Clipperton Atoll as a model to study small marine populations: Endemism and the genomic consequences of small population size

<div><p>Estimating population sizes and genetic diversity are key factors to understand and predict population dynamics. Marine species have been a difficult challenge in that respect, due to the difficulty in assessing population sizes and the open nature of such populations. Small, isolated islands with endemic species offer an opportunity to groundtruth population size estimates with empirical data and investigate the genetic consequences of such small populations. Here we focus on two endemic species of reef fish, the Clipperton damselfish, <i>Stegastes baldwini</i>, and the Clipperton angelfish, <i>Holacanthus limbaughi</i>, on Clipperton Atoll, tropical eastern Pacific. Visual surveys, performed over almost two decades and four expeditions, and genetic surveys based on genomic RAD sequences, allowed us to estimate kinship and genetic diversity, as well as to compare population size estimates based on visual surveys with effective population sizes based on genetics. We found that genetic and visual estimates of population numbers were remarkably similar. <i>S</i>. <i>baldwini</i> and <i>H</i>. <i>limbaughi</i> had population sizes of approximately 800,000 and 60,000, respectively. Relatively small population sizes resulted in low genetic diversity and the presence of apparent kinship. This study emphasizes the importance of small isolated islands as models to study population dynamics of marine organisms.</p></div

Fish biomass, abundance and size on Ulithi Atoll.

<p>Fish trophic categories (Piscivores, Carnivores, Corallivores, Planktivores, and Herbivores) are compared among site groups (cluster 1: uninhabited, oceanic; cluster 2: inhabited, oceanic; cluster 3: inhabited & uninhabited, lagoonal) for biomass (a-e), numerical abundance (g-k) and average length (TL, m-q). The stacked bar plots (f & l) show the mean values from sites within each of the 3 clusters, and the dot chart (r) compares the mean TL for fishes from trophic categories found within sites from the 3 clusters. The box-and-whisker plots show the median value (dark horizontal bar); the box length is the interquartile range, the upper whisker marks the smaller of the maximum value and quartile 3+1.5 interquartile range (IQR), and the lower whisker marks the larger of the smallest value and quartile 1–1.5 IQR. Outliers are not shown. Plots produced using the R package <i>graphics</i>, version 3.3.1.</p

Map of Clipperton Atoll and adjacent areas.

<p>Inset shows a detailed map of the Atoll and the sampling sites of the four different expeditions. Fish and benthos were surveyed at all sites in 1998, 2005 and 2016. In 2010, benthos was surveyed at all sites, and fish were surveyed at the labeled sites NC11 and NC12.</p

Structure plots of <i>Holacanthus</i> and <i>Stegastes</i>.

<p>Structure plots of closely related species <i>Holacanthus passer</i>, <i>H</i>. <i>clarionensis</i>, and <i>H</i>. <i>limbaughi</i> (top panel); and <i>Stegastes beebei</i>, <i>S</i>. <i>leucorus</i>, and <i>S</i>. <i>baldwini</i> (bottom panel); based on RAD seq molecular markers.</p

Atoll-scale patterns in coral reef community structure: Human signatures on Ulithi Atoll, Micronesia

<div><p>The dynamic relationship between reefs and the people who utilize them at a subsistence level is poorly understood. This paper characterizes atoll-scale patterns in shallow coral reef habitat and fish community structure, and correlates these with environmental characteristics and anthropogenic factors, critical to conservation efforts for the reefs and the people who depend on them. Hierarchical clustering analyses by site for benthic composition and fish community resulted in the same 3 major clusters: cluster 1–oceanic (close proximity to deep water) and uninhabited (low human impact); cluster 2–oceanic and inhabited (high human impact); and cluster 3–lagoonal (facing the inside of the lagoon) and inhabited (highest human impact). Distance from village, reef exposure to deep water and human population size had the greatest effect in predicting the fish and benthic community structure. Our study demonstrates a strong association between benthic and fish community structure and human use across the Ulithi Atoll (Yap State, Federated States of Micronesia) and confirms a pattern observed by local people that an ‘opportunistic’ scleractinian coral (<i>Montipora</i> sp.) is associated with more highly impacted reefs. Our findings suggest that small human populations (subsistence fishing) can nevertheless have considerable ecological impacts on reefs due, in part, to changes in fishing practices rather than overfishing per se, as well as larger global trends. Findings from this work can assist in building local capacity to manage reef resources across an atoll-wide scale, and illustrates the importance of anthropogenic impact even in small communities.</p></div

Benthic cover (% cover) compared across sites from cluster 1 (uninhabited, oceanic), cluster 2 (inhabited, oceanic), and cluster 3 (inhabited & uninhabited, lagoonal) (a-f).

<p>The relative abundance of hard coral morphotypes is shown for the 3 site clusters in e1-e3. Note that the opportunistic <i>Montipora</i> sp. is considered separately from all other stony corals for both cover and morphotype. The box-and-whisker plots show the median value (dark horizontal bar); the box length is the interquartile range, the upper whisker marks the smaller of the maximum value and quartile 3+1.5 interquartile range (IQR), and the lower whisker marks the larger of the smallest value and quartile 1–1.5 IQR. Outliers are not shown. Plots produced using the R package <i>graphics</i>, version 3.3.1.</p

Fish biomass, abundance and size on Ulithi Atoll.

<p>Fish trophic categories (Piscivores, Carnivores, Corallivores, Planktivores, and Herbivores) are compared among site groups (cluster 1: uninhabited, oceanic; cluster 2: inhabited, oceanic; cluster 3: inhabited & uninhabited, lagoonal) for biomass (a-e), numerical abundance (g-k) and average length (TL, m-q). The stacked bar plots (f & l) show the mean values from sites within each of the 3 clusters, and the dot chart (r) compares the mean TL for fishes from trophic categories found within sites from the 3 clusters. The box-and-whisker plots show the median value (dark horizontal bar); the box length is the interquartile range, the upper whisker marks the smaller of the maximum value and quartile 3+1.5 interquartile range (IQR), and the lower whisker marks the larger of the smallest value and quartile 1–1.5 IQR. Outliers are not shown. Plots produced using the R package <i>graphics</i>, version 3.3.1.</p

Dendrograms (Ward’s minimum variance method) of Ulithi Atoll sites based on benthic functional groups (2013 and 2014; bray-curtis dissimilarity index; left panel), and fish communities (2012, 2013 and 2014; cao dissimilarity index; right panel).

<p>The sites, ‘Mogp13a’ and ‘Mogp13b’, are, like all of the MogMog sites, ‘lagoonal’, but experience little if any fishing pressure due to the presence of a poisonous corallimorph [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0177083#pone.0177083.ref028" target="_blank">28</a>].</p

Environmental effects and fish community structure.

<p>PERMANOVA results from the model <i>fish ~ exposure + distance + population</i>, stratified by year and terms added sequentially (first to last). Df = degree(s) of freedom, SS = Sums of Squares, MS = Mean Squares, F = F statistic obtained from the model, R² = coefficient of determination, and p = probability of the obtained (model) F exceeding the predicted F statistic by chance.</p

Fish densities.

<p>Density (number per m²) from visual census for <i>Holacanthus limbaughi</i> and <i>Stegastes baldwini</i> shown as box plots separated by both year of census and depth of census.</p