Strengthened currents override the effect of warming on lobster larval dispersal and survival

Human‐induced climate change is projected to increase ocean temperature and modify circulation patterns, with potential widespread implications for the transport and survival of planktonic larvae of marine organisms. Circulation affects the dispersal of larvae, whereas temperature impacts larval development and survival. However, the combined effect of changes in circulation and temperature on larval dispersal and survival has rarely been studied in a future climate scenario. Such understanding is crucial to predict future species distributions, anticipate ecosystem shifts and design effective management strategies. We simulate contemporary (1990s) and future (2060s) dispersal of lobster larvae using an eddy‐resolving ocean model in south‐eastern Australia, a region of rapid ocean warming. Here we show that the effects of changes in circulation and temperature can counter each other: ocean warming favours the survival of lobster larvae, whereas a strengthened western boundary current diminishes the supply of larvae to the coast by restricting cross‐current larval dispersal. Furthermore, we find that changes in circulation have a stronger effect on connectivity patterns of lobster larvae along south‐eastern Australia than ocean warming in the future climate so that the supply of larvae to the coast reduces by ~4% and the settlement peak shifts poleward by ~270 km in the model simulation. Thus, ocean circulation may be one of the dominant factors contributing to climate‐induced changes of species ranges.     

Biophysical connectivity explains population genetic structure in a highly dispersive marine species

Connectivity, the exchange of individuals among locations, is a fundamental ecological process that explains how otherwise disparate populations interact. For most marine organisms, dispersal occurs primarily during a pelagic larval phase that connects populations. We paired population structure from comprehensive genetic sampling and biophysical larval transport modeling to describe how spiny lobster (Panulirus argus) population differentiation is related to biological oceanography. A total of 581 lobsters were genotyped with 11 microsatellites from ten locations around the greater Caribbean. The overall F _ST of 0.0016 (P = 0.005) suggested low yet significant levels of structuring among sites. An isolation by geographic distance model did not explain spatial patterns of genetic differentiation in P. argus (P = 0.19; Mantel r = 0.18), whereas a biophysical connectivity model provided a significant explanation of population differentiation (P = 0.04; Mantel r = 0.47). Thus, even for a widely dispersing species, dispersal occurs over a continuum where basin-wide larval retention creates genetic structure. Our study provides a framework for future explorations of wide-scale larval dispersal and marine connectivity by integrating empirical genetic research and probabilistic modeling.

     

Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow

Understanding patterns of connectivity among populations of marine organisms is essential for the development of realistic, spatially explicit models of population dynamics. Two approaches, empirical genetic patterns and oceanographic dispersal modelling, have been used to estimate levels of evolutionary connectivity among marine populations but rarely have their potentially complementary insights been combined. Here, a spatially realistic Lagrangian model of larval dispersal and a theoretical genetic model are integrated with the most extensive study of gene flow in a Caribbean marine organism. The 871 genets collected from 26 sites spread over the wider Caribbean subsampled 45.8% of the 1900 potential unique genets in the model. At a coarse scale, significant consensus between modelled estimates of genetic structure and empirical genetic data for populations of the reef-building coral Montastraea annularis is observed. However, modelled and empirical data differ in their estimates of connectivity among northern Mesoamerican reefs indicating that processes other than dispersal may dominate here. Further, the geographic location and porosity of the previously described east-west barrier to gene flow in the Caribbean is refined. A multi-prong approach, integrating genetic data and spatially realistic models of larval dispersal and genetic projection, provides complementary insights into the processes underpinning population connectivity in marine invertebrates on evolutionary timescales.     

Designing connected marine reserves in the face of global warming

Marine reserves are widely used to protect species important for conservation and fisheries and to help maintain ecological processes that sustain their populations, including recruitment and dispersal. Achieving these goals requires well‐connected networks of marine reserves that maximize larval connectivity, thus allowing exchanges between populations and recolonization after local disturbances. However, global warming can disrupt connectivity by shortening potential dispersal pathways through changes in larval physiology. These changes can compromise the performance of marine reserve networks, thus requiring adjusting their design to account for ocean warming. To date, empirical approaches to marine prioritization have not considered larval connectivity as affected by global warming. Here, we develop a framework for designing marine reserve networks that integrates graph theory and changes in larval connectivity due to potential reductions in planktonic larval duration (PLD) associated with ocean warming, given current socioeconomic constraints. Using the Gulf of California as case study, we assess the benefits and costs of adjusting networks to account for connectivity, with and without ocean warming. We compare reserve networks designed to achieve representation of species and ecosystems with networks designed to also maximize connectivity under current and future ocean‐warming scenarios. Our results indicate that current larval connectivity could be reduced significantly under ocean warming because of shortened PLDs. Given the potential changes in connectivity, we show that our graph‐theoretical approach based on centrality (eigenvector and distance‐weighted fragmentation) of habitat patches can help design better‐connected marine reserve networks for the future with equivalent costs. We found that maintaining dispersal connectivity incidentally through representation‐only reserve design is unlikely, particularly in regions with strong asymmetric patterns of dispersal connectivity. Our results support previous studies suggesting that, given potential reductions in PLD due to ocean warming, future marine reserve networks would require more and/or larger reserves in closer proximity to maintain larval connectivity.     

Population Genetics of a Trochid Gastropod Broadens Picture of Caribbean Sea Connectivity

Background

Regional genetic connectivity models are critical for successful conservation and management of marine species. Even though rocky shore invertebrates have been used as model systems to understand genetic structure in some marine environments, our understanding of connectivity in Caribbean communities is based overwhelmingly on studies of tropical fishes and corals. In this study, we investigate population connectivity and diversity of Cittarium pica, an abundant rocky shore trochid gastropod that is commercially harvested across its natural range, from the Bahamas to Venezuela.

Methodology/Principal Findings

We tested for genetic structure using DNA sequence variation at the mitochondrial COI and 16S loci, AMOVA and distance-based methods. We found substantial differentiation among Caribbean sites. Yet, genetic differentiation was associated only with larger geographic scales within the Caribbean, and the pattern of differentiation only partially matched previous assessments of Caribbean connectivity, including those based on larval dispersal from hydrodynamic models. For instance, the Bahamas, considered an independent region by previous hydrodynamic studies, showed strong association with Eastern Caribbean sites in our study. Further, Bonaire (located in the east and close to the meridional division of the Caribbean basin) seems to be isolated from other Eastern sites.

Conclusions/Significance

The significant genetic structure and observed in C. pica has some commonalities in pattern with more commonly sampled taxa, but presents features, such as the differentiation of Bonaire, that appear unique. Further, the level of differentiation, together with regional patterns of diversity, has important implications for the application of conservation and management strategies in this commercially harvested species.     

Coalescent and biophysical models of stepping‐stone gene flow in neritid snails

Marine species in the Indo‐Pacific have ranges that can span thousands of kilometres, yet studies increasingly suggest that mean larval dispersal distances are less than historically assumed. Gene flow across these ranges must therefore rely to some extent on larval dispersal among intermediate ‘stepping‐stone’ populations in combination with long‐distance dispersal far beyond the mean of the dispersal kernel. We evaluate the strength of stepping‐stone dynamics by employing a spatially explicit biophysical model of larval dispersal in the tropical Pacific to construct hypotheses for dispersal pathways. We evaluate these hypotheses with coalescent models of gene flow among high‐island archipelagos in four neritid gastropod species. Two of the species live in the marine intertidal, while the other two are amphidromous, living in fresh water but retaining pelagic dispersal. Dispersal pathways predicted by the biophysical model were strongly favoured in 16 of 18 tests against alternate hypotheses. In regions where connectivity among high‐island archipelagos was predicted as direct, there was no difference in gene flow between marine and amphidromous species. In regions where connectivity was predicted through stepping‐stone atolls only accessible to marine species, gene flow estimates between high‐island archipelagos were significantly higher in marine species. Moreover, one of the marine species showed a significant pattern of isolation by distance consistent with stepping‐stone dynamics. While our results support stepping‐stone dynamics in Indo‐Pacific species, we also see evidence for nonequilibrium processes such as range expansions or rare long‐distance dispersal events. This study couples population genetic and biophysical models to help to shed light on larval dispersal pathways.     

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.     

Reduced genetic diversity and increased reproductive isolation follow population‐level loss of larval dispersal in a marine gastropod

Population‐level consequences of dispersal ability remain poorly understood, especially for marine animals in which dispersal is typically considered a species‐level trait governed by oceanographic transport of microscopic larvae. Transitions from dispersive (planktotrophic) to nondispersive, aplanktonic larvae are predicted to reduce connectivity, genetic diversity within populations, and the spatial scale at which reproductive isolation evolves. However, larval dimorphism within a species is rare, precluding population‐level tests. We show the sea slug Costasiella ocellifera expresses both larval morphs in Florida and the Caribbean, regions with divergent mitochondrial lineages. Planktotrophy predominated at 11 sites, 10 of which formed a highly connected and genetically diverse Caribbean metapopulation. Four populations expressed mainly aplanktonic development and had markedly reduced connectivity, and lower genetic diversity at one mitochondrial and six nuclear loci. Aplanktonic dams showed partial postzygotic isolation in most interpopulation crosses, regardless of genetic or geographic distance to the sire's source, suggesting that outbreeding depression affects fragmented populations. Dams from genetically isolated and neighboring populations also exhibited premating isolation, consistent with reinforcement contingent on historical interaction. By increasing self‐recruitment and genetic drift, the loss of dispersal may thus initiate a feedback loop resulting in the evolution of reproductive isolation over small spatial scales in the sea.     

Reproductive timing alters population connectivity in marine metapopulations

Populations of most marine organisms are connected by the dispersal of larval stages, with profound implications for marine conservation. Because of the extreme effort needed to empirically measure larval exchange, multispecies conservation efforts must estimate connectivity by extrapolation using taxonomy, adult distribution, life history, behavior, or phenology. Using a 6-year record of connectivity realized through trace-elemental fingerprinting of larval shells, we document the seasonal and interannual variability of larval exchange for two congeneric mussel species with overlapping but distinct distribution, life history, and reproduction timing. We reveal consistent autumn poleward movement and spring equatorward movement for both species, coincident with near-shore surface currents. However, because the major reproductive seasons differ, the dominant source-sink dynamics of these two congeneric species are nearly opposite. Consideration of present and future reproductive timing as altered by climate change is crucial to marine connectivity and conservation, especially for the numerous coastal areas subject to seasonal current reversals.     

Reproductive output and duration of the pelagic larval stage determine seascape-wide connectivity of marine populations

Connectivity among marine populations is critical for persistence of metapopulations, coping with climate change, and determining the geographic distribution of species. The influence of pelagic larval duration (PLD) on connectivity has been studied extensively, but relatively little is known about the influence of other biological parameters, such as the survival and behavior of larvae, and the fecundity of adults, on population connectivity. Furthermore, the interaction between the seascape (habitat structure and currents) and these biological parameters is unclear. We explore these interactions using a biophysical model of larval dispersal across the Indo-Pacific. We describe an approach that quantifies geographic patterns of connectivity from demographically relevant to evolutionarily significant levels across a range of species. We predict that at least 95% of larval settlement occurs within 155?km of the source population and within 13 days irrespective of the species' life history, yet long-distant connections remain likely. Self-recruitment is primarily driven by the local oceanography, larval mortality, and the larval precompetency period, whereas broad-scale connectivity is strongly influenced by reproductive output (abundance and fecundity of adults) and the length of PLD. The networks we have created are geographically explicit models of marine connectivity that define dispersal corridors, barriers, and the emergent structure of marine populations. These models provide hypotheses for empirical testing.     

No Reef Is an Island: Integrating Coral Reef Connectivity Data into the Design of Regional-Scale Marine Protected Area Networks

We integrated coral reef connectivity data for the Caribbean and Gulf of Mexico into a conservation decision-making framework for designing a regional scale marine protected area (MPA) network that provides insight into ecological and political contexts. We used an ocean circulation model and regional coral reef data to simulate eight spawning events from 2008–2011, applying a maximum 30-day pelagic larval duration and 20% mortality rate. Coral larval dispersal patterns were analyzed between coral reefs across jurisdictional marine zones to identify spatial relationships between larval sources and destinations within countries and territories across the region. We applied our results in Marxan, a conservation planning software tool, to identify a regional coral reef MPA network design that meets conservation goals, minimizes underlying threats, and maintains coral reef connectivity. Our results suggest that approximately 77% of coral reefs identified as having a high regional connectivity value are not included in the existing MPA network. This research is unique because we quantify and report coral larval connectivity data by marine ecoregions and Exclusive Economic Zones (EZZ) and use this information to identify gaps in the current Caribbean-wide MPA network by integrating asymmetric connectivity information in Marxan to design a regional MPA network that includes important reef network connections. The identification of important reef connectivity metrics guides the selection of priority conservation areas and supports resilience at the whole system level into the future.     

Coral reef fish larvae settle close to home

Population connectivity through larval dispersal is an essential parameter in models of marine population dynamics and the optimal size and spacing of marine reserves. However, there are remarkably few direct estimates of larval dispersal for marine organisms, and the actual birth sites of successful recruits have never been located. Here, we solve the mystery of the natal origin of clownfish (Amphiprion polymnus) juveniles by mass-marking via tetracycline immersion all larvae produced in a population. In addition, we established parentage by DNA genotyping all potential adults and all new recruits arriving in the population. Although no individuals settled into the same anemone as their parents, many settled remarkably close to home. Even though this species has a 9-12 day larval duration, one-third of settled juveniles had returned to a 2 hectare natal area, with many settling <100 m from their birth site. This represents the smallest scale of dispersal known for any marine fish species with a pelagic larval phase. The degree of local retention indicates that marine reserves can provide recruitment benefits not only beyond but also within their boundaries.     

Kinship analyses identify fish dispersal events on a temperate coastline

Connectivity is crucial for the persistence and resilience of marine species, the establishment of networks of marine protected areas and the delineation of fishery management units. In the marine environment, understanding connectivity is still a major challenge, due to the technical difficulties of tracking larvae. Recently, parentage analysis has provided a means to address this question effectively. To be effective, this method requires limited adult movement and extensive sampling of parents, which is often not possible for marine species. An alternative approach that is less sensitive to constraints in parental movement and sampling could be the reconstruction of sibships. Here, we directly measure connectivity and larval dispersal in a temperate marine ecosystem through both analytical approaches. We use data from 178 single nucleotide polymorphism markers to perform parentage and sibship reconstruction of the black-faced blenny (Tripterygion delaisi) from an open coastline in the Mediterranean Sea. Parentage analysis revealed a decrease in dispersal success in the focal area over 1 km distance and approximately 6.5% of the juveniles were identified as self-recruits. Sibship reconstruction analysis found that, in general, full siblings did not recruit together to the same location, and that the largest distance between recruitment locations was much higher (11.5 km) than found for parent–offspring pairs (1.2 km). Direct measurements of dispersal are essential to understanding connectivity patterns in different marine habitats, and show the degree of self-replenishment and sustainability of populations of marine organisms. We demonstrate that sibship reconstruction allows direct measurements of dispersal and family structure in marine species while being more easily applied in those species for which the collection of the parental population is difficult or unfeasible.     

Influence of Biological Factors on Connectivity Patterns for Concholepas concholepas (loco) in Chile

In marine benthic ecosystems, larval connectivity is a major process influencing the maintenance and distribution of invertebrate populations. Larval connectivity is a complex process to study as it is determined by several interacting factors. Here we use an individual-based, biophysical model, to disentangle the effects of such factors, namely larval vertical migration, larval growth, larval mortality, adults fecundity, and habitat availability, for the marine gastropod Concholepas concholepas (loco) in Chile. Lower transport success and higher dispersal distances are observed including larval vertical migration in the model. We find an overall decrease in larval transport success to settlement areas from northern to southern Chile. This spatial gradient results from the combination of current direction and intensity, seawater temperature, and available habitat. From our simulated connectivity patterns we then identify subpopulations of loco along the Chilean coast, which could serve as a basis for spatial management of this resource in the future.     

Oceanographic features and limited dispersal shape the population genetic structure of the vase sponge Ircinia campana in the Greater Caribbean

Understanding population genetic structure can help us to infer dispersal patterns, predict population resilience and design effective management strategies. For sessile species with limited dispersal, this is especially pertinent because genetic diversity and connectivity are key aspects of their resilience to environmental stressors. Here, we describe the population structure of Ircinia campana, a common Caribbean sponge subject to mass mortalities and disease. Microsatellites were used to genotype 440 individuals from 19 sites throughout the Greater Caribbean. We found strong genetic structure across the region, and significant isolation by distance across the Lesser Antilles, highlighting the influence of limited larval dispersal. We also observed spatial genetic structure patterns congruent with oceanography. This includes evidence of connectivity between sponges in the Florida Keys and the southeast coast of the United States (>700 km away) where the oceanographic environment is dominated by the strong Florida Current. Conversely, the population in southern Belize was strongly differentiated from all other sites, consistent with the presence of dispersal-limiting oceanographic features, including the Gulf of Honduras gyre. At smaller spatial scales (<100 km), sites showed heterogeneous patterns of low-level but significant genetic differentiation (chaotic genetic patchiness), indicative of temporal variability in recruitment or local selective pressures. Genetic diversity was similar across sites, but there was evidence of a genetic bottleneck at one site in Florida where past mass mortalities have occurred. These findings underscore the relationship between regional oceanography and weak larval dispersal in explaining population genetic patterns, and could inform conservation management of the species.Subject terms: Genetic variation, Ecology     

Connectivity, sustainability, and yield: bridging the gap between conventional fisheries management and marine protected areas

A substantial shift toward use of marine protected areas (MPAs) for conservation and fisheries management is currently underway. This shift to explicit spatial management presents new challenges and uncertainties for ecologists and resource managers. In particular, the potential for MPAs to change population sustainability, fishery yield, and ecosystem properties depends on the poorly understood consequences of three critical forms of connectivity over space: larval dispersal, juvenile and adult swimming, and movement of fishermen. Conventional fishery management describes the dynamics and current status of fish populations, with increasing recent emphasis on sustainability, often through reference points that reflect individual replacement. These compare lifetime egg production (LEP) to a critical replacement threshold (CRT) whose value is uncertain. Sustainability of spatially distributed populations also depends on individual replacement, but through all possible paths created by larval dispersal and LEP at each location. Model calculations of spatial replacement considering larval connectivity alone indicate sustainability and yield depend on species dispersal distance and the distribution of LEP created by species habitat distribution and fishing mortality. Adding MPAs creates areas with high LEP, increasing sustainability, but not necessarily yield. Generally, short distance dispersers will persist in almost all MPAs, while sustainability of long distance dispersers requires a specific density of MPAs along the coast. The value of that density also depends on the uncertain CRT, as well as fishing rate. MPAs can increase yield in areas with previously low LEP but for short distance dispersers, high yields will require many small MPAs. The paucity of information on larval dispersal distances, especially in cases with strong advection, renders these projections uncertain. Adding juvenile and adult movement to these calculations reduces LEP near the edges in MPAs, if movement is within a home-range, but more broadly over space if movement is diffusive. Adding movement of fishermen shifts effort on the basis of anticipated revenues and fishing costs, leading to lower LEP near ports, for example. Our evolving understanding of connectivity in spatial management could form the basis for a new, spatially oriented replacement reference point for sustainability, with associated new uncertainties.     

Stretched to the limit; can a short pelagic larval duration connect adult populations of an Indo‐Pacific diadromous fish (Kuhlia rupestris)?

Freshwater species on tropical islands face localized extinction and the loss of genetic diversity. Their habitats can be ephemeral due to variability in freshwater run‐off and erosion. Even worse, anthropogenic effects on these ecosystems are intense. Most of these species are amphidromous or catadromous (i.e. their life cycle includes a marine larval phase), which buffers them against many of these effects. A long pelagic larval duration (PLD) was thought to be critical to ensure the colonization and persistence in tropical islands, but recent findings indicated that several species with short PLDs are successful in those ecosystems. To test the potential of a short PLD in maintaining genetic connectivity and forestalling extirpation, we studied Kuhlia rupestris, a catadromous fish species with an extensive distribution in the western Pacific and Indian Oceans. Using a combination of molecular genetic markers (13 microsatellite loci and two gene regions from mtDNA) and modelling of larval dispersal, we show that a short PLD constrains genetic connectivity over a wide geographical range. Molecular markers showed that the short PLD did not prevent genetic divergence through evolutionary time and speciation has occurred or is occurring. Modelling of larvae dispersal suggested limited recent connectivity between genetically homogeneous populations across the Coral Sea. However, a short PLD can maintain connectivity on a subocean basin scale. Conservation and management of tropical diadromous species needs to take into account that population connectivity may be more limited than previously suspected in those species.     

Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences

To help stem the precipitous decline of coral reef ecosystems world-wide, conservation efforts are focused on establishing interconnected reserve networks to protect threatened populations. Because many coral reef organisms have a planktonic or pelagic larval dispersal phase, it is critical to understand the patterns of ecological connectivity between reserve populations that result from larval dispersal. We used genetics to infer dispersal patterns among 24 Indo-West Pacific populations of the mantis shrimp, Haptosquilla pulchella. Contrary to predictions of high dispersal facilitated by the strong currents of the Indonesian throughflow, mitochondrial DNA sequences from 393 individuals displayed striking patterns of regional genetic differentiation concordant with ocean basins isolated during periods of lowered sea level. Patterns of genetic structuring indicate that although dispersal within geographical regions with semicontiguous coastlines spanning thousands of kilometres may be common, ecologically meaningful connections can be rare among populations separated by as little as 300 km of open ocean. Strong genetic mosaics in a species with high dispersal potential highlight the utility of genetics for identifying regional patterns of genetic connectivity between marine populations and show that the assumption that ocean currents will provide ecological connectivity among marine populations must be empirically tested in the design of marine reserve networks.     

Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish

The extent of dispersal by pelagic larvae in marine environments, including coral reefs, is central for understanding local population dynamics and designing sustainable marine reserves. We present here the first example of a clear stepping-stone genetic structure throughout the Caribbean basin for a common coral reef species, the French grunt (Haemulon flavolineatum). Analysis of microsatellite DNA markers indicated that French grunt population structure may be characterized by overlapping populations throughout the Caribbean, influenced by independent population dynamics but with no fixed geographical boundaries. In addition, different spatial genetic patterns were found in different oceanographic regions. A second species, the bluehead wrasse (Thalassoma bifasciatum), has a much longer pelagic larval duration than French grunts and showed no explicit spatial pattern of genetic variation. This finding is concordant with the hypothesis of a positive relationship between larval dispersal and duration in the plankton. While the magnitude of the genetic signal of population structure in French grunts was very low (F(ST) approximately 0.003), the pattern of isolation-by-distance throughout the Caribbean indicated considerable population structure with important ecological and conservation significance.     

Isolation and characterization of eight polymorphic microsatellite markers from pink conch (Strombus gigas)

Many marine organisms have pelagic larvae, and these are often important agents of dispersal. The larval phase and the multiple paternity that occur in marine gastropods such as Strombus gigas are crucial for the success of this species throughout the Caribbean Sea. To analyse these factors, we developed eight microsatellite loci specific to S. gigas. On the same set of individuals, the microsatellite loci exhibited a greater level of polymorphism than previously studied allozyme markers and thus, will permit fine‐scale analysis and larval pool studies.