Beaugregory Damselfish Research Articles

Effects of two common antibiotics on the skin microbiome of ornamental reef fishes: Implications for manipulative experiments in microbial dynamics

AbstractAn understanding of the mechanistic drivers of animal‐microbial symbiosis and associations generally requires experiments that manipulate specific symbionts or microbial communities. As part of an ongoing study of the mechanisms that drive microbial communities in coral reef fishes, and specifically the role of cleanerfish in microbial transmission, we tested the effects of the commonly used antibiotics Enrofloxacin and Nitrofurazone on the skin microbiome of three ornamental reef fish species: the four‐eyed butterflyfish, Chaetodon capistratus (Chaetodontidae), the cleanerfish neon goby Elacatinus oceanops (Gobiidae) and the beaugregory damselfish Stegastes leucostictus (Pomacentridae). Our main aim was to characterize dysbiosis prompted by the delivery of the two antibiotics and understand whether both could be used to establish good starting points for microbial transmission experiments. We bathed the fish in antibiotic (or no exposure in the controls), sampled the skin microbiota via swabbing at zero (before treatment) and 3 and 7 days during the treatments, and examined the microbial community using a 16S rRNA gene sequencing approach. Nitrofurazone reduced skin‐associated microbial diversity in all species, whereas the same effect for Enrofloxacin was only seen in S. leucostictus. Although each antibiotic had its own, unique impact in microbial community, all treatments showed positive and negative shifts in the most abundant microbial taxa over time. Moreover, soon after the delivery of both antibiotics, increases in the abundance of opportunistic bacteria or potential pathogens, such as Alteromonas and Vibrio, were observed. Although both antibiotics are effective, Nitrofurazone more successfully reduces microbial diversity and therefore may be more ideal for experiments seeking to disrupt fish microbiomes.

Lethal and sublethal impacts of a micropredator on post-settlement Caribbean reef fishes.

The transition from a planktonic larval stage to a benthic or demersal juvenile stage, "recruitment", is a crucial event in the life history of coral reef fishes, and has a strong influence on population size. Predation by piscivorous fishes is thought to be the main determinant of recruitment success, and has received the most attention. However, recent studies suggest that recently settled reef fishes are also an important target of micropredation from blood-feeding ectoparasites which may have significant lethal and sublethal effects. In this study, we quantified the relationship between levels of infestation by gnathiid isopods and mortality rates among juveniles of three species of reef fishes as a function of body mass both within and among species. We found that a single gnathiid isopod larva could kill fish of all three species shortly after settlement, up to 0.116g [18mm fork length (FL)] in French grunt (Haemulon flavolineatum), 0.027g (15mm FL) in masked goby (Coryphopterus personatus) and 0.01g (9mm FL) in beaugregory damselfish (Stegastes leucostictus). For juvenile S. leucostictus, we also compared the ability of fish to defend a territory when infested with a sublethal number of gnathiids versus uninfected individuals. Uninfected fish were significantly more likely to win-pairwise contests versus infected fish. These findings suggest that gnathiids can significantly impact juvenile coral reef fish survival, and affect population dynamics well past the settlement stage.

Do males measure body sizes of males and females similarly? A test in the beaugregory damselfish, Stegastes leucostictus

Body length in fishes appears to serve as a “signal” for intra-sexual selection (i.e., male–male competition) and inter-sexual selection (i.e., mate choice). Previous studies indicate that the size of males correlates with the ability to gain or control resources from other males, while the size of females corresponds to features related to reproductive success such as fecundity. However, it remains unclear whether male size, as it relates to success in territory defense, is assessed similarly to female size as it relates to fecundity. Using the beaugregory damselfish (Stegastes leucostictus), a Caribbean coral reef fish, we examined whether focal males measure the “signal”, body length, similarly in both sexes. We presented focal territorial males with pairs of males and pairs of females that differed in size by varying degrees, and judged whether the focal male used size to differentiate between the two stimuli. We found that focal males did respond differently based on sex (spent more time near the two male stimuli) and size (spent more time near the larger fish) but did not respond to size differences based on sex. Thus, focal males measured size differences in both sexes similarly in spite of the size reflecting different attributes in males and females.

A differential prey response to invasive lionfish, Pterois volitans: Prey naiveté and risk-sensitive courtship

The assimilation of behavioral and evolutionary processes into conservation management provides insights into how invasive predators affect native fauna. The Indo-Pacific lionfish (Pterois volitans) has caused extensive reduction in the abundance of small-bodied reef fish within their introduced range. One possible mechanism facilitating this high predation rate may be due to prey exhibiting evolutionary naiveté toward this invasive predator. Here, we tested for the potential role of prey naiveté by examining the behavioral response of a prey species, the beaugregory damselfish (Stegastes leucostictus), toward this invasive predator. Damselfish demonstrated invasive predator recognition and subsequent anti-predator behavior, which may attenuate the impact posed by this invasive predator. However, damselfish under predation threat failed to modulate courtship behavior in the presence of lionfish. Therefore, benefits derived from the ability to recognize and respond appropriately to lionfish may be of little consequence if damselfish are unable to curtail high-risk courtship behavior in their presence.

Individual Behavioral and Neuronal Phenotypes for Arginine Vasotocin Mediated Courtship and Aggression in a Territorial Teleost

The neuropeptide arginine vasotocin (AVT) is well known to modulate both aggression and affiliation, yet few studies relate individual behavioral state to a quantitative assessment of AVT distribution in the brain. Here, using a wild population of beaugregory damselfish, Stegastes leucostictus, we assess: (1) the effect of AVT on courtship, and (2) with reference to our previous study on AVT modulation of aggression in this species, the relationship between AVT-like immunoreactive (ir) fiber distribution in the forebrain’s preoptic area and individual courtship and aggression levels. Exogenous AVT did not affect courtship, yet Manning compound, an arginine vasopressin (AVP) V1a receptor antagonist, significantly lowered but did not eradicate courtship. Consistent with AVT’s known facilitation of aggression in this species, the density of AVT-ir fibers in the preoptic area was significantly negatively correlated to aggression. Our findings match similar behavioral and immunoreactive patterns of neuropeptide secretion in other taxa. Unlike aggression, preoptic AVT-ir fiber density was not significantly correlated to individual courtship levels. The results suggest a differential involvement of preoptic AVT neurons and/or their receptors in supporting the expression of aggression and courtship.

Interactions between inter- and intrasexually selected behaviors in the beaugregory damselfish (Stegastes leucostictus)

There is a trade-off between mutually incompatible behaviors involved in conspecific aggression and courtship by territorial male beaugregory damselfish (Stegastes leucostictus). This trade-off may be variable based on the proximity of each stimulus. We first tested whether presenting male and female conspecific stimuli at varying distances from the breeding site influenced the territorial male's behavioral response by placing a single female or a single male in a clear plastic bottle 1 m or 2 m from the breeding site of the focal male. We found that the focal males responded similarly to females at either distance while they decreased their response to males at the greater distance. To test how distance influences the trade-off between inter- and intrasexually selected behaviors, we simultaneously placed bottled males and females near a male's breeding site. Reducing the proximity of one stimulus resulted in an increased response to the other stimulus. We suggest that the trade-off between behaviors is variable and show that distance plays a role in territorial males' behavioral response to multiple conspecific stimuli.

Interactions of natural and sexual selection: damselfish prioritize brood defense with male–male competition or courtship

AbstractNatural and sexual selection often act in opposing directions, forcing individuals to prioritize activities necessary for survival with those required for reproduction. We examined the interaction of natural and sexual selection pressures on the behaviour of beaugregory damselfish, Stegastes leucostictus, by presenting territorial males with an egg predator and either a male or female conspecific, requiring males to prioritize brood defense with either courtship or intra-sexual competition. By measuring the time spent near stimuli, we examined the influence of several factors, including stimuli type, variation in predator number, and the presence of eggs in a nest site. Generally, males spent more time with conspecific stimuli than egg predators, suggesting that the sexual selection pressures of deterring rivals and attracting mates outweigh the natural selection pressure to engage in brood defense. This decision was affected by the sex of the conspecific presented, the presence of eggs in a male's territory, and a number of interactions of these factors, indicating that male damselfish consider multiple factors before investing in certain types and intensities of behaviours. Furthermore, observations of behaviours associated with courtship and intrasexual aggression show that a natural selection pressure impacts intra- and inter-sexually selected behaviours differently in this system.

Assessment and decision-making in a Caribbean damselfish: nest-site quality influences prioritization of courtship and brood defence

In systems where territory quality varies, animals are expected to exhibit plasticity in behaviour in order to maximize fitness relative to their present territory quality. This requires assessment of territory quality followed by decision-making in relation to the priority of activities necessary for survival and reproduction. We examined how differences in territory quality of beaugregory damselfish (Stegastes leucostictus) influence the prioritization of courtship and egg defence by comparing behavioural responses of males defending artificial sites (high quality) with males defending natural sites (low quality) when presented with an egg predator, a conspecific female, and a simultaneous choice between both. A significant three-way interaction of territory quality, presentation type and stimulus was observed for time near stimuli. In paired presentations, males defending low-quality territories spent more time near a female and less near an egg predator; while males on high-quality territories spent more time near a predator than a female. Additionally, comparing single and paired presentations reveals that behaviours towards egg predators remain constant while behaviours towards females decrease with paired stimuli. These data suggest that territory quality and ecological context impact decision-making and the relative values of potential reproduction and/or past reproductive effort.

Caribbean damselfish with varying territory quality: correlated behaviors but not a syndrome

The behavioral syndrome hypothesis suggests that individual animals within a population behave differently due to specific behavioral types, and these should be consistent across behaviors or in different contexts. In contrast, for animals that live within an environment in which territory quality can change over time, natural selection should have favored behavioral flexibility and modulation of the cost of defense in relation to territory quality. This would require assessment of the territory followed by displays of appropriate types and intensities of behavior. We examined the territorial behavior of male beaugregory damselfish (Stegastes leucostictus) by enhancing territory quality using artificial breeding sites and comparing their behavior to males on lower quality natural sites. When male fish were defending high-quality artificial territories, they had higher levels of aggression toward male conspecifics and courtship toward females than when on low-quality natural territories. We also found that aggression and courtship behaviors were correlated on natural sites but not on artificial sites. Behaviors were not correlated within individuals when males switched from natural to artificial territories or from artificial to natural territories. These results indicate that males assess their current territories and adjust behaviors accordingly and that courtship and aggressive behaviors are not linked within a permanent behavioral syndrome. Key words: adaptive plasticity, beaugregory damselfish, behavioral syndromes, Stegastes leucostictus, territory quality. [Behav Ecol]

A Comparison of Damselfish Densities on Live Staghorn Coral (Acropora cervicornis) and Coral Rubble in Dry Tortugas National Park

Over the past 30 years, cold events and disease have reduced much of the live Acropora cervicornis (Staghorn Coral) in Dry Tortugas National Park (DTNP), FL to fields of coral rubble. It is unclear how the resulting loss of three-dimensional reef structure has affected density and distribution of reef-dependent damselfishes. We compared densities of Stegastes adustus (Dusky Damselfish), Stegastes leucostictus (Beaugregory Damselfish), Microspathodon chrysurus (Yellowtail Damselfish), Stegastes planifrons (Three-spot Damselfish) and Stegastes variabilis (Cocoa Damselfish) inhabiting DTNP's last live Staghorn Coral formation with densities from surrounding coral rubble. Live Staghorn Coral supported a 65% higher damselfish density compared to coral rubble. Density of Dusky, Cocoa, Beaugregory, Yellowtail and Three-spot Damselfish on coral rubble (0.11, 0.58, 0.74, 0.02, and 0.06 fish/m2, respectively) was less than that found on living Staghorn Coral colonies (2.03, 0.45, 0.25, 0.50, and 0.96 fish/m2, respectively). Dusky Damselfish dominated the live Staghorn Coral site, while Cocoa and Beaugregory Damselfish dominated the coral rubble site. Juvenile density was ten times greater on coral rubble than on live Staghorn Coral, whereas adults had highest densities on live Staghorn Coral.

Mate inspection patterns in the female beaugregory damselfish (Stegastes leucostictus)

We observed female beaugregory damselfish (Stegastes leucostictus) as they interacted with males to see whether their movements fit the predictions of different mate-search models. We established high-quality and low-quality groups with low variance in breeding site quality and a medium-quality, high-variance breeding site group and compared focal observations of female nonforaging forays in each group. Only 8% of 137 forays monitored resulted in spawning events. Eighty-nine percent of the forays were less than 240 s and were within 7 m of the focal female’s territory. Average foray times and straight-line foray distances did not differ for females traveling between males in each group. Females entered high-quality breeding sites at a higher rate than low-quality sites and round-trip distances were also greatest in high-quality groups, indicating that females were following a more convoluted path. We interpret these results to mean that (a) female beaugregories separate the tasks of mate assessment and mate choice by conducting information-gathering forays between mating events, (b) forays are energetically costly and therefore usually short in duration and overall distance traveled, (c) information collection takes approximately the same time for high-quality and low-quality mates, but (d) females will alter their foray patterns in high-quality areas to collect additional information. These data are also consistent with the hypothesis that females optimize their search by employing a tiered process of assessment during information-gathering forays, first using an adjustable threshold to accept or reject each male based on his courtship and subsequently a fixed threshold to assess the quality of each breeding site.

New insights into neuropeptide modulation of aggression: field studies of arginine vasotocin in a territorial tropical damselfish

The neuropeptides arginine vasotocin (AVT) and arginine vasopressin are key modulators of affiliation and aggression among non-mammalian and mammalian vertebrates, respectively. Here, we explored AVT's effect on aggression in a wild population of beaugregory damselfish, Stegastes leucostictus, a highly territorial species. Aggression by territorial males towards 'intruders' (bottled fishes) was assessed before and after each male received intramuscular injections of either AVT, Manning compound (an AVT V1a receptor antagonist), isotocin (the teleost homologue of mammalian oxytocin differing from AVT by two amino acids) or saline (vehicle control). Compared to saline controls, AVT and Manning increased and decreased aggression, respectively, while isotocin had no effect. Response selectivity was further established in a dose-response study that revealed an inverted U-shaped function. Compared to saline controls, aggression levels for low and high AVT doses were similar, while medium dose treatments were significantly greater. This type of behavioural response, the first that we know of for a vertebrate neuropeptide, could depend on the binding of AVT to both V1-type and other AVT or non-AVT receptors. The pattern revealed here for damselfish may be symptomatic of species- and context-dependent specificity of AVT's modulation of aggression across teleosts, as is currently proposed for tetrapods.

CONSEQUENCES OF PATCH REEF SPACING FOR DENSITY-DEPENDENT MORTALITY OF CORAL-REEF FISHES

The spatial configuration of habitat patches can profoundly affect a number of ecological interactions, including those between predators and prey. I examined the effects of reef spacing on predator-prey interactions within coral-reef fish assemblages in the Bahamas. Using manipulative field experiments, I determined that reef spacing influences whether and how density-dependent predation occurs. Mortality rates of juveniles of two ecologically dissimilar species (beaugregory damselfish and yellowhead wrasse) were similarly affected by reef spacing; for both species, mortality was density dependent on reef patches that were spatially isolated (separated by 50 m), and density independent on reef patches that were aggregated (separated by 5 m). A subsequent experiment with the damselfish demonstrated that a common resident predator (coney) caused a substantial proportion of the observed mortality, independent of reef spacing. Compared to isolated reefs, aggregated reefs were much more likely to be visited by transient predators (mostly yellowtail snappers), regardless of prey density, and on these reefs, mortality rates approached 100% for both prey species. Transient predators exhibited neither an aggregative response nor a type 3 functional response, and consequently were not the source of density dependence observed on the isolated reefs. These patterns suggest that resident predators caused density-dependent mortality in their prey through type 3 functional responses on all reefs, but on aggregated reefs, this density dependence was overwhelmed by high, density-independent mortality caused by transient predators. Thus, the spatial configuration of reef habitat affected both the magnitude of total predation and the existence of density-dependent mortality. The combined effects of the increasing fragmentation of coral reef habitats at numerous scales and global declines in predatory fish may have important consequences for the regulation of resident fish populations.

A model of oxygen-mediated filial cannibalism in fishes

Parental male fishes may consume some of the egg clutches they guard in order to improve the survival of developing embryos under low oxygen conditions. However, the mechanism by which males determine the proportion of a clutch to consume is poorly understood. We conducted a modelling study for the beaugregory damselfish, Stegastes leucostictus, a marine teleost that does not ventilate its eggs, to investigate fitness benefits of different filial cannibalism strategies. We used three models of filial cannibalism. In the first model, males were able to track environmental conditions and cannibalise a clutch in relation to the available oxygen. In the second model, males cannibalised a fixed proportion of each clutch to varying degrees. In the final model, males did not engage in filial cannibalism. Our model for males that were able to track environmental conditions showed a good fit to empirical data, and this model proved the most successful male strategy in response to variability in spawning rate, water temperature and clutch size. Males that cannibalised a fixed but high proportion of their clutches had higher reproductive success than males cannibalising a low proportion or that did not cannibalise their clutches. We discuss our findings in the context of male cannibalism strategies and the evolution of male filial cannibalism.

Female Choice and Male Courtship Behaviour in the Beaugregory Damselfish

AbstractDuring courtship in the beaugregory (Stegastes leucostictus), a coral reef fish, males turn the dorsal half of their bodies from dull brown to bright yellow, and perform a series of rapid dipping movements in front of females. To look for evidence that females select males on the basis of these characteristics, we provided males with artificial breeding sites in the field, measured their reproductive success, and videotaped courtship. Reproductive success was measured by monitoring both the number and size of egg clutches present in the breeding site that was defended by the male. Both unmanipulated and experimentally induced courtship events were videotaped in separate groups of 88 (of which 32 were videotaped courting females) and 30 males, respectively. Experimental induction of courtship was done by placing a female in a clear plastic cylinder 0.5 m away from the breeding site of a territorial male; each of the 30 males received 8 different female presentations, but never more than one a day, and with a different female every time. We compared (i) the cumulative amount of eggs and number of clutches with the amount of yellow colouration and dipping rate for individual males in both the observational and experimental groups, (ii) individual variation in percentage yellow and dipping rate (for the experimental group only) with reproductive success on the same day when courtship was videotaped, and (iii) egg survivorship (ratio of final to early stage eggs) with yellow colouration and dipping rate, to see if these characteristics indicate male parental ability. Individual variation in courtship characteristics was not correlated with reproductive success on that day. In contrast, however, mean values of percentage yellow and dip rate were correlated with both the number of clutches and amount of eggs, for both the observational and experimental group of males, indicating that females preferentially spawn with males that have the brightest yellow colouration and the highest dip rate. Percentage yellow colouration was correlated with egg survival in the unmanipulated males, but not in the experimental group, while dipping rate was not correlated with egg survival in either group. We argue here that female assessment of male courtship is part of a complex process of female choice, in which females either simultaneously or sequentially examine territorial, breeding site, and male characteristics, and thereby attempt to enhance the survivorship of their offspring.

Adaptive filial cannibalism in the beaugregory damselfish

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. There are few empirical studies, however, to support this hypothesis. The beaugregory damselfish, Stegastes leucostictus, is a marine teleost that does not actively ventilate its eggs by fanning them. Partial cannibalism is common in this species, but in field studies was found to be unrelated to ration level. Filial cannibalism differed from predation in the pattern of egg eating; filial cannibalism was characterised by a random pattern of egg loss from a clutch rather than an aggregated distribution. Embryos developed quicker and had higher survival rates when they were at low densities and in nest sites where oxygen levels were high, and experimental reduction of oxygen levels increased rates of filial cannibalism. Here I present a hypothesis for filial cannibalism in the beaugregory damselfish; males cannibalise egg clutches in order to reduce clutch density and improve oxygen supply to the remaining embryos. I use a model of filial cannibalism to demonstrate how oxygen mediated cannibalism may be adaptive, and discuss the evolution of filial cannibalism in the beaugregory damselfish and other teleosts.

Interactions between ophiuroids and beaugregory damselfish

The interactions between beaugregory damselfish and ophiuroids, potential damselfish egg predators, were investigated using several field studies. A survey of back reef areas showed that the two most common ophiuroid species, Ophiocoma echinata and Ophioderma appressum, were significantly associated with the territories of beaugregory males within the coral rubble habitat where both ophiuroids and beaugregory's can be found. Feeding experiments showed that three ophiuroid species (Ophiocoma echinata, Ophioderma appressum and Ophiocoma wendtii) and Echinometra viridis consumed late development stage beaugregory eggs, whereas earlier stages were only consumed by Ophioderma appressum and Echinometra viridis. Manipulation of ophiuroid densities had no significant effect on the survival of beaugregory eggs and had no measurable impact on female mate choice. The aggressive response of male beaugregory damselfish towards three ophiuroid and one echinoid species showed significant differences among species but were lower than those shown to bluehead wrasse, Thallasoma bifasciatum; the principal daylight predator of eggs. The intensity of attacks by male beaugregory damselfish towards Thallasoma bifasciatum increased significantly if males were guarding eggs, but did not appear to change for the four echinoderm species. Male habitat selection was shown to be unaffected by the presence of ophiuroids.

The effect of clutch size on whole clutch cannibalism in the beaugregory damselfish

Parental male beaugregory damselfish Stegastes leucostictus commonly cannibalize entire egg clutches under natural conditions. Clutch size was experimentally reduced, but a relationship between the extent of clutch reduction and the frequency of total cannibalism was not detected.

Dominance Relationships Between Male Territorial Neighbors in the Beaugregory Damselfish (Stegastes leucostictus)

Using the permanently territorial beaugregory damselfish ( Stegastes leucostictus ), we examined behavioral differences between neighbors and how they relate to territory quality, male size, and social interactions. We manipulated territory quality by replacing some male's poor quality natural breeding sites with artificial sites. These artificial sites were known to rapidly increase a male's reproductive success. Three types of paired neighbors were tested: both males with high quality artificial sites (Group I); both neighbors with low quality natural sites (Group II); one male with a low quality natural site and his neighbor with a high quality artificial site (Group III). Because neighbors rarely interact, we stimulated interactions by placing a bottled male or a bottled female midway between the two breeding sites. The area between the 2 sites was rarely patrolled by either neighbor and we judged them to be outside of either male's territory. Although we found that both neighbors were in close proximity to each other while they simultaneously attacked a bottled male or courted a bottled female, the neighbors rarely interacted. Without one neighbor aggressively dominating the other neighbor, the neighbor that attacked or courted the bottled animal most intensively was termed 'dominant.' For pairs where both neighbors defended sites of similar quality (Group I and II), dominance was not related to male size. Reproductive success was only measured for Group I (both males with artificial sites) and relative reproductive success was not related to dominance. For heterogeneous pairs (Group III), dominance was related to territory quality (the male given the artificial site was always dominant when compared to his neighbor) but not male size. Irrespective of pair type (Groups I, II, or III), there was no inter-group differences in behavior among the dominants or among the subordinates. With the removal of the dominant individual, the remaining subordinates increased their aggressiveness toward bottled males and resembled the dominant individuals that were removed. Removing subordinate individuals caused no change in the behavior of remaining dominant individuals. Thus, the dominant males of all group types appeared to suppress the behavior of subordinates. We speculate that when neighbors have similar sites (Groups I and II), their past social interactions may be responsible for the development of the initial dominant-subordinate relationship. However, this dominant-subordinate relationship can be reversed by giving the subordinate male a higher quality breeding site ( i.e . Group III). We found no evidence that a subordinate's reproductive success was influenced by his more dominant neighbor and we speculate that it may influence his ability to secure a breeding site.

Filial cannibalism improves survival and development of beaugregory damselfish embryos

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. However, there are few empirical studies to support this hypothesis. We conducted field and laboratory experiments to investigate partial filial cannibalism in Stegastes leucostictus, a coral reef fish with paternal care. Partial cannibalism was shown to be common, and males were found to remove developing embryos from throughout a clutch in a random pattern, rather than in the more aggregated pattern seen during embryo predation. Males that received a diet supplement grew faster than control males, but did not engage in less cannibalism. Also, males did not concentrate cannibalism on early embryonic stages with the highest energetic value. Experimental reduction of embryo densities was found to significantly increase embryo development rate and survival from egg deposition to hatching, and experimental reduction of oxygen levels significantly increased rates of partial filial cannibalism by males. Artificial spawning sites with low oxygen levels were avoided by spawning females, and cannibalism rates by males were higher. We propose that partial filial cannibalism serves as an adaptive parental strategy to low oxygen levels in S. leucostictus by increasing the hatching success of embryos.