Associations of fish juveniles with rhizostome jellyfishes in the
Transcription
Associations of fish juveniles with rhizostome jellyfishes in the
Plankton Benthos Res 9(1): 51–56, 2014 Plankton & Benthos Research © The Plankton Society of Japan Associations of fish juveniles with rhizostome jellyfishes in the Philippines, with taxonomic remarks on a commercially harvested species in Carigara Bay, Leyte Island YUSUKE KONDO1, SUSUMU OHTSUKA1,*, JUN NISHIKAWA2, EPHRIME METILLO3, HONORIO PAGLIAWAN4, SHOZO SAWAMOTO5, MITSUYASU MORIYA2, SHUHEI NISHIDA2 & MAKOTO URATA1 1 Takehara Marine Science Station, Setouchi Field Science Center, Graduate School of Biosphere Science, Hiroshima University, 5–8–1 Minato-machi, Takehara, Hiroshima 725–0024, Japan 2 Atmosphere and Ocean Research Institute, University of Tokyo, 5–1–5 Kashiwanoha, Kashiwa, Chiba 277–8564, Japan 3 Department of Biological Sciences, Mindanao State University-Iligan Institute of Technology, Andres Bonifacio Ave., Tibanga, Iligan City, The Philippines 4 College of Fisheries and Aquatic Sciences, Western Philippines University, Puerto Princesa City, Palawan, Philippines 5 Department of Marine Biology, School of Marine Science and Technology, Tokai University, 3–20–1 Orido, Shimizu, Shizuoka 424–8610, Japan Received 25 October 2013; Accepted 5 December 2013 Abstract: A wide variety of fish and invertebrates are associated with marine jellyfishes, and their interactions are diverse. We preliminarily investigated symbionts on two species of rhizostome jellyfishes collected from Leyte and Palawan Islands, the Philippines, in August 2013. The collected jellyfishes were Lobonemoides robustus Stiasny on both islands and Acromitus maculosus Light on Palawan Island. Lobonemoides robustus is commercially harvested on both islands, and seems to have been previously misidentified as Lobonema smithi Mayer. The associated fish juveniles on these hosts were identified as Alepes djedaba (Forsskål) and Carangoides equula (Temminck & Schlegel). Alepes djedaba is closely associated with many species of scyphozoan jellyfish broadly in the southeastern Asian waters. The associations of carangids with jellyfish are also reviewed. Key words: Acromitus maculosus, carangid, Lobonemoides robustus, rhizostome, symbiosis, the Philippines Introduction Symbiotic interactions are essential to understand the marine ecosystem in general as well as the grazing and microbial food webs (Ohtsuka 2006). Recently much attention has been paid to symbioses in marine pelagic realms, partly because many kinds of parasitoids and parasites have great negative impacts on the population dynamics of their host zooplankters (e.g. Ianora et al. 1987, Kimmerer & McKinnon 1990, Gómez-Gutiérrez et al. 2003, Ohtsuka et al. 2004, 2007, 2010, Coats & Bachvaroff 2012). Some symbionts heavily depend on their host animals for sur* Corresponding author: Susumu Ohtsuka; E-mail, [email protected] vival. For example, the population dynamics of gadids are strongly influenced by the abundance of host jellyfishes, because their juveniles are protected from visual predators by the hosts (Lynam & Brierley 2007). Cnidarians are regarded to be somewhat special as hosts, due to the presence of venomous nematocysts, making symbioses tend to be such as in the mutualistic interactions between sea anemones and anemonefish (Mebs 1994). Large jellyfish can harbor a wide variety of symbionts such as dinoflagellates, cnidarians, helminths, crustaceans, ophiuroids and fishes (Mansueti 1963, Thiel 1970, 1978, Arai 1997, Purcell & Arai 2001, Ohtsuka et al. 2009, 2010, 2011). However, their symbiotic interactions are highly diversified, ranging from phoresy through parasitoidism to mutualism (Ohtsuka et al. 2009). We have been 52 Y. Kondo et al. Fig. 1. Location of the two sampling sites in the Philippines in August 2013. intensively investigating symbioses between jellyfish and other organisms in Asian waters since 2008, and found that juveniles of the shrimp scad Alepes djedaba (Forsskål) is widely associated with many species of large jellyfish in tropical Asian waters (Ohtsuka et al. 2010). In August 2013, we surveyed symbiotic relationships between two species of rhizostomes and their symbionts at two sites in the Philippines. The present paper deals with the symbiotic communities on these hosts, with a taxonomic comment on the Malampaya jellyfish. Two species of carangids, one of which was identified as A. djedaba, were found on the jellyfishes. Mansueti (1963), Thiel (1970, 1978) and Purcell & Arai (2001) comprehensively reviewed symbioses between carangids and host jellyfishes in the world oceans. In the Philippines, Light (1914) reported the association of juveniles of Caranx with Lobonema mayeri Light (=Lobonemoides robustus?) and Rhopilema hispidum (Vanhöffen) (as R. visayana Light). Information on such associations in Asian waters, however, is limited. Therefore, data published since the review of Purcell & Arai (2001) and our original results on Asian Carangidae-jellyfish associations are compiled here. Materials and Methods Sampling sites were located at two stations in the Philippines: Stn 1, Carigara Bay, Leyte Island (11°19′29.08″N, 124°42′49.54″E) on 23 August 2013; Stn 2, Malampaya Fig. 2. A. Stained canal system of Lobonemoides robustus (No. 3), abbreviations: iac, intra-circular anastomosing canal; irc, interrhopalar canal; rc, rhopalar canal; B. Acromitus maculosus (No. 2), exumbrellar view, part of umbrella cut off (No. 2); C. Carangoides equula associated with A. maculosus (No. 5 in Table 2); D. Alepes djedaba associated with A. maculosus (No. 1 in Table 2). Scale bars=1 cm (A); 2 cm (B); 0.5 cm (C, D). Sound, Palawan Island (10°52′09.20″N, 119°24′51.78″E) on 24 August 2013 (Fig. 1). We rented a fishing boat at each station. Each individual jellyfish was gently scooped with a scoop-net (diameter 50 cm; mesh size 2 mm), and put in a plastic bag together with their symbionts. Parts of the umbrella tissues of the jellyfish and the symbionts were preserved in 99.5% ethanol for stable isotopic analyses in the future. At Stn 2, fishermen kindly kept us an individual of the commercially harvested jellyfish (Lobonemoides robustus Stiasny) collected from a fixed net on 23 August 2013. Water temperature and salinity were measured near the surface with a salinometer (Model 556 MPS, YSI). Results and Discussion At Stn 1 (Leyte Is.) the surface water temperature and salinity were 30.3°C and 33.6, respectively. Only L. robustus was observed as a host. Omori & Nakano (2001) suggested that the fisheries target species in Carigara Bay might be Lobonema smithi Mayer. However, we examined the canal system, stained by methylene blue, and came to the conclusion that it is Lobonemoides robustus (Fig. 2A). The genus Lobonemoides is distinguished from the genus Lobonema in that the intra-circular anastomosing canal system does not communicate with the inter-rhopalar canals (Fig. 2A) (e.g. Kramp 1961, Kitamura & Omori 2010). The large-size of the umbrella, numerous exumbrellar papillae and long marginal lappets of the collected specimens are characteristic to L. robustus (Kitamura & Omori 2010). 53 Fish-jellyfish associations in Philippines Table 1. Associations between Lobonemoides robustus and symbionts in Carigara Bay, Leyte Island. Host indiv. 1 2 3 4 5 Umbrella diameter (cm) Wet weight (kg) 54 5.2 48 4.4 46 5.0 38 3.2 29 1.7 Symbionts [number of indiv.; range of body length in mm (mean±s.d.)] Alepes djedaba [n=112; 4.3–28.4 (10.1±4.9)] Charybdis feriata (megalopa) (n=1; 2.2*) Alepes djedaba [n=35; 4.3–36.2 (10.9±6.3)] Charybdis feriata (juvenile) (n=2; 3.9 ,4.7*) Alepes djedaba [n=41; 5.3–32.8 (14.2±7.0)] Charybdis feriata (megalopa) (n=1; 2.5*) Alepes djedaba [n=49; 5.0–29.7 (13.0±6.5)] Charybdis feriata (megalopa) (n=3; 2.0, 2.0, 2.2*) Alepes djedaba [n=10; 9.6–40.5 (19.8±8.3)] Charybdis feriata (juvenile) (n=3; 3.9, 4.6, 4.6*) * carapace width Table 2. Associations between Acromitus maculosus and symbionts in Malampaya Sound, Palawan Island. Host indiv. 1 2 3 4 5 Fig. 3. Body length of Alepes djedaba associated with Lobonemoides robustus collected from Leyte Island (Stn 1). Measurements from five host individuals and the prevalence and intensity of symbiont occurrence are shown in Table 1. Five individuals of L. robustus were captured, ranging from 29–54 cm in umbrella diameter and 1.7– 5.2 kg in wet weight. All hosts harbored juveniles of A. djedaba, with an average of 49.4 symbionts per medusa (prevalence=100%, intensity=49.4). The juveniles ranged from 4.3 to 40.5 mm in body length (n=247, mean±s.d.= 11.9±6.4 mm); the most abundant class was 5–10 mm (51.8%) (Fig. 3). At Stn 2 (Palawan Is.) the surface water temperature and salinity were 29.2°C and 27.5, respectively. Two species of rhizostomes, L. robustus and Acromitus maculosus Light (Fig. 2B) were recorded. Symbionts were found only on A. maculosus. An individual of L. robustus was collected on the previous day by local fishermen and kept in a meshed plastic bag at sea but any symbionts may have escaped. The measurements of five individuals of A. maculosus and prevalence and intensity of symbionts are shown in Table 2. Seven individuals of A. maculosus were collected, ranging from 4.5–16 cm in umbrella diameter and 132–532 g in 6 7 Umbrella diameter (cm) Wet weight (g) 16 532 16 527 13 332 13 327 11 317 11 317 4.5 132 Symbionts (number of indiv.; body length in mm) Alepes djedaba (n=2; 12.6, 16.5) Carangoides equula (n=2; 18.3, 20.5) None None Carangoides equula (n=1; 19.0) None None wet weight. Among them only three (Nos 1,2,5) were hosts to juveniles of A. djedaba and Carangoides equula (Temminck & Schlegel) (prevalence=42.9%). The mean intensity was much lower in A. maculosus (1.7) than in L. robustus at Stn 1 (49.4). The range of the body length of A. djedaba juveniles fell within the values reported at Stn 1. Juveniles of three taxonomic groups of fish (Carangidae, Gadidae, Centrolophidae) are known to associate with large jellyfish for school formation, predation avoidance and food collection (Dahl 1961, Mansueti 1963, Thiel 1970, 1978, Brodeur 1998, Arai 1997, Purcell & Arai 2001, Masuda et al. 2008, Masuda 2009). Mansueti (1963) listed 23 species of carangids associated with medusae, belonging to the Hydrozoa, Scyphozoa and Cubozoa. Purcell & Arai (2001) added 3 species of carangids (Pseudocaranx dentex (Bloch & Schneider), Trachurus novaezelandiae Richardson, Alepes djedaba) associated with jellyfish to the list of Mansueti (1963). The host jellyfish belong to a variety of taxonomic groups as follows: Hydrozoa (Physalia, Velella), 54 Y. Kondo et al. Table 3. Symbioses between jellyfish and carangids. Data mainly published since Purcell & Arai (2001). Taxonomic group: R, Rhizostomeae; S, Semaeostomeae; C, Cubozoa; H, Hydrozoa. Carangid species Alepes djedaba (Forsskål) Host jellyfish (taxonomic group) Acromitus flagellatus (Haeckel) (R) Acromitus maculosus Light (R) Catostylus townsendi (Mayer) (R) Chrysaoridae sp. (S) Lobonemoides robustus Stiasny (R) Phyllorhiza punctata von lendenfeld (R) Alepes djedaba (as Caranx kalla) Carangoides equula (Temminck & Schlegel) Carangoides malabaricus (Bloch & Schneider) (as Caranx malabaricus) Caranx bartholomaei (Cuvier) Caranx hippos (Linnaeus) Decapterus maruadsi (Temminck & Schlegel) Rhopilema hispidum (Vanhöffen) (R) Versuriga anadyomene (Maas) (R) Cyanea nozakii Kishinouye (S) Acromitus maculosus Light (R) Gnathanodon speciosus (Forsskål) Hemicaranx zelotes Gilbert Porpita porpita (Linnaeus) (as Porpita pacifica) (H) Cyanea nozakii Kishinouye (S) Stomolophus meleagris Agassiz (R) Stomolophus sp. (R) Aurelia aurita s. l. (S) Nemopilema nomurai (Kishinouye) (as Stomolophus nomurai) (R) Chironex yamaguchii Lewis & Bentlage (C) Stomolophus meleagris Agassiz (R) Trachurus japonicus (Temminck & Schlegel) Aequorea coerulescens (Brandt) (H) Aurelia aurita s. l. (S) Trachurus lathami Nichols Trachurus novaezelandiae Richardson Trachurus trachurus (Linnaeus) Chrysaora pacifica (Goette) (as Dactylometra pacifica) (S) Pelagia noctiluca (Forsskål) (as Pelagia panopyra) (S) Nemopilema nomurai (Kishinouye) (R) Morbakka virulenta (Kishinouye) (C) Chrysaora lactea Eschscholtz (S) Desmonema gaudichaudi (Lesson) (S) Aequorea forskalea Péron & Lesueur (H) Cubozoa (Chiropsalmus, Tamoya), Semaeostomeae (Aurelia, Chrysaora, Cyanea, Desmonema, Drymonema, Pelagia), and Rhizostomeae (Acromitus, Catostylus, Cephea, Cotylorhiza, Mastigias, Mastigietta, Netrostoma, Phyllorhiza, Pseudorhiza, Rhizostoma, Rhopilema, Stomolophus, Thysanostoma) (Mansueti 1963, Thiel 1970, 1978, Purcell & Arai 2001, López & Rodriguez 2008, Cevik et al. 2011) (see Table 3 also). Thiel (1970) pointed out that fish juveniles prefer rhizostomes to semaeostomes as hosts. Mansueti (1963) reported that these associations are only temporary, rarely extending for more than a few months, and suggested that these may be classified as commensalism or parasitism. Data mainly published after these reviews and some of our original observations on such associations are compiled in Table 3. In Asian waters, little data exists other Locality Source Gulf of Thailand Palawan Island Gulf of Thailand Gulf of Thailand Gulf of Thailand, Leyte Island Mediterranean, Turkey Gulf of Thailand Java Sea Hong Kong Palawan Island Kondo et al. (unpublished) Present study Kondo et al. (unpublished) Kondo et al. (unpublished) Present study, Kondo et al. (unpublished) Cevik et al. (2011) Ohtsuka et al. (2010) Ohtsuka et al. (2010) Morton (1972) Present study Karwar, India Noble (1963) Hong Kong North Carolina Gulf of Mexico Genkai-nada, Japan Genkai-nada, Japan Morton (1972) Rountree (1983) Gunter (1938) Shojima (1962) Shojima (1962) Okinawa, Japan Gulf of California Seto Inland Sea Seto Inland Sea, Japan Sea Seto Inland Sea Okada et al. (unpublished) López-Martínez & Rodríguez-Romero (2008) Shojima (1962) Shojima (1962), Masuda et al. (2009) Shojima (1962) Seto Inland Sea Shojima (1962) Japan Sea Seto Inland Sea southern Brazil northeastern New Zealand north-west Spain Masuda et al. (2009) Okada et al. (unpublished) Bonaldo et al. (2004) Kingsford et al. (2000) Villegas-Ríos (2009) than some studies on Alepes djedaba (Ohtsuka et al. 2010) and Trachurus japonicus (Temminck & Schlegel) (Masuda 2009, Masuda et al. 2008). Alepes djedaba and T. japonicas have been observed on a range of tropical and subtropical Asian jellyfishes, respectively. Masuda (2009) clearly revealed ontogenetic changes in the interactions between host jellyfish and the development of T. japonicus: the host jellyfish is suggested to play roles as a site for school formation for the early stages (mean standard length 11 mm), as a hiding place for the next stages (19 mm), and finally as a food source for the 38–50 mm stages. Alepes djedaba exhibited habitat segregation on the coasts of the Gulf of Thailand where two hosts, L. robustus and Rhopilema hispidum, sympatrically occurred: small juveniles (mean body length ca. 13 mm) preferred L. robustus, while larger juveniles (20 mm) favoured R. hispidum (Kondo et al., per- Fish-jellyfish associations in Philippines sonal observation). Differences in swimming speed and toxicity between these two hosts might be the cause of this phenomenon, implying ontogenetic changes in the jellyfish-fish interaction as seen between T. japonicus and jellyfish (Masuda et al. 2008, Masuda 2009). Adaptive strategies of these associated carangids to jellyfish toxins should be clarified in the future, as seen in sea anemone-anemonefish interactions (e.g. Dahl 1961, Mebs 1994). It is worth noting that the association of the family Carangidae with jellyfish seems to be confined mainly to the tribe Carangini (see Reed et al. 2002). Megalopa larvae and juveniles of the Christ crab Charybdis feriata (Linnaeus), the former of which was identified based on Fielder et al. (1984), were found on L. robustus collected from Stn 1. The prevalence and intensity were 100% and 2.0, respectively (Table 1). This association was also observed in L. robustus and R. hispidum found in the Gulf of Thailand from July to October (Kondo et al., personal observation), suggesting that it directly settles on jellyfishes and stays on them until the death of the host. Symbiosis of the ophiuroid Ophiocnemis marmorata (Lamarck) on the rhizostome Rhopilema esculentum Kishinouye has been reported from Palawan Island, the Philippines, in March 2004 (Fujita & Namikawa 2006). However, this association was not observed in the present study. Since this ophiuroid is reported to be abundant on L. robustus in the Gulf of Thailand in summer and fall and on the western coast of the Malayan Peninsula in March (Ohtsuka et al. 2010), on L. robustus–O. marmorata association may be found also in the Philippines in spring but not in summer. Acknowledgments We express our sincere thanks to two anonymous reviewers for their constructive comments on the manuscript. The present study was partially supported by grants-in-aid from the Japan Society of Promotion of Science (JSPS), awarded to SO (No. 25304031), to SN (No. 22380108) and to JN (No. 23405031), and by a grant of the Asian Core Program of the JSPS. References Arai MN (1997) A Functional Biology of Scyphozoa. 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