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And Nutrients JOTARO URABE* and ROBERT W Proc. Natl. Acad. Sci. USA Vol. 93, pp. 8465-8469, August 1996 Ecology Regulation of herbivore growth by the balance of light and nutrients JOTARO URABE* AND ROBERT W. STERNER Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108 Communicated by Eville Gorham, University of Minnesota, St. Paul, MN, April 19, 1996 (received for review November 11, 1995) ABSTRACT Experiments using planktonic organisms re- proportional to P supply/algal biomass. This ratio implies that vealed that the balance of radiant energy and available above a certain light intensity where P limitation becomes nutrients regulated herbivore growth rates through their increasingly severe, the algal P/C ratio would start to decline effects on abundance and chemical composition of primary (3, 4). As a result, the algal P/C ratio is expected to reach a low producers. Both algae and herbivores were energy limited at value at high light. low light/nutrient ratios, but both were nutrient limited at Herbivore responses were hypothesized based on ingestion high light/nutrient ratios. Herbivore growth increased with of C and P (Fig. IB). Because algal C content varies only increasing light intensity at low values of the light/nutrient slightly with growth conditions (18), C ingested by the herbi- ratio due to increases in algal biomass, but growth decreased vore per unit time (Ic) would be proportional to the rate of with increasing light at a high light/nutrient ratio due to ingestion of algal cells, which we took to be a rectilinear decreases in algal quality. Herbivore production therefore was functional response (19). P ingestion per unit time (Ip) is equal maximal at intermediate levels ofthe light/nutrient ratio. The results contribute to an understanding of mass transfer mech- to Ic multiplied by the algal P/C ratio. The small plateau ofIp anisms in ecosystems and illustrate the importance of integra- in Fig. 1B is due to our assumption that the light level tion of energy-based and material-based currencies in separating light limitation from combined limitation by light ecology. and P is less than the light level causing algal biomass to satiate the herbivore's functional response. Depending on the re- Both light and nutrients are essential in sustaining ecosystems, but very little is known about how relative changes in these sponse of algae to given light and nutrients regimes relative to abiotic factors extend into food chains (1, 2). Plants use solar the functional response of herbivores, alternate configurations radiation to fix carbon while they acquire nutrients at appro- without a plateau are possible. The critical feature here is that priate rates to maintain their biological integrity. However, Ip is expected to reach a maximum level at an intermediate photosynthesis and nutrient uptake are not perfectly coupled, light intensity due to the difference in the direction of response- and thus the contents of bioelements relative to carbon (C) in to light intensity between the algal biomass and P/C ratio. plant biomass vary within species (3-6). Because foraging and The net production of carbon by herbivores is given by the growth of many herbivore species respond to the chemical balance of assimilated carbon minus metabolic loss (mainly composition of their diet (7-10), the balance between photosyn- respiration). However, if Ip is too low compared with Ic, the thesis and nutrient uptake may in turn regulate herbivores carbon net production may be lower than otherwise expected. through the interplay of food quantity and quality. In this report, Under such a condition, the carbon net production would be we test the hypothesis that herbivore growth is dependent on the a product of net P intake divided by the P/C ratio of the body light/nutrient balance supplied to laboratory ecosystems. tissue. Because the P/C ratio of herbivore biomass is constant We focused on phosphorus (P) as a limiting nutrient because (20, 21) and because P excretion approaches zero when algal growth is frequently limited by P in freshwater systems herbivores ingest food with low P/C ratio (22), herbivore (11, 12), and because the algal P/C ratio has been most growth rate in carbon units (G) can be expressed as strongly implicated in regulating planktonic herbivores (13- 17). We first considered the likely responses of algae to light G = min[Ic x ac - ,3, Ip x ap/Zp/c] [1] intensity for a given P supply with a moderate but constant loss rate (Fig. 1A). Here, we expressed the response of algae by a where ac and ap are production efficiencies for C and P, Zp/c rectilinear form to show the essence of trends and qualitative is the ratio of differences along the light gradient. Precise response to light P/C the herbivore, and C is the metabolic loss and nutrients would depend on the identity of the algal species rate of C (respiration). As an example, we show the response and other environmental factors. At low light, algal growth of G to light intensity by setting 0.8 for ac and ap and 5% of should be limited by irradiance such that algal biomass in- a maximum Ic for X3 (Fig. 1B). Eq. 1 suggests that herbivore creases with light intensity. At high light, algal growth should growth will decrease with increasing light if they cannot be limited by finite P and algal biomass should reach a plateau. compensate for decreased algal P/C by increasing P produc- At extremely high light, algal growth may decrease due to tion efficiency, which of course must be the case at 100% photoinhibition, but Fig. 1A assumes light is below the pho- production. Thus, herbivore growth may be maximal at inter- toinhibition point. The response of algal P/C ratio is also mediate light intensity at the point where algal composition shown in Fig. 1A. At low light, the algal P/C ratio is expected becomes deficient in P relative to herbivore demands. Fur- to be high, close to the Redfield ratio (0.0094 by atoms), thermore, the light intensity where herbivores show maximal because algal growth is limited by irradiance alone and thus P growth rate may decrease with decreasing P supply rate, supply is sufficient relative to algal biomass. Because the P because the algal P/C ratio at a given light intensity is expected supply rate is constant, per capita P availability depends on to be lower at lower P supply rate. algal biomass and the algal P/C ratio is expected to be Abbreviations: C, carbon; P, phosphorus; N, nitrogen. The publication costs of this article were defrayed in part by page charge *To whom reprint requests should be sent at the present address: payment. This article must therefore be hereby marked "advertisement" in Center for Ecological Research, Kyoto University, Shimosakamoto accordance with 18 U.S.C. §1734 solely to indicate this fact. 4-1-23, Otsu, 520-01, Japan. e-mail: [email protected]. 8465 Downloaded by guest on September 26, 2021 8466 Ecology: Urabe and Sterner Proc. Natl. Acad. Sci. USA 93 (1996) obtusa born within a 12-hr time span from the second clutch A of the maternal individuals were placed into each flask. Neonate dry mass was 1.80 ,ug (SD, 0.05). Because D. obtusa Light Nutrient initiates reproduction within 1 week under preferable food limitation limitation conditions and because it is difficult to quantify individual growth rate (somatic growth + reproduction rates) after release of offspring, we incubated Daphnia for 6 days and then measured their dry mass for estimation of growth rate. During the 6-day run, algae continued to be diluted every 2 days but animals were not diluted. Potential complications that could invalidate our results include the possibility for interference or blocking in food collection by very high food density (25) or a direct inhibitory effect of high light on animal performance. To overcome such difficulties, a second experiment was performed with an "adjusted" treatment and effects of food quality and quantity were separately assessed. In this experiment, semibatch algal cultures with six different nutrient concentrations (N/P ra- tio = 80:1) were established and maintained under the high (260 ,uE m-2.s-) and low (12 ,uE m-2.s-) irradiance as mentioned above. These treatments were used as controls. In parallel with these treatments, algal suspensions of adjusted treatments were made every 2 days by adding 100 ml of algal suspension from the high-light treatments to 900 ml COMBO medium without P and N, and placed at the low irradiance. Thus, animals in the adjusted treatments were offered food of similar composition to the high-light treatment, but algal biomass was reduced 10-fold. Twenty neonates born within 12 h were introduced to each treatment and body mass on day 6 was measured. C and P contents of algae were examined using 250-ml culture suspensions collected for replacement at 2-day inter- vals while D. obtusa was incubated. Known aliquots of the Light intensity suspension were filtered onto precombusted glass fiber filters and analyzed for algal P content by spectrophotometric means FIG. 1. Qualitative model showing responses of algal biomass and after oxidation P/C ratio (A) and herbivore ingestion and growth rate (B) to changes by persulfate (26), and analyzed for C content in light intensity. We assumed that all chemical elements besides P are using a Perkin-Elmer model 2400 CHN analyzer. Animals in not limiting and that algae suffer from a moderate but constant loss each treatment were pooled into samples of 3 to 5 individuals, rate. The model does not incorporate feedbacks from the herbivore to placed in preweighed aluminum boats, and dried at 60°C algal biomass or physiology.
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