Results and Discussion

The 11 protist species differed markedly in their competitive ability (Fig. 1) and in their ability to tolerate disturbance (Fig. S1). When considered together, there was a strong tradeoff between the two traits (Fig. 1). This tradeoff appeared to be mediated by body size, as smaller species, which tended to be weaker competitors, were better at tolerating disturbance (Fig. S2). The better tolerance of smaller species largely reflected their greater resilience afforded by their higher growth rates and larger carrying capacities, as they showed similar vulnerability to the imposed disturbance as larger species (Fig. S3). Note that the tradeoff between species competitive ability and the ability to cope with disturbance, together with the assumption of competition being less important with increasing disturbance, formed the base of the intermediate disturbance hypothesis (IDH) (4, 6, 20), also known as the hump-back model (1). This hypothesis predicts that species richness peaks at intermediate levels of disturbance, with diversity limited by competitive exclusion and disturbance-induced extinction at the low and high ends of the disturbance gradient, respectively. However, we found that this unimodal relationship between disturbance and species diversity was short-lived, emerging only on day 24 of our multispecies experiment (Fig. 2C). Before day 22, species extinction occurred mostly at the high end of the disturbance gradient, resulting from the joint effects of competition and disturbance (discussed below). Between day 22 and day 24, however, competitive exclusion occurred rather rapidly at low disturbance levels, presumably because of strong competition associated with high population densities. As a result, diversity was temporarily high at intermediate disturbance levels on day 24. On all other sampling days, however, species richness always decreased monotonically with disturbance (Fig. 2 A, B, D, and E).

• Download figure
• Open in new tab
• Download powerpoint

Fig. 2.

Temporal patterns of species richness and extinction along the disturbance gradient. (A–E) Observed species richness in the multispecies experiment was plotted against disturbance intensity at different sampling dates; data are means ± SE. (F–J) Number of cumulative species extinctions, with and without interspecific competition, was plotted against disturbance intensity at each sampling date. As all populations reached equilibrium states in the single-species experiment by day 30, the expected cumulative species extinctions at t = 6 mo were the same as those on day 30.

Given the absence of all species across much of the disturbance gradient at the end of the multispecies experiment (Fig. 2E), one likely explanation for the observed decline of species diversity with disturbance is that high levels of disturbances directly eliminated most or all species. This idea, however, was not supported by our single-species experiment, which showed that several species, when alone, were able to sustain viable populations even at the highest disturbance intensities (Fig. S1). It should be noted that, under conventional thinking, these disturbance-tolerant species are expected to dominate under high disturbances; instead, all of these species became extinct under interspecific competition in our multispecies experiment (Fig. 2). These results support the hypothesis that competition can still play a significant structuring role in highly disturbed habitats (9).

If competition consistently regulates community structure throughout the disturbance gradient, the combined effect of competition and disturbance may potentially explain the negative disturbance–diversity relationships observed in our multispecies experiment. To explore this possibility, we assessed the importance of interspecific competition more quantitatively using a null community model approach (21). This was done by comparing the actual number of species extinctions in the presence of interspecific competition (that is, extinctions observed in the multispecies experiment) with the expected number of species extinctions in the absence of interspecific competition (that is, predicted extinctions based on the results of the single-species experiment) (Materials and Methods). We found that species extinctions that were attributable to interspecific competition occurred throughout the entire disturbance gradient (Fig. 2 F–J). Most interestingly, the tempo of competitive exclusion was greater at higher, not lower, disturbance intensities (Fig. 2 F–J). At the early stage (week 1) of the multispecies experiment, interspecific competition already resulted in the extinction of seven species at the two highest disturbance levels, contrasting with no species extinction observed at the two lowest disturbance levels (Fig. 2F). Most competitive extinctions at the lowest disturbance levels did not occur until after week 3 of the experiment (Fig. 2 G–J). Therefore, contrary to the common perception that disturbance tends to reduce the importance of competition and mitigate competitive exclusion (5, 6, 17), increasing disturbance intensities actually increased the importance of competition in controlling species extinction and community richness.

The above results may possibly be explained by increasing disturbance resulting in incrementally lower population densities of all species (Fig. S1), making these species (including disturbance-tolerant species) less tolerant of competition. To confirm this, we identified for each species the level of disturbance at which interspecific competition led to its most frequent extinctions, and compared this level to the highest disturbance level that the species can tolerate in the absence of interspecific competition (Materials and Methods). Strikingly, when all species were considered together, there was a strong positive relationship between the two levels, with the slope of the regression close to 1 (Fig. 3). This indicates that each species was most vulnerable to interspecific competition at its upper disturbance limit at which its density was most severely reduced, a finding supportive of the above hypothesis.

• Download figure
• Open in new tab
• Download powerpoint

Fig. 3.

The relationship between the highest disturbance level that the species can tolerate in the absence of interspecific competition as recorded in the single species experiment (Disturbance level_{limit of tolerance}) and the level of disturbance at which interspecific competition led to the most frequent extinctions of each species in the multispecies experiment (Disturbance level_{most competitive exclusion}). Solid and broken lines are the linear regression line and 1:1 line, respectively.

Current empirical evidence indicates that although the unimodal disturbance–diversity pattern predicted by the IDH has been frequently documented (4, 6, 22–27), other forms of disturbance–diversity relationships in fact tend to be more common (28). The persistent role of competition along the disturbance gradient found in our experiment, which challenges a major IDH assumption, provides a possible explanation for this mismatch between theory and empirical data. However, the extent to which this explanation can account for the abundant nonunimodal disturbance–diversity patterns observed in various systems remains unclear. In particular, we note three characteristics of our experimental system that may influence the applicability of our results to some other systems. First, protist species in our experiments competed exploitatively for shared bacterial resources. However, theory suggests that the mechanism of competition may influence how disturbance alters competitive outcomes (29). It thus may not be straightforward to extrapolate our findings based on exploitive competition to communities characterized by interference competition (e.g., competition for space). Second, there was no outside immigration into our experimental microcosms, contrasting with natural communities subject to various degrees of immigration. We chose to control for immigration because it would have effectively prevented species extinction, which may compromise our ability to estimate the importance of competition. This decision, however, means the loss of the opportunity of evaluating whether the competition-colonization tradeoff, known to exist among our study organisms (30), can result in IDH patterns, as often predicted (31, 32). More generally, we note that few empirical studies have established the linkage between the competition–colonization tradeoff and the unimodal disturbance–diversity pattern (33), an issue that clearly warrants further investigation. Third, given the small microcosm size, disturbance in our experiments can be considered as having a “global” effect throughout each microcosm. This contrasts with the more common situation in nature whereby localized disturbance generates spatial heterogeneity among different habitat patches, which characterizes many empirical studies supportive of the IDH (31). Direct extrapolation of our results to cases influenced by local disturbance is hampered by the fact that spatial heterogeneity in the latter case may additionally influence species coexistence and diversity (34, 35). Nevertheless, there is theoretical evidence that similar mechanisms could operate in both cases to generate IDH patterns (31), as well as experimental evidence that IDH patterns can emerge in the presence of global disturbance (14, 36). Comparable work in other systems is needed to determine the generality of our results. In addition to the above limitations, our explanation of persistent competition underlying the lack of IDH patterns is also complicated by the fact that a host of other factors, such as productivity (5), trophic interactions (29), and history of community assembly (14), may alter disturbance–diversity relationships.

Despite the above caveats regarding our results in relation to the IDH, our study provides unique experimental evidence that competition can consistently regulate species extinction and community richness over broad disturbance gradients. This result challenges conventional thinking (4–6) but is consistent with the prediction of the few theoretical investigations (9), with important implications for understanding relevant ecological issues, such as those related to biodiversity, community assembly, and conservation. For example, our study suggests that the reduced importance of competition with increasing disturbance is unlikely to be behind empirical patterns consistent with the IDH. More attention should thus be focused on examining other candidate mechanisms that may potentially contribute to IDH patterns (e.g., disturbance-induced spatial structure). Another corollary of our result is that priority effects associated with varying histories of community assembly may not necessarily be weak in highly disturbed habitats as previously thought (7, 14, 37), a hypothesis that needs to be evaluated experimentally. Our results also suggest that when evaluating species extinction risk, one needs to take into account the effect of interspecific competition, even in habitats strongly influenced by disturbance. Given that predation can reduce population sizes and make species more vulnerable to disturbance in a similar way (38), conservation biology can benefit from considering the roles of both abiotic and biotic interactions.