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     

Mesophotic coral ecosystems in the Hawaiian Archipelago

Efforts to map coral reef ecosystems in the Hawaiian Archipelago using optical imagery have revealed the presence of numerous scleractinian, zoothanthellate coral reefs at depths of 30–130+ m, most of which were previously undiscovered. Such coral reefs and their associated communities have been recently defined as mesophotic coral ecosystems (MCEs). Several types of MCEs are found in Hawai‘i, each of which dominates a different depth range and is characterized by a unique pattern of coral community structure and colony morphology. Although MCEs are documented near both ends of the archipelago and on many of the islands in between, the maximum depth and prevalence of MCEs in Hawai‘i were found to decline with increasing latitude. The Main Hawaiian Islands (MHI) had significantly deeper and greater percentages of scleractinian coral, and peaks in cover of both scleractinian corals and macroalgae occurred within depth bins 20 m deeper than in the Northwestern Hawaiian Islands (NWHI). Across the archipelago, as depth increased the combined percentage of living cover of mega benthic taxa declined sharply with increasing depth below 70 m, despite the widespread availability of hard substrate.     

Upper and lower mesophotic coral reef fish communities evaluated by underwater visual censuses in two Caribbean locations

Despite more than 60 yr of coral reef research using scuba diving, mesophotic coral ecosystems (MCEs) between 30 and 150 m depth remain largely unknown. This study represents the first underwater visual census of reef fish communities in the Greater Caribbean on MCEs at depths up to 80 m in Bermuda and 130 m in Curaçao. Sampling was performed using mixed-gas closed-circuit rebreathers. Quantitative data on reef fish communities were obtained for four habitats: coral reefs (45–80 m), rhodolith beds (45–80 m), ledges (85–130 m) and walls (85–130 m). A total of 38 species were recorded in Bermuda and 66 in Curaçao. Mesophotic reef fish communities varied significantly between the two localities. MCEs in Bermuda had lower richness and abundance, but higher biomass than those in Curaçao. Richness, abundance and biomass increased with depth in Bermuda, but decreased in Curaçao. A high turnover of species was found among depth strata and between Bermuda and other Caribbean upper MCEs (45–80 m), indicating that depth was an important driver of community structure at all localities. However, local and evolutionary factors (habitat and endemism) are likely the main factors shaping communities in isolated locations such as Bermuda. High fishing pressure is evident in both localities, as total biomass of apex predators was generally low, and thus may be driving a “refugia” scenario in Bermuda, as the abundance and biomass of macro-carnivores increased with depth and distance from the coast.     

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.     

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.     

Benthic structure and cryptic mortality in a Caribbean mesophotic coral reef bank system, the Hind Bank Marine Conservation District, U.S. Virgin Islands

Coral reef banks may form an important component of mesophotic coral ecosystems (MCEs) in the Caribbean, but remain poorly explored relative to shallower reefs and mesophotic habitats on slopes and walls. Consequently, the processes structuring mesophotic coral reef communities are not well understood, particularly the role of disturbance. A large and regionally important mesophotic system, the Hind Bank Marine Conservation District (MCD), St. Thomas, USVI, was systematically surveyed. Data were used to construct a comprehensive benthic habitat map for the MCD, describe the abiotic and biotic components of the benthos among habitats, and investigate patterns of coral health among habitats. Two-thirds of the MCD (23.6 km²) was found to be dense coral reef (Coral Cover = 24.1%) dominated by the Montastraea annularis species complex. Coral reef ecosystems were topographically complex, but could be classified into distinct habitat types, including high coral banks (35.8% of the MCD) and two large novel coral reef habitat types corresponding to an extremely flat basin (18%) and a highly rugose hillock basin (6.5%), containing thousands of coral knolls (2–10 m high). An extreme disease event with undescribed signs of mortality occurred on 47% of coral reefs and reached a high prevalence in affected areas (42.4% ± 6.3 SE, N = 26). The disease was significantly clustered in the basin habitats of the western MCD (global Moran’s I = 0.32, P < 0.01). Observations of the spatial pattern suggested that the driver was specific to the basin habitats and may have been caused by a coherent abiotic event.     

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.

     

<Emphasis Type="Italic">Euphyllia paradivisa</Emphasis>, a successful mesophotic coral in the northern Gulf of Eilat/Aqaba,Red Sea

Mesophotic coral ecosystems (MCEs) host a thriving community of biota that has remained virtually unexplored. Here we report for the first time on a large population of the endangered coral species Euphyllia paradivisa from the MCEs of the Gulf of Eilat/Aqaba (GOE/A), Red Sea. The mesophotic zone in some parts of the study site harbors a specialized coral community predominantly comprising E. paradivisa (73 % of the total coral cover), distributed from 36 to 72 m depth. Here we sought to elucidate the strict distribution but high abundance of E. paradivisa in the MCEs at the GOE/A. We present 4 yr of observations and experiments that provide insight into the physiological plasticity of E. paradivisa: its low mortality rates at high light intensities, high competitive abilities, successful symbiont adaptation to the shallow-water environment, and tolerance to bleaching conditions or survival during prolonged bleaching. Despite its ability to survive under high irradiance in shallow water, E. paradivisa is not found in the shallow reef of the GOE/A. We suggest several factors that may explain the high abundance and exclusivity of E. paradivisa in the MCE: its heterotrophic capabilities; its high competition abilities; the possibility of it finding a deep-reef refuge there from fish predation; and its concomitant adaptation to this environment.     

Spatial variability in reef-fish assemblages in shallow and upper mesophotic coral ecosystems in the Philippines

The variability in reef-fish species assemblages was examined at three geographic locations in the Philippines (Apo, Abra and Patn), each showing varying levels of disturbances (low to high) at two depths, shallow-water reef (SWR; 8–20 m) and the upper mesophotic coral ecosystem (MCE; 30–35 m). Fish species assemblages varied among locations and between depths. Differences in fish assemblages among locations corresponded to the variability in benthic assemblages and levels of disturbances, wherein locations with higher coral cover and less disturbances had the highest fish species richness, abundance and biomass. Variation in fish assemblages between depths was also associated with changes in benthic assemblages and possibly inaccessibility to local fishing techniques. Fish species richness decreased with depth in all locations, but biomass increased only in the MCEs of Apo and Abra, which is a similar pattern exhibited in many MCEs. Our results suggest that despite location differences, depth had a relatively consistent influence on fish species assemblages, particularly in locations exposed to low and intermediate disturbance. Under high disturbance, MCEs exhibit similar vulnerability to SWRs.     

Microbiome variation in corals with distinct depth distribution ranges across a shallow–mesophotic gradient (15–85 m)

Mesophotic coral ecosystems (MCEs) are generally poorly studied, and our knowledge of lower MCEs (below 60 m depth) is largely limited to visual surveys. Here, we provide a first detailed assessment of the prokaryotic community associated with scleractinian corals over a depth gradient to the lower mesophotic realm (15–85 m). Specimens of three Caribbean coral species exhibiting differences in their depth distribution ranges (Agaricia grahamae, Madracis pharensis and Stephanocoenia intersepta) were collected with a manned submersible on the island of Curaçao, and their prokaryotic communities assessed using 16S rRNA gene sequencing analysis. Corals with narrower depth distribution ranges (depth-specialists) were associated with a stable prokaryotic community, whereas corals with a broader niche range (depth-generalists) revealed a higher variability in their prokaryotic community. The observed depth effects match previously described patterns in Symbiodinium depth zonation. This highlights the contribution of structured microbial communities over depth to the coral’s ability to colonize a broader depth range.     

Gametogenesis and fecundity of <Emphasis Type="Italic">Acropora tenella</Emphasis> (Brook 1892) in a mesophotic coral ecosystem in Okinawa,Japan

Mesophotic coral ecosystems (below 30–40 m depth) host a large diversity of zooxanthellate coral communities and may play an important role in the ecology and conservation of coral reefs. Investigating the reproductive biology of mesophotic corals is important to understand their life history traits. Despite an increase in research on mesophotic corals in the last decade, their reproductive biology is still poorly understood. Here, gametogenesis and fecundity of the Indo-Pacific mesophotic coral, Acropora tenella, were examined in an upper mesophotic reef (40 m depth) in Okinawa, Japan for the first time. Acropora tenella is a hermaphrodite with a single annual gametogenic cycle, and both oogenesis and spermatogenesis occurring for 11–12 and 5–6 months, respectively. Timing of spawning of this species was similar to other shallow Acropora spp. in the region. However, colonies had longer gametogenic cycles and less synchronous gamete maturation compared to shallow acroporids with spawning extended over consecutive months. Both the polyp fecundity (number of eggs per polyp) and gonad index (defined as the number of eggs per square centimeter) of A. tenella were lower than most acroporids. Our findings contribute to understanding of the life history of corals on mesophotic reefs and suggest that the reproductive biology of upper mesophotic corals is similar to that of shallow-water corals.     

Fitness consequences of habitat variability,trophic position,and energy allocation across the depth distribution of a coral-reef fish

Environmental clines such as latitude and depth that limit species’ distributions may be associated with gradients in habitat suitability that can affect the fitness of an organism. With the global loss of shallow-water photosynthetic coral reefs, mesophotic coral ecosystems (~30–150 m) may be buffered from some environmental stressors, thereby serving as refuges for a range of organisms including mobile obligate reef dwellers. Yet habitat suitability may be diminished at the depth boundary of photosynthetic coral reefs. We assessed the suitability of coral-reef habitats across the majority of the depth distribution of a common demersal reef fish (Stegastes partitus) ranging from shallow shelf (SS, <10 m) and deep shelf (DS, 20–30 m) habitats in the Florida Keys to mesophotic depths (MP, 60–70 m) at Pulley Ridge on the west Florida Shelf. Diet, behavior, and potential energetic trade-offs differed across study sites, but did not always have a monotonic relationship with depth, suggesting that some drivers of habitat suitability are decoupled from depth and may be linked with geographic location or the local environment. Feeding and diet composition differed among depths with the highest consumption of annelids, lowest ingestion of appendicularians, and the lowest gut fullness in DS habitats where predator densities were highest and fish exhibited risk-averse behavior that may restrict foraging. Fish in MP environments had a broader diet niche, higher trophic position, and higher muscle C:N ratios compared to shallower environments. High C:N ratios suggest increased tissue lipid content in fish in MP habitats that coincided with higher investment in reproduction based on gonado-somatic index. These results suggest that peripheral MP reefs are suitable habitats for demersal reef fish and may be important refuges for organisms common on declining shallow coral reefs.

     

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.     

Topography, substratum and benthic macrofaunal relationships on a tropical mesophotic shelf margin, central Great Barrier Reef, Australia

Habitats and ecological communities occurring in the mesophotic region of the central Great Barrier Reef (GBR), Australia, were investigated using autonomous underwater vehicle (AUV) from 51 to 145 m. High-resolution multibeam bathymetry of the outer-shelf at Hydrographers Passage in the central GBR revealed submerged linear reefs with tops at 50, 55, 80, 90, 100 and 130 m separated by flat, sandy inter-reefal areas punctuated by limestone pinnacles. Cluster analysis of AUV images yielded five distinct site groups based on their benthic macrofauna, with rugosity and the presence of limestone reef identified as the most significant abiotic factors explaining the distribution of macrofaunal communities. Reef-associated macrofaunal communities occurred in three distinct depth zones: (1) a shallow (<60 m) community dominated by photosynthetic taxa, notably scleractinian corals, zooxanthellate octocorals and photosynthetic sponges; (2) a transitional community (60–75 m) comprising both zooxanthellate taxa and azooxanthellate taxa (notably gorgonians and antipatharians); and (3) an entirely azooxanthellate community (>75 m). The effects of depth and microhabitat topography on irradiance most likely play a critical role in controlling vertical zonation on reef substrates. The lower depth limits of zooxanthellate corals are significantly shallower than that observed in many other mesophotic coral ecosystems. This may be a result of resuspension of sediments from the sand sheets by strong currents and/or a consequence of cold water upwelling.     

Higher species richness of octocorals in the upper mesophotic zone in Eilat (Gulf of Aqaba) compared to shallower reef zones

Mesophotic coral-reef ecosystems (MCEs), which comprise the light-dependent communities of corals and other organisms found at depths between 30 and ~ 150 m, have received very little study to date. However, current technological advances, such as remotely operated vehicles and closed-circuit rebreather diving, now enable their thorough investigation. Following the reef-building stony corals, octocorals are the second most common benthic component on many shallow reefs and a major component on deep reefs, the Red Sea included. This study is the first to examine octocoral community features on upper MCEs based on species-level identification and to compare them with the shallower reef zones. The study was carried out at Eilat (Gulf of Aqaba, northern Red Sea), comparing octocoral communities at two mesophotic reefs (30–45 m) and two shallow reef zones (reef flat and upper fore-reef) by belt transects. A total of 30 octocoral species were identified, with higher species richness on the upper MCEs compared to the shallower reefs. Although the MCEs were found to host a higher number of species than the shallower reefs, both featured a similar diversity. Each reef zone revealed a unique octocoral species composition and distinct community structure, with only 16% of the species shared by both the MCEs and the shallower reefs. This study has revealed an almost exclusive dominance of zooxanthellate species at the studied upper MCE reefs, thus indicating an adequate light regime for photosynthesis there. The findings should encourage similar studies on other reefs, aimed at understanding the spatiotemporal features and ecological role of octocorals in reef ecosystems down to the deepest limit of the MCEs.     

Geomorphology of mesophotic coral ecosystems: current perspectives on morphology, distribution, and mapping strategies

This paper presents a general review of the distribution of mesophotic coral ecosystems (MCEs) in relationship to geomorphology in US waters. It was specifically concerned with the depth range of 30–100 m, where more than 186,000 km² of potential seafloor area was identified within the US Gulf of Mexico/Florida, Caribbean, and main Hawaiian Islands. The geomorphology of MCEs was largely inherited from a variety of pre-existing structures of highly diverse origins, which, in combination with environmental stress and physical controls, restrict the distribution of MCEs. Sea-level history, along with depositional and erosional processes, played an integral role in formation of MCE settings. However, mapping the distribution of both potential MCE topography/substrate and existing MCE habitat is only beginning. Mapping techniques pertinent to understanding morphology and MCE distributions are discussed throughout this paper. Future investigations need to consider more cost-effective and remote methods (such as autonomous underwater vehicles (AUVs) and acoustics) in order to assess the distribution and extent of MCE habitat. Some understanding of the history of known MCEs through coring studies would help understand their initiation and response to environmental change over time, essential for assessing how they may be impacted by future environmental change.     

Reef habitats and associated sessile-benthic and fish assemblages across a euphotic–mesophotic depth gradient in Isla Desecheo, Puerto Rico

Quantitative surveys of sessile benthos and fish populations associated with reef habitats across a 15–50 m depth gradient were performed by direct diver observations using rebreathers at Isla Desecheo, Puerto Rico. Statistically significant differences between depths were found for total live coral, total coral species, total benthic algae, total sponges and abiotic cover. Live coral cover was higher at the mid-shelf (20 m) and shelf-edge (25 m) stations, whereas benthic algae and sponges were the dominant sessile-benthic assemblage at mesophotic stations below 25 m. Marked shifts in the community structure of corals and benthic algae were observed across the depth gradient. A total of 119 diurnal, non-cryptic fish species were observed across the depth gradient, including 80 species distributed among 7,841 individuals counted within belt-transects. Fish species richness was positively correlated with live coral cover. However, the relationship between total fish abundance and live coral was weak. Abundance of several numerically dominant fish species varied independently from live coral cover and appeared to be more influenced by depth and/or habitat type. Statistically significant differences in the rank order of abundance of fish species at euphotic vs mesophotic stations were detected. A small assemblage of reef fishes that included the cherubfish, Centropyge argi, sunshine chromis, Chromis insolata, greenblotch parrotfish, Sparisoma atomarium, yellowcheek wrasse, Halichoeres cyanocephalus, sargassum triggerfish, Xanthichthys ringens, and the longsnout butterflyfish, Chaetodon aculeatus was most abundant or only present from stations deeper than 30 m, and thus appear to be indicator species of mesophotic habitats.     

Mesophotic depths as refuge areas for fishery-targeted species on coral reefs

Coral reefs are subjected to unprecedented levels of disturbance with population growth and climate change combining to reduce standing coral cover and stocks of reef fishes. Most of the damage is concentrated in shallow waters (<30 m deep) where humans can comfortably operate and where physical disturbances are most disruptive to marine organisms. Yet coral reefs can extend to depths exceeding 100 m, potentially offering refuge from the threats facing shallower reefs. We deployed baited remote underwater stereo-video systems (stereo-BRUVs) at depths of 10–90 m around the southern Mariana Islands to investigate whether fish species targeted by fishing in the shallows may be accruing benefits from being at depth. We show that biomass, abundance and species richness of fishery-targeted species increased from shallow reef areas to a depth of 60 m, whereas at greater depths, a lack of live coral habitat corresponded to lower numbers of fish. The majority of targeted species were found to have distributions that ranged from shallow depths (10 m) to depths of at least 70 m, emphasising that habitat, not depth, is the limiting factor in their vertical distribution. While the gradient of abundance and biomass versus depth was steepest for predatory species, the first species usually targeted by fishing, we also found that fishery-targeted herbivores prevailed in similar biomass and species richness to 60 m. Compared to shallow marine protected areas, there was clearly greater biomass of fishery-targeted species accrued in mesophotic depths. Particularly some species typically harvested by depth-limited fishing methods (e.g., spearfishing), such as the endangered humphead wrasse Cheilinus undulatus, were found in greater abundance on deeper reefs. We conclude that mesophotic depths provide essential fish habitat and refuge for fishery-targeted species, representing crucial zones for fishery management and research into the resilience of disturbed coral reef ecosystems.