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.     

Defence of Females by Dominant Males of Artibeus jamaicensis (Chiroptera: Phyllostomidae)

Defence of females by dominant males of the Jamaican fruit‐eating bat Artibeus jamaicensis was observed in two natural colonies over 2 yr. A log‐linear model was used to evaluate the frequency distribution of visits to harems by sex, season and agonistic interaction of dominant males. Harem group size varied from four to 18 females, with one adult male in the small and medium‐sized groups and two males in the large groups (> 14 females). A highly significant interaction was noted between the age and sex of the visitor and the response of the dominant male. Male visitors were attacked more often than female and juvenile visitors. Aggressive defence increased during the reproductive seasons, with dominant males showing more agonistic responses towards male visitors. An increase in the frequency of visits by male visitors was noted in harem groups that ranged in size from four to 12 females, but the frequency of male visits declined in harem groups that contained more than 14 females.     

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.     

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     

Subordinate Males in Harem Groups of Jamaican Fruit‐Eating Bats (Artibeus jamaicensis): Satellites or Sneaks?

In the caves of Yucatan, Mexico, the Jamaican fruit‐eating bat, Artibeus jamaicensis, forms harems consisting of four to 18 females and a dominant male that defends the group against foreign males. Large groups (>14 females) contain an additional subordinate male. In theory, subordinate males can associate with harem groups either as satellites, if they provide at least some benefits to the dominant male, or as sneaks, if they only impose costs on the dominant male. We assessed the costs and benefits of subordinate males in three removal experiments. In the first experiment, when a dominant male was removed from its group, its role was occupied by the subordinate male (in large groups) or by a foreign male (in small groups). Former subordinate males took less time to gain control of the harems and stayed longer with the groups than foreign males. In the second experiment, when a subordinate male was removed, the rate of visitation by foreign males and the number of agonistic displays by the dominant male both increased. In the third experiment, when the number of females in large groups was reduced, subordinate males spent less time with their groups and the rate of visitation by foreign males increased. However, the frequency of agonistic displays by dominant males towards subordinate males did not change. Dominant males invest large amounts of energy in defending the harems, but obtain direct and immediate benefits from the presence of subordinate males in the form of access to a larger number of females, and suffer no obvious costs. Subordinate males apparently invest little energy in defending the harems, obtain no obvious immediate benefit, but gain long‐term benefits by having priority access to vacant positions left by dominant males. Subordinate males in harem groups of the Jamaican fruit‐eating bat can be considered satellites because their presence brings immediate benefits to the dominant males.     

Social organization of the spotted sharpnose puffer,Canthigaster punctatissima (Tetraodontidae)

Synopsis Tagged individuals of the Eastern Pacific sharpnose puffer, Canthigaster punctatissima, were studied at Punta Santa Inez, Baja California Sur. Territories were maintained by both sexes in this sexually dimorphic fish. Male puffers appear to have harems; one large male interacts with one to four smaller females. Puffers from different harems were not seen to interact except for occasional aggressive contact. Removal of a male puffer resulted in the overnight takeover of his harem by a neighboring male. Harem-forming behavior is discussed, as well as the possible role of predation.     

Alternative Contexts of Sex Change with Social Control in the Bucktooth Parrotfish, Sparisoma radians

Social control of sex change occurs in a variety of hermaphroditic fishes; upon removal of the dominant individual, the largest individual of the opposite sex typically changes sex and acquires mating priority with the remaining members of the social group. Social control may allow a phenotypically plastic response to social situations that convey cues about the relative advantages of functioning as one sex or the other, and should be advantageous in highly heterogeneous habitats such as coral reefs. Parrotfishes (family Scaridae) are dominant members of herbivorous coral reef fish assemblages, and numerous histological examinations of gonads have demonstrated the hermaphroditic life history of many species in the family. However, social control of sex change has never been conclusively demonstrated in the parrotfishes. To test a new version of the size-advantage model for sex change, we conducted removal experiments of dominant male bucktooth parrotfish, Sparisoma radians, in St. Croix, U.S. Virgin Islands. A total of seven females from five different reefs changed sex following removals, clearly demonstrating social control of sex change. In addition, all but one of those individuals changing sex were smaller than the largest females remaining in the harems, and this contrasts with nearly all previous studies of sex change in fishes. Sex change proceeds via a novel sequence of events when compared with previous studies. Rather than behavioral sex change preceding morphological sex change, the appearance of male coloration is followed by the development of male behavior that is fully expressed approximately 20 days after removal. We show how differing arrival rates of bachelor males at our study sites may facilitate alternative contexts of sex change, with sex change occurring within social groups in some locations and with bachelor males filling harem vacancies in other locations. Alternative contexts of sex change further illustrate the astonishing phenotypic plasticity in the social and mating behavior of parrotfishes.     

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     

The dynamics of male harem dominance in southern elephant seals (Mirounga leonina) at the South Shetland Islands

Breeding chronology, harem structure and changes in male harem dominance were studied at Stranger Point, Isla 25 de Mayo/King George Island, principally by extensive field census work during the 2003 breeding season. Males were individually identified and their size estimated by using a photogrammetric method. Peak female haul out for the population occurred on 31 October, when a total of 276 females were observed along 7 km of coastline, distributed in ten harems with a median size of 16 females. Overall sex ratio and harem sex ratio for the breeding population were 1:6.7 and 1:10.6, respectively. A total of 33 males were identified associated with harems. Male size conferred an advantage in terms of dominance hierarchy, since dominant males (4.91±0.15 m) were significantly longer than subordinate males (4.63±0.19 m). Harems were dominated by an average of 4.5 (range 2–7) different males during the breeding season. Elephant seals at Stranger Point breed in very low density aggregations. The main breeding events in this population occurred later than at other breeding sites, which agrees with previous observations in the area. Male movement among harems suggests that differences in mating success among males could be achieved through their different behaviours.     

Spawning dynamics of orange roughy,Hoplostethus atlanticus,in mid-slope waters of New Zealand

Synopsis The social and reproductive biology of the sand tilefish,Malacanthus plumieri (Malacanthidae), was studied at Glover's Reef, Belize, where this species occurs in colonies over sand-rubble flats. Individuals each occupy a home burrow refuge and a surrounding home range. Home range overlap among adjacent fish of the same sex is low, and individuals defend exclusive use of much of their home range against all conspecifics except mates (i.e., territoriality). Areas defended by males overlap the territories of up to 6 females; and male territory area is positively related to the number of female residents. Males maintain dominance over females within their territories by aggression, including intervention into some female disputes. Females spawn pelagically-dispersed eggs as frequently as every day. Each female spawns near her burrow, almost exclusively with the male whose defended area encompasses her territory (harem polygyny). Tilefish colonies therefore consist of a mosaic of female territories over which adjacent male territories are superimposed. Histological evidence and observation of behavioral sex change in one female revealed thatM. plumieri is capable of protogynous sex reversal. Females did not change sex in response to removal of one male. Occurrence of small transitional fish indicates that the onset of sex change is controlled by factors other than size-related social hierarchies within harems or colonies.     

Harem size and oviposition behaviour in a polygynous bark beetle

Abstract. 1. Harem polygyny can have fitness benefits and costs on females. In bark beetles of the genus Ips the latter may include within‐harem competition between larvae. However, earlier competition between females for male care and mating opportunities may also influence oviposition behaviour. There has been relatively little investigation into the relationship between harem size and initial egg output. The present study investigated this relationship in the bark beetle Ips grandicollis. 2. The measure of egg output used was the number of eggs in the gallery with the most eggs in each harem. Mean (±SE) harem size of 242 observed harems was 3.25 ± 0.10. A curvilinear relationship was found between egg output and harem size, with females in smaller harems (one to four females) laying more eggs with increased harem size. However, females in larger harems (five to seven females) laid fewer eggs as harem size increased. The optimal harem size (in terms of number of eggs laid) was close to four females. 3. We found no evidence from a behavioural assay that females could preferentially choose unmated males over mated males with harems of two females. Additionally, the distribution of harem sizes suggests that females distribute themselves among males randomly. 4. The results suggest that harem size has effects on female reproduction that extend beyond larval competition and influence patterns of oviposition. The mechanism that determines why egg laying is greatest at intermediate levels is unknown. There is no evidence that smaller harems belong to lower quality males, but females may adjust egg‐laying behaviour in large harems as a result of reduced male attendance or anticipated larval competition.     

Early sex change: A possible mating strategy ofCentropyge angelfishes (Pisces: Pomacanthidae)

Although the presence of socially controlled sex change in pomacanthid fishes of the genusCentropyge has been known since 1978, it has always been assumed that such sex change occurred only after the death or disappearance of the dominant male in single male social groups. Between 1978 and 1983, we observed several incidences of sex change by ranking female angelfishes within their harems and in the presence of the dominant male in each such harem. This phenomenon was observed inCetropyge interruptus andCentropyge tibicen, and occurred frequently enough to suggest the possibility of early sex change as a normal reproductive strategy in these species. Possible advantages of early sex change are discussed.     

Transition of nonharem male to harem male status in the short-nosed fruit bat Cynopterus sphinx

The short-nosed fruit bat Cynopterus sphinx is known to exhibit resource defence polygyny as its primary mating strategy. Tent construction by harem males to recruit females represents a heavy investment of time and effort, which is not done by nonharem males. The previously unobserved mode of harem formation by the solitary males was studied using mark-recapture and radio-telemetry. In our observation, the solitary males roosting near to harems started recruiting females by occupying the tent abandoned by the harems. This result suggests that the transition of nonharem male to harem male status possibly by a previously unobserved mode and the female recruitment is associated with resource (roost). It implies that the solitary males are actively involving in female recruitment and also presumably mating.     

Red deer females collect on male clumps at mating areas

Mating strategies in mammalian herbivores are adapted to thedispersion of females, and female dispersion is mainly determinedby resource dispersion, although it is frequently unclear whetherfemales may also be influenced by the location of males. Inthe red deer (Cervus elaphus) the distribution of females beforethe rut predicts the places were males should establish territoriesand even their relative success. However, the number of femalesusing the mating areas in Doñana increases during therut. We observed 20 areas of meadows, used by grazing femalesbefore the rut. At the onset of the rut, the number of females increasedin some of these areas and decreased in others, and the opposite patternwas found after the rutting period. Changes in the vegetationat mating and nonmating areas could not account for the changesin female distribution; even some of the highest quality meadowswere vacated by females during rut. In selecting the matingareas, females avoided isolated small meadows within the scrubarea and preferred larger meadows where a number of neighboringrutting males could be found. Females also avoided those areas heavilyused by fallow deer (Dama dama), a competing sympatric species.We found that females suffered less sexual harassment when inlarger harems and when their harem was surrounded by other harems.Our results, together with those in the literature about thispopulation, indicate that red deer females collect during theearly rut in mating areas containing several rutting males,although once there they may select particular sites based on availabilityof food rather than based on the presence of a particular male. Byjoining harems in large meadows they are less harassed, andat the same time they probably increase their chances of matingwith highly competitive males. The results from Doñanasupport the idea that harassment avoidance may lead to femalemovements to areas with male territories without lek breedingor female comparison of male phenotypes and may bring an insightinto those factors leading to clumps of male territories andleks.     

Experimental tests of copying and mate choice in fallow deer (Dama dama)

In fallow deer (Dama dama), as well as in other lek-breedingungulates, receptive females arriving at leks commonly joinmales that are defending large harems. This tendency enhancesdifferences in harem size and mating success between males.It could occur because females independendy move to the samemales, because females are attracted to males with females,or because females are attracted to each other. Using controlledexperiments with estrous female fallow deer, we show that, althoughfemales are more attracted to males with harems than to thosewithout, they are as frequently attracted to groups of femaleswithout a male as to female groups with males. We conclude thatfemale fallow deer joining leks are attracted to each otherand copy each other's movements. As yet, there is no firm evidencein fallow deer or in other lek-breeding ungulates that femalescopy each other's choice of mating partners. Key words: Damadama, fallow deer, lek breeding, mate choice, copying behavior.[Behav Ecol 4: 191–193 (1993)]     

One-male harems and female social dynamics in Guinea baboons

Little is known about the mating system and social organization of Guinea baboons. This study investigated whether Guinea baboons have a harem-based mating system similar to that of hamadryas and gelada baboons and whether one-male mating units also correspond to social units. Ten adult females in a captive multi-male multi-female group of Guinea baboons were focally observed 2 h per week for 12 weeks, and all observed copulations within the group were recorded. Some males copulated with a single female while others had harems of 2-4 females. All females copulated with a single male except 1 female that switched harems early in the study. The focal females had higher rates of social interaction with their harem members, especially their harem male, than with individuals outside the harem. Females appeared to be subordinate to the harem male but little or no physical aggression or herding behavior from the male was observed. Variation in female social interactions within the harem was not accounted for by their sexual interactions with the male or their genetic relatedness with the females. Females, however, appeared to maintain social relationships with their female relatives in other harems. Taken together, the results of this study show that both mating and affiliative interactions in Guinea baboons are concentrated within one-male units and that the social dynamics within and between these units share some similarities as well as differences with those of hamadryas and gelada baboons.     

Genetic mating system and the significance of harem associations in the bat Saccopteryx bilineata

We analysed the polygynous mating system of the bat Saccopteryx bilineata using behaviour observations and genetic data on 11 microsatellite DNA loci. Basic social units in S. bilineata are harem groups that consist of single males and up to eight females. Colonies comprise several harem groups, and the composition of colonies and harems is often stable over several reproductive seasons. The combination of parentage exclusion and likelihood-based parentage assignment in this study produced detailed parentage information for a large colony of S. bilineata. Reproduction occurred mostly within the colony (17% extra-colony paternity), but social associations in harems within the colony did not represent reproductive units (70% extra-harem paternity). The latter finding was consistent over three reproductive seasons. Spatial association of the roosting sites of males and females could not explain parentage patterns in the colony. Even though intra-harem paternity was less frequent than expected, it contributed significantly to reproduction of harem males. On average, the number of offspring sired by a male with females in his harem territory increased significantly with harem size, which corresponds to the higher energetic investment that is related to the maintenance of large harems. However, extra-harem paternity was not correlated with a male's harem size or intra-harem reproductive success. This suggests that individual preferences of females rather than male traits associated with the ability to defend large harems are most likely to cause the detected differences between social association and genetic mating system.     

Reconstruction of Parentage in a Band of Captive Hamadryas Baboons

The male leaders of free-ranging harem groups of hamadryas baboons are believed to mate exclusively with the female members of their harems, which typically contain no more than 2–3 females. Using no-parent parentage exclusion analysis (PEA) we identified the paternity of 25 offspring born in a captive band of hamadryas baboons (Papio hamadryas hamadryas) containing five adult males, each with a stable harem of about five females. Nine of 13 microsatellite (SSR) loci known to be highly polymorphic in rhesus macaques (Macaca mulatta) were successful in identifying the sires of all but two offspring without knowledge of the dams' genotypes, and we were able to determine the sires of all offspring when the dams' genotypes were considered. Mating success of the males ranged between 2 and 7 offspring and bore no clear relationship to the males' ages, ranks or the number of females in their harems. The males sired 7 of the 25 offspring with females outside their own harems, with higher-ranking males exhibiting greater success monopolizing access to females in their harem than lower-ranking males did. More surprisingly, the females assigned as the dams of 14 of the 25 offspring could be unequivocally excluded from parentage. The identity of the true dam could be determined for each of these 14 offspring using single-parent PEA and was uncorrelated with the ranks of these offsprings' sires and whether the offspring were born to dams outside the sires' harem groups. The combined effect of this extraharem mating and kidnapping was that only 12 of the 25 offspring were raised within their sires' harem groups. A second group of hamadryas baboons of identical structure exhibited the same high incidences of infant kidnapping and mating outside the harem group. It is unclear whether these behaviors provide an adaptive advantage or represent aberrant behavior resulting from captivity or other circumstances.     

Queuing for harem access in colonies of the greater sac-winged bat

Colonies of the greater sac-winged bat, Saccopteryx bilineata, consist of nonterritorial males and males that defend harem territories in which females roost. The traits of nonterritorial males that define their success in harem take-overs are so far unknown. We predicted that the time nonterritorial males spent in the colony and their proximity to harems would be important factors. We temporarily removed harem holders from a colony of 60 greater sac-winged bats on consecutive days and observed which of the nonterritorial males took over the harem. To test for consistency of results, we repeated the experiments in some of the territories. In a second set of experiments, we removed both the harem holder and the corresponding usurper from the first experiment. On average, usurping males preferred territories with a large harem over territories with a small harem and they belonged to groups of males who spent the daytime near the corresponding harems. Usurpers in the second experiment were present in the colony for a shorter time than usurpers in the first experiment. Overall, the results support the hypothesis that nonterritorial males form overlapping peripheral groups for harems and that they live in a hierarchy according to their tenure in the group. Group membership and hierarchy seemed to be the factors that determined whether a male occupied a vacant harem. Hence, instead of floating, the pattern of harem succession in greater sac-winged bats is best described by queuing of nonterritorial males for access to a harem. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.