LARGE-SCALE EXPERIMENTS IN APPLIED ECOLOGY
Two main obstacles in conducting large-scale experiments are valid controls and replication (Diamond 1986). Due to ethical or logistical circumstances, these obstacles are often insuperable. Many studies of plant–herbivore dynamics have been plagued by shortcomings in experimental design, particularly spatial scale (Crawley 1990) and statistical inferences resulting in pseudoreplication (Hurlbert 1984; Brown & McDonald 1995). While in this study an adjacent island served as a large-scale control, the treatment effects at the level of islands were not replicated. Rather, we gain insight and inference by combining the large-scale manipulation with smaller-scale replicated mechanistic experiments (Frost et al. 1988). This integrative approach avoids problematic issues with statistical inference (Hurlbert 1984) and extrapolations from small-scale studies to larger scales (Crawley 1990; Carpenter 1996). The value of this approach is especially apparent in this study. The inevitable lack of replication at the island scale, the conservation objectives outweighing the possibility for additional temporal data collection pre-eradication, and the environmental variance imposed by ENSO-related precipitation make inferences challenging. The combination of large- and small-scale approaches allows for such inferences.
Large-scale experiments are scaled properly for important management issues and thus will play a critical role in resource management in the face of environmental change (Carpenter 1990). An ecosystem approach to conservation and restoration will also play a decisive role (Power 2001; Zavaleta, Hobbs & Mooney 2001). A blend between ecosystem restoration and large-scale experimentalism has much to offer conservation and ecology. The restorationist provides the large-scale manipulation, while the ecologist provides a quantitative assessment of the restoration action. Ecologists exploiting such opportunities to overcome the obstacles of large-scale experiments will greatly benefit pure ecology and environmental problem-solving (Walters & Holling 1990; Ormerod & Watkinson 2000).
EL NIÑO, HERBIVORE RELEASE AND TOP-DOWN EFFECTS
Deserts are stressed environments with low primary productivity and scarce, variable rainfall, and consequently are viewed as pulse-reserve ecosystems regulated by abiotic factors, particularly water availability (Noy-Meir 1973; Evenari, Noy-Meir & Goodall 1985; although see Polis 1991). As a result, ENSO-related precipitation events have large impacts on arid ecosystems (Brown & Heske 1990; Meserve et al. 1999; Jaksic 2001). For example, during the 1992–93 ENSO, Polis et al. (1997) documented dramatic changes on small island communities in the Gulf of California, Mexico (i.e. an increase in mean plant cover from 1% to 40%).
Heavy rain on the San Benito Islands during the 1997–98 ENSO resulted in elevated vegetative cover and diversity (Fig. 2). The germination of annuals resulting from the precipitation dominated plant community structure on both islands early in the study, whereas post-ENSO vegetative changes showed island differences attributable to selective herbivory. On SBE (with herbivores), vegetative cover and diversity declined due to a combination of a return to arid conditions and selective herbivory, while cover and diversity on SBW (herbivores removed) levelled off after an initial decline (Fig. 2). The ENSO rains and the release of herbivory facilitated the germination and growth of select perennials on SBW. For example, following herbivore removal localized flowering patches of the previously rare Malva pacifica were common on SBW. In contrast, rabbits on SBE had almost extirpated this once abundant endemic perennial in less than 3 years (Junak & Philbrick 2000; Fig. 3). The plant community differences at the island scale attributed to selective herbivory are corroborated by the results of the food-preference trials.
Food-preference trials show that the endemic Malva pacifica is overwhelmingly preferred by rabbits. Historically, anecdotal data also suggest a strong herbivore preference for the endemic Dudleya linearis (Moran & Lindsay 1951). Shortly after the introduction of rabbits, Dudleya linearis became increasingly rare, approaching extinction (Donlan et al. 2000). The precipitous decline of Dudleya linearis and Malva pacifica on the San Benito Islands is probably due to the polyphagous but hierarchical diet of rabbits (Crawley 1983; Thompson & King 1994). Rabbits with their catholic diet can switch forage species, permitting an abundant rabbit population despite a decrease in preferred plant species. Despite diet switching, the presence of rabbits prevents new recruitment of preferred species. Suppression of recruitment and subsequent depletion of the seed bank leads towards extinction (Hunt 2001). The results of the food-preference trials, coupled with anecdotal data, lend support to the generalization that herbivores prefer insular endemic plants to non-endemic native species (Carlquist 1974; Bowen & Van Vuren 1997).
The strong relationship between rabbit food preference and changes in plant species cover is evidence of a strong top-down effect on the perennial plant community (Figs 3 and 4). On SBE (with herbivores), the perennial plant community appears to have come under top-down regulation, whereas on SBW (herbivores removed) the community appears to have been released from top-down control. The time series of regression models illuminate this pattern (Fig. 4). By December 1997, rabbits had been present on SBE for 2–3 years. Although their impact on preferred plant species was observable, their herbivory failed to explain the abundance of perennials (Fig. 4). Perennial plant abundances may have been influenced by ENSO precipitation and the short duration of herbivore presence. By July 1998, herbivory shifted perennial plant community structure: preferred plants declined and non-preferred species increased in abundance. The strong inverse relationship between preference and cover was present on SBE for the remainder of the study. On SBW, rabbits had been present for approximately 6 years (by December 1997) and rabbit preference correlated strongly with the abundance of perennial plant species. Following rabbit removal, preferred plants increased and non-preferred species declined in abundance. By July 1999, there was no relationship between preference and plant cover, suggesting a release from top-down control (Fig. 4).
The island-wide vegetation response to herbivore removal (Fig. 2), coupled with the predictable perennial plant species responses (Figs 3 and 4), suggest that the herbivore-induced changes are reversible on the San Benito Islands. However, this evidence of a strong reversible herbivore effect is disparate with the outcome of the exclosure experiments on the control island (SBE). For example, we observed germination of the preferred Malva pacifica on SBW, but not inside the SBE exclosures. In fact, we observed no germination or increase in cover in any of the exclosures despite the release of herbivory. The timing of exclosure construction and the subsequent interaction between top-down and bottom-up processes could explain this difference. It is possible that on SBW, ENSO precipitation and the removal of herbivores synergistically facilitated the germination and survival of Malva pacifica between January and July 1998 (Fig. 3). In contrast, herbivore pressure was high on SBE throughout the ENSO rains and exclosures were not constructed until July 1998, 4 months after any precipitation on the island (Fig. 2). Despite the absence of herbivory inside the SBE exclosures after July 1998, germination did not occur due to lack of water availability (July 1998–July 1999 rainfall = 21 mm). Alternatively, Malva pacifica seed was not present inside the exclosures although this is unlikely, due to the presence of dead plants inside the exclosures, its widespread abundance historically on the island, and a persistent seed bank (B.R. Tershy, personal observation; Kivilaan & Bandurski 1981; Junak & Philbrick 2000). Thus, it appears that while exotic herbivores exhibit a top-down effect on the perennial plant community, recovery after the removal of herbivores may be limited by a bottom-up mechanism (i.e. water availability).
The predictable herbivore impacts and signs of recovery after eradication are indeed short-term and may not forecast the island’s long-term dynamics. The interaction between herbivore and abiotic effects, and subsequent management implications, could be better understood by extending the short-time period of this study. While eradications cannot often be postponed due to conservation priorities, islands with planned eradications can be identified early during planning stages, thus allowing for a longer time series of data collection pre-eradication. Long-term monitoring post-eradication with a sampling interval of a few years will also help to identify the relative importance of biotic and abiotic factors influencing the ecosystem (Brown et al. 2001). Bullock, North and colleagues have followed the ecology of Round Island (Mauritius) for 10 years following rabbit and goat eradication (North & Bullock 1986; North, Bullock & Dulloo 1994; Bullock et al. 2002). Vegetation responses were predictable in the short term, but some long-term changes were dramatic and unpredictable, particularly an increasing influence by exotic plants (Bullock et al. 2002). The undesirable increase in abundance and influence of exotic plants after exotic herbivore removal has also been observed on Carnac Island, Australia (Abbott, Marchant & Cranfield 2000) and the Channel Islands, USA (Halvorson, Fenn & Allardice 1988; Klinger, Schuyler & Sterner 1994). However, the interaction between exotic herbivores and invasive plants remains largely unstudied and examples are mostly anecdotal (Driesche & Driesche 2000). Exotic plants are not present in high abundance on the San Benito Islands, and low, variable, rainfall is likely to play a role [mean exotic cover was less than 3·1% (SBW) and 9·3% (SBE) during all sampling periods]. Arid ecosystems that lack large influences by exotic plants may require less management, from an ecosystem perspective, following exotic herbivore removal, compared with more mesic systems (Donlan 2000).
Exotic herbivores have affected islands for over a century, leading to numerous plant extinctions (Wallace 1892; Melville 1979). Our study demonstrates that introduced herbivores can change plant community structure through selective herbivory. This top-down effect led, in this case, to the increase of unpalatable plants species and the decline of preferred species toward extinction. While top-down effects of herbivores might damage communities rapidly, recovery can depend on the bottom-up effects of resources, such as water availability. In desert ecosystems with low and variable rainfall, island recovery may be delayed by prolonged drought. However, the reduced presence of exotic plants, as found on the arid San Benito Islands, may aid in the recovery towards original pre-disturbance conditions. This study is unique in that we exploited the conservation action of exotic herbivore removal as a large-scale controlled experiment. Large-scale experimental approaches combined with smaller-scale mechanistic experiments, particularly the exploitation of conservation action as a perturbation, might offer useful models in applied ecology more widely.