Shortening winter ice-cover duration in lakes highlights an urgent need for research focused on under-ice ecosystem dynamics and their contributions to whole-ecosystem processes. Low temperature, reduced light and consequent changes in autotrophic and heterotrophic resources alter the diet for long-lived consumers, with consequences on their metabolism in winter. We show in a survival experiment that the copepod Leptodiaptomus minutus in a boreal lake does not survive five months under the ice without food. We then report seasonal changes in phytoplankton, terrestrial and bacterial fatty acid (FA) biomarkers in seston and in four zooplankton species for an entire year. Phytoplankton FA were highly available in seston (2.6 µg L−1) throughout the first month under the ice. Copepods accumulated them in high quantities (44.8 µg mg dry weight−1), building lipid reserves that comprised up to 76% of body mass. Terrestrial and bacterial FA were accumulated only in low quantities (<2.5 µg mg dry weight−1). The results highlight the importance of algal FA reserve accumulation for winter survival as a key ecological process in the annual life cycle of the freshwater plankton community with likely consequences to the overall annual production of aquatic FA for higher trophic levels and ultimately for human consumption.
Accumulation of carotenoid pigments in copepods has often been described as a plastic adaptation providing photoprotection against ultraviolet radiation (UVR). However, reports of seasonal carotenoid maxima in winter, when UVR is low, challenge the proposed driving role of UVR. Therefore, we here evaluate the mechanistic connection between UVR and the seasonal pattern of copepod carotenoid pigmentation. We assessed the carotenoids, fatty acid content and reproduction of Leptodiaptomus minutus along with UVR exposure, water temperature, phytoplankton pigments, and fish predation in a boreal lake during 18 months covering two winter seasons. The predominant carotenoid astaxanthin occurred in free form as well as esterified with fatty acids. Mono-and diesters accounted for 62-93% of total astaxanthin and varied seasonally in close correlation with fatty acids. The seasonal variability in total astaxanthin content of the copepods was characterized by net accumulation in late fall of up to 0.034 lg (mg dry mass) 21 d 21, which led to the mid-winter maximum of 3.89 6 0.31 lg mg 21 . The two periods of net loss (20.018 lg mg 21 d 21 and 20.021 lg mg 21 d 21) coincided with peaks of egg production in spring and summer leading to minimum astaxanthin content (0.86 6 0.03 lg mg 21 ) in fall. This period was also characterized by the highest predation pressure by young-of-the-year fish. The results suggest that accumulation of astaxanthin in copepods is strongly related to lipid metabolism but not to UVR-photoprotection, and that seasonal changes of fatty acids and carotenoids are related to the reproduction cycle.The red pigmentation of many zooplankton has long puzzled biologists, and various hypotheses have been offered to explain the phenomenon via proximate and ultimate causes (e.g., Brehm 1938). The red coloration of copepods is due to carotenoids, a large family of lipid-soluble pigments that are synthesized only in primary producers but may be either accumulated by zooplankton or biologically converted to other carotenoids, notably astaxanthin, which is the primary carotenoid among crustaceans (Matsuno 2001;Andersson et al. 2003;Rhodes 2006). Astaxanthin is a powerful antioxidant (McNulty et al. 2007) occurring both in free form and esterified with fatty acids or associated with proteins (Cheesman et al. 1967;Matsuno 2001).In zooplankton, carotenoid accumulation is a highly variable trait that has been linked to photoprotection against ultraviolet radiation (UVR) in field studies comparing lakes with differential UVR exposure and in experimental studies (Hairston 1976;Moeller et al. 2005;Hylander et al. 2009;Rautio and Tartarotti 2010;Sommaruga 2010). The underlying mechanism ascribing astaxanthin photoprotection properties involves the quenching of singlet oxygen ( 1 O 2 ) produced during UVR exposure rather than direct absorption or reflectance of the hazardous wavelengths (Krinsky 1979;Kobayashi and Sakamoto 1999). UV-exposed copepods at low water temperatures have especially been suggested to profit from...
The freshwater copepod Leptodiaptomus minutus in boreal lakes has its main annual reproductive period at the end of winter. This follows months of ice cover and limited food production, yet the females transfer large quantities of algal‐derived carotenoids (predominantly astaxanthin) and fatty acids (FAs) to their eggs at this time, thereby providing the offspring with antioxidant protection and energy reserves. We hypothesised that this winter transfer of carotenoid pigments and FAs is based on accumulated reserves that are reinvested into reproduction (i.e. capital breeding). This strategy would allow the animals to produce offspring in time for the nauplii to feed on the spring phytoplankton bloom, thus gaining a competitive advantage. To test this hypothesis, we evaluated the seasonal production of precursor carotenoids and essential FAs by the phytoplankton, the amounts of these compounds required for egg production and the transfer rates from phytoplankton to copepod eggs. Pelagic primary production vastly outweighed the demand for copepod eggs during summer–autumn. However, the major peak of egg production in spring could not be sustained by the low phytoplankton productivity during winter, indicating reliance on previously accumulated reserves as hypothesised. High rates of lipid reserve accumulation in L. minutus in late autumn and early winter accounted for up to 128% (astaxanthin precursors) and 70% (FAs) of the daily production by the phytoplankton, further indicating the importance of pre‐winter primary production for reserve building in this copepod. During winter, the sum of carotenoid pigments as well as the sum of essential FAs stocked in copepods exceeded the concentrations in the seston. Consequently, adult copepods act as a lipid storage pool linking the biosynthesis of carotenoids and FAs by primary producers in autumn to the production of copepod eggs at the end of winter.
Zooplankton from clear alpine lakes is exposed to stressful levels of solar UV radiation (UVR). As these pelagic organisms experience high UVR and large changes in solar radiation conditions between ice‐free and ice‐cover periods, they have evolved various strategies to minimize UVR exposure and damage. Here, we studied the relation between photoprotection levels (mycosporine‐like amino acids, carotenoids), antioxidant capacities, and gene expression of heat shock proteins (hsps) as indicator of stress in the copepod Cyclops abyssorum tatricus during the course of a year. Expression of hsp60, hsp70, and hsp90 was measured in the field (baseline expression [BE]) and after UVR exposure in the laboratory. The BE differed among genes and seasons (hsp60: high during summer, hsp70 and hsp90: high during the ice‐cover period). The gene expression of hsp70 was upregulated after exposure to UVR (up to 5.2‐fold change), while hsp60 and hsp90 were only constitutively expressed. A strong seasonal pattern was found in the photoprotective compounds and antioxidant capacities, with highest levels during the ice‐free period. The extent of upregulation of hsp70 gene expression increased with decreasing photoprotection levels and peaked 24 h post UVR exposure (9.6‐fold change) at the time of lowest photoprotection (February). Our data suggest that hsp70 gene expression is modulated by seasonal plasticity in photoprotection. This ability of adequate stress response is essential for survival in highly variable ecosystems such as alpine lakes.
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