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Front. Mar. Sci. | doi: 10.3389/fmars.2019.00536

Corals in the mesophotic zone (40-115 m) at the barrier reef complex from San Andrés Island (Southwestern Caribbean)

  • 1Biological Sciences, University of Los Andes, Colombia, Colombia
  • 2University of Los Andes, Colombia, Colombia
  • 3Universidad Nacional de Colombia, Colombia
  • 4Corporación para el Desarrollo Sostenible del Archipiélago de San Andrés, Providencia y Santa Catalina (CORALINA), Colombia

Abstract
This data report included the collection and zonation of corals sensu lato (stony corals, hydrocorals, black corals and octocorals) from mesophotic coral ecosystems (MCEs). The ultimate goal was to contribute to the understanding of sensible and vulnerable environments, in the SeaFlower Biosphere reserve, in which San Andrés Island is immersed. The dataset included 113 specimens from 33 species collected below 40 m (8 black corals, 1 lace coral, 8 scleractinian corals, and 16 gorgonian corals). Zooxanthellate corals such Agaricia undata are replaced below 80 m by azooxanthellate cup corals, including Javania cailleti, Phacelocyathus flos, Balanophyllia cyathoides and Thalamophyllia riisei forma solida. The lower mesophotic reef is also the habitat of black corals (e.g., Stichopathes spp., Rhipidipathes colombiana and Tanacetipathes hirta) and hydrocorals (Stylaster duchassaingi) but the most abundant group are gorgonian corals.

Background
Shallow reefs in the SeaFlower Biosphere Reserve, even at the remotest bank atolls, are showing a steady decline in coral cover overall health condition during the last twenty years (Sánchez et al. 2019b). Mesophotic Coral Ecosystems (MCEs), located between 30 and >150 m of water depth, may act as a refuge of coral population due to favorable conditions in this less altered environment (Bongaerts et al. 2010). Particularly, in our study area, San Andres island, populations of corals reaching the lower (>60 m) mesophotic zone, 40 to 90 m, such as Agaricia undata exhibit genetic connectivity throughout its depth range (Gonzalez-Zapata et al. 2018a), supporting this zone as a major reef-building coral refuge. It has been suggested that depending on the type of endosymbiont, corals can acclimatize to deeper depths (Ziegler et al. 2015), which was in fact observed in the bacteria population from A. undata in San Andrés Island (Gonzalez-Zapata et al. 2018a). In addition, many species of fish, corals and other invertebrates from shallow reefs are also found in mesophotic reefs and it is proposed that these populations could contribute to the recovery of affected populations in shallower areas following a disturbance (Kramer et al. 2019).

There are potential new species of corals and associated species, including common shallow-water fauna, in mesophotic reefs (Luck et al. 2013; Petrescu et al. 2014), which urges studies surveying coral diversity at these depths. However, these reefs have been rarely explored below 60 m in water depth. The dataset presented in this study, provide the first exploration of the mesophotic zone (40 to 120 m deep) in an oceanic barrier reef complex (SeaFlower Biosphere Reserve), San Andrés Island, Southwestern Caribbean. The dataset presented here includes the collection information, and community composition of corals sensu lato (stony corals, hydrocorals, black corals and octocorals). The ultimate goal was to contribute to the understanding of sensible and vulnerable environments, in the SeaFlower Biosphere reserve, in which San Andrés island is immersed.

Data Collection

We concentrated the study in the fore-reef slope of San Andrés island barrier reef complex near the location called “Trampa de Tortugas” or “Trampa Tortuga”, which offered a number of logistic advantages. The site bears a shelter to anchor the supporting boat despite its location on the fore-reef terrace. In addition, this site provides the only accessible glimpse of the oldest slope of the barrier-reef complex of San Andrés (Geister 1975; Díaz, J.M. et al. 1995; Diaz et al. 1996). We explored the reef using Close-Circuit Rebreather (CCR) (Megalodon, Inner Space Systems) and hypoxic trimix techniques (e.g., 11% Oxygen and 60% Helium) with complete bail-out support for each diver. At the site, we installed a mooring block at 24 m as a gas station that had high oxygen bail-outs (O2 96%) and from where we tied a 200m long reel down to a depth of 114 m. The reel was used to safely explore down the site and to have an easy return to shallower waters. Seven dives were planned with a maximum of 20-30 min of bottom time and the longest dives spanned 133-328 minutes including decompression stops. The sampling included digital imagery (NikonTM D7000, Nikkor micro 60 mm lens, Sea & SeaTM YS-D1 strobe and AquaticaTM AD7000 housing) and 115 voucher specimens (dry and ethanol 96%), which were deposited at Museo de Historia ANDES (Bogotá, Colombia) (Table 1).

Coral identifications. All specimens were examined under the optical and/or compound microscope for morphological identification and contrasted against species keys (if available) and/or taxonomic descriptions. For scleractinian corals we used (Cairns 2000); for Stylasteridae (Cairns et al. 1986); for black corals (Opresko & Sánchez 2005); for octocorals (Bayer 1961; Bayer & Grasshoff 1994, 1995; Sánchez & Wirshing 2005; Sánchez 2009). In addition, several species accounts for Colombia were also useful in species identification (Flórez et al. 2010; Chacón-Gómez et al. 2012; Santodomingo et al. 2013). When needed, Scanning Electron Microscopy (SEM) images were obtained at the microscopy laboratory in the Universidad de los Andes to increase the certainty of identifications.

Dataset Outcomes and Discussion
The dataset included 115 specimens from 33 species collected below 40 m (8 black corals, 1 lace coral, 8 scleractinian corals, and 16 gorgonian corals: Table 1). Exploring “Trampa de Tortugas”, we noticed the disappearance of most reef-building corals and zooxanthellate octocorals at different depths. Some reef-building corals, notably Mycethophyllia reesi, Agaricia undata, A. fragilis and Madracis sp., distributed well into the lower mesophotic zone (~90m) and are characterized by an increase in the presence of the euendolithic algae Ostreobium, which is clearly observable at the colony surface (Gonzalez-Zapata et al. 2018b). These colonial corals are replaced below 80m by azooxanthellate cup corals, including Javania cailleti, Phacelocyathus flos, Balanophyllia cyathoides and Thalamophyllia riisei forma solida (Fig. 1). A noteworthy observation was the presence of Ostreobium at the basal portion of T. riisei cup-corals.

The lower mesophotic reef is also the habitat of many unique black corals (e.g., Rhipidipathes colombiana and Tanacetipathes hirta) and hydrocorals (Stylaster duchassaingi) but the most abundant group are azoxanthellate octocorals mostly from the Plexauridae family (Sánchez 2017; Sánchez et al. 2019a). The species replacement is enhanced by short terraces intertwined with abrupt steps at every 10 m starting at 60, 90, 100 and 115 m, at ‘Trampa Tortuga’ reef in San Andrés island. On the leeward side of the island, there is parallel slope sand corridor (mostly from Halimeda copiosa flocks) following the reef slope, which end at about 60-80, where the reef growth continues. The deepest zooxanthellate gorgonian coral was Antillogorgia hystrix (65 m), followed by Eunicea pinta (55 m). Occasionally, Muricea laxa, A. bipinnata and A. americana were seen at depths of about 40 m. These zooxanthellate octocorals share habitat with some azooxanthellate octocorals such as Iciligorgia schrammi and diverse ellisellids (Sánchez et al. 2019a).

Black corals (Antipatharia) are also common from 30 m down to the lower mesophotic area(Bo et al. 2019). The most abundant black corals are Antipathes furcata (Fig. 1A), A. caribbeana, A. atlantica (Fig. 1B), Plumapathes pennacea, Stichopathes lutkeni and S. occidentalis. Wire corals, Stichopathes spp., with colonies reaching more than 2 m long were seen in high densities of to have more than 10 colonies per square meter (Fig. 1C-D). Below 70 m, the aforementioned black corals are less seen and other species emerge such as Rhipidipathes colombiana, first seen off the Colombian coast (Opresko & Sánchez 2005), and Tanacetipathes hirta. There is also a great amount of wire corals from species we could not identify and probably comprise new undescribed species. Despite the clear characters of S. lutkeni and S. occidentalis under the electron microscope, there were specimens, Stichopathes sp., with conspicuously smaller spines not found in any other species described for this region (Fig. 1H).

The most unexpected finding comprised a number of new records for several deep-sea corals, which have been usually found on deeper waters. Stylaster duchassaingi Pourtalès, 1867, a hydrocoral (Stylasteridae) was observed from 80 to 115 m forming seafan colonies up to 40 cm in height (Figure 1I-K). This is the southernmost record of the species and one of the shallower observations in its range. Stylaster roseus is commonly observed in the same reef but above 40 m (JAS, personal observation). San Andrés island is the only coral reef complex so far in the Caribbean with two documented species of Stylaster.

As expected, the exploration of the lower mesophotic zone uncovered a great amount of new species records and potential discoveries (e.g., Stichopathes sp.). In addition, this is the first time that many of the species have been ever seen and photographed in their natural environment (Sánchez et al. 2019a). Continuing research in this environment will enrich the ecology, systematics, and conservation of understudied corals such as cup corals. For instance, the Thallamophyllia riisei cup coral found in San Andrés is extremely different to the reported T. riisei from the Colombian coast (Flórez et al. 2010), which is colonial with great differences in morphological traits. It is worth mention that this is the product of only seven dives (and less than 140 minutes of total bottom time) for San Andres island.

Reuse Potential
The specimens collected and properly curated (deposited and IN-ANDES in Bogota, Colombia) comprise a valuable resource for further systematic studies in several groups of corals, which could comprise new species. In addition, it is important to mention that the specimens in this data report have not been monitored in the past, giving the logistic constraints of deep-sea diving. As the interest in MCEs increases biodiversity data becomes crucial for comparisons.

Data Availability
Data package title: “Biodiversidad y Conectividad de los arrecifes mesofóticos (30-120m) de la costa Caribe colombiana”
Resource link: https://ipt.biodiversidad.co/cr-sib/resource.do?r=0359_mesofoticos_20190729
Data format:
Darwin Core Archive (DwC-A)
Description:
The data presented here corresponds to coral specimens (Cnidaria: Anthozoa and Hydrozoa) collected between 40 and 115 m in the mesophotic corals ecosystems from San Andrés island (SeaFlower Biosphere Reserve).

Author contributions
JAS, LFD, JA and NB conceived the study. JAS, JA and NB collected the data. FG-Z, AS, DV, ALP & JAS identified and processed the material. JAS wrote the report with the help of LFD, FG-Z and NB. All authors read and accepted the manuscript.

Funding
This work was supported by an agreement between Corporación para el Desarrollo Sostenible del Departamento Archipiélago de San Andrés Providencia y Santa Catalina, CORALINA-Universidad de los Andes (Convenios No. 13, 2014 and No. 21, 2015: “Protección y conservación de los recursos de la biodiversidad y de los ecosistemas estratégicos dentro de la Reserva de Biosfera Seaflower” Fondo de Compensación Ambiental FCA del Ministerio de Ambiente y Desarrollo Sostenible). Additional funding was possible thanks to the University of Los Andes (Vicerrectoría de Investigaciones and Facultad de Ciencias) and COLCIENCIAS (Project code 120465944147).

Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments
The support from Bluelife dive shop (family Garcia) was fundamental to accomplish this study. The San Andres Hospital kindly supplied medical oxygen for CCR. We are very grateful with Gregg Stanton, Wakulla Dive Center, for continuing support and advise for deep diving. We are thankful with Fabian García, Santiago Herrera, Mariana Gnecco, Manu Forero, Federico Botero and Camilo Martinez for fieldwork support. We recognize the participation and support
from local communities.

Keywords: Mesophotic Coral Ecosystem (MCE), coral, Octocoral, black coral, Stylaster, Scleractinia, San Andrés Island, Caribbean

Received: 05 Jun 2019; Accepted: 15 Aug 2019.

Copyright: © 2019 Sanchez, Gonzalez-Zapata, Dueñas, Andrade, Pico-Vargas, Sarmiento and Bolaños. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Juan A. Sanchez, University of Los Andes, Colombia, Biological Sciences, Bogotá, 111711, DC, Colombia, juansanc@uniandes.edu.co