Habitat patch size and mating system as determinants of social group size in coral-dwelling fishes

It is thought that the size and dispersion of habitat patches can determine the size and composition of animal social groups, however, this has rarely been tested. The relationship between group size, the mating system, and habitat patch size in six species of coral-dwelling gobies was examined. For all species, there was a positive correlation between coral colony size and social group size, however the strength of this relationship varied among species. Paragobiodon xanthosomus exhibited the strongest relationship and a manipulative field experiment confirmed that coral colony size limited group size in this species. For other species including Paragobiodon melanosomus and Eviota bifasciata, either a highly conservative mating system (P. melanosomus), or increased mobility (E. bifasciata) appeared to disrupt the relationship between habitat patch size and group size. There was no consistent relationship between the mating system exhibited and group size among the species investigated. These results demonstrate that habitat patch size, mobility, and mating systems can interact in complex ways to structure group size even among closely related species.     

Both-ways sex change in monogamous coral gobies, Gobiodon spp.

Synopsis We confirmed both-ways sex change in the coral-dwelling gobies Gobiodon micropus, G. oculolineatus, G. quinquestrigatus and G. rivulatus rivulatus by mate-removal experiment in the field and by the aquarium experiment of keeping two consexual fish in a coral. Eight species of Gobiodon were found in Acropora corals on the reef flat of Sesoko Island, Okinawa, southern Japan. The 4 species mentioned above bred in monogamous pairs composed of a male and a female matched by size, and the male took care of eggs deposited on the coral branch. In G. quinquestrigatus and G. rivulatus rivulatus males were larger than females in newly formed pairs, and females grew faster than their mates until breeding. The growth-rate advantage in females seems to be the major factor in the evolution of female to male sex change. The gobies strongly depended on host corals, but they moved between the corals after mate loss or coral death to form new pairs. This provides opportunities for the evolution of male to female sex change; the ability to change sex in both directions reduces the frequency of risky movement between host corals to form new pairs. These conditions are very similar to those reported in the both-ways sex change of another coral-dwelling goby Paragobiodon echinocephalus.     

The evolution of mating systems in bark and ambrosia beetles (Coleoptera: Scolytidae and Platypodidae)

The extraordinary array of mating systems in the Scolytidae and Platypodidae has been largely overlooked by researchers interested in the evolution of sexual behaviour. This paper provides the first overview of reproductive behaviour in this important and widespread group, known to most biologists only by the reputations of tree-killing taxa. Referred to generally as ‘bark beetles’, these insects chew egg tunnels inside a variety of (usually dead) plant tissues, though most species are either phloeophagous (breeding in the inner bark of woody plants) or xylomycetophagous (all stages feeding on mutualistic fungi growing on sapwood or heartwood). In most species, permanent records of many aspects of reproductive behaviour are etched in the host; in many, engravings reveal female fecundity, eggs sired per male, hatching success, and offspring survivorship. Each gallery arm represents a good portion of a given female's lifetime reproduction, but in many species females commonly re-emerge to reproduce in one or two additional sites. In most species of bark beetles, each female initiates her own gallery, to be joined later by a male. These monogynous gallery systems are associated with mating systems defined by how long males stay with females: in a few species, males seldom if ever join females under the bark; in the vast majority of species, males stay for part or all of the oviposition period then leave to seek other mates; and a few groups exhibit permanent monogamy, in that both sexes die in their only gallery system. While these patterns emerge from an overview of the world scolytid fauna, the length of male residency has seldom been quantified, and the costs and benefits associated with male mating strategies have not been measured for any bark beetle. Male-initiated monogyny is uncommon in Scolytidae, though the rule in Platypodidae; all instances of which I am aware are summarized from a phylogenetic perspective. Inbreeding polygyny with highly biased sex ratios has arisen at least seven times in Scolytidae. These taxa are usually characterized by males being dwarfed, flightless, and uncommon. Sex determination is known for only a few examples, but both haplodiploidy and diplodiploidy have been reported. Multiple origins of harem polygyny (otherwise rare in invertebrates) add an exciting dimension to the comparative and experimental study of scolytid mating systems. In harem polygynous taxa, males initiate gallery construction. I summarize what little can be learned from the literature about the fine structure of harem polygynous mating systems in bark beetles, and the problem of measuring reproductive success. Data on the nature of harem polygyny in Pityophthorus lautus are presented, illustrating (a) the fluidity of harems; (b) that average eggs laid per gallery arm is relatively unaffected by harem size, but strongly influenced by resource quality; (c) that male egg-gain is strongly correlated with territory quality (a consequence of (b) above); and (d) the temporal patterning of immigration and emigration and its effects on gallery system sex ratios. The second half of this paper is a discussion of the evolution of bark and ambrosia beetle mating Mating systems, emphasizing sexual selection and the role of resources. Male, residence is interpreted as postcopulalory guarding—preventing sexual liaisons with wandering males. Operational sex ratio, encounter rate, synchrony of breeding, ejaculate competition, and spatiotemporal distribution of resources are discussed as evolutionary forces moulding scolytid and platypodid male postmating behaviour. The nature of male male competition is reviewed. The paucity of information on male behaviour in gallery systems is mentioned; whether or not males significantly aid females is not known. Three hypotheses are presented for why females re-emerge, a feature which strongly affects operational sex ratios. Finally, I summarize features of bark beetle existence predisposing them to the evolution of post-inseminative guarding. Male-initiated monogyny presents a puzzle. I propose that most uncontested examples can be explained by monogyny re-evolving from (male-initiated) harem polygyny, and I present an argument for the evolution of harem polygyny leading to the development of male gallery initiation. The evolution of harem polygyny in birds and mammals has attracted considerable attention. The Verner Willson Orians polygyny threshold model is discussed with respect to bark beetles in general and P. lautus in particular. Resource quality is a major factor in P. lautus harem dynamics: the cost to females of joining harems is apparently slight compared to benefits accrued from moving into sites with higher quality inner bark. Female-biased adult sex ratios have been suggested to lead to harem polygyny, and literature and original data pertinent to this hypothesis are examined. The geometric constraints model, based on the polygyny threshold concept but tailored to bark beetles, is proposed to account for the failure of most species to evolve harem polygyny, and testable predictions are derived that interrelate breeding systems, habitat quality, and progeny size. The evolution of Inbreeding is briefly covered, and two routes to inbreeding polygyny are suggested.     

Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce

Corals are an essential and threatened habitat for a diverse range of reef-associated animals. Episodes of coral bleaching are predicted to increase in frequency and intensity over coming decades, yet the effects of coral-host bleaching on the associated animal communities remain poorly understood. The present study investigated the effects of host-colony bleaching on the obligate coral-dwelling crab, Trapezia cymodoce, during a natural bleaching event in the lagoon of Lizard Island, Australia. Branching corals, which harbour the highest diversity of coral associates, comprised 13% of live coral cover at the study site, with 83% affected by bleaching. Crabs on healthy and bleached colonies of Pocillopora damicornis were monitored over a 5-week period to determine whether coral bleaching affected crab density and movement patterns. All coral colonies initially contained one breeding pair of crabs. There was a significant decline in crab density on bleached corals after 5 weeks, with many corals losing one or both crabs, yet all healthy colonies retained a mating pair. Fecundity of crabs collected from bleached and healthy colonies of P. damicornis was also compared. The size of egg clutches of crabs collected from bleached hosts was 40% smaller than those from healthy hosts, indicating a significant reduction in fecundity. A laboratory experiment on movement patterns found that host-colony bleaching also prompted crabs to emigrate in search of more suitable colonies. Emigrant crabs engaged in aggressive interactions with occupants of healthy hosts, with larger crabs always usurping occupants of a smaller size. Decreased densities and clutch sizes, along with increased competitive interactions, could potentially result in a population decline of these important coral associates with cascading effects on coral health.     

Evolution of mating systems in coral reef gobies and constraints on mating system plasticity

Social and mating systems can be influenced by the distribution, abundance, and economic defendability of breeding partners and essential resources. Polygyny is predicted where males can economically defend multiple females or essential resources used by females. In contrast, monogamy is predicted where neither sex can monopolise multiple partners, either directly or through resource control, but where one mate is economically defendable. The mating system and reproductive behaviour of five species of coral reef goby were investigated and contrasted with population density and individual mobility. The two most abundant species (Asterropteryx semipunctatus and Istigobius goldmanni) were polygynous. In contrast, the less populous and more widely dispersed epibenthic species (Amblygobius bynoensis, Amblygobius phalaena and Valenciennea muralis) were pair forming and monogamous. All five species had low mobility, mostly remaining within metres (3 epibenthic species) or centimetres (2 cryptobenthic species) of a permanent shelter site. Interspecific differences in the mating system may have been shaped by differences in population density and the ability of reproductive individuals to economically defend breeding partners/sites. However, in a test of mating system plasticity, males of the three monogamous species did not mate polygynously when given the opportunity to do so in experimental manipulations of density and sex ratio. Mate guarding and complex spawning characteristics, which have likely co-evolved with the monogamous mating system, could contribute to mating system inflexibility by making polygynous mating unprofitable for individuals of the pair forming species, even when presented with current-day ecological conditions that usually favour polygyny.     

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.     

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.     

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.     

THE INFLUENCE OF MATING SYSTEM AND OVERLAPPING GENERATIONS ON EFFECTIVE POPULATION SIZE

The effective population size (N_e) depends strongly on mating system and generation time. These two factors interact such that, under many circumstances, N_e is close to N/2, where N is the number of adults. This is shown to be the case for both simple and highly polygynous mating systems. The random union of gametes (RUG) and monogamy are two simple systems previously used in estimating N_e, and here a third, lottery polygyny, is added. Lottery polygyny, in which all males compete equally for females, results in a lower N_e than either RUG or monogamy! Given nonoverlapping generations the reduction is 33% for autosomal loci and 25% for sex-linked loci. The highly polygynous mating systems, harem polygyny and dominance polygyny, can give very low values of N_e/N when the generation time (T) is short. However, as T is lengthened, N_e approaches N/2. The influence of a biased sex ratio depends on the mating system and, in general, is not symmetrical. Biases can occur because of sex differences in either survival or recruitment of adults, and the potential for a sex-ratio bias to change N_e is much reduced given a survival bias. The number of juveniles present also has some influence: as the maturation time is lengthened, N_e increases.     

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.     

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.     

Hypoxia tolerance and air-breathing ability correlate with habitat preference in coral-dwelling fishes

Hypoxia tolerance and air-breathing occur in a range of freshwater, estuarine and intertidal fishes. Here it is shown for the first time that coral reef fishes from the genera Gobiodon, Paragobiodon and Caracanthus, which all have an obligate association with living coral, also exhibit hypoxia tolerance and a well-developed air-breathing capacity. All nine species maintained adequate respiration in water at oxygen concentrations down to 15–25% air saturation. This hypoxia tolerance is probably needed when the oxygen levels in the coral habitat drops sharply at night. Air-breathing abilities of the species correlated with habitat association, being greatest (equaling oxygen uptake in water) in species that occupy corals extending into shallow water, where they may become air exposed during extreme low tides. Air-breathing was less well-developed or absent in species inhabiting corals from deeper waters. Loss of scales and a network of subcutaneous capillaries appear to be key adaptations allowing cutaneous respiration in air. While hypoxia tolerance may be an ancestral trait in these fishes, air-breathing is likely to be a more recent adaptation exemplifying convergent evolution in the unrelated genera Gobiodon and Caracanthus in response to coral-dwelling lifestyles.     

Facultative monogamy in obligate coral-dwelling hawkfishes (Cirrh tidae)

Synopsis Obligate coral-dwelling hawkfishes have been hypothesized to be monogamous. This hypothesized mating system is at odds with what is known of those of other cirrhitids. Neocirrhites armatus, which inhabits Pocillopora spp. corals, and Oxycirrhites typus, which inhabits gorgonians and antipatharian corals, were examined for evidence of a monogamous mating system. Life history criteria that favor monogamy in reef fishes (Barlow 1986) were examined for these two species. Facultative monogamy was found in both. In this mating system, males are limited in their ability to acquire and maintain females, and thus have only a single mate, but may acquire additional females if conditions for doing so are favorable.     

Systematics of the candelabrum gorgonian corals (Eunicea Lamouroux; Plexauridae; Octocorallia; Cnidaria)

Candelabrum gorgonian corals (genus Eunicea Lamouroux, 1816 ), with 15 valid species, comprise the most diverse and abundant group of octocorals in Caribbean coral reefs. The systematics of Eunicea was estimated based on 17 discrete morphological characters, mostly from sclerite morphology. Club sclerites, found on the surface of gorgonian tissue, provided the largest number of informative characters. A maximum parsimony analysis corroborated the monophyletic status of the group and the two internal groups (subgenera Eunicea s.s. and Euniceopsis Verrill). Differentiation based on the distribution and architecture of modules (e.g. polyps and calyces), as well as colony size and fecundity in females, was consistent amongst sister species (e.g. the new species and their closest morphological sister species) but not within species [e.g. amongst Eunicea succinea (Pallas) morphotypes], suggesting species boundaries for this group. Candelabrum gorgonian corals seem to be distributed indistinctively throughout the Caribbean province, where habitat requirements are met. One new species widely distributed in the Caribbean was described ( Eunicea tayrona sp. nov. ) using electron microscopy. Eunicea tayrona is externally similar to Eunicea fusca but there are numerous morphological and ecological differences between them. The morphotypes and phenotypic plasticity from Eunicea clavigera Bayer, Eunicea calyculata (Ellis & Solander), and Eunicea tourneforti Milne Edwards & Haime still deserve further study and might clarify the presence of additional new Eunicea species.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Microhabitat use and prey selection of the coral-feeding snail <Emphasis Type="Italic">Drupella cornus</Emphasis> in the northern Red Sea

Corallivorous gastropods of the genus Drupella are known for population outbreaks throughout the Indo-Pacific region. Despite their potential to destroy wide areas of coral reef, prey preferences have never been analyzed with respect to prey availability, and juvenile ecology and food selectivity remain largely unknown. Here, the influence of water depth, coral abundance, colony shape, prey species, and intraspecific attraction among snails on distribution patterns, prey selection, and microhabitat use of D. cornus was studied in the northern Red Sea. Special emphasis was put on ontogenetic differences. The snails were most abundant in the shallowest reef zone (1 m depth). Adults were associated with several substrates and coral growth forms, whereas juveniles were highly cryptic and restricted to live branching corals. The genus Acropora was significantly preferred over other acroporid and pocilloporid corals. As revealed by resource selection ratios, Acropora acuminata was preferred by juveniles, A. selago by adults. In aquarium experiments, intraspecific attraction was high among both life stages. Overall, significant differences in juvenile and adult microhabitat and prey use suggest that juveniles have more specific habitat requirements, and indicate ecological impacts on coral communities different from that of adults. Prey preferences seem to depend on both coral genus and colony shape. Acropora corals provide the best combination of food and shelter and therefore determine distribution patterns of D. cornus.     

Polygynous supercolonies of the acacia‐ant Pseudomyrmex peperi,an inferior colony founder

In ant–plant protection mutualisms, plants provide nesting space and nutrition to defending ants. Several plant–ants are polygynous. Possessing more than one queen per colony can reduce nestmate relatedness and consequently the inclusive fitness of workers. Here, we investigated the colony structure of the obligate acacia‐ant Pseudomyrmex peperi, which competes for nesting space with several congeneric and sympatric species. Pseudomyrmex peperi had a lower colony founding success than its congeners and thus, appears to be competitively inferior during the early stages of colony development. Aggression assays showed that P. peperi establishes distinct, but highly polygynous supercolonies, which can inhabit large clusters of host trees. Analysing queens, workers, males and virgin queens from two supercolonies with eight polymorphic microsatellite markers revealed a maximum of three alleles per locus within a colony and, thus, high relatedness among nestmates. Colonies had probably been founded by one singly mated queen and supercolonies resulted from intranidal mating among colony‐derived males and daughter queens. This strategy allows colonies to grow by budding and to occupy individual plant clusters for time spans that are longer than an individual queen’s life. Ancestral states reconstruction indicated that polygyny represents the derived state within obligate acacia‐ants. We suggest that the extreme polygyny of Pseudomyrmex peperi, which is achieved by intranidal mating and thereby maintains high nestmate relatedness, might play an important role for species coexistence in a dynamic and competitive habitat.     

Effect of female group size on harem male roosting behavior of the Indian short-nosed fruit bat <Emphasis Type="Italic">Cynopterus sphinx</Emphasis>

Mate guarding has been known to incur costs and cause constraints for harem males in many polygynous species. However, the effect of female group size on the harem male’s time budget in bats has received very limited attention. The Indian short-nosed fruit bat, Cynopterus sphinx, exhibits resource defense polygyny, in which tent roosting males construct tents and defend multiple female bats. We studied the effect of female group size on three aspects of harem male behavior: social grooming by reciprocal licking, tent maintenance, and tent guarding in the mast tree Polyalthia longifolia. In the process of reciprocal licking, all the bats in the harem were drenched in saliva before emergence, and this activity was positively and significantly correlated with female group size. Once females departed for foraging, harem males remained in their respective tents at night-time between intermittent foraging bouts and engaged in tent maintenance and tent guarding. Time invested by harem male bats in tent maintenance and tent guarding were positively and significantly correlated with female group size. Harem males extended their presence in tent by utilizing tents as feeding roosts. Female group size also influenced the emergence time of harem male bats, where males with largest group emerged later than did the smallest group. Likewise, harem male with the smallest group had more time available for foraging than the male with the largest group. Findings of this study suggest that having a larger harem may indeed be costly for the males by reducing their foraging time.