Arctic Marine Phytobenthos of Northern Baffin Island1
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J. Phycol. 52, 532–549 (2016) © 2016 The Authors. Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution ARCTIC MARINE PHYTOBENTHOS OF NORTHERN BAFFIN ISLAND1 Frithjof C. Kupper€ 2 Scottish Association for Marine Science, Dunbeg, Oban, Argyll PA37 1QA, UK Oceanlab, University of Aberdeen, Main Street, Newburgh AB41 6AA, UK Akira F. Peters BEZHIN ROSKO, 40 rue des pecheurs,^ 29250 Santec, France Dawn M. Shewring Oceanlab, University of Aberdeen, Main Street, Newburgh AB41 6AA, UK Martin D. J. Sayer UK National Facility for Scientific Diving, Scottish Association for Marine Science, Dunbeg, Oban, Argyll PA37 1QA, UK Alexandra Mystikou Oceanlab, University of Aberdeen, Main Street, Newburgh AB41 6AA, UK Hugh Brown, Elaine Azzopardi UK National Facility for Scientific Diving, Scottish Association for Marine Science, Dunbeg, Oban, Argyll PA37 1QA, UK Olivier Dargent Centre International de Valbonne, 190 rue Fred eric Mistral, 06560 Valbonne, France Martina Strittmatter, Debra Brennan Scottish Association for Marine Science, Dunbeg, Oban, Argyll PA37 1QA, UK Aldo O. Asensi 15, rue Lamblardie, F-75012 Paris, France Pieter van West Institute of Medical Sciences, College of Life Sciences and Medicine, Aberdeen Oomycete Laboratory, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, UK and Robert T. Wilce Department of Biology, University of Massachusetts, Amherst, Massachusetts 01003, USA Global climate change is expected to alter the polar documentation of the phytobenthos of the American bioregions faster than any other marine environment. Arctic. Molecular barcoding of isolates raised from This study assesses the biodiversity of seaweeds and incubated substratum samples revealed the presence associated eukaryotic pathogens of an established of 20 species of brown seaweeds, including study site in northern Baffin Island (72° N), providing gametophytes of kelp and of a previously a baseline inventory for future work assessing impacts unsequenced Desmarestia closely related to D. viridis, of the currently ongoing changes in the Arctic marine two species of Pylaiella, the kelp endophyte environment. A total of 33 Phaeophyceae, 24 Laminariocolax aecidioides and 11 previously Rhodophyceae, 2 Chlorophyceae, 12 Ulvophyceae, 1 unsequenced species of the Ectocarpales, Trebouxiophyceae, and 1 Dinophyceae are reported, highlighting the necessity to include molecular based on collections of an expedition to the area in techniques for fully unraveling cryptic algal diversity. 2009, complemented by unpublished records of This study also includes the first records of Robert T. Wilce and the first-ever photographic Eurychasma dicksonii, a eukaryotic pathogen affecting seaweeds, from the American Arctic. Overall, this 1Received 18 November 2015. Accepted 19 February 2016. study provides both the most accurate inventory of 2 Author for correspondence: e-mail [email protected]. seaweed diversity of the northern Baffin Island Editorial Responsibility: C. Lane (Associate Editor) 532 PHYTOBENTHOS OF NORTHERN BAFFIN ISLAND 533 region to date and can be used as an important basis The exploration of Arctic seaweeds was pioneered to understand diversity changes with climate change. by Kjellman (1883). His “The Algae of the Arctic Sea” was the first – and until now only – work taking Key index words: COI; cox3; Desmarestia; germling a holistic view of the Arctic phytobenthos. The his- emergence; macroalgae; molecular barcoding; Phaeo- tory of Arctic seaweed exploration and the issue of phyceae; Pylaiella describing the genuinely “Arctic” features of the sea- Abbreviations: COI, cytochrome c oxidase subunit I; weed biodiversity has been reviewed by Wilce ML, maximum likelihood; NJ, neighbor-joining (2015). Lee (1980) published the first checklist for the region; however, this includes many records from sub-Arctic (boreal) rather than genuinely Arc- In the Arctic and Antarctic bioregions, average tic locations, shifting the focus from a strictly Arctic temperatures are expected to rise by as much as 5°C flora towards a wider boreal, North American flora. until the end of the 21st century, twice more than Nevertheless, knowledge of the American Arctic’s the global mean (IPCC 2014). Recent decades have seaweeds is, at best, sketchy – in particular, in terms seen massive loss of Arctic sea ice, combined with of their biodiversity, ecology, biomass and contribu- rising sea surface temperature in the ice-free areas tions to biogeochemical cycles of the Arctic. There in the summer – accelerating over the last decade is a pressing need for an inventory of seaweeds of to a loss exceeding 2 million km2 with a new mini- the American High Arctic considering that it would mum reached in 2012 (Parkinson and Comiso 2013, constitute an important baseline dataset, which Kwok 2015) which is unprecedented for the last needs to be completed prior to the major environ- 1,450 years at least (Kinnard et al. 2011). The disap- mental changes that have started in recent years. A pearance of Arctic summer sea ice is considered a recent study (Saunders and McDevit 2013) has high- critical tipping element for the global environment lighted the need of complementing morphology- (Lenton et al. 2008) and contrasts the development based identifications of macroalgae by DNA barcod- in the Antarctic (Turner and Overland 2009). The ing and that much of the current data, at least for transition from a high-albedo sea ice surface to an the Canadian Arctic, should be used with caution – open sea, absorbing most of the solar irradiance, is also because purely morphological approaches may also a major factor amplifying warming in the Arctic miss part of the actual diversity. DNA barcoding is (Serreze and Barry 2011). A recent study (Halfar widely considered a suitable approach for identify- et al. 2013) provided a high-resolution, multi-cen- ing marine taxa due to lack of reliable morphologi- tury time series documenting the decline of Arctic cal features for diagnosis (Radulovici et al. 2010). sea ice, using the buildup of coralline red algae as The scope of this study was to conduct a state-of- proxy. This development may have far-reaching the-art identification of the macroalgal flora of the environmental, political, and socio-economic northern Baffin Island region for establishing a spe- impacts for the Arctic and the entire world (Hassol cies checklist, based upon an expedition in summer 2004), including the opening of new, trans-Arctic 2009 (led by FCK) and unpublished materials from shipping routes (Smith and Stephenson 2013) and previous expeditions (led by RTW). A major driver major ecological consequences both in the sea and was the consideration that there is an urgent need on land (Post et al. 2013). Sea ice (with variable for such a survey for establishing an important snow cover) creates a spatially and seasonally very knowledge base to understand diversity changes heterogeneous light environment for the light-lim- with the rapid climate change in the region. Our ited Arctic shallow benthic ecosystems at the under- 2009 expedition aimed to complement collections side of the ice (Glud et al. 2007). of several decades, enhanced by the availability of Seaweeds are major primary producers and consti- DNA barcoding (Saunders and McDevit 2013) and tute significant standing stock in Arctic inshore algal culturing based on the Germling Emergence waters. In Young Sound, a study site in NE Green- Method (Peters et al. 2015). The chosen study site land, comparable to those in northern Baffin Island at Cape Hatt and Ragged Channel had been the site discussed here, macroalgae accounted for 23% of of a major investigation about the effects of an oil the fjord’s primary production, compared to 16% spill in the Arctic marine environment, the Baffin for benthic diatoms and 60% for phytoplankton Island Oil Spill (BIOS) project (Snow et al. 1987) (Glud et al. 2002). At the same site, foliose macroal- which included a preliminary survey of the site’s gae occurred in the depth range of 2–25 m. They dominant seaweed species (Cross et al. 1987). Given contributed markedly to primary production in shal- that our data were generated in the Eclipse Sound/ low water but became insignificant at water depths Ragged Channel area of northern Baffin Island, it is >15 m, while benthic diatoms contributed most to at present not clear to what extent they will be rele- primary production at intermediate water depths vant to the wider Canadian Archipelago also consid- (Krause-Jensen et al. 2007). Here, at water depths ering that studies on macrofauna in the region greater than 30 m, only coralline algae occurred (Cusson et al. 2007, Piepenburg et al. 2011, Gold- (Roberts et al. 2002, Krause-Jensen et al. 2007). smit et al. 2014) have shown considerable diversity even at small spatial scales. 534 FRITHJOF C. KUPPER€ ET AL. Also, the approach applied in this study is unprece- (Muller€ and Ramırez 1994). Where appropriate, algal speci- dented for the Arctic as a whole in that it combines mens were investigated in the field with a small compound 9 9 9 an array of complementary techniques. The isolation microscope with 25 , 100 and 750 magnification. During the dives and where appropriate (e.g., to assess coverage or of algal cultures from sediment and other benthic canopy composition), biomass estimates were made by visual substratum samples is particularly suitable for study- assessment in rough classes (no vegetation, partial cover, or ing the algal flora of remote locations (Muller€ and complete cover, respectively – not shown). Ramırez 1994), complementing the collection of Diving also enabled the collection of sediment and benthic herbarium specimens on-site, documentation by substratum samples in sterile 15 or 50 mL FalconTM tubes. underwater photography and filming and the evalua- Samples were collected between 21 and 30 August 2009 in tion of historic herbarium records, in order to cap- order to cover all types of substratum occurring in the study region.