Box Jellyfish Alatina Alata Has a Circumtropical Distribution
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Reference: Biol. Bull. 231: 152–169. (October 2016) © 2016 Marine Biological Laboratory Box Jellyfish Alatina alata Has a Circumtropical Distribution JONATHAN W. LAWLEY1,2,*, CHERYL LEWIS AMES2,3, BASTIAN BENTLAGE2, ANGEL YANAGIHARA4, ROGER GOODWILL5, EHSAN KAYAL2, KIKIANA HURWITZ5, AND ALLEN G. COLLINS2,6 1Departamento de Ecologia e Zoologia, Universidade Federal de Santa Catarina, Floriano´polis, SC 88040-970, Brazil; 2Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20013; 3Biological Sciences Graduate Program, University of Maryland, College Park, Maryland 20742; 4Department of Tropical Medicine, Medical Microbiology and Pharmacology, John A. Burns School of Medicine, University of Hawai’i at Manoa, Honolulu, Hawaii 96822; 5Department of Biology, Brigham Young University–Hawaii, Laie, Hawaii 96792; and 6National Systematics Laboratory of NOAA’s Fisheries Service, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20013 Abstract. Species of the box jellyfish (Cubozoa) genus the swimming medusa stage, and perhaps via dispersal of Alatina are notorious for their sting along the beaches of encysted planulae, which are described here for the first time in several localities of the Atlantic and Pacific. These species Alatina. include Alatina alata on the Caribbean Island of Bonaire (the Netherlands), A. moseri in Hawaii, and A. mordens in Introduction Australia. Most cubozoans inhabit coastal waters, but Ala- tina is unusual in that specimens have also been collected in Life-cycle and life-history characteristics have profound the open ocean at great depths. Alatina is notable in that impacts on the basic biology of marine species, affecting populations form monthly aggregations for spermcast mat- geographic ranges and population dynamics. For instance, ing in conjunction with the lunar cycle. Nominal species are species possessing both benthic and planktonic life stages difficult to differentiate morphologically, and it has been may be expected to display lower dispersal abilities and unclear whether they are distinct or a single species with smaller geographic ranges than species lacking benthic worldwide distribution. Here we report the results of a stages (Gibbons et al., 2010). Many marine species possess population genetic study, using nuclear and mitochondrial pelagic larval stages that are often thought to be most sequence data from four geographical localities. Our anal- responsible for dispersal (Bradbury et al., 2008; Bowen yses revealed a general lack of geographic structure among et al., 2013), but the mobility of all stages in a life cycle are Alatina populations, and slight though significant isolation relevant to determining species ranges (Johannesson, 1988). by distance. These data corroborate morphological and be- Species of the phylum Cnidaria exhibit a wide variety of havioral similarities observed in the geographically dispa- life-cycle plasticity and dispersal capabilities (reviewed in rate localities, and indicate the presence of a single, pan- Fautin, 2002). Jellyfish species (of the cnidarian subphylum tropically distributed species, Alatina alata. While repeated, Medusozoa) typically possess a benthic, sessile stage human-mediated introductions of A. alata could explain the (polyp) that reproduces asexually by budding new polyps or patterns we have observed, it seems more likely that genetic medusae, the latter of which represent the sexually repro- metapopulation cohesion is maintained via dispersal through ductive stage of the textbook medusozoan life cycle. Short- lived, ciliated larval forms known as planulae usually pre- * To whom correspondence should be addressed. E-mail: jonathan. cede the benthic polyp stage. A sometimes overlooked life [email protected] stage present in some medusozoans is the podocyst, a rest- Received 1 March 2016; accepted 15 June 2016. ing stage produced by polyps. Podocysts are essentially 152 This content downloaded from 193.052.039.001 on November 08, 2016 01:06:25 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). DISTRIBUTION OF ALATINA ALATA 153 polyp-derived tissues encysted in a protective layer of peri- zoans are generally not thought to disperse across the open sarc, and are able to withstand extreme salinity changes and ocean (but see Bentlage et al., 2010). In addition, numerous desiccation, sometimes for years (Dumont, 1994; Ikeda Alatina specimens have been collected from surface waters et al., 2011; Carrette et al., 2014). in the open ocean and from depths as great as 2282 m For scyphozoan and cubozan species, the medusa stage is (Lewis et al., 2013). usually the life stage chosen for investigating global pat- Among the eight nominal species of Alatina, A. alata is terns of abundance, distribution, and diversity (Dawson found in the eastern Atlantic and Caribbean, and displays et al., 2014; Lucas et al., 2014), because the polyp stage is what appears to be an identical life history to that of two often difficult to locate in the field. Recent focus has been on Pacific species, A. moseri and A. mordens (Carrette et al., the sudden or periodic increases in biomass of scyphozoans 2014). Bentlage et al. (2010) found that the two Pacific that often have detrimental impacts on human activities; species share mtDNA (16S) haplotypes, and suggested that such increases are commonly known as “jellyfish blooms” they belong to a widespread population from a single spe- (Condon et al., 2013; Dawson et al., 2014). Much debate cies, despite the large geographic distance separating them. exists surrounding the identification of the main factors In this contribution, we integrated molecular analyses and driving jellyfish population dynamics, such as eutrophica- early development and morphological data to clarify the tion, species introductions, and global climate change (for geographic distribution of Alatina from Bonaire, Hawaii, reviews of jellyfish blooms see Graham et al., 2001; Gra- Saipan, and Australia. We show that Alatina does not follow ham and Bayha, 2007; Purcell et al., 2007; Condon et al., the current paradigm, which restricts cnidarians with a ben- 2013; Dawson et al., 2014; Lucas et al., 2014). While tho-pelagic life cycle to relatively narrow geographic ranges “blooms” of scyphozoans have been most heavily studied, (Gibbons et al., 2010). Rather, we propose that they are the population dynamics of box jellyfish––in spite of their members of a single, widespread, possibly circumtropical potentially large public health impacts due to their potent species known as Alatina alata. venoms and their generally coastal, shallow water distribu- tions––remain poorly understood (Yoshimoto and Yanagi- Materials and Methods hara, 2002; Bentlage et al., 2009; Gershwin et al., 2009). Sampling and morphology Periodic or seasonal population dynamics of box jellyfish have long been documented in, and associated with, tropical We sampled Alatina specimens from four localities (Fig. Australia (Barnes, 1966; Fenner, 1998; Fenner and Harri- 1): Alatina alata from Karel’s Pier (Kralendijk, Bonaire, the son, 2000), and an apparent increase in box jellyfish abun- Netherlands); Alatina mordens from Osprey Reef (Coral dance on the Mediterranean Coast of Spain has been re- Sea, Queensland, Australia); Alatina moseri from Waikiki ported in recent years (Bordehore et al., 2011, 2015; (Oahu, Hawaii), and Alatina sp. from Man˜agaha Island Fontanet, 2014). (Saipan, Northern Mariana Islands). Medusae were col- In several tropical to subtropical localities, species of the lected individually by hand or by using dip nets at the sea box jellyfish genus Alatina display monthly nearshore ag- surface from a boat, docks, or the beach. Specimens were gregations (Thomas et al., 2001; Chiaverano et al., 2013; preserved in 5%–8% buffered formalin for morphological Lewis et al., 2013; Carrette et al., 2014). Unlike typical examination; a piece of tentacle was placed in 95% ethanol jellyfish blooms, which consist of sudden, and often unpre- (EtOH) for DNA extractions. Other than two specimens dictable, increases in single-species biomass linked to en- from Saipan, which we tentatively identified as Alatina vironmental conditions (Condon et al., 2013; Dawson et al., grandis (Agassiz & Mayer, 1902) (Bentlage et al., 2010) 2014), Alatina swarms are directly correlated with repro- (see Results section), all specimens had the same general ductive events related to the lunar cycle; mating aggrega- appearance in the field. The detailed morphology of Alatina tions occur 8 to 10 days after the full moon (Alatina moseri samples was examined using the methods outlined in Bent- Mayer 1906 in Hawaii, A. mordens Gershwin 2005 in lage and Lewis (2012) and Lewis et al. (2013). Bell height Australia, and A. alata (Reynaud, 1830) in Bonaire, the and bell width were measured, and the presence of taxon- Netherlands). Though the animals are present in large num- defining morphological characters was confirmed by con- bers (hundreds to thousands of individuals) during these sulting the taxonomic keys provided in Gershwin (2005) monthly reproductive swarms, the whereabouts of Alatina and the recent redescription of Alatina alata (Lewis et al., medusae in the interim is poorly known. Further, juveniles 2013). A list of the museum specimens examined is pro- have been reported only on few occasions (Arneson, 1976; vided in Appendix 1. Photography and videography were Arneson and Cutress, 1976;