Light competition explains diversity decline better than niche dimensionality

Transcription

1 Functional Ecology 2017, 31, doi: / COMMENTARY Light competition explains diversity decline better than niche dimensionality Niv DeMalach* and Ronen Kadmon Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Givat Ram, Jerusalem 91904, Israel Summary 1. One of the most widely documented patterns in plant ecology is the decrease in species diversity following nutrient enrichment. A long-standing explanation for this diversity decline is an increase in the relative importance of size-asymmetric light competition which accelerates the rate of competitive exclusion (the light asymmetry hypothesis ). 2. Recently, an alternative hypothesis has been proposed which attributes the negative effect of nutrient enrichment on species diversity to a reduction in the number of limiting resources (i.e. a reduced niche dimensionality ). A recent global-scale experiment demonstrating that increasing the number of added resources leads to a decrease in species diversity was interpreted as a support for this niche dimension hypothesis. 3. Here we highlight a number of theoretical considerations that question this interpretation and demonstrate that a deeper analysis of the new global-scale dataset provides a stronger support for the light asymmetry hypothesis. Key-words: biomass, fertilization, grassland, nutrient enrichment, productivity, resource limitation, richness, size asymmetry, species loss Nutrient additions are leading to biodiversity loss in various grasslands world-wide (Gough et al. 2000; Crawley et al. 2005; Harpole & Tilman 2007). Although the general pattern is clear, there is still a controversy concerning the mechanistic link between nutrient addition and species loss. In particular, there is a disagreement between two competing hypotheses, one relating the negative effect of nutrient addition on species diversity to a shift in the nature of competitive interactions from below-ground to aboveground competition (the light asymmetry hypothesis, Newman 1973; Lamb, Kembel & Cahill 2009; DeMalach, Zaady & Kadmon 2017) and the other relating this effect to a reduction in the number of limiting resources (the niche dimension hypothesis, Harpole & Tilman 2007; Harpole & Suding 2011; Harpole et al. 2016). In this contribution, we clarify the rationale behind these contrasting hypotheses and highlight a number of problems in the interpretation of previous tests of the niche dimension hypothesis. We also reanalyse the data of a recent, globalscale resource addition experiment originally interpreted as a support for the niche dimension hypothesis (Harpole et al. 2016), and demonstrate that, contrary to the original *Correspondence author. nivdemalach@gmail.com interpretation, light competition is the main factor explaining species loss in this large-scale experiment. Before elaborating on the two hypotheses, it should be emphasized that many processes act together and probably interact with each other when nutrients are added to grasslands (Grace et al. 2016; Kaspari & Powers 2016). Thus, one may argue that presenting light limitation and reduced niche dimensionality as competing hypotheses is conceptually misleading. However, both the niche dimension hypothesis (Harpole & Tilman 2007) and the light asymmetry hypothesis (DeMalach, Zaady & Kadmon 2017) were proposed as distinct mechanisms that differ from other mediators of species loss. We therefore believe that setting them as competing hypotheses is an effective strategy for evaluating which of the two mechanisms is more important in causing species loss. Still, statistical analyses attempting to distinguish between the two hypotheses should be performed within a multidimensional framework that takes into account the potential effects of other mediators (Harpole et al. 2016). The light asymmetry hypothesis Newman (1973) was probably the first author to explain the negative effect of soil fertility on species richness in 2017 The Authors. Functional Ecology 2017 British Ecological Society

2 Light competition explains diversity decline 1835 terms of size-asymmetric light competition. Since then, several conceptual models have incorporated this view for explaining diversity patterns along fertility gradients (Rajaniemi 2003; Lamb, Kembel & Cahill 2009) and various experimental studies were interpreted in light of this hypothesis (Goldberg & Miller 1990; Leps 1999; Lamb, Kembel & Cahill 2009). According to the light asymmetry hypothesis, nutrient enrichment causes a shift from below-ground competition to light competition, light competition is size asymmetric in the sense that taller plants receive larger amounts of light per unit size than shorter plants, and this asymmetry in resource partitioning accelerates the rates of competitive exclusion, thereby reducing species diversity (Goldberg & Miller 1990; Leps 1999; Lamb, Kembel & Cahill 2009). This hypothesis was recently supported by a mechanistic resource competition model showing that size-asymmetric light competition is a necessary and sufficient condition for explaining the decrease in species diversity under high level of soil resources (DeMalach et al. 2016). The main empirical support for this hypothesis comes from experiments demonstrating the role of above-ground competition (Lamb, Kembel & Cahill 2009) and limited light penetration (Hautier, Niklaus & Hector 2009; Borer et al. 2014) as drivers of species loss under high soil fertility. Recently, DeMalach, Zaady & Kadmon (2017) provided direct experimental evidence that nutrient enrichment increases the asymmetry of light partitioning among tall and short plants. They also showed that the increase in light asymmetry was the main mediator of the negative effect of nutrient enrichment on species diversity, but this link was demonstrated using a structural equation modelling approach rather than by direct manipulations of the degree of light asymmetry. The niche dimension hypothesis The term niche dimension hypothesis was first used by Harpole & Tilman (2007) as an alternative mechanistic explanation for the negative effect of nutrient enrichment on grassland diversity. Based on the idea that the number of species in a competitive community is limited by the number of limiting resources (Hutchinson 1957; Tilman 1982), these authors proposed that the mechanism underlying species loss following nutrient enrichment is a reduction in the number of limiting resources (which was interpreted as a reduction in the dimensionality of the niche space), rather than a shift in the type of the limiting resources, as proposed by the light asymmetry hypothesis. In an attempt to test their hypothesis, Harpole & Tilman (2007) performed a factorial experiment of resource enrichment in which they added all combinations of four types of resources [nitrogen, phosphorus, base cations (K +,Mg 2+,Ca 2+ ) and water] to a grassland community, and tested how the number of added resources affects the number of species in the community. They found that an increase in the number of added resources decreased the number of species surviving in the community, and interpreted this result as a support for the niche dimension hypothesis. A study applying a similar experiment in an arid ecosystem provided similar results and led to similar conclusions (Harpole & Suding 2011). Recently, this experimental approach has been applied in a global-scale experiment focusing on 45 grasslands in different parts of the world, and the results were the same: increasing the number of added nutrients led to a significant decrease in species diversity (Harpole et al. 2016). The fact that this effect was statistically significant after controlling for the effect of plant biomass, and even when biomass production was not nutrient limited, was interpreted as a further support for the niche dimension hypothesis. Problems in the interpretation of previous tests of the niche dimension hypothesis The main hypothesis tested in previous tests of the niche dimension hypothesis was that species diversity should decline with increasing number of added resources (Harpole & Tilman 2007; Harpole & Suding 2011; Harpole et al. 2016). This prediction was based on the assumption that increasing the number of added resources decreases the number of limiting resources, thereby, reducing the dimensionality of the niche space. Harpole et al. (2016) suggested that increasing the number of added resources should also lead to a divergence of species composition from the control plots by modifying resource supply ratios. Clearly, there is a strong support for both predictions. However, we believe that these empirically documented patterns do not necessarily support the niche dimension hypothesis for reasons which we outline below. 1. An empirically observed relationship between the number of added resources and species diversity (or compositional divergence) demonstrates a pattern, not a mechanism. While experimental demonstration of these patterns does indicate a causal relationship between resource addition and species loss (or compositional divergence), it does not tell us anything about the mechanisms underlying these patterns. A mechanistic test of the niche dimension hypothesis (or any alternative hypotheses) should provide evidence confirming the mechanism assumed to generate the observed pattern (e.g. modification of resource supply ratios), rather than the predicted pattern itself. As far as we are aware, no study has demonstrated such a mechanistic link. 2. Since empirical quantification of the number of limiting resources or the dimensionality of the niche space (as perceived by the relevant species) is difficult and probably unfeasible, experimental tests of the niche dimension hypothesis are based on the assumption that the number of added resources is (negatively) correlated with the number of limiting resources. However, this simplistic assumption does not have any theoretical or empirical support. Moreover, as recently shown by Kaspari & Powers (2016), both theoretical and empirical evidence

3 1836 N. DeMalach & R. Kadmon suggests that the addition of added resources may influence the availability of non-added resources through complex pathways which they called limitation cascades (Kaspari & Powers 2016). These complex processes suggest that the whole concept of discrete number of limiting resources is too simplistic and should be replaced by more realistic concepts of co-limitation by multiple essential elements (Kaspari & Powers 2016). 3. Harpole et al. (2016) interpreted their finding that nutrient addition reduced richness even in systems where biomass was not affected by nutrient addition as a support for the niche dimension hypothesis. This interpretation implicitly assumes that the addition of nutrients affected the number and/or ratios of limiting resources in those systems. However, an alternative, and in our view, a more parsimonious interpretation, is that the added nutrients did not increase biomass production simply because they were not limiting resources. Clearly, if a particular nutrient is not a limiting resource in a particular system, adding it to the system cannot reduce the number of limiting resources, and an observed negative effect of its addition on species diversity should be attributed to other mechanisms [e.g. soil acidification (Crawley et al. 2005) or modification of the canopy structure which influences the vertical distribution of light (DeMalach, Zaady & Kadmon 2017)]. 4. A common property of all previous tests of the niche dimension hypothesis is that only soil resources were added to the community. Since light supplementation was kept constant in all experiments, reducing the number of limiting soil resources was unavoidably associated with an increase in the relative importance of light limitation, thereby confounding the effects of the number and type of limiting resources. Moreover, in all experiments, the quantity of each added resource was kept constant across all treatments, causing a strong correlation between the number of added resources and the total amount of resources added to the experimental communities. These confounding effects strongly complicate the interpretation of the results obtained from such experiments. 5. The strongest support for the hypothesis that nutrient enrichment reduces species diversity by reducing the number of limiting resources comes from the globalscale analysis performed by Harpole et al. (2016). In this study, the number of added resources had a statistically significant effect on species diversity even after controlling for the effects of dead and live biomass, proportion of light penetration below the canopy (hereafter light penetration ) and other variables (Harpole et al. 2016). However, analyses attempting to discriminate among alternative explanations for an observed response should focus on the magnitude of the relevant effects (i.e. on effect sizes), rather than on a binary discrimination between significant and non-significant effects (Tredennick et al. 2016). Below we provide evidence that such a more informative analysis leads to a different conclusion. Reanalysing the results of Harpole et al. (2016) We used the same linear mixed model used by Harpole et al. (2016) and the same dataset for quantifying the effect size of the number of added resources, biomass (live and dead separately) and light penetration, on species diversity (see Appendix S1 in the Supporting Information for details). All of these variables were considered by them potential mediators of the effect of nutrient addition on species diversity (e.g. Al-Mufti et al. 1977; Huston 1994). We applied two complementary methods for transforming the regression coefficients to comparable units standardized regression coefficients (Grace & Bollen 2005) and information theoretic averaging (Grueber et al. 2011). The first method is based on transformation of the model coefficients to standard deviation units and the second is based on comparing all possible subsets of the original model, ranking them based on AICc and then averaging the coefficients of the best models. The two methods produced very similar results: both methods showed that light penetration was the best predictor of species diversity, while all other factors, including the number of added resources had much weaker effects (Fig. 1). Actually, the real difference between the effects of light penetration and number of added resources is probably even larger, because the former effect has a measurement error while the latter is error free, and it is known that measurement errors may artificially inflate co-linear coefficients (Freckleton 2011). Clearly, the assertion that the decline in diversity was mechanistically related to a reduction in the number of limiting resources (i.e. by the niche dimension hypothesis) is not supported by this large-scale analysis. Discussion The debate regarding the mechanisms responsible for the decline of species diversity under high nutrient levels has started more than 40 years ago (Grime 1973; Newman 1973) and it is now clear that none of the mechanisms proposed since then is mutually exclusive. Based on the recognition that multiple processes simultaneously determine this decline and therefore, a simplistic approach based on the quantification of P values may obscure important information, Tredennick et al. (2016) have recently argued that It is time to focus on effect sizes and variance explained rather than just P values. Our analysis of the global-scale data from Harpole et al. (2016) is fully consistent with this claim: the original analysis was based on P values (obtained from a linear mixed model) and concluded that the number of added resources was the main mediator of the effect of nutrient addition on species diversity. We quantified the effect size of the same variables

4 Light competition explains diversity decline 1837 Standardized coefficients IT averaging LB DB LP NR LB DB LP NR Fig. 1. Effect size of (log) live biomass (LB), (log) dead biomass (DB), light penetration (LP) and number of added resources (NR) on species diversity. Effect size is measured in terms of absolute values of standardized coefficients in the left panel and information theoretic (IT) averaging coefficients in the right panel. Error bars represent standard errors (unconditional standard errors for the IT averaging coefficients). The original signs of all coefficients except light penetration were negative. Results are shown in absolute values for allowing easier comparison. using the same model and the same data, and found that the effect size of light penetration was much larger than that of the number of added resource. This result not only can be viewed as supporting the light asymmetry hypothesis, but can also support alternative light related hypotheses (Tilman & Pacala 1993; Huston & Deangelis 1994) since size asymmetry was not quantified in this study. The main problem with previous tests of the niche dimension hypothesis is that, in all of these tests, only soil resources were added to the community. This approach is problematic for two reasons. First, because light supplementation is kept constant in such experiments, this approach inevitably generates a negative correlation between the number of added resources and the relative importance of light limitation. Second, because of this correlation, the niche dimension hypothesis and the light asymmetry hypothesis produce a similar prediction: a decrease in species diversity with increasing number of added soil resources. One possible approach to distinguish between the two hypotheses is to include a treatment of light addition in the experimental setup. We are aware of only two experiments in which both nutrients and light were added in a multiple resource addition framework, a glasshouse experiment (Hautier, Niklaus & Hector 2009) and a field experiment (Eek & Zobel 2001). The experiment of Hautier, Niklaus & Hector (2009) had three treatments: control, supplementation of nutrients and supplementation of both nutrients and light. If the number of limiting resources is the main factor determining species diversity (as assumed by the niche dimension hypothesis), the latter treatment should have shown the lowest species diversity. However, the experimental results showed that this treatment had the highest diversity, a pattern contrasting the fundamental prediction of the niche dimension hypothesis. Similar results were obtained by Eek & Zobel (2001). These authors added light to both fertilized and non-fertilized plots of a grassland community using glass mirrors, and found that increasing light availability increased species diversity in fertilized, but not in unfertilized plots. The fact that light additions compensated rather than intensified species loss caused by nutrient addition in these two experiments suggests that such species loss was caused by light limitation, and not by a decrease in the number of limiting resources. It should be emphasized, however, that the niche dimension hypothesis and the light asymmetry hypotheses represent only a small fraction of the complex processes involved in determining the diversity of grassland communities (Grace et al. 2016). Furthermore, both hypotheses pool together resources with different characteristics (Craine & Dybzinski 2013): the niche dimension hypothesis focuses only on the number of resources, ignoring resource specific characteristics, while the light asymmetry hypothesis distinguishes between light and soil resources, but pool together water and all types of nutrient resources. We believe that such pooling is too crude to allow a rigorous discrimination between the various mediators of diversity responses to nutrient enrichment. Based on the above considerations, we recommend that future tests of these hypotheses should focus on experimental manipulations of the mechanisms that generate diversity responses to nutrient addition (i.e. the actual variables mediating these responses), rather than on simple resource additions. For example, experiments focusing on the light asymmetry hypothesis should incorporate measurements of light asymmetry (e.g. DeMalach, Zaady & Kadmon 2017) and should manipulate the asymmetry of light supply while keeping the overall amount of light constant. Similarly, experiments testing the niche dimension hypothesis should incorporate measurements of resource ratios (e.g. Lewandowska et al. 2016) and should manipulate resource supply ratios while keeping the overall amount of resources constant (as proposed by Cardinale et al. 2009). While such experiments are not simple and are logistically challenging, we believe that they are crucial for disentangling the complex processes and interactions involved in mediating the effects of nutrient enrichment on species diversity.

5 1838 N. DeMalach & R. Kadmon Conclusions We highlight a number of critical problems in the design and interpretation of previous tests of the niche dimension hypothesis and argue that the concept of a discrete number of limiting resources (on which all previous tests of this hypothesis were relied) is too simplistic and does not allow a mechanistic understanding of the causal relationship between resource addition and species loss. We also demonstrate that the results of experiments manipulating the amounts of both nutrient and light resources, as well as the global-scale experiment conducted by Harpole et al. (2016), support the hypothesis that light competition is the main mediator of species loss following nutrient enrichment. Based on these theoretical and empirical considerations, we conclude that current knowledge provides a strong support for the light asymmetry hypothesis and no support for the niche dimension hypothesis. Authors contributions N.D. analysed the data. N.D and R.K. wrote the manuscript. Acknowledgements We thank D. Robinson, K. Thompson and additional anonymous reviewer for comments on a previous version of this manuscript. We also thank W. S. Harpole and his colleges for providing us their raw data. The study was supported by the Israel Science Foundation grant no. 447/15, the Hebrew University Advanced School of Environmental Studies, the Ring Foundation, and the Nature and Parks Authority. The authors declare no conflicts of interests. Data accessibility All the data presented in this contribution are derived from a Nature paper by Harpole et al. (2016). Nature s policy demands authors of published papers to make the raw data available upon personal request. References Al-Mufti, M.M., Sydes, C.L., Furness, S.B., Grime, J.P. & Band, S.R. (1977) Quantitative analysis of shoot phenology and dominance in herbaceous vegetation. Journal of Ecology, 65, Borer, E.T., Seabloom, E.W., Gruner, D.S. et al. 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