Introduced herbivores restore Late Pleistocene ecological functions

Abstract

Large-bodied mammalian herbivores dominated Earth's terrestrial ecosystems for several million years before undergoing substantial extinctions and declines during the Late Pleistocene (LP) due to prehistoric human impacts. The decline of large herbivores led to widespread ecological changes due to the loss of their ecological functions, as driven by their unique combinations of traits. However, recently, humans have significantly increased herbivore species richness through introductions in many parts of the world, potentially counteracting LP losses. Here, we assessed the extent to which introduced herbivore species restore lost-or contribute novel-functions relative to preextinction LP assemblages. We constructed multidimensional trait spaces using a trait database for all extant and extinct mammalian herbivores ≥10 kg known from the earliest LP (∼130,000 ybp) to the present day. Extinction-driven contractions of LP trait space have been offset through introductions by ∼39% globally. Analysis of trait space overlap reveals that assemblages with introduced species are overall more similar to those of the LP than native-only assemblages. This is because 64% of introduced species are more similar to extinct rather than extant species within their respective continents. Many introduced herbivores restore trait combinations that have the capacity to influence ecosystem processes, such as wildfire and shrub expansion in drylands. Although introduced species have long been a source of contention, our findings indicate that they may, in part, restore ecological functions reflective of the past several million years before widespread human-driven extinctions.

Keywords: functional ecology; invasion; megafauna; novel ecosystems; restoration ecology.

Fig. 1.

Trait space changes resulting from LP extinctions and recent introductions. (A) Species richness per continent. Introductions have numerically replaced lost species richness by between 11% (Asia) and 50% (Australia and Europe). Fill color indicates species fate with the legend shared with C. Inclusive = native + introduced modern assemblages. (B) Global herbivore trait space. Arrows indicate how particular traits shape trait space axes. The first two PCoA axes (∼62% of variation) of trait space are shown (see the SI Appendix, Fig. S1 for PCoA axes 3 and 4). Points indicate species, and the fill density indicates their density distribution with the legend shared with C. (C) Changes in continental trait space (PCoA 1 and 2) from extinctions and introductions. Crosses indicate centroids of the first two PCoA axes. Locally extinct species went extinct within the respective continent but survived elsewhere. Native only = modern native assemblages; inclusive = native + introduced modern assemblages.

Fig. 2.

Change in trait space volume and functional dissimilarity. (A) Difference between native-only and inclusive trait space volumes from the LP volume for each continent. Trait space volume is the four-dimensional volume of each trait space (also known as functional richness). Contractions in trait space volume following LP extinctions (native-only points) have been offset by introductions in inclusive assemblages. The dashed line indicates no change from LP. Native only = modern native assemblages (blue); inclusive = native + introduced modern assemblages (gray). (B) Total functional dissimilarity to the LP, calculated from the overlap of four-dimensional trait spaces. Functional dissimilarity (measured as Sørensen’s β) is composed of two additive components: nestedness is dissimilarity caused by being a subset of another trait space, while turnover is the degree to which assemblages do not overlap (e.g., novelty).

Fig. 3.

Select introduced herbivores and their extinct nearest neighbors in those continents most impacted by extinctions and introductions. The color of the top bar indicates the number of extant species (per body mass bin and climate zone) that are more similar to the nearest neighbor than the introduced species is, while the lower bar color indicates dietary guild. For a full list of pairs see the SI Appendix, Fig. S3.

Fig. 4.

The loss and restoration of key metabolic ecosystem functions. Forty-four percent of introductions restore extinct functional groups, restoring 14 of 51 extinct dietary body mass groups across continents. Body mass groups were determined analytically with the Sturges algorithm, which finds natural breakpoints in continuous distributions. Three species introduce novel groups to Australia and Europe. Points indicate species and are jittered randomly for visualization within each cell.