Pelagic spawning of the hawkfish Oxycirrhites typus (Cirrhitidae)

Synopsis Pelagic spawning of the deep slope coral-dwelling cirrhitid Oxycirrhites typus was observed for two social groups at Papua New Guinea. This species was previously reported to be a demersal spawner in an aquarium. Courtship in social groups consisting of a single male and one or two females commenced just prior to or after sunset among the branches of gorgonian or antipatharian corals. Males and females occupied separate corals; males either visited females at their corals or met them at an adjacent coral just prior to courtship. Courtship was sequential and consisted of two or more bouts with each female that culminated in a rapid ascent into the water column and the release of floating eggs. Fertilized eggs, taken from a third social group, were spherical and averaged 0.69 mm in diameter. Spawning pairs sought refuge in their resident corals or in the coral where courtship occurred immediately after spawning was completed.     

Control of different mating systems in a coral reef fish by one environmental factor

The Red Sea coral-dwelling damselfish Dascyllus marginatus is organized in stable terri torial groups with males dominating all females. The fish live in pairs, harems or multi-male groups. Group size, and the number of sexually active males in a group, are correlated with coral size. Males monopolize and control the coral, attracting potential mates. The experimental alteration of coral sizes, using spherical Stylophora corals, resulted in an increase of male numbers, in artificially composed groups, with the increase of coral size. Thus pairs and harems were produced on small corals, multimale groups on big corals. Experiments with unisexual groups revealed a higher survival of females; males are more aggressive to each other, and cause a stronger emigration of subdominants. In D. marginatus, group size and the number of sexually active males are essentially restricted by one environmental factor: the number of available hiding places on a coral.     

Habitat Patch Size,Facultative Monogamy and Sex Change in a Coral-dwelling Fish, <Emphasis Type="Italic">Caracanthus unipinna</Emphasis>

Synopsis We investigated the inter-relationships between coral colony size, social group size, mating system, and patterns of sex allocation in the pygmy coral croucher, Caracanthus unipinna (Caracanthidae), an obligate coral-dwelling fish. Histological examination of the gonads from all individuals in social groups revealed that the predominant mating system was harem polygyny. However, both group size and mating system co-varied with coral colony size, with pair forming and monogamy occurring on small corals and group forming and harem polygyny on large corals. This species therefore displays mating system plasticity in response to varying habitat patch size. Within-group sexual size dimorphism and individual gonad structure indicate that C. unipinna is also likely to be a protogynous hermaphrodite. These social and reproductive features of C. unipinna contrast with some other coral-dwelling fishes, which display a lack of social and mating system plasticity in response to habitat patch size, and either bi-directional or protandrous sex change. Possible reasons for this dichotomy include differences in spawning mode, parental care and levels of intrasexual aggression.     

Does gonad structure reflect sexual pattern in all gobiid fishes?

Synopsis In immature and adult females of protogynous gobies, small distinctive masses of cells associated with the ovarian wall develop into testis-associated glandular structures during sex change. These precursive accessory gonadal structures, or pAGS, have been found in females of known protogynous goby species, but not among gonochoric goby species, suggesting that their presence can be used as a species-specific indicator of protogyny within the family. However, a detailed examination of a developmental series of ovaries in two gonochoric species,Gobiosoma illecebrosum andG. saucrum, revealed the presence of a gonadal feature previously thought to be restricted to protogynous gobies. Among immature females of both species, pAGS-like structures having a similar appearance and placement as functional pAGS of protogynous gobies were found. In femaleG. illecebrosum, the size of these structures among immatures progressively decreased with maturation and were absent in all but the smallest adult females. A similar pattern was evident in a small sample ofG. saucrum. Population demography based on field collections showed thatG. illecebrosum exhibits sex ratios and male and female size-frequency distributions typical of gonochores and laboratory experiments indicated that final sexual identity was unaffected by social environment during the juvenile period. Thus, the presence of pAGS in juvenile femaleG. illecebrosum is not related to an ability to change sex at that ontogenic interval. Whether the transient pAGS observed here are vestiges of an ancestral protogynous condition is unknown. Based on their presence among immatures in two gonochore gobies, however, only the presence of pAGS in adult females should be used to predict protogyny among gobies.     

Toxic coral gobies reduce the feeding rate of a corallivorous butterflyfish on Acropora corals

The obligate coral-dwelling gobiid genus Gobiodon inhabits Acropora corals and has developed various physiological, morphological and ethological adaptations towards this life habit. While the advantages of this coral-fish association are well documented for Gobiodon, possible fitness-increasing factors for the host coral are unknown. This study examines the influence of coral-dwelling gobies on the feeding behaviour of obligate corallivorous butterflyfishes. In an aquarium experiment using video observation, the corallivorous butterflyfish Chaetodon austriacus fed significantly less on corals inhabited by two Gobiodon species compared to unoccupied coral colonies of similar size. The more agonistic species G. histrio, which mostly displayed directed movements towards butterflyfishes, decreased butterflyfish bite rate by 62–98 % compared to uninhabited colonies. For Gobiodon sp. 3, which mostly displayed undirected movements in response to visits by C. austriacus, bite rate reduction was 64–68 %. The scale-less skin of Gobiodon spp. is covered by mucus that is toxic and multi-functional by reducing predation as well as affecting parasite attachment. A choice flume experiment suggests that the highly diluted skin mucus of Gobiodon spp. also functions as a corallivore repellent. This study demonstrates that Gobiodon spp. exhibit resource defence against coral-feeding butterflyfishes and also that coral colonies without resident Gobiodon suffer higher predation rates. Although the genus Gobiodon is probably a facultative corallivore, this study shows that by reducing predation on inhabited colonies by other fishes, these obligate coral-dwellers either compensate for their own fitness-decreasing impact on host colonies or live in a mutualistic association with them.     

Gonad Morphology, Colony Demography and Evidence for Hermaphroditism in Gobiodon Okinawae (Teleostei, Gobiidae)

Gobiodon okinawae is a small-sized, obligate coral-dwelling goby. The majority of species in this Indo-Pacific genus exhibit an obligatory association with branching live corals and a number have been shown to be bi-directional hermaphrodites in which adults have the capacity to shift between male and female function. Gonadal histology in G. okinawae demonstrated that all individuals had either an ovotestis or an ovary. Some females had an ovary with vitellogenic oocytes, indicating adult female function. Hermaphrodites having an ovotestis were either functionally male, as evidenced by the presence of spermatozoa or, in one instance, functionally female so judged by the presence of vitellogenic oocytes. No individuals were found to have mature gametes of both sexes, although a number of hermaphrodites had an inactive ovotestis with no mature gametes of either sex. Based on size ranges for fish having different gonad morphologies, individuals in this species appear to develop first as a female. They then either mature and function solely as a female, or become hermaphroditic. Findings based on experimentally maintained individuals suggests that adult hermaphrodites can shift sexual function in either direction. Accessory gonadal structures (AGS) were found in both sexes. These consisted of two fully differentiated pairs of lobes, each compartmentalized internally by lumina and containing PAS+secretions. The secretions of the dorsally located AGS were colloidal while those of the ventrally located AGS were fibrillar and granular in nature. The presence of two sets of AGS among males appears to be characteristic of both Gobiodon and its putative sister genus, Paragobiodon. However, the occurrence of fully developed AGS in both females and males has not previously been reported and may be unique to G. okinawae.     

Planktonic and symbiotic organisms in nutrition of coralobiont fish

Nutrition of coral reef fish closely associated with the colonies of scleractinian corals Acropora spp. (South China Sea, Gulf of Nha Trang) was investigated. Parabionts Dascyllus reticulatus and Chromis caeruleus (Pomacentridae) feed mainly on zooplankton in the water column above the hosts’ colony, and inbionts Gobiodon quinquestrgatus (Gobiidae) rarely leave a host colony and feed generally on coral reef invertebrates. A high part of secondary nutrition objects (on average 19–29%) that indicates deficiency in main food were noted in both categories of fish. Food of all three fish species contains parasites (from 19% in C. caeruleus and up to 25% in G. quinquestrigatus) whose significant part is represented by parasites of coral (approximately 7% in D. reticulatus and C. caeruleus and 15% in G. quinquestrigatus). In addition, larvae of parasites of Isopoda and Facetotecta that are fed by fish in the water column were found. Mucus from the surface of host coral which was recognized on the basis of a high number of nematocysts in fish stomachs was found in food of G. quinquestrigatus for the first time. Positive and negative effects of symbiosis of fish and host-coral were discussed. A commensal character of symbiosis was supposed.     

Interactions Between Habitat Use and Patterns of Abundance in Coral-dwelling Fishes of the Genus <Emphasis Type="Italic">Gobiodon</Emphasis>

Coral-dwelling fishes from the genus Gobiodon are some of the most habitat specialised fishes on coral reefs. Consequently, we might expect that their population dynamics will be closely associated with the abundance of host corals. I used a combination of log-linear modelling and resource selection ratios to examine patterns of habitat use among eight species of Gobiodon in Kimbe Bay, Papua New Guinea. I then used multiple regression analysis to investigate relationships between the abundance of each species of Gobiodon and the abundance of the corals they inhabited. Each species of Gobiodon used one or more species of coral more frequently than expected by chance. The pattern of habitat use exhibited by each species of Gobiodon did not vary among reef zones or among reefs with different exposures to prevailing winds, despite changes in the relative abundances of corals among reef zones. This consistency in habitat use might be expected if the coral species inhabited confer considerable fitness advantages and, therefore, are strongly preferred. For most species of Gobiodon, abundances among reef zones and exposure regimes were correlated with the abundance of the coral species usually inhabited. Therefore, it appears that habitat availability helps determine abundances of most species of Gobiodon in Kimbe Bay. In addition to correlations with habitat availability, the abundances of G. histrio, G. quinquestrigatus, G. rivulatus (dark form) and the group others were also associated with particular reef zones and exposure regimes. Therefore, in these species, reef type appears to influence patterns of abundance independently of coral availability. In contrast to other species of Gobiodon, the abundance of the most specialised species, Gobiodon sp.A, was not closely associated with the abundance of the only coral species it inhabited. This study demonstrates that even for habitat specialised species, the relationship between habitat availability and abundance varies widely and is multiscale.     

Cleaning activity of two Caribbean cleaning gobies: intra- and interspecific comparisons

Sharknose cleaning gobies Elacatinus evelynae were found predominantly in male—female pairs at cleaning stations located almost exclusively on coral heads. By contrast, broadstripe cleaning gobies Elacatinus prochilos were found at cleaning stations on two distinct substrata: coral and sponge, which were linked to marked differences in social behaviour, cleaning activity and diet. Elacatinus prochilos at coral cleaning stations were more frequently solitary or found in small groups, while groups of up to 40 individuals were observed on sponge cleaning stations. Coral-dwelling E. prochilos spent, on average, 25 times longer cleaning and took 16 times more bites on clients than those on sponge, which was reflected in the larger proportion of client-gleaned material in their gut (40% v . <1%). These substratum-linked differences may result from differences in availability of food items at different cleaning stations. Few differences in cleaning activity were found between E. evelynae and coral-dwelling E. prochilos , although the latter contained a higher proportion of client-gleaned items (40% v . 25%). Most coral-dwelling cleaning gobies had ingested fish scales, although the variation among individuals was high (0–81 fish⁻¹). Intra- and interspecific variability in cleaning activity of cleaner fishes implies that cleaning services for clients may vary significantly between cleaning stations.     

Cleaning behavior is riskier and less profitable than an alternative strategy for a facultative cleaner fish

Cleaning symbioses on coral reefs involve small cleaner fish or shrimps picking ectoparasites from the exterior surfaces of larger client organisms. These mutualisms are thought to evolve in part because the cleaner receives a reliable source of profitable prey items and immunity from predation. However, the benefits of cleaning behavior have never been measured relative to those of alternative, non-cleaning strategies. This study examined these costs and benefits in the sharknose goby, Elacatinus evelynae, a facultative cleaner fish, at the Caribbean island of St. Croix. Sharknose gobies are found on coral heads, where they maintain cleaning stations, and on basket sponges, where they spend little time cleaning and feed predominantly on nonparasitic copepods. For immature gobies that are not allocating energy to reproduction, hindcast otolith growth rates (a reliable proxy for somatic growth) were significantly higher for non-cleaning sponge-dwellers than for coral-dwellers. Furthermore, tagging large, competitively dominant gobies on sponges and corals revealed that mortality rates were higher for coral-dwelling gobies. These unexpected results provide further evidence that cleaning mutualisms are context dependent: far from being a uniformly profitable life history strategy, cleaning may be a suboptimal choice at some times and places.     

Socially controlled sex-change in the half-moon grouper,Epinephelus rivulatus,at Ningaloo Reef,Western Australia

The cues controlling sex-change have been elucidated for various species of hermaphroditic fishes that inhabit coral reefs, but not for the epinepheline serranids. A male removal experiment conducted on an assemblage of the half-moon grouper, Epinephelus rivulatus, demonstrated that protogynous sex-change in this species is socially controlled, possibly by the suppressive dominance of males and a threshold sex ratio. The experiment showed that a reproductively ripe female can change sex and become a male with ripening testis within 3 weeks. However, this process can be delayed, slowed, or stopped by the presence of other males in the area.     

Why selection favors protandrous sex change for the parasitic isopod, Ichthyoxenus fushanensis (Isopoda: Cymothoidae)

A flesh burrowing parasitic isopod, Ichthyoxenus fushanensis, was found infecting the body cavity of a freshwater fish, Varicorhinus bacbatulus, in pairs. The marked sexual size dimorphism, with much larger females than males, and the presence of penes vestige on mature females suggest a protandrous sex change in I. fushanensis. Here we investigate the question of why selection favors protandrous sex change for I. fushanensis, by analyzing the interactions among clutch size, female size, male size, and their host size. The number of manca, the first free-living juvenile stage released, per brood was closely related to the size of the female. Excluding the effects of interaction among causal variables, the negative correlation of male size alone on clutch size suggests that a small male did not limit an individual's mating and fertilization success. When the effect of host size is removed statistically, there exists a significant negative relationship between the sizes of paired males and females. This indicates that the resources available from host fish are limited, and that competition exists between paired male and female resulting in a trade-off of body size. Due to the very low success rate of hunting for a host of mancas, a female with larger body size and higher fecundity has a fitness advantage. To augment the clutch size, a productive combination is a smaller male and a larger female in a host. The constraints of the limited resources and the trade-off between the sizes of paired male and female may favor I. fushanensis to adopt the reproductive strategy of protandrous sex change resulting in a larger female and hence more mancas. The pattern of the interactions among male, female, and the number of mancas, may be considered as a selective force for I. fushanensis protandrous sex change, where the available resources are constrained by the size of the host. This revised version was published online in July 2006 with corrections to the Cover Date.     

Does habitat availability determine geographical-scale abundances of coral-dwelling fishes?

The role of local-scale processes in determining large-scale patterns of abundance is a key issue in ecology. To test whether habitat use determines local and large-scale patterns of abundance of obligate coral-dwelling fishes (genus Gobiodon), the author compared habitat availability with the abundance of four species, G. axillaris, G. brochus, G. histrio, and G. quinquestrigatus, among four locations, from the southern Great Barrier Reef to northern Papua New Guinea. Habitat availability, measured at tens of meters, explained 47-65% of the variation in abundance of these species among geographic locations spanning over 2,000 km. Therefore, local-scale patterns of habitat use appear to determine much larger-scale patterns of abundance in these habitat-specialist fish. The abundances of all species, except G. brochus, were also closely associated with particular exposure regimes, independently of the abundance of corals. Broad-scale habitat selection for reef types within locations can most easily explain this pattern. The abundances of all species, except G. brochus, also varied among geographic locations, independently of coral abundances. Therefore, the abundances of these species are influenced by either geographic variation in local-scale processes that was not measured, or additional processes acting at very large spatial scales.     

Effect of elevated summer temperatures on gonadal steroid production, vitellogenesis and egg quality in female Atlantic salmon

Sex change in the coral-dwelling goby Gobiodon histrio was induced by placing two adult fish of the same sex on a coral colony. The sex change of individual fish was confirmed using histology, and whole-body concentrations of the gonadal steroids testosterone (T), 11-ketotestosterone (11-KT), and 17β-oestradiol (E₂) were examined. The results show that T, 11-KT and E₂ occurred in both female and male G. histrio . E₂ concentration in females was twice that in males, while concentrations of T did not differ between the sexes. Contrary to predictions, concentrations of T and E₂ did not differ between fish that changed sex and those that did not. Most samples had 11-KT concentrations below minimum levels of detection (  i.e. <0·15 ng ml⁻¹) and were therefore not analysed statistically. The results suggest that: (i) specific activation or de-activation of the T–E₂ (aromatase) pathway is a probable candidate for mediating serial adult sex change in G. histrio , and (ii) low levels of 11-KT may be important in allowing serial adult sex change in G. histrio .     

Size-assortative Monogamy and Paternal Egg Care in a Coral Goby Paragobiodon echinocephalus

Paragobiodon echinocephalus (Pisces; Gobiidae) inhabits the branching coral Stylophora pistillata. Only the largest two fish bred in a coral irrespective of group size, which was larger in larger corals. Breeding pairs consisted of a male and female of similar body size. Eggs were spawned on the coral branch and guarded by the male parent for about 4 days until hatching. Successive spawning occurred usually one day after hatching. The reproductive success of a pair, measured as the number of newly hatched larvae, was positively correlated with the body size of the male as well as the female. That is, not only female fecundity but also male ability of egg guarding were limited by body size almost equally. This should promote size-assortative monogamy in the goby.     

Why Be a Both-ways Sex Changer?

Sex change is a rather common phenomenon among aquatic animals, but only a few have been reported to change sex in both directions. In laboratory experiments we demonstrated that the coral goby, Paragobiodon echinocephalus, changed sex in both directions with the same likelihood. When the goby lost its mate in the field, it preferred changing sex in either direction over moving a long distance in search of a heterosexual mate. Change in social rank, which is likely to occur in many other hermaphroditic fish, corresponded exactly with the direction of sex change. This constitutes a new condition for the evolution of both-ways sex change among plants and animals.     

Variation in the structure of epifaunal invertebrate assemblages among coral hosts

The high biodiversity of coral reefs is attributable to the many invertebrate groups which live in symbiotic relationships with other reef organisms, particularly those which associate with the living coral habitat. However, few studies have examined the diversity and community structure of coral-dwelling invertebrates and how they vary among coral species. This study quantified the species richness and composition of animals associated with four common species of branching corals (Acropora nasuta, A. millepora, Pocillopora damicornis, and Seriatopora hystrix) at Lizard Island in the northern Great Barrier Reef. One hundred and seventy-eight nominal species from 12 different phyla were extracted across 50 replicate colonies of each coral host. A single coral colony, approximately 20 cm in diameter, harbored as many as 73 individuals and 24 species. There were substantial differences in invertebrate species composition among coral hosts of different families as well as genera. Twenty-seven species (15% of all taxa collected) were found on only one of the four different coral species, which may potentially indicate some level of specialization among coral hosts. The distinct assemblages on different coral species, and the presence of potential specialists, suggests invertebrate communities will be sensitive to the differential loss of branching coral species resulting from coral reef degradation.     

Sex change in either direction by growth-rate advantage in the monogamous coral goby, Paragobiodon echinocephalus

The size-advantage model predicts the evolution of sex changeif the relative reproductive success of the sexes changes withsize or age. In the goby (Paragobiodon echinocephalus) the largesttwo fish, a male and a female matched by size, breed monogamouslyin each host coral. Because the female fecundity and male abilityof egg care increase with body size in a similar way, no size-fecundityadvantage exists. However, we found both protogyny and infrequentprotandry in a natural population of this species in Okinawa.New pairs were often formed after movement between host coralsand also sex change or sex differentiation of one or both members.In most new pairs males were larger than females, and femalesgrew much faster than their mates until breeding (growth-rateadvantage). The smaller member of a new pair should be the femalethat grows faster, because the smaller limits the reproductivesuccess of the pair. To form such a pair, the goby changed sexaccording to the sex and relative size of a new mate, as a status-dependentconditional strategy. The growth-rate advantage predicts predominanceof protogyny, but movement between host corals provides opportunitiesalso for protandry.     

The influence of colony size and coral health on the occupation of coral-associated gobies (Pisces: Gobiidae)

Fishes of the genus Gobiodon are habitat specialists by their association with Acropora corals. Little is known about the parameters that define host coral quality for these fishes, in particular their breeding pairs. Data were collected in the northern Red Sea using 10 × 1-m belt transects in different reefs and zones. Gobiid density was highly correlated with coral density over all sites and zones, and the more specialized goby species preferred coral species that are less vulnerable to environmental stress. Moreover, the occupation rate of corals by goby breeding pairs significantly increased with colony size and decreased with partial mortality of colonies. Logistic regression showed that both coral size (being most important) and partial mortality are key factors influencing the occupation by breeding pairs. This study provides the first evidence that breeding pairs of coral-associated gobiids have more advanced habitat requirements than con-specifics in other social states. As coral reefs are threatened worldwide and habitat loss and degradation increase, this information will help predict the potential effects on those reef fishes obligatorily associated with live corals.     

Phenotypic variations in the preferred host coral impact the occupancy of an obligate coral-dwelling fish

Habitat specialists form tight relationships with their host habitat and are able to make microscale decisions when selecting final habitat locations. The obligate coral-dwelling fish, Gobiodon histrio, is thought to make habitat choices based on the coloration and structural characteristics of Acropora nasuta, their preferred coral host. Yet, most studies on the habitat preference of G. histrio have been conducted on Australia’s Great Barrier Reef with no understanding if geographic differences in preferences exist. Here, we tested the habitat preference of G. histrio toward A. nasuta on the reefs of Kadavu and Tavewa Islands, Fiji. First, to assess the natural distribution, belt transect surveys of all acroporid corals were conducted. Transects indicated that, while G. histrio is most frequently found in A. nasuta over other acroporid corals, the coral’s structural characteristics rather than the coral’s color variation were the preferred characteristic. In contrast, the Australian G. histrio have been found to be more frequent in blue A. nasuta opposed to the brown color variation, suggesting a geographic difference in habitat preferences among the species. In addition, we conducted two in situ behavioral field experiments to determine whether G. histrio would (1) move from dead A. nasuta to a live brown or blue A. nasuta and (2) preferentially select between the brown- or blue-colored A. nasuta when placed on a dead A. nasuta. The results of the in situ experiments support the finding that Fijian G. histrio does not discriminate between A. nasuta using color but uses only structural morphologies to guide its habitat selection process. Habitat selection is a complex process, and microscale habitat preferences within a species can vary between geographic locations. This study sheds light on the need to expand research findings to incorporate large geographic regions when attempting to understand the preferences of coral reef symbionts.