Abstract
Sexual reproduction of the cyanobacteriosponge, Terpios hoshinota, was studied at Lyudao (Green Island), Taiwan, from 2011 to 2013 through histological examinations, electron microscopy, and in situ observations of larval release. Histological examinations identified five reproductive structures: oocytes, sperm cysts, cell masses, early-stage embryos, and mature embryos. These reproductive structures were often observed in the same specimens, indicating that T. hoshinota is a hermaphroditic brooder. No cyanobacteria were seen in the gametes, and transmission of symbiotic cyanobacteria from parental tissues to larvae likely occurred during embryogenesis. The cell mass, a loose aggregate of numerous symbiotic cyanobacteria and maternal sponge cells, appeared to be eventually incorporated and constitutes the inner part of pre-hatching larvae, suggesting that the larval type is pseudoblastula instead of parenchymella as previously suggested. A clear lunar periodicity was seen in the reproductive cycle; larvae were released mostly around the full moon and occasionally around the new moon. Reproductive activity declined during months with low temperatures (January–April). The larvae were characterized by negative buoyancy and limited mobility, suggesting a larval dispersal distance on a scale of meters under calm weather. However, long-distance dispersal of larvae could still be possible through occasional strong currents during bad weather, such as typhoons, if the larvae survived during the dispersal period by accessing extra energy from the symbiotic cyanobacteria through their photosynthates and/or consuming the cyanobacteria as a source of nutrients. This study showed that T. hoshinota has high fecundity, with a monthly release of numerous larvae over a long reproductive season. This high fecundity, along with local larval dispersal and rapid post-settlement growth, enables rapid population expansion of T. hoshinota.
References
Bryan PG (1973) Growth rate, toxicity, and distribution of the encrusting sponge Terpios sp. (Hadromerida: Suberitidae) in Guam, Mariana Islands. Micronesica 9:237–242
de Voogd N, Cleary D, Dekker F (2013) The coral-killing sponge Terpios hoshinota invades Indonesia. Coral Reefs 32:755
Elliott J, Patterson M, Vitry E, Summers N, Miternique C (2015) Morphological plasticity allows coral to actively overgrow the aggressive sponge Terpios hoshinota (Mauritius, Southwestern Indian Ocean). Mar Biodivers 2015:1–5
Ereskovsky AV (2010) The comparative embryology of sponges. Springer, Dordrecht, Heidelberg, London, New York
Ereskovsky AV, Bouryesnault N (2002) Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha): transmission of maternal cells and symbiotic bacteria. J Nat Hist 36:1761–1775
Ereskovsky AV, Gonobobleva E, Vishnyakov A (2005) Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar Biol 146:869–875
Fujii T, Keshavmurthy S, Zhou W, Hirose E, Chen C, Reimer J (2011) Coral-killing cyanobacteriosponge (Terpios hoshinota) on the Great Barrier Reef. Coral Reefs 30:483
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
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
Hsu C-M, Wang J-T, Chen CA (2013) Larval release and rapid settlement of the coral-killing sponge, Terpios hoshinota, at Green Island, Taiwan. Mar Biodivers 43:259–260
Lévi C, Lévi P (1976) Embryogenese de Chondrosia reniformis (Nardo), demosponge ovipare, et transmission des bacteries symbiotiques. Ann Sci Nat Zool 18:367–380
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
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
Plucer-Rosario G (1987) The effect of substratum on the growth of Terpios, an encrusting sponge which kills corals. Coral Reefs 5:197–200
Reimer JD, Nozawa Y, Hirose E (2011a) 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 (2011b) Current status of the distribution of the coral-encrusting cyanobacteriosponge Terpios hoshinota in southern Japan. Galaxea 13:35–44
Rützler K, Muzik K (1993) Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs. Sci Mar 57:395–403
Schils T (2012) Episodic eruptions of volcanic ash trigger a reversible cascade of nuisance species outbreaks in pristine coral habitats. PloS One 7:e46639
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
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
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 2015:1–11
Wang J-T, Hirose E, Hsu C-M, Chen Y-Y, Meng P-J, Chen CA (2012) A coral-killing sponge, Terpios hoshinota, releases larvae harboring cyanobacterial symbionts: an implication of dispersal. Zool Stud 51:314–320
Yamaguchi M (1986) Introduction to the study of coral reefs 4—Coral-reef sponges (1) Sponges as destroyers of reef-building corals. Aquabiology 8:88–92 (in Japanese)
Acknowledgments
The authors are grateful to A-C Chung, C-H Lin, C-H Liu, C-N Yang, H-S Hsieh, S-L Chen, T-Y Huang, and the Chiu-Fu Diving Shop for their assistance. Invaluable comments and suggestions from two anonymous reviewers improved the original manuscript. This study was supported by a research grant from the Ministry of Science and Technology, Taiwan, R.O.C. (NSC 98-2321-B-001-023-MY3), an internal research grant from the Biodiversity Research Center, Academia Sinica, and the International Research Hub Project for Climate Change and Coral Reef/Island Dynamics from the University of the Ryukyus.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Mark R. Patterson
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nozawa, Y., Huang, YS. & Hirose, E. Seasonality and lunar periodicity in the sexual reproduction of the coral-killing sponge, Terpios hoshinota . Coral Reefs 35, 1071–1081 (2016). https://doi.org/10.1007/s00338-016-1417-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-016-1417-0