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Light, Nutrients, and Food-Chain Length Constrain Planktonic Energy Transfer Efficiency Across Multiple Trophic Levels

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Light, nutrients, and food-chain length constrain planktonic energy transfer efficiency across multiple trophic levels Elizabeth M. Dickman1, Jennifer M. Newell1, María J. Gonza´ lez, and Michael J. Vanni2 Department of Zoology, Miami University, Oxford, OH 45056 Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved October 3, 2008 (received for review June 8, 2008) The efficiency of energy transfer through food chains [food chain carnivores, because their tissue chemical composition is similar efficiency (FCE)] is an important ecosystem function. It has been to that of their prey (8). Thus, it has been proposed that the hypothesized that FCE across multiple trophic levels is constrained carbon/nutrient stoichiometry of primary producers constrains by the efficiency at which herbivores use plant energy, which energy transfer across multiple trophic levels, i.e., from primary depends on plant nutritional quality. Furthermore, the number of producers to carnivores (8, 9), but this hypothesis has not been trophic levels may also constrain FCE, because herbivores are less explicitly tested. efficient in using plant production when they are constrained by The stoichiometry of aquatic primary producers (algae) often carnivores. These hypotheses have not been tested experimentally reflects the supply of nutrients and light (8, 10, 11). Algal cell in food chains with 3 or more trophic levels. In a field experiment carbon/nitrogen (C/N) and carbon/phosphorus (C/P) ratios de- manipulating light, nutrients, and food-chain length, we show that crease with increasing nutrients and decreasing light intensity FCE is constrained by algal food quality and food-chain length. FCE (10, 12, 13), and the ecological efficiency of aquatic herbivores across 3 trophic levels (phytoplankton to carnivorous fish) was is often higher under low light and/or high nutrient conditions, highest under low light and high nutrients, where algal quality was when algal C/P is relatively low (14–16). However, other aspects best as indicated by taxonomic composition and nutrient stoichi- of algal food quality may also covary with stoichiometry, such as ometry. In 3-level systems, FCE was constrained by the efficiency at morphological features (e.g., size, shape, presence of gelatinous which both herbivores and carnivores converted food into pro- sheaths) and biochemicals (e.g., essential fatty acid and sterol duction; a strong nutrient effect on carnivore efficiency suggests a concentrations) (11, 17). Because algal species differ in these carryover effect of algal quality across 3 trophic levels. Energy characteristics, phytoplankton taxonomic identity may be a transfer efficiency from algae to herbivores was also higher in surrogate of food quality. 2-level systems (without carnivores) than in 3-level systems. Our We explored the general hypothesis that FCE depends on light results support the hypothesis that FCE is strongly constrained by intensity, nutrient supply, and food-chain length. This field study light, nutrients, and food-chain length and suggest that carryover explicitly quantifies how light and nutrients interactively regulate effects across multiple trophic levels are important. Because many FCE in systems with 3 trophic levels. In a field experiment using environmental perturbations affect light, nutrients, and food- aquatic mesocosms, we tested 3 specific hypotheses: (i) FCE (in chain length, and many ecological services are mediated by FCE, it food chains of equal length) is highest under low light/high will be important to apply these findings to various ecosystem nutrient conditions and lowest at high light/low nutrients; (ii) types. herbivore ecological efficiency is higher in food chains with just 2 trophic levels than with 3 trophic levels, because herbivores are ͉ ͉ ͉ ͉ ecological efficiency ecological stoichiometry fish zooplankton unconstrained by predation in 2-level systems; and (iii) because phytoplankton herbivores are more constrained than carnivores by food quality, FCE across 3 trophic levels is constrained by herbivore ecological lucidating the constraints on the efficiency of energy transfer efficiency (ratio of herbivore production to primary production). Ethrough food chains is necessary for understanding many ecological processes (1–6). Food chain efficiency (FCE), defined Results as the proportion of energy fixed by primary producers that is In treatments with 3 trophic levels, FCE increased with decreas- transferred to the top trophic level, depends on the ecological ing light (P Ͻ 0.0001) and increasing nutrients (P ϭ 0.0004), and efficiencies at each trophic coupling (1). FCE can regulate was highest in the low light/high nutrient treatment, as predicted attributes such as food-chain length and biomass (7) and eco- by our first hypothesis (Fig. 1A). Across all treatments, herbivore system services such as fisheries production (2, 3), export of efficiency was affected by the main and interactive (P ϭ 0.0010) carbon from ecosystems (4), and concentrations of contaminants effects of light and fish and was greater under low light condi- in organisms (5). tions than under high light (P ϭ 0.0003). In support of our second Although FCE may regulate the number of trophic levels, the hypothesis, herbivore efficiency was much higher in the absence reverse may also be true: the number of trophic levels may of fish than in their presence (P Ͻ 0.0001; Fig. 1 B and C). determine FCE (1). With 3 trophic levels (plants, herbivores, and carnivores), herbivores may be held in check by carnivores and thus inefficiently consume plant biomass. However, with 2 (or 4) Author contributions: E.M.D., J.M.N., M.J.G., and M.J.V. designed research; E.M.D. and levels, herbivore biomass is unconstrained (or less constrained) J.M.N. performed research; E.M.D., J.M.N., M.J.G., and M.J.V. analyzed data; and E.M.D., by predation, possibly leading to higher herbivore production J.M.N., M.J.G., and M.J.V. wrote the paper. relative to primary production (1). The authors declare no conflict of interest. Ecological efficiencies often depend on food-quality attributes This article is a PNAS Direct Submission. such as edibility and nutritional quality. The ecological efficiency 1E.M.D. and J.M.N. contributed equally to this work. of herbivores often depends on plant nutrient stoichiometry 2To whom correspondence should be addressed. E-mail: [email protected]. (carbon/nutrient ratio) relative to the respiratory demands, This article contains supporting information online at www.pnas.org/cgi/content/full/ nutrient demands, and assimilation efficiency of the herbivore 0805566105/DCSupplemental. (6, 7). Stoichiometric constraints may be less important for © 2008 by The National Academy of Sciences of the USA 18408–18412 ͉ PNAS ͉ November 25, 2008 ͉ vol. 105 ͉ no. 47 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0805566105 Downloaded by guest on September 29, 2021 Fish Present Fish Absent A Food Chain Efficiency (Phytoplankton to Fish) 0.07 A 300 B 350 a a 0.06 250 300 a 250 0.05 200 b 0.04 200 b b 150 c 0.03 150 d c Seston C:P 100 0.02 100 c Fish production / c 0.01 c 50 50 phytoplankton production 0.00 High Low High Low 0 0 Nutrients Nutrients Nutrients Nutrients High Light Low Light 14 14 C D a 12 12 Herbivore Efficiency (Phytoplankton to Zooplankton) a a 0.20 2.0 10 a a 10 b Fish Present Fish Absent b b B C 8 8 0.15 1.5 a a 6 6 b Seston C:N 0.10 1.0 4 4 b b 2 2 0.05 0.5 b 0 0 b b Zooplankton production / phytoplankton production 0.00 0.0 High Low High Low High Low High Low E 1.5 F 1.5 Nutrients Nutrients Nutrients Nutrients Nutrients Nutrients Nutrients Nutrients a High Light Low Light High Light Low Light a 1.0 1.0 Carnivore Efficiency (Zooplankton to Fish) ab D 1.5 b b b D b food quality 0.5 0.5 1.2 b a 0.9 a Phytoplankton compositional 0.0 0.0 0.6 High Low High Low High Low High Low Nutrients Nutrients Nutrients Nutrients Nutrients Nutrients Nutrients Nutrients ab Fish production / 0.3 High Light Low Light High Light Low Light zooplankton production b 0.0 High Low High Low Fig. 2. Quality of phytoplankton as a food resource based on cell stoichi- Nutrients Nutrients Nutrients Nutrients High Light Low Light ometry (A–D) and taxonomic composition (E and F). Phytoplankton responses were measured in each mesocosm throughout the study, and each point Fig. 1. Light, nutrient, and fish effects on FCE (2-way ANOVA, n ϭ 12, P ϭ represents a mesocosm mean, averaged over the experiment. Horizontal lines 0.0009) (A), herbivore efficiency (3-way ANOVA, n ϭ 23, P ϭ 0.0003) (B and C), represent treatment means, and letters indicate treatments that are signifi- and carnivore efficiency (2-way ANOVA, n ϭ 12, P ϭ 0.0138) (D). Each point cantly different from each other (Tukey post hoc test). Treatments with fish represents the efficiency for an individual mesocosm, obtained by using present and absent were analyzed separately. production rates averaged over the experiment for each trophic level. Hori- zontal lines represent treatment means, and letters indicate treatments that are significantly different from each other (Tukey post hoc test). For herbivore Nutrients decreased seston C/P at low light (as expected), but efficiency, all 8 treatments (fish absent and fish present) were analyzed increased C/P at high light (Fig. 2 A and B and Table S1). It is together, although they are graphically depicted separately. Note that the unclear why C/P increased in response to nutrients in the high scale differs in fish present vs. fish absent treatments for herbivore efficiency. In 2 mesocosms, carnivore efficiency exceeded 1, possibly because toward the light treatments; perhaps the marked increase in phytoplankton end of the experiment fish consumed some benthic algae, although zooplank- biomass (Fig.
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