Speciation in coral-reef fishes

Covering <0·1% of the ocean’s surface, coral reefs harbour about one‐third of all marine fishes or c. 5000 species. Allopatry (geographic isolation) is believed to be the primary mode of speciation, yet few biogeographic barriers exist between reefs, and most reef fishes have a pelagic larval stage capable of extensive dispersal. Under these circumstances, why are there so many species of reef fishes? Since most biogeographic barriers in the oceans are either spatially or temporally permeable on a relatively short time frame, the requirement of isolation during allopatric speciation is hard to satisfy. Evidence from empirical and theoretical studies, the biological characteristics of coral reefs, and a reanalysis of biogeographic barriers indicate that sympatric speciation is possible but not common at small spatial scales and that parapatric speciation is a common (and probably the prevalent) mode of diversification in coral‐reef fishes. Regardless of the speciation mode, previous hypotheses of accelerated diversification in the Pleistocene due to sea level fluctuations are not supported by phylogenetic analyses. Recent developments in the area of comparative genomics can fuel a new revolution in the way marine speciation is studied.     

Early survivorship of juvenile coral reef fishes

Data on early survivorship of newly settled reef fish were collected by monitoring individuals which recruited to 30 small lagoonal patch reefs over three summers. Preliminary survivorship curves spanning the first 45 days after settlement were derived for 17 species. Most species showed greatest rates of mortality in the first 1–2 weeks in the reef environment however there were substantial differences among species in the extent and the temporal pattern of this. In six species, 75% of individuals survived the 45 days, while in 5 others, 20% or fewer survived that long. In eight species, mortality was negligible after the first 14 days. In the other 9, significant mortality occurred in subsequent weeks. Patterns of survivorship did not appear to differ substantially among years in five of the six species for which data were adequate. In particular, survivorship did not appear to be different among years even when levels of recruitment varied greatly.     

Modelling larval dispersal and behaviour of coral reef fishes

Coral reef fish spend their first few weeks developing in the open ocean, where eggs and larvae appear merciless to tides and currents, before attempting to leave the pelagic zone and settle on a suitable reef. This pelagic dispersal phase is the process that determines population connectivity and allows replenishment of harvested populations across multiple coral reef habitats. Until recently this pelagic larval dispersal phase has been poorly understood and has often been referred to as the ‘black-box’ in the life-history of coral reef fishes. In this perspective article we highlight three areas where mathematical and computational approaches have been used to aid our understanding of this important ecological process. We discuss models that provide insights into the evolution of the pelagic larval phase in coral reef fish, an unresolved question which lends itself well to a modelling approach due to the difficulty in obtaining empirical data on this life history strategy. We describe how studies of fish hearing and physical sound propagation models can be used to predict the detection distance of reefs for settling larval fish, and the potential impact of anthropogenic noise. We explain how random walk models can be used to explore individual- and group-level behaviour in larval fish during the dispersal and settlement stage of their life-history. Finally, we discuss the mutual benefits that mathematical and computational approaches have brought to and gained from the field of larval behaviour and dispersal of reef fishes.     

Predation on juvenile coral reef fishes: an exclusion experiment

The densities of recruits on caged and uncaged areas were compared in an experiment done to show the extent of predation on recently metamorphosed coral reef fishes. The design was unlike typical caging experiments, however, in that areas were caged only for short periods of 20–30 days and several independent trials, testing the same null hypothesis, were run. This was done to avoid confounding the effects of excluding herbivorous fishes with the effects of excluding piscivorous fishes. A third treatment, partially-meshed cages, revealed that the experiment was complicated by several other factors. Some prey species were attracted to the high relief offered by the experimental structures. Others responded to the differences in shelter from predators by redispersing themselves among the treatments shortly after settlement. There was also at least one significant edge effect caused by fishes preferring to settle near the boundaries of all treatments. In spite of these difficulties, observations on known individuals revealed that rates of mortality were age-dependent and decreased rapidly after metamorphosis. More than 25% of such fishes disappeared during their first five days in the benthic habitat compared with >10% of fishes aged 6–10 days and no losses of fishes aged 11–15 days. These early losses are the greatest instantaneous rates of mortality yet documented for recruited reef fishes. The experiment also suggested different rates of early mortality for various groupings of species: individuals of solitary, sedentary species disappeared approximately half as fast as individuals of the more mobile, and the more gregarious, species. This is probably a true reflection of the different vulnerability of these groups to predation and it may be caused by the different ways in which these fishes use the coral substratum. Our experience suggests that caging artifacts can have major impacts on the results obtained from this type of experiment and they must be controlled for adequately. We conclude that studies of predation on reef fishes may be done more easily using other methods.     

Vertical distribution behaviour and its spatial variation in late-stage larvae of coral-reef fishes during the day

Daytime vertical distribution behaviour of settlement-stage reef-fish larvae in the upper 18 m was documented by diver observations of 497 pelagic larvae of 7 species 100-1000 m offshore of Lizard Island, Great Barrier Reef. Four species were studied on 2 sides of the island. Depth amplitude and depth frequency differed among species, locations and times. Four pomacentrids had modal depths in the upper 30-50% of the water column. A lutjanid and 2 chaetodontids had modal depths 0-2 m deeper than the deepest-swimming pomacentrid. On the leeward side, 6 of 7 species swam deeper and/or more variably offshore. On the windward side, 1 of 4 species swam deeper or more variably offshore. No larvae swam deeper than 18 m on the leeward side, but 31% of larvae of 3 species did so on the windward side. Three of 4 species swam deeper and/or more variably on the windward than leeward side. Vertical distributions in relatively shallow water are apparently strongly influenced by water-column depth and bottom type.     

Physiology,endocrinology and chemical communication in aggressive behaviour of fishes

Fishes show remarkably diverse aggressive behaviour. Aggression is expressed to secure resources; adjusting aggression levels according to context is key to avoid negative consequences for fitness and survival. Nonetheless, despite its importance, the physiological basis of aggression in fishes is still poorly understood. Several reports suggest hormonal modulation of aggression, particularly by androgens, but contradictory studies have been published. Studies exploring the role of chemical communication in aggressive behaviour are also scant, and the pheromones involved remain to be unequivocally characterized. This is surprising as chemical communication is the most ancient form of information exchange and plays a variety of other roles in fishes. Furthermore, the study of chemical communication and aggression is relevant at the evolutionary, ecological and economic levels. A few pioneering studies support the hypothesis that aggressive behaviour, at least in some teleosts, is modulated by “dominance pheromones” that reflect the social status of the sender, but there is little information on the identity of the compounds involved. This review aims to provide a global view of aggressive behaviour in fishes and its underlying physiological mechanisms including the involvement of chemical communication, and discusses the potential use of dominance pheromones to improve fish welfare. Methodological considerations and future research directions are also outlined.     

Vertical distribution behaviour and its spatial variation in late-stage larvae of coral-reef fishes during the day

Daytime vertical distribution behaviour of settlement-stage reef-fish larvae in the upper 18?m was documented by diver observations of 497 pelagic larvae of 7 species 100–1000?m offshore of Lizard Island, Great Barrier Reef. Four species were studied on 2 sides of the island. Depth amplitude and depth frequency differed among species, locations and times. Four pomacentrids had modal depths in the upper 30–50% of the water column. A lutjanid and 2 chaetodontids had modal depths 0–2?m deeper than the deepest-swimming pomacentrid. On the leeward side, 6 of 7 species swam deeper and/or more variably offshore. On the windward side, 1 of 4 species swam deeper or more variably offshore. No larvae swam deeper than 18?m on the leeward side, but 31% of larvae of 3 species did so on the windward side. Three of 4 species swam deeper and/or more variably on the windward than leeward side. Vertical distributions in relatively shallow water are apparently strongly influenced by water-column depth and bottom type.     

Nocturnal relocation of adult and juvenile coral reef fishes in response to reef noise

Juvenile and adult reef fishes often undergo migration, ontogenic habitat shifts, and nocturnal foraging movements. The orientation cues used for these behaviours are largely unknown. In this study, the use of sound as an orientation cue guiding the nocturnal movements of adult and juvenile reef fishes at Lizard Island, Great Barrier Reef was examined. The first experiment compared the movements of fishes to small patch reefs where reef noise was broadcast, with those to silent reefs. No significant responses were found in the 79 adults that were collected, but the 166 juveniles collected showed an increased diversity each morning on the reefs with broadcast noise, and significantly greater numbers of juveniles from three taxa (Apogonidae, Gobiidae and Pinguipedidae) were collected from reefs with broadcast noise. The second experiment compared the movement of adult and juvenile fishes to reefs broadcasting high (>570 Hz), or low (<570 Hz) frequency reef noise, or to silent reefs. Of the 122 adults collected, the highest diversity was seen at the low frequency reefs; and adults from two families (Gobiidae and Blenniidae) preferred these reefs. A similar trend was observed in the 372 juveniles collected, with higher diversity at the reefs with low frequency noises. This preference was seen in the juvenile apogonids; however, juvenile gobiids were attracted to both high and low sound treatments equally, and juvenile stage Acanthuridae preferred the high frequency noises. This evidence that juvenile and adult reef fishes orientate with respect to the soundscape raises important issues for management, conservation and the protection of sound cues used in natural behaviour.     

Contrasts in algal food processing among five herbivorous coral-reef fishes

There were significant differences among five sympatric herbivorous reef fish species in their ranking of seven food-processing characters. Between them Zebrasoma scopas and Stegastes nigricans had the lowest bite rates, longest filling times, lowest defaecation activities and slowest gut turnover. Acanthurus nigrofuscus and Scarus sordidus were similar in having the fastest filling times, and high bite rates, gut-contents masses, gut turnover and defaecation activities. Ctenochaetus striatus was intermediate between those species pairs in five out of seven characters. Rich algal diets of S. nigricans and Z. scopas were contrasted with the carbonate intake of S. sordidus . The food-processing pattern of C. striatus was related to the siliceous content of a diatom diet. Food-processing characteristics of A. nigrofuscus were attributed to a diet which is readily absorbed and/or is of high nutritional quality.     

Non-lethal measurement of pectoral fin aspect ratio in coral-reef fishes

This study describes a novel method for measuring pectoral fin aspect ratio (AR) on live coral-reef fishes and tests the method against traditional measurements taken from a dissected fin. No significant differences were detected among repeated fin measurements, which validates the accuracy (intact v. dissected) and precision (repeatability over several days) of fin AR measurements on live fishes. One exception highlighted issues that may arise when working with species prone to fin damage.     

Larval history influences post-metamorphic condition in a coral-reef fish

Upon settlement, many fishes undergo an energetically costly metamorphic period that requires substantial nutritional reserves. Larval growth and the accumulation of lipids prior to metamorphosis are likely to influence growth and survival following this critical period. On the Caribbean island of St. Croix, I investigated relationships between larval growth, early life-history characteristics, and post-metamorphic lipid content in the bluehead wrasse Thalassoma bifasciatum. Lipid reserves remaining after metamorphosis were positively related (r2 = 0.62) to the width of the metamorphic band; thus, this otolith-derived trait may be used to estimate the condition at emergence of survivors collected at some later time. In contrast, pelagic larval duration, average larval growth, and otolith size at settlement were negatively related to post-metamorphic lipid content. Interestingly, the trend for slower growth among fish in good condition was not consistent over the entire pelagic larval duration. Analyses of daily larval growth histories indicated that fish with high lipid reserves grew rapidly in the last week prior to settlement, but relatively slowly during the early phases of larval life; those emerging with low lipid concentrations, however, displayed strikingly opposite patterns. These contrasting patterns of growth and energy storage were consistent at two sites and over three recruitment events. Otolith chemistry data suggested that differences in growth histories and body condition were consistent with the hypothesis of larval development in distinct oceanic environments (characterized by Pb concentration); but, within a water mass, differences reflected life-history trade-offs between growth and energy storage. The results have implications for understanding the processes driving juvenile survival, which may be condition dependent.     

In situ observation of settlement behaviour in larvae of coral reef fishes at night

The swimming behaviour of 534 coral reef fish larvae from 27 species was explored at Moorea Island (French Polynesia) while they searched for a suitable settlement habitat, on the first night of their lagoon life. Most larvae swam actively (74%) and avoided the bottom (77%). A significant relationship was highlighted between the vertical position of larvae in the water column and the distance they travelled from lagoon entrance to settlement habitat: larvae swimming close to the surface settled farther away on the reef than bottom-dwelling larvae.     

Role of predators in the early post-settlement demography of coral-reef fishes

Populations with dispersive larvae are often demographically open such that local reproduction and subsequent larval settlement are not linked. Thus, understanding whether and how settlement patterns are established and subsequently modified is central to understanding local demography. Settlement is typically not measured directly, but rather it is estimated by recruitment, which is the observation of new individuals sometime after settlement. At Lizard Island on the Great Barrier Reef, I examined how patterns of recruitment of coral-reef fishes were modified across a range of natural recruit densities in the presence and absence of resident predators. Resident predators decreased recruitment and increased mortality for all species, but these effects varied considerably among species. The effects of predators on recruitment were at least partly due to mortality within 2 days after settlement. At their most extreme, predators caused recruitment failure of several species of butterflyfish. For one species of damselfish (Pomacentrus amboinensis), predators both induced weakly density-dependent mortality and obscured any relationship between recruitment and subsequent abundance, while for another damselfish (Neopomacentrus cyanomos), mortality was density-independent and subsequent abundance was a function of recruitment. These contrasting results may reflect differences in prey behavior. P. amboinensis tended to feed near or within the branches of coral inhabited by resident predators, while N. cyanomos tended to feed higher in the water column above the reefs, and thus farther away from resident predators. These results highlight the speed and extent to which patterns of settlement are modified, indicating that caution should be exercised when attributing patterns of recruitment to patterns of settlement. Tremendous between-species variation in how patterns of recruitment, and presumably settlement, were modified by predation indicates that generalizations or between-species extrapolations about the magnitude of these effects may be unwarranted.     

Settlement preferences in coral-reef fishes: Effects on patterns of adult and juvenile distributions,individual fitness and population structure

Abstract Coral-reef fishes exhibit a wide range of habitat preferences at settlement. However, the consequences of these preferences to fitness and population dynamics are poorly known. We critically evaluate evidence for these consequences from recent studies of settlement preferences, and note that most studies have concentrated on only a few common taxa. We recommend that this taxonomic base be broadened, and that settlement preferences be incorporated into future studies of the link between larval supply and population dynamics of reef fishes.     

Early behaviour in fishes

Synopsis The ethological approach to the study of early life histories of fishes is illustrated by examples of behavioural ontogeny in cichlid and salmonid fishes. In both species recognition and social organization, early experience is of crucial importance.Paper presented in the symposium \lsEmbryonic and larval periods of fishes: present status and significance\rs, Canadian Conference for Fisheries Research (CCFFR), Fredericton, New Brunswick, January 1977     

Positive indirect effects of top-predators on the behaviour and survival of juvenile fishes

Top-predators can suppress mesopredator behaviour through risk effects. However, there is limited understanding of whether such behavioural suppression can dampen the lethal and sub-lethal effects of mesopredators on bottom level prey. Here, we document a field experiment that examines whether the presence of top-predator cues (visual and chemical stimuli from a coral trout) can cascade to indirectly influence the behaviour and survival of juvenile fish prey of different species (Pomacentrus amboinensis and P. chrysurus) and size (small = 1.18 cm SL versus large = 1.32 cm SL). Results showed that habitat patches exposed to top-predator cues received fewer visits and foraging attacks from mesopredators, leading to higher space use (~ 46%), feeding rate (~ 95%) and survival (~ 67%) from juvenile fish prey. Survival was always higher for individuals of P. amboinensis and of large-size, independent of the presence or absence of top-predator cues. Our data indicate that predation risk from the top-predator indirectly favoured the persistence and behaviour of juvenile fishes by promoting risk-averse behavioural responses in mesopredators. This study underscores the behavioural mechanisms by which risk effects can cascade through the food web and highlights the consequences that harvesting top-predators may have on the replenishment of bottom prey populations.     

Linking functional morphology and feeding performance in larvae of two coral-reef fishes

Despite the well acknowledged phenomenon that the biology of marine teleost fish larvae is much different from that of juvenile and adult conspecifics, very little is known about the changes in design of the feeding apparatus as larvae develop from hatching through metamorphosis. Furthermore, our understanding of the consequences of these developmental changes for feeding performance is very limited. In this study, we examined the relationship between the development of the feeding apparatus and feeding performance in larvae of Amphiprion ocellaris and Pseudochromis fridmani using cluster analysis, multi-dimensional scaling (nMDS), and canonical correspondence analysis (CCA). Several patterns emerge from our analyses. First, the state of development of the feeding apparatus increased in complexity through ontogeny, from a simple, hyoid-driven system at the onset of exogenous feeding to a more complex feeding system involving all adult functional elements of the cranium just prior to metamorphosis. Although the feeding apparatus converged to the hyoid-opercular-mandible linkage state around metamorphosis in both species, P. fridmani had a lesser developed hyoid-mandible linkage system relative to A. ocellaris at the onset of first-feeding. Second, first-feeding larvae fed on smaller, less elusive zooplankton. In contrast, larvae that survived beyond the first-feeding stage fed on more diverse prey types, including larger, more elusive zooplankton. Third, intra- and inter-specific variation in the development of the feeding apparatus is associated with variation in feeding performance. The post-hatch developmental trajectory in both species showed a pattern consistent with stage (i.e., ontogenetic state)-specific shifts in morphology and performance. Furthermore, the number of developmental transitions in both feeding functional morphology and feeding performance differ between species that exhibit contrasting incubation periods.