Challenges to understanding the consequences of population bottlenecks for the conservation of endangered wildlife

The widespread decline of many species has brought new urgency to understanding the consequences of population bottlenecks. Even if conservation efforts succeed in returning endangered species to a less threatened status, their brief ‘flirt’ with extinction raises questions about any lingering effects of passing through a severe bottleneck. Although the genetic consequences of population bottlenecks are well documented (e.g. Nei, Maruyama & Chakraborty, 1975), it is unclear whether bottlenecks also lead to declines in the fitness of the recovered population that reduces its survival and ability to adapt to changing environments. As pointed out by Tompkins (2007), it would be useful for planning conservation initiatives if we knew whether the fitness effects of bottlenecks were just temporary, and which aspects of an animal’s life history were most affected. If the fitness consequences of bottlenecks are relatively minor or short term, then more attention could be focused on other urgent conservation problems. We agree with Hawley (2007) that conservation biologists indeed need to ‘look beyond genetics’ to determine whether bottlenecks warrant their serious attention. Our examination of two New Zealand robin Petroica australis populations, in which we compared a severely bottlenecked population with its ancestral source population, supports predictions that bottlenecks can lead to declines in the immune response of individuals in a postbottlenecked population (Hale & Briskie, 2007). Our conclusion is based on combined analyses of current parasite loads, differences in blood cell composition and immunocompetence assays in both populations over two seasons. The importance of using a multiple approach is illustrated by the difficulty in interpreting any single measure of fitness. For example, the similar ectoparasite levels in both populations of robins would suggest that bottlenecks have little detrimental effect on parasite loads (Hale & Briskie, 2007). However, as Hawley (2007) points out, the key measure is not simply current parasite load but parasite resistance, and a number of other explanations for our results are possible (including the ones we did not address). Perhaps the greatest drawback of using current parasite loads to assess immune response is the assumption that each population has been exposed to potential parasites at similar rates and other potential environment factors are equal. Such conditions are unlikely to be met, and without experimental exposures of birds to parasites under controlled conditions, one cannot be sure whether the lack of a difference in current parasite load is due to some confounding factor. The experimental exposure of endangered animals to novel parasites or pathogens would allow a direct way to test a decrease in resistance to parasites or lowered immune response, but such methods raise ethical issues that may be difficult to address with the current methodology. Despite potential problems, it is clear that future workers need to approach the study of fitness costs of bottlenecks with a variety of tests as not all aspects of an animal’s biology are likely to be affected equally or consistently over time. As highlighted by Smits (2007), measuring whether a bottleneck induces fitness costs on individuals in the postbottlenecked population requires a careful selection of tests. A poor selection of methods may lead to studies that wrongly conclude that the fitness effects of bottlenecks are minimal or even exaggerated. In our study, we experimentally measured the response of robins to phytohaemagglutinin (PHA) during two different times of the year (preand post-breeding) to minimize this risk and found differences in the strength of response to the antigen. If we had tested birds only during the spring, we would have concluded that there was no fitness cost (Hale & Briskie, 2007). Smits (2007) suggests that as we tested robins only during ‘benign’ periods of the annual cycle, we underestimated the fitness costs. Although stresses to birds likely differ over their annual cycle, our finding that robins in autumn show a compromised response to PHA should nonetheless raise concerns. If robins cannot cope with a foreign antigen during a supposed ‘benign’ period, how will they cope during the most stressful periods of their annual cycle?