454 Review TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 Viewing invasive species removal in a whole-ecosystem context Erika S. Zavaleta, Richard J. Hobbs and Harold A. Mooney Eradications of invasive species often have striking positive effects on native increasingly complex. Major damage caused by long- biota. However, recent research has shown that species removal in isolation established invaders, systems that are affected by can also result in unexpected changes to other ecosystem components. These multiple invaders, and systems that are affected by secondary effects will become more likely as numbers of interacting invaders both invaders and other global changes are now increase in ecosystems, and as exotics in late stages of invasion eliminate common. In these settings, straightforward deployment native species and replace their functional roles. Food web and functional role of standard eradication tools, such as poisons, trapping frameworks can be used to identify ecological conditions that forecast the and mechanical harvesting, might not accomplish the potential for unwanted secondary impacts. Integration of eradication into a desired level of recovery of native ecosystems5. holistic process of assessment and restoration will help safeguard against We suggest that, although there is a crucial need for accidental, adverse effects on native ecosystems. the continued development and application of effective eradication methodologies, a parallel need exists to Invasive alien species interact with other elements of place these methodologies in the context of the overall global change to cause considerable damage to ecosystem that is being managed. Ideally, there should managed and natural systems and to incur huge costs be both: (1) pre-eradication assessment, to tailor to society1. In response, several measures have been removal to avoid unwanted ecological effects; and developed and deployed to control, contain or (2) post-removal assessment of eradication effects, on eradicate a wide range of invasive species in affected both the target organism and the invaded ecosystem. areas. Where possible, ERADICATION (see Glossary) is The requirements for successful removal of an the favored approach. Control, which reduces the invader have been discussed recently2. We focus on presence of the invader, and containment, which the possible impacts that result from the successful limits further spread, both require indefinite removal of invasive species, regardless of the methods investments of time, tools and money to keep an employed to remove them. We reviewed recent invader at bay. Although eradication can require large literature for examples where the successful short-term investments, successful removal can be eradication of invasives had or was likely to have achieved within months or years and gives the best important secondary impacts, a task that was made chance for native biodiversity to recover. difficult by the relatively few verified eradication The results of eradication efforts so far are successes that included the monitoring of post- encouraging and have been detailed recently2. Many removal system behavior. case studies demonstrate success for a range of taxa, particularly on small islands and at local scales. Eradication: what can go wrong Additional examples include the removal of the exotic Successful eradication efforts have generally benefited little red fire ant Wasmannia auropunctata from biological diversity. However, there is also evidence that, Santa Fe Island in the Galapagos3 (which resulted in without sufficient planning, successful eradications can the increase in density of several native ant species), have unwanted and unexpected impacts on native and the nearly complete removal from Laysan Island, species and ecosystems. These inadvertent impacts are of Hawaii of the exotic annual grass Cenchrus many types. Excessive poisoning of non-target organisms echinatus, which once covered 30% of the vegetated and transfer of poisons up food chains6 are problems that area of the island (E.N. Flint, unpublished). can result from the removal method used7,8. Some Successful eradications often lead to dramatic eradication efforts fail because they do not eliminate the recovery of native species and ecosystems. Removal of target organism, because they either miss individuals or Erika Zavaleta* introduced rabbits from Pacific islands off Mexico do not include steps to reduce post-eradication Harold A. Mooney (C.J. Donlan, unpublished) and the USA have allowed susceptibility to reinvasion3. Eradication alone might not Dept of Biological recovery of two rapidly declining endemic species of allow ecosystems to recover, because some invaders Sciences, Stanford 4 University, Stanford, native succulents Dudleya linearis and D. traskiae . change the condition of the habitat so as to render it CA 94305, USA. Lowland vegetation on Santa Fe Island has recovered unsuitable for native species. For instance, in sites from *e-mail: steadily following the removal of exotic goats Capra the Middle East to the western USA, high soil salinity is [email protected] hircus nearly 30 years ago. caused by the invasive ice plant Mesembryanthemum Richard J. Hobbs However, other cases suggest that more refined and crystallinum, and tamarisk Tamarix spp., which makes School of Environmental integrated approaches to invasive removal could it difficult for salt-sensitive native species to re-establish9. Science, Murdoch University, Murdoch, improve results. Successes are still largely confined to In these cases, eradication must be followed by additional WA 6150, Australia. small islands. The ecological context of eradication is site restoration. http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02194-2 Review TRENDS in Ecology & Evolution Vol.16 No.8 August 2001 455 increases in exotic plant populations. Removal of one Box 1. When a harmful exotic harbors an endangered native species invader can lead to increased impacts of another invader; for example, when removal of exotic prey Exotic saltcedar Tamarix spp. shrubs have replaced much of the native riparian leads to increased predation on native prey by exotic vegetation of the arid western USA, where they consume large quantities of predators10. Finally, removal of invasive plant species water, narrow river channels, salinize soil and degrade wildlife habitata. can reduce habitat or resources available for native Saltcedar removal has been repeatedly delayed in parts of its range fauna if the removal is not accompanied by further because it provides significant nesting habitat for an endangered native restoration measures (Box 1). These unexpected songbirdb. The southwestern willow flycatcher Empidonax trailii extimus, outcomes will become more probable both as the currently reduced to fewer than 500 breeding pairs, nested historically in variety of interacting invaders contained in an riparian cottonwood (Populus spp.)–willow (Salix spp.) stands in the ecosystem increases, and as exotics in late stages of southwestern USA (Refs c,d). Urbanization, agriculture, fire, water invasion largely or wholly eliminate native species diversion and livestock grazing all contributed to the decline of its native and replace their functional roles. Although habitatb. The replacement of much of the habitat that remained by saltcedar researchers have begun to explore the implications of required the flycatcher to make use of the invader, which it seems to prefer multiple, interacting invaders, little attention has in some areas, despite its reduced breeding successe,f. been paid to the implications of these interactions for Stepwise saltcedar removal could strongly benefit the flycatcher by giving eradication efforts. native trees the opportunity to re-establish and provide replacement habitatg. However, some saltcedar-invaded areas might no longer be able Secondary effects: a conceptual framework to support native vegetation, because lowered water tables and saline A useful basis from which to tackle when and why soils, the results of saltcedar dominance, might complicate native secondary effects of eradication occur is that systems re-establishmenth–j. Region-wide flood suppression hinders containing invasives function according to the same re-establishment of flood-associated native species such as cottonwoods basic principles as do other systems. Invaded systems and increases the likelihood of saltcedar reinvasionj,k. can, therefore, be considered using the frameworks Managers are confident that, if accompanied by planning and careful that are usually used to analyze community and restoration, saltcedar removal can benefit the endangered flycatcher as well ecosystem dynamics. as other native speciesg. However, poorly planned removal without steps such as flooding and vegetation restoration, might fail, harming an Trophic cascades in multiply invaded systems endangered species in the process. A large literature has been devoted to how food-web interactions limit populations of producers, consumers References and predators11–13. Much work has been done on the a Zavaleta, E.S. (2000) Valuing ecosystem services lost to Tamarix invasion in the United States. In Invasive Species in a Changing World (Mooney, H.A. and Hobbs, R.J., eds), relative roles of top-down regulation of food-web pp. 261–300, Island Press components by higher-level consumers or predators, b USFWS (1997) Endangered and threatened wildlife and