Alternative spawning tactics of female angelfish according to two different contexts of sex change

Social conditions for sex change and reproductive success werestudied in the haremic marine angelfish, Centropyge ferrugatus,in the coral reefs of southern Japan. In this species the largestfemale in a harem changed sex not only after disappearance ofthe dominant male but also occasionally in his presence. Inisolated harems containing two to three females, strict socialcontrol by the dominant male resulted in females changing sexonly after the male disappeared (takeover sex change). In haremsadjacent to each other, however, takeover sex change did notoccur even when one of the males disappeared. Instead, largeharems including more than four females were formed by fusionof two adjacent harems. In such large harems, the dominant malewas unable to socially prevent the largest female from changingsex later to acquire a portion of the harem (harem-fission sexchange). Females in adjacent harems spawned less frequentlyand tended to grow faster than those in isolated harems, probablyto gain an advantage in dominance status over neighbors of similarsize. Thus, females changed spawning frequencies according tothe two different contexts of sex change. The takeover tacticresults in higher fitness than the harem-fission tactic, whichshould be the best in the bad situation of adjacent harems.     

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.     

Harem structure of the protogynous angelfish, Centropyge ferrugatus (Pomacanthidae)

Social structure of the protogynous angelfish, Centropyge ferrugatus, was examined on the coral reefs of Sesoko Island, Okinawa, Japan. Each individual male monopolized a harem of 1-6 females. Harems could be categorized as linear-type or branching-type based upon spatial and dominance relationships among the females. A linear harem consisted of different-sized females whose home ranges overlapped each other with a linear dominance order based on body size. Branching harems were composed of two linear sub-groups dividing a male's territory. Females of similar size did not have overlapping home ranges, which resulted in branching harems. These two systems appear to be a result of competition for opportunities of sex change, as only the largest fish of a harem (or a sub-group) can become a male. Comparison of the harem structures of some reef fishes suggests that the two harem structures may occur broadly in protogynous haremic fishes.c/o Prof. T. Kuwamura     

Reversed Sex Change in The Haremic Protogynous Hawkfish Cirrhitichthys falco in Natural Conditions

Bi‐directional sex change has recently been reported in a range of reef fishes, including haremic species that were earlier thought to be protogynous (female to male). However, the occurrence of this phenomenon and the social conditions driving the reversion of males to females (reversed sex change) have been poorly documented under natural conditions. Reversed sex change is predicted to occur in low‐density populations where facultative monogamy is common. However, few studies have evaluated this over a long period in such populations. We documented the occurrence of bi‐directional sex change during a 3‐yr demographic survey of a population characterised by small harem sizes in haremic hawkfish Cirrhitichthys falco. New males were derived following a change in sex of functional females (secondary males; n = 3) and juveniles always matured first as females (n = 3). Thus, C. falco exhibited a typical protogynous sexual pattern, consistent with a range of haremic fish species. We observed reversed sex change in two males. In both cases, all the females disappeared from their harems and the neighbouring males expanded their territories to encompass the territories of the sex changers. However, bachelor males did not always revert to females. A dominant male experienced bachelor status twice but regained mating opportunities following the immigration of a female into his territory or by taking a female from a neighbouring harem. Thus, we conclude that bachelor males use reversed sex change as a facultative tactic to regain reproductive status in a haremic mating system. In addition, we discuss the influence of harem size upon occurrence of reversed sex change.     

The influence of females on the initiation of female-to-male sex change in a coral reef fish

In the protogynous coral reef fish Anthias squamipinnis (Peters), all males are sex-reversed females. A sexually mature female can be induced to change sex by removing a male from her social group. The influence of non-sex-changing females on the initiation of sex change was evaluated in 109 social groups in the Gulf of Eilat. When the male and largest female were removed from each of 12 single-male groups, the second-largest female changed sex in 9 groups. This result distinguished between two behavioral hypotheses suggested by previous work and made it tenable that a particular behavioral measure, the profile of behavior-received, that depends on adult females, is critical to the initiation of sex change. This species forms all-female groups as well as bisexual groups. All-female groups can be expected to have some mechanism for the production of a male. The removal of the largest female from each of 8 all-female groups failed to induce sex change in any group. The dominant female in these groups thus does not function in the same way as does the male in bisexual groups, at least in terms of the initiation of sex change. Following the removal of the male from each of 8 bisexual groups containing five or fewer adult females, a female changed sex in only 4 groups. This 50% incidence of sex reversal was lower than the 77–80% incidence in control groups containing more than five adult females. Data suggest that a minimum of four adult females is probably required for the probability of sex change after male removal to equal 75%.     

Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef

Herbivorous fishes are a key functional group on coral reefs. These fishes are central to the capacity of reefs to resist phase shifts and regenerate after disturbance. Despite this importance few studies have quantified the direct impact of these fishes on coral reefs. In this study the roles of parrotfishes, a ubiquitous group of herbivorous fishes, were examined on reefs in the northern Great Barrier Reef. The distribution of 24 species of parrotfish was quantified on three reefs in each of three cross-shelf regions. Functional roles (grazing, erosion, coral predation and sediment reworking) were calculated as the product of fish density, bite area or volume, bite rate, and the proportion of bites taken from various substrata. Inner-shelf reefs supported high densities but low biomass of parrotfishes, with high rates of grazing and sediment reworking. In contrast, outer-shelf reefs were characterised by low densities and high biomass of parrotfish, with high rates of erosion and coral predation. Mid-shelf reefs displayed moderate levels of all roles examined. The majority of this variation in functional roles was attributable to just two species. Despite being rare, Bolbometopon muricatum, the largest parrotfish species, accounted for 87.5% of the erosion and 99.5% of the coral predation on outer-shelf reefs. B. muricatum displayed little evidence of selectivity of feeding, with most substrata being consumed in proportion to their availability. In contrast, the high density of Scarus rivulatus accounted for over 70% of the total grazing and sediment reworking on inner-shelf reefs. This marked variation in the roles of parrotfishes across the continental shelf suggests that each shelf system is shaped by fundamentally different processes. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Growth acceleration,behaviour and otolith check marks associated with sex change in the wrasse <Emphasis Type="Italic">Halichoeres miniatus</Emphasis>

In protogynous sex-changing fishes, females are expected to compete for the opportunity to change sex following the loss of a dominant male and may exhibit growth and behavioural traits that help them maintain their dominant status after sex change. A male removal experiment was used to examine changes in female growth and behaviour associated with sex change in the haremic wrasse Halichoeres miniatus and to test whether any changes in growth associated with sex change were recorded in otolith microstructure. Dominant females began displaying male-characteristic behaviour almost immediately after the harem male was removed. The frequency of interactions between females increased following male removal. In contrast, feeding frequency of females decreased. The largest one to three females in each social group changed sex following male removal and exhibited an increase in growth associated with sex change. Sex changers grew more than twice as fast as non-sex changers during the experimental period. This growth acceleration may enable new sex-changed males to rapidly reach a size where they can defend the remaining harem from other males. An optical discontinuity (check mark) was present in the otoliths of sex-changed fish, and otolith accretion rate increased significantly after the check mark, corresponding with the increased growth rate of sex-changing females. Wild caught males, but not females, exhibited an analogous check mark in their otoliths and similar increases in otolith increment widths after the check. This indicates that an increase in growth rate is a regular feature of sex-change dynamics of H. miniatus. Communicated by Environment Editor Prof. Rob van Woesik     

Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs

Around the globe, coral reefs and other marine ecosystems are increasingly overfished. Conventionally, studies of fishing impacts have focused on the population size and dynamics of targeted stocks rather than the broader ecosystem-wide effects of harvesting. Using parrotfishes as an example, we show how coral reef fish populations respond to escalating fishing pressure across the Indian and Pacific Oceans. Based on these fish abundance data, we infer the potential impact on four key functional roles performed by parrotfishes. Rates of bioerosion and coral predation are highly sensitive to human activity, whereas grazing and sediment removal are resilient to fishing. Our results offer new insights into the vulnerability and resilience of coral reefs to the ever-growing human footprint. The depletion of fishes causes differential decline of key ecosystem functions, radically changing the dynamics of coral reefs and setting the stage for future ecological surprises.     

Sex Change in Both Directions by Alteration of Social Dominance in Trimma okinawae (Pisces: Gobiidae)

The mating system of the gobiid fish Trimma okinawae is one of polygynous hermaphroditism, in which the largest female of a social unit changes sex following the removal of the dominant male. Histological observations of the gonads however, revealed that males have an ovarian tissue within a functional testis. The occurrence of ovarian tissue in the functional male suggests that T. okinawae males should be able to revert back into being functional females. To test this prediction, we placed females in an aquarium and allowed them to change sex. After confirming sex change from female to male, we individually placed new males into another aquarium and added a larger male to each. Our experiments revealed that females change sex and become males upon the removal of dominant males, and that those males changed sex again and became females in the presence of larger males. Sex change in both directions may be advantageous when a male is forced to become subordinate following the take over of the social unit by a larger male.     

Testing a new version of the size-advantage hypothesis for sex change: sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians

A variety of field studies suggest that sex change in animalsmay be more complicated than originally depicted by the size-advantagehypothesis. A modification of the size-advantage hypothesis,the expected reproductive success threshold model, proposesthat sperm competition and size-fecundity skew can stronglyaffect reproductive pay-offs. Size-fecundity skew occurs ifa large female's fecundity is markedly higher than the aggregateof the other members of her social group and, together withpaternity dilution from sperm competition, can produce situationsin which large females benefit by deferring sex change to smallerfemales. Deferral by large females can create sex-size distributionscharacterized by the presence of large females and small sex-changedmales, and it is precisely these distributions that the traditionalsize-advantage model cannot explain. We tested the predictionsof the new model with the bucktooth parrotfish, Sparisoma radians,on coral reefs in St. Croix, U.S. Virgin Islands. Collectionsand spawning observations determined that the local environmentalregime of S. radians is characterized by pervasive sperm competition(accompanying 30% of spawns) and factors that can produce substantialsize-fecundity skew in social groups. Dominant male removalexperiments demonstrate that the largest females in social groupsoften do not change sex when provided an opportunity. Instead,smaller, lower-ranking females change sex when a harem vacancyarises. This pattern of sex change is in contrast to virtuallyall previous studies of social control of sex change in fishes,but provides strong support for the general predictions of theexpected reproductive success threshold model.     

Sexually dichromatic protogynous angelfish Centropyge ferrugata (Pomacanthidae) males can change back to females

Protogynous hermaphroditism, female-to-male sex change, is well known among reef fishes where large males monopolize harems of females. When the dominant male disappears from a harem, the largest female may change sex within a few weeks. Recently, from experiments with some protogynous haremic fishes in which two males' cohabitated, it was confirmed that sexual behavior and gonads were completely reversible according to individual social status. However, the ability to reverse secondary-developed sexual body coloration has never been examined in any protogynous fish. We conducted two male cohabitation experiments with the protogynous haremic angelfish, Centropyge ferrugata, which has conspicuous sexual dichromatism on the dorsal fin. Smaller males of C. ferrugata soon performed female-specific mating behaviors when they became subordinated after losing a contest. They then completed gonadal sex change to females 47 or 89 d (n=2) after beginning cohabitation. In the course of the reversed gonadal sex change, male-specific coloration on the dorsal fin changed to that of a female. Thus, the sex of C. ferrugata, including secondary developed sexually dichromatic characteristics, can be completely reversible in accord with their social status.     

Reversed Sex-Change in the Protogynous Reef Fish Labroides dimidiatus

Protogynous hermaphroditism, or female-to-male sex change, is known for many reef fishes including wrasses (family Labridae) in which large males monopolize mating. When the dominant male disappears from a polygynous group, the largest female may change sex within a few weeks. Such social control of sex change was first documented in harems of the cleaner wrasse Labroides dimidiatus almost 30 yr ago. To examine whether change of social status would induce males of L. dimidiatus to perform reversed sex-change, we conducted experiments: (i) releasing single males near lone males whose mates have been removed in the field; and (ii) keeping two males in a tank. Smaller males changed back to females when they became subordinate: it took 53–77 d (n=3) for them to complete gonadal sex change and release eggs in the aquarium. The male–male pairs performed spawning behavior, with the smaller male in the female role already 5–58 d before completion of gonadal sex change. This is the first report of reversed sex-change among protogynous wrasses. Moreover, we conducted another experiment, keeping a pair of a male and a larger female in a tank (n=1). We found sex change by both mates, which has not been reported from any fishes. Thus, the sex of L. dimidiatus is strictly determined by social status whenever it changes after mate loss.     

Sleeping functional group drives coral-reef recovery

The world's coral reefs are in decline, with many exhibiting a phase shift from coral to macroalgal dominance . This change is often associated with habitat loss and overharvesting of herbivorous fishes, particularly parrotfishes and surgeonfishes . The challenge is to reverse this decline and enhance the resilience of coral-reef ecosystems . We demonstrate, by using a large-scale experimentally induced phase shift, that the rapid reversal from a macroalgal-dominated to a coral- and epilithic algal-dominated state was not a result of herbivory by parrotfishes or surgeonfishes. Surprisingly, phase-shift reversal was primarily driven by a single batfish species (Platax pinnatus), a fish previously regarded as an invertebrate feeder. The 43 herbivorous fishes in the local fauna played only a minor role, suggesting that biodiversity may not offer the protection we hoped for in complex ecosystems. Our findings highlight the dangers faced by coral reefs and other threatened complex ecosystems: Species or functional groups that prevent phase shifts may not be able to reverse phase shifts once they occur. Nevertheless, reversal is possible. The critical issue is to identify and protect those groups that underpin the resilience and regeneration of complex ecosystems.     

Polygamous mating system and protogynous sex change in the gobiid fish <Emphasis Type="Italic">Fusigobius neophytus</Emphasis>

Whereas mating behaviors and social structure have been studied extensively in monogamous hermaphroditic gobiid species, such studies are relatively limited for polygamous gobiid species. To investigate the reproductive strategy of polygamous gobies, mating groups of the common fusegoby Fusigobius neophytus were observed on reefs of Kuchierabu-jima Island, southern Japan. Males established mating nests on flat-rock surfaces within their territorial home ranges on sandy rubble flats. Females maintained independent home ranges outside the male home ranges during nonreproductive periods, but they shifted their home ranges to overlap with male ranges and actively visited male mating nests during their reproductive periods (1–3 days at ca. 7-day intervals). Females often changed mates during their serial mating. The mating system used by the common fusegoby fits with the definition of male-territory-visiting polygamy. The sex ratio within the study population was female-biased. Nest-holding males were significantly larger than females and were polygynous (mating with up to eight females). These characteristics fit well with the prediction of protogyny by the size-advantage model. Some of the females were observed to undergo functional sex changes to nest-holding males. In addition, small floating males demonstrated sneaking behavior. None of the floating males were derived from females that had changed sex, suggesting a diandric life-history pathway for F. neophytus.     

Herbivory, connectivity, and ecosystem resilience: response of a coral reef to a large-scale perturbation

Coral reefs world-wide are threatened by escalating local and global impacts, and some impacted reefs have shifted from coral dominance to a state dominated by macroalgae. Therefore, there is a growing need to understand the processes that affect the capacity of these ecosystems to return to coral dominance following disturbances, including those that prevent the establishment of persistent stands of macroalgae. Unlike many reefs in the Caribbean, over the last several decades, reefs around the Indo-Pacific island of Moorea, French Polynesia have consistently returned to coral dominance following major perturbations without shifting to a macroalgae-dominated state. Here, we present evidence of a rapid increase in populations of herbivorous fishes following the most recent perturbation, and show that grazing by these herbivores has prevented the establishment of macroalgae following near complete loss of coral on offshore reefs. Importantly, we found the positive response of herbivorous fishes to increased benthic primary productivity associated with coral loss was driven largely by parrotfishes that initially recruit to stable nursery habitat within the lagoons before moving to offshore reefs later in life. These results underscore the importance of connectivity between the lagoon and offshore reefs for preventing the establishment of macroalgae following disturbances, and indicate that protecting nearshore nursery habitat of herbivorous fishes is critical for maintaining reef resilience.     

Protogynous sex change in the haremic triggerfish Sufflamen chrysopterus (Tetraodontiformes)

The size-advantage model predicts that protogyny is likely to evolve in polygynous species. Polygynous mating systems have been reported from several species of triggerfishes (Balistidae), but sex change has never been confirmed among them. We performed male-removal experiments in the haremic triggerfish Sufflamen chrysopterus on the coral reefs of Sesoko Island, Okinawa. After removal and movement of territorial males, some females became single and later changed body color and sex. This is the first report of sequential hermaphroditism from Tetraodontiformes.     

Context-dependent corallivory by parrotfishes in a Caribbean reef ecosystem

This study assesses the patterns of corallivory by parrotfishes across reefs of the Florida Keys, USA. These reefs represent a relatively unique combination within the wider Caribbean of low coral cover and high parrotfish abundance suggesting that predation pressure could be intense. Surveys across eight shallow forereefs documented the abundance of corals, corallivorous parrotfishes, and predation scars on corals. The corals Porites porites and Porites astreoides were preyed on most frequently with the rates of predation an order of magnitude greater than has been documented for other areas of the Caribbean. In fact, parrotfish bite density on these preferred corals was up to 34 times greater than reported for corals on other reefs worldwide. On reefs where coral cover was low and corals such as Montastraea faveolata, often preferred prey for parrotfishes, were rare, predation rates on P. porites and P. astreoides, and other less common corals, intensified further. The intensity of parrotfish predation increased significantly as coral cover decreased. However, parrotfish abundance showed only a marginal positive relationship with predation pressure on corals, likely because corallivorous parrotfish were abundant across all reefs. Parrotfishes often have significant positive impacts on coral cover by facilitating coral recruitment, survival, and growth via their grazing of algae. However, abundant corallivorous parrotfishes combined with low coral cover may result in higher predation on corals and intensify the negative impact that parrotfishes have on remaining corals.     

Group sex ratio and sex reversal

In hermaphroditic fishes, the initiation of sex reversal by male removal explains the replacement of lost males but does not explain how the number of males in a group may increase. Since numerous species apparently cannot produce primary males, a second means of initiating sex reversal must exist. In the present study we formulate a model which suggests the existence of an additional mechanism governing sex change: as soon as the ratio of adult females to males within a group exceeds a certain threshold value, a female changes sex even though no male has been removed. This process is inferred from comparison of data collected in the Red Sea and the western Indian Ocean with the model's predictions concerning size at sex reversal and the sex ratio of groups. The results suggest how several ecological factors may influence the occurrence rate of sex reversal and the development and growth of social groups.     

Intragroup behavioural changes and the initiation of sex reversal in a coral reef fish in the laboratory

Observations of the coral reef fish Anthias squamipinnis (Peters) suggest that the behavioural control of female-to-male sex reversal is more complex than a simple dependence on the presence or absence of a male or on simple aspects of aggression or aggressive dominance. When the behavioural interactions of all group members of small, bisexual social groups of this fish were examined before and after male removal, two behavioural features were identified as possible factors controlling the initiation of sex change: the profile for behaviours received from, and the percentage of rushes given to other group members. Males and females each showed characteristic profiles both for behaviours given and for behaviours received. On the basis of the behaviour-given profile I identified two types of female. Both types were capable of changing sex following the removal of the male. Two to four weeks were required by sex-reversing fish for the profiles for behaviour given to change to a completely male form. After male removal, the remaining females began to treat the sex-reversing fish as though she the behavioural and coloration changes of sex reversal in a female.     

Reproductive behavior and social organization in the sand tilefish,Malacanthus plumieri

Synopsis Observations on the Caribbean sand tilefish, Malacanthus plumieri, were made during 3 dive trips in the Bahamas (Feb., 1986; July, 1986; Jan., 1987) at depths from 5 to 30 m. Eighteen mating groups contained 1 to 5 females (x = 2.9). Seven male home ranges (encompassing female ranges within mating groups) measured 250 to 700 m². Of 134 paired rises recorded between 1733 and 1925 h EST, 38 had an observed cloud of gametes. Mating times are presented in relation to time of sunset and depth of water. Courtship begins with conspicuous looping behavior of the male as he swims to a female. Close pairing, criss-crossing, and low rises (<1.5 m) often precede a high quivering upward swim (1.5 to 6 m) which culminates in the release of a cloud of gametes at the apex. M. plumieri is compared to the protogynous hermaphroditic razorfishes, Xyrichtys pentadactylus and X. martinicensis, with regard to social organization, size of male home ranges in exposed sandy habitats near coral reefs, sexual size dimorphism, and sex ratio.