Introduced Predators Transform Subarctic Islands from Grassland to Tundra
The collapse of the fur trade in the late 19th and early 20th centuries resulted in the introduction of foxes to >400 Alaskan islands as an additional fur source. However, several islands remained fox free from failed introductions or attempts at introductions were never made. As a result, these islands provided a natural setting for a large-scale experiment to evaluate the effects of exotic predators on ecosystems. It was observed that the introduction of foxes had large impact on the seabird populations. The authors of this paper attempt to further this understanding by investigating the role of seabird populations on islands with and without foxes on soil and plant nutrients.
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Top predators often have powerful direct effects on prey populations, but whether these direct effects propagate to the base of terrestrial food webs is debated. There are few examples of trophic cascades strong enough to alter the abundance and composition of entire plant communities. We show that the introduction of arctic foxes (Alopex lagopus) to the Aleutian archipelago induced strong shifts in plant productivity and community structure via a previously unknown pathway. By preying on seabirds, foxes reduced nutrient transport from ocean to land, affecting soil fertility and transforming grasslands to dwarf shrub/forb-dominated ecosystems.
Nearly half a century ago, Hairston et al. (1) proposed that plant productivity and composition were influenced by apex predators through cascading trophic interactions. According to their “Green World” view, the direct effects of predators on herbivore populations transcend multiple trophic levels indirectly to enhance plant community productivity and biomass. Despite great progress in food web ecology, the indirect effects of top predators on vegetation dynamics in terrestrial systems remain unresolved and actively debated (2–6). Compelling demonstrations of multitrophic predator impacts on entire plant communities are scarce, in part because the spatial and temporal scales necessary to perform the appropriate community-wide experiments are daunting.
The introduction of predators to islands provides an opportunity to explore the indirect effects of predators on vegetation. Introduced predators commonly have devastating direct effects on their prey (7). The histories of these introductions are often well known, and the relative simplicity and isolation of insular systems facilitate the study of whole-community responses. Here we investigate how the introduction of arctic foxes (Alopex lagopus) to the Aleutian archipelago affected terrestrial ecosystems across this 1900-km island chain.
The Aleutian archipelago is a remote series of physically similar volcanic islands extending westward from the Alaska Peninsula (Fig. 1). The archipelago currently supports 29 species of breeding seabirds, together numbering >10 million individuals (8). Seabirds deliver nutrient-rich guano from productive ocean waters (9) to the nutrient-limited plant communities (10, 11). Historically, seabirds inhabited most islands along the Aleutian chain. Following the collapse of the maritime fur trade in the late 19th and early 20th centuries, foxes were introduced to >400 Alaskan islands as an additional fur source (12). The introduced foxes severely reduced local avifaunas, especially seabirds (13). However, several islands remained fox free, either because introductions failed or were not undertaken (12–14). Hence, a large-scale natural experiment to evaluate the effects of exotic predators on insular ecosystems was unwittingly initiated more than a century ago. We use this experiment to show how differing seabird densities on islands with and without foxes affect soil and plant nutrients; plant abundance, composition, and productivity; and nutrient flow to higher trophic levels. These determinations were based on contrasts among 18 islands (9 with foxes and 9 fox free) (Fig. 1) that were matched as carefully as possible for size and location in the archipelago (12).
A geographical information system (GIS) was used to superimpose spatially explicit grids over maps of each island. All islands were sampled at the completion of the growing season (August) between 2001 and 2003. We established a 30 m by 30 m plot at each of the grid crosspoints (12 to 32 per island, depending on island size) (12), within which we sampled plant species presence and cover; aboveground plant biomass; total soil N, P, and δ15N; and %N and δ15N from a common grass (in most cases Leymus mollis but in some instances Calamagrostis nutkanensis) and forb (Achillea borealis) (12). At each island, we also haphazardly sampled δ15N in at least five individuals from a diverse group of terrestrial consumers, including a mollusk (Deroceras laeve), arachnid (Cybaeus reticulates), dipteran (Scathophaga impudicum), and passerine bird (Lapland longspurs, Calcarius lapponicus, and song sparrows, Melospiza melodia). δ15N was measured to determine the degree to which nitrogen-based nutrients were marine derived. Soils and organisms that obtain their N from locally fixed sources have lower δ15N values than those that obtain their N from higher trophic levels, such as marine fish and zooplankton (15, 16).
Breeding seabird densities were almost two orders of magnitude higher on fox-free than on fox-infested islands (Fig. 2B) (Mann-Whitney rank sum, T = 36, P < 0.001) (12). We estimate that this reduction in seabird abundance translates to a decline in annual guano input from 361.9 to 5.7 g m–2 (median values; T = 42, P = 0.005) (12). The resulting difference in marine nutrient input is reflected in soil fertility. Total soil phosphorus on fox-free islands was more than three times that on fox-infested islands (Fig. 2C) (F1,16 = 8.01, P = 0.012) (12). Although seabird colonies are often concentrated on the perimeter of islands, guano-derived nutrients can be broadly redistributed across islands and not solely concentrated within the colonies (17).
The different soil fertilities between fox-free and fox-infested islands corresponded with strong shifts among island types in the biomass and nutrient status of terrestrial plants, as well as overall composition of the plant community (Figs. 2, A to D, and 3A). Grass biomass was almost a factor of 3 higher (Fig. 2E) (F1,15 = 10.58, P = 0.005), shrub biomass was a factor of 10 lower (0.48 ± 0.31 versus 4.95 ± 0.84 g m–2; F1,15 = 19.97, P < 0.001), and the nitrogen content in grasses and forbs was significantly greater on fox-free versus fox-infested islands (Fig. 2, F and G) (F1,16 = 8.28, P = 0.01 and F1,13 = 12.51, P = 0.004 for grasses and forbs, respectively). Plant communities on fox-free islands were graminoid dominated, whereas those on fox-infested islands had a more equitable distribution of graminoids, shrubs, and forbs (Fig. 2D).
†15N measures from soils, plants, and consumers all indicate that fox introductions reduced nitrogen input from sea to land. δ15N was significantly greater in soils from fox-free islands compared with fox-infested islands (Fig. 3B) (F1,16 = 14.07, P = 0.002). Similar patterns in δ15N between fox-free and fox-infested islands were evident in grasses, forbs, mollusks, passerines, dipterans, and arachnids (Fig. 3B). These findings demonstrate that fox-free islands are strongly subsidized by marine-derived nutrients, which in turn assist in fueling the ecosystem at higher trophic levels.
To test whether differences in the magnitude of nutrient subsidies transported by seabirds onto fox-free versus fox-infested islands could have produced the observed differences in plant communities, we conducted a fertilization experiment on a large fox-infested island. Experimental nutrient additions to a community representative of fox-infested islands over 3 years caused a 24-fold increase in grass biomass (24.33 ± 6.05 g m–2) compared with control plots (0.51 ± 0.38 g m–2 increase; two-factor analysis of variance, F1,20 = 23.96, P < 0.001) and a rapid shift in the plant community to a grass-dominated state. In fertilized plots, grass increased from 22 (±2.7%) to 96 (±17.3%) of total plant biomass, whereas grass biomass in control plots was relatively unchanged (11.4 ± 3.0% and 12.1 ± 1.2% of total biomass at the start and end of the experiment, respectively) (12). In a parallel experiment (18), we disturbed and fertilized plots to mimic the effects of both seabird burrowing and guano addition. Here we found that disturbance negatively rather than positively affected grass biomass; the effects of fertilization alone were far greater than the joint effects of disturbance and fertilization. These results confirm the importance of nutrient limitation in these ecosystems and establish that nutrient delivery in the form of seabird guano is sufficient to explain observed differences in terrestrial plant communities between islands with and without foxes.
In total, our results show that the introduction of foxes to the Aleutian archipelago transformed the islands from grasslands to maritime tundra. Fox predation reduced seabird abundance and distribution, in turn reducing nutrient transport from sea to land. The more nutrient-impoverished ecosystem that resulted favored less productive forbs and shrubs over more productive grasses and sedges.
These findings have several broad implications. First, they show that strong direct effects of introduced predators on their na“ve prey can ultimately have dramatic indirect effects on entire ecosystems and that these effects may occur over large areas—in this case across an entire archipelago. Second, they bolster growing evidence that the flow of nutrients, energy, and material from one ecosystem to another can subsidize populations and, importantly, influence the structure of food webs (19–21). Finally, they show that the mechanisms by which predators exert ecosystem-level effects extend beyond both the original conceptual model provided by Hairston et al. and its more recent elaborations (22). Trophic cascades (23, 24) have traditionally been thought to involve a series of strictly top-down interactions, where predators, by affecting herbivore populations and altering the intensity of herbivory, ultimately influence plant production at the base of food webs (25). Our work illustrates that predators, by thwarting the transport of nutrients between systems, can have powerful indirect effects on systems via a route different from that of classic trophic cascades. The impact of highly mobile predators and their prey on the transport of materials between ecosystems remains poorly understood. Because few ecosystems support food webs that are undisturbed either through introductions or extirpations, it may be that the all-too-common addition or deletion of predators from systems have had substantial but largely unexplored effects.
Supporting Online Material
SOM References and Notes
References and Notes
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- We thank S. Buckelew, S. Elmendorf, and the Fox/Seabird field teams for field assistance; K. Bell and crew of the M/V Tiglax for ship support; and S. Talbot, J. Williams, and the Alaska Maritime National Wildlife Refuge for advice and logistical assistance. R. Ostfelt, J. Kitchell, T. Martin, D. Pearson, R. Callaway, and R. Holt provided important comments on the manuscript. Supported by NSF OPP-9985814 (J.A.E. and D.A.C.) and NSF OPP-0296208 (J.L.M.).