early November, could infect crab hosts directly from the water column, and exhibited density‐dependent gregarious settlement.     

Host Imprinting in Anemonefishes (Pisces: Pomacentridae): Does it Dictate Spawning site Preferences?

The olfactory cues, to which some species of anemonefish embryos imprint, are secreted in the mucus on the tentacles and the oral disc of the host anemone. Close contact of the eggs of anemonefishes with the host's tentacles seems therefore important to imprinting. A corollary of this observation is that if local environmental conditions sweep tentacles in one specific direction, then the eggs will be placed leeward of the tentacles, rather than to foremost way from the tentacles. Other known factors such as egg predation can also cause a spawning site preference. No study has examined the possibility of the existence of such a preference. In this study, we addressed two questions: (1) Does spawning site preference exist in anemonefishes? (2) If yes, is it possible to relate this to the imprinting hypothesis, i.e. does local ocean currents over the host anemone have any influence on this preference? Two different coral reef areas were surveyed for anemonefish groups with eggs present: Eilat and Na'ama in the Aquaba-bight, the Red Sea (RS), and areas at Lizard Island, the northern Great Barrier Reef (GBR). We found the anemonefishes Amphiprion akindynos (GBR), A. bicinctus (RS), A. melanopus (GBR), and A. perideraion (GBR), to have a distinctive spawning site preference. We discuss the relevance of these findings to anemonefish host imprinting.     

Mitochondrial DNA Genomes Organization and Phylogenetic Relationships Analysis of Eight Anemonefishes (Pomacentridae: Amphiprioninae)

Anemonefishes (Pomacentridae Amphiprioninae) are a group of 30 valid coral reef fish species with their phylogenetic relationships still under debate. The eight available mitogenomes of anemonefishes were used to reconstruct the molecular phylogenetic tree; six were obtained from this study (Amphiprion clarkii, A. frenatus, A. percula, A. perideraion, A. polymnus and Premnas biaculeatus) and two from GenBank (A. bicinctus and A. ocellaris). The seven Amphiprion species represent all four subgenera and P. biaculeatus is the only species from Premnas. The eight mitogenomes of anemonefishes encoded 13 protein-coding genes, two rRNA genes, 22 tRNA genes and two main non-coding regions, with the gene arrangement and translation direction basically identical to other typical vertebrate mitogenomes. Among the 13 protein-coding genes, A. ocellaris (AP006017) and A. percula (KJ174497) had the same length in ND5 with 1,866 bp, which were three nucleotides less than the other six anemonefishes. Both structures of ND5, however, could translate to amino acid successfully. Only four mitogenomes had the tandem repeats in D-loop; the tandem repeats were located in downstream after Conserved Sequence Block rather than the upstream and repeated in a simply way. The phylogenetic utility was tested with Bayesian and Maximum Likelihood methods using all 13 protein-coding genes. The results strongly supported that the subfamily Amphiprioninae was monophyletic and P. biaculeatus should be assigned to the genus Amphiprion. Premnas biaculeatus with the percula complex were revealed to be the ancient anemonefish species. The tree forms of ND1, COIII, ND4, Cytb, Cytb+12S rRNA, Cytb+COI and Cytb+COI+12S rRNA were similar to that 13 protein-coding genes, therefore, we suggested that the suitable single mitochondrial gene for phylogenetic analysis of anemonefishes maybe Cytb. Additional mitogenomes of anemonefishes with a combination of nuclear markers will be useful to substantiate these conclusions in future studies.     

Parasitism ofAcyrthosiphon pisum byAllothrombium pulvinum (Acariformes: Trombidiidae): Host attachment site,host size selection,superparasitism and effect on host

Several aspects of parasitism of the pea aphid,Acyrthosiphon pisum (Harris), by the mite parasiteAllothrombium pulvinum Ewing, were examined in the laboratory. Larvae ofA. pulvinum were fastmoving mites that find their host by contact of their foretarsi with the host. They can attach to all parts of the host body, but insert their chelicerae only into weakly sclerotized parts such as intersegmental membranes. Of the attached larval mites, most (63.5–74.1%) were on the thorax of their hosts, regardless of host size. In hosts of small and medium size, the ventral side receives most parasitism, whereas in large hosts the lateral sites are most often attacked. Larval mites prefer large hosts when allowed to select between pairs of large and small hosts, but show no significant preference when allowed to choose between pairs of large and medium hosts or pairs of medium and small hosts. In two-choice tests, larval mites prefer previously parasitized hosts to umparasitized hosts, which results in superparasitism of the hosts. When the mite load is fiveA. pulvinum kills all small hosts within three days, and all medium hosts and 50% of large hosts within four days, the reproduction of surviving adult aphids were significantly reduced. Host-finding behavior, attachment site preference, host size selection, superparasitism, and effect on hosts are briefly reviewed for larval parasites of Trombidiidae. The potential role of larvalAllothrombium in integrated and biological aphid control is also discussed.     

Life-history pathways in relation to gonadal sex differentiation in the anemonefish,Amphiprion clarkii,in temperate waters of Japan

Synopsis The process of gonadal sex differentiation in Amphiprion clarkii was investigated for 2 years at Murote Beach, Shikoku Island, Japan. Six color phases were discriminated on the basis of the caudal fin coloration, which corresponded well to six gonadal phases. From changes of the color phases with growth, three life history pathways were detected: (1) subadult male subadult female adult female, (2) subadult male adult male adult female, (3) subadult male adult male. Different pathways were due to the difference of timing among individuals in the development of ovarian tissues of the hermaphroditic gonads involving the atrophy of testicular tissues. Irreversible differentiation of ovarian tissues of the gonads occurred more frequently among nonbreeders (10 cases) than among breeders (4 cases). The second pathway, which has been thought the norm of tropical anemonefishes, was therefore not primary in this population. This can be attributed to ecological conditions: fish are able to move between host sea anemones and nonbreeders can escape from social suppression by adult pairs because of high population density of hosts.     

Mate acquisition by a solitary crabZebrida adamsii,a symbiont of the sea urchin

A small crabZebrida adamsii, an obligate symbiont of the sea urchin, lives solitary on a host from the earliest stage of its benthic life. In the breeding season males frequently move between hosts to search for mates. Analysis of daily positional changes of individually marked crabs indicates that males often land on the substrate to migrate between separate hosts. Females also change hosts before they copulate, but after oviposition they stay on the same hosts for a long time, similarly to crabs in the nonbreeding season.     

Mancae of the parasitic cymothoid isopod, <Emphasis Type="Italic">Anilocra apogonae</Emphasis>: early life history,host-specificity,and effect on growth and survival of preferred young cardinal fishes

Juvenile parasitic cymothoid isopods (mancae) can injure or kill fishes, yet few studies have investigated their biology. While the definitive host of the adult cymothoids is usually a single host from a particular fish species, mancae may use so-called optional intermediate hosts before settling on the definitive host. Little, however, is known about these early interactions. The cymothoid isopod, Anilocra apogonae, infests the definitive host, Cheilodipterus quinquelineatus. This study examined their host preference among potential optional intermediate hosts. Their effect on the growth and mortality of the young of three apogonid fishes, including the definitive host, was investigated. The number of mancae produced per brood was positively correlated with female length. When given a choice of intermediate hosts, significantly more mancae attached to Apogon trimaculatus (Apogonidae) than to Apogon nigrofasciatus. When presented with Ap. trimaculatus and Pomacentrus amboinensis (Pomacentridae), mancae only attached to Ap. trimaculatus suggesting that mancae may show a taxonomic affiliation with preferred hosts. Mancae fed on all three apogonid species, with C. quinquelineatus being fed on earlier than Ap. trimaculatus and Ap. nigrofasciatus. Mancae feeding frequency, adjusted for fish survival, was lowest on C. quinquelineatus and highest on Ap. trimaculatus. Infested apogonids had reduced growth and increased mortality compared with uninfested fish. A. apogonae mancae can use several species of young apogonid fishes as optional intermediate hosts. Via reduced growth and increased mortality, mancae have the potential to negatively influence definitive host populations and also other young species of apogonid fishes.     

Asymmetric priority effects influence the success of invasive forest insects

1. Settlement timing is often an important factor in interspecific herbivore interactions, as early‐arriving species may encounter higher resource availability and/or avoid induced defences. Despite the general importance of priority effects to the outcome of herbivore interactions, there has been little exploration of such interactions on woody host plants where their impact can only be measured over multiple years. 2. In the eastern U.S.A., two invasive species, the hemlock woolly adelgid Adelges tsugae and the elongate hemlock scale Fiorinia externa, share a native host, eastern hemlock Tsuga canadensis. Their interaction and its consequences were investigated for plant growth – hemlock saplings that had been inoculated with either A. tsugae or F. externa, starting in spring 2007, were cross‐infested with the other insect in spring 2009. A set of uninfested trees was simultaneously infested with A. tsugae, F. externa, both, or neither insect (= control), and insect density and plant growth was assessed in all treatments. 3. Adelges tsugae settlement rates did not differ if it settled alone or simultaneously with F. externa, but were ～45% lower on trees previously infested with F. externa. There was no difference in F. externa settlement rates, and plant growth did not differ substantively between any of the herbivore treatments. 4. At a temporal scale (i.e. multiple growing seasons) appropriate to interactions between woody plants and their herbivores, this work demonstrates that plant‐mediated priority effects can substantially affect herbivore settlement and thus the outcome of interspecific competition.     

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.     

Temporal patterns of breeding and larval settlement in a temperate population of the tropical anemonefish,Amphiprion clarkii

The breeding of the anemonefish,Amphiprion clarkii, and the settlement of larvae were observed in temperate Japan. Spawning had two peaks near the first and the third quarter of the moon in 1983, but did not in 1984. The clutch size varied greatly during the breeding season, with a peak from the second half of June to the second half of July. Adult fishes inhibited larval settlement. The proportion of disappeared 0-year olds to the total was higher in 1984 than in 1983. This difference might be mainly due to the difference in the degree of crowding in each sea anemone. The period of larval settlement closely paralleled the breeding season. The larvae settled abundantly around the first quarter and the third quarter of the moon in 1983, and did from the third quarter to the first quarter in 1984. In both years, the number of settled larvae was more from the full moon to the new moon than the new moon to the full moon. The daily pattern of larval settlement did not reflect that of breeding.     

High mobility of the protandrous anemonefish Amphiprion frenatus: nonrandom pair formation in limited shelter space

Protandry in anemonefishes has been attributed to random pair formation, which results from their limited mobility after random recruitment to isolated host anemones. The recruitment and movement of the anemonefish Amphiprion frenatus were investigated in relation to its group structure and the spatial distribution of its host anemone on a coral reef, where it inhabits isolated single hosts and interhost movement is rare. A juvenile tended to be recruited to a host from which a former resident(s) had disappeared, indicating that larval recruitment is not random. After mass bleaching of corals during which many hosts died, a quarter of adults moved between hosts on average 42m in 3 weeks, indicating that their mobility is potentially high. The few migrations under normal conditions were probably due to the low benefit of movements. Even after the movements, a female was much larger than her mate in a host, and a large female tended to pair with a large male. Although body size of females was positively correlated with their host size, that of males was not. It is suggested that the size of a single host does not allow the coexistence of two or more large fish, and the size composition of each pair is affected by the host size. Protandry in the monogamous fish may be attributed to the nonrandom pair formation in the limited space of a host.