Trophic Cascades and Disease Ecology

Appendices

Introducing the Trophic Vortex: Response to Stapp

A cascade is reminiscent of falling water, so it’s natural to envision a “trophic cascade” as a sort of top-down process. But must we always place primary producers near the bottom of the cascade? It’s a bit of an accident that a top-down process is defined in ecology as one directed by species at “higher” trophic levels, such as predators, that impact species on “lower” trophic levels, such as primary producers. The tradition of placing primary producers among the “lower” trophic levels reflects both their fundamental role in ecosystems, as well as the predominantly terrestrial perspective of most ecologists, in which productivity tends to spring upward from ground level.

In practice, it is often more illustrative to place primary producers near the top of a trophic diagram. This is especially true when the intent is to emphasize impacts of primary production on other trophic levels for an audience that tends to read from top to bottom. We considered this issue when developing a diagram to illustrate what has been termed, up to now, the trophic-cascade model for plague (Fig. 1 from Collinge et al., 2005, reproduced in part here as Fig. 1a). The intent of this diagram was to illustrate, vividly and explicitly, the assumptions underlying previous plague models associated with the trophic-cascade terminology (Parmenter et al., 1999; Enscore et al., 2002). Given this diagram, no one can be misled regarding our definition of a trophic cascade.

In this case, as in many others, the definition of a familiar and evocative term has been expanded to serve a broader purpose to which it is pre-adapted. It seems almost inevitable that the definition of a trophic cascade would be broadened to include any one-way chain of impacts among species on several trophic levels. An alternative approach would be to define a new term like “trophic upwelling” that could be used explicitly for processes originating in the “lower” trophic levels. But that approach just leads to the proliferation of specialized, idiosyncratic jargon.

On the other hand, it is clear that a new term is warranted to describe the potentially complex interactions between the plague pathogen and its environment. Like all models, Figure 1a focuses on only a fraction of the potential interactions. If the keystone effects of both a pathogen and its host are considered, the potential for trophic feedbacks can lead to very complex dynamics (Collinge et al., in press). We need a term that can evoke the potential “feedbacks between the structure of prairie communities and the potential for plague to structure those communities” (Ray and Collinge, 2006). In Figure 1b, we extend the trophic diagram for plague to include effects of the disease on prairie dogs, and effects of prairie dogs on primary and secondary productivity. The result suggests a trophic vortex in which plague can be fueled, or fizzle, depending on the relative strength of the trophic cycles involved.

Figure 1.

Hypothesized trophic cascade (a) and potential trophic feedbacks (b) associated with sylvatic plague in prairie communities. Effect signs represent dominant hypotheses or results drawn from the literature. Note that although prairie dogs reduce the amount of above-ground plant biomass, their “mowing” activities can actually increase primary productivity. Longer-term feedbacks may develop resulting from effects of community structure on the potential for re-invasion of both prairie dogs and plague, following local epizootics and extinction. Outcomes should depend on the relative strength and frequency of each effect.

By the way, we would define a trophic vortex quite generally, as a network of trophic interactions capable of episodes of positive feedback. This broad class of dynamics may or may not lead to an “extinction vortex” (Gilpin and Soulé, 1986), and certainly encompasses both clockwise and counter-clockwise cycles!

CHRIS RAY AND SHARON K. COLLINGE

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309-0334. Email: cray@colorado.edu, Sharon.Collinge@colorado.edu

Acknowledgments

This research was supported by a grant from the NSF/NIH joint program in Ecology of Infectious Diseases (DEB-0224328).

References

• 1. Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully JF Jr, Gage KL, Kosoy MY, Loye JE, Martin AP (2005) Testing the generality of a trophic-cascade model for plague. EcoHealth 2:1–11

• 2. Collinge SK, Ray C, Cully JF Jr. (in press) Effects of disease on keystone species, dominant species, and their communities. In: Effects of Ecosystems on Disease and of Diseases on Ecosystems, Ostfeld RS, Eviener VT, Keesing F (editors), Princeton, NJ: Princeton University Press, New York

• 3. Enscore RE, Biggerstaff BJ, Brown TL, Fulgham RE, Reynolds PJ, Engelthaler DM, et al. (2002) Modeling relationships between climate and the frequency of human plague cases in the southwestern United States, 1960–1997. American Journal of Tropical Medicine and Hygiene 66:186–196

• 4. Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinction. In: Conservation Biology: The Science of Scarcity and Diversity, Soulé ME (editor), Sunderland, MA: Sinauer, pp 19–34

• 5. Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL (1999) Incidence of plague associated with increased winter-spring precipitation in New Mexico. American Journal of Tropical Medicine and Hygiene 61:814–821

• 6. Ray C, Collinge SK (2006) Potential effects of a keystone species on the dynamics of sylvatic plague. In: Disease Ecology: Community Structure and PathogenDynamics, Collinge SK, Ray C (editors), Oxford University Press, pp 202–216