New Ulvaceae (Ulvophyceae, Chlorophyta) from Mesophotic Ecosystems Across the Hawaiian Archipelago1
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J. Phycol. 52, 40–53 (2016) © 2015 Phycological Society of America DOI: 10.1111/jpy.12375 NEW ULVACEAE (ULVOPHYCEAE, CHLOROPHYTA) FROM MESOPHOTIC ECOSYSTEMS ACROSS THE HAWAIIAN ARCHIPELAGO1 Heather L. Spalding,2 Kimberly Y. Conklin, Celia M. Smith Department of Botany, University of Hawai’i at Manoa, 3190 Maile Way, Honolulu, Hawaii 96822, USA Charles J. O’Kelly Friday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, Washington 98250, USA and Alison R. Sherwood Department of Botany, University of Hawai’i at Manoa, 3190 Maile Way, Honolulu, Hawaii 96822, USA Ulvalean algae (Chlorophyta) are most commonly Key index words: Hawai’i; ITS; mesophotic coral described from intertidal and shallow subtidal ecosystem; molecular species concept; rbcL; sea let- marine environments worldwide, but are less well tuce; tufA; Ulva; Ulvales; Umbraulva known from mesophotic environments. Their Abbreviations: BI, Bayesian inference; ITS, Internal morphological simplicity and phenotypic plasticity Transcribed Spacer; ML, maximum likelihood; rbcL, make accurate species determinations difficult, even large subunit ribulose bis-phosphate carboxylase/ at the generic level. Here, we describe the oxygenase; tufA, elongation factor tufA mesophotic Ulvales species composition from 13 locations across 2,300 km of the Hawaiian Archipelago. Twenty-eight representative Ulvales specimens from 64 to 125 m depths were collected Mesophotic coral ecosystems (MCEs) are charac- using technical diving, submersibles, and remotely terized by communities of light-dependent corals, operated vehicles. Morphological and molecular sponges, algae, and other organisms that are typi- characters suggest that mesophotic Ulvales in cally found at depths from 30 to over 150 m in trop- Hawaiian waters form unique communities ical and subtropical regions (Hinderstein et al. comprising four species within the genera Ulva and 2010). Although MCEs often occur close to well-stu- Umbraulva, each with discrete geographic and/or died shallow coral reefs, an understanding of their depth-related distributional patterns. Three biodiversity and connectivity is limited by the techni- genetically distinct taxa are supported by both cal and logistical constraints of accessing these dee- plastid (rbcL and tufA) and nuclear (ITS1) markers, per depths. Despite these challenges, mesophotic and are presented here as new species: Umbraulva surveys to date have suggested that MCEs in the kaloakulau, Ulva ohiohilulu, and Ulva iliohaha.We Main Hawaiian Islands (MHI) contain significant also propose a new Umbraulva species (Umbraulva and diverse cover of macroalgae (Doty et al. 1974, kuaweuweu), which is closely related to subtidal Agegian and Abbott 1985). Non-coralline, foliose records from New Zealand and Australia, but not macroalgae have been found at maximum depths formally described. To our knowledge, these are the ranging from 130 m (Kahng and Kelley 2007, Roo- first marine species descriptions from Hawai‘i ney et al. 2010) to 212 m (Spalding 2012). MCEs in resulting from the collaboration of traditional the Northwestern Hawaiian Islands (NWHI) contain Hawaiian nomenclature specialists, cultural unique macroalgal assembalges (McDermid and practitioners and scientists. The difficulty of finding Abbott 2006), dominated by species such as Microd- reliable diagnostic morphological characters for ictyon umbilicatum (Velley) Zanardini (Huisman et al. these species reflects a common problem worldwide 2007) that form significant habitat for mesophotic of achieving accurate identification of ulvalean taxa reef fish (Kane et al. 2014). using solely morphological criteria. Mesophotic Sea lettuces in the family Ulvaceae (e.g., tubular Ulvales appear to be distinct from shallow-water and blade-like Ulva, Umbraulva, and Ulvaria) are most populations in Hawai‘i, but their degree of similarity commonly described from intertidal and shallow sub- to mesophotic floras in other locations in the Pacific tidal marine or freshwater environments worldwide remains unknown. (Guiry and Guiry 2015). Morphologically, this group of green algae is composed of simple, bistromatic blades (Ulva, Umbraulva), monostromatic, hollow 1Received 18 June 2015. Accepted 28 October 2015. tubes (Ulva, formerly Enteromorpha), or more rarely, 2Author for correspondence: e-mail [email protected]. monostromatic blades (Ulvaria and some expanded Editorial Responsibility: H. Verbruggen (Associate Editor) tubes such as U. compressa). Physiologically, sea 40 HAWAIIAN MESOPHOTIC ULVALES 41 lettuces are typically characterized by rapid growth distribution of mesophotic sea lettuces. Molecular and nutrient acquisition in high light, eutrophic and morphological data were obtained and analyzed environments (Nelson et al. 2008), and would not be from collected ulvalean specimens to elucidate the expected to be significant components of low-light, taxon identities. Our goals were to (i) determine oligotrophic mesophotic environments. Neverthe- the species composition of mesophotic Ulvales in less, sea lettuces have been reported from MCEs and Hawai‘i, (ii) resolve any overlap between shallow other deep-water marine habitats. For example, in and mesophotic populations in Hawai‘i, and (iii) the eastern Gulf of Mexico, Leichter et al. (2008) discern if Hawaiian mesophotic specimens belong recorded a sea lettuce, assigned to Ulva lactuca L., as to species previously characterized from other areas a dominant species at up to 50 m depth, and showed of the world. photographic evidence of ulvoid recruitment at 70 m. In the MHI, Abbott and Huisman (2004) reported sea lettuces dredged from mesophotic MATERIALS AND METHODS depths (up to 200 m); they assigned the specimens Specimen collection and preservation. Ulvales were collected to Ulva expansa (Setchell) Setchell & N.L. Gardner, with the Hawai‘i Undersea Research Laboratory (HURL) sub- U. fasciata Delile, and U. reticulata Forsskal. In her mersibles Pisces IV and Pisces V, HURL ROV RCV-150, and by investigations of MCEs in the MHI, Spalding (2012) technical divers using closed circuit rebreathers from 2004 to 2013 (Table S1 in the Supporting Information). Samples found that ulvalean algae grew epiphytically (i.e., on were collected from 40 to 125 m depths at seven locations in rhodoliths, Halimeda distorta (Yamada) Hillis-Colin- the MHI and from 30 to 85 m depths at six locations in the vaux and H. kanaloana Vroom), attached to hard NWHI (Table S1, Fig. 1). The GPS coordinates for each loca- substrate, or as small single blades attached to pieces tion were reported as the starting point of the submersible of shell in soft sediment areas, and were often in dive. All green thalli visible to the naked eye were targeted high abundance with up to 75% cover in localized for collection. Algae were photographed in situ with the GPS ~ – 2 coordinates, depth, and habitat noted for each specimen. patches ( 1 5m). Individual specimens were perfo- Collected macroalgae were saved in triplicate as herbarium rate or non-perforate, and up to 80 cm in length. presses for voucher specimens, in silica gel for molecular An accurate description of sea lettuce biodiversity analyses, and in a 4% buffered formaldehyde solution in sea- in any habitat is challenging. Since the discovery water. Each specimen was given an “HS” collection number that morphological characters poorly reflect species in the field and an “ARS” accession number in the laboratory diversity among populations of Ulvaceae based on for molecular analyses. Algae were tentatively identified using the systematic keys and taxonomic information provided in comparisons of DNA sequence data with morpho- Abbott and Huisman (2004) and Huisman et al. (2007). logical measurements (Tan et al. 1999, Hayden Vouchers were deposited at the Herbarium Pacificum, B. P. et al. 2003, Hayden and Waaland 2004), numerous Bishop Museum, Honolulu, Hawai‘i (BISH). studies have recorded the extent to which floras Morphological assessment. In the laboratory, the morphology have been mis- or under-reported (Shimada et al. of each specimen was examined, and the thallus shape, size, 2003, 2008, Jiang et al. 2007, Loughnane et al. texture, and color were recorded. Preserved slides were made 2008, Heesch et al. 2009, Hofmann et al. 2010, for microscopic analyses according to Tsuda and Abbott (1985). Morphological and anatomical observations were Kraft et al. 2010, O’Kelly et al. 2010, Mares et al. made using a Zeiss Stereo Discovery V12 microscope (Carl 2011, Duan et al. 2012, Kirkendale et al. 2012, Wolf Zeiss Microscopy, LLC, Thornwood, NY, USA) with a Canon et al. 2012, Guidone et al. 2013, Guoying et al. PowerShot A640 digital camera attachment (Canon U.S.A., 2014). In the Hawaiian Islands, nearly all the names Inc., Lake Success, NY, U.S.A.), and an Olympus BX41 com- used historically for the Ulvaceae (Abbott and Huis- pound light microscope (Olympus America Inc., Center Val- man 2004) have been misapplied (O’Kelly et al. ley, PA, U.S.A.) with an Olympus DP12 digital camera 2010). With the exception of the tropical Hawaiian attachment. Cellular features were examined using wet-pre- served material and herbarium samples that were rehydrated study by O’Kelly et al. (2010), most work to date on for at least 30 min. Digital images of whole-mounted and this family has been done on temperate shallow- cross-sectioned basal, medial, and distal thallus regions were water biotas. In addition, understudied floras have used to examine cell shape, cell size (maximum length and consistently