Abstract
Terpios hoshinota is a black, encrusting sponge that hosts numerous symbiotic cyanobacteria in its tissues. The sponge often overgrows live scleractinian corals, thereby causing widespread and accelerated coral loss. However, our understanding of how subtropical waters influence the seasonal change in the progression rate of the sponge is poor. To elucidate the progression dynamics over a year, we obtained monthly measurements of linear progression of T. hoshinota (mm month−1) on the branching coral Montipora digitata in the subtropical waters of Sesoko Island, Okinawa, Japan from 2019 to 2020. The progression rate of T. hoshinota varied monthly throughout the year. The progression rates were the highest in summer (July, August, and October) with a mean value of 66 mm month−1, except in September, when strong typhoons came close to Okinawa and the progression rate decreased temporarily. The progression rates were the lowest in February 2020, at 9 mm month−1. The mean annual linear progression rate was estimated to be 28 mm month−1. Therefore, the progression dynamics of T. hoshinota could be linked to their growth mechanisms in relation to the seasonal changes in subtropical waters.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.
References
Baird AH, Pratchett MS, Hoey AS, Herdiana Y, Campbell SJ (2013) Acanthaster planci is a major cause of coral mortality in Indonesia. Coral Reefs 32:803–812. https://doi.org/10.1007/s00338-013-1025-1
Barthel D (1986) On the ecophysiology of the sponge Halichondria panicea in Kiel Bight, I. Substrate specificity, growth and reproduction. Mar Ecol Prog Ser 32:291–298. https://doi.org/10.3354/meps032291
Bell J, Barnes D, Turner J (2002) The importance of micro and macro morphological variation in the adaptation of a sublittoral demosponge to current extremes. Mar Biol 140:75–81. https://doi.org/10.1007/s002270100665
Bryan PG (1973) Growth rate, toxicity, and distribution of the encrusting sponge Terpios sp. (Hadromerida: Suberitidae) in Guam. Mariana Islands Micronesica 9:237–242
Chadwick NE, Morrow KM (2010) Competition among sessile organisms on coral reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, New York, pp 347–371
De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27–year decline of coral cover on the great barrier reef and its causes. Proc Natl Acad Sc USA 109:17995–17999. https://doi.org/10.1073/pnas.1208909109
Elliott JB, Patterson M, Vitry E, Summers N, Miternique C (2016) Morphological plasticity allows coral to actively overgrow the aggressive sponge Terpios hoshinota (Mauritius, Southwestern Indian Ocean). Mar Biodiv 46:489–493. https://doi.org/10.1007/s12526-015-0370-4
Fujii T, Keshavmurthy S, Zhou W, Hirose E, Chen CA, Reimer JD (2011) Coral-killing cyanobacteriosponge (Terpios hoshinota) on the Great Barrier Reef. Coral Reefs 30:483. https://doi.org/10.1007/s00338-011-0734-6
Garrabou J, Zabala M (2001) Growth dynamics in four mediterranean demosponges. Estuar Coast Shelf Sci 52:293–303
Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:7537. https://doi.org/10.1038/nature14140
Hirose E, Murakami A (2011) Microscopic anatomy and pigment characterization of coral-encrusting black sponge with cyanobacterial symbiont, Terpios hoshinota. Zool Sci 28:199–205. https://doi.org/10.2108/zsj.28.199
Hoeksema BW, Waheed Z, de Voogd NJ (2014) Partial mortality in corals overgrown by the sponge Terpios hoshinota at Tioman Island, Peninsular Malaysia (South China Sea). Bull Mar Sci 90:989–990. https://doi.org/10.5343/bms.2014.1047
Hohenegger J (2006) The importance of symbiont-bearing benthic foraminifera for West Pacific carbonate beach environments. Mar Micropaleontol 61:4–39. https://doi.org/10.1016/j.marmicro.2006.05.007
Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933. https://doi.org/10.1126/science.1085046
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloh MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83. https://doi.org/10.1126/science.aan8048
Japan Meteorological Agency (2019a) Annual report on the activities of the RSMC Tokyo – Typhoon Center 2019. 115 pp.
Jones RS, Randall RH, Wilder MJ (1976) Biological impact caused by changes on a tropical reef – Final report. Environmental Protection Agency, Narragansett, Rhode Island. EPA-600/3–76–027, NTIS, Springfield, Virginia. 209 pp
Kuta KG, Richardson LL (1996) Abundance and distribution of black band disease on coral reefs in the northern Florida Keys. Coral Reefs 15:219–223. https://doi.org/10.1007/BF01787455
Leys SP, Lauzon NRJ (1998) Hexactinellid sponge ecology: growth rates and seasonality in deep water sponges. J Exp Mar Biol Ecol 230:111–129. https://doi.org/10.1016/S0022-0981(98)00088-4
Liao M-H, Tang S-L, Hsu C-M, Wen K-C, Wu H, Chen W-M, Wang J-T, Meng P-J, Twan W-H, Lu C-K (2007) The ‘“black disease”’ of reef-building corals at Green Island, Taiwan outbreak of a cyanobacteriosponge Terpios hoshinota (Suberitidae; Hadromerida). Zool Stud 46:520
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131. https://doi.org/10.1046/j.1461-0248.2001.00203.x
Madduppa H, Schupp PJ, Faisal MR, Sastria MY, Thoms C (2017) Persistent outbreaks of the “black disease” sponge Terpios hoshinota in Indonesian coral reefs. Mar Bio 47:149–151. https://doi.org/10.1007/s12526-015-0426-5
May LA, Burnett AR, Miller CV, Pisarski E, Webster LF, Moffitt ZJ, Pennington P, Wirth E, Baker G, Ricker R, Woodley CM (2020) Effect of Louisiana sweet crude oil on a Pacific coral. Pocillopora damicornis Aquat Toxicol 28:105454. https://doi.org/10.1016/j.aquatox.2020.105454
McMurray SE, Blum JE, Pawlik JR (2008) Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. Mar Biol 155:159–171. https://doi.org/10.1007/s00227-008-1014-z
Japan Meteorological Agency (2019b) https://www.data.jma.go.jp/gmd/kaiyou/db/wave/chart/wavepoint/wave_point.html?point=15&year=2019&month=9
Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925–937. https://doi.org/10.1007/s00338-010-0695-1
Montano S, Chou W-H, Chen CA, Galli P, Reimer JD (2015) First record of the coral-killing sponge Terpios hoshinota in the Maldives and Indian Ocean. Bull Mar Sci 91:97–98. https://doi.org/10.5343/bms.2014.1054
Nozawa Y, Huang YS, Hirose E (2016) Seasonality and lunar periodicity in the sexual reproduction of the coral-killing sponge, Terpios hoshinota. Coral Reefs 35:1071–1081. https://doi.org/10.1007/s00338-016-1417-0
Osborne K, Dolman AM, Burgess SC, Johns KA (2011) Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995–2009). PLoS ONE 6:e17516. https://doi.org/10.1371/journal.pone.0017516
Plucer-Rosario G (1987) The effect of substratum on the growth of Terpios, an encrusting sponge which kills corals. Coral Reefs 5:197–200. https://doi.org/10.1007/BF00300963
Pratchett MS, Hoey AS, Wilson SK, Messmer V, Graham NAJ (2011) Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3:424–452. https://doi.org/10.3390/d3030424
Reimer JD, Nozawa Y, Hirose E (2010) Domination and disappearance of the black sponge: a quarter century after the initial Terpios outbreak in southern Japan. Zool Stud 50:394
Reimer JD, Mizuyama M, Nakano M, Fujii T, Hirose E (2011) Current status of the distribution of the coral-encrusting cyanobacteriosponge Terpios hoshinota in southern Japan. Galaxea J Coral Reef Stud 13:35–44. https://doi.org/10.3755/galaxea.13.35
Rützler K, Muzik K (1993) Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs. Sci Mar 57:395–403
Shi Q, Liu GH, Yan HQ, Zhang HL (2012) Black disease (Terpios hoshinota): a probable cause for the rapid coral mortality at the northern reef of Yongxing Island in the South China Sea. Ambio 41:446–455. https://doi.org/10.1007/s13280-011-0245-2
Singh T, Iijima M, Yasumoto K, Sakai K (2019) Effects of moderate thermal anomalies on Acropora corals around Sesoko Island Okinawa. PLoS ONE 14:e0210795. https://doi.org/10.1371/journal.pone.0210795
Sipkema D, Yosef NAM, Adamczewski M, Osinga R, Mendola D, Tramper J, Wijffels RH (2006) Hypothesized kinetic models for describing the growth of globular and encrusting demosponges. Mar Biotechnol (NY) 8:40–51. https://doi.org/10.1007/s10126-005-5002-8
Sokolow S (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Org 87:5–18. https://doi.org/10.3354/dao02099
Soong K, Yang S-L, Chen CA (2009) A novel dispersal mechanism of a coral-threatening sponge, Terpios hoshinota (Suberitidae, Porifera). Zool Stud 48:596
Tada K, Sakai K, Nakano Y, Takemura A, Montani S (2003) Size-fractionated phytoplankton biomass in coral reef waters off Sesoko Island, Okinawa, Japan. J Plankton Res 25:991–997. https://doi.org/10.1093/plankt/25.8.991
Tang S-L, Hong M-J, Liao M-H, Jane W-N, Chiang P-W, Chen C-B, Chen CA (2011) Bacteria associated with an encrusting sponge (Terpios hoshinota) and the corals partially covered by the sponge. Environ Microbiol 13:1179–1191. https://doi.org/10.1111/j.1462-2920.2010.02418.x
Teruya T, Nakagawa S, Koyama T, Arimoto H, Kita M, Uemura D (2004) Nakiterpiosin and nakiterpiosinone, novel cytotoxic C-nor-D-homosteroids from the Okinawan sponge Terpios hoshinota. Tetrahedron 60:6989–6993. https://doi.org/10.1016/j.tet.2003.08.083
Thinesh T, Mathews G, Raj KD, Edward JKP (2017) Outbreaks of Acropora white syndrome and Terpios sponge overgrowth combined with coral mortality in Palk Bay, southeast coast of India. Dis Aquat Org 126:63–70. https://doi.org/10.3354/dao03155
Thinesh T, Meenatchi R, Pasiyappazham R, Jose PA, Selvan M, Kiran GS, Selvin J (2017) Short-term in situ shading effectively mitigates linear progression of coral-killing sponge Terpios hoshinota. PLoS ONE 12:e0187004. https://doi.org/10.1371/journal.pone.0182365
Turon X, Tarjuelo I, Uriz MJ (1998) Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: correlation with population structure and investment in defense. Funct Eco 12:631–639. https://doi.org/10.1046/j.1365-2435.1998.00225.x
Van der Ent E, Hoeksema BW, de Voogd NJ (2015) Abundance and genetic variation of the coral-killing cyanobacteriosponge Terpios hoshinota in the Spermonde Archipelago, SW Sulawesi, Indonesia. J Mar Biol Assoc UK 96:453–463. https://doi.org/10.1017/S002531541500034X
Van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76. https://doi.org/10.3354/meps09203
Veron JEN, Minchin PR (1992) Correlation between sea surface temperature, circulation patterns and the distribution of hermatypic corals of Japan. Cont Shelf Res 12:835–857. https://doi.org/10.1016/0278-4343(92)90047-N
Wang J-T, Hsu C-M, Kuo C-Y, Meng P-J, Kao S-J, Chen CA (2015) Physiological outperformance at the morphologically-transformed edge of the cyanobacteriosponge Terpios hoshinota (Suberitidae: Hadromerida) when confronting opponent corals. PLoS ONE 10:e0131509. https://doi.org/10.1371/journal.pone.0131509
Wulff J (2016) Sponge contributions to the geology and biology of reefs: past, present, and future. In: Hubbard DK, Lipps JH, Rogers CS, Stanley Jr GD (eds) Coral reefs of the world 6, Coral reefs at the crossroads, pp 103–126. https://doi.org/10.1007/978-94-017-7567-0
Yamano H, Hori K, Yamauchi M, Yamagawa O, Ohmura A (2001) Highest-latitude coral reef at Iki Island, Japan. Coral Reef 20:9–12. https://doi.org/10.1007/s003380100137
Yomogida M, Mizuyama M, Kubomura T, Reimer JD (2017) Disappearance and return of an outbreak of the coral-killing cyanobacteriosponge Terpios hoshinota in Southern Japan. Zool Stud 56:1–7. https://doi.org/10.6620/ZS.2017.56-07
Acknowledgments
This work was supported by JSPS (Japan Society for the Promotion of Science) KAKENHI (no. 19K06091 to HY). We thank the staff of Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus for their kind support. Coral sampling was carried out with the approval of the authorities of Okinawa Prefecture, Japan. We are grateful to anonymous reviewers with their comments and suggestions. All necessary permits for sampling and observational field studies were obtained from the concerned authorities and are mentioned in the acknowledgments section
Funding
This work was supported by a grant from the Japan Society for the Promotion of Science (JSPS) KAKENHI (grant no. 19K06091).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by SNA and HY. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Topic Editor Anastazia Teresa Banaszak
Rights and permissions
About this article
Cite this article
Aini, S.N., Tang, SL. & Yamashiro, H. Monthly progression rates of the coral-killing sponge Terpios hoshinota in Sesoko Island, Okinawa, Japan. Coral Reefs 40, 973–981 (2021). https://doi.org/10.1007/s00338-021-02099-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-021-02099-6