Indirect effects of parasites in invasions

Recent research emerging from the Global Invasions Network increases our understanding of the subtle but important role of parasites in invaded communities through density mediated and trait mediated indirect effects. The extent to which eco-evolutionary dynamics will shape the adaptive landscape of both native and invasive species in these communities as yet remains unknown.

One of the most dramatic and long-lasting effects of humans on the natural environment is the global spread of non-native species. As is well known, the astounding demographic success of non-native biological invaders has had dramatic effects on ecological communities and is considered a major driver of global losses of biodiversity, second only to degradation and destruction of habitat due to human development according to the International Union for the Conservation of Nature (IUCN). As biological invasions play a central role in the global environmental crisis, the global spread of species has significant consequences for contemporary ecological processes and can also fundamentally alter evolutionary trajectories, not only for native communities, but for the invaders themselves. Considering biological invasions under an eco-evolutionary framework is critical, as it can provide important insights providing a more complete understanding of the causes and consequences of biological invasions in this globalized ‘brave new world’ we’re heading toward that will have, effectively, a single continent: Neo-Pangea.

Recognizing the need to understand the ecological and evolutionary implications of biological invasions on a global scale, an international consortium of scientists convenes under the banner of the Global Invasions Network (GIN), a Research Coordination Network (RCN) funded by the NSF (PI’s: Ruth Hufbauer, Associate Professor at Colorado State and Mark Torchin, staff scientist at the Smithsonian Tropical Research Institute, in Panama). The 2011 GIN meeting in Panama City, Panama, generated some exciting new ideas about the effects of parasites in invasions. Over the past year, I’ve been involved in a working group that emerged out of this GIN meeting, chaired by Alison Dunn and Sarah Perkins, to consider various ways – some rather non-obvious – in which parasites can affect biological invasions.

Parasites are known to strongly influence the success of biological invasions across taxa, since parasite infection (or the absence thereof) can affect both native and invading species. The most obvious impact that parasites have on shaping the ecology and evolution of invaded systems is through direct effects on their hosts, but parasites also have widespread density and trait mediated indirect effects on other species, whether competitors, resources, consumers, or other parasites that interact with a given host that mediate the impact and success of invasion. These indirect effects include both density-mediated effects, resulting from decreases in host survival and reproduction, and trait-mediated indirect effects that result from changes in host life history traits, physiology and behavior. In a review recently published in Functional Ecology (Dunn et al. 2012), we considered the importance of these density- and trait-mediated indirect effects of parasites on the success of biological invasions, and discussed the extent to which these effects scale up to the community and ecosystem levels through the process of invasion. The extent to which parasites affect the eco-evolutionary dynamics of native and invasive species is as yet unknown, but provides exciting opportunities for empirical and theoretical research by identifying the mechanisms by which infectious processes shape the adaptive landscape in invaded systems and the traits that are likely under strong selection. Here I will draw on several examples in the review that illustrate how understanding the indirect indirections of parasites in invaded systems clearly generates natural experiments for evolutionary biology.

Parasites can affect competitive interactions between native and introduced species, which can facilitate the success of invasion by shifting the competitive balance in favor of the invasive species through density mediated indirect effects. For example, the invasive Pox virus, which is not highly virulent to the invasive grey squirrel (S. carolinensis), spills over from the grey squirrel to the native red squirrel (Sciurus vulgaris), which suffers high levels of mortality due to the virulent infection of this invasive pathogen. Theoretical models predict that parasites therefore increase the competitive replacement of red squirrels by the invader (Tompkins White & Boots 2003). Competitive interactions can also be affected by trait mediated indirect effects, affecting both the behavior and physiology of competing species that facilitates the success of invasion. The native ant, Solenopsis geminata) adopts a defensive behavior in the presence of a native phorid parasitoid, Pseudacton browni, that causes a very significant decline in their foraging rates. However, the behavior of the invasive ant, S. invicta, is less affected by the parasitoid, and can usurp available resources, increasing their competitive ability (Morrison 1999). Competitive interactions with invasive species can impose strong selection pressure on native species. Yet as these examples demonstrate, these competitive interactions are mediated by density mediated and trait mediated indirect effects of parasites. Using an eco-evolutionary approach to understand the consequences of these parasitic interactions can generate a framework for predicting how native communities will respond to the impacts of the parasite to mediate the selection strength of the competitive interaction with the invasive species.

Parasites can also increase the demographic success and ecological impact of an introduced species through trait mediated indirect effects on potential resources. For example, a native spionid polychaete (Polydora sp.) weakens the structural integrity of native whelks’ (Nucella lapillus) shells, which broadens the size range of individuals that can be preyed upon by the invasive green grab (Carcinus maenas). By amplifying the resource base of the invasive crab, polychaete infection thus increases both the ecological impact and success of the invasive crab (Fisher 2010). If predation by the invasive green crab imposes strong selection pressure on the whelk population, we can predict an evolutionary response for resistance to the polychaete, or the development of a thicker shell, in order to mediate the impact of infection which increases the ecological impact of the invasive predator. Examples from the plant literature also demonstrate that parasites of resources can increase the ecological impact of invasion through indirect effects on host physiology. For example, an invasive scale insect, Cryptococcus fagisuga, attacks the native American beech Fagus grandifolia, causing mechanical damage to the tree that facilitates infection by an emerging fungal pathogen, causing significant populating declines in the beech across the United States (Kenis et al. 2009). In a similar manner, the invasive bark beetle, scolytus multistriatus, burrows into the elm tree, Ulmus americana, transporting the invasive fungi, Ophiostoma ulm & O. novo-ulmi, which cause Dutch elm disease. This pathogen has caused significant losses (>50%) to elm trees in North America, changing both the community composition and structure of elm forests in North America. By imposing strong selection pressures on elm populations, the bark beetle and the fungal pathogen have the potential to induce an evolutionary response from the elm to resist the impact of either the beetle or the fungus.

Parasites can impose strong selection pressures on affected species, stronger yet if parasites increase the success and impact of invasive species. Ultimately, we need to integrate eco-evolutionary dynamics into investigations of invaded communities to generate a predictive framework of the causes and consequences of biological invasions. Recent investigations elucidate both the direct and indirect effects of parasites in mediating the impacts of invasion. By identifying the underlying processes by which parasites affect the process of invasion through density and trait mediated indirect effects, we may identify traits that are under strong selection, are likely to generate an eco-evolutionary response, and ultimately shape the adaptive landscape in invaded communities.

Dunn, Alison M.; Torchin, Mark E.; Hatcher, Melanie J.; Kotanen, Peter M.; Blumenthal, Dana M.; Byers, James E.; Coon, Courtney A. C.; Frankel, Victor M.; Holt, Robert D.; Hufbauer, Ruth A.; Kanarek, Andrew R.; Schierenbeck, Kristina A.; Wolfe, Lorne M.; Perkins, Sarah E.. 2012. Invasions and Infections: Indirect effects of parasites in invasions. Functional Ecology. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2435.2012.02041.x/full