Could Offspring Predation Offset the Successful Reproduction of the Arctic
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Progress in Oceanography 170 (2019) 107–118 Contents lists available at ScienceDirect Progress in Oceanography journal homepage: www.elsevier.com/locate/pocean Could offspring predation offset the successful reproduction of the arctic copepod Calanus hyperboreus under reduced sea-ice cover conditions? T ⁎ Gérald Darnisa, , Anette Woldb, Stig Falk-Petersenc,d, Martin Graevee, Louis Fortiera a Québec-Océan, Département de biologie, Université Laval, Québec, QC G1V 0A6, Canada b Norwegian Polar Institute, N-9296 Tromsø, Norway c Akvaplan-niva, Fram Centre for Climate and the Environment, N-9296 Tromsø, Norway d Institute of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, University of Tromsø, N-9037 Tromsø, Norway e Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, D-27570 Bremerhaven, Germany ARTICLE INFO ABSTRACT Keywords: Life cycle and reproduction of Calanus hyperboreus were studied during a year of record low ice cover in the Arctic Ocean southeastern Beaufort Sea. Stages CIV, adult females and CV dominated the overwintering population, sug- Beaufort Sea gesting a 2- to 3-year life cycle. Within two spring-summer months in the upper water column females filled their Marine ecology energy reserves before initiating their downward seasonal migration. From February to March, vigorous re- Zooplankton − − − production (20–65 eggs f 1 d 1) delivered numerous eggs (29 000 eggs m 2) at depth and nauplii N1-N3 Calanus hyperboreus − (17 000 ind. m 2) in the water column. However, CI copepodite recruitment in May, coincident with the Lipids phytoplankton bloom, was modest in Amundsen Gulf compared to sites outside the gulf. Consequently, C. hy- perboreus abundance and biomass stagnated throughout summer in Amundsen Gulf. As a mismatch between the first-feeding stages and food was unlikely under the favourable feeding conditions of April-May 2008, predation on the egg and larval stages in late winter presumably limited subsequent recruitment and population growth. Particularly abundant in Amundsen Gulf, the copepods Metridia longa and C. glacialis were likely important consumers of C. hyperboreus eggs and nauplii. With the ongoing climate-driven lengthening of the ice-free season, intensification of top-down control of C. hyperboreus recruitment by thriving populations of mesopelagic omnivores and carnivores like M. longa may counteract the potential benefits of increased primary production over the Arctic shelves margins for this key prey of pelagic fish, seabirds and the bowhead whale. 1. Introduction life-history strategies to adapt to a short and unpredictable season of food supply constrained by the variable timing of ice melt (Falk- Sea-ice variability is a major structuring factor of the Arctic marine Petersen et al., 2009, 2007). When C. hyperboreus has accumulated ecosystem, the climate-driven decline in ice-cover extent is bound to sufficient lipid reserves, it performs a long-range seasonal migration to have serious implications for all levels of the trophic web (Darnis et al., spend the cold and dark overwintering season of up to 10 months in 2012). A 20% increase in phytoplankton annual net primary production diapause at depths several hundred to thousand metres below the sur- over the Arctic Ocean and its marginal seas between 1998 and 2009 face (Ashjian et al., 2003; Dawson, 1978; Hirche, 1997; Vinogradov, was driven by the lengthening of the growth season (+45 days) (Arrigo 1997). This copepod stores lipids, mostly as wax esters, in oil sacs ex- and van Dijken, 2011). Zooplankton of the genus Calanus are expected ceeding 65% of dry mass (Falk-Petersen et al., 2009; Pasternak et al., to respond positively to such rise in pelagic primary production, par- 2001). The wax esters contain high amounts of the long-chained 20:1 ticularly on the continental margins prone to upwelling (Tremblay and 22:1 fatty acids and fatty alcohols of high energy content per unit et al., 2011). mass that are synthesized de novo by Calanus to provide energy for The oceanic large copepod Calanus hyperboreus constitutes the overwintering and reproduction (Sargent and Falk-Petersen, 1988). prime herbivore in the Arctic Ocean and deep margins of its shelf seas Without food, winter reproduction is solely fuelled by the females’ lipid where the species dominates mesozooplankton biomass (Auel and reserves (Hirche and Niehoff, 1996). The adaptive advantage for the Hagen, 2002; Darnis and Fortier, 2012; Kosobokova and Hirche, 2009; offspring, hatched ahead of the phytoplankton bloom and slowly de- Ringuette et al., 2002). This endemic species has developed specialized veloping on endogenous reserves to first-feeding stage Nauplius 3, is ⁎ Corresponding author. E-mail address: [email protected] (G. Darnis). https://doi.org/10.1016/j.pocean.2018.11.004 Received 4 November 2017; Received in revised form 15 November 2018; Accepted 21 November 2018 Available online 22 November 2018 0079-6611/ © 2018 Elsevier Ltd. All rights reserved. G. Darnis et al. Progress in Oceanography 170 (2019) 107–118 that they are ready beforehand to fully exploit the intense but brief toward the Canada Basin (Carmack and Macdonald, 2002; Ingram summer season of biological production (Conover and Huntley, 1991). et al., 2008). Below ∼80 m depth, the Beaufort shelf-break jet trans- Within a few weeks, grazing on microalgal cells enables them to rapidly ports waters of both Pacific and Atlantic origin along the continental grow and recruit to copepodites large enough to overwinter (CIII- slope and into Amundsen Gulf (Carmack and Macdonald, 2002; Pickart, adults). Over its vast geographical range, C. hyperboreus can modulate 2004). Within the gulf, deep circulation is usually weak and highly its generation time between 1 and at least 4 years depending on pre- variable (Ingram et al., 2008). Sea-ice starts to form in October at the vailing environmental conditions (Hirche, 1997). coastal margins of the gulf and consolidation over the entire area is To model the response of this key copepod to changes in the Arctic completed by December (Galley et al., 2008). Ice breakup usually be- sea-ice regime, important traits of its life history need to be better gins in late May-early June (1979–2000 average) and the section of the documented, particularly for the poorly studied winter months when flaw lead polynya at the mouth of the gulf enlarges to form the Cape reproduction occurs. In this study, we provide a detailed description of Bathurst Polynya complex (Barber and Hanesiak, 2004). In Franklin the reproduction cycle and population dynamics of C. hyperboreus based Bay, robust landfast ice coverage usually lasts until June. Remote sen- on a quasi-annual time series during a period of record low ice cover in sing revealed considerable inter-annual variability in the extent and the southeastern Beaufort Sea (October 2007-July 2008) that is com- persistence of open water (Arrigo and van Dijken, 2004). pared with the situation during an average year (2003–2004). We ad- dress the hypothesis presented by Ringuette et al. (2002) that a 2.2. Sampling lengthening of the ice-free season on Arctic shelves will promote po- pulation growth of large herbivore copepods such as C. hyperboreus. Zooplankton samples were collected between 16 October 2007 and 30 July 2008 at 101 stations (Supplementary Table 1) in the south- 2. Material and methods eastern Beaufort Sea during the International Polar Year expedition of the research icebreaker CCGS Amundsen (Fig. 1). Most of the stations 2.1. Study area (88) were sampled in western Amundsen Gulf and the 13 remaining were located on the Mackenzie outer shelf and slope, Darnley and The Amundsen Gulf system, including Franklin and Darnley bays to Franklin bays, and along the northwest coast of Banks Island as far the south and bounded by Banks Island to the north, bridges the north as McClure Strait. Sampling for abundance estimates, egg pro- Beaufort Sea and eastern Mackenzie Shelf with the Canadian Arctic duction experiments and carbon-content measurement on Calanus hy- Archipelago (Fig. 1). Three main water masses lie in the region: the perboreus had also been carried out at 88 stations (Supplementary Polar-Mixed Layer (PML; salinity < 31.6; 0–50 m), the Pacific Halo- Table 2) in the southeastern Beaufort Sea during a previous over- cline (PH; 32.4 < S < 33.1; 50–200 m), and the warmer Atlantic wintering program, the Canadian Arctic Shelf Exchange Study (CASES) Waters (AW; S > 34; > 200 m) (Carmack and Macdonald, 2002). The project from September 2003 to September 2004 (Fortier and Cochran, generally weak surface circulation is influenced by the anticyclonic 2008). The CASES sampling grid covered mainly the Mackenzie shelf Beaufort Gyre that carries the pack ice and surface waters westward and slope and Amundsen Gulf (Fig. 1), whereas winter sampling took Fig. 1. Bathymetry of the southeastern Beaufort Sea with the location of mesozooplankton sampling stations during the CASES and CFL scientific projects in 2003–2004 and 2007–2008, respectively. 108 G. Darnis et al. Progress in Oceanography 170 (2019) 107–118 place at one fixed overwintering site in the landfast ice over Franklin taxonomic analysis were counted in this study as potential predators of Bay, contiguous to the south of Amundsen Gulf, from November 2003 early developmental stages of C. hyperboreus. to May 2004. The Calanus hyperboreus females incubated for egg production ex- Zooplankton sampling procedures in 2007–2008 as well as the periments were carefully blotted with absorbing material and preserved characterization of environmental variables (sea-ice, temperature, individually in cryovials at −20 °C. On land, at least 10 of them were salinity and pelagic chlorophyll a (chl a)) are detailed in Darnis and transferred to pre-weighed tin cups and oven-dried at 60 °C for 48 h Fortier (2012). Wold et al. (2011) and Riedel et al. (2008) provided a before dry weight (DW) measurement on a Sartorius ME5® micro- description of ice-algae sampling and data on ice-algae concentration in balance (precision ± 1 μg).