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Incursion of the killer hoshinota Rützler & Muzik, 1993 on the coral reefs of the Lakshadweep archipelago, Arabian Sea

Rocktm Ramen Das, Chemmencheri Ramakrishnan Sreeraj, Gopi Mohan, Kotarathil Rajendran Abhilash, Vijay Kumar Deepak Samuel, Purvaja Ramachandran & Ramesh Ramachandran

26 October 2020 | Vol. 12 | No. 14 | Pages: 17009–17013 DOI: 10.11609/jot.5790.12.14.17009-17013

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Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2020 | 12(14): 17009–17013 ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) PLATINUM OPEN ACCESS DOI: htps://doi.org/10.11609/jot.5790.12.14.17009-17013

#5790 | Received 19 February 2020 | Final received 03 October 2020 | Finally accepted 07 October 2020

S h o Incursion of the killer sponge Terpios hoshinota Rützler & Muzik, 1993 on r t the coral reefs of the Lakshadweep archipelago, Arabian Sea C o 1 2 3 m Rocktm Ramen Das , Chemmencheri Ramakrishnan Sreeraj , Gopi Mohan , m Kotarathil Rajendran Abhilash 4 , Vijay Kumar Deepak Samuel 5 , Purvaja Ramachandran 6 & u 7 n Ramesh Ramachandran i c 1–7 a Natonal Centre for Sustainable Coastal Management, Ministry of Environment, Forest and Climate Change, Chennai, t Tamil Nadu 600025, India. i 1Graduate School of Engineering and Science, University of the Ryukyus, Nishihara 903-0213, Okinawa, Japan. o [email protected], [email protected], [email protected], [email protected], [email protected] n (corresponding author), [email protected], [email protected]

Abstract: Our study documents the outbreak of a coral-killing sponge sponge Terpios hoshinota Rützler & Muzik, 1993 also Terpios hoshinota in the coral reefs of Lakshadweep archipelago and known as the black disease* (Liao et al. 2007) frst highlights that it has further extended its territory into the isolated atolls of Arabian Sea and maybe a growing threat to the existng coral reported from Guam (Bryan 1973) and later described reefs in the region. from the coral reefs of the Ryukyu archipelago (Japan)

Keywords: Atoll, Black disease, Indian Ocean. (Rützler & Muzik 1993) is identfed by its gray to blackish encrustatons. Since its frst occurrence, it has Abbreviatons: GOM—Gulf of Mannar | PB—Palk Bay | QGIS— been observed in several localites around the Quantum Geographic Informaton System. *The terms Black disease and Killer sponge are used synonymously. globe, viz., the (Fujii et al. 2011), Papua New Guinea (Ekins et al. 2017), Taiwan (Liao et al. 2007), Philippines (Plucer-Rosario 1987), Indonesia (De Voogd et al. 2013), South China Sea (Shi et al. 2012; Hoeksema Coral killing have the potental to overgrow et al. 2014; Yang et al. 2018) , Thailand (Plucer-Rosario live corals, eventually killing the coral polyps, and thus 1987), Palk Bay (PB)/Gulf of Mannar (GOM) (India) leading to an epidemic (Bryan 1973). The cyanobacterio (Thinesh et al. 2015, 2017; Raj et al. 2018a), Maldives

Editor: M. Nithyanandan, Kuwait Insttute for Scientfc Research (KISR), Salmiya, Kuwait. Date of publicaton: 26 October 2020 (online & print)

Citaton: Das, R.R., C.R. Sreeraj, G. Mohan, K.R. Abhilash, V.K.D. Samuel, P. Ramachandran & R. Ramachandran (2020). Incursion of the killer sponge Terpios hoshinota Rützler & Muzik, 1993 on the coral reefs of the Lakshadweep archipelago, Arabian Sea. Journal of Threatened Taxa 12(14): 17009–17013. htps://doi. org/10.11609/jot.5790.12.14.17009-17013

Copyright: © Das et al. 2020. Creatve Commons Atributon 4.0 Internatonal License. JoTT allows unrestricted use, reproducton, and distributon of this artcle in any medium by providing adequate credit to the author(s) and the source of publicaton.

Funding: Ministry of Environment, Forests and Climate Change, Govt. of India, and The World Bank.

Competng interests: The authors declare no competng interests. A preprint of this manuscript was posted on bioRxiv Preprint server on April 29, 2019.

Acknowledgements: This study was undertaken as part of the grant-in-aid project of “Mapping of Ecologically Sensitve Areas (ESAs) and Critcally Vulnerable Coastal Areas (CVCAs) along the Coast of India”, “[F.No. 22-29/2008-WBICZM-IA-III; 19 June 2014]”. The authors acknowledge the fnancial and technical support provided by MoEF&CC, Government of India, and the World Bank under the India ICZM Project. The authors are grateful to Dr. S.L Liu (Tunghai University, Taiwan) for comments, to Dr. S.L. Tang (Biodiversity Research Center, Academia Sinica, Taiwan) and to Dr. S.Y. Yang (Shimoda Marine Research Center, University of Tsukuba, Japan) for important literature and informaton on the killer sponge outbreak in the South China Sea. The authors acknowledge the secton editor for further improving the manuscript.

17009 J TT Incursion of killer sponge on coral reefs Das et al.

Image 1. Bangaram & Thinnakara atoll (Inset - red star) (QGIS 3.6).

(Montano et al. 2015), Mauritus (Elliot et al. 2016) radiatng network of canals, was clearly visible and the and our present observaton, confrms that the species thickness of the mat was less than 1mm (Image 2). It was has further extended its habitat into the pristne atolls observed that the encrustng sponges were propagatng of Lakshadweep (Image 1) (Arabian Sea) and requires laterally and infectng the other live coral colonies. urgent atenton. Other associated communites such as ascidians and During the coral reef surveys conducted at clams remain unafected but interestngly the calcareous Lakshadweep in November 2016, T. hoshinota was serpulid tubes, though overgrown by the Terpios, the observed overgrowing on several colonies of was unharmed (Elliot et al. 2016) (Image 2d). muricata, Isopora palifera, Cyphastrea sp., Dipsastraea Further, in some colonies along with T. hoshinota, algal lizardensis and lutea (Image 2 and 3) in the atoll presence was noted (Image 3a) but the sponge was encircling Bangaram and Thinnakara Islands. Out of 34 absent in the colonies which were completely covered sites surveyed, six exhibited the presence of T. hoshinota with turf algae (Image 3b). Environmental parameters (Image 1). The coral colonies in atoll were patchy and assessed with a multparameter water quality probe (YSI the depth of the atoll varied between 2 and 12 meters. optc probe no. 15K100034) revealed that the area was As depth increased, (i.e., >5m) large boulder corals unpolluted with an optmum level of dissolved oxygen were observed whereas the shallow regions (<5m) had (5.04~8.21 mg/l), and low turbidity (0.3 to 0.8 NTU). greater coral diversity. Certain areas consistng of large Sea surface temperature (SST) during the survey was Acropora beds, rocks, rubbles, and dead reef were also 28.2°~30.1°C. It is important to note that, Bangaram observed. The afected corals displayed grayish/blackish and Thinnakara is one of the few atolls in Lakshadweep encrustatons of T. hoshinota forming a mat-like layer where tourism is permited, as a result, limited amounts on live corals taking the shape of the coral in all cases. of diving and other water-related recreatonal actvites The osculum in the sponge, a primary character with a can be seen in the area.

17010 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2020 | 12(14): 17009–17013 J TT Incursion of killer sponge on coral reefs Das et al.

Image 2. A—Incrustatons of T. hoshinota on A. muricata, A1. T. hoshinota exhibitng osculum with radiatng networks | B—Incrustaton on I. palifera, B1. T. hoshinota mat, B2. Bleached ring, B3. Live coral | C—T. hoshinota taking shape of a Coral (Cyphastrea sp.) | D—T. hoshinota overgrowing calcareous serpulid tubes, D1. animal unafected.

Previous studies (Rützler & Muzik 1993; Thinesh et sponge has afected several coral species in diferent al. 2015) suspected that the outbreak of T. hoshinota parts of the world (Bryan 1973; Thinesh et al. 2015; is related to increased water turbidity or due to high Elliot et al. 2016; Raj et al. 2018a) and in the reefs of anthropogenic stress/polluton its close proximity to Palk Bay (PB), it has afected all genus surveyed (Thinesh mainland, as reported in the south eastern reefs of India et al. 2015). In Vaan Island (GOM) the dominant genus (~800km from Lakshadweep) (Thinesh et al. 2015, 2017; Montpora was the most susceptble (Raj et al. 2018a). Raj et al. 2018a), Guam (Plucer-Rosario 1987; Rützler & Our observaton though could not reveal any specifc Muzik 1993) and in Green island (Chen et al. 2009). A host coral selectvity, we can speculate that the dense similar conclusion, however, cannot be applied in the branching Acropora coral beds (ACB) in site 3, 5 and 6 case of Lakshadweep because of its isolated geography were more easily overgrown because the killer sponge (Arthur et al. 2005) and with comparatvely less prefers branching corals as reported from Mauritus anthropogenic actvites. As a result, our observaton (Elliot et al. 2016). We would further conclude that the contradicts the above statements and is more in line coral compositon in any specifc locaton may play an with the fndings of Shi et al. (2012) who observed T. important role in determining its host. hoshinota outbreak in unpolluted areas of Yongxing T. hoshinota is a belligerent contender for space Island (South China Sea), highlightng the difculty in (Plucer-Rosario 1987) and is known to overgrow corals establishing a negatve co-relatonship between water from its base where it interacts with turf algae (Elliot quality and black disease outbreak (Sung-Yin Yang pers et al. 2016). Branching Acropora beds in site 3, 5 and comm. 2020). In terms of host selectvity, the killer 6 (Image 3a) consisted both algae (e.g., Dictyota sp.)

Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2020 | 12(14): 17009–17013 17011 J TT Incursion of killer sponge on coral reefs Das et al.

Image 3. Acropora colonies (Site 3): A—A1. T. hoshinota A2. Algae | B—Acropora colonies (Site 5) completely over grown by turf algae, killer sponge/black disease absent.

and the killer sponge. Additonally, a massive turf algae nearby atolls as seen in other regions (Bryan 1973; Reimer covered area of ~0.35km in T. hoshinota occurrence site et al. 2011), large-scale damage cannot be concluded (5, 6) highlights a complex ecological scenario (Image at this stage. This is in fact the frst documentaton of 3b). Such complexity between sponges, corals and algae T. hoshinota on the reefs of Lakshadweep and can be can be only understood through long term monitoring. regarded as a baseline for subsequent studies. Further, González-Rivero et al. (2011) stated that sponges can to protect the reefs of Lakshadweep, a long term coral act as a potental group that can facilitate and infuence health monitoring program is required which will allow coral-algal shifs by actng as a “third antagonist” as us to understand the nature of occurrence, distributon, observed in Glover’s atoll (Belize). the impact and the causatve factors of the killer sponge Based on our knowledge of the life history of T. and to understand it’s larger threat to the reefs. Black hoshinota we can hypothesize site 5/6 scenario as disease along with other coral associated diseases needs follows: - (1) T. hoshinota invades and overgrows the enlarged emphasis according to which various coral reef Acropora beds → (2) The coral dies which is followed by management plans can be initated. the death of the killer sponge → (3) Turf algae takes over (Image 3a, b). Moreover, reports of turf algae being a References dominant component in the atolls (Arthur et al. 2005) might indicate a faster transiton. Globally Elevated Arthur, R., T.J. Done & H. Marsh (2005). Benthic recovery four years afer an El Nino-induced coral mass mortality in the Lakshadweep SST is a major threat to coral reefs (Hughes et al. 2018), atolls. Current Science 89(4): 694–699. and the reefs of India (Edward et al. 2018; Krishnan et Bell, J.J., S.K. Davy, T. Jones, M.W. Taylor & N.S. Webster (2013). Could al. 2018; Raj et al. 2018b) including the atolls (Vinoth et some coral reefs become sponge reefs as our climate changes? Global Change Biology 19: 2613–2624. htps://doi.org/10.1111/ al. 2012) are no diferent. With reports indicatng that gcb.12212 elevated SST has already depleted the coral ecosystem Bryan, P. (1973). Growth rate, toxicity, and distributon of the of Lakshadweep, which was evident during 1998 (Arthur encrustng sponge Terpios sp. (Hadromerida: Suberitdae) in Guam, Mariana Islands. Micronesica 9(2): 237–242. et al. 2005), 2010 (Vinoth et al. 2012), and 2016 (Hughes Chen, S.L., C.Y. Kuo & C.A. Chen (2009). Spatal distributon and et al. 2018) mass bleaching events, it can provide an temporal variaton of the cyanobacteriosponge, Terpios hoshinota, opportunity for sponges to invade (Bell et al. 2013) . The and benthos compositon on the coral reefs of Green Island. Journal of Natonal Park 19: 33–45. dynamics of waterfow (Arthur et al. 2005) may also play De Voogd, N.J., F. Dekker & D.F.R. Cleary (2013). The coral-killing a crucial role in this regard. sponge Terpios hoshinota invades Indonesia. Coral Reefs 32: 755. htps://doi.org/10.1007/s00338-013-1030-4 Our fndings confrm that the infestaton of T. Edward, J.K.P., G. Mathews, K.D. Raj, R.L. Laju, M.S. Bharath, A. hoshinota on the coral colonies of Lakshadweep is Arasamuthu, P.D. Kumar, D.S. Bilgi & H. Malleshappa (2018). currently limited to only Bangaram and Thinnakara as it Coral mortality in the Gulf of Mannar, southeastern India, due to bleaching caused by elevated sea temperature in 2016. Current was not observed in the other atolls surveyed. Although Science 114(9): 1967–1972. htps://doi.org/10.18520/cs/v114/ there is a possibility that the killer sponge could invade i09/1967-1972

17012 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2020 | 12(14): 17009–17013 J TT Incursion of killer sponge on coral reefs Das et al.

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Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2020 | 12(14): 17009–17013 17013 PLATINUM The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservaton globally by publishing peer-reviewed artcles online every month at a reasonably rapid rate at www.threatenedtaxa.org. OPEN ACCESS All artcles published in JoTT are registered under Creatve Commons Atributon 4.0 Internatonal License unless otherwise mentoned. JoTT allows allows unrestricted use, reproducton, and distributon of artcles in any medium by providing adequate credit to the author(s) and the source of publicaton.

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)

October 2020 | Vol. 12 | No. 14 | Pages: 16927–17062 Date of Publicaton: 26 October 2020 (Online & Print) www.threatenedtaxa.org DOI: 10.11609/jot.2020.12.14.16927-17062

Artcle Contributon to the macromycetes of West Bengal, India: 63–68 – Rituparna Saha, Debal Ray, Anirban Roy & Krishnendu Acharya, Pp. 17014– Elevatonal patern and seasonality of avian diversity in Kaligandaki River 17023 Basin, central Himalaya – Juna Neupane, Laxman Khanal, Basant Gyawali & Mukesh Kumar Chalise, Pp. 16927–16943 Notes

A rare camera trap record of the Hispid Hare Caprolagus hispidus from Dudhwa Communicatons Tiger Reserve, Terai Arc Landscape, India – Sankarshan Rastogi, Ram Kumar Raj & Bridesh Kumar Chauhan, Pp. 17024– A highway to hell: a proposed, inessental, 6-lane highway (NH173) that 17027 threatens the forest and wildlife corridors of the Western Ghats, India – H.S. Sathya Chandra Sagar & Mrunmayee, Pp. 16944–16953 First distributonal record of the Lesser Adjutant Leptoptlos javanicus Horsfeld, 1821 (Ciconiiformes: Ciconiidae) from Sindhuli District, Nepal Species diversity and feeding guilds of birds in Malaysian agarwood – Badri Baral, Sudeep Bhandari, Saroj Koirala, Parashuram Bhandari, plantatons Ganesh Magar, Dipak Raj Basnet, Jeevan Rai & Hem Sagar Baral, Pp. 17028–17031 – Nor Nasibah Mohd Jamil, Husni Ibrahim, Haniza Hanim Mohd Zain & Nur Hidayat Che Musa, Pp. 16954–16961 First record of African Sailfn Flying Fish Parexocoetus mento (Valenciennes, 1847) (Beloniformes: Exocoetdae), from the waters of Andaman Islands, India Evaluatng performance of four species distributon models using Blue-tailed – Y. Gladston, S.M. Ajina, J. Praveenraj, R. Kiruba-Sankar, K.K. Bineesh & Green Darner Anax gutatus (Insecta: Odonata) as model organism from the S. Dam Roy, Pp. 17032–17035 Gangetc riparian zone – Kritsh De, S. Zeeshan Ali, Niladri Dasgupta, Virendra Prasad Uniyal, A frst distributon record of the Indian Peacock Sofshell Turtle Nilssonia hurum Jeyaraj Antony Johnson & Syed Ainul Hussain, Pp. 16962–16970 (Gray, 1830) (Reptlia: Testudines: Trionychidae) from Mizoram, India – Gospel Zothanmawia Hmar, Lalbiakzuala, Lalmuansanga, Dadina Zote, Buterfy species richness and diversity in rural and urban areas of Sirajganj, Vanlalhruaia, Hmar Betlu Ramengmawii, Kulendra Chandra Das & Hmar Tlawmte Bangladesh Lalremsanga, Pp. 17036–17040 – Sheikh Muhammad Shaburul Imam, Amit Kumer Neogi, M. Ziaur Rahman & M. Sabbir Hasan, Pp. 16971–16978 A frog that eats foam: predaton on the nest of Polypedates sp. (Rhacophoridae) by Euphlycts sp. (Dicroglossidae) Chroococcalean blue green algae from the paddy felds of Satara District, – Pranoy Kishore Borah, Avrajjal Ghosh, Bikash Sahoo & Aniruddha Data-Roy, Maharashtra, India Pp. 17041–17044 – Sharada Jagannath Ghadage & Vaneeta Chandrashekhar Karande, Pp. 16979– 16992 New distributon record of two endemic plant species, Euphorbia kadapensis Sarojin. & R.R.V. Raju (Euphorbiaceae) and Lepidagathis keralensis Madhus. & N.P. Singh (Acanthaceae), for Karnataka, India Short Communicatons – P. Raja, N. Dhatchanamoorthy, S. Soosairaj & P. Jansirani, Pp. 17045–17048

Avifaunal diversity along the riverine habitats of Papikonda Natonal Park, Cirsium wallichii DC. (Asteraceae): a key nectar source of buterfies Andhra Pradesh, India – Bitupan Boruah, Amit Kumar & Abhijit Das, Pp. 17049–17056 – Paromita Ray, Giridhar Malla, Upma Manral, J.A. Johnson & K. Sivakumar, Pp. 16993–16999 Hypecoum pendulum L. (Papaveraceae: Ranunculales): a new record for the fora of Haryana, India Medetomidine may cause heart murmur in Cougars and Jaguars: case report – Naina Palria, Nidhan Singh & Bhoo Dev Vashistha, Pp. 17057–17059 – Thiago Cavalheri Luczinski, Gediendson Ribeiro de Araújo, Matheus Folgearini Silveira, Murillo Daparé Kirnew, Roberto Andres Navarrete, Jorge Aparecido Salomão-Jr, Letcia Alecho Requena, Jairo Antonio Melo dos Santos, Marcell Addendum Hideki Koshiyama, Cristane Schilbach Pizzuto & Pedro Nacib Jorge-Neto, Pp. 17000–17002 Erratum and addenda to the artcle ‘A history of primatology in India’ – Mewa Singh, Mridula Singh, Honnavalli N. Kumara, Dilip Chetry & Santanu Descripton of a new species of Omyomymar Schauf from India with a key Mahato, Pp. 17060–17062 to Oriental species and frst report of Palaeoneura markhoddlei Triapitsyn (Hymenoptera: Mymaridae) from the Indian subcontnent – H. Sankararaman & S. Manickavasagam, Pp. 17003–17008

Incursion of the killer sponge Terpios hoshinota Rützler & Muzik, 1993 on the coral reefs of the Lakshadweep archipelago, Arabian Sea Publisher & Host – Rocktm Ramen Das, Chemmencheri Ramakrishnan Sreeraj, Gopi Mohan, Kotarathil Rajendran Abhilash, Vijay Kumar Deepak Samuel, Purvaja Ramachandran & Ramesh Ramachandran, Pp. 17009–17013

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