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.

Stream and ocean hydrodynamics mediate partial migration strategies in an amphidromous Hawaiian goby.

Partial migration strategies, in which some individuals migrate but others do not, are widely observed in populations of migratory animals. Such patterns could arise via variation in migratory behaviors made by individual animals, via genetic variation in migratory predisposition, or simply by variation in migration opportunities mediated by environmental conditions. Here we use spatiotemporal variation in partial migration across populations of an amphidromous Hawaiian goby to test whether stream or ocean conditions favor completing its life cycle entirely within freshwater streams rather than undergoing an oceanic larval migration. Across 35 watersheds, microchemical analysis of otoliths revealed that most adult Awaous stamineus were freshwater residents (62% of n = 316 in 2009, 83% of n = 274 in 2011), but we found considerable variation among watersheds. We then tested the hypothesis that the prevalence of freshwater residency increases with the stability of stream flows and decreases with the availability of dispersal pathways arising from ocean hydrodynamics. We found that streams with low variation of daily discharge were home to a higher incidence of freshwater residents in each survey year. The magnitude of the shift in freshwater residency between survey years was positively associated with predicted interannual variability in the success of larval settlement in streams on each island based on passive drift in ocean currents. We built on these findings by developing a theoretical model of goby life history to further evaluate whether mediation of migration outcomes by stream and ocean hydrodynamics could be sufficient to explain the range of partial migration frequency observed across populations. The model illustrates that the proportion of larvae entering the ocean and differential survival of freshwater-resident versus ocean-going larvae are plausible mechanisms for range-wide shifts in migration strategies. Thus, we propose that hydrologic variation in both ocean and stream environments contributes to spatiotemporal variation in the prevalence of migration phenotypes in A. stamineus. Our empirical and theoretical results suggest that the capacity for partial migration could enhance the persistence of metapopulations of diadromous fish when confronted with variable ocean and stream conditions.

Evidence of local adaptation in a waterfall-climbing Hawaiian goby fish derived from coupled biophysical modeling of larval dispersal and post-settlement selection.

BACKGROUND: Local adaptation of marine and diadromous species is thought to be a product of larval dispersal, settlement mortality, and differential reproductive success, particularly in heterogeneous post-settlement habitats. We evaluated this premise with an oceanographic passive larval dispersal model coupled with individual-based models of post-settlement selection and reproduction to infer conditions that underlie local adaptation in Sicyopterus stimpsoni, an amphidromous Hawaiian goby known for its ability to climb waterfalls. RESULTS: Our model results demonstrated that larval dispersal is spatio-temporally asymmetric, with more larvae dispersed from the southeast (the Big Island) to northwest (Kaua'i) along the archipelago, reflecting prevailing conditions such as El Niño/La Niña oscillations. Yet connectivity is nonetheless sufficient to result in homogenous populations across the archipelago. We also found, however, that ontogenetic shifts in habitat can give rise to adaptive morphological divergence when the strength of predation-driven post-settlement selection crosses a critical threshold. Notably, our simulations showed that larval dispersal is not the only factor determining the likelihood of morphological divergence. We found adaptive potential and evolutionary trajectories of S. stimpsoni were greater on islands with stronger environmental gradients and greater variance in larval cohort morphology due to fluctuating immigration. CONCLUSIONS: Contrary to expectation, these findings indicate that immigration can act in concert with selection to favor local adaptation and divergence in species with marine larval dispersal. Further development of model simulations, parameterized to reflect additional empirical estimates of abiotic and biotic factors, will help advance our understanding of the proximate and ultimate mechanisms driving adaptive evolution, population resilience, and speciation in marine-associated species.

Modeled Population Connectivity across the Hawaiian Archipelago.

We present the first comprehensive estimate of connectivity of passive pelagic particles released from coral reef habitat throughout the Hawaiian Archipelago. Potential connectivity is calculated using a Lagrangian particle transport model coupled offline with currents generated by an oceanographic circulation model, MITgcm. The connectivity matrices show a surprising degree of self-recruitment and directional dispersal towards the northwest, from the Main Hawaiian Islands (MHI) to the northwestern Hawaiian Islands (NWHI). We identify three predicted connectivity breaks in the archipelago, that is, areas in the mid and northern part of the archipelago that have limited connections with surrounding islands and reefs. Predicted regions of limited connectivity generally match observed patterns of genetic structure reported for coral reef species in the uninhabited NWHI, but multiple genetic breaks observed in the inhabited MHI are not explained by passive dispersal. The better congruence in our modeling results based on physical transport of passive particles in the low-lying atolls of the uninhabited NWHI, but not in the anthropogenically impacted high islands of the MHI begs the question: what ultimately controls connectivity in this system?

The DNA of coral reef biodiversity: predicting and protecting genetic diversity of reef assemblages.

Conservation of ecological communities requires deepening our understanding of genetic diversity patterns and drivers at community-wide scales. Here, we use seascape genetic analysis of a diversity metric, allelic richness (AR), for 47 reef species sampled across 13 Hawaiian Islands to empirically demonstrate that large reefs high in coral cover harbour the greatest genetic diversity on average. We found that a species's life history (e.g. depth range and herbivory) mediates response of genetic diversity to seascape drivers in logical ways. Furthermore, a metric of combined multi-species AR showed strong coupling to species richness and habitat area, quality and stability that few species showed individually. We hypothesize that macro-ecological forces and species interactions, by mediating species turnover and occupancy (and thus a site's mean effective population size), influence the aggregate genetic diversity of a site, potentially allowing it to behave as an apparent emergent trait that is shaped by the dominant seascape drivers. The results highlight inherent feedbacks between ecology and genetics, raise concern that genetic resilience of entire reef communities is compromised by factors that reduce coral cover or available habitat, including thermal stress, and provide a foundation for new strategies for monitoring and preserving biodiversity of entire reef ecosystems.

Exploration of the "larval pool": development and ground-truthing of a larval transport model off leeward Hawai'i.

Most adult reef fish show site fidelity thus dispersal is limited to the mobile larval stage of the fish, and effective management of such species requires an understanding of the patterns of larval dispersal. In this study, we assess larval reef fish distributions in the waters west of the Big Island of Hawai'i using both in situ and model data. Catches from Cobb midwater trawls off west Hawai'i show that reef fish larvae are most numerous in offshore waters deeper than 3,000 m and consist largely of pre-settlement Pomacanthids, Acanthurids and Chaetodontids. Utilizing a Lagrangian larval dispersal model, we were able to replicate the observed shore fish distributions from the trawl data and we identified the 100 m depth strata as the most likely depth of occupancy. Additionally, our model showed that for larval shore fish with a pelagic larval duration longer than 40 days there was no significant change in settlement success in our model. By creating a general additive model (GAM) incorporating lunar phase and angle we were able to explain 67.5% of the variance between modeled and in situ Acanthurid abundances. We took steps towards creating a predictive larval distribution model that will greatly aid in understanding the spatiotemporal nature of the larval pool in west Hawai'i, and the dispersal of larvae throughout the Hawaiian archipelago.