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The coral killing sponge Terpios hoshinota in Kimbe Bay, Papua New Guinea

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This is the first record of T. hoshinota from Papua New Guinea, extending its range into the South Pacific Ocean.
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60
Ekins et al.
174 Memoirs of the Queensland Museum | Nature 2017 60
The coral killing sponge Terpios hoshinota in Kimbe Bay, Papua
New Guinea.
The coral killing cyanobacteriosponge Terpios hoshinota was
initially described from Japan and Guam following an
outbreak in 1984 (Rützler & Muzik 1993), but since then has
expanded its range to other areas, including Taiwan (Liao et
al. 2007), Australia (Fuji et al. 2011), Indonesia (de Voogd
et al. 2013, van der Ent et al. 2016), Malaysia (Hoeksema et
al. 2014), the Maldives (Montano et al. 2015) and Mauritius
(Elliot et al. 2016). Terpios hoshinota encrusts a wide range
of coral species and outbreaks cause mortality over large
areas of reef (Rützler & Muzik 1993). Outbreaks may be
devastating on local scales, but reefs can recover, even
when the sponge co-exists in the area for 25 years (Reimer
et al. 2010) and of course outbreaks can reoccur (Yomogida
et al. 2017)
During recent sponge biodiversity and coral health surveys
in Kimbe Bay, Papua New Guinea, the dark gray encrusting
sponge was observed overgrowing live corals in the
genera Acropora (branching and plate species), Montipora
(branching and encrusting species), Goniastrea, Leptoria,
and Pocillopora on the reef flat at Kimbe Island (Figure 1).
When preserved, the sponge tinted ethanol a green colour,
indicating the presence of cyanobacteria. Examination of
the sponge spicules under light and scanning electron
microscopes confirmed the distinctive spicule tylostyles
to be those of T. hoshinota. The specimen of T. hoshinota
collected from Kimbe Bay was compared to specimens of
T. hoshinota previously collected from Japan and Australia
(Fuji et al. 2011). This particular specimen from Kimbe Bay
(QM G336069), along with another specimen from Australia
(QM G331911) and the specimen from Japan (QM G331910),
show a larger maximum tylostyle width than the original
description (Rützler & Muzik 1993) see Table 1. The head
of the tylostyles of these specimens (Figure 2) match those
of T. hoshinota which have characteristic lobes that separate
it from other Terpios species with a similar colouration i.e.
T. granulosa Bergquist, 1967, T. viridis Keller, 1891, T. fugax
Duchassaing & Michelotti, 1864 and T. manglaris Rützler &
Smith, 1993.
This is the first record of T. hoshinota from Papua New
Guinea, extending its range into the South Pacific Ocean.
Kimbe Bay has previously been searched by the authors for
sponge biodiversity in 2007 and corals from 1997 till 2016 with
no previous signs of corals affected by T. hoshinota. In addition,
the authors have been conducting sponge biodiversity
surveys in other parts of Papua New Guinea, including
Milne Bay (2005), South Papua New Guinea Barrier Reef
(1996), and Vanuatu (1996, 1997, 2008), and T. hoshinota
has never been recorded before, further strengthening the
hypothesis that this is a recent introduction into Kimbe
Bay. The influence of disturbances such as coral bleaching,
disease and naturally-occurring predators such as the
crown-of-thorns starfish, Acanthaster planci (Linnaeus
1758) on coral abundance is well documented, but the
current and potential future impact of invasive species
FIG. 1. Terpios hoshinota overgrowing live corals at Kimbe Island,
Kimbe Bay, Papua New Guinea on the 19th of November 2016
(5.20328°S, 150.3803°E).
Specimen, location n Total Length Maximum width Neck Width Head Width Head Length
Description ? 160-290 2.0-4.0 1.5-3.5 3.5-7.0 4.0-7.5
USNM43144, Japan ? 180-252-290 3.0-3.5-4.0 2.0-2.7-3.0 5.5-6.1-7.0 4.5-5.2-6.0
G331910, Japan 25 175-244-283 2.2-5.2-7.0 2.4-3.7-4.9 3.2-6.4-8.9 3.7-6.6-8.2
G331911, Australia 25 171-222-251 2.2-3.2-4.2 1.2-2.2-3.2 3.9-5.8-8.9 2.7-4.6-5.9
G336069, PNG 45 152-216-329 2.2-6.4-10.7 2.5-4.0-5.9 4.1-6.8-9.5 3.9-4.0-9.2
TABLE 1. Tylostyle measurements (minimum, average, maximum) of specimens of Terpios hoshinota (in µm).
FIG. 2. Tylostyle heads of Terpios hoshinota QM G336069
Terpios hoshinota
Memoirs of the Queensland Museum | Nature 2017 60 175
on Indo-Pacific coral reefs has received little attention. Our
observations highlight the potential significance of invasive
species as an agent of coral decline warranting greater
attention.
Acknowledgements
The authors would like to thank Thomas Roberts and
Andrew Baird for their assistance and Mahonia Na Dari
Research and Conservation and Walindi Plantation Resort.
Literature Cited
Bergquist, P.R. 1967. Additions to the sponge fauna of the Hawaiian
Islands. Micronesica 3:159-174.
De Voogd, N.J., Cleary, D.F.R. & Dekker, F. 2013. The coral-killing
sponge Terpios hoshinota invades Indonesia. Coral Reefs 32:
755. https://dx.doi.org/10.1007/s00338-013-1030-4.
Duchassaing De Fonbressin, P. Michelotti, G. (1864). Spongiaires
de la mer Caraibe. Natuurkundige verhandelingen van de
Hollandsche maatschappij der wetenschappen te Haarlem. 21(2):
1-124, pls I-XXV.
Elliott, J., Patterson, M., Summers, N., Miternique, C., Montocchio,
E. & Vitry, E. 2016. How does the proliferation of the coral-
killing sponge Terpios hoshinota affect benthic community
structure on coral reefs? Coral Reefs 35: 1083. https://
dx.doi.org/10.1007/s00338-016-1434-z
Fujii, T., Keshavmurthy, S., Zhou, W., Hirose, E., Chen, C.A. &
Reimer, J.D. 2011. Coral-killing cyanobacteriosponge (Terpios
hoshinota) on the Great Barrier Reef. Coral Reefs 30: 483.
https://dx.doi.org/10.1007/s00338-011-0734-6
Hoeksema, B.W., Waheed, Z. & De Voogd, N.J. 2014. Partial
mortality in corals overgrown by the sponge Terpios hoshinota
at Tioman Island, Peninsular Malaysia (South China Sea).
Bulletin of Marine Science 90:989–990.
Keller, C. 1891. Die Spongienfauna des Rothen Meeres (II. Halfte).
Zeitschrift für wissenschaftliche Zoologie 52: 294-368, pls XVI-XX.
Montano, S., Chou, W.H., Chen, C.A., Galli, P. & Reimer, J.D. 2015.
First record of the coral-killing sponge Terpios hoshinota in
the Maldives and Indian Ocean. Bulletin of Marine Science
91:97–98.
Reimer, J.D, Nozawa, Y. & Hirose, E. 2010. Domination and
disappearance of the black sponge: a quarter century after
the initial Terpios outbreak in southern Japan. Zoological
Studies 50:394
Rützler, K. & Muzik, K. 1993. Terpios hoshinota, a new
cyanobacteriosponge threatening Pacific reefs. Scientia Marina
57(4):395-403.
Rützler, K. & Smith, K.P. 1993. The genus Terpios (Suberitidae)
and new species in the ‘Lobiceps’ complex Scientia Marina
57(4):381-393.
Van Der Ent, E., Hoeksema, B.W. & De Voogd, N.J. 2016.
Abundance and genetic variation of the coral-killing
cyaonobacteriosponge Terpios hoshinota in the Spermonde
Archipelago, SW Sulawesi, Indonesia. Journal of the Marine
Biological Association of the United Kingdom 96(2):453-463.
Yomogida, M., Mizuyama, M., Kubomura, T. & Reimer, J.D. 2017.
Disappearance and Return of an Outbreak of the Coral-
killing Cyanobacteriosponge Terpios hoshinota in Southern
Japan. Zoological Studies 56(7):1-7.
Merrick EKINS1, Bette WILLIS2,3, Tom BRIDGE1,2, Maya
SRINIVASAN3, Sonia ROWLEY4 & John HOOPER1,5. 1Queensland
Museum, PO Box 3300, South Brisbane Qld 4101, Australia; 2ARC
Centre of Excellence for Coral Reef Studies; 3College of Science
and Engineering, James Cook University, Townsville Qld 4811;
4University of Hawai’i at Manoa, Honolulu, HI 96822, USA; 5 Griith
University, Brisbane Qld, 4111.
Accepted: 2 June 2017. First published online: 30 October 2017 –
https://dx.doi.org/10.1082/j.2204-1478.60.2017.2017-02
LSID: urn:lsid:zoobank.org:pub:1427CF44-FAE3-456D-B491-
30DC444A8761
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