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water Article Integrated Taxonomy for Halistemma Species from the Northwest Pacific Ocean Nayeon Park 1 , Andrey A. Prudkovsky 2,* and Wonchoel Lee 1,* 1 Department of Life Science, Hanyang University, Seoul 04763, Korea; [email protected] 2 Faculty of Biology, Lomonosov Moscow State University, 119991 Moscow, Russia * Correspondence: [email protected] (A.A.P.); [email protected] (W.L.) Received: 16 October 2020; Accepted: 20 November 2020; Published: 22 November 2020 Abstract: During a survey of the siphonophore community in the Kuroshio Extension, Northwest Pacific Ocean, a new Halistemma Huxley, 1859 was described using integrated molecular and morphological approaches. The Halistemma isabu sp. nov. nectophore is most closely related morphologically to H. striata Totton, 1965 and H. maculatum Pugh and Baxter, 2014. These species can be differentiated by their nectosac shape, thrust block size, ectodermal cell patches and ridge patterns. The new species’ bracts are divided into two distinct types according to the number of teeth. Type A bracts are more closely related to ventral bracts in H. foliacea (Quoy and Gaimard, 1833) while Type B bracts are more similar to H. rubrum (Vogt, 1852). Each type differs, however, from the proximal end shape, distal process and bracteal canal. Both of the new species’ morphological type and phylogenetic position within the genus Halistemma are supported by phylogenetic analysis of concatenated DNA dataset (mtCOI, 16S rRNA and 18S rRNA). Integrated morphological and molecular approaches to the taxonomy of siphonophores showed a clear delimitation of the new species from the congeners. Halistemma isabu sp. nov. is distributed with the congeners H. rubrum, H. cupulifera, H. foliacea and H. striata in the northwestern Pacific Ocean. Keywords: zooplankton; jellyfish; mitochondria; systematics; hydrozoa 1. Introduction Siphonophores, belonging to the class Hydrozoa Owen, 1843, live in oceans and are mostly holoplanktonic organisms [1]. Approximately, 190 species have been described as siphonophores, though there are likely more in the marine environment [2]. Siphonophores have gelatinous bodies and form unique colonies throughout their life [3]. Each individual in a colony has a variety of functions and morphological characteristics [4]. Siphonophorae are traditionally classified into three suborders (Calycophorae Leuckart, 1854; Cystonectae Haeckel, 1887; Physonectae Haeckel, 1888) depending on the presence of a gas bubble float, called a pneumatophore, and medusoids, known as nectophores [1,5,6]. Approximately 65 species with pneumatophores and nectophores are recognized as Physonectae [7]. Physonects’s descriptions are often incomplete because Siphonophores have fragile gelatinous bodies and many research records are based on dissociated specimens, where only a few nectophores or bracts were collected [1,8]. Morphological changes throughout their life cycle, phenotypic plasticity and cryptic species are also responsible for erroneous species diversity estimations. Molecular methods can be used for species identification, reconstructing life cycles, and clarifying phylogeny [2,8–13]. Molecular data show that Cystonectae and Calycophorae are monophyletic taxa while Physonectae is polyphyletic [2,8]. Some families, such as Apolemiidae Huxley, 1859 and Pyrostephidae Moser, 1925, are not included in the clade unifying physonects and Calycophorae. Most physonects, however, can be combined into the monophyletic clade Euphysonectae. This includes Agalmatidae, Physophoridae Water 2020, 12, 3283; doi:10.3390/w12113283 www.mdpi.com/journal/water Water 2020, 12, x FOR PEER REVIEW 2 of 21 includes Agalmatidae, Physophoridae Eschscholtz, 1829, Forskaliidae Haeckel, 1888 and other Waterfamilies2020 ,[2].12, 3283General Physonectae systematics and phylogenetic affinities of some genera are under2 of 18 debate. Eschscholtz,Agalmatidae 1829, Forskaliidaeis the most Haeckel,specious 1888 family and within otherfamilies the Physonectae. [2]. General The Physonectae family’s diversity systematics is andlimited phylogenetic to five genera affinities (Agalmatidae of some genera sensu arestricto under) including debate. short-stem (Athorybia Eschscholtz, 1829 and MelophysaAgalmatidae Haeckel, is the 1888) most and specious long-stem family (Agalma within Eschscholtz, the Physonectae. 1825, Halistemma The family’s Huxley, diversity 1859, is limitedNanomia to A. five Agassiz, genera 1865) (Agalmatidae genera [6,7,14].sensu stricto The )short-stem including short-stemgenus Athorybia (Athorybia, withEschscholtz, no nectophores, 1829 was and MelophysapreviouslyHaeckel, classified 1888) outside and long-stemof the Agalmatidae. (Agalma Eschscholtz, However, 1825, molecularHalistemma data Huxley,show they 1859, areNanomia likely A.neotenic Agassiz, relatives 1865) genera of the Agalma [6,7,14]. species The short-stem [2,8,14]. Melophysa genus Athorybia melo (Quoy, with and no nectophores, Gaimard, 1827) was has previously a spiral classifiedsiphosome outside and tricornuate of the Agalmatidae. tentilla and However, is related molecular to Athorybia datashow and Agalma they are species likely neotenic [14]. Long-stem relatives ofagalmatids the Agalma (Agalmaspecies, Halistemma [2,8,14]. Melophysa, Nanomia melo) include(Quoy monoecious and Gaimard, species 1827) with has dorsal a spiral nectosoma siphosome and and a tricornuatedescending tentillamantle andcanal is in related its nectophores to Athorybia [6,7,14].and Agalma The agalmatidspecies [14 genera]. Long-stem are delimited agalmatids based (Agalma on the, Halistemmanectophores’, Nanomia shape, ridge) include pattern, monoecious and tentilla species type. with Nevertheless, dorsal nectosoma these morphologic and a descending differences mantle and canaltaxonomic in its nectophoresboundaries [were6,7,14 only]. The generalize agalmatidd generain a short are delimitedMapstone based (2015) on [7] the review. nectophores’ Halistemma shape,, ridgewhich pattern, we address and tentillain this type.paper, Nevertheless, is a genus establis these morphologiched by Huxley di ff(1859)erences [15]. and It taxonomichas a long boundariestaxonomic werehistory only which generalized Pugh and in Baxter a short (2014) Mapstone [16] recently (2015) [7 ]reviewed. review. Halistemma A total of ,six which Halistemma we address species in thisare paper,known. is a genus established by Huxley (1859) [15]. It has a long taxonomic history which Pugh and BaxterIn (2014)this study, [16] recently we describe reviewed. a new A Halistemma total of six speciesHalistemma foundspecies in the areNorthwest known. Pacific Ocean. Our descriptionIn this uses study, morphological we describe characteristics a new Halistemma and aspecies three-gene found molecular in the Northwestapproach. Pacific Ocean. Our description uses morphological characteristics and a three-gene molecular approach. 2. Materials and Methods 2. Materials and Methods 2.1. Sample Collections 2.1. Sample Collections Plankton samples were collected in October 2019 during a R/V ISABU cruise in the Kuroshio ExtensionPlankton (Figure samples 1). We were used collected a Multiple in OctoberOpening/Closing 2019 during Net a and R/V Environmental ISABU cruise inSensing the Kuroshio System Extension(MOCNESS, (Figure 1 × 11 m²,). We mesh used size: a Multiple 200 µm) Opening towed between/Closing 200 Net m and and Environmental the surface. Immediately Sensing System after (MOCNESS,towing, we 1split1 mplankton2, mesh size:samples 200 µ m)into towed 1/2 aliquots between 200using m anda Folsom the surface. plankton Immediately splitter. afterFor × towing,morphological we split observation, plankton samples one aliquot into 1/ 2was aliquots fixed using in neutralized a Folsom plankton5% formalin splitter. solution For morphological and stored at observation,room temperature. one aliquot For wasfuture fixed molecular in neutralized analysis, 5% we formalin fixed solutionthe other and aliquot stored in at 99.9% room temperature.ethanol and Forstored future at 4 molecular °C. All material analysis, was we fixeddeposited the other at the aliquot National in 99.9% Institute ethanol of andBiological stored atResources 4 ◦C. All material(NIBR), wasKorea’s deposited invertebrate at the Nationalcollection. Institute of Biological Resources (NIBR), Korea’s invertebrate collection. Figure 1.1. Map of sampling stations. (QGIS, Version: 3.6.0). Water 2020, 12, 3283 3 of 18 2.2. Morphological Analysis For morphological observation, specimens were sorted from 5% neutralized formalin plankton samples using a Live Insect Forceps (26029-10, Fine Science Tools Inc., Foster City, CA, USA) and a stereomicroscope (Olympus SZX7, Tokyo, Japan). We placed sorted specimens in 20 mL glass vials with the formalin solution at room temperature. We observed specimens on a Petri dish (Ø: 5 cm) filled with 5% neutralized formalin solution under the stereomicroscope. We identified all specimens using descriptions and illustrations from Kirkpatrick and Pugh (1984) [17], Mapstone (2009) [18], Totton (1954) [19], Totton and Bargmann (1965) [1] and Pugh and Baxter (2014) [16] and used Pugh and Baxter (2014) [16] terminology. Digital photographs of specimens were taken using a digital camera (Olympus PEN Lite E-PL3, Tokyo, Japan) connected to the stereomicroscope with side lights on the dark field. We took the digital photographs at various focal points and performed multi-focus stacking using Helicon Focus 7 software (Version: 7.5.1). We cropped the photographed objects and moved them to a
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  • The Lower Bathyal and Abyssal Seafloor Fauna of Eastern Australia T

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    O’Hara et al. Marine Biodiversity Records (2020) 13:11 https://doi.org/10.1186/s41200-020-00194-1 RESEARCH Open Access The lower bathyal and abyssal seafloor fauna of eastern Australia T. D. O’Hara1* , A. Williams2, S. T. Ahyong3, P. Alderslade2, T. Alvestad4, D. Bray1, I. Burghardt3, N. Budaeva4, F. Criscione3, A. L. Crowther5, M. Ekins6, M. Eléaume7, C. A. Farrelly1, J. K. Finn1, M. N. Georgieva8, A. Graham9, M. Gomon1, K. Gowlett-Holmes2, L. M. Gunton3, A. Hallan3, A. M. Hosie10, P. Hutchings3,11, H. Kise12, F. Köhler3, J. A. Konsgrud4, E. Kupriyanova3,11,C.C.Lu1, M. Mackenzie1, C. Mah13, H. MacIntosh1, K. L. Merrin1, A. Miskelly3, M. L. Mitchell1, K. Moore14, A. Murray3,P.M.O’Loughlin1, H. Paxton3,11, J. J. Pogonoski9, D. Staples1, J. E. Watson1, R. S. Wilson1, J. Zhang3,15 and N. J. Bax2,16 Abstract Background: Our knowledge of the benthic fauna at lower bathyal to abyssal (LBA, > 2000 m) depths off Eastern Australia was very limited with only a few samples having been collected from these habitats over the last 150 years. In May–June 2017, the IN2017_V03 expedition of the RV Investigator sampled LBA benthic communities along the lower slope and abyss of Australia’s eastern margin from off mid-Tasmania (42°S) to the Coral Sea (23°S), with particular emphasis on describing and analysing patterns of biodiversity that occur within a newly declared network of offshore marine parks. Methods: The study design was to deploy a 4 m (metal) beam trawl and Brenke sled to collect samples on soft sediment substrata at the target seafloor depths of 2500 and 4000 m at every 1.5 degrees of latitude along the western boundary of the Tasman Sea from 42° to 23°S, traversing seven Australian Marine Parks.
  • Deep‐Sea Coral Taxa in the U.S. Gulf of Mexico: Depth and Geographical Distribution

    Deep‐Sea Coral Taxa in the U.S. Gulf of Mexico: Depth and Geographical Distribution

    Deep‐Sea Coral Taxa in the U.S. Gulf of Mexico: Depth and Geographical Distribution by Peter J. Etnoyer1 and Stephen D. Cairns2 1. NOAA Center for Coastal Monitoring and Assessment, National Centers for Coastal Ocean Science, Charleston, SC 2. National Museum of Natural History, Smithsonian Institution, Washington, DC This annex to the U.S. Gulf of Mexico chapter in “The State of Deep‐Sea Coral Ecosystems of the United States” provides a list of deep‐sea coral taxa in the Phylum Cnidaria, Classes Anthozoa and Hydrozoa, known to occur in the waters of the Gulf of Mexico (Figure 1). Deep‐sea corals are defined as azooxanthellate, heterotrophic coral species occurring in waters 50 m deep or more. Details are provided on the vertical and geographic extent of each species (Table 1). This list is adapted from species lists presented in ʺBiodiversity of the Gulf of Mexicoʺ (Felder & Camp 2009), which inventoried species found throughout the entire Gulf of Mexico including areas outside U.S. waters. Taxonomic names are generally those currently accepted in the World Register of Marine Species (WoRMS), and are arranged by order, and alphabetically within order by suborder (if applicable), family, genus, and species. Data sources (references) listed are those principally used to establish geographic and depth distribution. Only those species found within the U.S. Gulf of Mexico Exclusive Economic Zone are presented here. Information from recent studies that have expanded the known range of species into the U.S. Gulf of Mexico have been included. The total number of species of deep‐sea corals documented for the U.S.
  • The Histology of Nanomia Bijuga (Hydrozoa: Siphonophora) SAMUEL H

    The Histology of Nanomia Bijuga (Hydrozoa: Siphonophora) SAMUEL H

    RESEARCH ARTICLE The Histology of Nanomia bijuga (Hydrozoa: Siphonophora) SAMUEL H. CHURCH*, STEFAN SIEBERT, PATHIKRIT BHATTACHARYYA, AND CASEY W. DUNN Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island ABSTRACT The siphonophore Nanomia bijuga is a pelagic hydrozoan (Cnidaria) with complex morphological organization. Each siphonophore is made up of many asexually produced, genetically identical zooids that are functionally specialized and morphologically distinct. These zooids predominantly arise by budding in two growth zones, and are arranged in precise patterns. This study describes the cellular anatomy of several zooid types, the stem, and the gas-filled float, called the pneumatophore. The distribution of cellular morphologies across zooid types enhances our understanding of zooid function. The unique absorptive cells in the palpon, for example, indicate specialized intracellular digestive processing in this zooid type. Though cnidarians are usually thought of as mono-epithelial, we characterize at least two cellular populations in this species which are not connected to a basement membrane. This work provides a greater understanding of epithelial diversity within the cnidarians, and will be a foundation for future studies on N. bijuga, including functional assays and gene expression analyses. J. Exp. Zool. (Mol. Dev. Evol.) 324B:435– 449, 2015. © 2015 The Authors. Journal of Experimental Zoology Part B: Molecular and J. Exp. Zool. Developmental Evolution Published by Wiley Periodicals, Inc. (Mol. Dev. Evol.) 324B:435–449, How to cite this article: Church SH, Siebert S, Bhattacharyya P, Dunn CW. 2015. The histology of 2015 Nanomia bijuga (Hydrozoa: Siphonophora). J. Exp. Zool. (Mol. Dev. Evol.) 324B:435–449. Siphonophores are pelagic hydrozoans (Cnidaria) with a highly and defense (Dunn and Wagner, 2006; Totton, '65).