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.     

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.     

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.     

Coexistence of two anemonefishes,Amphiprion clarkii and A. perideraion,which utilize the same host sea anemone

Synopsis Social structure and interactions between the anemonefishes, Amphiprion clarkii and A. perideraion, which utilize the same host sea anemone Radianthus kuekenthali, were investigated on a coral reef of Okinawa Islands, Japan. In an 87 × 373 m² study area, 98 sea anemones were inhabited by both species (32.5%), by only A. clarkii (48.9%), or by only A. perideraion (18.6%). A group of A. clarkii often occupied two or more individual hosts, and group members often interchanged. However, a group of A. perideraion usually used only one host and migration between groups was rare. The larger A. clarkii suppressed reproduction of A. perideraion in cohabiting groups, while A. perideraion suppressed settlement of Juvenile A. clarkii to its own hosts. Juvenile A. clarkii settled on small hosts as well as on large hosts, whereas juvenile A. perideraion settled only on large hosts. Coexistence appears to be possible in part by differences in settlement patterns between juveniles of the two anemonefishes.     

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.     

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.     

Spacing behaviour and habitat use of rock ptarmigan (Lagopus mutus) at low density in the Italian Alps

Studies of rock ptarmigan Lagopus mutus in northern latitudes have shown that, in the breeding season, the majority of cocks pair monogamously and defend small territories, whilst in most populations, a small proportion of cocks are polygynous or remain unmated. Little is known, however, on spacing behaviour and habitat use of alpine rock ptarmigan populations occurring at low densities at the southern edge of the species’ range. From 1995 to 1997, we trapped, radio-tracked and observed birds in the Central Italian Alps (elevation 2,000–3,000 m) in order to investigate spacing behaviour and habitat use in alpine landscapes where habitats offering rich food and cover are patchy. Both sexes were selective in their habitat use, and cocks did not establish territories on bare ground, artificial or nutrient rich grasslands or bogs. In the breeding season, cocks had larger home ranges than hens (cocks 99 ± 57 ha, hens 50 ± 25 ha) that overlapped with the ranges of neighbouring cocks and hens. Cocks were monogamous and defended relatively large territories (core areas of home ranges: cocks 37 ± 26 ha, hens 24 ± 12 ha), which corresponded with low spring densities (0.47–2.29 cocks km⁻² and 0.35–1.60 pairs km⁻²). Territory size of individual cocks was negatively correlated with the amount of high quality habitat in the core-area. Our results suggest increased home ranges and large breeding territories in low density alpine rock ptarmigan populations, compared to populations occurring at higher densities in the central and northern alps, and on subarctic and arctic grounds at northern latitudes, confirming the predictions of models on food-based territoriality.     

The role of sea anemones as refuges and feeding habitats for the temperate fish Oxylebius pictus

Synopsis This study describes an association between the temperate zone fish Oxylebius pictus and sea anemones in Barkley Sound, Vancouver Island, British Columbia, Canada. Fish were observed swimming and resting unharmed among the tentacles, or next to a column of Urticina lofotensis (98% of all observations) and U. piscivora (2% of all observations). These associations were most commonly observed at moderately exposed sites where there were relatively high densities of O. pictus and anemones. Most associations occurred at night when the fish were inactive. Small young-of-year fish (< 6 cm total length) associated closely with sea anemones, larger individuals spent less time with their hosts, and most adults (> 12 cm total length) sheltered in rock holes and crevices. Experiments demonstrated that small O. pictus were more vulnerable to predators than large individuals. Urticina lofotensis and U. piscivora were large, persistent structures in the study habitats that provided effective refuge for O. pictus from predators. Anemone size, shape, tentacular adhesive force, and presence of copepod associates influenced patterns of host specificity. Oxylebius pictus fed on copepods and other crustaceans that associated with U. lofotensis and host sea anemones served as both refuges and feeding habitats for the fish. The sea anemones did not appear to receive any significant benefit from the relationship and the fish was considered to be a facultative commensal.     

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.     

Life-history variations of the Lesser Sheathbill Chionis minor in contrasting habitats

From 1987 until 1995, life-history traits of the Lesser Sheathbill Chionis minor in the Kerguelen Archipelago were compared with those at other localities, where this species breeds in seabird colonies. At Kerguelen Island only, some pairs breed on shores free of penguin and cormorant colonies. Moreover, pairs, including nonbreeders, and solitary individuals maintain territories all the year round. Site and mate changes were not linked, and all divorces were permanent. Fidelity rates were similar in all localities and so were the annual survival rates of adults. The survival rate of immature individuals was highest at Kerguelen Island, where sheathbills laid smaller clutches, produced fewer fledglings and had lower breeding success than in the other islands. At Kerguelen Island, pairs breeding on shores had similar clutch sizes but fledged fewer offspring than those breeding in seabird colonies. Further, the proportion of vacant territories and nonbreeders was higher on shores. Kerguelen sheathbills devoted less time to food acquisition than those on Marion Island, being exceptionally kleptoparasitic, and spent a smaller part of their foraging time exploiting seabird colonies. Their diet was mainly algae. The differences on Kerguelen Island as compared with other localities were caused by the presence of an extensive intertidal zone on the former, which reduced competition, making many more sites suitable and the environment more predictable. These life-history and behavioural traits are discussed in relation to life-history theory. As differences were also found, although less extensive, within the Kerguelen Archipelago, we suggest that some traits represent an adaptive response to external constraints and that the life-history strategy of the Lesser Sheathbill is particularly opportunistic.     

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.     

Co-existence of subadult males and females as alternative tactics of breeding post acquisition in a monogamous and protandrous anemonefish

Summary The monogamous and protandrous anemonefish,Amphiprion clarkii, utilizes only large host sea anemones as breeding sites. Under conditions of breeding site shortage, an important strategy for unmated fish may be to prepare themselves to enter quickly a breeding site from which a breeding male or female has recently disappeared. There are two types of subadults. Some juveniles become subadult males, which can change either to male or female afterwards, but others become subadult females, which can change only to female. Subadult females seem to acquire female posts more easily than subadult males. We develop an ESS model which evaluates the future reproductive success of subadult females and subadult males and test whether coexistence of subadult males and females can be interpreted as adaptive alternative tactics, using field data from two populations. The model predicts that if mortality does not differ between adult males and females the frequency for juveniles to become subadult females should be equal to the proportion of breeding post acquisition by subadult females among that by all subadults. The model also predicts that if mortality does not differ between subadult males and females, nor in adults, the frequency of subadult females among all subadults should be equal to the proportion of post acquisition. The model, with data from two study sites, suggests that alternative life-history pathways found inA. clarkii have evolved through adaptive tactics of breeding post acquisition.     

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.     

Territorial Behavior and Ecology of the Anemonefish Amphiprion melanopus on Guam1)

Field observations and experiments on the Indo-Pacific anemonefish Amphiprion melanopus at Guam show that it colonizes the aggregating sea anemone Physobrachia douglasi extensively and nearly exclusively. There are an average of four fish per colony. The total standard length of anemonefish at each aggregation is highly correlated with the total area covered by resident anemones, suggesting both a carrying capacity and some form of social control of growth of anemonefish²). Inter-colony migration of juveniles, as well as larval recruitment, may contribute to maintenance of the optimum colony size. Adults do not migrate. Both juveniles and adults defend territory. Juvenile territories are mutually exclusive areas within the confines of the anemone aggregation, while adult territories are considerably larger than the area covered by the anemone aggregation. Though territories of mated ♀♀ and ♂♂ overlap completely, female emphasis is peripheral relative to the ♂. Adult conspecific intruders are attacked more heavily and at greater distances than are juveniles. Intraspecific territoriality in juveniles probably reflects the limited availability of critical habitat. In adults it may function to protect the pair bond. Interspecific aggression is less intense and appears to protect both the spawn and host anemones from various predators.     

Striking difference in response to expanding brood parasites by birds in western and eastern Beringia

Two species of obligate brood‐parasitic Cuculus cuckoos are expanding their ranges in Beringia. Both now breed on the Asian side, close to the Bering Strait, and are found in Alaska during the breeding season. From May to July 2017, we used painted 3D‐printed model eggs of two cuckoo host‐races breeding in northeastern Siberia to test behavioral responses of native songbirds on both sides of the Bering Strait, with particular attention to species that are known cuckoo hosts in their Siberian range. Each host nest was tested after the second egg was laid and, if possible, again 4 days later with a model of a different type. Although our Siberian study site was also outside the known breeding ranges of the cuckoos, we found that Siberian birds had strong anti‐parasite responses, with 14 of 22 models rejected. In contrast, birds in Alaska had virtually no detectable anti‐parasite behaviors, with only one of 96 models rejected; the rejecters were Red‐throated Pipits (Anthus cervinus). Such differences suggest that the cuckoos might successfully parasitize naïve hosts and become established in North America whether or not their historic host species are widely available.     

Scaring Nemo: Contrasting effects of observer presence on two anemonefish species

Behaviours of Clark's anemonefish Amphiprion clarkii and the dusky anemonefish Amphiprion melanopus were studied in Vanuatu. Six anemones and their resident fish were observed for typical behaviours (hiding, watching, roaming, inter-, and intraspecific behaviour) with and without the presence of a snorkelling observer. Observer presence had significant but contrasting effects on hiding behaviour in A. clarkii and A. melanopus. Bolder anemonefish species may be able to outcompete other species in areas with high human presence.     

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.     

Feeding of the exotic Louisiana red swamp crayfish,Procambarus clarkii (Crustacea,Decapoda), in an African tropical lake: Lake Naivasha,Kenya

The Louisiana red swamp crayfish, Procambarus clarkii, has had a major impact on aquatic ecosystems in Europe and America where it has been introduced for human consumption. In Lake Naivasha, where it was introduced in 1970, it is suspected of causing the complete disappearance of native floating-leaved and submerged plants by 1982 and again by 1996; recovery of submerged plants occurred in between, concurrent with a decline in P. clarkii. Examination of the feeding of P. clarkii by microscopic analysis of gut contents collected from the lake confirmed information from both its native and exotic ranges; that it is an omnivore with green plants and insects the predominant items recognised. Feeding experiments confirmed this omnivory, with a preference from herbivory over carnivory. They further showed the importance of native plants as opposed to exotic water hyacinth Eichhornia crassipes. It is concluded that P. clarkii could well have accounted for the observed elimination of native plant species in Lake Naivasha; the cyclical nature of populations of submerged plant species and of P. clarkii in inverse proportion to each other lead us to hypothesise that P. clarkii is a `keystone' species in the lake ecosystem.     

Competitive abilities of oystercatchers ( Haematopus ostralegus ) occupying territories of different quality

In territorial species, habitat heterogeneity results in some individuals occupying poor quality sites while others occupy high quality sites. Floaters (mature nonbreeders) may accept a low quality territory, because it is the best they can get and defend (‘inferior phenotype hypothesis’), or because it is a strategic alternative for a high quality territory in the long run (‘queue hypothesis’). Oystercatcher Haematopus ostralegus territories differ consistently in the amount of offspring produced each year and this is related to the distance between the nesting and feeding territories. The inferior phenotype hypothesis was previously rejected on the basis of the absence of morphometric differences (assumed to indicate competitive abilities) among breeders. We investigated social dominance, in the field and in captivity, in relation to the quality of the breeding territory. In the field, birds with high-quality territories won more often compared to those occupying low-quality territories. However, this difference was not apparent in a small dataset of captive birds. These results are discussed in the framework of the long-term fitness prospects of settling in a high or low quality territory.     

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.