Simon R. Thorrold

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.

Larval dispersal connects fish populations in a network of marine protected areas

Networks of no-take marine protected areas (MPAs) have been widely advocated for the conservation of marine biodiversity. But for MPA networks to be successful in protecting marine populations, individual MPAs must be self-sustaining or adequately connected to other MPAs via dispersal. For marine species with a dispersive larval stage, populations within MPAs require either the return of settlement-stage larvae to their natal reserve or connectivity among reserves at the spatial scales at which MPA networks are implemented. To date, larvae have not been tracked when dispersing from one MPA to another, and the relative magnitude of local retention and connectivity among MPAs remains unknown. Here we use DNA parentage analysis to provide the first direct estimates of connectivity of a marine fish, the orange clownfish (Amphiprion percula), in a proposed network of marine reserves in Kimbe Bay, Papua New Guinea. Approximately 40% of A. percula larvae settling into anemones in an island MPA at 2 different times were derived from parents resident in the reserve. We also located juveniles spawned by Kimbe Island residents that had dispersed as far as 35 km to other proposed MPAs, the longest distance that marine larvae have been directly tracked. These dispersers accounted for up to 10% of the recruitment in the adjacent MPAs. Our findings suggest that MPA networks can function to sustain resident populations both by local replenishment and through larval dispersal from other reserves. More generally, DNA parentage analysis provides a direct method for measuring larval dispersal for other marine organisms.

Larval export from marine reserves and the recruitment benefit for fish and fisheries

Marine reserves, areas closed to all forms of fishing, continue to be advocated and implemented to supplement fisheries and conserve populations. However, although the reproductive potential of important fishery species can dramatically increase inside reserves, the extent to which larval offspring are exported and the relative contribution of reserves to recruitment in fished and protected populations are unknown. Using genetic parentage analyses, we resolve patterns of larval dispersal for two species of exploited coral reef fish within a network of marine reserves on the Great Barrier Reef. In a 1,000 km(2) study area, populations resident in three reserves exported 83% (coral trout, Plectropomus maculatus) and 55% (stripey snapper, Lutjanus carponotatus) of assigned offspring to fished reefs, with the remainder having recruited to natal reserves or other reserves in the region. We estimate that reserves, which account for just 28% of the local reef area, produced approximately half of all juvenile recruitment to both reserve and fished reefs within 30 km. Our results provide compelling evidence that adequately protected reserve networks can make a significant contribution to the replenishment of populations on both reserve and fished reefs at a scale that benefits local stakeholders.

Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs.

Design and decision-making for marine protected areas (MPAs) on coral reefs require prediction of MPA effects with population models. Modeling of MPAs has shown how the persistence of metapopulations in systems of MPAs depends on the size and spacing of MPAs, and levels of fishing outside the MPAs. However, the pattern of demographic connectivity produced by larval dispersal is a key uncertainty in those modeling studies. The information required to assess population persistence is a dispersal matrix containing the fraction of larvae traveling to each location from each location, not just the current number of larvae exchanged among locations. Recent metapopulation modeling research with hypothetical dispersal matrices has shown how the spatial scale of dispersal, degree of advection versus diffusion, total larval output, and temporal and spatial variability in dispersal influence population persistence. Recent empirical studies using population genetics, parentage analysis, and geochemical and artificial marks in calcified structures have improved the understanding of dispersal. However, many such studies report current self-recruitment (locally produced settlement/settlement from elsewhere), which is not as directly useful as local retention (locally produced settlement/total locally released), which is a component of the dispersal matrix. Modeling of biophysical circulation with larval particle tracking can provide the required elements of dispersal matrices and assess their sensitivity to flows and larval behavior, but it requires more assumptions than direct empirical methods. To make rapid progress in understanding the scales and patterns of connectivity, greater communication between empiricists and population modelers will be needed. Empiricists need to focus more on identifying the characteristics of the dispersal matrix, while population modelers need to track and assimilate evolving empirical results.

Estimating connectivity in marine populations: an empirical evaluation of assignment tests and parentage analysis under different gene flow scenarios

The application of spatially explicit models of population dynamics to fisheries management and the design marine reserve network systems has been limited due to a lack of empirical estimates of larval dispersal. Here we compared assignment tests and parentage analysis for examining larval retention and connectivity under two different gene flow scenarios using panda clownfish (Amphiprion polymnus) in Papua New Guinea. A metapopulation of panda clownfish in Bootless Bay with little or no genetic differentiation among five spatially discrete locations separated by 2–6 km provided the high gene flow scenario. The low gene flow scenario compared the Bootless Bay metapopulation with a genetically distinct population (FST = 0.1) located at Schumann Island, New Britain, 1500 km to the northeast. We used assignment tests and parentage analysis based on microsatellite DNA data to identify natal origins of 177 juveniles in Bootless Bay and 73 juveniles at Schumann Island. At low rates of gene flow, assignment tests correctly classified juveniles to their source population. On the other hand, parentage analysis led to an overestimate of self‐recruitment within the two populations due to the significant deviation from panmixia when both populations were pooled. At high gene flow (within Bootless Bay), assignment tests underestimated self‐recruitment and connectivity among subpopulations, and grossly overestimated self‐recruitment within the overall metapopulation. However, the assignment tests did identify immigrants from distant (genetically distinct) populations. Parentage analysis clearly provided the most accurate estimates of connectivity in situations of high gene flow.

Coral reef fish smell leaves to find island homes

Recent studies have shown that some coral reef fish larvae return to natal reefs, while others disperse to distant reefs. However, the sensory mechanisms used to find settlement sites are poorly understood. One hypothesis is that larvae use olfactory cues to navigate home or find other suitable reef habitats. Here we show a strong association between the clownfish Amphiprion percula and coral reefs surrounding offshore islands in Papua New Guinea. Host anemones and A. percula are particularly abundant in shallow water beneath overhanging rainforest vegetation. A series of experiments were carried out using paired-choice flumes to evaluate the potential role of water-borne olfactory cues in finding islands. Recently settled A. percula exhibited strong preferences for: (i) water from reefs with islands over water from reefs without islands; (ii) water collected near islands over water collected offshore; and (iii) water treated with either anemones or leaves from rainforest vegetation. Laboratory reared-juveniles exhibited the same positive response to anemones and rainforest vegetation, suggesting that olfactory preferences are innate rather than learned. We hypothesize that A. percula use a suite of olfactory stimuli to locate vegetated islands, which may explain the high levels of self-recruitment on island reefs. This previously unrecognized link between coral reefs and island vegetation argues for the integrated management of these pristine tropical habitats.

Persistence of self‐recruitment and patterns of larval connectivity in a marine protected area network

The use of marine protected area (MPA) networks to sustain fisheries and conserve biodiversity is predicated on two critical yet rarely tested assumptions. Individual MPAs must produce sufficient larvae that settle within that reserves boundaries to maintain local populations while simultaneously supplying larvae to other MPA nodes in the network that might otherwise suffer local extinction. Here, we use genetic parentage analysis to demonstrate that patterns of self-recruitment of two reef fishes (Amphiprion percula and Chaetodon vagabundus) in an MPA in Kimbe Bay, Papua New Guinea, were remarkably consistent over several years. However, dispersal from this reserve to two other nodes in an MPA network varied between species and through time. The stability of our estimates of self-recruitment suggests that even small MPAs may be self-sustaining. However, our results caution against applying optimization strategies to MPA network design without accounting for variable connectivity among species and over time.

Connectivity dominates larval replenishment in a coastal reef fish metapopulation

Direct estimates of larval retention and connectivity are essential to understand the structure and dynamics of marine metapopulations, and optimize the size and spacing of reserves within networks of marine-protected areas (MPAs). For coral reef fishes, while there are some empirical estimates of self-recruitment at isolated populations, exchange among sub-populations has been rarely quantified. Here, we used microsatellite DNA markers and a likelihood-based parentage analysis to assess the relative magnitude of self-recruitment and exchange among eight geographically distinct sub-populations of the panda clownfish Amphiprion polymnus along 30 km of coastline near Port Moresby, Papua New Guinea. In addition, we used an assignment/exclusion test to identify immigrants arriving from genetically distinct sources. Overall, 82 per cent of the juveniles were immigrants while 18 per cent were progeny of parents genotyped in our focal metapopulation. Of the immigrants, only 6 per cent were likely to be genetically distinct from the focal metapopulation, suggesting most of the connectivity is among sub-populations from a rather homogeneous genetic pool. Of the 18 per cent that were progeny of known adults, two-thirds dispersed among the eight sub-populations and only one-third settled back into natal sub-populations. Comparison of our data with previous studies suggested that variation in dispersal distances is likely to be influenced by the geographical setting and spacing of sub-populations.

Geochemical Signatures in Otoliths Record Natal Origins of American Shad

Abstract Population connectivity is a critical component in the life history dynamics of anadromous fishes and in the persistence of local populations. We used geochemical signatures in the otoliths of American shad Alosa sapidissima to determine natal origins and estimate rates of straying among river-specific populations along the U.S. Atlantic coast. Stable isotope (δ13C, δ18O and 87Sr:86Sr) and elemental (Mg: Ca, Mn: Ca, Sr: Ca and Ba: Ca) signatures in otoliths of juvenile American shad from rivers from Georgia to New Hampshire varied significantly, allowing for an average of 91% cross-validated accuracy when classifying individual fish to their natal rivers. We also found significant interannual variability in the geochemical signatures from several rivers, due largely to differences in δ18O values among years. We then used the ground-truthed geochemical signatures in the otoliths of juvenile American shad to identify the natal origins of spawning adults in the York River system in Virginia. Approxi...

Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein.

1. Analysis of stable carbon isotopes is a valuable tool for studies of diet, habitat use and migration. However, significant variability in the degree of trophic fractionation (Delta(13)C(C-D)) between consumer (C) and diet (D) has highlighted our lack of understanding of the biochemical and physiological underpinnings of stable isotope ratios in tissues. 2. An opportunity now exists to increase the specificity of dietary studies by analyzing the delta(13)C values of amino acids (AAs). Common mummichogs (Fundulus heteroclitus, Linnaeus 1766) were reared on four isotopically distinct diets to examine individual AA Delta(13)C(C-D) variability in fish muscle. 3. Modest bulk tissue Delta(13)C(C-D) values reflected relatively large trophic fractionation for many non-essential AAs and little to no fractionation for all essential AAs. 4. Essential AA delta(13)C values were not significantly different between diet and consumer (Delta(13)C(C-D) = 0.0 +/- 0.4 per thousand), making them ideal tracers of carbon sources at the base of the food web. Stable isotope analysis of muscle essential AAs provides a promising tool for dietary reconstruction and identifying baseline delta(13)C values to track animal movement through isotopically distinct food webs. 5. Non-essential AA Delta(13)C(C-D) values showed evidence of both de novo biosynthesis and direct isotopic routing from dietary protein. We attributed patterns in Delta(13)C(C-D) to variability in protein content and AA composition of the diet as well as differential utilization of dietary constituents contributing to the bulk carbon pool. This variability illustrates the complicated nature of metabolism and suggests caution must be taken with the assumptions used to interpret bulk stable isotope data in dietary studies. 6. Our study is the first to investigate the expression of AA Delta(13)C(C-D) values for a marine vertebrate and should provide for significant refinements in studies of diet, habitat use and migration using stable isotopes.