Disrupted seasonal clockwork in the population dynamics of a freshwater copepod by climate warming

Life history responses are expected to accompany climate warming, yet little is known how long-term effects of climate and environmental change affect the seasonal dynamics of planktonic organisms. We used an historical data set from Lake Washington (U.S.A.) to quantify population responses of a calanoid copepod (Leptodiaptomus ashlandi) to long-term changes in temperature and resource availability and explore potential mechanisms for the responses. Increasing water temperatures (annual mean increase of 1.5uC in the upper 10-m water volume) and longer stratification periods (about 4 weeks) were observed between 1962 and 2005, coincident with a pronounced decline in Leptodiaptomus densities. However, production was maintained because of an increase in the production to biomass ratio and a life cycle shift in Leptodiaptomus from an annual to a 6-month cycle. Cross-wavelet analyses demonstrated that the annual thermal forcing of copepod recruitment observed during the first two decades of the study weakened substantially, leading to more stochastic population dynamics during the past two decades. This shift from one to two generations per year was most likely produced by a longer and warmer growing period combined with changing fluctuations in resource (phytoplankton) availability. Climate change can lead to higher-frequency voltinism in ectothermic organisms and to temporal reorganization of their population dynamics. Population dynamics of ectothermic organisms are strongly linked to the seasonality of temperature and resource availability. Subtle variation in extrinsic factors can modify the temporal population fluctuations in these organisms. Temperature is a key parameter affecting physiological rates in ectotherms (Beisner et al. 1997; Gillooly and Dodson 2000; Strecker et al. 2004), and their population growth shows strong coherence with seasonal temperature fluctuations. The direct effect of temperature on metabolic and vital rates have been inferred from experimental manipulations, observations along altitudinal and latitudinal gradients, and correlational studies between distribution patterns and climate variables (Magnuson et al. 1990; Wilhelm and Schindler 2000; Blais et al. 2003). These studies demonstrate that increasing temperature within the tolerance range of a species accelerates both growth and developmental rates of individual organisms given sufficient resources. Changes in these vital parameters caused by elevated temperature ultimately affect population dynamics (McCauley and Murdoch 1987) and have the potential to generate a shift from stable to more fluctuating dynamics (Halbach 1970; Beisner et al. 1997). Larger-amplitude cycles further increase the likelihood of extinction because of stochastic processes, as the population trajectory approaches zero density more closely and more often (Murdoch and McCauley 1985). The emerging view from these research syntheses is that elevated turnover rates, increased number of generations per year, greater population instability, and changes in life history strategies such as dormancy are anticipated for ectotherms with climate warming (reviewed by Bale et al. 2002; Drake 2005). The response of ectotherms to climatically driven environmental change, however, will depend not only on the direct effect of temperature on population vital rates but also on the synchronization of key life stages with food availability (Cushing 1990). This is particularly important for pelagic herbivores in temperate regions where quantity and quality of phytoplankton, their major food resource, is highly variable on a seasonal basis (Sommer et al. 1986). Moreover, climate change alters the density gradient of the water column and consequently the relative strength of mixing and stratification. Mixing processes are usually accompanied by changes in phytoplankton resource availability of light and nutrients and affect the seasonal dynamics of consumers (Winder and Schindler 2004b). As a result, climate may indirectly affect population dynamics and life histories of zooplankton through its effect on seasonality of resource availability and other components of the ecosystem, such as the extent of the growing season (Ottersen et al. 2001). Such modifications in the environment are expected to affect life cycle responses particularly in copepods (Chen and Folt 1996; Drake 2005), given the plasticity of their life histories and their extended longevity compared to cladocerans and rotifers (Allan and Goulden 1980). Copepods are important organisms in both freshwater and marine ecosystems, and their secondary production supports carnivores in many pelagic food webs (Mauchline 1998). Growth and development of these key planktonic taxa are subject to periodic (seasonal) and stochastic environmental variation, and their populations undergo extensive cyclic fluctuations both within and among years (Burns 1992; Twombly et al. 1998). Copepods have distinct reproductive pulses and recurring population oscillations produced through endogenous and exogenous drivers. 1 Present address: Tahoe Environmental Research Center, University of California, Davis, California * Corresponding author: [email protected] Limnol. Oceanogr., 54(6, part 2), 2009, 2493–2505 E 2009, by the American Society of Limnology and Oceanography, Inc.