Linking a cougar decline, trophic cascade, and catastrophic regime shift in Zion National Park

Abstract

The strength of top-down forces in terrestrial food webs is highly debated as there are few examples illustrating the role of large mammalian carnivores in structuring biotic and abiotic systems. Based on the results of this study we hypothesize that an increase in human visitation within Zion Canyon of Zion National Park ultimately resulted in a catastrophic regime shift through pathways involving trophic cascades and abiotic environmental changes. Increases in human visitors in Zion Canyon apparently reduced cougar (Puma concolor) densities, which subsequently led to higher mule deer (Odocoileus hemionus) densities, higher browsing intensities and reduced recruitment of riparian cottonwood trees (Populus fremontii), increased bank erosion, and reductions in both terrestrial and aquatic species abundance. These results may have broad implications with regard to our understanding of alternative ecosystem states where large carnivores have been removed or are being recovered.

Introduction

Humans can have a major role in food web dynamics by displacing or extirpating top predators. Over a half century ago, the iconoclast Aldo Leopold was among the first to argue that elimination of large mammalian predators had strong top-down influences on ecosystems (Leopold et al., 1947). Based on widespread empirical observations in the early to mid-20th century, when large carnivores were being extirpated from significant portions of the United States, Leopold and colleagues suggested that the loss of these carnivores set the stage for ungulate irruptions and ecosystem damage. Perhaps the most notable example was the Kaibab plateau in Arizona (Leopold, 1943, Leopold et al., 1947, Ripple and Beschta, 2005). Widely reported in early biology and ecology textbooks as a lesson in top-down importance, the Kaibab study was more recently deleted from textbooks after alternative hypotheses for ungulate irruptions were suggested (Caughley, 1970, Burke, 1973).

Within only one to two centuries the widespread effects of Euro-American settlement and development across the continental United States resulted in range collapse for most large mammalian carnivore species (Laliberte and Ripple, 2004). Yet, potential long-term cascading effects involving the loss of these large carnivores are largely unknown. A trophic cascade occurs when the presence of a top predator significantly affects consumers and this interaction alters or influences species composition, age structure, or spatial distribution of producers (plants). While current discussions on terrestrial food webs continue to question the relative strength of top-down forcing versus bottom-up controls (Estes, 1996, Pace et al., 1999, Terborgh et al., 1999, Terborgh et al., 2001, Polis et al., 2000, Borer et al., 2005), there is often little consideration beyond tri-trophic cascades, especially concerning potential pathways involving changes in the abiotic environment that could contribute to a loss of habitats, a loss of biodiversity, or regime shifts resulting in alternative states (Schmitz et al., 2006). Catastrophic regime shifts can occur when perturbations dramatically alter ecosystem structure and function (Holling, 1986, Scheffer and Carpenter, 2003). A regime shift typically occurs as a relatively abrupt restructuring of an ecosystem, but with prolonged consequences. The likelihood of a shift to a less desired state is increased when humans remove whole trophic levels (top-down forces), thereby reducing an ecosystem’s capacity to generate services (Folke et al., 2004).

From a theoretical perspective, a major academic debate regarding trophic cascades was initiated when Hairston, Smith, and Slobodkin proposed the Green World Hypothesis, which indicated that predators maintain global plant biomass at high levels by limiting herbivore densities (Hairston et al., 1960). Yet even with recent advances in food web ecology, the debate about the Green World Hypothesis continues due to ongoing disagreement on the frequency and relative role of top-down versus bottom-up forces, as well as a paucity of studies regarding the effects of large mammalian predators on terrestrial vegetation (Pace et al., 1999, Polis et al., 2000, Shurin et al., 2002, Borer et al., 2005).

Ecosystem properties and processes in the presence or absence of large carnivores are not widely understood. For example, there is a lack of controlled, large-scale, and long-term studies of large carnivores, prey, and plant communities. This scarcity of research is attributable to a lack of functional populations of large carnivores, the cost of such studies, the need for relatively large spatial and temporal scales, the difficulty of experimentally manipulating populations of large carnivores, and the problem of separating confounding effects including the role of humans. To date, the vast majority of trophic cascades studies in terrestrial ecosystems have taken place at the scale of meters to hectares involving very small predators over short time periods. This limits the transfer of results to large landscapes, large carnivores, and long time scales (Schmitz, 2005).

A top-down trophic cascades model would predict an increase in consumer biomass and a decrease in producer biomass following predator removal, while the bottom-up model would predict little or no change in consumer or producer biomass after their removal (Ray et al., 2005). In addition to these basic top-down linkages, many other interaction pathways resulting from predator effects are likely, such as increased species interactions, improved nutrient cycling, limited mesopredator populations, and food web support for scavengers (Soulé et al., 2003, Soulé et al., 2005, Côté et al., 2004, Reisewitz et al., 2006). One little known pathway is a linkage from predators to consumers to producers to streambank habitats to species abundance (i.e., how the change in abiotic environment due to trophic cascades affects the occurrence of native species).

Herein we report on a discovery that appears to link the loss of predators to a catastrophic regime shift via trophic cascades (cougar → deer → cottonwoods) and changes in abiotic environmental conditions (channel morphology). We took advantage of an unplanned landscape-scale experiment to document the status of an ecosystem where the presence of a large mammalian predator (cougar) had been greatly diminished in one of two landscape areas within Zion National Park, Utah. While an experimental design that includes spatial control of “predator rare” versus “predator common” areas seldom occurs in large carnivore-trophic cascades research (Terborgh et al., 2001), such a design greatly reduces the potential for confounding interactions associated with climate, natural disturbances, or habitat. An underlying hypothesis of this study is that Fremont cottonwood tree recruitment: (1) has been low in areas where cougars are scarce and mule deer abundant (treatment, Zion Canyon); and (2) has continued to occur in areas where cougars remain common and deer scarce (control, North Creek). Additionally, in the area with a reduced cougar presence, we hypothesized that reductions in riparian trees and other palatable hydrophytic plants caused increases in bank erosion, which in turn contributed to reductions in the abundance of riparian wildflowers, amphibians, lizards, and butterflies. We considered alternative hypotheses that might affect cottonwood recruitment including climate, human interventions to stream channels, and differences in geomorphology and runoff regimes between Zion Canyon and North Creek.