No consistent effect of plant diversity on productivity.

Hector et al. (1) reported on BIODEPTH, a major international experiment on the response of plant productivity to variation in the number of plant species. They found “an overall loglinear reduction of average aboveground biomass with loss of species,” leading to what the accompanying Perspective (2) described as “a rule of thumb—that each halving of diversity leads to a 10 to 20% reduction in productivity.” These conclusions, if true, imply that the continuing high rate of plant extinction threatens the future productivity of Earth’s natural and managed ecosystems and could impair their ability to produce resources essential for human survival and to regulate the concentration of atmospheric CO2. Several problems with the Hector et al. article, however, lead us to question its major conclusions. First, the experimental approach of random species addition or removal in immature plant assemblages mimics neither natural nor human-caused processes of species extinction, accumulation, or combination and, thus, likely has little practical relevance. Second, the statistical analyses of Hector et al. made assumptions incompatible with the experimental design, thereby undermining many of the study’s conclusions. And, third, the article did not quantify crucial treatment and response variables, which reduces confidence in any conclusions about treatment effects. Other authors have thoroughly discussed the nonrandom nature of species establishment and extinction (3–5); here, we focus on issues of experimental design and statistical analysis. The most important conclusion was that “a single general relationship” may exist between species richness and productivity (1). This conclusion rested on two statistical findings: (i) that across all eight sites there were no statistically significant differences between the patterns observed, and (ii) that within seven of the eight sites there were statistically significant differences in productivity between the diversity treatments imposed at the individual site, which led to the reported within-site regressions and analyses of variance (ANOVAs). Even if both findings were technically correct, however, they do not necessarily imply that increasing species number causes a predictable increase in plant productivity. The data of Hector et al. do not support the conclusion that all sites showed a similar positive relationship between diversity and productivity. For three of the sites (Greece, Ireland, and Silwood), the authors’ own analysis showed no consistent change in biomass with species number, which our own regression of their data confirmed (Fig. 1). Moreover, two of the five sites at which Hector et al. identified significant positive regressions (Germany and Switzerland) included more species in their highest-diversity treatments than in the monocultures, so these treatments cannot be included in the regression without violating a crucial statistical constraint. The demonstration that plant productivity increases with species number in a mixture requires that the mixture’s productivity be greater than that of any species from the mixture grown separately, a response known as overyielding (6–11). If a mixture includes species whose growth has not been measured in a monoculture, it is impossible to determine whether the higher productivity of the mixture results from the biological processes that potentially cause overyielding or simply from the addition of a very productive species that was not evaluated in monoculture. Thus, the maximum number of species in the highest-diversity mixture must be no greater than the number of species that are grown in monoculture, and all of the highest-diversity mixtures must be identical in species composition, since each must contain only species grown in monoculture. The species assemblage codes in the BIODEPTH dataset show that only at the Portugal, Sweden, and Sheffield sites do all replicates of the highest-diversity treatment (species number half the number of monoculture plots) have identical species composition. At the other five sites, multiple species codes in the high-diversity treatments indicate that these mixtures include species not evaluated in monoculture. Five of the eight sites, therefore, cannot legitimately be used in statistical analyses of overyielding and diversity-productivity relationships, because the analysis may be biased toward increasing the productivity of high-diversity mixtures. The inclusion of unevaluated species in mixtures may explain the high variability in the biomass responses at these five sites compared with the three sites with properly designed experiments. That high variability allowed the authors to conclude that all sites had statistically similar responses. However, the inability to distinguish “no response” from “positive response” suggests that the real treatment effects were weak. The three sites with proper experimental design (Portugal, Sweden, and Sheffield) all showed significant positive regressions of productivity across two or three doublings of species richness [Fig. 1; (12)]. This is the pattern expected from random selection from a set of objects with different properties (13– 15), because the probability of including any specific member of the set—such as a plant species that grows rapidly or fixes nitrogen— increases with the number of objects selected. Such a pattern, found consistently in randomly assembled experimental plant communities but only rarely in natural plant communities (4, 5, 13–15), has been identified as a statistical artifact of experimental design (5, 13, 14). Although one study (15) suggested that the pattern constitutes a natural mechanism by which diversity affects productivity, this requires the biologically unrealistic assumption that plant communities are randomly assembled with respect to productivity (5). Separation of the effects of random selection from those of biological interactions that