First Record of the Genus Umimayanthus from Palau

Home , Antipathozoanthus, Epizoanthidae, Parazoanthidae, Parazoanthus

Marine Biodiversity Records, page 1 of 5. # Marine Biological Association of the United Kingdom, 2015 doi:10.1017/S1755267215001177; Vol. 8; e143; 2015 Published online First record of the genus Umimayanthus from Palau and Micronesia javier montenegro1, julien lorion1,2,3 and james davis reimer1,4 1Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213, Japan, 2Palau International Coral Reef Center, P.O. Box 7086, 1 M-Dock Road, Koror, PW 96940, Palau, 3Palau Community College, P.O. Box 9, Koror, PW 96940, Palau, 4Tropical Biosphere Research Center, University of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213, Japan

Until recently, the only sponge-associated genera in the order Zoantharia were Parazoanthus (family Parazoanthidae), Epizoanthus and Thoracactis (family Epizoanthidae), both within the suborder Macrocnemina. The taxonomy of the genus Parazoanthus, as originally described, has been undergoing revision since 2010, with several species, genera and even families described. In 2015, multiple molecular markers were used in combination with morphological characteristics to erect the genus Umimayanthus inside the family Parazoanthidae. It included three species described from southern Japan, with other records for some of the species from the Great Barrier Reef, New Caledonia and the Red Sea. However, little is known of its distribution in the Pacific Islands. Here we report on the finding of Umimayanthus specimens in Palau, Micronesia, representing the first records for this region. A total of 32 specimens of Umimayanthus were collected from seven different locations; eight of the specimens were identified as Umimayanthus chanpuru, while the remaining 24 colonies were only identified to genus level.

Keywords: Umimayanthus chanpuru, Umimayanthus miyabi, sponge, Palau

Submitted 5 June 2015; accepted 25 August 2015

INTRODUCTION are currently three newly erected Indo-Pacific species in the genus, with another species, Umimayanthus parasiticus Until recently, the only sponge-associated genera in the order (Duchassaing de Fonbressin & Michelotti, 1860), in the Zoantharia were Parazoanthus (family Parazoanthidae), and Caribbean region. Umimayanthus chanpuru has been reported Epizoanthus and Thoracactis (family Epizoanthidae), both from southern Japan, the Great Barrier Reef (GBR), New within the suborder Macrocnemina. The taxonomy of the Caledonia and the Red Sea, while Umimayanthus miyabi has genus Parazoanthus has been a challenge throughout its taxo- also been reported from southern Japan and the GBR nomic history, as the ecological ranges of the genus are wide (Montenegro et al., 2015). Finally, Umimayanthus nakama is and useful morphological characteristics are few (Sinniger only known from southern Japan (Montenegro et al., 2015). et al., 2005). In recent years, the genus has undergone major Zoantharians of taxa such as Umimayanthus are easily over- modifications, with several genera, species and even families looked and also difficult to survey given their cryptic habitat described. Its revision started with Sinniger et al. (2010), and inconspicuous morphologies. As the three Indo-Pacific who used molecular and ecological characteristics to divide Umimayanthus spp. have been recently described and are also the genus Parazoanthus into the genus Antipathozoanthus inconspicuous, more studies are needed to confirm the true within the family Parazoanthidae for species associated with extent of their distributions. In this study, we report on the antipatharians, genus Hydrozoanthus within the family first records of Umimayanthus from Palau, and by extension Hydrozoanthidae for species associated with hydrozoans, and from Micronesia. Parazoanthus sensu stricto for zoantharians living on sponges. However, Sinniger et al.(2010) noted that Parazoanthus was still a polyphyletic group composed of three clades. Recently, MATERIAL, METHODS AND Montenegro et al. (2015) used multiple molecular markers RESULTS combined with morphological characteristics to erect the genus Umimayanthus inside the family Parazoanthidae to for- Specimens were collected by SCUBA at depths between 8 and mally describe one of these Parazoanthus clades. 37 m during surveys conducted between 11 September and 17 Umimayanthus, the most recently described genus of September 2014. A total of 32 colonies were collected from sponge-associated zoantharians, is believed to be widely distrib- seven different locations (Figure 1; Table 1). All specimens uted in the Indo-Pacific region (Montenegro et al., 2015). There were identified as belonging to the genus Umimayanthus by confirmation of the following characteristics: specimens were associated with encrusting sponges, most of the speci-

Corresponding author: mens were found in shaded environments and all colonies J. Montenegro had small polyps (polyp diameter range ¼ 0.3–1.7 mm, x ¼ Email: [email protected] 0.79, SD ¼ 0.22, N ¼ 359) that were smaller than any other

1 2javiermontenegroet al.

Fig. 1. Map of southern part of Palau showing sampling locations and specimen pictures for representative specimens collected in this study.

known sponge-associated zoantharian species in the lividum Cutress, 1971 from Australia has diameters of 2 mm Indo-Pacific. Eight of the samples were identified as and 29 tentacles (see Table 3 in Montenegro et al., 2015). Umimayanthus chanpuru by the number of tentacles (16 to The above evidence leaves us confident that all specimens 18) (Figure 2), while 24 specimens were only identified to reported in this study belong to the genus Umimayanthus. genus level as Umimayanthus sp. (Figure 3). There is one previous record in Reimer et al. (2013)ofa sponge-associated Zoantharia specimen from Palau, at Nikko Bay, site XXIX, depth 3 m, reported as ‘Parazoanthus sp.’. We also refer this specimen to the genus DISCUSSION Umimayanthus, given that it was associated with an encrusting sponge and had a small polyp diameter. Nevertheless, The genus Umimayanthus was originally defined as: molecular and morphological analyses are required to accur- ately identify the majority of our Umimayanthus specimens ... exclusively associated with sponges, usually encrusting to the species level. and cushion sponges, occasionally with massive sponges. Some of the specimens reported here were identified as Polyps generally scattered over the sponge surface... Umimayanthus chanpuru due to their habitat, host sponge Polyps may be solitary or connected to each other by a morphology, and tentacle numbers. Specimens 80J, 82J, 86J, stolon through a thin but clearly visible coenenchyme 89J, 93J, 97J, 77JR and 81JR (Figure 2) were found associated either over or under the sponge surface... Tentacles with encrusting sponges inhabiting cracks and holes on the equal or longer than the expanded oral disc diameter... (Montenegro et al., 2015). reef, and had tentacle numbers ranging from 16 to 18 (Umimayanthus chanpuru original description 14 to 20 tenta- All of the above characteristics match very well with the speci- cles, Montenegro et al., 2015). Three specimens (75J, 94J and mens reported in this study. Additionally, Umimayanthus has 95J; Figure 3) had morphological similarities to the smallest polyp sizes (0.16–2.3 mm) of all formally Umimayanthus miyabi, with delicate and slender tentacles, described sponge-associated Parazoanthidae species inhabit- different from Umimayanthus chanpuru’s tentacles, with a ing the Pacific Ocean; Parazoanthus aruensis Pax, 1910 from more robust morphology. Therefore, given that in these Indonesia has polyp diameters of 5 mm and 36 tentacles, three specimens the number of tentacles and the morphology Parazoanthus darwini Reimer & Fujii, 2010 from the of the host sponge did not match the original description of Galapagos has diameters of 3–6 mm and 24–30 tentacles, Umimayanthus miyabi (18 to 22 tentacles, and exclusively Parazoanthus elongatus McMurrich, 1904 from New Zealand associated with non-encrusting sponges, Montenegro et al., and Chile has diameters of 6 mm and 40–48 tentacles, 2015), they were identified as belonging to Umimayanthus Parazoanthus juanfernandezii Carlgren, 1922 from Chile has sp. The remaining specimens (23) were classified only to diameters of 5 mm and 40–44 tentacles, and Parazoanthus genus level given that no tentacles were visible in the pictures. Table 1. List of specimens of genus Umimayanthus collected in Palau.

Samples Taxonomic identiﬁcation No. of Polyps Sponge Polyp colour Latitude Longitude Locality Area Country Ocean Depth Date Collected by ID # tentacles diameter colour (m) range(mm)

80J Umimayanthus chanpuru 16–18 0.32–0.85 Orange Yellow 7818′24.6′′N 134813′53.4′′E Siaes Corner Siaes Palau Pacific 17.2 14/9/2014 J. Montenegro 82J Umimayanthus chanpuru 16–18 0.49–1.15 Pink Yellow 7808′12.3′′N 134813′16.5′′E Blue Corner Ngemelis Palau Pacific 15.9– 14/9/2014 J. Montenegro 27 86J Umimayanthus chanpuru 18 0.93–1.59 Orange Yellow 7818′54.9′′N 134813′13.3′′E Siaes Tunnel Siaes Palau Pacific 18.4 15/9/2014 J. Montenegro 89J Umimayanthus chanpuru 16–18 0.70–1.02 Orange Yellow 7818′54.9′′N 134813′13.3′′E Siaes Tunnel Siaes Palau Pacific 13.4 15/9/2014 J. Montenegro 93J Umimayanthus chanpuru 18 0.67–0.97 White Yellow 7808′29.5′′N 134813′23.3′′E Blue Hole Ngemelis Palau Pacific 18.5 15/9/2014 J. Montenegro 97J Umimayanthus chanpuru 16–18 0.58–0.68 Purple Yellow 7815′34.8′′N 134831′06.4′′E Short Drop-Off Uchelbeluu Palau Pacific 30.5 17/9/2014 J. Montenegro North 77JR Umimayanthus chanpuru 18 0.56–1.21 Orange White/ 7814′35.3′′N 134822′19.9′′E Cemetery Reef Taoch Palau Pacific 9.5 12/9/2014 J. Reimer orange 81JR Umimayanthus chanpuru 16 0.44-0.84 Green Yellow 7808′12.3′′N 134813′16.5′′E Blue Corner Ngemelis Palau Pacific 18.2 14/9/2014 J. Reimer 75J Umimayanthus sp. 16 0.61–0.81 Green Yellow/ 7814′35.3′′N 134822′19.9′′E Cemetery Reef Taoch Palau Pacific 16 12/9/2014 J. Montenegro transparent 94J Umimayanthus sp. 16 0.57–0.95 Green Yellow/ 7810′08.5′′N 134822′32.8′′E Near Jellyfish Jellyfish Palau Pacific 15.9 16/9/2014 J. Montenegro transparent Lake area Lake 95J Umimayanthus sp. 16–18 0.55–0.94 Orange White/ 7810′08.5′′N 134822′32.8′′E Near Jellyfish Jellyfish Palau Pacific 15 16/9/2014 J. Montenegro orange Lake area Lake 76J Umimayanthus sp. N.A. 0.67–1.05 Orange Yellow 7815′34.8′′N 134831′06.4′′E Short Drop-Off Uchelbeluu Palau Pacific 29.9 13/9/2014 J. Montenegro 78J Umimayanthus sp. N.A. 0.75–1.21 Orange Yellow 7818′24.6′′N 134813′53.4′′E Siaes Corner Siaes Palau Pacific 37 14/9/2014 J. Montenegro 79J Umimayanthus sp. N.A. 0.52–0.99 Green Yellow 7818′24.6′′N 134813′53.4′′E Siaes Corner Siaes Palau Pacific 26.1 14/9/2014 J. Montenegro 81J Umimayanthus sp. N.A. 0.50–0.92 Orange Yellow 7808′12.3′′N 134813′16.5′′E Blue Corner Ngemelis Palau Pacific 27 14/9/2014 J. Montenegro 83J Umimayanthus sp. N.A. 0.96–1.70 White Orange 7818′54.9′′N 134813′13.3′′E Siaes Tunnel Siaes Palau Pacific 31.8 15/9/2014 J. Montenegro 84J Umimayanthus sp. N.A. 0.30–0.68 Orange/ Yellow 7818′54.9′′N 134813′13.3′′E Siaes Tunnel Siaes Palau Pacific 34.2 15/9/2014 J. Montenegro yellow 85J Umimayanthus sp. N.A. 0.50–1.12 Orange Yellow 7818′54.9′′N 134813′13.3′′E Siaes Tunnel Siaes Palau Pacific 20.9 15/9/2014 J. Montenegro 87J Umimayanthus sp. N.A. 0.39–0.76 Orange Yellow 7818′54.9′′N 134813′13.3′′E Siaes Tunnel Siaes Palau Pacific 14.1 15/9/2014 J. Montenegro 88J Umimayanthus sp. N.A. 0.63–1.23 Green Yellow 7818′54.9′′N 134813′13.3′′E Siaes Tunnel Siaes Palau Pacific 13.3 15/9/2014 J. Montenegro 90J Umimayanthus sp. N.A. 0.54–0.93 White Brown 7808′29.5′′N 134813′23.3′′E Blue Hole Ngemelis Palau Pacific 24.2 15/9/2014 J. Montenegro 91J Umimayanthus sp. N.A. 0.45–1.16 Red White 7808′29.5′′N 134813′23.3′′E Blue Hole Ngemelis Palau Pacific 21.5 15/9/2014 J. Montenegro 92J Umimayanthus sp. N.A. 0.92–1.38 Orange/ White 7808′29.5′′N 134813′23.3′′E Blue Hole Ngemelis Palau Pacific 18.5 15/9/2014 J. Montenegro red 96J Umimayanthus sp. N.A. 0.69–1.09 Orange Yellow 7806′39.0′′N 134821′56.4′′E Ngerchong Ngerchong Palau Pacific 16.3 17/9/2014 J. Montenegro 98J Umimayanthus sp. N.A. 0.38–0.60 Purple/ Yellow 7815′34.8′′N 134831′06.4′′E Short Drop-Off Uchelbeluu Palau Pacific 14.8 17/9/2014 J. Montenegro white North 76JR Umimayanthus sp. N.A. 0.42–0.78 Grey Orange 7814′35.3′′N 134822′19.9′′E Cemetery Reef Taoch Palau Pacific 10.1 12/9/2014 J. Reimer 78JR Umimayanthus sp. N.A. 0.47–1.00 Orange White/orange 7814′35.3′′N 134822′19.9′′E Cemetery Reef Taoch Palau Pacific 4.2 12/9/2014 J. Reimer 79JR Umimayanthus sp. N.A. 0.88–1.46 Red White/orange 7819′34.2′′N 134829′40.0′′E Nikko1 Nikko Bay Palau Pacific 19 12/9/2014 J. Reimer 80JR Umimayanthus sp. N.A. 0.52–0.97 White/ Brown 7815′34.8′′N 134831′06.4′′E Short Drop-Off Uchelbeluu Palau Pacific 27.8 13/9/2014 J. Reimer pink 82JR Umimayanthus sp. N.A. 0.67–1.19 White Brown 7808′29.5′′N 134813′23.3′′E Blue Hole Ngemelis Palau Pacific 26.4 15/9/2014 J. Reimer 83JR Umimayanthus sp. N.A. 0.48–0.90 Orange Yellow 7808′29.5′′N 134813′23.3′′E Blue Hole Ngemelis Palau Pacific 26.4 15/9/2014 J. Reimer 84JR Umimayanthus sp. N.A. 0.51–0.76 Orange Yellow 7806′39.0′′N 134821′56.4′′E Ngerchong Ngerchong Palau Pacific 22.4 17/9/2014 J. Reimer

All specimens were preserved in 99% EtOH. 4javiermontenegroet al.

Fig. 2. In situ images of Umimayanthus chanpuru specimens. Pictures 93J, 97J, 80J, 89J, 86J and 82J are specimens from this study identiﬁed as U. chanpuru.

Fig. 3. In situ images of Umimayanthus sp. specimens collected in this study. Compare similarity of 75J, 94J, 95J with Umimayanthus miyabi images in Montenegro et al.(2015).

Further molecular and morphological analyses are needed to International Coral Reef Center (PICRC) and Palau achieve conclusive identifications of these specimens. Community College (PCC). Dr Yimnang Golbuu (PICRC) However, this report supports the observation that zoanthar- is thanked for his generous support throughout the course ians of the genus Umimayanthus, and in particular of this research. Jay Oruetamor, Arius Merep, Geory Merep Umimayanthus chanpuru, are common and widespread in and Assap Bukurrou at PICRC are thanked for logistical the Indo-Pacific region, as previously hypothesized by support. This is contribution PCoRIE Biodiversity #4. Two Montenegro et al.(2015), and confirms that their distribution anonymous reviewers’ comments improved the manuscript. includes Micronesia. In this study, we have confirmed that the genus Umimayanthus is present in Micronesia. With other reports REFERENCES from the GBR and the Red Sea, it appears that this genus is widely represented in the Indo-Pacific. Future work along the Carlgren O. (1922) Actiniaria and Zoantharia. Further Zoological Results of the Swedish Antarctic Expedition 2, 1–102. east African coast, and in further afield regions such as Polynesia, the Galapagos, the Pacific coast of the Americas Cutress C.E. (1971) Chapter 7: Corallimorpharia, actiniaria and zoanthi- and the east coast of Africa should help to determine the true dea. In Edmund D.G. (ed.) Memoirs of the National Museum of extent of Umimayanthus’s distribution in the Indo-Pacific. Victoria 32. Melbourne, Australia: National Museum of Victoria, 202 pp. Duchassaing de Fonbressin P. and Michelotti J. (1860) Me´moire sur les Coralliaires des Antilles. Turin: Imprimerie Royale, 112 pp., pls. 1–11. ACKNOWLEDGEMENTS [Note: This is separate of a publication with identical title and text in the Memorie della Reale Accademia delle Sci-enze di Torino, Ser. 2, This research was supported by the Science and Technology Vol. 19, pp. 279–365, that appeared in 1861.] Research Partnership for Sustainable Development Montenegro J., Sinniger F. and Reimer J.D. (2015) Unexpected diversity (SATREPS), ‘Project for sustainable management of coral and new species in the sponge-Parazoanthidae association in southern reef and island ecosystems: responding to the threat of Japan. Molecular Phylogenetics and Evolution 89, 73–90, doi: 10.1016/ climate change’ in Palau, funded by the Japan Science and j.ympev.2015.04.002. Technology Agency (JST) and the Japan International Pax F.A. (1910) Aktinien der Aru-Inseln. In Merton H. (ed.) Zoologischen Cooperation Agency (JICA) in cooperation with the Palau Forschungsreise in den su¨do¨stlichen Molukken, Vol. 33. Abhandlungen record of umimayanthus in palau and micronesia 5

der Senckenbergischen Naturforschenden Gesellschaft (1910–1911). and Frankfurt am Main, Germany: Waldemar Kramer, pp. 300–302. Sinniger F., Reimer J.D. and Pawlowski J. (2010) The Parazoanthidae Reimer J.D., Albinsky D., Yang S-Y. and Lorion J. (2013) Zoanthid (Hexacorallia: Zoantharia) DNA taxonomy: description of two new (Cnidaria: Anthozoa: Hexacorallia: Zoantharia) species of coral reefs in genera. Marine Biodiversity 40, 57–70, doi: 10.1007/s12526-009-0034-3. Palau. Marine Biodiversity 44, 37–44, doi: 10.1007/s12526-013-0180-5. Reimer J. and Fujii T. (2010) Four new species and one new genus of Correspondence should be addressed to: zoanthids (Cnidaria, Hexacorallia) from the Gala´pagos Islands. J. Montenegro ZooKeys 42, 1–36, doi: 10.3897/zookeys.42.378. Molecular Invertebrate Systematics and Ecology Laboratory Sinniger F., Montoya-Burgos J-I., Chevaldonne P. and Pawlowski J. Graduate School of Engineering and Science (2005) Phylogeny of the order Zoantharia (Anthozoa, Hexacorallia) University of the Ryukyus, Senbaru 1, Nishihara based on the mitochondrial ribosomal genes. Marine Biodiversity Okinawa 903-0213, Japan 147, 1121–1128, doi: 10.1007/s00227-005-0016-3. email: [email protected]