Catchment to sea connection: Impacts of terrestrial run-off on benthic ecosystems in American Samoa.

Variation in water quality can directly affect the composition of benthic assemblages on coral reefs. Yet, few studies have directly quantified nutrient and suspended particulate matter (SPM) to examine their potential impacts on benthic community structure, especially around high oceanic islands. We assessed the spatio-temporal variation of nutrients and SPM across six sites in American Samoa over a 12-month period and used exploratory path analysis to relate dissolved inorganic nutrients, land use, and natural and anthropogenic drivers to benthic assemblages on adjacent shallow reefs. Multivariate analyses showed clear gradients in nutrient concentrations, sediment accumulation and composition, and benthic structure across watersheds. Instream nutrients and land uses positively influenced reef flat nutrient concentrations, while benthic assemblages were best predicted by wave exposure, runoff, stream phosphate and dissolved inorganic nitrogen loads. Identifying locality-specific drivers of water quality and benthic condition can support targeted management in American Samoa and in other high islands.

The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs.

BACKGROUND: In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. The most divergent, S. perrico, separated from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressus was the result of ongoing hybridization among the other three species by sequencing four nuclear markers and a mitochondrial locus in samples spanning 2/3 of the latitudinal extent of the TEP. RESULTS: A Structure model indicated that K = 3 fit the nuclear data and that S. compressus individuals had admixed genomes. Our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2s was also high in some cases. NewHybrids models revealed that 89.8% (n = 59) of the S. compressus samples were F1 hybrids between either S. perrico × S. ghobban or S. perrico × S. rubroviolaceus. Similarly, the most recently diverged S. ghobban and S. rubroviolaceus were hybridizing in small numbers, with half of the admixed individuals assigned to F1 hybrids and the remainder likely > F1 hybrids. We observed strong mito-nuclear discordance in all hybrid pairs. Migrate models favored gene flow between S. perrico and S. ghobban, but not other species pairs. CONCLUSIONS: Mating between divergent species is giving rise to a region-wide, multispecies hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of > F1 hybrids. Trimodal structure, and evidence for fertility of both male and female F1 hybrids, suggest that fitness declines sharply in later generation hybrids. In contrast, the hybrid population of the two more recently diverged species had similar frequencies of F1 and > F1 hybrids, suggesting accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids suggest that indiscriminate mating by male S. perrico is driving pre-zygotic breakdown, which may reflect isolation of this endemic species for millions of years resulting in weak selection for conspecific mate recognition. Despite overlapping habitat use and high rates of hybridization, species boundaries are maintained by a combination of pre- and post-mating processes in this complex.

Population genomic response to geographic gradients by widespread and endemic fishes of the Arabian Peninsula.

Genetic structure within marine species may be driven by local adaptation to their environment, or alternatively by historical processes, such as geographic isolation. The gulfs and seas bordering the Arabian Peninsula offer an ideal setting to examine connectivity patterns in coral reef fishes with respect to environmental gradients and vicariance. The Red Sea is characterized by a unique marine fauna, historical periods of desiccation and isolation, as well as environmental gradients in salinity, temperature, and primary productivity that vary both by latitude and by season. The adjacent Arabian Sea is characterized by a sharper environmental gradient, ranging from extensive coral cover and warm temperatures in the southwest, to sparse coral cover, cooler temperatures, and seasonal upwelling in the northeast. Reef fish, however, are not confined to these seas, with some Red Sea fishes extending varying distances into the northern Arabian Sea, while their pelagic larvae are presumably capable of much greater dispersal. These species must therefore cope with a diversity of conditions that invoke the possibility of steep clines in natural selection. Here, we test for genetic structure in two widespread reef fish species (a butterflyfish and surgeonfish) and eight range-restricted butterflyfishes across the Red Sea and Arabian Sea using genome-wide single nucleotide polymorphisms. We performed multiple matrix regression with randomization analyses on genetic distances for all species, as well as reconstructed scenarios for population subdivision in the species with signatures of isolation. We found that (a) widespread species displayed more genetic subdivision than regional endemics and (b) this genetic structure was not correlated with contemporary environmental parameters but instead may reflect historical events. We propose that the endemic species may be adapted to a diversity of local conditions, but the widespread species are instead subject to ecological filtering where different combinations of genotypes persist under divergent ecological regimes.

Demographic plasticity facilitates ecological and economic resilience in a commercially important reef fish.

Variation in life-history characteristics is evident within and across animal populations. Such variation is mediated by environmental gradients and reflects metabolic constraints or trade-offs that enhance reproductive outputs. While generalizations of life-history relationships across species provide a framework for predicting vulnerability to overexploitation, deciphering patterns of intraspecific variation may also enable recognition of peculiar features of populations that facilitate ecological resilience. This study combines age-based biological data from geographically disparate populations of bluespine unicornfish (Naso unicornis)-the most commercially valuable reef-associated species in the insular Indo-Pacific-to explore the magnitude and drivers of variation in life span and examine the mechanisms enabling peculiar mortality schedules. Longevity and mortality schedules were investigated across eleven locations encompassing a range of latitudes and exploitation levels. The presence of different growth types was examined using back-calculated growth histories from otoliths. Growth-type-dependent mortality (mortality rates associated with particular growth trajectories) was corroborated using population models that incorporated size-dependent competition. We found a threefold geographic variation in life span that was strongly linked to temperature, but not to anthropogenic pressure or ocean productivity. All populations consistently displayed a two-phase mortality schedule, with higher than expected natural mortality rates in earlier stages of post-settlement life. Reconstructed growth histories and population models demonstrated that variable growth types within populations can yield this peculiar biphasic mortality schedule, where fast growers enjoy early reproductive outputs at the expense of greater mortality, and benefits for slow growers derive from extended reproductive outputs over a greater number of annual cycles. This promotes population resilience because individuals can take advantage of cycles of environmental change operating at both short- and long-term scales. Our results highlight a prevailing, fundamental misperception when comparing the life histories of long-lived tropical ectotherms: the seemingly incongruent combination of extended life spans with high mortality rates was enabled by coexistence of variable growth types in a population. Thus, a demographic profile incorporating contrasting growth and mortality strategies obscures the demographic effects of harvest across space or time in N. unicornis and possibly other ectotherms with the combination of longevity and asymptotic growth.

Contrasting population genetic structure in three aggregating groupers (Percoidei: Epinephelidae) in the Indo-West Pacific: the importance of reproductive mode.

BACKGROUND: Understanding the factors shaping population genetic structure is important for evolutionary considerations as well as for management and conservation. While studies have revealed the importance of palaeogeographic changes in shaping phylogeographic patterns in multiple marine fauna, the role of reproductive behaviour is rarely considered in reef fishes. We investigated the population genetics of three commercially important aggregating grouper species in the Indo-West Pacific, namely the camouflage grouper Epinephelus polyphekadion, the squaretail coral grouper Plectropomus areolatus, and the common coral trout P. leopardus, with similar life histories but distinct spatio-temporal characteristics in their patterns of forming spawning aggregations. RESULTS: By examining their mitochondrial control region and 9-11 microsatellite markers, we found an overarching influence of palaeogeographic events in the population structure of all species, with genetic breaks largely coinciding with major biogeographic barriers. The divergence time of major lineages in these species coincide with the Pleistocene glaciations. Higher connectivity is evident in E. polyphekadion and P. areolatus that assemble in larger numbers at fewer spawning aggregations and in distinctive offshore locations than in P. leopardus which has multiple small, shelf platform aggregations. CONCLUSIONS: While palaeogeographic events played an important role in shaping the population structure of the target species, the disparity in population connectivity detected may be partly attributable to differences in their reproductive behaviour, highlighting the need for more investigations on this characteristic and the need to consider reproductive mode in studies of connectivity and population genetics.

Giant coral reef fishes display markedly different susceptibility to night spearfishing.

The humphead wrasse (Cheilinus undulatus) and bumphead parrotfish (Bolbometopon muricatum) are two of the largest, most iconic fishes of Indo-Pacific coral reefs. Both species form prized components of subsistence and commercial fisheries and are vulnerable to overfishing. C. undulatus is listed as Endangered and B. muricatum as Vulnerable on the IUCN Red List of Threatened Species. We investigated how night spearfishing pressure and habitat associations affected both species in a relatively lightly exploited setting; the Kia fishing grounds, Isabel Province, Solomon Islands. We used fisheries-independent data from underwater visual census surveys and negative binomial models to estimate abundances of adult C. undulatus and B. muricatum as a function of spearfishing pressure and reef strata. Our results showed that, in Kia, night spearfishing pressure from free divers had no measurable effect on C. undulatus abundances, but abundances of B. muricatum were 3.6 times lower in areas of high spearfishing pressure, after accounting for natural variations due to habitat preferences. It is likely the species' different nocturnal aggregation behaviors, combined with the fishers' use of night spearfishing by spot-checking underpin these species' varying susceptibility. Our study highlights that B. muricatum is extremely susceptible to night spearfishing; however, we do not intend to draw conservation attention away from C. undulatus. Our data relate only to the Kia fishing grounds, where human population density is low, the spot-checking strategy is effective for reliably spearing large numbers of fish, particularly B. muricatum, and fisheries have only recently begun to be commercialized; such conditions are increasingly rare. Instead, we recommend that regional managers assess the state of their fisheries and the dynamics affecting the vulnerability of the fishes to fishing pressure based on local-scale, fisheries-independent data, where resources permit.

Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes.

Ectotherms exhibit considerable plasticity in their life-history traits. This plasticity can reflect variability in environmental and social factors, but the causes of observed patterns are often obscured with increasing spatial scales. We surveyed dichromatic parrotfishes across the northern Great Barrier Reef to examine variation in body size distributions and concomitant size at sex change (L∆50 ) against hypotheses of directional influence from biotic and abiotic factors known to affect demography. By integrating top-down, horizontal, and bottom-up processes, we demonstrate a strong association between exposure regimes (which are known to influence nutritional ecology and mating systems) and both body size distribution and L∆50 (median length at female-to-male sex change), with an accompanying lack of strong empirical support for other biotic drivers previously hypothesized to affect body size distributions. Across sites, body size was predictably linked to variation in temperature and productivity, but the strongest predictor was whether subpopulations occurred at sheltered mid and inner shelf reefs or at wave-exposed outer shelf reef systems. Upon accounting for the underlying influence of body size distribution, this habitat-exposure gradient was highly associated with further L∆50 variation across species, demonstrating that differences in mating systems across exposure gradients affect the timing of sex change beyond variation concomitant with differing overall body sizes. We posit that exposure-driven differences in habitat disturbance regimes have marked effects on the nutritional ecology of parrotfishes, leading to size-related variation in mating systems, which underpin the observed patterns. Our results call for better integration of life-history, social factors, and ecosystem processes to foster an improved understanding of complex ecosystems such as coral reefs.

The historical biogeography of groupers: Clade diversification patterns and processes.

Groupers (family Epinephelidae) are a clade of species-rich, biologically diverse reef fishes. Given their ecological variability and widespread distribution across ocean basins, it is important to scrutinize their evolutionary history that underlies present day distributions. This study investigated the patterns and processes by which grouper biodiversity has been generated and what factors have influenced their present day distributions. We reconstructed a robust, time-calibrated molecular phylogeny of Epinephelidae with comprehensive (∼87%) species sampling, whereby diversification rates were estimated and ancestral ranges were reconstructed. Our results indicate that groupers originated in what is now the East Atlantic during the mid-Eocene and diverged successively to form six strongly supported main clades. These clades differ in age (late Oligocene to mid-Miocene), geographic origin (West Atlantic to West Indo-Pacific) and temporal-spatial diversification pattern, ranging from constant rates of diversification to episodes of rapid radiation. Overall, divergence within certain biogeographic regions was most prevalent in groupers, while vicariant divergences were more common in Tropical Atlantic and East Pacific groupers. Our findings reveal that both biological and geographical factors have driven grouper diversification. They also underscore the importance of scrutinizing group-specific patterns to better understand reef fish evolution.

The likelihood of extinction of iconic and dominant herbivores and detritivores of coral reefs: the parrotfishes and surgeonfishes.

Parrotfishes and surgeonfishes perform important functional roles in the dynamics of coral reef systems. This is a consequence of their varied feeding behaviors ranging from targeted consumption of living plant material (primarily surgeonfishes) to feeding on detrital aggregates that are either scraped from the reef surface or excavated from the deeper reef substratum (primarily parrotfishes). Increased fishing pressure and widespread habitat destruction have led to population declines for several species of these two groups. Species-specific data on global distribution, population status, life history characteristics, and major threats were compiled for each of the 179 known species of parrotfishes and surgeonfishes to determine the likelihood of extinction of each species under the Categories and Criteria of the IUCN Red List of Threatened Species. Due in part to the extensive distributions of most species and the life history traits exhibited in these two families, only three (1.7%) of the species are listed at an elevated risk of global extinction. The majority of the parrotfishes and surgeonfishes (86%) are listed as Least Concern, 10% are listed as Data Deficient and 1% are listed as Near Threatened. The risk of localized extinction, however, is higher in some areas, particularly in the Coral Triangle region. The relatively low proportion of species globally listed in threatened Categories is highly encouraging, and some conservation successes are attributed to concentrated conservation efforts. However, with the growing realization of man's profound impact on the planet, conservation actions such as improved marine reserve networks, more stringent fishing regulations, and continued monitoring of the population status at the species and community levels are imperative for the prevention of species loss in these groups of important and iconic coral reef fishes.

The spoIIE homolog of Epulopiscium sp. type B is expressed early in intracellular offspring development.

Epulopiscium sp. type B is an enormous intestinal symbiont of the surgeonfish Naso tonganus. Intracellular offspring production in Epulopiscium shares features with endospore formation. Here, we characterize the spoIIE homolog in Epulopiscium. The timing of spoIIE gene expression and presence of interacting partners suggest that the activation of σ(F) occurs early in Epulopiscium offspring development.

Cytology of terminally differentiated Epulopiscium mother cells.

Epulopiscium sp. type B, a member of the Firmicutes, is a large (up to 300 microm), cigar-shaped bacterial symbiont of surgeonfish that propagates itself by forming multiple intracellular offspring. This unusual form of reproduction is an apparent modification of a developmental program used by some Firmicutes to produce an endospore. At the onset of offspring formation, the Epulopiscium cell divides at both poles. The polar cells are engulfed by the larger mother cell and grow within the mother cell. At the final stages of development, the Epulopiscium mother cell lyses. Here we describe changes in Epulopiscium cell structure, focusing on mother cell DNA replication and cell death. DNA replication was examined by labeling cells with the nucleotide analog bromodeoxyuridine. As expected, DNA replication occurs in the developing offspring. However, well after passage of genetic information from parent to offspring is complete, DNA within the mother cell continues to replicate. Using fluorescence microscopy, we found that near the end of the offspring growth cycle, mother cell DNA disintegrates. The mother cell membrane and wall deteriorate as well. DNA replication within this terminally differentiated cell indicates the importance of mother cell nucleoids in cell maintenance and the development of offspring. The synchronized timing of mother cell deterioration within a population suggests that the Epulopiscium mother cell undergoes a programmed cell death. The programmed death of the mother cell may allow for the timely release of resources accumulated in the mother cell to provide nutrients to populations of these intestinal microbes and their host.