Assessing the vulnerability of marine life to climate change in the Pacific Islands region.

Our changing climate poses growing challenges for effective management of marine life, ocean ecosystems, and human communities. Which species are most vulnerable to climate change, and where should management focus efforts to reduce these risks? To address these questions, the National Oceanic and Atmospheric Administration (NOAA) Fisheries Climate Science Strategy called for vulnerability assessments in each of NOAA's ocean regions. The Pacific Islands Vulnerability Assessment (PIVA) project assessed the susceptibility of 83 marine species to the impacts of climate change projected to 2055. In a standard Rapid Vulnerability Assessment framework, this project applied expert knowledge, literature review, and climate projection models to synthesize the best available science towards answering these questions. Here we: (1) provide a relative climate vulnerability ranking across species; (2) identify key attributes and factors that drive vulnerability; and (3) identify critical data gaps in understanding climate change impacts to marine life. The invertebrate group was ranked most vulnerable and pelagic and coastal groups not associated with coral reefs were ranked least vulnerable. Sea surface temperature, ocean acidification, and oxygen concentration were the main exposure drivers of vulnerability. Early Life History Survival and Settlement Requirements was the most data deficient of the sensitivity attributes considered in the assessment. The sensitivity of many coral reef fishes ranged between Low and Moderate, which is likely underestimated given that reef species depend on a biogenic habitat that is extremely threatened by climate change. The standard assessment methodology originally developed in the Northeast US, did not capture the additional complexity of the Pacific region, such as the diversity, varied horizontal and vertical distributions, extent of coral reef habitats, the degree of dependence on vulnerable habitat, and wide range of taxa, including data-poor species. Within these limitations, this project identified research needs to sustain marine life in a changing climate.

Integrating larval connectivity with local demography reveals regional dynamics of a marine metapopulation.

Many ocean species exist within what are called marine metapopulations: networks of otherwise isolated local populations connected by the exchange of larval offspring. In order to manage these species as effectively as possible (e.g., by designing and implementing effective networks of marine protected areas), we must know how many offspring are produced within each local population (i.e., local demography), and where those offspring disperse (i.e., larval connectivity). Although there is much interest in estimating connectivity in the relatively simple sense of identifying the locations of spawning parents and their settling offspring, true measures of demographic connectivity that account for among-site variation in offspring production have been lacking. We combined detailed studies of local reproductive output and larval dispersal of a coral reef fish to quantify demographic connectivity within a regional metapopulation that included four widely spaced islands in the Bahamas. We present a new method for estimating demographic connectivity when the levels of dispersal among populations are inferred by the collection of genetically "tagged" offspring. We estimated that 13.3% of recruits returned to natal islands, on average (95% CI = 1.1-50.3%), that local retention was high on one of the islands (41%, 95% CI = 6.0-97.0%), and that larval connectivity was appreciable, even between islands 129 km apart (mean = 1.6%, 95% CI = 0.20-8.8%). Our results emphasize the importance of properly integrating measurements of production with measurements of connectivity. Had we not accounted for among-site variation in offspring production, our estimates of connectivity would have been inaccurate by a factor as much as 6.5. At a generational timescale, lifetime offspring production varied substantially (a fivefold difference among islands) and the importance of each island to long-term metapopulation growth was dictated by both larval production and connectivity. At the scale of our study (local populations inhabiting 5-ha reefs), the regional metapopulation could not grow without external input. However, an exploratory analysis simulating a network of four marine protected areas suggested that reserves of >65 ha each would ensure persistence of this network. Thus, integrating studies of larval connectivity and local demography hold promise for both managing and conserving marine metapopulations effectively.

Parasitism in Pterois volitans (Scorpaenidae) from coastal waters of Puerto Rico, the Cayman Islands, and the Bahamas.

Recently, Pterois volitans, a Pacific species of lionfish, invaded the Atlantic Ocean, likely via the aquarium trade. We examined for internal and external parasites 188 individuals from 8 municipalities of Puerto Rico collected during 2009-2012, 91 individuals from Little Cayman, Cayman Islands, collected during the summers of 2010 and 2011, and 47 individuals from Lee Stocking Island, Bahamas, collected during the summer of 2009. In total, 27 parasite taxa were found, including 3 previously reported species from lionfish, the digenean Lecithochirium floridense, the leech Trachelobdella lubrica, and an Excorallana sp. isopod. We also report another 24 previously unreported parasite taxa from lionfish, including digeneans, monogeneans, cestodes, nematodes, isopods, a copepod, and an acanthocephalan. Among these parasites, several were previously unreported at their respective geographic origins: We report 5 new locality records from Puerto Rico, 9 from Cayman Islands, 5 from the Bahamas, 5 from the Caribbean, and 3 from the subtropical western Atlantic region. Three parasites are reported to associate with a fish host for the first time. The parasite faunas of P. volitans among our 3 study sites were quite different; most of the species infecting lionfish were generalists and/or species that infect carnivorous fishes. Although our study did not assess the impact of parasites on the fitness of invasive lionfish, it provides an important early step. Our results provide valuable comparative data for future studies at these and other sites throughout the lionfish's invaded range.

Spatial and temporal patterns of larval dispersal in a coral-reef fish metapopulation: evidence of variable reproductive success.

Many marine organisms can be transported hundreds of kilometres during their pelagic larval stage, yet little is known about spatial and temporal patterns of larval dispersal. Although traditional population-genetic tools can be applied to infer movement of larvae on an evolutionary timescale, large effective population sizes and high rates of gene flow present serious challenges to documenting dispersal patterns over shorter, ecologically relevant, timescales. Here, we address these challenges by combining direct parentage analysis and indirect genetic analyses over a 4-year period to document spatial and temporal patterns of larval dispersal in a common coral-reef fish: the bicolour damselfish (Stegastes partitus). At four island locations surrounding Exuma Sound, Bahamas, including a long-established marine reserve, we collected 3278 individuals and genotyped them at 10 microsatellite loci. Using Bayesian parentage analysis, we identified eight parent-offspring pairs, thereby directly documenting dispersal distances ranging from 0 km (i.e., self-recruitment) to 129 km (i.e., larval connectivity). Despite documenting substantial dispersal and gene flow between islands, we observed more self-recruitment events than expected if the larvae were drawn from a common, well-mixed pool (i.e., a completely open population). Additionally, we detected both spatial and temporal variation in signatures of sweepstakes and Wahlund effects. The high variance in reproductive success (i.e., 'sweepstakes') we observed may be influenced by seasonal mesoscale gyres present in the Exuma Sound, which play a prominent role in shaping local oceanographic patterns. This study documents the complex nature of larval dispersal in a coral-reef fish, and highlights the importance of sampling multiple cohorts and coupling both direct and indirect genetic methods in order disentangle patterns of dispersal, gene flow and variable reproductive success.

Low susceptibility of invasive red lionfish (Pterois volitans) to a generalist ectoparasite in both its introduced and native ranges.

Escape from parasites in their native range is one of many mechanisms that can contribute to the success of an invasive species. Gnathiid isopods are blood-feeding ectoparasites that infest a wide range of fish hosts, mostly in coral reef habitats. They are ecologically similar to terrestrial ticks, with the ability to transmit blood-borne parasites and cause damage or even death to heavily infected hosts. Therefore, being highly resistant or highly susceptible to gnathiids can have significant fitness consequences for reef-associated fishes. Indo-Pacific red lionfish (Pterois volitans) have invaded coastal habitats of the western tropical and subtropical Atlantic and Caribbean regions. We assessed the susceptibility of red lionfish to parasitic gnathiid isopods in both their native Pacific and introduced Atlantic ranges via experimental field studies during which lionfish and other, ecologically-similar reef fishes were caged and exposed to gnathiid infestation on shallow coral reefs. Lionfish in both ranges had very few gnathiids when compared with other species, suggesting that lionfish are not highly susceptible to infestation by generalist ectoparasitic gnathiids. While this pattern implies that release from gnathiid infestation is unlikely to contribute to the success of lionfish as invaders, it does suggest that in environments with high gnathiid densities, lionfish may have an advantage over species that are more susceptible to gnathiids. Also, because lionfish are not completely resistant to gnathiids, our results suggest that lionfish could possibly have transported blood parasites between their native Pacific and invaded Atlantic ranges.

Functional responses and scaling in predator-prey interactions of marine fishes: contemporary issues and emerging concepts.

Predator-prey interactions are a primary structuring force vital to the resilience of marine communities and sustainability of the world's oceans. Human influences on marine ecosystems mediate changes in species interactions. This generality is evinced by the cascading effects of overharvesting top predators on the structure and function of marine ecosystems. It follows that ecological forecasting, ecosystem management, and marine spatial planning require a better understanding of food web relationships. Characterising and scaling predator-prey interactions for use in tactical and strategic tools (i.e. multi-species management and ecosystem models) are paramount in this effort. Here, we explore what issues are involved and must be considered to advance the use of predator-prey theory in the context of marine fisheries science. We address pertinent contemporary ecological issues including (1) the approaches and complexities of evaluating predator responses in marine systems; (2) the 'scaling up' of predator-prey interactions to the population, community, and ecosystem level; (3) the role of predator-prey theory in contemporary fisheries and ecosystem modelling approaches; and (4) directions for the future. Our intent is to point out needed research directions that will improve our understanding of predator-prey interactions in the context of the sustainable marine fisheries and ecosystem management.

Genetic correlations between adults and larvae in a marine fish: potential effects of fishery selection on population replenishment.

Correlated genetic responses have been hypothesized as important components of fishery-induced evolution, although predictive data from wild populations have been difficult to obtain. Here, we demonstrate substantial genetic correlations between a trait often subjected to fishery selection (adult body length) and traits that affect survival of larvae (length and swimming performance) in a wild population of a marine fish (bicolor damselfish, Stegastes partitus). Through both genetic covariance and size-dependent maternal effects, selection on adult size may cause a considerable, correlated response in larval traits. To quantify how variation in larval traits may affect survival, we introduce a flexible method that uses information from selection measurements to account for frequency dependence and estimate the relationship between phenotype and relative survival across a broad range of phenotypic values. Using this method, we synthesize studies of selective mortality on larval size for eight species of fish and show that variation in larval size may result in considerable variation in larval survival. We predict that observed rates of fishery selection on adult marine fishes may substantially reduce larval size and survival. The evolution of smaller larvae in response to fishery selection may therefore have substantial consequences for the viability of fished populations.

Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish.

Identifying patterns of larval dispersal within marine metapopulations is vital for effective fisheries management, appropriate marine reserve design, and conservation efforts. We employed genetic markers (microsatellites) to determine dispersal patterns in bicolour damselfish (Pomacentridae: Stegastes partitus). Tissue samples of 751 fish were collected in 2004 and 2005 from 11 sites encompassing the Exuma Sound, Bahamas. Bayesian parentage analysis identified two parent-offspring pairs, which is remarkable given the large population sizes and 28 day pelagic larval duration of bicolour damselfish. The two parent-offspring pairs directly documented self-recruitment at the two northern-most sites, one of which is a long-established marine reserve. Principal coordinates analyses of pair-wise relatedness values further indicated that self-recruitment was common in all sampled populations. Nevertheless, measures of genetic differentiation (F(ST)) and results from assignment methods suggested high levels of gene flow among populations. Comparisons of heterozygosity and relatedness among samples of adults and recruits indicated spatially and temporally independent sweepstakes events, whereby only a subset of adults successfully contribute to subsequent generations. These results indicate that self-recruitment and sweepstakes reproduction are the predominant, ecologically-relevant processes that shape patterns of larval dispersal in this system.

Larval connectivity in an effective network of marine protected areas.

Acceptance of marine protected areas (MPAs) as fishery and conservation tools has been hampered by lack of direct evidence that MPAs successfully seed unprotected areas with larvae of targeted species. For the first time, we present direct evidence of large-scale population connectivity within an existing and effective network of MPAs. A new parentage analysis identified four parent-offspring pairs from a large, exploited population of the coral-reef fish Zebrasoma flavescens in Hawai'i, revealing larval dispersal distances ranging from 15 to 184 km. In two cases, successful dispersal was from an MPA to unprotected sites. Given high adult abundances, the documentation of any parent-offspring pairs demonstrates that ecologically-relevant larval connectivity between reefs is substantial. All offspring settled at sites to the north of where they were spawned. Satellite altimetry and oceanographic models from relevant time periods indicated a cyclonic eddy that created prevailing northward currents between sites where parents and offspring were found. These findings empirically demonstrate the effectiveness of MPAs as useful conservation and management tools and further highlight the importance of coupling oceanographic, genetic, and ecological data to predict, validate and quantify larval connectivity among marine populations.

Biodiversity, population regulation, and the stability of coral-reef fish communities.

Unprecedented population declines and extinctions because of human activities, combined with a growing recognition that such losses affect the stability of ecosystems, underscore the need to better understand how populations persist naturally. We provide field experimental evidence that high biodiversity-in particular, the combined effects of predators and competitors-acts in a way that regulates the size of local fish populations within their coral-reef community. These results indicate that complex interactions among multiple species are necessary for the stability of a highly diverse community, and so forewarn that overexploiting such species may have cascading negative consequences for the entire system.

Food ration and condition affect early survival of the coral reef damselfish, Stegastes partitus.

The supply of larvae is a major determinant of population and community structure in coral reef fishes. However, spatial and temporal variation in condition (i.e. quality) of potential recruits, as well as their density (i.e. quantity), may influence survival and growth of juveniles. We conducted an experiment to test whether recent feeding history could affect growth, condition and post-recruitment survival in a Caribbean damselfish, Stegastes partitus. Fish were collected soon after settlement, and fed either low or high rations in aquaria for 7 days. Fish fed the high ration grew faster in aquaria and were in a better condition (higher total lipids and Fulton's condition factor) at the end of the feeding period. Subsequently, we released 50 fish in 25 pairs (one fish subjected to low rations, the other to high rations) on a Bahamian coral reef and monitored survival for 10 days. Survivorship of high-ration fish was double that of low-ration fish (80 vs 40% over 10 days). However, low-ration fish that survived 10 days were of similar condition and grew at similar rates to high-ration fish, suggesting that short-term ration differences may not persist in surviving fish. Laboratory experiments showed that low-ration fish were taken by piscivorous fishes before high-ration fish, indicating that differential predation may account for survival differences. This study highlights the potential of feeding history and condition to affect the relationship between patterns of larval arrival at reefs, and subsequent juvenile and adult population densities.