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Freshwater Biology, in Press Freshwater Biology (2008) 53, 1291–1302 doi:10.1111/j.1365-2427.2008.01962.x Stoichiometric relationships in vernal pond plankton communities CARLA E. CA´ CERES*,ALANJ.TESSIER†, ANDRI ANDREOU* AND MEGHAN A. DUFFY‡ *School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, U.S.A. †Division of Environmental Biology, National Science Foundation, Arlington, VA, U.S.A. ‡School of Biology, Georgia Institute of Technology, Atlanta, GA, U.S.A. SUMMARY 1. The light-nutrient hypothesis (LNH) predicts that changes in light supply can alter the balance of nutrient and energy limitation in primary producers. We tested this prediction by examining temporal changes in vernal forest ponds, which are highly dynamic systems with respect to seasonal change in light and nutrient supply. In three vernal ponds that differ in productivity, we measured changes in light, total and seston nitrogen and phosphorus, and seston carbon and chlorophyll during the spring, before and after tree leaf-out. We also quantified changes in the population dynamics of the major zooplankton grazers in these systems. 2. In each pond, nutrient levels increased and light levels declined, creating a temporal shift in light-nutrient supply to the plankton. Results generally supported predictions of stoichiometric theory and the LNH, but there were notable exceptions. 3. Seston C : N : P ratios rapidly changed in response to dramatic increases in N and P supply rates. However, seston N : P was typically lower than values for total N : P in the water. Furthermore, as predicted, we observed a decline in seston C : P as the light : nutrient ratio declined, but seston C : N simultaneously increased. These results suggest an unexpected shift towards potential nitrogen limitation. Alternatively, this change in nutrient ratios may be driven by a seasonal change in phytoplankton composition or nutritional mode. 4. Seston carbon concentrations remained stable despite seasonal changes in grazing intensity associated with the phenology of large-bodied Daphnia grazers. However, chlorophyll concentrations declined dramatically as the season progressed, resulting in a simultaneous decline in the C : Chlorophyll ratio of seston. Both pond shading and increased grazing probably contributed to the decline in chlorophyll. Keywords: carbon, Daphnia, light-nutrient hypothesis, nitrogen, phosphorus questions of energy versus nutrient limitation can be Introduction addressed at multiple trophic levels (Hassett et al., Ecological stoichiometry, the balance of nutrients and 1997; Elser et al., 2000; Hall et al., 2006). The elemental energy in ecological interactions, provides a valuable composition of primary producers fluctuates in framework for investigating trophic interactions response to external changes in nutrient supply (Sterner & Elser, 2002). By tracking supply rates of whereas that of grazers is more constant (Andersen elements such as carbon, nitrogen and phosphorus & Hessen, 1991; Hessen & Faafeng, 2000). Hence, through the primary producers and into grazers, stoichiometric theory predicts thresholds of change where, depending upon the nutrient supply ratios, it Correspondence: Carla E. Ca´ceres, 515 Morrill Hall, Urbana, IL is expected that grazers can become limited by 61801, U.S.A. Email: [email protected] nutrients (food quality) rather than energy (food Ó 2008 The Authors, Journal compilation Ó 2008 Blackwell Publishing Ltd 1291 1292 C. E. Ca´ceres et al. quantity). Such transitions impact energy flow and reasons. First, these systems tend to exhibit dramatic nutrient recycling within ecosystems, can shift com- temporal changes in light and nutrient supply levels petitive relationships among species, and shape the (Colburn, 2004). In forested ponds, tree leaves pre- evolution of organism physiology and life history dictably open out over the course of a few weeks, (Andersen, 1997; Sterner & Elser, 2002). decreasing light levels dramatically. In addition, The stoichiometric framework considers more than vernal ponds form from nutrient-dilute snowmelt just the supply of elemental nutrients. Light is also and rain, but should experience a large increase in important, as is the interaction between light and nutrient supply due to decomposition from forest nutrients. In their light-nutrient hypothesis (LNH), floor litter (Wilbur, 1997). Second, temporary ponds Sterner et al. (1997) make several predictions regard- are often dominated by mixotrophic algae (Colburn, ing how nutrient use efficiency should vary across 2004). As the season progresses, this ability to change systems experiencing different light to nutrient ratios. nutritional mode as light and nutrient supply ratios The general concept is that as light becomes more are altered, coupled with overall changes in species limiting to primary producers, their elemental com- composition, may contribute to variance in the stoi- position should become enriched in nutrients such as chometric ratios of the seston. Third, the influence of nitrogen and phosphorus relative to carbon, resulting top-down factors on seston stoichiometry can fluctu- in increased food quality for grazers and higher ate just as dramatically as the bottom-up factors of trophic transfer efficiency. Of course, low light condi- light and nutrients (DeMott & Tessier, 2002). Hall tions will also reduce overall primary productivity, et al. (2007) showed evidence that grazers may play a decreasing food quantity for grazers. However, the key role in explaining field patterns of variation in evidence available from lakes suggests that limitation seston stoichiometry. In particular, top-down effects via food quality (including stoichiometry, phyto- of grazers increase turnover rate of the producers and plankton assemblage, fatty acid composition, etc.) is recycling rates of elements, both of which are often more important than is limitation by food expected to influence the stoichiometry of producers. quantity (Sterner & Schulz, 1998). Large-bodied daphniid species, which are a hallmark Several predictions of the LNH have been con- of temporary ponds (Schneider & Frost, 1996; firmed by focusing on comparisons among lakes that Colburn, 2004), hatch from diapausing eggs and can differ in mixing depth (mean light conditions for the quickly attain high biomass. Just as quickly, these phytoplankton), transparency and productivity either populations can disappear from the water entirely, as by using short-term manipulations such as mesocosm the result of producing diapausing rather than imme- experiments or broad-scale comparative studies (e.g. diately hatching eggs and increased predation. This Urabe & Sterner, 1996; Sterner et al., 1997; Hessen, creates a highly dynamic system with respect to Færøvig & Andersen, 2002; Diehl, Berger & Wohrl, grazer-imposed mortality rates on the primary pro- 2005; Schade et al., 2005; Dickman, Vanni & Horgan, ducers. 2006). Hall et al. (2007) extended the LNH to include In this study, we ask how temporal changes in light ponds that differ in light caused by tree shading, but and nutrient supply coupled with seasonal changes in still considered only spatial variation among commu- grazer abundance relate to seston stoichiometry in nities. However, light limitation has long been viewed three temporary ponds located in southwestern MI, as central in explaining temporal variation in primary U.S.A. Specifically, we addressed the following ques- productivity in most temperate ecosystems, and is tions (1) Are the patterns of temporal changes in pivotal to our understanding of seasonal succession in seston stoichiometry similar across ponds that differ the plankton (Sommer et al., 1986). The LNH predicts in trophic state (nutrient supply)? (2) Are these that an annual reduction in light level may cause a temporal changes related to the reduction in light shift in the balance of nutrient and light limitation in supply caused by tree leaf-out? In addition, we the phytoplankton. However, this prediction has discuss how seasonal changes in grazer abundance received limited testing (Chrzanowski & Grover, may influence, or be influenced by, seston stoichiom- 2001). etry. Our study was motivated by the premise that Vernal ponds are intriguing systems in which to temporal shifts in elemental ratios, including light, address these stoichiometric concepts for a number of may be particularly important in forested temporary Ó 2008 The Authors, Journal compilation Ó 2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 1291–1302 Stoichiometry in temporary ponds 1293 ponds, where canopy closure, temporal variation in <15 lm and <3 lm) were also filtered onto GF ⁄F glass- supply rates and variable grazing pressure can create fibre filters, extracted in cold 95% ethanol and mea- substantial seasonal changes. sured by use of narrow band fluorometry (Welsch- meyer, 1994). To sample the zooplankton assemblage, we col- Methods lected three replicate zooplankton samples (12–21 L We studied three natural, vernal forest ponds that each) on each date by pooling 4–7 (depending on differ in productivity as reflected by nutrient concen- pond size) grab samples, taken with a 3-L pitcher. trations of nitrogen and phosphorus (Roughwood, The grab samples were taken while walking a Woodfrog and West Gull). The ponds, located in transect through the middle of each pond, taking Kalamazoo County, MI, U.S.A., fill with snowmelt care not to resample previously disturbed areas and rainwater in early spring (March–early April), at (Dudycha, 2004). Two of the samples
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