Eleven polymorphic microsatellite loci in a coral reef fish,Pterapogon kauderni

We describe the isolation and characterization of 11 polymorphic tetranucleotide microsatellite loci from a male mouthbrooding coral reef fish, the Banggai cardinalfish Pterapogon kauderni. In a sample of 37 fish from a natural population, polymorphism at these loci ranged from two to 15 alleles, with expected heterozygosities ranging from 0.107 to 0.928, enabling high‐resolution genetic studies of this coral reef fish.     

Genetic structure in the coral-reef-associated Banggai cardinalfish, Pterapogon kauderni

In this study, we used 11 polymorphic microsatellite loci to show that oceanic distances as small as 2-5 km are sufficient to produce high levels of population genetic structure (multilocus F(ST) as high as 0.22) in the Banggai cardinalfish (Pterapogon kauderni), a heavily exploited reef fish lacking a pelagic larval dispersal phase. Global F(ST) among all populations, separated by a maximum distance of 203 km, was 0.18 (R(ST) = 0.35). Moreover, two lines of evidence suggest that estimates of F(ST) may actually underestimate the true level of genetic structure. First, within-locus F(ST) values were consistently close to the theoretical maximum set by the average within-population heterozygosity. Second, the allele size permutation test showed that R(ST) values were significantly larger than F(ST) values, indicating that populations have been isolated long enough for mutation to have played a role in generating allelic variation among populations. The high level of microspatial structure observed in this marine fish indicates that life history traits such as lack of pelagic larval phase and a good homing ability do indeed play a role in shaping population genetic structure in the marine realm.     

Sex-Specific Territorial Behaviour in the Banggai Cardinalfish, Pterapogon kaunderni

In a field experiment, we studied how levels of aggression in males and females in established pairs of the Banggai cardinalfish were influenced by the sex of an experimentally introduced individual larger and more attractive than its resident counterpart. Contrary to previous studies on other cardinalfish species, and contrary to expectations in a sex role reversed species, the male was the main aggressor towards an intruder. Moreover, residents were more aggressive towards an intruder of the same sex as themselves. Furthermore, even though females often courted introduced, larger males, no intruder managed to take over the partnership of any resident. We suggest that our findings imply relatively equal sex roles in the Banggai cardinalfish and we discuss the evolution of sex specific territory defence and its significance in the Banggai cardinalfish as well as the implications of such behaviour in the interpretations of sex roles in general.     

Dispersal in the spiny damselfish,Acanthochromis polyacanthus,a coral reef fish species without a larval pelagic stage

The spiny damselfish, Acanthochromis polyacanthus, is widely distributed throughout the Indo‐Australian archipelago. However, this species lacks a larval dispersal stage and shows genetic differentiation between populations from closely spaced reefs. To investigate the dispersal strategy of this unique species, we used microsatellite markers to determine genetic relatedness at five dispersal scales: within broods of juveniles, between adults within a collection site (~30 m²), between sites on single reefs, between nearby reefs in a reef cluster, and between reef clusters. We sampled broods of juveniles and adults from seven reefs in the Capricorn‐Bunker and Swain groups of the Great Barrier Reef. We found that extra‐pair mating is rare and juveniles remain with their parents until fledged. Adults from single sites are less related than broods but more related than expected by chance. However, there is no evidence of inbreeding suggesting the existence of assortative mating and/or adult migration. Genetic differences were found between all of the reefs tested except between Heron and Sykes reefs, which are separated only by a 2‐km area of shallow water (less than 10 m). There was a strong correlation between genetic distance, geographical distance and water depth. Apparently, under present‐day conditions spiny damselfish populations are connected only between sites of shallow water, through dispersal of adults over short distances. Assuming that dispersal behaviour has not changed, the broad distribution of A. polyacanthus as a species is likely based on historical colonization patterns when reefs were connected by shallow water at times of lower sea levels.     

The Reproductive Biology and Early Ontogeny of the Mouthbrooding Banggai Cardinalfish, Pterapogon Kauderni (Perciformes, Apogonidae)

Pterapogon kauderni differs from most apogonids in several aspects of its reproductive biology. A breeding pair often allows a secondary male to intervene during mating. Each clutch consists of about 40 eggs 3 mm in diameter, held together by chorionic filaments and is incubated in the buccal pouch of the male for approximately 19 days. P. kauderni is the first apogonid in which direct development is described. Embryos hatch at post-flexion stages measuring about 6 mm SL and remain in the male's oral cavity for another ten days. When released as juveniles they measure 8 mm SL, their large yolksac is almost entirely consumed, and they do not pass through a planktonic interval. After release, juveniles do not return to the male's mouth for refuge, and any association between the male and newly released juveniles ceases. Juveniles reach 30 mm TL after four months and mature in another five to seven months. The embryo and juvenile development is presented.     

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.     

The adaptive significance of larval dispersal in coral reef fishes

Synopsis Coral reef fishes almost universally disperse over relatively great distances during a pelagic larval phase. Barlow (1981) suggested that this dispersal is adaptive because adult fishes inhabit a patchy, uncertain environment. This reiterated an older idea that the random extinction of local populations necessarily favours dispersal, since ultimately all populations of non-dispersers will disappear. Whereas this view is based on adult survival, we emphasize a less frequent view that substantial larval dispersal may be adaptive when offspring experience patchy and unpredictable survival in the pelagic habitat. We do not address the question of why these animals ‘broadcast’ rather than ‘brood’, but suggest that species committed to pelagic offspring will be under selection to disperse siblings to spread the risk of failure among members of a cohort. Our arguments are supported by a heuristic computer simulation.     

On the spatial scale of dispersal in coral reef fishes

Marine biologists have gone through a paradigm shift, from the assumption that marine populations are largely ‘open’ owing to extensive larval dispersal to the realization that marine dispersal is ‘more restricted than previously thought’. Yet, population genetic studies often reveal low levels of genetic structure across large geographic areas. On the other side, more direct approaches such as mark‐recapture provide evidence of localized dispersal. To what extent can direct and indirect studies of marine dispersal be reconciled? One approach consists in applying genetic methods that have been validated with direct estimates of dispersal. Here, we use such an approach—genetic isolation by distance between individuals in continuous populations—to estimate the spatial scale of dispersal in five species of coral reef fish presenting low levels of genetic structure across the Caribbean. Individuals were sampled continuously along a 220‐km transect following the Mesoamerican Barrier Reef, population densities were estimated from surveys covering 17 200 m² of reef, and samples were genotyped at a total of 58 microsatellite loci. A small but positive isolation‐by‐distance slope was observed in the five species, providing mean parent‐offspring dispersal estimates ranging between 7 and 42 km (CI 1–113 km) and suggesting that there might be a correlation between minimum/maximum pelagic larval duration and dispersal in coral reef fishes. Coalescent‐based simulations indicate that these results are robust to a variety of dispersal distributions and sampling designs. We conclude that low levels of genetic structure across large geographic areas are not necessarily indicative of extensive dispersal at ecological timescales.     

Probability of successful larval dispersal declines fivefold over 1 km in a coral reef fish

A central question of marine ecology is, how far do larvae disperse? Coupled biophysical models predict that the probability of successful dispersal declines as a function of distance between populations. Estimates of genetic isolation-by-distance and self-recruitment provide indirect support for this prediction. Here, we conduct the first direct test of this prediction, using data from the well-studied system of clown anemonefish (Amphiprion percula) at Kimbe Island, in Papua New Guinea. Amphiprion percula live in small breeding groups that inhabit sea anemones. These groups can be thought of as populations within a metapopulation. We use the x- and y-coordinates of each anemone to determine the expected distribution of dispersal distances (the distribution of distances between each and every population in the metapopulation). We use parentage analyses to trace recruits back to parents and determine the observed distribution of dispersal distances. Then, we employ a logistic model to (i) compare the observed and expected dispersal distance distributions and (ii) determine the relationship between the probability of successful dispersal and the distance between populations. The observed and expected dispersal distance distributions are significantly different (p < 0.0001). Remarkably, the probability of successful dispersal between populations decreases fivefold over 1 km. This study provides a framework for quantitative investigations of larval dispersal that can be applied to other species. Further, the approach facilitates testing biological and physical hypotheses for the factors influencing larval dispersal in unison, which will advance our understanding of marine population connectivity.     

Parasites of coral reef fish larvae: its role in the pelagic larval stage

The pelagic larval stage is a critical component of the life cycle of most coral reef fishes, but the adaptive significance of this stage remains controversial. One hypothesis is that migrating through the pelagic environment reduces the risk a larval fish has of being parasitised. Most organisms interact with parasites, often with significant, detrimental consequences for the hosts. However, little is known about the parasites that larval fish have upon settlement, and the factors that affect the levels of parasitism. At settlement, coral reef fishes vary greatly in size and age (pelagic larval duration), which may influence the degree of parasitism. We identified and quantified the parasites of pre-settlement larvae from 44 species of coral reef fishes from the Great Barrier Reef and explored their relationship with host size and age at settlement, and phylogeny. Overall, less than 50% of the larval fishes were infected with parasites, and over 99% of these were endoparasites. A Bayesian phylogenetic regression was used to analyse host-parasite (presence and intensity) associations. The analysis showed parasite presence was not significantly related to fish size, and parasite intensity was not significantly related to fish age. A phylogenetic signal was detected for both parasite presence and intensity, indicating that, overall, closely related fish species were likely to have more similar susceptibility to parasites and similar levels of parasitism when compared to more distantly related species. The low prevalence of infection with any parasite type and the striking rarity of ectoparasites is consistent with the ‘parasite avoidance hypothesis’, which proposes that the pelagic phase of coral reef fishes results in reduced levels of parasitism.

     

Life history,larval dispersal,and connectivity in coral reef fish among the Scattered Islands of the Mozambique Channel

The Western Indian Ocean harbors one of the world’s most diverse marine biota yet is threatened by exploitation with few conservation measures in place. Primary candidates for conservation in the region are the Scattered Islands (Îles Éparses), a group of relatively pristine and uninhabited islands in the Mozambique Channel. However, while optimal conservation strategies depend on the degree of population connectivity among spatially isolated habitats, very few studies have been conducted in the area. Here, we use highly variable microsatellite markers from two damselfishes (Amphiprion akallopisos and Dascyllus trimaculatus) with differing life history traits [pelagic larval duration (PLD), adult habitat] to compare genetic structure and connectivity among these islands using classic population structure indices as well as Bayesian clustering methods. All classical fixation indexes F _ST, R _ST, G′_ST, and Jost’s D show stronger genetic differentiation among islands for A. akallopisos compared to D. trimaculatus, consistent with the former species’ shorter PLD and stronger adult site attachment, which may restrict larval dispersal potential. In agreement with these results, the Bayesian analysis revealed clear genetic differentiation among the islands in A. akallopisos, separating the southern group (Bassas da India and Europa) from the center (Juan de Nova) and northern (Îles Glorieuses) islands, but not for D. trimaculatus. Local oceanographic patterns such as eddies that occur along the Mozambique Channel appear to parallel the results reported for A. akallopisos, but such features seem to have little effect on the genetic differentiation of D. trimaculatus. The contrasting patterns of genetic differentiation between species within the same family highlight the importance of accounting for diverse life history traits when assessing community-wide connectivity, an increasingly common consideration in conservation planning.

     

Spatial connectivity in an adult‐sedentary reef fish with extended pelagic larval phase

Understanding the spatial scale of demographic connectivity in marine reef fishes dispersing pelagic larvae is a challenging task because of the technical difficulties associated with tagging and monitoring the movements of progeny at early life stages. Several studies highlighted a strong importance of local retention with levels of dispersal of ecological significance restricted to short distances. To date little information is available in species where pelagic dispersal lasts for long periods of time. In this work, population structure and connectivity were studied in the grey triggerfish, Balistes capriscus. Grey triggerfish larvae and juveniles remain associated with floating Sargassum sp. beds for an estimated period of 4–7 months before settling on benthic habitats where they remain sedentary as adults. Analysis of genetic variation among populations along the continental shelf of the northern Gulf of Mexico and U.S. east coast, encompassing over 3,100 km of coastline, revealed homogeneous allele frequencies and a weak isolation‐by‐distance pattern. Moment and maximum‐likelihood estimates of dispersal parameters both indicated occurrence of large neighbourhoods with estimates of the dispersal distribution parameter σ of 914 and 780 km, respectively. Simulated distributions of dispersal distances using several distribution functions all featured substantial fractions of long‐distance dispersal events with the 90% percentiles of travel distance prior to settlement averaging 1,809 km. These results suggest a high dependency of local recruitment on the output of nonlocal spawning stocks located hundreds of kilometres away and a reduced role of local retention in this species.     

Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage

Aim Most reef fishes are site‐attached, but can maintain a broad distribution through their highly dispersive larval stage. The whitetip reef shark (Triaenodon obesus) is site‐attached, yet maintains the largest Indo‐Pacific distribution of any reef shark while lacking the larval stage of bony (teleost) fishes. Here we use mitochondrial DNA (mtDNA) sequence data to evaluate the enigma of the sedentary reef shark that maintains a distribution across two‐thirds of the planet. Location Tropical Pacific and Indian Oceans. Methods We analysed 1025 base pairs of the mtDNA control region in 310 individuals from 25 locations across the Indian and Pacific Oceans. Phylogeographic and population genetic analyses were used to reveal the dispersal and recent evolutionary history of the species. Results We resolved 15 mtDNA control region haplotypes, but two comprised 87% of the specimens and were detected at nearly every location. Similar to other sharks, genetic diversity was low (h = 0.550 ± 0.0254 and π = 0.00213 ± 0.00131). Spatial analyses of genetic variation demonstrated strong isolation across the Indo‐Pacific Barrier and between western and central Pacific locations. Pairwise Φ_ST comparisons indicated high connectivity among archipelagos of the central Pacific but isolation across short distances of contiguous habitat (Great Barrier Reef) and intermittent habitat (Hawaiian Archipelago). In the eastern Pacific only a single haplotype (the most common one in the central Pacific) was observed, indicating recent dispersal (or colonization) across the East Pacific Barrier. Main conclusions The shallow haplotype network indicates recent expansion of modern populations within the last half million years from a common ancestor. Based on the distribution of mtDNA diversity, this began with an Indo‐West Pacific centre of origin, with subsequent dispersal to the Central Pacific and East Pacific. Genetic differences between Indian and Pacific Ocean populations are consistent with Pleistocene closures of the Indo‐Pacific Barrier associated with glacial cycles. Pairwise population comparisons reveal weak but significant isolation by distance, and notably do not indicate the high coastal connectivity observed in other shark species. The finding of population structure among semi‐contiguous habitats, but population connectivity among archipelagos, may indicate a previously unsuspected oceanic dispersal behaviour in whitetip reef sharks.     

Employing a highly fragmented,weedy coral species in reef restoration

A major determinant in reef restoration programs is the choice of species employed. In this paper, we concentrate on the potential use of Montipora digitata (Dana, 1846), a highly fragmented and weedy coral species, for reef restoration and for recreation of reef physiognomy in Bolinao, The Philippines, under the ‘gardening concept’. Coral ramets (n = 1960) were reared in a shallow lagoon nursery for 1 year and then, the resulting nursery-grown colonies were transplanted onto denuded reef knolls at two different sites and according to three transplantation designs (grid design with high or low density and patch design). The nursery grown ramets, which had initially exhibited a 99% survivorship, were reduced to 87% by a super typhoon. Low detachment rates, low mortality (<1% both) and low bleaching (<3% over most months), have been indicating good nursery conditions for corals. Monitoring transplanted colonies for over 15 months showed no significant differences between the sites or among the three different transplantation designs. The major events of mortality and detachment were documented during the first 3 months post-transplantation and in the wake of a bleaching event. M. digitata transplants exhibited rapid growth (a 384% increase in ecological volume) and frequent fragmentation. Some fragments remained by their colonies of origin entangled in the attached branches, while other fragments fell onto the surrounding sandy substrate, forming M. digitata ‘beds’ around the knolls. In both, nursery and transplanted corals, creation of complex 3D structures was followed by recruitment of juvenile fishes into aggregations. Above results reveal that employing fast growing, weedy and easily fragmenting branching species, which are also considered as ‘modifier species’, in reef restoration may result in a fast regeneration of reef physiognomy. Instead of ‘copying’ natural processes, reef managers should therefore concentrate on recovering the reef's ability for self-maintenance.     

Barriers to gene flow in Embiotoca jacksoni, a marine fish lacking a pelagic larval stage

Abstract.— Marine species generally show high dispersal capabilities, which should be accompanied by high levels of gene flow and low speciation rates. However, studies that focused on the relationship between dispersal and gene flow in marine fishes have been inconclusive. This study focuses on the black surfperch, Embiotoca jacksoni , a temperate reef fish that lacks a pelagic larval stage and lives on almost continuous reefs along the California and Baja California coasts. Mitochondrial control-region sequences from 240 individuals were obtained, and phylogeographic patterns were analyzed. A major phylogeographic break was found at Santa Monica Bay, a sandy expanse that prevents adult dispersal. Deep water separating the southern California Channel Islands was also found to be a major barrier to gene flow. Minor phylogeographic breaks were also detected in the Big Sur/Morro Bay and in the Punta Eugenia/Guerrero Negro regions, but none in the Point Conception region. Gene flow levels in E. jacksoni were found to be almost identical to those of another species with limited dispersal, Acanthochromis polyacanthus , thus indicating that the lack of a pelagic larval stage combined with barriers to adult dispersal may have had similar effects on these two species.     

Isolation and characterization of 12 microsatellites from the black surfperch, Embiotoca jacksoni, a reef fish that lacks a pelagic larval phase

A set of 12 microsatellite markers was developed from Embiotoca jacksoni genomic DNA and tested for polymorphism using 64 individuals from two populations. All loci were polymorphic with a number of alleles ranging from two to 19 with expected heterozygosities ranging from 0.17 to 0.89. There was no evidence of linkage disequilibrium and all loci were in Hardy-Weinberg equilibrium, except for four loci in one population. High numbers of private alleles were consistent with strong population structure, and very limited dispersal. Six microsatellite markers successfully cross amplified and were polymorphic in closely related species, Embiotoca lateralis and Hyspurus caryi.     

Local retention,dispersal and fluctuating connectivity among populations of a coral reef fish

The persistence and resilience of marine populations in the face of disturbances is directly affected by connectivity among populations. Thus, understanding the magnitude and pattern of connections among populations and the temporal variation in these patterns is critical for the effective management and conservation of marine species. Despite recent advances in our understanding of marine connectivity, few empirical studies have directly measured the magnitude or pattern of connections among populations of marine fishes, and none have explicitly investigated temporal variation in demographic connectivity. We use genetic assignment tests to track the dispersal of 456 individual larval fishes to quantify the extent of connectivity, dispersal, self-recruitment and local retention within and among seven populations of a coral reef fish (Stegastes partitus) over a three-year period. We found that some larvae do disperse long distances (~200 km); however, self-recruitment was a regular phenomenon. Importantly, we found that dispersal distances, self-recruitment, local retention and the pattern of connectivity varied significantly among years. Our data highlight the unpredictable nature of connectivity, and underscore the need for more, temporally replicated, empirical measures of connectivity to inform management decisions.     

Intraspecific variation in the pelagic larval duration of tropical reef fishes

Estimates of pelagic larval duration (PLD) for 10 species of Pomacentridae and two species of Gobiidae were made. In eight of the 12 species examined, within‐population mean PLDs differed between sampling times, locations within regions and among regions. In contrast, the range of these same PLD estimates overlapped at all spatial and temporal scales examined in 11 of the 12 species, but not between regions in one species ( Amphiprion melanopus ). Therefore, despite tight error estimates typically associated with estimates of PLD taken from a particular population at a particular time in some taxa, the overlapping ranges in PLD reported here indicate that the length of the pelagic larval phase is a much more plastic trait than previously appreciated. Within‐species variation in PLD has considerable potential to provide further insights into the ecology and evolution of tropical reef fishes.