Population Structure of Montastraea cavernosa on Shallow versus Mesophotic Reefs in Bermuda

Mesophotic coral reef ecosystems remain largely unexplored with only limited information available on taxonomic composition, abundance and distribution. Yet, mesophotic reefs may serve as potential refugia for shallow-water species and thus understanding biodiversity, ecology and connectivity of deep reef communities is integral for resource management and conservation. The Caribbean coral, Montastraea cavernosa, is considered a depth generalist and is commonly found at mesophotic depths. We surveyed abundance and size-frequency of M. cavernosa populations at six shallow (10m) and six upper mesophotic (45m) sites in Bermuda and found population structure was depth dependent. The mean surface area of colonies at mesophotic sites was significantly smaller than at shallow sites, suggesting that growth rates and maximum colony surface area are limited on mesophotic reefs. Colony density was significantly higher at mesophotic sites, however, resulting in equal contributions to overall percent cover. Size-frequency distributions between shallow and mesophotic sites were also significantly different with populations at mesophotic reefs skewed towards smaller individuals. Overall, the results of this study provide valuable baseline data on population structure, which indicate that the mesophotic reefs of Bermuda support an established population of M. cavernosa.     

Into the depth of population genetics: pattern of structuring in mesophotic red coral populations

Deep-sea reef-building corals are among the most conspicuous invertebrates inhabiting the hard-bottom habitats worldwide and are particularly susceptible to human threats. The precious red coral (Corallium rubrum, L. 1758) has a wide bathymetric distribution, from shallow up to 800 m depth, and represents a key species in the Mediterranean mesophotic reefs. Several studies have investigated genetic variability in shallow-water red coral populations, while geographic patterns in mesophotic habitats are largely unknown. This study investigated genetic variability of C. rubrum populations dwelling between 55 and 120 m depth, from the Ligurian to the Ionian Sea along about 1500 km of coastline. A total of 18 deep rocky banks were sampled. Colonies were analyzed by means of a set of microsatellite loci and the putative control region of the mitochondrial DNA. Collected data were compared with previous studies. Both types of molecular markers showed high genetic similarity between populations within the northern (Ligurian Sea and Tuscan Archipelago) and the southern (Tyrrhenian and Ionian seas) study areas. Variability in habitat features between the sampling sites did not affect the genetic variability of the populations. Conversely, the patchy distribution of suitable habitats affected populations’ connectivity within and among deep coral banks. Based on these results and due to the emphasis on red coral protection in the Mediterranean Sea by international institutions, red coral could be promoted as a ‘focal species’ to develop management plans for the conservation of deep coralligenous reefs, a reservoir of marine biodiversity.     

Quantifying Spatial Genetic Structuring in Mesophotic Populations of the Precious Coral Corallium rubrum

While shallow water red coral populations have been overharvested in the past, nowadays, commercial harvesting shifted its pressure on mesophotic organisms. An understanding of red coral population structure, particularly larval dispersal patterns and connectivity among harvested populations is paramount to the viability of the species. In order to determine patterns of genetic spatial structuring of deep water Corallium rubrum populations, for the first time, colonies found between 58–118 m depth within the Tyrrhenian Sea were collected and analyzed. Ten microsatellite loci and two regions of mitochondrial DNA (mtMSH and mtC) were used to quantify patterns of genetic diversity within populations and to define population structuring at spatial scales from tens of metres to hundreds of kilometres. Microsatellites showed heterozygote deficiencies in all populations. Significant levels of genetic differentiation were observed at all investigated spatial scales, suggesting that populations are likely to be isolated. This differentiation may by the results of biological interactions, occurring within a small spatial scale and/or abiotic factors acting at a larger scale. Mitochondrial markers revealed significant genetic structuring at spatial scales greater then 100 km showing the occurrence of a barrier to gene flow between northern and southern Tyrrhenian populations. These findings provide support for the establishment of marine protected areas in the deep sea and off-shore reefs, in order to effectively maintain genetic diversity of mesophotic red coral populations.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia

Approximately one quarter of zooxanthellate coral species have a depth distribution from shallow waters (<30 m) down to mesophotic depths of 30-60 m. The deeper populations of such species are less likely to be affected by certain environmental perturbations, including high temperature/high irradiance causing coral bleaching. This has led to the hypothesis that deep populations may serve as refuges and a source of recruits for shallow reef habitats. The extent of vertical connectivity of reef coral species, however, is largely unquantified. Using 10 coral host microsatellite loci and sequences of the host mtDNA putative control region, as well as ribosomal DNA (rDNA) ITS2 sequences of the coral's algal endosymbionts (Symbiodinium), we examine population structure, connectivity and symbiont specificity in the brooding coral Seriatopora hystrix across a depth profile in both northwest (Scott Reef) and northeast Australia (Yonge Reef). Strong genetic structuring over depth was observed in both regions based on the microsatellite loci; however, Yonge Reef exhibited an additional partitioning of mtDNA lineages (associated with specific symbiont ITS2 types), whereas Scott Reef was dominated by a single mtDNA lineage (with no apparent host-symbiont specificity). Evidence for recruitment of larvae of deep water origin into shallow habitats was found at Scott Reef, suggesting that recovery of shallow water habitats may be aided by migration from deep water refuges. Conversely, no migration from the genetically divergent deep slope populations into the shallow habitats was evident at Yonge Reef, making recovery of shallow habitats from deeper waters at this location highly unlikely.     

Vertical and Horizontal Genetic Connectivity in Chromis verater,an Endemic Damselfish Found on Shallow and Mesophotic Reefs in the Hawaiian Archipelago and Adjacent Johnston Atoll

Understanding vertical and horizontal connectivity is a major priority in research on mesophotic coral ecosystems (30–150 m). However, horizontal connectivity has been the focus of few studies, and data on vertical connectivity are limited to sessile benthic mesophotic organisms. Here we present patterns of vertical and horizontal connectivity in the Hawaiian Islands-Johnston Atoll endemic threespot damselfish, Chromis verater, based on 319 shallow specimens and 153 deep specimens. The mtDNA markers cytochrome b and control region were sequenced to analyze genetic structure: 1) between shallow (<30 m) and mesophotic (30–150 m) populations and 2) across the species'' geographic range. Additionally, the nuclear markers rhodopsin and internal transcribed spacer 2 of ribosomal DNA were sequenced to assess connectivity between shallow and mesophotic populations. There was no significant genetic differentiation by depth, indicating high levels of vertical connectivity between shallow and deep aggregates of C. verater. Consequently, shallow and deep samples were combined by location for analyses of horizontal connectivity. We detected low but significant population structure across the Hawaiian Archipelago (overall cytochrome b: Φ_ST = 0.009, P = 0.020; control region: Φ_ST = 0.012, P = 0.009) and a larger break between the archipelago and Johnston Atoll (cytochrome b: Φ_ST = 0.068, P<0.001; control region: Φ_ST = 0.116, P<0.001). The population structure within the archipelago was driven by samples from the island of Hawaii at the southeast end of the chain and Lisianski in the middle of the archipelago. The lack of vertical genetic structure supports the refugia hypothesis that deep reefs may constitute a population reservoir for species depleted in shallow reef habitats. These findings represent the first connectivity study on a mobile organism that spans shallow and mesophotic depths and provide a reference point for future connectivity studies on mesophotic fishes.     

Intraspecific variability in the life histories of endemic coral-reef fishes between photic and mesophotic depths across the Central Pacific Ocean

Mesophotic coral ecosystems (MCEs) represent the lowest depth distribution inhabited by many coral reef-associated organisms. Research on fishes associated with MCEs is sparse, leading to a critical lack of knowledge of how reef fish found at mesophotic depths may vary from their shallow reef conspecifics. We investigated intraspecific variability in body condition and growth of three Hawaiian endemics collected from shallow, photic reefs (5–33 m deep) and MCEs (40–75 m) throughout the Hawaiian Archipelago and Johnston Atoll: the detritivorous goldring surgeonfish, Ctenochaetus strigosus, and the planktivorous threespot chromis, Chromis verater, and Hawaiian dascyllus, Dascyllus albisella. Estimates of body condition and size-at-age varied between shallow and mesophotic depths; however, these demographic differences were outweighed by the magnitude of variability found across the latitudinal gradient of locations sampled within the Central Pacific. Body condition and maximum body size were lowest in samples collected from shallow and mesophotic Johnston Atoll sites, with no difference occurring between depths. Samples from the Northwestern Hawaiian Islands tended to have the highest body condition and reached the largest body sizes, with differences between shallow and mesophotic sites highly variable among species. The findings of this study support newly emerging research demonstrating intraspecific variability in the life history of coral-reef fish species whose distributions span shallow and mesophotic reefs. This suggests not only that the conservation and fisheries management should take into consideration differences in the life histories of reef-fish populations across spatial scales, but also that information derived from studies of shallow fishes be applied with caution to conspecific populations in mesophotic coral environments.

     

Fine‐scale structure among mesophotic populations of the great star coral Montastraea cavernosa revealed by SNP genotyping

Mesophotic reefs (30‐150 m) have been proposed as potential refugia that facilitate the recovery of degraded shallow reefs following acute disturbances such as coral bleaching and disease. However, because of the technical difficulty of collecting samples, the connectivity of adjacent mesophotic reefs is relatively unknown compared with shallower counterparts. We used genotyping by sequencing to assess fine‐scale genetic structure of Montastraea cavernosa at two sites at Pulley Ridge, a mesophotic coral reef ecosystem in the Gulf of Mexico, and downstream sites along the Florida Reef Tract. We found differentiation between reefs at Pulley Ridge (~68 m) and corals at downstream upper mesophotic depths in the Dry Tortugas (28–36 m) and shallow reefs in the northern Florida Keys (Key Biscayne, ~5 m). The spatial endpoints of our study were distinct, with the Dry Tortugas as a genetic intermediate. Most striking were differences in population structure among northern and southern sites at Pulley Ridge that were separated by just 12km. Unique patterns of clonality and outlier loci allele frequency support these sites as different populations and suggest that the long‐distance horizontal connectivity typical of shallow‐water corals may not be typical for mesophotic systems in Florida and the Gulf of Mexico. We hypothesize that this may be due to the spawning of buoyant gametes, which commits propagules to the surface, resulting in greater dispersal and lower connectivity than typically found between nearby shallow sites. Differences in population structure over small spatial scales suggest that demographic constraints and/or environmental disturbances may be more variable in space and time on mesophotic reefs compared with their shallow‐water counterparts.     

Phase shift to algal dominated communities at mesophotic depths associated with lionfish (<Emphasis Type="Italic">Pterois volitans</Emphasis>) invasion on a Bahamian coral reef

Mesophotic coral reefs (30–150 m) have been assumed to be physically and biologically connected to their shallow-water counterparts, and thus may serve as refugia for important taxonomic groups such as corals, sponges, and fish. The recent invasion of the Indo–Pacific lionfish (Pterois volitans) onto shallow reefs of the Caribbean and Bahamas has had significant, negative, effects on shallow coral reef fish populations. In the Bahamas, lionfish have extended their habitat range into mesophotic depths down to 91 m where they have reduced the diversity of several important fish guilds, including herbivores. A phase shift to an algal dominated (>50% benthic cover) community occurred simultaneously with the loss of herbivores to a depth of 61 m and caused a significant decline in corals and sponges at mesophotic depths. The effects of this invasive lionfish on mesophotic coral reefs and the subsequent changes in benthic community structure could not be explained by coral bleaching, overfishing, hurricanes, or disease independently or in combination. The significant ecological effects of the lionfish invasion into mesophotic depths of coral reefs casts doubt on whether these communities have the resilience to recover themselves or contribute to the recovery of their shallow water counterparts as refugia for key coral reef taxa.     

Modeling vertical coral connectivity and mesophotic refugia

Whether mesophotic reefs will behave as refugia for corals threatened by global climate change and coastal development depends on vertical exchange of larvae between diverse habitats. Here we use a biophysical model of larval dispersal to estimate vertical connectivity of a broadcasting (Orbicella faveolata) and a brooding (Porites astreoides) species of coral in the US Virgin Islands. Modeling predicts subsidy to shallow areas by mesophotic larvae of both species based on local hydrology, adult reproductive characteristics, larval traits, and a wide range of scenarios developed to test depth-sensitive factors, such as fertilization rates and post-settlement survivorship. In extreme model scenarios of reduced fertilization and post-settlement survivorship of mesophotic larvae, 1–10 % local mesophotic subsidy to shallow recruitment is predicted for both species, which are demographically significant. Although direct vertical connectivity is higher for the broadcaster, the brooder demonstrates higher local multigenerational vertical connectivity, which suggests that local P. astreoides populations are more resilient than those of O. faveolata, and corroborates field studies. As shallow habitat degrades, mesophotic–shallow subsidy is predicted to increase for both species. This study is the first of its kind to simulate larval dispersal and settlement between habitats of different depths, and these findings have local, regional, and global implications for predicting and managing coral reef persistence in a changing climate.     

Depth-Independent Reproduction in the Reef Coral Porites astreoides from Shallow to Mesophotic Zones

Mesophotic coral ecosystems between 30–150 m may be important refugia habitat for coral reefs and associated benthic communities from climate change and coastal development. However, reduced light at mesophotic depths may present an energetic challenge to the successful reproduction of light-dependent coral organisms, and limit this refugia potential. Here, the relationship of depth and fecundity was investigated in a brooding depth-generalist scleractinian coral, Porites astreoides from 5–37 m in the U.S. Virgin Islands (USVI) using paraffin tissue histology. Despite a trend of increasing planulae production with depth, no significant differences were found in mean peak planulae density between shallow, mid-depth and mesophotic sites. Differential planulae production over depth is thus controlled by P. astreoides coral cover, which peaks at 10 m and ~35 m in the USVI. These results suggest that mesophotic ecosystems are reproductive refuge for P. astreoides in the USVI, and may behave as refugia for P. astreoides metapopulations providing that vertical larval exchanges are viable.     

Are mesophotic coral ecosystems distinct communities and can they serve as refugia for shallow reefs?

We analyzed an extensive dataset of over 9000 benthic and suprabenthic species found throughout the Gulf of Mexico (GoMx) to assess whether mesophotic coral ecosystems represent distinct assemblages and evaluate their potential to serve as refugia for shallow reef communities. We assessed community structure of the overall benthic community from 0 to 300 m via non-metric multidimensional scaling (NMDS) of species presence across depth bands. We used the Jaccard index of similarity to calculate the proportion of shared species between adjacent depth bands, measure species turnover with depth, and assess taxonomic overlap between shallow reefs versus progressively deeper depth bands. NMDS ordinations showed that the traditionally defined mesophotic range (30–150 m) as a whole is not a distinct community. In contrast, taxonomically distinct communities, determined by hierarchical clustering, were found at 0–70, 60–120, 110–200, and 190–300 m. Clustering highlighted an important separation in the benthic community at ~60 m, which was especially important for actinopterygian fishes. Species turnover between adjacent depths decreased with depth for all taxa combined and individual taxa, with peaks at ~60, 90–120, and 190–200 m. Fishes showed lower turnover from shallow to upper mesophotic depths (0–50 m) than all taxa combined, a substantial peak at 60 m, followed by a precipitous and continued decline in turnover thereafter. Taxonomic overlap between shallow (0–20 m) and progressively deeper zones declined steadily with depth in all taxa and individual taxa, suggesting that mid- and lower mesophotic habitats have less (but not inconsequential) potential to serve as refugia (60–150 m, 15–25% overlap with shallow habitats) than upper mesophotic zones (30–60 m, 30–45% overlap with shallow habitats) for all taxa combined. We conclude that the traditional mesophotic zone is home to three ecological communities in the GoMx, one that is confluent with shallow reefs, a distinct mesophotic assemblage spanning 60–120 m, and a third that extends onto the outer continental shelf.     

Increased genetic structuring of isolated Salamandra salamandra populations (Caudata: Salamandridae) at the margins of the Carpathian Mountains

The traditional southern Pleistocene refugia hypothesis in Europe has lately been challenged for several animal and plant species. The Carpathian Basin, especially at the marginal regions, is one of the recently recognized biodiversity hotspots in Europe. Marginal populations are prone to have lower genetic diversity and higher genetic differentiation than central populations. Here, we examined one mitochondrial DNA fragment (D‐loop) and nine nuclear (microsatellite) loci to describe the genetic diversity and phylogeographical pattern of fire salamander (Salamandra salamandra) populations in the Carpathian Basin with focusing on the southern margins of the Western Carpathians, where isolated populations of this species are present. Analyses of microsatellites indicated reduced genetic diversity for most of the isolated populations. Based on the mitochondrial DNA, only two haplotypes were found, whereas the analyses with the nuclear markers revealed a more recent genetic split between Western (Alpine) and Eastern (Carpathian) populations, and separated the Apuseni Mountains population (part of the Western Carpathians). Using approximate Bayesian computation analyses, we identified the most probable colonization scenario for the isolated North Hungarian Carpathian Basin populations. The split between isolated salamander populations from the central populations in the Carpathian Mountains dates back to the beginning of the Late Pleistocene, while the split between most of the Hungarian populations can be associated with the Last Glacial Maximum. We found evidence for long‐time isolation between the marginal Carpathian Basin and central populations. Our results also show that S. salamandra survived glacial periods in the temperate forests of north‐east Pannonia (North Hungarian Mountains), confirming that the Carpathian Basin served as important northerly refugia during the Pleistocene climatic oscillations.     

Stress and adaptation in conservation genetics

Stress, adaptation and evolution are major concerns in conservation biology. Stresses from pollution, climatic changes, disease etc. may affect population persistence. Further, stress typically occurs when species are placed in captivity. Threatened species are usually managed to conserve their ability to adapt to environmental changes, whilst species in captivity undergo adaptations that are deleterious upon reintroduction into the wild. In model studies using Drosophila melanogaster, we have found that; (a) inbreeding and loss of genetic variation reduced resistance to the stress of disease, (b) extinction rates under inbreeding are elevated by stress, (c) adaptive evolutionary potential in an increasingly stressful environment is reduced in small population, (d) rates of inbreeding are elevated under stressful conditions, (e) genetic adaptation to captivity reduces fitness when populations are reintroduced into the 'wild', and (f) the deleterious effects of adaptation on reintroduction success can be reduced by population fragmentation.     

Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths

The deep reef refugia hypothesis proposes that deep reefs can act as local recruitment sources for shallow reefs following disturbance. To test this hypothesis, nine polymorphic DNA microsatellite loci were developed and used to assess vertical connectivity in 583 coral colonies of the Caribbean depth‐generalist coral Montastraea cavernosa. Samples were collected from three depth zones (≤10, 15–20 and ≥25 m) at sites in Florida (within the Upper Keys, Lower Keys and Dry Tortugas), Bermuda, and the U.S. Virgin Islands. Migration rates were estimated to determine the probability of coral larval migration from shallow to deep and from deep to shallow. Finally, algal symbiont (Symbiodinium spp.) diversity and distribution were assessed in a subset of corals to test whether symbiont depth zonation might indicate limited vertical connectivity. Overall, analyses revealed significant genetic differentiation by depth in Florida, but not in Bermuda or the U.S. Virgin Islands, despite high levels of horizontal connectivity between these geographic locations at shallow depths. Within Florida, greater vertical connectivity was observed in the Dry Tortugas compared to the Lower or Upper Keys. However, at all sites, and regardless of the extent of vertical connectivity, migration occurred asymmetrically, with greater likelihood of migration from shallow to intermediate/deep habitats. Finally, most colonies hosted a single Symbiodinium type (C3), ruling out symbiont depth zonation of the dominant symbiont type as a structuring factor. Together, these findings suggest that the potential for shallow reefs to recover from deep‐water refugia in M. cavernosa is location‐specific, varying among and within geographic locations likely as a consequence of local hydrology.     

Candidate gene SNP variation in floodplain populations of pedunculate oak (Quercus robur L.) near the species' southern range margin: Weak differentiation yet distinct associations with water availability

Populations residing near species' low‐latitude range margins (LLMs) often occur in warmer and drier environments than those in the core range. Thus, their genetic composition could be shaped by climatic drivers that differ from those occurring at higher latitudes, resulting in potentially adaptive variants of conservation value. Such variants could facilitate the adaptation of populations from other portions of the geographical range to similar future conditions anticipated under ongoing climate change. However, very few studies have assessed standing genetic variation at potentially adaptive loci in natural LLM populations. We investigated standing genetic variation at single nucleotide polymorphisms (SNPs) located within 117 candidate genes and its links to putative climatic selection pressures across 19 pedunculate oak (Quercus robur L.) populations distributed along a regional climatic gradient near the species' southern range margin in southeastern Europe. These populations are restricted to floodplain forests along large lowland rivers, whose hydric regime is undergoing significant shifts under modern rapid climate change. The populations showed very weak geographical structure, suggesting extensive genetic connectivity and gene flow or shared ancestry. We identified eight (6.2%) positive F_ST‐outlier loci, and genotype–environment association analyses revealed consistent associations between SNP allele frequencies and several climatic variables linked to water availability. A total of 61 associations involving 37 SNPs (28.5%) from 35 annotated genes provided important insights into putative functional mechanisms in our system. Our findings provide empirical support for the role of LLM populations as sources of potentially adaptive variation that could enhance species’ resilience to climate change‐related pressures.     

Low connectivity and declining genetic variability along a depth gradient in Corallium rubrum populations

This study examines the possible effect of depth on the connectivity and genetic variability in red coral (Corallium rubrum; Octocorallia: Alcyonacea) populations. Patterns of genetic structuring along a depth gradient (from 20 to 70 m) were investigated in two locations of the western Mediterranean coast (northern Catalan and eastern Ligurian Seas) using 10 microsatellite loci. Strong patterns of genetic structuring among the samples were found both within and between the two study sites. In both locations, consistent patterns of reduction in genetic variability along the depth gradient were also observed, suggesting that depth has an important role in determining the patterns of genetic structure in Corallium rubrum. Moreover, a threshold in connectivity was observed among the samples collected across 40–50 m depth, supporting the hypothesis that discrete shallow- and deep-water red coral populations occur. This finding has major implications for management strategies and the conservation of commercially exploited deep red coral populations.     

Theme section on “Mesophotic Coral Ecosystems: Characterization, Ecology, and Management”

Mesophotic coral ecosystems (MCEs) are characterized by the presence of light-dependent corals and associated communities that are typically found at depths ranging from 30 to 40 m and extending to over 150 m in tropical and subtropical regions. The dominant communities providing structural habitat in the mesophotic zone can be comprised of coral, sponge, and algal species. Because working in this depth range is constrained by traditional SCUBA limits, less is known about corals and associated organisms there compared to shallower coral communities. Following the first-ever gathering of international scientists to review and discuss existing knowledge of MCEs, this issue focuses on the ecological characterization, geomorphology, and concept of MCEs as refugia for shallow-water populations. The review and research papers comprising this special issue reflect the current scientific understanding of these ecosystems and the underlying mechanisms that regulate them, as well as potential resource management implications. It is important to understand the value and role of mesophotic coral ecosystems in tropical and subtropical regions as these areas face increasing environmental change and human impacts