Impact of climate change on Antarctic krill

Antarctic krill Euphausia superba (hereafter ‘krill’) occur in regions undergoing rapid environmental change, particularly loss of winter sea ice. During recent years, harvesting of krill has in creased, possibly enhancing stress on krill and Antarctic ecosystems. Here we review the overall impact of climate change on krill and Antarctic ecosystems, discuss implications for an ecosystem-based fisheries management approach and identify critical knowledge gaps. Sea ice decline, ocean warming and other environmental stressors act in concert to modify the abundance, distribution and life cycle of krill. Although some of these changes can have positive effects on krill, their cumulative impact is most likely negative. Recruitment, driven largely by the winter survival of larval krill, is probably the population parameter most susceptible to climate change. Predicting changes to krill populations is urgent, because they will seriously impact Antarctic eco systems. Such predictions, however, are complicated by an intense inter-annual variability in recruitment success and krill abundance. To improve the responsiveness of the ecosystem-based management ap proach adopted by the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR), critical knowledge gaps need to be filled. In addition to a better understanding of the factors influencing recruitment, management will require a better un derstanding of the resilience and the genetic plasticity of krill life stages, and a quantitative understanding of under-ice and benthic habitat use. Current precautionary management measures of CCAMLR should be maintained until a better understanding of these processes has been achieved. Antarctic krill Euphausia superba under a piece of sea ice in an aquarium. Photo: Jan Andries van Franeker OPEN ACCESS Mar Ecol Prog Ser 458: 1–19, 2012 (Gille 2002) and ocean acidification (Orr et al. 2005). Rates of warming and sea ice loss are fastest in the southwest (SW) Atlantic sector, thus affecting key nursery habitats and feeding grounds of krill (Fig. 1A). These and other environmental changes are considered manifestations of the post-19th century anthropogenic carbon dioxide (CO2) surplus (IPCC 2007), here summarised in the term ‘climate change’. In addition, the commercial catch of krill has increased, in part as a consequence of new, efficient fishing techniques and the development of new products and markets between 2008 and the present (Nicol et al. 2012). Recently, concern was expressed by several scientists about the future sustainability of krill harvesting under the cumulative pressure of climate change and fisheries (Jacquet et al. 2010, Schiermeier 2010). Such concern has been initiated by reports of a 2 Fig. 1. (A) Circumpolar distribution of post-larval Antarctic krill (re-drawn from Atkinson et al. 2008). The plot shows arithmetic mean krill densities (ind. m−2) within each 5° latitude by 10° longitude grid cell derived from KRILLBASE. (B) CCAMLR convention area, with FAO statistical subareas 48.1 to 88.3. (C) Trends of change in ice season duration between 1979 and 2006 in d yr−1 (provided by E. Maksym, British Antarctic Survey). Trends were calculated from satellite-based daily sea ice concentration data provided by the National Snow and Ice Data Center (University of Colorado at Boulder, http://nsidc.org), using the methodology described by Stammerjohn et al. (2008). (D) Trend of midwater ocean temperature change during the period 1930 to 2000 in °C yr−1 (modified from Gille 2002, with permission). The analysis was based on archived shipboard measurements (1930−1990) and Autonomous Lagrangian Circulation Explorer (ALACE) float data (1990−2000) from 700 to 1100 m depth (© American Association for the Advancement of Science 2002) Flores et al.: Krill and climate change decrease in krill abundance in the SW Atlantic sector, paralleled by a decline in winter sea ice coverage during the last quarter of the 20th century (Atkinson et al. 2004), and declines in a number of krill-dependent predators (e.g. Trivelpiece et al. 2011). Furthermore, evidence is increasing that krill fulfil complex roles in ecosystem feedback loops through grazing and nutrient recycling (Tovar-Sanchez et al. 2007, Whitehouse et al. 2009, Nicol et al. 2010, Schmidt et al. 2012). Because Antarctic krill populations and marine eco systems are responding to climate change, resource and conservation management in the Southern Ocean will need to become much more adaptive. Conservation of Southern Ocean ecosystems falls under the responsibility of the Convention for the Conservation of Antarctic Marine Living Resources (CCAMLR), which was established in 1982 (Fig. 1B). As part of the Antarctic Treaty system, CCAMLR consists of 24 member countries plus the European Union. The aim of the Convention is to conserve Antarctic marine life and, at the same time, allow for the rational use of marine living resources (CCAMLR 1982). A multi-national group of experts on krill and Antarctic environmental sciences met at a scientific workshop on the island Texel (The Netherlands) from 11 to 15 April 2011 to produce an up-to-date evaluation of present scientific knowledge on the impacts of climate change and increasing human exploitation on krill. Here we present the conclusions reached during this workshop, focusing on major agents of climate change, such as sea ice loss, ocean warming and ocean acidification, as well as recent developments in the krill fishery. The main objective of this review was to highlight the likely impact of important drivers of climate change on krill and Ant arctic ecosystems, to discuss potential implications for CCAMLR’s ecosystem-based management ap proach and to identify resulting future research priorities. PAST AND FUTURE CHANGES IN THE ENVIRONMENT AND THEIR IMPACT ON KRILL Changing sea ice habitats There has been considerable regional variability in the trend of Antarctic sea ice extent over the past decades. In the western Antarctic Peninsula region, average monthly sea ice extent has been declining at a rate of almost 7% decade−1 between 1979 and 2008 (Turner et al. 2009b). This trend has been counterbalanced over the past 3 decades by an increase in sea ice extent in other regions, particularly an almost 5% decade−1 increase in the Ross Sea, leading to an overall increase in sea ice extent on the order of 1% (Stammerjohn et al. 2008, Turner et al. 2009b). For the period 1979–1998, Zwally et al. (2002) estimated an overall increase in sea ice extent by about 10 950 km2 yr−1, with a regional variability between −13 20 km2 yr−1 in the Bellingshausen and Ammund sen Seas, and +17 600 km2 yr−1 in the Ross Sea. This growth, however, has so far not compensated for a decline of the average sea ice coverage between 1973 and 1977, which accounted for ~2 × 106 km2 (Cavalieri et al. 2003, Parkinson 2004). Re con struct ions of the position of the ice edge in the pre-satellite era give strong evidence that the overall areal sea ice coverage in the Southern Ocean declined considerably during the second half of the 20th century (Turner et al. 2009a). For example, de la Mare (1997) demonstrated an abrupt 25% decline (~5.7 × 106 km2) in Antarctic summer sea ice extent between the 1950s and 1970s based on whaling records. More important ecologically than the areal extent of ice coverage may be its duration and thickness distribution. Be tween 1979 and 2004, the sea ice season in the western Antarctic Peninsula region and southern Bellingshausen Sea has shortened by 85 d, i.e. at a rate of 37.7 d decade−1 (our Fig. 1C; Parkinson 2004, Stammerjohn et al. 2008). This trend is consistent with a declining areal ice coverage and increasing temperatures in these regions (Turner et al. 2009b). In other regions, particularly the Ross Sea, the sea ice season has been lengthening at a rate of 23.1 d decade−1 be tween 1979 and 2004, associated with the ob served overall increase of areal ice coverage in this region (Parkinson 2004, Stammerjohn et al. 2008). Only recently, reliable circumpolar ice thickness distributions have been generated for the Antarctic, averaged over the period 1981–2005 (Worby et al. 2008). These data show that the western Weddell Sea (between 45 and 60° W), an area of high krill abundance and key target region for fishing, has the highest annual mean ice thickness, but also the highest variability in ice thickness compared to other regions of the Antarctic sea ice zone. Long-term trends in ice thickness of the Southern Ocean, however, are not yet available. Warning signs come from the Arc tic Ocean, where average ice thickness may have decreased by up to 42% between the periods of 1958− 1976 and 1993−1997, concomitant with a signi ficant decline of the areal extent of sea ice (Roth rock et al. 1999). The regionally divergent trends in the 3 Mar Ecol Prog Ser 458: 1–19, 2012 duration and extent of Antarctic sea ice coverage may temporarily have masked a negative circumpolar trend. In the course of the 21st century, air temperatures in the Antarctic region are predicted to further increase (IPCC 2007). As climate warming continues, coupled ice−ocean−atmosphere models predict a 33% decrease in the areal extent of Antarctic winter sea ice by the end of this century (Bracegirdle et al. 2008). Krill are associated with sea ice at all stages of their life cycle (Marschall 1988, Hamner et al. 1989, Daly 1990, Siegel et al. 1990, Flores et al. 2012). Probably the most striking evidence of this association, integrating a complexity of ice−krill interactions, is the known positive relationship of krill abundance with winter sea ice extent (Atkinson et al. 2004). Larval krill depend on sea ice biota as a food source, because they have no capacity to store energy from food taken up during autumn phytoplankton blooms (Meyer et al. 2002, 2009, Daly 2004). When the duration of the sea ice season changes, this dependency is particularly critical, because the timing of ice formation at a specific latitude significantly determines food availability in winter sea ice (Quetin et al. 2007). Sea ice also offers a structured habitat with pressure ridges and rafted ice floes, which can retain larvae in favourable conditions, transport developing juvenile krill and protect them from predators (Meyer et al. 2009). For example, the timing of break-off and transport of sea ice can be decisive to the recruitment of juvenile krill from the Scotia Sea to the South Georgia region (Fach et al. 2006, Fach & Klinck 2006, Thorpe et al. 2007). Important spawning grounds are located in areas of fastest sea ice loss, such as the Bellingshausen, Amundsen and Southern Scotia Seas (Hofmann & Husrevoglu 2003, Schmidt et al. 2012). A southward redistribution of spawning grounds is limited by the Antarctic shelf, because the development of krill eggs towards the first feeding stage involves sinking to 700 to 1000 m water depth (Marr 1962, Hempel 1979, Quetin & Ross 1984). Declining sea ice may thus impact krill recruitment due to multiple and probably cumulative effects. These include the role of sea ice as a shelter, as a feeding ground, and as a transport platform for larvae. Post-larval krill survive winter by using a variety of strategies, including reduced metabolism, shrinkage and lipid storage, as well as utilisation of food sources other than phytoplankton, such as zooplankton, ice algae and seabed detritus (e.g. Kawa guchi et al. 1986, Meyer et al. 2010, Schmidt et al. 2011). In winter, due to metabolic depression, they feed opportunistically at low rates under sea ice and/or at the benthos. This energy input, even at low rates, complements reduced metabolism and lipid utilisation and is a requirement for successfully reproducing in the subsequent spring (Meyer et al. 2010, Meyer 2011). Juvenile krill do not have the storage capacity and metabolic plasticity of their adult congeners, and are thought to depend more on sea ice biota (Atkinson et al. 2002). In midwinter, the underside of sea ice was found to attract both juvenile and adult krill (Flores et al. 2012), while adults were also observed at depths >150 m (Lawson et al. 2008), demonstrating the highly variable nature of krill distribution during this season. This also means that changes in the structural composition and extent of sea ice will disproportionally impact larvae and juveniles. In older krill, winter survival may be enhanced by a longer open water season, allowing them to build up more energy reserves feeding on phytoplankton. Ice algae are most productive during spring and early summer. Krill can take advantage of this productivity and concentrate under sea ice, along with a variety of other species (Brierley et al. 2002, Flores et al. 2011, 2012). As melting proceeds, sea ice releases algae and nutrients into the water, stimulating in tense phytoplankton blooms in the marginal ice zone (Hempel 1985). It is these sea ice-induced blooms that play a key role in the summer feeding of krill and have been suggested to sustain large populations of top predators (Hempel 1985, Perissinotto et al. 1997). Also deep within ice-covered areas, a large portion of krill populations can aggregate in the ice−water interface layer, supporting a food chain of major importance, as shown by year-round high abundances of krill and top predators deep in the pack-ice (van Franeker et al. 1997, Brandt et al. 2011, Flores et al. 2012). The total area of ice algae grazing grounds and ice edge blooms is likely to shrink, and the distribution of these areas will move southwards. A southward shift of the winter sea ice zone will reduce ice algal productivity due to lower light availability at higher latitudes. In summary, sea ice has multiple benefits for krill, and reductions in duration, extent and geographical distribution of this winter habitat will likely have additive cumulative negative effects, all impacting the reproductive success and survival of krill, with possible cascading effects on food web structure. If declines in the spatial and seasonal coverage of sea ice remain concentrated in the main population centre of krill and key recruitment areas as predicted, sea ice retreat may become a dominant driver of krill decline. 4 Flores et al.: Krill and climate change