Larval dispersal in marine fishes: novel methods reveal patterns of self-recruitment and population connectivity

Abstract

Many marine fish populations are severely declining due to over-fishing, loss of both juvenile and adult habitats, and accelerating environmental degradation. Fisheries management and the implementation of marine protected areas (MPAs) and other conservation tools are currently hindered by large gaps in knowledge about larval dispersal and its subsequent effects on population dynamics and regulation. This lack of knowledge is due to the inherent difficulty associated with tracking miniscule marine fish larvae. Population genetics approaches are particularly promising, but current methods have been of limited use for inferring ecologically relevant rates of population connectivity because of the large population sizes and high amounts of gene flow present in most marine species. To address these issues, I developed novel genetic methods of identifying parent-offspring pairs to directly track the origin and settlement of larvae in natural populations. These parentage methods fully account for large numbers of pair-wise comparisons and do not require any demographic assumptions or observational data. Furthermore, these methods can be used when only a small proportion of candidate parents can be sampled, which is often the case in large marine populations. I also employed Bayes’ theorem to take into account the frequencies of shared alleles in putative parent-offspring pairs, which can maximize statistical power when faced with fixed numbers of loci. I accounted for genotyping errors by introducing a quantitative method to determine the number of loci to allow to mismatch based upon study-specific error rates. These novel parentage methods were applied to yellow tang (Zebrasoma flavescens, Acanthuridae) sampled around the Island of Hawai'i (measuring 140 km by 129 km) during the summer of 2006. We identified four parent-offspring pairs, which documented dispersal distances ranging from 15 to 184 kilometers. Two of the parents were located within MPAs and their offspring dispersed to unprotected areas. This observation provided direct evidence that MPAs can successfully seed unprotected sites with larvae that survive to become established juveniles. All four offspring were found to the north of their parents and a detailed oceanographic analysis from relevant time periods demonstrated that passive transport initially explained the documented dispersal patterns. However, passive dispersal could not explain how larvae eventually settled on the same island from which they were spawned, indicating a role for larval behavior interacting with fine-scale oceanographic features. Two findings together suggested that sampled reefs did not contribute equally to successful recruitment: (1) low levels of genetic differentiation among all recruit samples, and (2) the fact that the 4 documented parents occurred at only 2 sites. These findings empirically demonstrated the effectiveness of MPAs as useful conservation and management tools and highlighted the value of identifying both the sources and successful settlement sites of marine larvae. I next examined patterns of larval dispersal in bicolor damselfish (Stegastes partitus, Pomacentridae) collected during the summers of 2004 and 2005 from reefs lining the Exuma Sound, Bahamas (measuring 205 km by 85 km). Parentage analysis directly documented two parent-offspring pairs located within the two northern-most sites, which indicated self-recruitment at these sites. Multivariate analyses of pair-wise relatedness values confirmed that self-recruitment was common at all sampled populations. I also found evidence of “sweepstakes events”, whereby only a small proportion of mature adults contributed to subsequent generations. Independent sweepstakes events were indentified in both space and time, bolstering the direct observations of self-recruitment and suggesting a role for sweepstakes analyses to identify the scale of larval dispersal events. This dissertation provides insights into the patterns of larval dispersal in coral-reef fishes. The coupling of direct (e.g., parentage) and indirect (e.g., assignment methods, sweepstakes analyses) methods in conjunction with continued technological and methodological advances will soon provide large-scale, ecologically relevant, rates of larval exchange. By uncovering the dynamics of these enigmatic processes, the implementation of conservation and management strategies for marine fishes in general will undoubtedly experience greater success

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