Introduction
Research on cnidarian diversity has gained significant attention due to their crucial ecological roles in marine ecosystems. Among cnidarians, Scleractinian corals have been of particular importance, given their central role in coral reef ecosystems and the profound impacts that climate change is expected to have on their survival and associated biodiversity. The evolutionary success of Scleractinian corals is primarily linked to their symbiotic association with photosynthetic dinoflagellates of the family Symbiodiniaceae (Vuleta et al., Reference Vuleta, Nakagawa and Ainsworth2024). However, not all Scleractinian corals have symbiosis with dinoflagellate and those that do not, are broadly categorized as azooxanthellate corals (Cairns, Reference Cairns1999). These corals are exclusively heterotrophic, obtaining nutrients from the surrounding water column, including organic matter, phytoplankton, and zooplankton (Houlbrèque et al., Reference Houlbrèque, Rodolfo and Ferrier2015). Azooxanthellate corals host diverse microbial assemblages that plays vital role in nutrient cycling (Houlbrèque et al., Reference Houlbrèque, Rodolfo and Ferrier2015). Even when azooxanthellate corals covers nearly half of the known Scleractinian diversity globally, their distribution, life history traits and ecological role are less studied compared to their photo endosymbiotic counterparts. Research on azooxanthellate corals is limited, primarily due to the perceived lack of environmental significance, insufficient information on potential environmental threats and ecosystem complexities in which they occur.
Globally, azooxanthellate Scleractinian corals are distributed across 14 families (Cairns, Reference Cairns2004; Cairns and Kitahara, Reference Cairns and Kitahara2012). However, only four families—Caryophyllidae, Flabellidae, Rhizangiidae, and Dendrophyllidae—have been documented in Indian waters (Singarayan and Rethnaraj, Reference Singarayan and Rethnaraj2016). While the environmental, ecological, and socio-economic significance of coral reefs is well recognized, early research on coral taxonomy in India predominantly focused on zooxanthellate, or photosymbiotic scleractinian corals, with limited attention given to azooxanthellate species (Pillai, Reference Pillai1967b; Venkataraman et al., Reference Venkataraman, Satyanarayana, Alfred and Wolstenholme2003). In recent years, there has been an increasing awareness of the need for comprehensive studies on all vulnerable coral species, regardless of their symbiotic status. This has led to a surge in research focusing on azooxanthellate corals in Indian waters (Singarayan and Rethnaraj, Reference Singarayan and Rethnaraj2016; Viswambharan et al., Reference Viswambharan, Sreenath, Jasmine, Joshi, Sreeraj, Mohan and Rohit2021; Mondal and Raghunathan, Reference Mondal and Raghunathan2022), with particular emphasis on the taxonomy and distribution of species within the families Caryophyllidae, Flabellidae, and Dendrophyllidae.
The family Rhizangiidae, a subgroup within the azooxanthellate Scleractinia, is among the least studied groups of azooxanthellate corals, both in India and globally. Species within this family are characterized by small, encrusting colonies of corallites that are interconnected at their bases. Nearly six decades ago, two species of azooxanthellate Rhizangiids, Cladangia exusta and Culicia rubeola, were documented in Indian waters (Pillai, Reference Pillai1967a, Reference Pillai1967b). Despite numerous studies conducted in various coastal ecosystems following Pillai's work, these species have not been recorded in Indian coastal waters. The under-documentation of Rhizangiid corals is often attributed to their small size, challenges in morphological identification, and the lack of information on their ecological preferences. Conservation efforts are further hampered by a lack of comprehensive data on their distribution, taxonomy, and ecology. This study was therefore undertaken to rediscover these Rhizangiid corals, map their distribution, and identify their ecological preferences along the southwest coast of India, with a special focus on documenting their morphological diagnostic characteristics.
The coastal waters of the southwest coast of India (northeastern Laccadive Sea) were selected for this study, as these regions were the first to record these corals in India. Comprehensive underwater surveys were conducted across diverse marine habitats, including rocky reefs and submerged shipwrecks. These surveys led to the identification of two Rhizangiid coral species in the coastal water ecosystem. Given the challenges of accurately identifying these corals, efforts were made to delineate distinct morphological traits to effectively differentiate them from other azooxanthellate corals with similar morphology and habitats.
Materials and Methods
A comprehensive series of exploratory surveys were undertaken across diverse marine habitats encompassing rocky reefs, coral reefs, inshore islands, and submerged shipwrecks within the expanse of the Laccadive Sea. Employing SCUBA-assisted underwater visual census techniques, observations were carried out to document the distribution patterns of Rhizangiid corals in specific locales, namely Netrani Island (off Murudeshwara), Hog Island (off Bhatkal), Bhatkal Wreck (off Bhatkal), Mulki Rocks (off Kaup), a shipwreck site (off Kaup), St. Mary's Island (off Malpe), and the rocky reef in vicinity of Paduthonse. Details of exploratory surveys conducted are given in Table 1.
Table 1. Details on sampling sites and sampling period
During the underwater survey, live coral specimens were documented in situ using a Nikon Coolpix W300 camera. To ensure accurate species identification, coral specimens were collected from two locations: Mulki Rocks (off Kaup, Dakshina Kannada, Karnataka) and a submerged shipwreck site (off Bhatkal, Uttara Kannada, Karnataka). The collected specimens were soaked in freshwater, meticulously cleaned using a fine-bristle brush, and subsequently air-dried at room temperature. Detailed morphological features of the coralla were then photographed using a stereoscopic microscope. Species identification was carried out using relevant scientific literature, including Dana (Reference Dana1846), Lütken (Reference Lütken1873), Pillai (Reference Pillai1967a, Reference Pillai1967b), Cairns and Zibrowius (Reference Cairns and Zibrowius1997), Cairns (Reference Cairns2004), and Viswambharan et al. (Reference Viswambharan, Sreenath, Jasmine, Joshi, Sreeraj, Mohan and Rohit2021). Additionally, information on the distribution of Rhizangiid corals was corroborated using previously published sources (Pillai, Reference Pillai1967a, Reference Pillai1967b; Cairns, Reference Cairns2004).
Georeferenced data were collected during field surveys using GPS devices to accurately capture the location of coral colonies. Additionally, location data from existing literature were compiled to ensure a comprehensive dataset. The integrated data were then used to generate a spatial map in NextGIS QGIS.Ink (version 23.11.0).
Results
The comprehensive survey, recorded the presence of Culicia stellata and Cladangia exusta in the Laccadive Sea, and this finding is a significant contribution to the limited knowledge of Rhizangiid corals in Indian waters. Our study documents the presence of Cladangia exusta in the Laccadive Sea, nearly six decades after its initial observation in 1967. Additionally, the discovery of Culicia stellata is particularly noteworthy as it represents the first recorded occurrence of this species within the Indian Exclusive Economic Zone (EEZ).
Cladangia exusta Lütken, Reference Lütken1873 (Figure 1)
Figure 1. (A) Live photographs of Cladangia exusta Lütken, Reference Lütken1873 in Bhatkal Wreck. (B) Calicular view showing the septal size and arrangement in corallites (black arrows showing the costae ridges in the inter-corallite area).
Systematics
Order: Scleractinia Bourne, 1900
Family: Rhizhangiidae d'Orbigny, 1851
Genus: Cladangia Milne Edwards & Haime, 1851
Species: Cladangia exusta Lutken, 1873
Recorded locality: Bhatkal Wreck, off Bhatkal, Karnataka State, India. Depth: 30–32 m
Remarks: Previously recorded from off-Cochin, Laccadive Sea and in Moreton Bay (Queensland). Details on the exact location and depth of occurrence are not available in the previous studies (Pillai, Reference Pillai1967a; Cairns, Reference Cairns2004). In Indian EEZ, the species was found to grow over submerged metal surfaces.
Species Characteristics: Details about this species, including species description based on their morphological traits are outlined in Table 2.
Table 2. Diagnostic characters of Cladangia exusta Lütken, Reference Lütken1873
Distribution: Coastal waters of Indian EEZ (Laccadive Sea-Indian Ocean); Queensland (Moreton Bay- Pacific Ocean)
Culicia stellata Dana, Reference Dana1846 (Figure 2)
Figure 2. (A) Live photographs of Culicia stellata Dana, Reference Dana1846 in Mulki Rocks (black arrows shows the solan covered by epifauna). (B) Calicular view showing the septal size and arrangement in corallites.
Systematics
Order: Scleractinia Bourne, 1900
Family: Rhizhangiidae d'Orbigny, 1851
Genus: Culicia Dana, 1846
Species: Culicia stellata Dana, Reference Dana1846
Recorded locality: Mulki Rocks, Off Kaup, Karnataka State, India. Depth: 6–8 m.
Remarks: The habitat preference of Culicia seems to be natural substances like rocks or dead corals in shallow water with high turbidity. First record from Indian EEZ. The species is recorded in the atolls of Maldives in the Laccadive Sea.
Species Characteristics: Details about this species, including species description based on their morphological traits are outlined in Table 3.
Table 3. Diagnostic characters of Culicia stellata Dana, Reference Dana1846
Distribution: Coastal waters of Indian EEZ (Laccadive Sea-Indian Ocean), West and Central Pacific Ocean
Discussion
Despite the ecological importance of azooxanthellate corals, particularly Rhizangiids, significant gaps remain in our understanding of their distribution in the Laccadive Sea. These gaps are largely due to limited survey efforts and the challenges posed during species identification, which arise from their small colony sizes and complex morphology. This lack of comprehensive data hinders the development of effective conservation and management strategies for these marine organisms. To date, only two Rhizangiid species have been documented in Indian waters: Cladangia exusta (Pillai, Reference Pillai1967a) from the waters off Cochin and Culicia rubeola (Pillai, Reference Pillai1967b) from three islands in the Gulf of Mannar. Our study addresses this critical knowledge gap by documenting the presence of Culicia stellata for the first time within the Indian EEZ and expanding the known range of C. exusta beyond shallow coastal waters.
In the family Rhizangiidae, the genus Culicia possess significant challenges in species delineation, necessitating thorough review and revision. The morphological characteristics used to identify Culicia stellata are discussed in Table 3. Prior studies in the Gulf of Mannar had recorded Culicia rubeola from Krusadai Island, Manauli Island, and Hare Island, where the species was found on natural rocks as well as dead Porites spp (Pillai, Reference Pillai1967b). Culicia stellata can be distinguished from C. rubeola by the differences in the septal lobes, where the septal lobes in C. stellata are observed only in the S1, while in C. rubeola, S1, S2, and S3 are lobed (Cairns, Reference Cairns1995; Cairns and Zibrowius, Reference Cairns and Zibrowius1997).
The map on the recorded distribution of azooxanthellate corals of Rhizangiidae in Laccadive Sea are shown in Figure 3. Interestingly, these corals are uncommonly recorded in well-established coral reef locations within the Laccadive Sea, including the Laccadive atolls or the coral reefs surrounding Netrani. Despite comprehensive survey efforts, the occurrences of these corals were restricted to Mulki Rocks, as well as submerged shipwrecks situated off Bhatkal. Multiple colonies of Culicia stellata were exclusively observed on Mulki rocks, off the coast of Kaup in Karnataka. These live colonies, found at depths ranging from 6 to 8 meters, were surrounded by encrusting epifauna to such an extent that the stolon of the colony was fully concealed. Finding these corals were difficult due to their minuscule size and the presence of epifauna that nearly concealed each of their tiny corallites. This study had shown that Culicia preferred coastal rocky/coral reef areas and are unaffected by high turbidity. The colonies were predominantly located on the upper surfaces of rocks, where sufficient light penetration occurred during post monsoon season but visibility falls to less than one meter during the pre-monsoon and monsoon season.
Figure 3. Map showing the distribution of Rhizangiid corals in Laccadive Sea.
Present survey has recorded the occurrence of Cladangia exusta in the submerged wreck, off-Bhatkal in Karnataka in the south west coast of India (north eastern Laccadive Sea). A thorough literature review was undertaken and distinctive feature of Cladangia exusta are given in Table 2. Since Astrangia and Cladangia are often confused and misidentified in Indian Coast, the discriminative attributes demarcating Astrangia woodsi from Cladangia exusta are elucidated in Table 4. Three live colonies of Cladangia were observed on the starboard side of the wrecked ship. The site is a fishing ground for off shore vessels, mainly purse seiners. The site was highly turbid with visibility limited to less than 0.5 m in February–May (pre-monsoon). The corals were surrounded by hydroid (Aglaophenia sp) and few unidentified sea anemones. The earlier study conducted by Pillai (Reference Pillai1967a) had identified the species on a submerged metal piece but specific details on the location of sample collection and depth of its occurrence were not recorded. This observation marks the reporting of live Cladangia exusta in the Laccadive Sea since its first discovery nearly six decades ago within the coastal waters off Cochin. The historical research conducted by Lütken (Reference Lütken1873) had initially constrained habitat of Cladangia to littoral regions; however, present day findings indicate that the species might exhibit a broader distribution extending into deeper waters, contrasting with Lütken's original assertion.
Table 4. Difference between Astrangia woodsi Wells, 1955 and Cladangia exusta Lütken, Reference Lütken1873 found in coastal area along the west coast of India
The habitat preference of the Rhizangiid coral Cladangia exusta appears to be somewhat atypical. In this study, live colonies of C. exusta were observed at a depth of 30–32 m on a submerged shipwreck (Figure 1a). Although these three colonies were well-established on the wreck, no occurrences of C. exusta were found on natural rocky substrates at similar depths. Despite extensive surveys conducted during the research period, C. exusta was consistently absent from natural rock formations. Coral habitat preference is initially influenced by broad environmental cues that help identify suitable habitats. Upon contacting a surface, corals detect chemical cues, such as biotic signals or external biochemicals, which indicate habitats where successful recruitment has previously occurred (Price, Reference Price2010). Notably, C. exusta seems to exhibit a distinct preference for submerged metallic structures. This inclination is supported by both the findings of this survey and the initial record by Pillai (Reference Pillai1967a), which documented the species exclusively in association with submerged metal. But more studies are required to determine whether this preference for submerged metallic structures is a consistent ecological trait of Cladangia exusta or if it represents an adaptive response to specific environmental conditions. Hence further investigations are essential to better understand the habitat preferences and ecological requirements of Cladangia exusta.
This study on Culicia stellata and Cladangia exusta within the Indian EEZ significantly enhances the global understanding of azooxanthellate corals in the family Rhizangiidae, advancing both taxonomic and ecological knowledge through detailed descriptions of their morphological characteristics and habitat preferences. Our findings aid in facilitating easier identification and monitoring of these species, which is crucial for developing effective conservation strategies and conducting comprehensive biodiversity assessments. The study also underscores the importance of habitat diversity in sustaining the rich marine life within the Indian EEZ, a paramount aspect of global marine biodiversity conservation efforts (Bellwood et al., Reference Bellwood, Hughes, Folke and Nystrom2004; Foster et al., Reference Foster, Baums, Sanchez, Paris, Chollett, Agudelo, Vermeij and Mumby2013).
Acknowledgements
The authors are grateful to the Director of ICAR-CMFRI for constant encouragement and funding. We are obliged to the officials of the Forest, Environment and Ecology Department, Government of Karnataka for the research permit. The first author would like to acknowledge the help rendered by the coral experts, Dr H. Zibrowius and Dr Stephen Cairns. The help rendered by the diving team of West Coast Adventures and Capt. Jayapakash Mendon is gratefully acknowledged. The Authors are grateful to the Head and staffs of Mangalore Regional Centre for the support rendered in undertaking the exploratory survey. This work forms part of the ICAR-CMFRI in-house project MBD/CRL/31.
Data availability statement
The data that support the findings of this study are available from the corresponding author, DV, upon reasonable request.
Author contribution
DV- diving, sampling, photography, mapping, species taxonomy, literature review, and writing (original draft); SKR – writing (original draft, review and editing).
Financial support
No external funding was received for the study.
Competing interest
The authors declare no conflict of interest.
Ethical standards
No animal testing was performed during this study.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgments. The study is compliant with CBD and Nagoya protocols.
