Deep reefs are not refugium for shallow‐water fish communities in the southwestern Atlantic

1. The deep reef refugia hypothesis (DRRH) predicts that deep reef ecosystems may act as refugium for the biota of disturbed shallow waters. Because deep reefs are among the most understudied habitats on Earth, formal tests of the DRRH remain scarce. If the DRRH is valid at the community level, the diversity of species, functions, and lineages of fish communities of shallow reefs should be encapsulated in deep reefs.
2. We tested the DRRH by assessing the taxonomic, functional, and phylogenetic diversity of 22 Brazilian fish communities between 2 and 62 m depth. We partitioned the gamma diversity of shallow (<30 m) and deep reefs (>30 m) into independent alpha and beta components, accounted for species’ abundance, and assessed whether beta patterns were mostly driven by spatial turnover or nestedness.
3. We recorded 3,821 fishes belonging to 85 species and 36 families. Contrary to DRRH expectations, only 48% of the species occurred in both shallow and deep reefs. Alpha diversity of rare species was higher in deep reefs as expected, but alpha diversity of typical and dominant species did not vary with depth. Alpha functional diversity was higher in deep reefs only for rare and typical species, but not for dominant species. Alpha phylogenetic diversity was consistently higher in deep reefs, supporting DRRH expectations.
4. Profiles of taxonomic, functional, and phylogenetic beta diversity indicated that deep reefs were not more heterogeneous than shallow reefs, contradicting expectations of biotic homogenization near sea surface. Furthermore, pairwise beta‐diversity analyses revealed that the patterns were mostly driven by spatial turnover rather than nestedness at any depth.
5. Conclusions. Although some results support the DRRH, most indicate that the shallow‐water reef fish diversity is not fully encapsulated in deep reefs. Every reef contributes significantly to the regional diversity and must be managed and protected accordingly.

     

Allelopathy in the tropical alga Lobophora variegata (Phaeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs?

Macroalgal phase shifts on Caribbean reefs have been reported with increasing frequency, and recent reports of these changes on mesophotic coral reefs have raised questions regarding the mechanistic processes behind algal population expansions to deeper depths. The brown alga Lobophora variegata is a dominant species on many shallow and deep coral reefs of the Caribbean and Pacific, and it increased in percent cover (>50%) up to 61 m on Bahamian reefs following the invasion of the lionfish Pterois volitans. We examined the physiological and ecological constraints contributing to the spread of Lobophora on Bahamian reefs across a mesophotic depth gradient from 30 to 61 m, pre‐ and post‐lionfish invasion. Results indicate that there were no physiological limitations to the depth distribution of Lobophora within this range prior to the lionfish invasion. Herbivory by acanthurids and scarids in algal recruitment plots at mesophotic depths was higher prior to the lionfish invasion, and Lobophora chemical defenses were ineffective against an omnivorous fish species. In contrast, Lobophora exhibited significant allelopathic activity against the coral Montastraea cavernosa and the sponge Agelas clathrodes in laboratory assays. These data indicate that when lionfish predation on herbivorous fish released Lobophora from grazing pressure at depth, Lobophora expanded its benthic cover to a depth of 61 m, where it replaced the dominant coral and sponge species. Our results suggest that this chemically defended alga may out‐compete these species in situ, and that mesophotic reefs may be further impacted in the near future as Lobophora continues to expand to its compensation point.     

Incident light and morphology determine coral productivity along a shallow to mesophotic depth gradient

1. While the effects of irradiance on coral productivity are well known, corals along a shallow to mesophotic depth gradient (10–100 m) experience incident irradiances determined by the optical properties of the water column, coral morphology, and reef topography.
2. Modeling of productivity (i.e., carbon fixation) using empirical data shows that hemispherical colonies photosynthetically fix significantly greater amounts of carbon across all depths, and throughout the day, compared with plating and branching morphologies. In addition, topography (i.e., substrate angle) further influences the rate of productivity of corals but does not change the hierarchy of coral morphologies relative to productivity.
3. The differences in primary productivity for different coral morphologies are not, however, entirely consistent with the known ecological distributions of these coral morphotypes in the mesophotic zone as plating corals often become the dominant morphotype with increasing depth.
4. Other colony‐specific features such as skeletal scattering of light, Symbiodiniaceae species, package effect, or tissue thickness contribute to the variability in the ecological distributions of morphotypes over the depth gradient and are captured in the metric known as the minimum quantum requirements.
5. Coral morphology is a strong proximate cause for the observed differences in productivity, with secondary effects of reef topography on incident irradiances, and subsequently the community structure of mesophotic corals.

     

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.     

New records of the snow bass Serranus chionaraia (Perciformes: Serranidae) confirm an established population in the Brazilian Province

The snow bass Serranus chionaraia is a small-bodied reef fish presumed to be restricted to the Caribbean Province, with a single specimen captured south of the Amazon River mouth. Recent surveys with baited remote underwater stereo-video systems detected the species c. 1900 km southward. Meristic and morphometric characters of two specimens examined in this study confirmed the species identity, which greatly extends the speciesʼ range southward on the eastern coast of Brazil and indicates the presence of an established population of S. chionaraia in the Brazilian Province.     

Azooxanthellate? Most Hawaiian black corals contain Symbiodinium

The ecological success of shallow-water reef-building corals (Hexacorallia: Scleractinia) is framed by their intimate endosymbiosis with photosynthetic dinoflagellates in the genus Symbiodinium (zooxanthellae). In contrast, the closely related black corals (Hexacorallia: Anthipatharia) are described as azooxanthellate (lacking Symbiodinium), a trait thought to reflect their preference for low-light environments that do not support photosynthesis. We examined 14 antipatharian species collected between 10 and 396 m from Hawai'i and Johnston Atoll for the presence of Symbiodinium using molecular typing and histology. Symbiodinium internal transcribed spacer-2 (ITS-2) region sequences were retrieved from 43 per cent of the antipatharian samples and 71 per cent of the examined species, and across the entire depth range. The ITS-2 sequences were identical or very similar to those commonly found in shallow-water scleractinian corals throughout the Pacific. Histological analyses revealed low densities of Symbiodinium cells inside antipatharian gastrodermal tissues (0-92 cells mm(-3)), suggesting that the Symbiodinium are endosymbiotic. These findings confirm that the capacity to engage in endosymbiosis with Symbiodinium is evolutionarily conserved across the cnidarian subclass Hexacorallia, and that antipatharians associate with Symbiodinium types found in shallow-water scleractinians. This study represents the deepest record for Symbiodinium to date, and suggests that some members of this dinoflagellate genus have extremely diverse habitat preferences and broad environmental ranges.     

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.     

Repeated invasions into the twilight zone: evolutionary origins of a novel assemblage of fishes from deep Caribbean reefs

Mesophotic and deeper reefs of the tropics are poorly known and underexplored ecosystems worldwide. Collectively referred to as the ‘twilight zone’, depths below ~30–50 m are home to many species of reef fishes that are absent from shallower depths, including many undescribed and endemic species. We currently lack even a basic understanding of the diversity and evolutionary origins of fishes on tropical mesophotic reefs. Recent submersible collections in the Caribbean have provided new specimens that are enabling phylogenetic reconstructions that incorporate deep‐reef representatives of tropical fish genera. Here, we investigate evolutionary depth transitions in the family Gobiidae (gobies), the most diverse group of tropical marine fishes. Using divergence‐time estimation coupled with stochastic character mapping to infer the timing of shallow‐to‐deep habitat transitions in gobies, we demonstrate at least four transitions from shallow to mesophotic depths. Habitat transitions occurred in two broad time periods (Miocene, Pliocene–Pleistocene), and may have been linked to the availability of underutilized niches, as well as the evolution of morphological/behavioural adaptations for life on deep reefs. Further, our analysis shows that at least three evolutionary lineages that invaded deep habitats subsequently underwent speciation, reflecting another unique mode of radiation within the Gobiidae. Lastly, we synthesize depth distributions for 95 species of Caribbean gobies, which reveal major bathymetric faunal breaks at the boundary between euphotic and mesophotic reefs. Ultimately, our study is the first rigorous investigation into the origin of Caribbean deep‐reef fishes and provides a framework for future studies that utilize rare, deep‐reef specimens.     

Fish biodiversity of Saint Peter and Saint Paulʼs Archipelago,Mid-Atlantic Ridge,Brazil: new records and a species database

Saint Peter and Saint Paul's Archipelago (SPSPA), one of the smallest and most isolated island groups in the world, is situated on the Mid-Atlantic Ridge, between Brazil and the African continent. SPSPA has low species richness and high endemism; nonetheless, the diversity of fishes from deep habitats (>30 m depth) had not been previously studied in detail. Several expeditions conducted between 2009 and 2018 explored the shallow and deep reefs of SPSPA using scuba, closed-circuit rebreathers, manned submersibles, baited remote underwater stereo-videos (stereo-BRUV) and fishing between 0 and 1050 m depth. These expeditions yielded 41 new records of fishes for SPSPA: 9 in open waters, 9 in shallow waters (0–30 m), 8 in mesophotic ecosystems (30–150 m) and 15 in deeper reefs (>150 m). Combined with literature records of adult pelagic, shallow and deep-reef species, as well as larvae, the database of the fish biodiversity for SPSPA currently comprises 225 species (169 recorded as adult fishes and 79 as larvae, with 23 species found in both stages). Most of them (112) are pelagic, 86 are reef-associated species and 27 are deep-water specialists. Species accumulation curves show that the number of fish species has not yet reached an asymptote. Whereas the number of species recorded in SPSPA is similar to that in other oceanic islands in the Atlantic Ocean, the proportion of shorefishes is relatively lower, and the endemism level is the third highest in the Atlantic. Twenty-nine species are listed as threatened with extinction. Observations confirm the paucity of top predators on shallow rocky reefs of the island, despite the presence of several pelagic shark species around SPSPA. Because all of the endemic species are reef associated, it is argued that the new marine-protected areas created by the Brazilian government do not ensure the protection and recovery of SPSPA's biodiversity because they allow exploitation of the most vulnerable species around the archipelago itself. This study suggests a ban on reef fish exploitation inside an area delimited by the 1000 m isobath around the islands (where all known endemics are concentrated) as the main conservation strategy to be included in the SPSPA management plan being prepared by the Brazilian government.     

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.     

Assembly rules of coral reef fish communities along the depth gradient

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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.     

Unexpected diversity and a new species of Epizoanthus (Anthozoa,Hexacorallia) attached to eunicid worm tubes from the Pacific Ocean

Epizoanthus species are generally found in association with other marine invertebrates such as hermit crabs and gastropods. Although Epizoanthus spp. are relatively common, there is limited information about their diversity and ecology due to their habitats or hosts, often being below the depths of SCUBA diving (>~50 m). In particular, the Epizoanthus fauna of the Indo-Pacific Ocean remains poorly understood. In this study, the diversity of Epizoanthus species associated with eunicid worm tubes from shallow waters in the Pacific Ocean we investigated using molecular analyses (mitochondrial cytochrome oxidase subunit 1 = COI, mitochondrial 16S ribosomal DNA = mt 16S-rDNA, nuclear internal transcribed spacer region of ribosomal DNA = ITS-rDNA) combined with morphological and ecological data. The combined data set leads us to describe two new species; Epizoanthus inazuma sp. n. and Epizoanthus beriber sp. n. Both new species are found in low-light environments: Epizoanthus inazuma sp. n. on mesophotic coral reef slopes and reef floors, or on the sides of overhangs; Epizoanthus beriber sp. n. has only been found in caves. Morphological characteristics of these two new species are very similar to Epizoanthus illoricatus Tischbierek, 1930 but the two new species are genetically distinct. Mesentery numbers and coloration of polyps may be useful diagnostic characteristics among eunicid-associated Epizoanthus species. These results demonstrate that there is high potential for other potentially undescribed zoantharian species, particularly in underwater cave habitats.