Are invasive species the drivers of ecological change?.

Invasive species are widely accepted as one of the leading direct causes of biodiversity loss. However, much of the evidence for this contention is based on simple correlations between exotic dominance and native species decline in degraded systems. Although appealing, direct causality is not the only possible interpretation. A plausible alternative hypothesis is that exotic dominance could be the indirect consequence of habitat modification driving native species loss. In a new paper, MacDougall and Turkington now provide the first direct test of whether invasive species are the drivers of community change, or merely ‘passengers’ along for the environmental ride.

The Homogocene

Almost 20 years after Gordon Orians popularized the dawning of the ‘Homogocene’ era, the term has become evocative of an unprecedented global redistribution of species. Non-native species now dominate most landscapes in most parts of the world, owing to the propagation of ‘beneficial’ species and the inadvertent spread of ‘pest’ species by humans. However, as recently as 1996, Peter Vitousek and colleagues considered that even the ecologists and conservation biologists working to control pest invasions were not taking the problem seriously enough, and called for wider recognition of the global consequences of invasions for the loss of biodiversity. There has since been a significant increase in the emphasis placed on invasive species as one of the leading causes of species decline, and biological invasion is now considered to be one of the ‘big five’ environmental issues of public concern. Media attention has engendered considerable hyperbole about the global impacts of invasive species, but there is a growing disquiet among ecologists that the scientific literature has also become rife with uncritical generalizations.

A recent Opinion article in TREE focuses the scientific issues more clearly and questions whether there is strong evidence for invasive species as a direct cause of native species decline. Of central importance is whether the ubiquitous positive correlation between native species decline and invasive species dominance necessarily means that invasive species are the drivers of the observed change. Many invasive species take opportunistic advantage of other forms of ecosystem change, such as habitat disturbance, rather than being the drivers of change themselves. In itself, this observation is nothing new, and similar statements have been echoed in every major review of invasive species impacts in the past ten years. What is important is recognizing that, if we are to better understand the impacts of invasive species and mitigate threats to native species, we must be able to distinguish between different causal mechanisms of population decline. Strong correlations with putative drivers are no substitute for mechanistic discrimination among factors.

Unfortunately, research on the two major recognized drivers of species decline, habitat loss and species invasions, is often approached as though they are independent single-factor problems, rather than factors that interact additively or synergistically. When multiple causal agents of decline are considered, it is usually in a qualitative or conditional sense, rather than in quantitative analyses. Furthermore, even the few invasion studies that do take a mechanistic experimental approach typically have a singular invasion focus, rather than first testing the causal linkages between invasion and habitat disturbance. In this context, a new paper by MacDougall and Turkington brings a decisive and much-needed hypothesis-testing approach to evaluating whether invasive species are the cause of widespread ecological change, or simply a correlate of habitat disturbance by humans.

Invasive species: drivers or passengers of ecological change?

The garry oak Quercus garryana meadows of southwest Canada and northwest USA are a good system in which to tease apart the relative impacts of habitat disturbance and invasion on native species decline. Species invasion has been severe, with 144 naturalized exotic plant species (32% of the regional flora) representing 55–75% of local species richness and 80–90% of biomass. The overwhelming impression is that native species have all but been displaced by invasive species, with the inference being that the invaders are competitively dominant over resident natives. However, anthropogenic habitat alteration covaries strongly with invasion impacts, with only 1–5% of original habitat remaining and a history of long-term fire suppression. Consequently, exotic dominance could have less to do with strong species interactions, such as competitive displacement, than with non-interactive processes, such as relative dispersal ability or altered disturbance regimes that are more limiting for native species than they are for invasive species.

The experimental approach taken to test between these contrasting hypotheses was straightforward. MacDougall and Turkington reasoned that, if interactive processes are responsible for native species decline, then removal of invasive species should result in a direct increase in the richness and relative abundance of native species (the ‘driver’ model). Conversely, if invasive species are not the limiting factor for native species, then eradication should have minimal impact (the ‘passenger’ model).

MacDougall and Turkington established a factorial field experiment examining the impact of biomass reduction (mowing) and complete removal (weeding) of the two dominant exotic grasses, Poa pratensis and Dactylis glomerata (comprising ca. 50–80% total cover), on native plant richness and relative abundance. After three years of treatment imposition, both treatments caused a rapid and persistent decrease in total production and a gradual shift in dominance from perennial grasses to perennial forbs. Most of the compensation was by native forbs already established before experimental treatments, and there was little recruitment of either native or exotic perennial species into plots within three years. In fact, almost half of the resident species showed no change or decreased significantly in percent cover following exotic dominant removal. The recovery of native species dominance predicted by the driver model following invasive species removal did not occur, and the data suggest that the passenger model is the underlying cause of exotic dominance in this system.

Under the passenger model, non-interactive processes, such as inferior dispersal ability and sensitivity to habitat disturbance, are hypothesized to limit native species. The field experiment showed that natural recruitment of native species was negligible over a three-year period. However, to distinguish between recruitment limitation and germination success, a seed addition experiment was performed that showed that native seedling survival (although low) was possible even under heavy exotic cover in control plots, and that survival was significantly enhanced by exotic dominant removal. Similar results from previous studies suggest that recruitment limitation of native species is a more widespread explanation for exotic dominance in degraded systems than is competitive exclusion.

Additive or synergistic effects of habitat disturbance and species invasions

Invasive species can have significant effects on resource availability and can suppress or enhance the relative abundance of native species, without necessarily being the driving force behind community change. In spite of general support for the passenger model, there was evidence that some native species increased significantly in percent cover or productivity following removal of exotic dominants. This implies that the sequestration of light, space and nutrients by P. pratensis and D. glomerata did limit growth for these species. If we interpret this as some form of cause and effect relationship (whether direct or indirect), then it points more toward an ‘interacting drivers’ explanation than a strict interpretation of the passenger model would suggest. It is probably more realistic to consider the driver and passenger models as extreme cases of a general model incorporating additive or synergistic effects of the two factors, with the relative importance of invasive species and habitat disturbance varying between species and between ecosystems. For example, in Hawai'i, Petren and Case found experimental evidence that direct exploitation competition by the invasive gecko Hemidactylus frenatus caused population decline in the native gecko Lepidodactylus lugubrus, but only in the context of altered resource distributions (increased clumping of insect prey) that occurred following anthropogenic habitat disturbance.

MacDougall and Turkington make the interesting observation that there are also positive impacts of exotic dominant grasses in garry oak meadows. Most importantly, P. pratensis and D. glomerata dominance appears to maintain the open savannah structure that is so characteristic of garry oak ecosystems by inhibiting succession to exotic woodland. Of course, this same role would probably be performed by functionally equivalent native perennial grasses if they were not so dispersal limited relative to the exotic dominants. Nevertheless, dominance by exotic perennial grasses does appear to be the lesser of the two evils. Furthermore, P. pratensis and D. glomerata might also act as ‘nursery plants’, which enhance the survival of native seedlings if aboveground exotic biomass is reduced by mowing in autumn. In combination with the overall conclusion that native seed supply is limiting ecosystem recovery, these results present obvious management prescriptions for restoring native dominance in garry oak meadows.

Limitations on a small-scale experimental approach

There are several limitations on experimental demonstration of invasive species impacts. First, not all invasive species, or invaded ecosystems, are amenable to experimental manipulation. Although manipulative experiments can typically provide greater mechanistic understanding of the drivers of ecological change, judicious use of comparative quantitative data can also be powerful in testing the degree of intercorrelation among multiple drivers. For example, Farnsworth found that the decline of rare native plants across New England, USA, was determined by the same habitat disturbance and site management variables that were associated with invasive species presence, rather than by the presence of invasive species alone.

Second, even when systems can be manipulated, an inherent limitation of any small-scale experiment is the inability to detect the historical drivers of ecological change in situations where the system has been irreversibly altered. For example, invasive species might alter disturbance regimes and cause an ecosystem to shift to an alternative stable state, yet it might not be possible to detect this driving role because invasive species removal does not result in ecosystem recovery. Third, when three or more drivers of ecological change are acting in concert, the direct and indirect linkages among factors might be too complex to test experimentally. In all of these cases, discriminating among potential drivers of species decline will require a combination of approaches incorporating quantitative empirical data, experimentation and structural equation modelling, such as path analysis.

Prospects

Although the generality of the passenger model as an explanation for exotic dominance in degraded systems is highly contentious in its own right, in many respects it is not the overall conclusions of MacDougall and Turkington that are the most important contribution of their paper. After all, the ultimate causes of population decline are species specific and context dependent, and there will be other systems in which the driver model is more applicable. Instead, the real value of their paper lies in the fact that they raised testable hypotheses to discriminate among different explanatory models in the first place. Their study highlights the need for a greater awareness of the interactions among multiple drivers of species loss and greater scientific rigour in assessing the mechanistic causes of population decline.