Use of deep autochthonous resources by zooplankton: Results of a metalimnetic addition of 13C to a small lake

Abstract

Resources in lakes are vertically partitioned due to stratification and trophic interactions. Metalimnetic phytoplankton could be an important resource for zooplankton that either reside in the metalimnion or migrate through this layer. However, it is difficult to estimate metalimnetic resource use, especially using isotope approaches, because surface and deep phytoplankton often have similar isotopic compositions. To overcome this limitation, we experimentally enriched the metalimnetic dissolved inorganic carbon (DIC) 13C pool in Peter Lake to enhance the isotopic separation between metalimnetic phytoplankton and other resources. Metalimnetic d13CDIC peaked at 73.2% after the isotope addition and maintained an average enrichment of 34.5% above epilimnetic d13C-DIC for 62 d. Combining hydrogen and carbon stable isotope values, we estimated the epilimnetic, metalimnetic, and terrestrial resource use by zooplankton, using a Bayesian mixing model that accounted for uncertainties in both consumers and sources. We also measured diel vertical migration and net ecosystem production with in situ bottle incubations over the course of the experiment. Metalimnetic resource use was minor (0–8%) for zooplankton that either resided in the epilimnion of the lake during the day or migrated there at night. For consumers that resided in the metalimnion, metalimnetic phytoplankton accounted for 18– 21% of zooplankton isotope composition. The most important resource for all zooplankton was terrestrial organic matter (56–73% of consumer mass), regardless of habitat. This experiment indicates that, in lakes like Peter Lake, metalimnetic autochthonous resources are of minor importance to zooplankton relative to epilimnetic autochthonous and allochthonous resources. In lake ecosystems, consumers have varying quantities and qualities of autochthonous (aquatically derived) resources and allochthonous (terrestrially derived) subsidies available for consumption (Marcarelli et al. 2011; Wilkinson et al. 2013a). In the pelagic zone of lakes, autochthonous resources can be further divided based on strong vertical gradients that determine the distribution of aquatic resources and consumers. These gradients are both abiotic (light, temperature, dissolved oxygen) and biotic (resource quantity and quality, predation threat). Metalimnetic primary production (production in the thermocline in stratified lakes) has been suggested to be a significant pelagic resource exploited by aquatic consumers, which augments resources from epilimnetic production (Matthews and Mazumder 2006; Francis et al. 2011; Batt et al. 2012). Though light limited, phytoplankton growing in the metalimnion have access to the large pool of recycled nutrients that are unavailable to epilimnetic phytoplankton (Sawatzky et al. 2006), generally increasing their resource quality (Elser and George 1993). Metalimnetic resources are available to consumers residing in that thermal layer as well as to zooplankton that migrate vertically and inhabit the metalimnion only part of the time (Gliwicz 1986; Lampert and Grey 2003). Patterns of diel vertical migration in zooplankton are the result of predator avoidance, competition for resources, and thermal requirements for growth and reproduction (Lampert 1989). In lakes with primary production in the metalimnion, zooplankton that migrate deep in the water column during the day can potentially exploit resources that can be rich in phosphorus (Sterner and Schwalbach 2001), thereby aiding growth (DeMott et al. 2004) while avoiding visual predators such as fish (Beklioglu et al. 2008). However, the cold water within the thermocline can significantly slow zooplankton growth and reproduction rates (Loose and Dawidowicz 1994). It is also unclear whether the resources available in the metalimnion are ideal for zooplankton growth and reproduction, especially at metalimnetic temperatures (Williamson et al. 1996; Cole et al. 2002; Winder et al. 2004). The trade-off between predator avoidance and food quality and quantity among systems leads to varying strengths of diel vertical migration and metalimnetic resource exploitation by consumers (Loose and Dawidowicz 1994; Brosseau et al. 2012). Whereas there have been numerous mesocosm studies (Williamson et al. 1996; Kessler and Lampert 2004) investigating how migration trade-offs affect metalimnetic resource consumption by zooplankton, there have been few studies that have explicitly quantified metalimnetic, epilimnetic, and terrestrial resource exploitation by migrating pelagic consumers in natural lakes (Armengol et al. 2012). Stable isotopes are useful for quantifying consumer resources. Stable hydrogen isotopes (2H and 1H) have recently been used to trace aquatic consumer resource use (Doucett et al. 2007; Finlay et al. 2010; Karlsson et al. 2012) because the separation in isotopic composition between terrestrial and aquatic resources is larger for hydrogen than for those of carbon. Although the separation * Corresponding author: gmw6yy@virginia.edu Limnol. Oceanogr., 59(3), 2014, 986–996 E 2014, by the Association for the Sciences of Limnology and Oceanography, Inc. doi:10.4319/lo.2014.59.3.0986

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