Trophic consequences of terrestrial eutrophication for a threatened ungulate

Abstract

Changes in primary productivity have the potential to substantially alter food webs, with positive outcomes for some species and negative outcomes for others. Understanding the environmental context and species traits that give rise to these divergent outcomes is a major challenge to the generality of both theoretical and applied ecology. In aquatic systems, nutrient-mediated eutrophication has led to major declines in species diversity, motivating us to seek terrestrial analogues using a large-mammal system across 598 000 km² of the Canadian boreal forest. These forests are undergoing some of the most rapid rates of land-use change on Earth and are home to declining caribou (Rangifer tarandus caribou) populations. Using satellite-derived estimates of primary productivity, coupled with estimates of moose (Alces alces) and wolf (Canis lupus) abundance, we used path analyses to discriminate among hypotheses explaining how habitat alteration can affect caribou population growth. Hypotheses included food limitation, resource dominance by moose over caribou, and apparent competition with predators shared between moose and caribou. Results support apparent competition and yield estimates of wolf densities (1.8 individuals 1000 km^-2) above which caribou populations decline. Our multi-trophic analysis provides insight into the cascading effects of habitat alteration from forest cutting that destabilize terrestrial predator-prey dynamics. Finally, the path analysis highlights why conservation actions directed at the proximate cause of caribou decline have been more successful in the near term than those directed further along the trophic chain.

Keywords: apparent competition; boreal; food webs; global change; path analysis; woodland caribou.

Figure 1.

Wolf survey units (WSU) used to evaluate the relationship between productivity, moose density, wolf density and caribou population growth rates in the boreal forest of western Canada. The colour gradient represent the per cent anthropogenic habitat alteration. Light grey shading is boreal caribou range, and dark grey shading represents focal areas where caribou demographic data were collected. Numbers for each WSU correspond to the raw data labels in GitHub (https://github.com/ctlamb/borealcaribou-pathanalysis/blob/master/data/final.csv). (Online version in colour.)

Figure 2.

Directed acyclic graphs displaying six hypothesized ecological pathways impacting caribou λ. A, Habitat alteration leading to food limitation; B, habitat alteration leading to increased predator vagility; C, resource dominance of moose over caribou; D, apparent competition; E, apparent competition combined with food limitation; F, increased productivity benefitting caribou and moose. Vegetation represents our estimate of primary productivity (ΔEVI), moose and wolves are densities, caribou refers to λ, and habitat alteration is the percentage area covered by anthropogenic habitat alteration. For (C, D and F), the link from habitat alteration to vegetation was estimated as part of separate analyses (figure 3 and electronic supplementary material, appendix S2).

Figure 3.

Vegetation index (ΔEVI) time series before and after habitat alteration from forest harvesting. Vertical line denotes the year of alteration. Error bars show 95% CIs based on 500 bootstrapped samples. A mixed model with each cut block as the random slope predicts 35.6% (s.e. = 0.27) greater ΔEVI post logging. (Online version in colour.)

Figure 4.

Bivariate relationships included in the path analyses (figure 2). Note that the top performing model includes panels (b), (c) and (d) (table 1 and figure 5) which describe apparent competition (model D, figure 2). Caribou population growth refers to λ values, and the horizontal dashed line represents a stable population where λ = 1. Pairwise relationships among all variables are in the electronic supplementary material, figure S1-1.

Figure 5.

Results of the path analysis used to explain ecosystem dynamics. (a) Relative support for each pathway based on 1000 bootstrapped samples, top path (ΔAICc = 0) retained from each run. (b) Strength (R² shown along the path, with standardized coefficients in brackets) and direction of relationships for top model identified in (a). The dashed line represents a link estimated as part of separate analyses (figure 3 and electronic supplementary material, appendix S2). (Online version in colour.)