Thorrold
Simon R.
Thorrold
Simon R.
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ArticleTransgenerational marking of embryonic otoliths in marine fishes using barium stable isotopes(NRC Research Press, 2006-04-13) Thorrold, Simon R. ; Jones, Geoffrey P. ; Planes, Serge ; Hare, Jonathan A.We describe a new technique for transgenerational marking of embryonic otoliths that promises significant advancements in the study of larval dispersal and population connectivity in marine fishes. The approach is based on maternal transmission of 137Ba from spawning females to egg material that is ultimately incorporated into the otoliths of embryos produced by an individual after exposure to the isotope. We injected females of a benthic-spawning clownfish (Amphiprion melanopus) and a pelagic-spawning serranid (Centropristis striata) with enriched 137BaCl2 and then reared the resulting progeny through to settlement. Barium isotope ratios in the cores of larval otoliths were quantified using laser ablation inductively coupled plasma mass spectrometry. Larval otoliths from both species contained unequivocal Ba isotope signatures over a wide range of doses (0.8–23 μg 137Ba·g female–1). Female A. melanopus continued to produce marked larvae over multiple clutches and for at least 90 days after a single injection. The ability to administer different combinations of stable Ba isotopes provides a new means of mass-marking larvae of benthic- and pelagic-spawning fishes from multiple populations over extended spawning periods.
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PreprintMarine dispersal scales are congruent over evolutionary and ecological time( 2016-10) Pinsky, Malin L. ; Saenz-Agudelo, Pablo ; Salles, Océane C. ; Almany, Glenn R. ; Bode, Michael ; Berumen, Michael L. ; Andrefouet, Serge ; Thorrold, Simon R. ; Jones, Geoffrey P. ; Planes, SergeThe degree to which offspring remain near their parents or disperse widely is critical for understanding population dynamics, evolution, and biogeography, and for designing conservation actions. In the ocean, most estimates suggesting short-distance dispersal are based on direct ecological observations of dispersing individuals, while indirect evolutionary estimates often suggest substantially greater homogeneity among populations. Reconciling these two approaches and their seemingly competing perspectives on dispersal has been a major challenge. However, here we show for the first time that evolutionary and ecological measures of larval dispersal can closely agree by using both to estimate the distribution of dispersal distances. In orange clownfish (Amphiprion percula) populations in Kimbe Bay, Papua New Guinea, we found that evolutionary dispersal kernels were 17 [95% CI: 12–24] km wide, while an exhaustive set of direct larval dispersal observations suggested kernel widths of 27 [19–36] km or 19 [15–27] km across two years. The similarity between these two approaches suggests that ecological and evolutionary dispersal kernels can be equivalent, and that the apparent disagreement between direct and indirect measurements can be overcome. Our results suggest that carefully applied evolutionary methods, which are often less expensive, can be broadly relevant for understanding ecological dispersal across the tree of life.
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PreprintConnectivity dominates larval replenishment in a coastal reef fish metapopulation( 2011-01-25) Saenz-Agudelo, Pablo ; Jones, Geoffrey P. ; Thorrold, Simon R. ; Planes, SergeDirect 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 8 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% of the juveniles were immigrants while 18% were progeny of parents genotyped in our focal metapopulation. Of the immigrants, only 6% 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% that were progeny of known adults, two thirds dispersed among the 8 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 geographic setting and spacing of sub-populations.
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ArticleSeascape and life-history traits do not predict self-recruitment in a coral reef fish(The Royal Society, 2016-08-09) Herrera, Marcela ; Nanninga, Gerrit ; Planes, Serge ; Jones, Geoffrey P. ; Thorrold, Simon R. ; Saenz-Agudelo, Pablo ; Almany, Glenn R. ; Berumen, Michael L.The persistence and resilience of many coral reef species are dependent on rates of connectivity among sub-populations. However, despite increasing research efforts, the spatial scale of larval dispersal remains unpredictable for most marine metapopulations. Here, we assess patterns of larval dispersal in the angelfish Centropyge bicolor in Kimbe Bay, Papua New Guinea, using parentage and sibling reconstruction analyses based on 23 microsatellite DNA loci. We found that, contrary to previous findings in this system, self-recruitment (SR) was virtually absent at both the reef (0.4–0.5% at 0.15 km2) and the lagoon scale (0.6–0.8% at approx. 700 km2). While approximately 25% of the collected juveniles were identified as potential siblings, the majority of sibling pairs were sampled from separate reefs. Integrating our findings with earlier research from the same system suggests that geographical setting and life-history traits alone are not suitable predictors of SR and that high levels of localized recruitment are not universal in coral reef fishes.
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PreprintOtolith geochemistry does not reflect dispersal history of clownfish larvae( 2010-06) Berumen, Michael L. ; Walsh, Harvey J. ; Raventos, N. ; Planes, Serge ; Jones, Geoffrey P. ; Starczak, Victoria R. ; Thorrold, Simon R.Natural geochemical signatures in calcified structures are commonly employed to retrospectively estimate dispersal pathways of larval fish and invertebrates. However, the accuracy of the approach is generally untested due to the absence of individuals with known dispersal histories. We used genetic parentage analysis (genotyping) to divide 110 new recruits of the orange clownfish, Amphiprion percula, from Kimbe Island, Papua New Guinea, into two groups: “self-recruiters” spawned by parents on Kimbe Island and “immigrants” that had dispersed from distant reefs (>10km away). Analysis of daily increments in sagittal otoliths found no significant difference in PLDs or otolith growth rates between self-recruiting and immigrant larvae. We also quantified otolith Sr/Ca and Ba/Ca ratios during the larval phase using laser ablation inductively coupled plasma mass spectrometry. Again, we found no significant differences in larval profiles of either element between self-recruits and immigrants. Our results highlight the need for caution when interpreting otolith dispersal histories based on natural geochemical tags in the absence of water chemistry data or known-origin larvae with which to test the discriminatory ability of natural tags.
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ArticleRank change and growth within social hierarchies of the orange clownfish, Amphiprion percula(Springer, 2022-10-05) Fitzgerald, Lucy M. ; Harrison, Hugo B. ; Coker, Darren J. ; Sáenz-Agudelo, Pablo ; Srinivasan, Maya ; Majoris, John E. ; Boström Einarsson, Lisa ; Pujol, Benoit ; Bennett-Smith, Morgan ; Thorrold, Simon R. ; Planes, Serge ; Jones, Geoffrey P. ; Berumen, Michale L.Social hierarchies within groups define the distribution of resources and provide benefits that support the collective group or favor dominant members. The progression of individuals through social hierarchies is a valuable characteristic for quantifying population dynamics. On coral reefs, some clownfish maintain size-based hierarchical communities where individuals queue through social ranks. The cost of waiting in a lower-ranked position is outweighed by the reduced risk of eviction and mortality. The orange clownfish,Amphiprion percula, maintains stable social groups with subordinate individuals queuing to be part of the dominant breeding pair. Strong association with their host anemone, complex social interactions, and relatively low predation rates make them ideal model organisms to assess changes in group dynamics through time in their natural environment. Here, we investigate the rank changes and isometric growth rates ofA. percula from 247 naturally occurring social groups in Kimbe Island, Papua New Guinea (5° 12′ 13.54″ S, 150° 22′ 32.69″ E). We used DNA profiling to assign and track individuals over eight years between 2011 and 2019. Over half of the individuals survived alongside two or three members of their original social group, with twelve breeding pairs persisting over the study period. Half of the surviving individuals increased in rank and experienced double the growth rate of those that maintained their rank. Examining rank change in a wild fish population provides new insights into the complex social hierarchies of reef fishes and their role in social evolution.
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PreprintFirst genealogy for a wild marine fish population reveals multi-generational philopatry( 2016-10) Salles, Océane C. ; Pujol, Benoit ; Maynard, Jeffrey A. ; Almany, Glenn R. ; Berumen, Michael L. ; Jones, Geoffrey P. ; Saenz-Agudelo, Pablo ; Srinivasan, Maya ; Thorrold, Simon R. ; Planes, SergeNatal philopatry — the return of individuals to their natal area for reproduction — has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation but may also increase the probability of inbreeding that can compromise persistence. While natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multi-generational pedigrees that are currently lacking for marine fishes. Here we present the first multi-generational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) over a 10-year period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multi-generational pedigrees over a relatively short time period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.
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PreprintEstimating connectivity in marine populations : an empirical evaluation of assignment tests and parentage analysis under different gene flow scenarios( 2008-11-21) Saenz-Agudelo, Pablo ; Jones, Geoffrey P. ; Thorrold, Simon R. ; Planes, SergeThe application of spatially explicit models of population dynamics to fisheries management and the design marine reserves 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 5 spatially discrete locations separated by 2-6km 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, 1,500km to the north-east. 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.
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PreprintCoral reef fish populations can persist without immigration( 2015-10) Salles, Océane C. ; Maynard, Jeffrey A. ; Joannides, Marc ; Barbu, Corentin M. ; Saenz-Agudelo, Pablo ; Almany, Glenn R. ; Berumen, Michael L. ; Thorrold, Simon R. ; Jones, Geoffrey P. ; Planes, SergeDetermining the conditions under which populations may persist requires accurate estimates of demographic parameters, including immigration, local reproductive success, and mortality rates. In marine populations, empirical estimates of these parameters are rare, due at least in part to the pelagic dispersal stage common to most marine organisms. Here, we evaluate population persistence and turnover for a population of orange clownfish, Amphiprion percula, at Kimbe Island in Papua New Guinea. All fish in the population were sampled and genotyped on five occasions at 2-year intervals spanning eight years. The genetic data enabled estimates of reproductive success retained in the same population (reproductive success to self-recruitment), reproductive success exported to other subpopulations (reproductive success to local connectivity), and immigration and mortality rates of sub-adults and adults. Approximately 50% of the recruits were assigned to parents from the Kimbe Island population and this was stable through the sampling period. Stability in the proportion of local and immigrant settlers is likely due to: low annual mortality rates and stable egg production rates, and the short larval stages and sensory capacities of reef fish larvae. Biannual mortality rates ranged from 0.09 to 0.55 and varied significantly spatially. We used these data to parameterize a model that estimated the probability of the Kimbe Island population persisting in the absence of immigration. The Kimbe Island population was found to persist without significant immigration. Model results suggest the island population persists because the largest of the subpopulations are maintained due to having low mortality and high self-recruitment rates. Our results enable managers to appropriately target and scale actions to maximize persistence likelihood as disturbance frequencies increase.
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PreprintHomogeneity of coral reef communities across 8 degrees of latitude in the Saudi Arabian Red Sea( 2015-11) Roberts, May B. ; Jones, Geoffrey P. ; McCormick, Mark I. ; Munday, Philip L. ; Neale, Stephen ; Thorrold, Simon R. ; Robitzch, Vanessa S. N. ; Berumen, Michael L.Coral reef communities between 26.8°N and 18.6°N latitude in the Saudi Arabian Red Sea were surveyed to provide baseline data and an assessment of fine-scale biogeography of communities in this region. Forty reefs along 1100 km of coastline were surveyed using depth-stratified visual transects of fish and benthic communities. Fish abundance and benthic cover data were analyzed using multivariate approaches to investigate whether coral reef communities differed with latitude. A total of 215 fish species and 90 benthic categories were recorded on the surveys. There were no significant differences among locations in fish abundance, species richness, or among several diversity indices. Despite known environmental gradients within the Red Sea, the communities remained surprisingly similar. The communities do, however, exhibit subtle changes across this span of reefs that likely reflect the constrained distributions of several species of reef fish and benthic fauna.
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ArticleConnectivity and resilience of coral reef metapopulations in marine protected areas : matching empirical efforts to predictive needs(Springer, 2009-02-11) Botsford, L. W. ; White, J. Wilson ; Coffroth, M.- A. ; Paris, Claire B. ; Planes, Serge ; Shearer, T. L. ; Thorrold, Simon R. ; Jones, Geoffrey P.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.