Coral-dwelling gall crabs ascribed to the family Cryptochiridae Paulson, 1875 are obligate symbionts of a wide range of scleractinian corals [
1,
2]. Although these crabs inhabit coral reefs, they are often overlooked because of their small size and cryptic lifestyle [
3,
4]. Moreover, most of the research on this family has focused on shallow-water species, although gall crabs are known to occur as deep as 512 m [
5], and crab dwellings have been observed in coral specimens obtained from 620–635 m depths [
6]. Strictly deep-sea cryptochirids have been reported in association with the coral families Dendrophylliidae Gray, 1847 from Walvis Ridge in the southern Atlantic Ocean, Mayotte, Walters Shoal (off Madagascar), and New Caledonia [
6,
7], and Caryophylliidae Dana, 1846 from Madagascar and the Philippines [
8]. There are only a few records of gall crabs in the mesophotic zone (~30–150 m depth
sensu [
9]), all associated with zooxanthellate species of the coral family Agariciidae Gray, 1847 [
4,
8,
10,
11]. Agariciids can be a dominant component of the Mesophotic Coral Ecosystems (MCEs) worldwide (see [
9] for an overview). In the Atlantic Ocean, the gall crab
Opecarcinus hypostegus (Shaw & Hopkins, 1977) is known to occur in mesophotic waters off Curaçao, where it was recorded from
Agaricia lamarcki Milne Edwards & Haime, 1951, at approximately a 60 m depth [
11]. Van Tienderen and Van der Meij (2016) [
4] showed that
O. hypostegus, associated with Atlantic agariciids, has a higher prevalence at deeper depths, following the vertical distribution of its hosts. In the Pacific Ocean, the gall crab
Luciades agana Kropp and Manning, 1996 was recorded on
Leptoseris papyracea (Dana, 1846) from Guam (128–137 m depth) and Tonga (34 m depth) [
8,
10]. The genus
Luciades is likely a junior synonym of
Opecarcinus Kropp & Manning, 1987, a genus currently under revision (Xu et al. in prep). In the shallow waters of the Indo-Pacific Ocean,
Opecarcinus is known to inhabit the genus
Leptoseris Milne Edwards and Haime, 1849 [
12] which occurs from the shallow coral reefs to the MCEs [
9,
13]. However,
Opecarcinus has never been recorded at mesophotic depths from the Indian Ocean or the Red Sea.
In order to characterize the benthic diversity in the NEOM area, the largest of the Saudi Arabia development projects encompassing the Gulf of Aqaba and Northern Red Sea, Remotely Operated Vehicle (ROV) explorations at mesophotic depths were carried out from October to November 2020 during the Red Sea Deep Blue (RSDB) expedition onboard the M/V OceanXplorer. During a survey with the Argus Mariner XL ROV on the 28th of October 2020, a coral colony of
Leptoseris cf.
mycetoseroides Wells, 1954 was observed and collected in the Northern Red Sea (27°42′26.4″ N, 35°10′06.0″ E) at 89 m depth (
Figure 1A). On its surface, two characteristic canopy-like tunnels with a crescent-shaped opening typical for the genus
Opecarcinus were visible [
11,
14] (
Figure 1B). A male and female crab were extracted from the colony, and based on their overall morphology (vase-shaped carapace longer than broad, widest posterior to mid-length, deflected anteriorly and convex in lateral view, see [
2]), the crabs were identified to belong to the genus
Opecarcinus. At King Abdullah University of Science and Technology (KAUST), high-quality DNA was extracted using a DNAeasy
® Blood and Tissue kit (Qiagen Inc., Hilden, Germany), following the manufacturer’s protocol, from the muscle tissue of the fifth pereiopod. The DNA was amplified with the universal primers LCO1490 and HCO2198 [
15] and then sequenced in forward and reverse directions using an ABI 3730xl DNA analyzer (Applied Biosystems, Foster City, CA, USA). Forward and reverse sequences were assembled and edited using Geneious Prime 2019 (Biomatters) and BioEdit Sequence Alignment Editor 7.2.6 [
16]. The final nucleotide sequence was blasted against the dataset of Xu et al. (2022) [
12] and had 100% identity with
Opecarcinus SET.04, a species currently under description (Xu et al. in prep).
The circumtropical genus
Opecarcinus includes ca. 25 species, all associated with the coral family Agariciidae. Depth records span from shallow to mesophotic waters (1–60 m) [
3,
11,
12,
17,
18]. Nine cryptochirid species, including
Opecarcinus SET.04, have been recorded to date from the shallow waters (0–30 m) of the Saudi Arabian Red Sea [
12]. Hence, our discovery represents a new depth record from the Saudi Arabian Red Sea of the genus
Opecarcinus, specifically of the soon-to-be-described
Opecarcinus SET.04, and the deepest record for
Opecarcinus to date. Our findings further reconfirm the depth range flexibility of
Opecarcinus species (see also [
11]). Moreover, a study in Hawai’i showed that most brachyuran crab assemblages are highly stratified by depth, with deeper reefs hosting different brachyuran communities than the shallower reefs [
19]. The depth generalist
Opecarcinus SET.04 found in this study represents an exception, highlighting that it is likely the gall crabs’ host specificity that influences their depth range.
The RSDB expedition allowed us to explore and assess the marine biodiversity at mesophotic depths in the NEOM marine area. The species richness of coral reef taxa changes with depth, shaping distinct assemblages in mesophotic coral ecosystems [
20]. Little is known about the effects of depth on reef-affiliated invertebrates, which are some of the most understudied taxa in reef ecosystems. In order to understand the diversity of coral reef assemblages at mesophotic depths and to better protect this low-light environment, further mesophotic explorations, focusing on less studied components of the reef-associated fauna, are required.
Author Contributions
ROV sampling and processing, S.V., F.B., T.I.T., F.M., G.C. and S.J.P.; analyses, S.V.; conceptualization and supervision, S.V., S.E.T.v.d.M. and F.B.; writing—original draft preparation, S.V., S.E.T.v.d.M. and F.B.; writing—review and editing, S.V., S.E.T.v.d.M., T.I.T., F.M., G.C., S.J.P., A.A.E., M.R. and F.B.; funding, A.A.E. and F.B. All authors have read and agreed to the published version of the manuscript.
Funding
The research expedition was funded by NEOM. The material and KAUST team logistics and molecular analyses were supported by KAUST (award FCC/1/1973-50-01 and baseline research funds to F. Benzoni). G. Chimienti was supported by the Italian Ministry of Education, University and Research (PON 2014–2020, Grant AIM 1807508-1, Linea 1).
Institutional Review Board Statement
Not applicable.
Data Availability Statement
The genetic sequence data that support this study’s finding are openly available in GenBank of NCBI under the accession number OQ941777.
Acknowledgments
This research was undertaken in accordance with the policies and procedures of the King Abdullah University of Science and Technology (KAUST). Permission relevant for KAUST to undertake the research was obtained from the applicable governmental agencies in the Kingdom of Saudi Arabia. We thank NEOM for facilitating and coordinating the Red Sea Deep Blue expedition and, specifically, in addition to A.A.E., Thamer Habis, Justin Myner, Paul Marshall, Giacomo Palavicini, Peter Mackelworth, and Abdulaziz Alghamdi. We want to thank OceanX and the crew of OceanXplorer for their operational and logistical support for the duration of this expedition. In particular, we would like to acknowledge Andrew Craig, Olaf Dieckoff, and Ewan Bason for sample collection and OceanX for support of scientific operations on board OceanXplorer. We also wish to thank OceanX Media for documenting and communicating the scientific outcomes of the RSDB expedition with the larger public. Finally, we thank the KAUST Sanger Sequencing Core Lab for helping with sequencing.
Conflicts of Interest
No potential conflict of interest was reported by the authors.
References
- Fize, A.; Serène, R. Les Hapalocarcinidés du Viet-Nam; Sèptieme Série; Archives du Museum national d’Histoire naturelle: Paris, France, 1857; volume 5, pp. i–xiii + 1–202, pls. I–XVIII. [Google Scholar]
- Kropp, R.K. Revision of the genera of gall crabs (Crustacea: Cryptochiridae) occurring in the Pacific Ocean. Pac. Sci. 1990, 44, 94–95. [Google Scholar]
- Hoeksema, B.W.; Van der Meij, S.E.T. Gall crab city: An aggregation of endosymbiotic crabs inhabiting a colossal colony of Pavona clavus. Coral Reefs 2013, 32, 59. [Google Scholar] [CrossRef]
- van Tienderen, K.M.; van der Meij, S.E.T. Occurrence patterns of coral-dwelling gall crabs (Cryptochiridae) over depth intervals in the Caribbean. PeerJ 2016, 4, e1794. [Google Scholar] [CrossRef] [PubMed]
- Kropp, R.K.; Manning, R.B. The Atlantic gall crabs, family Cryptochiridae (Crustacea: Decapoda: Brachyura). Smithson. Contrib. Zool. 1987, 462, 1–21. [Google Scholar] [CrossRef]
- Zibrowius, H.; Gili, J.M. Deep-water Scleractinia (Cnidaria: Anthozoa) from Namibia, South Africa, and Walvis Ridge, southeastern Atlantic. Sci. Mar. 1990, 54, 19–46. [Google Scholar]
- Manning, R.B. Crustacea Decapoda: Cecidocarcinus zibrowii, a new deep-water gall crab (Cryptochiridae) from New Caledonia. Résultats Camp. MUSORSTOM 1991, 9, 515–520. [Google Scholar]
- Kropp, R.K.; Manning, R.B. Crustacea Decapoda: Two new genera and species of deep water gall crabs from the Indo-west Pacific (Cryptochiridae). Résultats Camp. MUSORSTOM 1996, 15, 531–539. [Google Scholar]
- Pyle, R.L.; Copus, J.M. Mesophotic coral ecosystems: Introduction and overview. In Mesophotic Coral Ecosystems; Loya, Y., Puglise, K.A., Bridge, T.C.L., Eds.; Springer: New York, NY, USA, 2019; pp. 3–27. [Google Scholar]
- Komatsu, H.; Takeda, M. Second record of Luciades agana Kropp and Manning, 1996 (Crustacea, Decapoda, Cryptochiridae) from Tonga, South Pacific. Bull. Natl. Mueums Nat. Sci. Ser. A 2013, 39, 11–14. [Google Scholar]
- van der Meij, S.E.T.; van Tienderen, K.M.; Hoeksema, B.W. A mesophotic record of the gall crab Opecarcinus hypostegus from a Curaçaoan reef. Bull. Mar. Sci. 2015, 91, 205–206. [Google Scholar] [CrossRef]
- Xu, T.; Bravo, H.; Paulay, G.; van der Meij, S.E.T. Diversification and distribution of gall crabs (Brachyura: Cryptochiridae: Opecarcinus) associated with Agariciidae corals. Coral Reefs 2022, 41, 699–709. [Google Scholar] [CrossRef]
- Kahng, S.E.; Garcia-Sais, J.R.; Spalding, H.L.; Brokovich, E.; Wagner, D.; Weil, E.; Hinderstein, L.; Toonen, R.J. Community ecology of mesophotic coral reef ecosystems. Coral Reefs 2010, 29, 255–275. [Google Scholar] [CrossRef]
- Wei, T.P.; Chen, H.C.; Lee, Y.C.; Tsai, M.L.; Hwang, J.S.; Peng, S.H.; Chiu, Y.W. Gall polymorphism of coral-inhabiting crabs (Decapoda, Cryptochiridae): A new perspective. J. Mar. Sci. Technol. 2013, 21, 40. [Google Scholar]
- Folmer, O.; Black, M.; Hoeh, W.; Lutz, R.; Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 1994, 3, 294–299. [Google Scholar] [PubMed]
- Hall, T. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41, 95–98. [Google Scholar]
- Kropp, R.K. A revision of the Pacific species of gall crabs, genus Opecarcinus (Crustacea: Cryptochiridae). Bull. Mar. Sci. 1989, 45, 98–129. [Google Scholar]
- van der Meij, S.E.T. A new species of Opecarcinus Kropp & Manning, 1987 (Crustacea: Brachyura: Cryptochiridae) associated with the stony corals Pavona clavus (Dana, 1846) and P. bipartita Nemenzo, 1980 (Scleractinia: Agariciidae). Zootaxa. 2014, 3869, 44–52. [Google Scholar] [PubMed]
- Hurley, K.K.C.; Timmers, M.; Godwin, L.S.; Copus, J.M.; Skillings, D.J.; Toonen, R.J. An assessment of shallow and mesophotic reef brachyuran crab assemblages on the south shore of O’ahu, Hawai’i. Coral Reefs 2016, 35, 103–112. [Google Scholar] [CrossRef]
- Pinheiro, H.T.; MacDonald, C.; Quimbayo, J.P.; Shepherd, B.; Phelps, T.A.; Loss, A.C.; Teixeira, J.B.; Rocha, L.A. Assembly rules of coral reef fish communities along the depth gradient. Curr. Biol. 2023, 33, 1421–1430. [Google Scholar] [CrossRef]
| Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).