Fertile fathoms: Deep reproductive refugia for threatened shallow corals

Abstract

The persistence of natural metapopulations may depend on subpopulations that exist at the edges of species ranges, removed from anthropogenic stress. Mesophotic coral ecosystems (30-150 m) are buffered from disturbance by depth and distance, and are potentially massive reservoirs of coral diversity and fecundity; yet we know little about the reproductive capabilities of their constituent species and the potential for these marginal environments to influence patterns of coral reef persistence. We investigated the reproductive performance of the threatened depth-generalist coral Orbicella faveolata over the extent of its vertical range to assess mesophotic contributions to regional larval pools. Over equal habitat area, mesophotic coral populations were found to produce over an order of magnitude more eggs than nearby shallow populations. Positive changes with depth in both population abundance and polyp fecundity contributed to this discrepancy. Relative larval pool contributions of deeper living corals will likely increase as shallow habitats further degrade due to climate change and local habitat degradation. This is a compelling example of the potential for marginal habitat to be critical to metapopulation persistence as reproductive refugia.

Figure 1. The northern US Virgin Islands of St. Thomas and St. John.

Considerable mesophotic habitat (30–150 m) exists on the broad insular platform, and well-mapped linear coral habitat exists on submerged banks near the shelf edge south of St. Thomas. Sample sites from 2010 (gray) ranged in depth from 6–43 m. In 2011 a subset of 2010 sites were visited weekly for five weeks bracketing spawning in August: Black Point (5–10 m), Flat Cay (15–22 m), and Grammanik Bank (35–40 m). Map created using ArcGIS 10.

Figure 2. Histological cross-sections of fully fecund O. faveolata polyps just prior to spawning (week 4) from each site.

From left to right, in order of descending depth, Black Point (8 m), Flat Cay (19 m) and Grammanik Bank (39 m). In each example the polyp has at least 12 ripe gonads, all ova are stage IV (stained gold), and spermaries are stage V (stained red). Bar = 500 μm. See Supplementary Fig. S2 and Supplementary Fig. S3 for further reproductive structure identification.

Figure 3. O. faveolata gametogenic stages of spermaries (left column) and oocytes (right column) observed in histological sections collected weekly (July 28^th to August 26^th 2011, 5 sampling times) from three sites: a shallow near-shore site (red); an offshore island mid-depth site (green); and a mesophotic submerged bank site (blue).

Gametocytes were staged as I–V for spermaries and I–IV for oocytes, however only stages II and later are shown. Plots represent the percentage of colonies that contained each stage. n = 5 or more for each date at each site. Note that colonies can simultaneously contain gametocytes of different stages. The lunar cycle is shown below the x-axis, as well as a black bar that represents expected spawning dates 6–9 days after full moon in August 2011.

Figure 4. Boxplot of O. faveolata oocyte/ova diameters measured from histological sections from each site each sampling week.

Upper and lower hinges correspond to the first and third quartiles, bars correspond to medians and whiskers extend to the highest and lowest values within 1.5 IQR (inter-quartile range). Data beyond whiskers are outliers represented as dots. Significant differences between sites were found in weeks 2 and 3 (multiple comparisons from linear mixed effect models, step-wise adjusted; see Table 1 for more information and exact adjusted p-values). The dotted line denotes that spawning was expected between weeks 4 and 5. Oocytes (likely stage III) were retained beyond expected spawning in August at all sites.

Figure 5. O. faveolata fecundity estimates and comparisons between 2011 study sites.

The number of (A) ripe gonads and the number of (B) oocytes/ova per gonad were estimated for three polyps per sample. Ova production per polyp (C) is the product of the number of ripe gonads multiplied by the number of oocytes/ova per gonad. Data was pooled from sampling weeks 1 through 4. Comparisons were made with Kruskal-Wallis ANOVAs and the Bonferroni post-hoc method to arrive at adjusted p-values. Significant results are noted using lower-case letters in each boxplot (p < 0.05). See Fig. 4 for explanation of boxplot.

Figure 6. Regressions over depth of polyp fecundity, polyp-spacing, Orbicella spp. coral cover, and the resulting product which estimates the number of ova produced over a 1 km² unit reef over depth.

(a) A significant positive linear relationship was found between per polyp ova production and depth (p = 0.001, R² = 0.18). (b) Mid-depth and mesophotic corals were found to have similar polyp-spacing, whereas shallow corals had significantly higher polyp densities (one-way ANOVA, p = 0.012, N = 15). A significant negative linear relationship was found after log transformation (p = 0.014, R² = 0.381). (c) Third degree polynomial model of Orbicella spp. coral cover versus depth (p < 0.0001, R² = 0.51). Orbicella spp. cover is used as a proxy for O. faveolata cover. (d) Expected Orbicella spp. reproductive output from hypothetical 1 km² USVI reefs over depth. (I) Assumes equal polyp fecundity over depth (96 eggs per polyp32); (II) assumes empirically estimated depth-specific fecundity.