Turkish Journal of Zoology Turk J Zool (2015) 39: 432-437 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1403-50

First records of the sea anemones Stichodactyla tapetum and (: Actiniaria: ) from the southeast of Iran, Chabahar (Sea of Oman)

Gilan ATTARAN-FARIMAN*, Pegah JAVID Department of Marine Biology, Faculty of Marine Sciences, Chabahar Maritime University, Chabahar, Iran

Received: 26.03.2014 Accepted: 28.08.2014 Published Online: 04.05.2015 Printed: 29.05.2015

Abstract: Sea anemones (order Actiniaria) are among the most widespread invertebrates in the tropical waters. The anthozoans Stichodactyla haddoni (Saville-Kent, 1893) and Stichodactyla tapetum (Hemprich & Ehrenberg in Ehrenberg, 1834) (family Stichodactylidae) were reported for the first time from the southeastern coast of Iran, Chabahar Bay, Tiss zone. The specimens of S. haddoni and S. tapetum were collected by hand from the intertidal zone of sand and rock substrates in April 2012. The samples characteristics were morphologically studied in the field and laboratory. This study presents a new locality record and information about S. haddoni and S. tapetum found in this part of the tropical sea.

Key words: Exocoelic tentacles, endocoelic tentacles, tropical sea, morphological identification, symbiotic life

1. Introduction like and shrimps (Khan et al., 2004; The order Actiniaria Hertwig, 1882 (phylum ), Katwate and Sanjeevi, 2011, Nedosyko et al., 2014), but with 46 families, includes solitary polyps with soft bodies there has been no report from Stichodactyla tapetum and nonpinnate tentacles (Daly et al., 2007). The family hosting anemonefish (Fautin et al., 2008). Stichodactyla Stichodactylidae Andres, 1883 covers 2 genera and 10 tapetum has 49 records and S. haddoni has 75 records of (Daly et al., 2007). This family is characterized by reports from tropical and subtropical seas (Fautin, 2013). a column having verrucae, a weak endodermal marginal Stichodactyla haddoni occurs in tropical and subtropical sphincter, and short tentacles organized in multiple seas and has been reported in the Red Sea, from the Indian endocoelic rows (Daly et al., 2007). Some factors could be Ocean to New Caledonia, and from Japan and Singapore important in the ’s external morphology and to Australia (Dunn, 1981; Fautin and Allen, 1992; Fautin identification: habitat preferences and coloration pattern et al., 2008; Fautin et al., 2009). In this study, we report (Daly and Fautin, 2004, Fautin et al., 2008), the size of for the first time the species Stichodactyla tapetum and specimen and diameter of the oral disc, the type and size Stichodactyla haddoni from the tropical southeastern of tentacles and their arrangement on the oral disc, and the coasts of Iran and the northern part of the Sea of Oman. kind of verrucae on column (Fautin et al., 2008). All these characteristic differences can be seen among Stichodactyla 2. Materials and methods haddoni (Saville-Kent, 1893) and Stichodactyla tapetum The sampling area was the coast of Tiss located in (Hemprich & Ehrenberg in Ehrenberg, 1834) (Fautin et al., Chabahar Bay on the southeastern coast of Iran (25°22′N, 2008). Most species of Stichodactyla (Brandt, 1835) 60°36′E) and the 8 km around it (Figure 1). The substrata serve as host for the anemonefish, genus Amphiprion of intertidal zone sampling sites were sand flats and rocks. (Bloch and Schneider, 1801). Amphiprion ocellaris (Cuvier, Specimens were collected by hand during low tide, and the 1830) is associated with (Forsskål, temperature and the salinity of the water were recorded. 1775) (Mitchell, 2003). Amphiprion sebae (Bleeker, 1853) Specimens were photographed alive and identified in the is associated with Stichodactyla haddoni and Amphiprion field, and then were transferred alive to the laboratory and clarkii (Bennet, 1830) is symbiotic with Stichodactyla kept in aquaria containing seawater and sand. The external mertensii (Brandt, 1835) (Patzner, 2008). Stichodactyla morphology of the specimens (i.e. size, coloration pattern, haddoni has been reported in symbiotic associations with column, verrucae, and types of tentacles) was assessed. * Correspondence: [email protected] 432 ATTARAN-FARIMAN and JAVID / Turk J Zool

km 0 96 120 290

Figure 1. Map of sampling sites on the southeastern coast of Iran, Chabahar Bay, Tiss, 25°35′N, and 60°11′E to 60°60′E (figuredesigned by Siamak Rahmani).

3. Results Stoichactis haddoni (Saville-Kent, 1893) During low tide at the intertidal sampling site the Stoichactis amboinensis (Pax, 1924) water temperature was 28 °C and the salinity was 34 Stichodactyla haddoni (Dunn, 1981) PSU. Stichodactyla haddoni lives exclusively in sand or Common name: Haddon’s anemone. rubble and it has a different range of patterns and Material examined: CHIAS1, Stichodactyla haddoni, colorations of the oral disc and tentacles. Stichodactyla intertidal zone of Tiss coast, after Tiss Fishing Port, 2012; tapetum is seen on rock beds with different colorations CHIAS2, Stichodactyla haddoni, intertidal zone of Tiss and appearances from S. haddoni. These species have not Beach Resorts, 2012; CHIAS4, Stichodactyla haddoni, Tiss been reported previously from the southeastern coast of coast, 2013; CHIAS8, Stichodactyla haddoni, intertidal Iran. zone of Tiss Beach Resorts, 2013. 3.1. External morphology description Distribution: From Japan to Australia, Indian Ocean SYSTEMATICS to New Caledonia, Red Sea (Dunn, 1981; Fautin and Phylum CNIDARIA Allen, 1992; Fautin et al., 2007), and Singapore (Fautin Class ANTHOZOA et al., 2009); this is the first record of this species for the Subclass southeastern coast of Iran. Order ACTINIARIA Hertwig, 1882 Habitat: Solitary in sandy flat substrata and between Suborder NYNANTHEAE Carlgren, 1899 coral rubbles. Family STICHODACTYLIDAE Andres, 1883 Size: Average size of oral disc 250–400 mm when Genus Stichodactyla Brandt, 1835 expanded. Description: Flat or undulating oral disc, short Remarks: Undulating oral disc wider than pedal disc, tentacles arranged in radial endocoelic rows covering various coloration patterns, 2 distinct types of sticky the oral disc, may or may not be sticky, all tentacles are tentacles: white pointed long ones at the edge of the oral similar but the length may vary and exocoelic tentacles are disc (exocoelic tentacles) and shorter tentacles on the more robust, developed adherent pedal disc, column with entire parts of oral disc with equal length. The rows of verrucae. nonadhesive verrucae are arranged along the entire length Stichodactyla haddoni (Saville-Kent, 1893) of column. Synonym section: Discosoma haddoni (Saville-Kent, This species lives attached firmly to the substrate by 1893) its strong pedal disc, with the column buried in the sandy

433 ATTARAN-FARIMAN and JAVID / Turk J Zool substrate, but can bury the entire body in the sand when it or white streaks at the margin of oral disc. Sometimes it is stimulated. The oral disc has many short tentacles with is completely amethystine to brown. It has been seen to sticky tips. The tentacles are not all alike, and their density associate with anemone shrimp brevicarpalis is lower near the mouth. About 12 mm around the mouth is Schenkel, 1902 in this zone (Figure 2D). devoid of tentacles. At the undulating edge of the oral disc, Stichodactyla tapetum (Hemprich & Ehrenberg in there are short pointed white tentacles emerging in a radial Ehrenberg, 1834) alignment. Each of these tentacles alternates with many Synonym section: Homactis rupicola (Verrill, 1879) rows of small spherical tentacles. These internal tentacles Discosoma amboinensis (Kwietniewski, 1898) with same length are located between the white ones. They Stoichactis tapetum (Carlgren, 1900) are endocoelic tentacles. The marginal white tentacles Stoichactis australis (Lager, 1911) are called exocoelic tentacles, the approximate measured Stoichactis rupicola (Carlgren, 1949) lengths of which were 5 mm. There are nonadhesive Common name: Mini carpet anemone. verrucae on the entire length of the yellow or cream to Material examined: CHIAS9, Stichodactyla tapetum, light green column (Figure 2A). This species is seen in various colorations (Figures 2A–2D). The coloration of intertidal zone of Tiss coast, Tiss Fishing Port, 2012. endocoelic tentacles on the oral disc can be cream and Distribution: From Japan to Australia, Indian Ocean light or dark brown with white streaks. The mouth is to New Caledonia and Red Sea (Dunn, 1981; Fautin and orange and pedal disc is light brown to cream (Figure 2A). Allen, 1992; Fautin, 2008), and Singapore (Fautin et al., The other specimen is a blend of different colors: dark 2009); this is the first record for the southeastern coast of brown and green and purple in some parts, mouth is red Iran. and pedal disc is white to yellow or light brown (Figure Habitat: Solitary (not clonal) and on rocks. 2B). This species is seen with other colorations, too. It can Size: The average diameter of the oral disc is be green, opaque green, or green brown with light green approximately 80–100 mm (Figures 3A and 3B).

Figure 2. Stichodactyla haddoni (Saville-Kent, 1893): (A) S. haddoni under laboratory conditions; cream and light or dark brown with white streaks. The mouth is orange and pedal disc is light brown to cream. About 12 mm around the mouth is devoid of tentacles. (B) The other one is a blend of different colors, dark brown and green and purple in some parts. (C) Green or opaque green with light green streaks at the margin of oral disc. (D) S. haddoni associated with anemone shrimp Periclimenes brevicarpalis (Schenkel, 1902). In all photos: P.d = pedal disc; M = mouth; En = endocoelic tentacles; Ex = exocoelic tentacles; A.S= anemone shrimp. Scale bars: A, 9 cm; B, 10 cm; C, 7 cm; D, 2.54 cm. Photos A–C: Mohammad Bahman; Photo D: Sina Manavi Shaad.

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Figure 3. Stichodactyla tapetum (Hemprich & Ehrenberg in Ehrenberg, 1834): (A) Pedal disc and column are red to dark pink with narrow white strips. (A & B) Oral disc is flat and its average diameter is approximately 8–10 cm. The expanded oral disc is broader than the pedal disc. Tentacles are short and cover the whole oral disc. Coloration of tentacles on oral disc is brown or cream with opaque pink tips. Scale bars: 2.5 cm. In all photos: P.d = pedal disc; O.d = oral disc; M: mouth. Photos A and B: Pegah Javid.

Remarks: This is the smallest species of the genus and biology (Hirose, 1985; Fautin, 1991; Khan et al., 2004) Stichodactyla; it is not clonal, flat oral disc, expanded oral and distribution and (Dunn, 1985; Fautin, 1988; disc broader than the pedal disc, very short similar tightly Uchida and Soyama, 2001; Paulay et al., 2003). packed corn kernel-like tentacles at entire part of oral disc Stichodactyla tapetum is very small, and the measured from mouth to margin, coloration of tentacles on oral disc diameter of the oral disc in the current study was brown or cream with opaque pink tips with light and dark approximately 80–100 mm. It is reported that usually it is brown radial strips; not very strong pedal disc, not firmly not more than 40 mm and a maximum of 100 mm (Fautin attached to rocky substrates, no verrucae on column; pedal et al., 2008). The distribution and taxonomy of S. tapetum disc and column red to dark pink with narrow white strips have been previously reported (Dunn, 1981; Uchida and (Figure 3A); host for no anemonefish. Soyama, 2001; Song and Cha, 2004). However, the species has not been previously reported from Iran. 4. Discussion The type of the symbiont could be a way of identification There are several previous reports from Stichodactyla (Trivedi, 1975). The anemone shrimp Periclimenes sp. haddoni and Stichodactyla tapetum (Table). The accessibility Schenkel, 1902 is associated with S. haddoni (Trivedi, of S. haddoni can be specific in 30–60 m; the species is 1975) and approximately 2 shrimps per S. haddoni are widely distributed throughout the West Pacific (Roelofs reported from Moreton Bay, Australia (Khan et al., 2004). and Silcock, 2008). Stichodactyla haddoni and S. tapetum This symbiont was seen among Iranian specimens. The are not endemic species like (Ellis, inhabitation of anemone shrimp amboinensis (De 1767), which is only known in the Caribbean Sea (Hayes Man, 1888) and (Schmitt, 1924) and Trimm, 2008). has been reported with Stichodactyla helianthus (Hayes and Stichodactyla haddoni is reported as the largest sea Trimm, 2008; Baeza and Piantoni, 2010). Adult specimens anemone in Moreton Bay (Fautin et al., 2008). Exocoelic of anemone shrimps T. amboinensis and Periclimenes tentacles compared with endocoelic ones are more robust, ornatus (Bruce, 1969) are commonly found with Entacmaea approximately 5 mm, but Fautin et al., (2008) reported 3 quadricolor (Leuckart in Ruppell & Leuckart, 1828) and S. mm. Stichodactyla haddoni is morphologically similar tapetum respectively in Taiwan and the Pescadore Islands to Stichodactyla gigantea: all tentacles in S. gigantea are (insular China) (Guo et al., 1996). Stichodactyla tapetum alike, whereas tentacles at the margin of the oral disc in S. is the host for no anemonefish (Fautin et al., 2008). There haddoni are larger and more pointed and all tentacles are was no symbiotic life, neither anemonefish nor anemone not identical (Fautin et al., 2009). Average size of S. haddoni shrimp, for S. tapetum in Iranian species. ranges from 300 to 500 mm and rarely more (Dunn, 1981; Stichodactyla haddoni is reported from substrata with Fautin and Allen, 1992; Katwate and Sanjeevi, 2011); dead coral pieces and sandy clay (Sen Gupta et al., 2003) or this size in the current study was 250–400 mm. Further clay and silt with patches of fine coralline sand (Hashimi et reports have been presented about the species’ ecology al., 1978). It is also observed abundantly in sea grass beds

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Table. Some previous reports of Stichodactyla haddoni and Stichodactyla tapetum.

Species Locality Reference S. tapetum Red Sea Fishelson, 1970 S. haddoni Red sea Dunn, 1981 S. haddoni Seychelles den Hartog, 1994 S. tapetum Northern Taiwan Guo et al., 1996 S. haddoni Indonesia den Hartog, 1997 S. haddoni Australia Khan et al., 2003, 2004 S. tapetum Korea Song and Cha, 2004 S. haddoni & S. tapetum Moreton Bay Fautin et al., 2008 S. tapetum Great Barrier Reef Fautin et al., 2008 S. haddoni & S. tapetum Singapore Fautin et al., 2009 S. haddoni Queensland, Australia Nedosyko, 2014 and muddy sand (Fautin et al., 2009). Iranian samples of S. Acknowledgments haddoni were found in the sand flat substrates and among We are grateful to Sina Manavi Shaad and Mohammad coral pieces, and S. tapetum was found on rocks and it was Bahman for their great help during the field trips and their reported before from sand flats and rock crevices (Fautin photography, and we are thankful to Siamak Rahmani for et al., 2008). his help in preparing the map and photos.

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