Margaret W. Miller

Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata.

The movements of larvae between marine populations are difficult to follow directly and have been the subject of much controversy, especially in the Caribbean. The debate centres on the degree to which populations are demographically open, such that depleted populations can be replenished by recruitment from distant healthy populations, or demographically closed and thus in need of local management. Given the depressed state of many tropical reef populations, the understanding of these movements now bears critically on the number, placement, and size of marine reserves. Most genetic analyses assume that dispersal patterns have been stable for thousands of generations, thus they commonly reflect past colonization histories more than ongoing dispersal. Recently developed multilocus genotyping approaches, however, have the demonstrated ability to detect both migration and population isolation over far shorter timescales. Previously, we developed five microsatellite markers and demonstrated them to be both Mendelian and coral‐specific. Using these markers and Bayesian analyses, we show here that populations of the imperiled reef‐building coral, Acropora palmata, have experienced little or no recent genetic exchange between the western and the eastern Caribbean. Puerto Rico is identified as an area of mixing between the two subregions. As a consequence of this regional isolation, populations in the western and eastern Caribbean should have the potential to adapt to local conditions and will require population‐specific management strategies.

Recent Region-wide Declines in Caribbean Reef Fish Abundance

Profound ecological changes are occurring on coral reefs throughout the tropics, with marked coral cover losses and concomitant algal increases, particularly in the Caribbean region. Historical declines in the abundance of large Caribbean reef fishes likely reflect centuries of overexploitation. However, effects of drastic recent degradation of reef habitats on reef fish assemblages have yet to be established. By using meta-analysis, we analyzed time series of reef fish density obtained from 48 studies that include 318 reefs across the Caribbean and span the time period 1955-2007. Our analyses show that overall reef fish density has been declining significantly for more than a decade, at rates that are consistent across all subregions of the Caribbean basin (2.7% to 6.0% loss per year) and in three of six trophic groups. Changes in fish density over the past half-century are modest relative to concurrent changes in benthic cover on Caribbean reefs. However, the recent significant decline in overall fish abundance and its consistency across several trophic groups and among both fished and nonfished species indicate that Caribbean fishes have begun to respond negatively to habitat degradation.

Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata

Ocean acidification (OA) refers to the ongoing decline in oceanic pH resulting from the uptake of atmospheric CO2. Mounting experimental evidence suggests that OA will have negative consequences for a variety of marine organisms. Whereas the effect of OA on the calcification of adult reef corals is increasingly well documented, effects on early life history stages are largely unknown. Coral recruitment, which necessitates successful fertilization, larval settlement, and postsettlement growth and survivorship, is critical to the persistence and resilience of coral reefs. To determine whether OA threatens successful sexual recruitment of reef-building corals, we tested fertilization, settlement, and postsettlement growth of Acropora palmata at pCO2 levels that represent average ambient conditions during coral spawning (∼400 μatm) and the range of pCO2 increases that are expected to occur in this century [∼560 μatm (mid-CO2) and ∼800 μatm (high-CO2)]. Fertilization, settlement, and growth were all negatively impacted by increasing pCO2, and impairment of fertilization was exacerbated at lower sperm concentrations. The cumulative impact of OA on fertilization and settlement success is an estimated 52% and 73% reduction in the number of larval settlers on the reef under pCO2 conditions projected for the middle and the end of this century, respectively. Additional declines of 39% (mid-CO2) and 50% (high-CO2) were observed in postsettlement linear extension rates relative to controls. These results suggest that OA has the potential to impact multiple, sequential early life history stages, thereby severely compromising sexual recruitment and the ability of coral reefs to recover from disturbance.

Effects of fish predation and seaweed competition on the survival and growth of corals

Abstract On Caribbean coral reefs, high rates of grazing by herbivorous fishes are thought to benefit corals because fishes consume competing seaweeds. We conducted field experiments in the Florida Keys, USA, to examine the effects of grazing fishes on coral/seaweed competition. Initially, fragments of Porites divaracata from an inshore habitat were transplanted into full-cage, half-cage, and no-cage treatments on a fore-reef. Within 48 h, 56% of the unprotected corals in half-cage and no-cage treatments (62 of 111) were completely consumed. Stoplight parrotfish (Sparisoma viride) were the major coral predators, with redband parrotfish (S. aurofrenatum) also commonly attacking this coral. Next, we transplanted fragments of P. porites collected from the fore-reef habitat where our caging experiments were being conducted into the three cage treatments, half in the presence of transplanted seaweeds, and half onto initially clean substrates. The corals were allowed to grow in these conditions, with concurrent development of competing seaweeds, for 14 weeks. Although seaweed cover and biomass were both significantly greater in the full-cage treatment, coral growth did not differ significantly between cage treatments even though corals placed with pre-planted seaweeds grew significantly less than corals placed on initially clean substrate. This surprising result occurred because parrotfishes not only grazed algae from accessible treatments, but also fed directly on our coral transplants. Parrotfish feeding scars were significantly more abundant on P. porites from the half and no-cage treatments than on corals in the full cages. On this Florida reef, direct fish predation on some coral species (P. divaracata) can exclude them from fore-reef areas, as has previously been shown for certain seaweeds and sponges. For other corals that live on the fore-reef (P. porites), the benefits of fishes removing seaweeds can be counterbalanced by the detrimental effects of fishes directly consuming corals.

An analysis of the loss of acroporid corals at Looe Key, Florida, USA: 1983-2000

Abstract. The Caribbean reef-building corals Acropora palmata and Acropora cervicornis have undergone widespread declines in the past two decades, leading to their designation as candidates for listing under the United States Endangered Species Act. Whole-reef censuses in 1983 and 2000 at Looe Key National Marine Sanctuary in the Florida Keys provide estimates of areal loss of live Acropora spp. cover. Area (square meters) of live coral cover was quantified from depiction on scaled base maps of extent of coral cover observed by a snorkeler on each reef spur at each census. Certain thickets appear to have been persistent (though none expanded), but the total area of live A. palmata at Looe Key is estimated to have declined by 93% and A. cervicornis by 98% during this 17-year interval. It is likely that acroporid populations may have already undergone substantial decline prior to our initial census in 1983.

Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean

In preparation for a large-scale coral restoration project, we surveyed host population genetic structure and symbiont diversity of two reef-building corals in four reef zones along the Florida reef tract (FRT). There was no evidence for coral population subdivision along the FRT in Acropora cervicornis or Montastraea faveolata based on microsatellite markers. However, in A. cervicornis, significant genetic differentiation was apparent when extending the analysis to broader scales (Caribbean). Clade diversity of the zooxanthellae differed along the FRT. A. cervicornis harbored mostly clade A with clade D zooxanthellae being prominent in colonies growing inshore and in the mid-channel zones that experience greater temperature fluctuations and receive significant nutrient and sediment input. M. faveolata harbored a more diverse array of symbionts, and variation in symbiont diversity among four habitat zones was more subtle but still significant. Implications of these results are discussed for ongoing restoration and conservation work.

Nuclear sequences reveal mid‐range isolation of an imperilled deep‐water coral population

The mitochondrial DNA of corals and their anthozoan kin evolves slowly, with substitution rates about two orders of magnitude lower than in typical bilateral animals. This has impeded the delineation of closely related species and isolated populations in corals, compounding problems caused by high morphological plasticity. Here we characterize rates of divergence and levels of variation for three nuclear gene regions, then use these nuclear sequences as markers to test for population structure in Oculina, a taxonomically confused genus of corals. Rates of sequence divergence (obtained by comparison to Solenastrea hyades) were at least five (and sometimes over 10) times faster for the three nuclear markers than for a mitochondrial reference sequence. Nuclear sequence variation was also high within populations, although it tended to decline north of Cape Canaveral. Significant subdivision was evident among samples from 10 locations from between North Carolina and the Florida Panhandle, but neither nominal species designation nor population depth explained much of this variation. Instead, a single population from the unique deep (> 70 m) water reefs at the Oculina Banks off central Florida was a strong genetic outlier: all pairwise measures of subdivision involving this population were greater than those involving all other populations, and multilocus clustering recognized the Oculina Banks as distinct from other populations, despite its close proximity (≤ 36 km) to populations from shallower waters nearby and its location at the centre of the sampled range. Genetic isolation of the Oculina Banks population suggests that focused efforts will be needed to conserve the foundation species of these monotypic reefs and that depth may play a role in isolating marine populations and perhaps facilitating initial steps towards speciation.

Shifting paradigms in restoration of the world's coral reefs

Abstract Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine‐protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014–2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.

Coral disease outbreak at Navassa, a remote Caribbean island

In November 2004, a high prevalence of coral disease was observed at several sites around Navassa, an uninhabited Caribbean island between Haiti and Jamaica. At least fifteen mounding and foliaceous scleractinian species were affected with ‘white disease’ signs. Coral disease incidence was observed to be absent in quantitative surveys in 2002, but in 2004 average prevalence (i.e., % of colonies) of active disease ranged up to 15% and an additional 19% prevalence of colonies with patterns of recent mortality consistent with disease. Large and/or Montastraea spp. colonies were disproportionately affected and the anticipated loss of these large, reef-building colonies will impact coral community structure. One or more potential factors may influence the initiation and persistence of disease outbreak conditions at Navassa including recent hurricane disturbance, regional patterns of increasing disease impact in deep or remote Caribbean reefs, or vectoring of disease by the corallivorous worm, Hermodice carunculata.

Corallivorous snail removal: evaluation of impact on Acropora palmata

Abstract With the continuing decline of Acropora palmata throughout the Caribbean region, impacts of the gastropod corallivore, Coralliophila abbreviata, are becoming more noticeable. A snail removal experiment was performed in remnant A. palmata populations in the Florida Keys National Marine Sanctuary to quantify the area of coral tissue consumed by ambient snail aggregations and to assess the possible effectiveness of snail removal in conserving live coral tissue. Corals where ambient snail aggregations were removed maintained significantly more live tissue area during the 2-month experiment than those where feeding snail aggregations were left in place. The corals with feeding snails left in place lost more than 3 cm2 tissue day−1 on average. Thus, removal of C. abbreviata may be an effective measure for conserving depressed A. palmata populations, though secondary effects of such a manipulation remain to be carefully evaluated.