A multiplex set for microsatellite typing and sexing of the European bee-eater (Merops

2017 
The rapid warming of the West Antarctic Peninsula region has led to reduced sea ice cover and enhanced glacial melt water input. This has potential implications for marine ecosystems, notably phytoplankton growth, biomass, and composition. Fifteen years (1997–2012) of year-round size fractionated chlorophyll a (Chl a), phytoplankton pigment fingerprinting and environmental data were analyzed to identify the relationship between sea ice cover, water column stability and phytoplankton dynamics in northern Marguerite Bay, Antarctica. Over the investigated period, both summer (December–February) and winter biomass declined significantly, 38.5% and 33.3% respectively. Winter phytoplankton biomass was low ( 20 lm) fraction was strongly decreased in the low biomass years, from 92% to 39%, coinciding with a smaller diatom fraction in favor of nanophytoplankton ( 95%) during summers with average-to-high biomass. We advance a conceptual model whereby low winter sea ice cover leads to low phytoplankton biomass and enhanced proportions of nanophytoplankton, when this coincides with reduced stratification during summer. These changes are likely to have a strong effect on the entire Antarctic marine food web, including krill biomass, and distribution. Climate change strongly affects the physical environment in many different regions of our planet. One of the regions most profoundly affected is the West Antarctic Peninsula (WAP). Annual mean air temperatures over the WAP have increased by 2–38C over the past 50 years (Turner et al. 2005), whilst summertime sea surface temperatures increased by more than 18C (Meredith and King 2005). The increase in temperatures in the WAP region is associated with a shortening of the sea ice season and an increase in glacial ice discharge (Depoorter et al. 2013; Rignot et al. 2013). These large-scale changes are strongly affecting the physical and chemical properties of the water column and may thereby affect marine food webs as well (Constable et al. 2014). Pronounced changes in sea ice cover have been observed in the coastal WAP region (Vaughan et al. 2003; Meredith and King 2005; Harangozo 2006). Sea ice duration has decreased by almost 90 days in the 1979–2004 period. This decrease contrasts with the general trend of modestly increasing sea ice extent around Antarctica as a whole, which is driven in particular by major advances in the Ross Sea with much slower rates of change elsewhere (Stammerjohn et al. 2008b; Montes-Hugo et al. 2009). The reduction of sea ice at the WAP is primarily due to a strong trend towards a later autumn advance and a somewhat weaker trend towards an earlier spring retreat (Stammerjohn et al. 2008b). As a *Correspondence: P.D.Rozema@rug.nl Additional Supporting Information may be found in the online version of this article. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 00, 2016, 00–00 VC 2016 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10391 consequence, mean annual sea ice cover in the WAP area has decreased by 40% over a 26-year period (Smith and Stammerjohn 2001). Another effect of warming of the WAP region is the enhanced influx of glacial melt water during summer, due to accelerated glacial retreat (Cook et al. 2005). Marguerite Bay, a major embayment in the central part of the WAP, is surrounded by retreating glaciers and is strongly influenced by the changing sea ice dynamics (Cook et al. 2005; MontesHugo et al. 2009; Meredith et al. 2010). In Marguerite Bay, decreased ice cover has been linked to a deepening of the winter mixed layer (Venables et al. 2013). Occasional strong winds during summer can cause well-described mixing events and can lead to a relatively short-term change in mixed layer depth (MLD). However, recent findings from northern Marguerite Bay have associated decreased winter ice cover to reduced stratification during the following spring and summer (Venables et al. 2013). Strong winds and decreased buoyancy during winter can mix the water column to greater depths during periods of low ice cover. These waters then require more buoyancy to be stabilized to the same level during the subsequent spring and summer, thus potentially leading to persistently weaker stratification. Additionally, the production of less sea ice in winter can lead to smaller volumes of ice being available to melt the following spring and summer, thus reducing the potential buoyancy input to restratify the upper ocean. Seasonal dynamics of phytoplankton are strongly regulated by the timing of sea ice retreat. Austral spring marks the beginning of significant phytoplankton growth after a period of near darkness during winter, in particular when coinciding with water column stabilization caused by warming or freshening due to melt water input from melting sea ice or glaciers. Stabilization of the water column leads to a decreased MLD, thus light conditions become favorable for phytoplankton growth and bloom formation (Sverdrup 1953). Deep mixing due to periods of strong wind or convection can reduce the light available for photosynthesis. Even though the timing of the onset of the phytoplankton bloom may not change with a deeper mixed layer (Venables et al. 2013), it can influence the phytoplankton community through total biomass and/or species composition. In coastal Antarctic waters, phytoplankton spring blooms under stratified conditions typically consist of large (> 20 lm) diatoms that are favored under relatively high irradiance conditions (Arrigo et al. 1999; Clarke et al. 2008; van de Poll et al. 2009; Annett et al. 2010). In well-mixed waters around Antarctica, dominance can shift to the common and widespread haptophyte Phaeocystis antarctica (Arrigo et al. 1999; Alderkamp et al. 2012b). The periods of dominance by nanophytoplankton other than Phaeocystis, mainly cryptophytes, seem to be associated with glacial melt water stratification during summer, decreased nutrient stocks after spring and summer blooms (Buma et al. 1992; Moline et al. 2004; Kozlowski et al. 2011; Mendes et al. 2012), and low irradiance conditions during winter (Clarke et al. 2008). Other phytoplankton groups frequently observed, although often in relative low and constant absolute abundances, are chlorophytes, dinoflagellates and prasinophytes (Kozlowski et al. 2011). A negative trend in microphytoplankton biomass in the northern WAP region, as observed by satellite, was linked previously to a deeper mixed layer and decreased ice cover (Montes-Hugo et al. 2009). This trend is opposite to that observed along the southern most sections of the WAP, where microphytoplankton is increasing due to the opening up of areas previously covered by sea ice. Shifts within the size class distribution of phytoplankton have the potential to alter the Southern Ocean food web drastically (Atkinson et al. 2004). Krill abundance, pivotal within this ecosystem, has shown a strong dependence on sea ice-associated phytoplankton biomass (Saba et al. 2014). Declining phytoplankton stocks, mainly the microphytoplankton that is the preferred food for krill, are causing decreased success in krill recruitment north of Anvers Island (northern WAP; Montes-Hugo et al. 2009; Saba et al. 2014). So far, krill stocks in January-February in the southern section of the WAP appear to be stable (Steinberg et al. 2015). But juvenile krill depends on sea ice algae during winter, and are therefore affected negatively by the disappearance of sea ice (Trivelpiece et al. 2011; Flores et al. 2012; Reiss et al. 2015). As a result, future krill stocks in the southern WAP could be affected. Thus, the already observed changes within the Southern Ocean food web could be propagated to the region of the WAP (Schofield et al. 2010; Constable et al. 2014). In northern Marguerite Bay, phytoplankton biomass estimated by remote sensing has been declining recently in comparison to the 1978–1986 period (Montes-Hugo et al. 2009). A clear example of reduced sea ice cover is the winter of 1998, which led to deeper mixing that persisted through to the subsequent summer (Meredith et al. 2004; Stammerjohn et al. 2008a) and which was associated with a decrease in phytoplankton biomass (Clarke et al. 2008; Venables et al. 2013). While data describing phytoplankton species composition in Marguerite Bay are sparse, available data are comparable to those of the larger WAP region (Garibotti et al. 2005; Kozlowski et al. 2011), showing the dominance of microphytoplankton (> 20 lm; Clarke et al. 2008). Diatoms dominate this size class, however there is large variability with respect to species composition (Garibotti et al. 2003, 2005; Annett et al. 2010; Piquet et al. 2011). No long-term year-round phytoplankton studies are available for the area. Data from the adjacent Palmer Long-Term Ecological Research (LTER) grid spans 20 years, however these are limited to the summer period (Kozlowski et al. 2011). In the present study we analyzed phytoplankton dynamics in northern Marguerite Bay as a function of winter sea ice conditions and summer stratification, obtained from a Rozema et al. Changing phytoplankton at the coastal WAP
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