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Can Morphology Reliably Distinguish Between the Copepods Calanus Finmarchicus and C. Glacialis, Or Is DNA the Only Way?

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Can Morphology Reliably Distinguish Between the Copepods Calanus Finmarchicus and C. Glacialis, Or Is DNA the Only Way? View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Brage IMR LIMNOLOGY and Limnol. Oceanogr.: Methods 16, 2018, 237–252 VC 2018 The Authors Limnology and Oceanography: Methods published by Wiley OCEANOGRAPHY: METHODS Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lom3.10240 Can morphology reliably distinguish between the copepods Calanus finmarchicus and C. glacialis, or is DNA the only way? Marvin Choquet ,1* Ksenia Kosobokova,2 Sławomir Kwasniewski,3 Maja Hatlebakk,1,4 Anusha K. S. Dhanasiri,1 Webjørn Melle,5 Malin Daase,6 Camilla Svensen,6 Janne E. Søreide,4 Galice Hoarau1 1Faculty of Biosciences and Aquaculture, Nord University, Bodø, Norway 2P.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia 3Institute of Oceanology, Polish Academy of Sciences, Sopot, Poland 4Department of Arctic Biology, The University Centre in Svalbard, Longyearbyen, Norway 5Institute of Marine Research, Bergen, Norway 6Faculty of Biosciences, Fisheries and Economics, Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, Norway Abstract Copepods of the genus Calanus play a key role in marine food webs as consumers of primary producers and as prey for many commercially important marine species. Within the genus, Calanus glacialis and Calanus finmarchi- cus are considered indicator species for Arctic and Atlantic waters, respectively, and changes in their distributions are frequently used as a tool to track climate change effects in the marine ecosystems of the northern hemisphere. Despite the extensive literature available, discrimination between these two species remains challenging. Using genetically identified individuals, we simultaneously checked the morphological characters in use for C. glacialis and C. finmarchicus identification to compare the results of molecular and morphological identification. We stud- ied the prosome length (1); the antennules and the genital somite pigmentation (2); the morphology of the fifth pair of swimming legs and of the mandible (3). Our results show that none of these morphological criteria can reli- ably distinguish between C. glacialis and C. finmarchicus. This has severe implications for our current understand- ing of plankton ecology as a large part of our knowledge of Calanus may be biased due to species misidentification and may subsequently require reinvestigation with the systematic use of molecular tools. Copepods of the genus Calanus are the dominant compo- 2009). Furthermore, they are key drivers of the vertical nent of the zooplankton in the North Atlantic and the Arctic export of material from the upper part of the water column (Jaschnov 1972; Fleminger and Hulsemann 1977; Conover due to the ability of packing organic material into large fast- 1988; Kosobokova et al. 2011; Kosobokova 2012) and are by sinking fecal pellets (Wilson et al. 2008). In marine food far the most studied zooplankton species, with ca. 100 scien- webs, Calanus spp. are essential agents of matter and energy tific publications per year for the last 30 years (Web of Sci- transfer between phyto- and microzooplankton and higher ence). They play a key role in marine food webs as trophic levels. consumers of primary producers and microzooplankton and In the North Atlantic and Arctic regions, the Arctic spe- as prey for many commercially and non-commercially cies Calanus glacialis and the smaller north Atlantic Calanus important species (Gislason and Astthorsson 2002; Beau- finmarchicus account for most of the zooplankton biomass grand et al. 2003; Skjoldal 2004; Varpe et al. 2005; Michaud (Fleminger and Hulsemann 1977; Hassel 1986; Blachowiak- and Taggart 2007; Steen et al. 2007; Falk-Petersen et al. Samolyk 2008; Søreide et al. 2008; Kosobokova and Hirche 2009; Kosobokova 2012). The spatial distribution of these *Correspondence: [email protected] two copepods is linked to the distribution of Arctic and Atlantic waters, respectively, and they are thus considered Additional Supporting Information may be found in the online version indicator species for these water masses (Jaschnov 1966; of this article. Jaschnov 1970; Unstad and Tande 1991; Bonnet and Frid € This is an open access article under the terms of the Creative Commons 2004; Daase and Eiane 2007; Helaouet and Beaugrand 2007; Attribution License, which permits use, distribution and reproduction in Blachowiak-Samolyk 2008; Broms et al. 2009). Recently, C. any medium, provided the original work is properly cited. glacialis and C. finmarchicus have been regarded as beacons 237 Choquet et al. Morphological misidentification in Calanus of climate change (Hays et al. 2005; Wassmann et al. 2015), estimates and for studying distribution patterns, particularly if as changes in their distribution are interpreted as changes in species are considered indicative for specific water masses and Atlantic water circulation and potential “Atlantification” of if changes in their distribution are assumed to have far reach- the Arctic (Wassmann et al. 2006; Falk-Petersen et al. 2007). ing ecosystem impacts. The ecological importance of C. finmarchicus and C. glacia- Both species differ in life strategies such as energy require- lis is unquestionable, but distinguishing between them in ments for reproduction and growth, timing of reproduction, regions of co-occurrence has always been challenging composition of overwintering populations, and seasonal ver- (Unstad and Tande 1991; Hirche et al. 1994). Three main tical migration patterns. These differences reflect adaptations morphological characters have been used, (1) prosome to the environmental conditions in their main areas of dis- length; (2) redness of antennules and genital somite (the tribution (Falk-Petersen et al. 2009), with C. glacialis having two spermathecae); (3) structure of the fifth pair of swim- adapted more flexible life history strategy to deal with the ming legs and the coxal endid of the mandible (in adults). constrains of seasonally ice-covered seas (Daase et al. 2013) Because of convenience, the prosome length measure- and low temperature leading to a larger body size and longer ments (1) have been and remain the most commonly used life span compared to C. finmarchicus. It is crucial to cor- method to separate the two species (see, for example: Unstad rectly identify them to understand their life history adapta- and Tande 1991; Kwasniewski et al. 2003; Arnkværn et al. tions fully, how they have evolved differently in each 2005; Forest et al. 2011; Hirche and Kosobokova 2011; Koso- species and how climate change will be affecting each spe- bokova 2012) although several recent studies have demon- cies’ productivity, population success, distribution and role strated a size-overlap in specific regions (Lindeque et al. in the food web. Using prosome length to discriminate 2006; Parent et al. 2011; Gabrielsen et al. 2012). between species has shown to underestimate smaller sized C. Another trait that has been recently suggested to distin- glacialis (Gabrielsen et al. 2012), which may bias species- guish between C. finmarchicus and C. glacialis is the presence or specific biomass estimates and our understanding of energy absence of red pigmentation on their antennules and, in the allocations in that species. case of adult females, on their genital somite (originally genital In the present study, we use molecular tools to assess the field) (2) (Nielsen et al. 2014). Examination of this character reliability of the morphological characters used to discrimi- requires that individuals are alive, so the samples have to be nate between C. finmarchicus and C. glacialis across a large sorted directly after collection, which is also a challenge. part of their distributional range. The classical, but most complex and time-consuming approach to identify C. finmarchicus and C. glacialis is to examine their morphological characters (3) that have been Material and procedures suggested as diagnostic of the two species. Most common is Samples collection and pre-sorting the examination of the structure of the fifth pair of swim- Zooplankton were sampled in fjords along the Norwegian ming legs in adult females and males (Jaschnov 1955), and coast, in the White Sea, in Svalbard waters and in the Nansen the morphology of the coxal endid of the mandible (gnatho- Basin (Table 1) by vertically towed plankton nets (WP-2/Juday base) (Beklemishev 1959). Examination of both characters types) with mesh sizes between 150 lm and 200 lm. The requires performing a fastidious and specific preparation on whole water column was sampled for most of the locations, each specimen, and is therefore seldom applied during rou- except for the White Sea (100–0 m) and the Svalbard fjords tine zooplankton samples analyses. Although several diagnostic molecular markers have been (20–0 m). The sampling locations were selected to represent a developed for Calanus, from mtDNA RFLP (Lindeque et al. latitudinal gradient from the southernmost (Lurefjord) to the 1999) to nuclear InDels (Smolina et al. 2014), their use in the northernmost (Nansen Basin) areas of co-occurring of C. fin- zooplankton research community has so far remained limited. marchicus and C. glacialis. The White Sea, where only C. glacia- A recent reappraisal of Calanus spp. distribution in the North lis occurrence was reported historically (Jaschnov 1955; Atlantic/Arctic Oceans relying on large scale sampling and Jaschnov 1966) and recently confirmed genetically (Choquet molecular
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