Biotic and anthropogenic forces rival climatic/abiotic factors in determining global plant population growth and fitness

Discussion

Our analysis of the best available data shows that there is no one main type of driver (abiotic, biotic, or anthropogenic) that has overwhelmingly stronger effects on plant population growth and fitness relative to the others. Using a portion of the full dataset, we did find that λ was marginally significantly less sensitive on average to changes in biotic relative to abiotic drivers (when changes are measured in units of SDs; Fig. 2B), but this difference is weakly supported and deserves to be examined further when more data become available. The best estimates of the average scaled sensitivities suggest that biotic changes will be more than one-half as influential as abiotic changes of comparable magnitude, and thus worthy of consideration. Our conclusion based on analysis of the full dataset that changes in abiotic, biotic, and anthropogenic drivers all need to be considered largely holds for plants with different growth forms, for different latitudinal zones, and for both harsher and more benign abiotic environments (as indicated by biome-level NPP). The generality of this result has 4 important ecological and evolutionary implications.

First, when predicting how the distributions and abundances of plant species will respond to climate change, considering only the effects of changes in climatic drivers is not likely to yield accurate predictions. Despite widespread recognition that interspecific interactions may influence distributions, the lion’s share of work to predict how climate change will shift distributions has used species distribution models (SDMs), which typically use only climate variables (less often nonclimate abiotic variables, and only very rarely biotic variables) as predictors of species’ occurrences (refs. 12 and 13, but see refs. 14 and 15). However, if the influence of biotic interactions is substantial, even if lower on average than the influence of climate and other abiotic drivers, then changes in the distributions and abundances of interacting species, which may reflect indirect effects of climate change, species introductions, or other environmental changes, may be just as important to weigh as the direct effects of climate change per se. While this warning has often been made in the ecological literature, our finding that the average effect magnitude of biotic drivers is substantial relative to abiotic drivers makes this warning more poignant, and suggests that changes in biotic drivers cannot be safely ignored, unless we know that biotic and abiotic drivers are tightly correlated and will continue to be so as the environment changes.

While the major driver types exerted similar effects on average, we did see significant differences among driver subtypes (Fig. 1A). Interestingly, within the class of abiotic drivers, climate was less influential than was disturbance (which in our database was mainly fire). Indirect effects of climate change on disturbance frequency (e.g., a reduction in precipitation leading to an increase in fire frequency) or alteration of disturbance by humans may therefore be more important to consider than direct effects of climate change per se (and few SDMs consider disturbance). We also note that climate and natural enemies (primarily herbivores) received the most attention in the studies in our database among the abiotic and biotic drivers, respectively (see numbers at Top of Fig. 1A), but neither were the most influential drivers within its class, suggesting a potential value in altering future research priorities to improve projections of environmental change responses.

A second important implication of our results is that the effect magnitudes of abiotic, biotic, and anthropogenic drivers defy simple hypotheses about when and where one should be stronger than the others. Some evolutionary biologists have argued that biotic forces should impose stronger selection than abiotic forces over the long run because interacting species are also undergoing evolutionary change (16⇓–18), but others have argued that abiotic factors have been more influential as past agents of selection (19), or that humans impose the strongest current impact (ref. 20, but see ref. 21). Darwin (10) argued that biotic forces (in particular, competition and natural enemies) should increase in importance relative to abiotic forces as the low latitude or abiotically more benign range limit of a species is approached, but decrease in importance toward the high latitude or more abiotically harsh range limit. Our results indicate that both abiotic and biotic forces are influential, both in abiotically benign (e.g., at low latitudes and in high NPP biomes) and in seemingly more challenging environments. It may be that latitude and biome are not good proxies for harshness of the abiotic environment, and that a more nuanced treatment of harshness is necessary (as in ref. 11). However, assuming our results hold, perhaps the necessary first step of evolving the ability to tolerate harsh abiotic conditions, both in plants and in interacting species, then sets the stage for biotic forces to become as influential on fitness as are abiotic forces. Similarly, abiotic stress in harsh environments may have preadapted plants to anthropogenic stress, leading to similar effects of all 3 main driver types in such environments. However, interestingly, we did find that plants at middle and high latitudes (Fig. 4) and in less productive biomes (Fig. 5) were more sensitive to drivers of all 3 main types, suggesting that more marginal habitats may increase the influence of all drivers. In contrast, a woody growth form may make plants more resilient on average to changes in all types of drivers (Fig. 3).

A third important implication of our findings is that, because the strength of the impacts of anthropogenic drivers rivals those of abiotic and biotic drivers, we must always consider the possibility that changes in the ways that humans use or manage landscapes will modify or even overwhelm the effects of changes in climate. We did find that anthropogenic drivers had a weaker effect on woody plants than on herbaceous plants (Fig. 2). However, this result is likely due to the fact that harvesting studies of herbaceous plants frequently included lethal harvest of entire plants, but few studies of woody plants did (see SI Appendix). In addition, our database does not include complete destruction of entire populations by humans, as occurs, for example, in conversion of forest to agriculture. Widespread anthropogenic habitat destruction means that effects of humans on biodiversity are certainly even greater than what we show here.

Fourth, that no one driver type (abiotic, biotic, or anthropogenic) is overwhelmingly more influential has 3 important evolutionary implications. First, as all of our estimates of driver effects are based on total fitness (i.e., λ), they may more accurately indicate the importance of potential selective agents than would certain fitness components that might weakly translate into total fitness (e.g., fecundity in long-lived plants). The great majority of the selection estimates in recent metaanalyses (e.g., >98% in refs. 22 and 23) were based upon fitness components rather than total fitness. Second, selection on traits that modulate the fitness effects of the driver should be substantial on average for all of the main driver types. For example, traits that reduce negative effects of climate, traits that reduce herbivory or its impacts, and traits that compensate for harvesting effects should on average experience selection strengths that do not differ greatly. Third, because λ measures mean absolute (not relative) fitness, effects of a driver on λ can alter selection strength even when the driver has equivalent effects on all genotypes, because it affects the variance in relative fitness among genotypes (the so-called “opportunity for selection”) (21, 23⇓⇓–26). Because the magnitudes of the effects of abiotic, biotic, and anthropogenic drivers on mean absolute fitness (and thus on the opportunity for selection) are similar, their indirect effects on the strength of selection on traits that do not directly modulate the impacts of those drivers are also likely to be of a similar order of magnitude (SI Appendix). Caruso et al. (23) found that experimental manipulation of biotic and abiotic factors had equivalent effects on the strength of trait selection, and they showed that selection was stronger when mean absolute fitness was lower, implicating a change in the opportunity for selection. Similarly, Fugère and Hendry (21) argued that anthropogenic disturbance indirectly weakened selection on traits by increasing mean absolute fitness (presumably because the benefits of disturbance outweighed its costs).

Future comparative studies of the effects of different types of drivers on plant population growth and fitness would benefit if demographers measured driver levels along with vital rates (3). For most (57.8%) of the |L| values we used to measure the magnitudes of driver effects, the source papers did not specify an actual level of the driver associated with the 2 λ values, and a majority of the others did not measure the driver mean and SD, thus making it impossible to assess how the difference in driver levels compares to the average and range of variation the plant population might normally experience. This lack of information also limits our ability to extrapolate λ to future driver levels. In addition, most of the original studies did not account for effects of intraspecific density on λ values; relaxation of negative density dependence when driver levels were unfavorable may have reduced driver impacts on λ (27). Therefore, to improve upon the analyses we have presented here, the next generation of demographic studies, both observational and experimental, should invest more effort to actually measure levels of putative drivers and to account for the joint effects of drivers and intraspecific density (for a good example of both, see ref. 28).

In conclusion, our intention in using the best available information to evaluate effects of drivers on plant population growth and fitness was to look both backward and forward in time. Looking backward, we find no evidence to conclude that abiotic forces have been dramatically more or less influential than biotic forces in shaping the plant traits, abundances, and geographical distributions that we see today. Looking forward, our findings make it clear that we must simultaneously account for abiotic, biotic, and (increasingly, given growth in human population size and per-capita resource consumption) anthropogenic forces if we are to accurately forecast the ecological and evolutionary futures of terrestrial plants (and thus ecosystem services such as carbon sequestration in which they play a disproportionate global role).