Genetic parentage analysis as a tool for measuring larval connectivity in a network of marine reserves

Harrison, Hugo B. (2012) Genetic parentage analysis as a tool for measuring larval connectivity in a network of marine reserves. PhD thesis, James Cook University.

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Networks of no‐take marine reserves are widely advocated as a means to conserve biodiversity and manage coastal fisheries. Reserves not only deliver rapid and long‐term benefits within their boundaries, they also provide a broader framework that augments the resilience of coral reef ecosystems. Understanding the level of demographic connectivity between discreet populations is essential to determine a network's efficacy to supplement fisheries and protect biodiversity. In theory, the larger biomass of exploited fishes within reserves, and higher reproductive capacity, increase recruitment to nearby populations due to larval export, and connectivity between reserves support stable populations. However, for large exploited fishes, it has been seemingly impossible to determine where the larvae from populations within reserves go or assess the relative importance of the supply of juveniles from reserves. One of the major challenges is identifying methods that can be applied to large species at the scale at which reserve networks have been implemented. Recent developments in genetic parentage analysis show that this is possible for small reef species, but techniques have not been tested on and applied to important fishery species. The overall aim of this thesis was to develop and apply parentage analysis to assess the conservation and fisheries objectives of a network of no‐take marine reserves of the Great Barrier Reef Marine Park (GBRMP), Australia. It focuses on two of the most important inshore fishery species on the GBRMP, the coral trout (Plectropomus maculatus) and stripey snapper (Lutjanus carponotatus), and provides the first empirical description of the dispersal of larvae from marine reserves.

The use of parentage analysis has become an increasingly popular approach to investigate ecological processes in animal populations. While this is an extremely powerful technique, one aspect of parentage studies has received limited attention: How accurate are they, and what errors are they most likely to encounter? A number of different assignment methods have emerged in common use, and the accuracy of each may differ in relation to the number of loci examined, allelic diversity, incomplete sampling of all candidate parents, and the presence of genotyping errors. In Chapter 2, I examine how these factors affect the accuracy of three popular parentage inference methods to resolve true parent-offspring pairs.

Using simulated data, I was able to capture a wide diversity of conditions that are commonly encountered in parentage studies and identified key factors for the identification of true parent-offspring pairs in natural populations. The findings of this study clearly demonstrate that the number and diversity of loci were the most important factors in obtaining accurate assignments, while the proportion of candidate parents sampled had only a small impact on the susceptibility of each method to either false positive or false negative assignments.

Recent technical advances in the isolation of molecular markers and the high throughput screening of multi-locus genotypes have made it possible to screen large numbers of individuals with unprecedented resolution. Microsatellite markers, short tandem repeats in the nuclear genome, have become a marker of choice in parentage studies for their high level of allelic diversity (polymorphism). As identified in the previous chapter, this is an important factor in obtaining accurate parentage assignments. In Chapter 3, I develop novel sets of microsatellite loci specifically designed for parentage analyses in natural populations of coral trout (P. maculatus) and stripey snapper (L. carponotatus). This resulted in a panel of 11 and 13 highly polymorphic microsatellite markers for P. maculatus and L. carponotatus, respectively. These unique marker sets resulted in an exclusion power of over 99.98% for assignments to single parents, thus providing a high level of accuracy for parentage studies.

Our understanding of the spatial scale of dispersal in coral reef fishes has certainly altered our perception of how populations are regulated, however our knowledge-base largely stems from unique study systems involving small habitat- specialised species with high site fidelity. For large exploited species of commercial value and greatest need of effective management, it has been seemingly impossible to identify where or how far larvae go. In Chapter 4, I describe the first conclusive field evidence that larval supply from marine reserves benefits both fish and fisheries, which fills a major knowledge gap that has impeded wider acceptance of marine reserve networks as an effective fisheries management strategy. Over the course of an extensive field study, tissue samples were collected from adult coral trout and adult stripey snapper within three focal no-take marine reserves in the Keppel Island group, an inshore island archipelago of the GBRMP. During the following 15 months, juveniles of both species were collected throughout the island group up to 30 km from focal reserves. Using DNA parentage analysis, I assigned juveniles collected in both fished and protected locations throughout the island group back to their parents sampled inside reserves. Based on the observed dispersal trajectories, I was able to show that populations within reserves were responsible for supplying approximately half of all juvenile recruitment within 30km of reserves. These findings settle a 20-year long debate as to whether marine reserves actually work as a fisheries management tool in reef systems.

In Chapter 5, I build on previous chapters to explore some of the majors assumptions in our understanding of population dynamics for the management of coral reef fishes: (1) whether the spatial patterns of recruitment are persistent over time; (2) whether patterns of larval supply are consistent across multiple cohorts; (3) whether larger adult fishes account for a greater proportion of local recruitment (settlement) than smaller adult fish; (4) whether fish below the legal length limit contribute to local recruitment; and (5) whether the more abundant and larger fish in reserves are important to local recruitment. By combining genetic and demographic data, this study offers a rare insight into the demographic processes of wild reef fish populations and provides critical information for the management of two commercially and recreationally important fish species. Over the course of three successive cohorts of juvenile coral trout and stripey snapper, recruitment was unevenly distributed throughout the Keppel Islands with three main 'recruitment hotspots'. However, spatial patterns were temporally consistent and successive cohorts were genetically homogeneous, suggesting that the adult source population supplying juvenile recruitment was consistent and largely local. Using genetic parentage analysis I identified which specific adults had contributed to local recruitment, providing a unique perspective on the reproductive success of individual size classes for these species and the influence of reserves on local recruitment.

In summary, this thesis provides a unique perspective on the accuracy of parentage studies in natural populations and identifies key recommendations for the development of microsatellite marker sets for parentage analysis. It provides the first conclusive evidence that larval supply from marine reserves benefits both fish and fisheries, and fills a major knowledge gap that has impeded wider acceptance of marine reserve networks as a viable and effective fisheries management strategy.

Item ID: 34418
Item Type: Thesis (PhD)
Keywords: coral reef fishes; fish populations; GBR; Great Barrier Reef; Keppel Island; Marine protected areas; MPAs; networks; No take zones; No-take marine reserves; parentage analysis; population dynamics; recruitment
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Harrison, Hugo B., Saenz-Agudelo, Pablo, Planes, Serge, Jones, Geoffrey P., and Berumen, Michael L. (2013) Relative accuracy of three common methods of parentage analysis in natural populations. Molecular Ecology, 22 (4). pp. 1158-1170.

Chapter 4: Harrison, Hugo B., Williamson, David H., Evans, Richard D., Almany, Glenn R., Thorrold, Simon R., Russ, Garry R., Feldheim, Kevin A., van Herwerden, Lynne, Planes, Serge, Srinivasan, Maya, Berumen, Michael L., and Jones, Geoffrey P. (2012) Larval export from marine reserves and the recruitment benefit for fish and fisheries. Current Biology, 22 (11). pp. 1023-1028.

Date Deposited: 19 Nov 2014 23:57
FoR Codes: 05 ENVIRONMENTAL SCIENCES > 0502 Environmental Science and Management > 050202 Conservation and Biodiversity @ 33%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070403 Fisheries Management @ 34%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 33%
SEO Codes: 83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8302 Fisheries - Wild Caught > 830201 Fisheries Recreational @ 33%
83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8302 Fisheries - Wild Caught > 830204 Wild Caught Fin Fish (excl. Tuna) @ 33%
96 ENVIRONMENT > 9605 Ecosystem Assessment and Management > 960507 Ecosystem Assessment and Management of Marine Environments @ 34%
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