Integrating larval connectivity with local demography reveals regional dynamics of a marine metapopulation

Many ocean species exist within what are called marine metapopulations: networks of otherwise isolated local populations connected by the exchange of larval offspring. In order to manage these species as effectively as possible (e.g., by designing and implementing effective networks of marine protected areas), we must know how many offspring are produced within each local population (i.e., local demography), and where those offspring disperse (i.e., larval connectivity). Although there is much interest in estimating connectivity in the relatively simple sense of identifying the locations of spawning parents and their settling offspring, true measures of demographic connectivity that account for among-site variation in offspring production have been lacking. We combined detailed studies of local reproductive output and larval dispersal of a coral reef fish to quantify demographic connectivity within a regional metapopulation that included four widely spaced islands in the Bahamas. We present a new method for estimating demographic connectivity when the levels of dispersal among populations are inferred by the collection of genetically "tagged" offspring. We estimated that 13.3% of recruits returned to natal islands, on average (95% CI = 1.1-50.3%), that local retention was high on one of the islands (41%, 95% CI = 6.0-97.0%), and that larval connectivity was appreciable, even between islands 129 km apart (mean = 1.6%, 95% CI = 0.20-8.8%). Our results emphasize the importance of properly integrating measurements of production with measurements of connectivity. Had we not accounted for among-site variation in offspring production, our estimates of connectivity would have been inaccurate by a factor as much as 6.5. At a generational timescale, lifetime offspring production varied substantially (a fivefold difference among islands) and the importance of each island to long-term metapopulation growth was dictated by both larval production and connectivity. At the scale of our study (local populations inhabiting 5-ha reefs), the regional metapopulation could not grow without external input. However, an exploratory analysis simulating a network of four marine protected areas suggested that reserves of >65 ha each would ensure persistence of this network. Thus, integrating studies of larval connectivity and local demography hold promise for both managing and conserving marine metapopulations effectively.