Assessing relative resilience potential of coral reefs to inform management

International audienceEcological resilience assessments are an important part of resilience-based management (RBM) and can help prioritize and target management actions. Use of such assessments has been limited due to a lack of clear guidance on the assessment process. This study builds on the latest scientific advances in RBM to provide that guidance from a resilience assessment undertaken in the Commonwealth of the Northern Mariana Islands (CNMI). We assessed spatial variation in ecological resilience potential at 78 forereef sites near the populated islands of the CNMI: Saipan, Tinian/Aguijan, and Rota. The assessments are based on measuring indicators of resilience processes and are combined with information on anthropogenic stress and larval connectivity. We find great spatial variation in relative resilience potential with many high resilience sites near Saipan (5 of 7) and low resilience sites near Rota (7 of 9). Criteria were developed to identify priority sites for six types of management actions (e.g., conservation, land-based sources of pollution reduction, and fishery management and enforcement) and 51 of the 78 sites met at least one of the sets of criteria. The connectivity simulations developed indicate that Tinian and Aguijan are each roughly 10 × the larvae source that Rota is and twice as frequent a destination. These results may explain the lower relative resilience potential of Rota reefs and indicates that actions in Saipan and Tinian/Aguijan will be important to maintaining supply of larvae. The process we describe for undertaking resilience assessments can be tailored for use in coral reef areas globally and applied to other ecosystems

Evolutionary Ecology of the Corallivorous Gastropod, Coralliophila abbreviata: Implications for Imperiled Caribbean Corals

As the resiliency of coral reefs is eroded by a variety of natural and anthropogenic stressors, corallivory is becoming an increasingly important factor affecting the structure and function of these important ecosystems. Yet, little is known about the mechanistic drivers of coral-corallivore dynamics in many regions, including the Caribbean. In this dissertation, I used an integrated approach to investigate the evolutionary ecology of the coral-eating gastropod, Coralliophila abbreviata, on the reefs of Florida and the Caribbean. Coralliophila abbreviata snails live and feed on most of the major reef-building corals in the region and cause substantial and chronic mortality of the threatened acroporid corals, Acropora palmata and A. cervicornis. The overall objective of this research was to elucidate feedback mechanisms between coral community structure and snail population structure and dynamics. In the first age-based analysis of C. abbreviata populations, I identified remarkable coral-host-associated variation in life-history traits of snails on Florida reefs. Based on estimates of fitness correlates such as growth, longevity, and female reproductive output, A. palmata appears to be a superior host for C. abbreviata compared to two other common coral taxa investigated (Diploria spp. and Montastraea spp.). However, host-specific life-history trade-offs may exist for individual snails that act to balance snail population fitness across hosts. I then developed a set of five polymorphic microsatellite loci that were used in conjunction with mitochondrial cytochrome b sequence data to assess the population genetic structure and demographic history of C. abbreviata from three coral host taxa (A. palmata, Montastraea spp., Mycetophyllia spp.) and six geographic locations spanning most of the species’ range. I found no evidence of genetic differentiation among the snail populations sampled. Demographic analyses of population genetic data support a scenario of a large population expansion during the Pleistocene, a time of major carbonate reef development in the region. These results indicate that C. abbreviata are successful generalist coral predators with unrestricted gene flow throughout the greater Caribbean. On a reef scale, the density and identity of neighboring corals indirectly affected predation pressure on focal A. cervicornis colonies in a manipulative field experiment. Snails exhibited a strong feeding preference for A. cervicornis during the experiment but the presence of the alternative prey, M. faveoloata, also contributed to predator abundance in the experimental plots. Thus, M. faveolata neighbors had a negative effect on A. cervicornis colonies through apparent competition. Overall, these results have implications for coral reef community structure and dynamics. Understanding these processes is necessary to develop effective conservation and management strategies for imperiled corals and predict how these communities will respond to further perturbations in the future

Assessment of Host-Associated Genetic Differentiation among Phenotypically Divergent Populations of a Coral-Eating Gastropod across the Caribbean

<div><p>Host-associated adaptation is emerging as a potential driver of population differentiation and speciation for marine organisms with major implications for ecosystem structure and function. <em>Coralliophila abbreviata</em> are corallivorous gastropods that live and feed on most of the reef-building corals in the tropical western Atlantic and Caribbean. Populations of <em>C. abbreviata</em> associated with the threatened acroporid corals, <em>Acropora palmata</em> and <em>A. cervicornis</em>, display different behavioral, morphological, demographic, and life-history characteristics than those that inhabit other coral host taxa, indicating that host-specific selective forces may be acting on <em>C. abbreviata</em>. Here, we used newly developed polymorphic microsatellite loci and mitochondrial cytochrome b sequence data to assess the population genetic structure, connectivity, and demographic history of <em>C. abbreviata</em> populations from three coral host taxa (<em>A. palmata</em>, <em>Montastraea</em> spp., <em>Mycetophyllia</em> spp.) and six geographic locations across the Caribbean. Analysis of molecular variance provided some evidence of weak and possibly geographically variable host-associated differentiation but no evidence of differentiation among sampling locations or major oceanographic regions, suggesting high gene flow across the Caribbean. Phylogenetic network and Bayesian clustering analyses supported a hypothesis of a single panmictic population as individuals failed to cluster by host or sampling location. Demographic analyses consistently supported a scenario of population expansion during the Pleistocene, a time of major carbonate reef development in the region. Although further study is needed to fully elucidate the interactive effects of host-associated selection and high gene flow in this system, our results have implications for local and regional community interactions and impact of predation on declining coral populations.</p> </div

Genetic diversity indices, neutrality test statistics, and mismatch distribution parameters for mitochondrial <i>cyt b</i> sequences of <i>Coralliophila abbreviata</i> collected from Florida (FL), Navassa (NAV), St. Vincent and the Grenadines (SVG), Curacao (CUR), Panama (PAN), as well as all individuals combined (GLOBAL).

<p>Genetic diversity indices: <i>N</i>, sample size; <i>N</i>_h, number of haplotypes; <i>N</i>_p, number of polymorphic sites; <i>h</i>, haplotype diversity; <i>π</i>, nucleotide diversity. Neutrality statistics: <i>D</i>, Tajima's statistic (Tajima 1989); <i>F</i>_S, Fu's statistic (FU 1997). Mismatch distribution: <i>τ</i> (tau), time since beginning of expansion in mutational units; θ₀ and θ₁, initial and final population size estimators, respectively; <i>P</i> (SSD), probability of sum of squared deviations; Rg, raggedness statistic (Harpending 1994); <i>P</i> (Rg), probability of Rg.</p>*<p><i>P</i><0.01.</p>**<p><i>P</i><0.001.</p

Map of sampling localities across the greater Caribbean.

<p>Dashed line represents the major regional break tested, between the eastern and western Caribbean.</p

AMOVA results for tests of host-associated differentiation among populations of <i>Coralliophila abbreviata</i> using mtDNA and microsatellite (msats) data.

<p>Populations were defined by host taxon (i.: ACR, MON) or host and locality (ii.–iv.: FL ACR, FL MON, BAH ACR [msats only], NAV ACR, NAV MON, CUR ACR [msats only], CUR MON, SVG ACR, SVG MON). <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0047630#s3" target="_blank">Results</a> for microsatellite data represent the weighted averages over all loci.</p><p>Bold values were significant (α = 0.05) before Bonferroni correction for multiple comparisons,</p>*<p>indicates significance after correction.</p

Sample sizes of <i>Coralliophila abbreviata</i> by coral host and locality for mitochondrial cytochrome b sequences (mtDNA) and microsatellite markers (Msats).

<p>Sample sizes of <i>Coralliophila abbreviata</i> by coral host and locality for mitochondrial cytochrome b sequences (mtDNA) and microsatellite markers (Msats).</p

Median joining network for <i>cyt b</i> haplotypes from a sample of 130 <i>Coralliophila abbreviata</i>.

<p>Circles represent individual haplotypes. The size of the circle is proportional to the frequency of the haplotype in the sample and branch lengths are proportional to the number of mutational steps (range: 1–3). Small black circles represent missing/theoretical haplotypes.</p

Global characteristics of five polymorphic microsatellite loci for <i>Coralliophila abbreviata</i>.

<p>Shown, for each locus, are the forward (F) and reverse (R) primer sequences, repeat motif, size range of alleles in base pairs (bp), global sample size (<i>N</i>), number of observed alleles (<i>N</i>_a), observed (<i>H</i>_O) and expected (<i>H</i>_E) heterozygosities, fixation index (<i>F</i>_IS), and uncorrected <i>P</i>-value for test of departure from Hardy Weinberg Equilibrium (<i>P</i>_HW). Loci correspond to GenBank accession numbers HM156485, HM156486, HM156490–HM156492.</p