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Species Richness Enhances Both Algal Biomass and Rates of Oxygen Production in Aquatic Microcosms

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Species Richness Enhances Both Algal Biomass and Rates of Oxygen Production in Aquatic Microcosms Oikos 118: 1703Á1711, 2009 doi: 10.1111/j.1600-0706.2009.17585.x, # 2009 The Authors. Journal compilation # 2009 Oikos Subject Editor: Daniel Gruner. Accepted 24 April 2009 Species richness enhances both algal biomass and rates of oxygen production in aquatic microcosms Lillian D. Power and Bradley J. Cardinale L. D. Power and B. J. Cardinale ([email protected]), Dept of Ecology, Evolution and Marine Biology, Univ. of California-Santa Barbara, Santa Barbara, CA 93106, USA. LDP also at: Biomathematics Graduate Program, North Carolina State Univ., Raleigh, NC 27695, USA. Accelerating rates of species extinction have generated much recent interest in understanding how biodiversity affects the functioning of ecosystems. Experiments to date have shown communities composed of fewer species generally capture a smaller fraction of available resources, and achieve lower standing stock biomass than more diverse communities. However, it is uncertain how changes in biodiversity and the resulting alterations in biomass affect the rates of important ecological processes like primary production, which regulates fluxes of CO2 and O2 between the biotic and abiotic components of the environment. Here we show that species richness influences not only the standing stock biomass of primary producers, but also rates of gross primary production measured by changes in O2 concentrations in aquatic systems. We manipulated the richness of five widespread species of algae in laboratory microcosms and then quantified how richness impacts algal biomass, rates of gross primary production (GPP), and the ratio of production to respiration. Algal biomass increased by a factor of 1.82 for each level of species richness, and GPP by a factor of 1.20, for each additional species. Production to respiration ratios increased about 10% for each additional species, indicating that systems with more species were increasingly autotrophic Á that is, they produced more O2 than they consumed, and accumulated CO2 faster than they released it. These trends were driven by two highly productive species that became co-dominant in species rich polycultures at the expense of other taxa. Our experiment suggests that changes in biodiversity may influence not only the rates at which O2 and CO2 are produced and released in ecosystems, but also the total amount of carbon that is sequestered and stored as biomass. Over the past several decades, more than 150 experiments certain communities, such as terrestrial grasslands that are have manipulated the number of species of bacteria, fungi, dominated by annual plants, it is often assumed that the plants and animals in a variety of terrestrial and aquatic amount of aboveground biomass accrued over a single ecosystems to examine how biodiversity affects the effi- growing season is a reasonable proxy for rates of primary ciency by which communities capture limited resources and production. convert those into new biomass (Hooper et al. 2005, However, several authors have suggested that long-term Balvanera et al. 2006). Recent meta-analyses of these accumulation of standing biomass might not respond to experiments have shown that diverse communities are, on diversity in the same way as instantaneous rates of average, twice as efficient at capturing limited resources and production (Stocker et al. 1999, Petchey 2003, Balvanera achieve roughly twice the biomass as communities that et al. 2006). For example, Schulze (1996) argued that the are highly reduced in diversity (Cardinale et al. 2006, fluxes of CO2 that are driven by primary production should Stachowicz et al. 2007). While there appears to be be independent of plant diversity because these fluxes are considerable generality in how species richness impacts instead regulated by environmental constraints after plant the standing stock biomass achieved by a group of cover exceeds a relatively low critical value. In contrast, organisms, it is much less certain how species diversity Korner (2004) argued that plant species richness should affects the rates of ecological processes like primary stimulate photosynthesis and the rate at which plant production. This is because studies have only rarely communities sequester carbon from their environment; quantified rates of photosynthesis, or the fluxes of O2 or however, this might not translate into long-term carbon CO2 into/out of plants. Rather, most experiments have storage due to increased turnover of biomass. These simply examined how the initial number of species placed contrasting perspectives are not easily resolved by ecological in some experimental unit (field plot, greenhouse pot, etc.) theory, much of which predicts that species diversity will impacts standing biomass (mass area1 or volume1) after increase standing stock biomass and, in turn, the fraction of some period of growth (usually months or years). For available carbon, nutrients, and other inorganic resources 1703 that are stored in tissue (Tilman et al. 1997, Loreau 1998a, both standing stock biomass, as well as rates of primary Cardinale et al. 2004, Ives et al. 2005). However, these production that control fluxes of O2. models tend to focus on communities that have achieved an equilibrium biomass where gains and losses of carbon are balanced (i.e. zero net change). As such, they offer few Methods predictions about how species diversity might influence instantaneous fluxes of carbon between biotic and abiotic Focal species components of the environment (but see Cardinale et al. 2004, Weis et al. 2007 for mathematical explorations of the We used five species of freshwater algae that are common in of the effects of diversity on short-term changes in standing North American phytoplankton communities (Graham and stocks for non-equilibrium communities). Wilcox 2000). These included two species of diatoms Á Unfortunately, empirical work has also failed to provide Achnanthidium minutissimum (Ac), Navicula cryptocephalus any consistent answer to how species richness impacts the (Na), and three chlorophycean green algae Á Chlorella stocks verses fluxes of energy and matter. Balvanera et al. vulgaris (Ch), Scenedesmus quadricauda (Sc) and Selenastrum (2006), who analyzed biodiversity studies performed with minutum (Se). All species were acquired from commercial primary producers, decomposers and higher consumers, culture collections, two from Carolina Biological Supply found no difference in the magnitude of diversity effects on (Ch, Sc), and three from the culture collection at the Univ. long-term accumulation of standing stocks verses short- of Texas at Austin (Ac, Na, Se). Aside from being abundant term rates of carbon flux. Schmid et al. (2009), who and common in lakes, these taxa were chosen because all combined the data of Balvanera et al. (2006) with those grow well under laboratory conditions using common from the meta-analysis of Cardinale et al. (2006), came to a growth media, and are morphologically diverse, making different conclusion, stating ‘‘Our analyses clearly showed them easy to distinguish from one another. that there were differences between stocks and rates and that, in fact, biodiversity influenced stocks more strongly and more positively than rates.’’ Srivastava et al. (2009), Experimental design who performed a meta-analysis of studies focusing more The experimental units for this study were 105 sterilized narrowly on experiments performed with detritivores glass jars filled with 120 ml of Chu algal growth media. Jars feeding on clearly defined carbon sources (usually leaf were randomly assigned to one of 21 treatments represent- litter), came to an even different conclusion. Their results ing each of the five species grown alone in monoculture, five revealed no evidence that detritivore diversity influences the combinations of 2, 3 and 4 species selected randomly from standing stock biomass of carbon resources; yet, there was all possible combinations, and all five species grown strong evidence that detritivore diversity increased the rate together in full polyculture. Species were inoculated at the at which carbon was sequestered from these resources. start of the experiment according to a replacement-series Of course, one reason these meta-analyses have poten- design where total algal density was held constant at tially come to differing conclusions is that they have 5000 cells ml1 across all levels of species richness, S; compared biodiversity effects on stocks and fluxes that thus, the number of cells of any single species added to an were typically measured for different response variables experimental unit was 50001/S. Each species monocul- across different groups of organisms. It is fairly rare to find ture was replicated in nine jars, each two through four experiments that have manipulated the diversity of a focal species polyculture was replicated in three jars, and the full group of organisms and then simultaneously measured the five species polyculture was replicated in 15 jars (for 105 effect of diversity on both stocks and fluxes of a focal jars total). After inoculation, experimental units were placed material. However, aquatic ecologists have recently started upright at randomly selected positions on a shaker table, to weigh in on this debate by using model systems of algae and exposed to cool white fluorescent lights that were set to in which it is tractable to measure both the accrual of an 18:6 hour light dark cycle inside a growth chamber biomass as well as the instantaneous rates of photosynthesis where temperature was maintained
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