Population bottlenecks and avian immunity: implications for conservation
Article first published online: 24 JAN 2007
Volume 10, Issue 1, pages 11–13, February 2007
How to Cite
Tompkins, D. M. (2007), Population bottlenecks and avian immunity: implications for conservation. Animal Conservation, 10: 11–13. doi: 10.1111/j.1469-1795.2006.00091.x
- Issue published online: 24 JAN 2007
- Article first published online: 24 JAN 2007
The study of immune function in the bottlenecked endemic New Zealand robin, presented by Hale & Briskie (2007), is a timely and informative addition to the growing body of literature on the effects that passing through genetic bottlenecks can have on bird species, and the resulting implications for their population management, recovery and long-term resilience. In a critical review of the implications of this work for conservation of both this species and bottlenecked populations in general, however, three key questions need to be asked. Is there sufficient evidence that bottlenecks cause reduced immune function? Does such a reduction actually impact on the resilience and long-term viability of such species? If there is indeed an issue, can it be addressed by management?
Is there sufficient evidence that bottlenecks cause reduced immune function?Hale & Briskie (2007) conclude ‘Our results confirm that severe bottlenecks reduce the immunocompetence of birds …’ In support of this statement, their work has demonstrated that two measures of immune function are significantly lower in a recently bottlenecked population of the New Zealand robin compared with its source population. Although trade-offs in the different branches of the immune system may occur, lower levels of function in two different measures are generally taken as good evidence for a meaningful reduction in immune function (Norris & Evans, 2000; Lindström et al., 2004; Tompkins, Mitchell & Bryant, 2006). However, results from a single bottlenecked population versus a single source population do not demonstrate that the bottleneck caused the reduction – other confounding factors may be involved.
Although this study alone does not confirm a bottleneck/immune function link, the accumulated evidence in the literature, as Hale & Briskie (2007) note, is heavily in favour of there being such a link. For conservation purposes, I would argue that the weight of evidence is sufficient for these considerations to be taken into account in species management programmes – definitive proof for such a link (requiring long-term manipulations at the population scale) may never be obtained, avoidable losses of species may occur while waiting for such proof.
Having made such a recommendation, however, there are two further considerations that may inform any management undertaken, and hence need to be taken into account. First, there is no evidence that immune function reductions linked to bottlenecks are not just relatively short-term transient effects. All studies to date have focused on time points relatively soon after bottleneck events. Repeated observations on subsequently expanding populations are thus required to demonstrate that reductions in immune function are maintained and, hence, are a long-term concern to population viability. Second, due to the complex life-history interactions of immunity (Norris & Evans, 2000), reductions in such functions may not be a simple direct consequence of loss of genetic variation. For example, a potential alternative mechanism is that the more frequent failure to breed successfully in bottlenecked populations (Briskie & Mackintosh, 2004) may be energetically costly, drawing resources away from immunocompetence. Whether reduced immune function is directly or indirectly caused by bottlenecks has implications for its management.
Does such a reduction actually impact on the resilience and long-term viability of such species? As many studies have documented, including Hale & Briskie (2007), temporal changes in measures of immune function in birds are common. Such changes are hypothesized as being due to either immune components being adapted to cope with a greater impact of parasites at certain times (Møller, Erritzoe & Saino, 2003), as a consequence of an increased need for wound-healing and resisting infection capabilities during periods when the likelihood of injury is greater (Zuk & Johnsen, 1998), lymphatic organ size peaking in relation to winter conditions (Nelson & Demas, 1996), or (related to the point made above) lack of resource availability due to the demands of reproduction and increased investments in other aspects of immunity (Zuk & Johnsen, 1998; Norris & Evans, 2000). Regardless of the cause, however, such changes indicate that investment in immunity is relatively fluid. Hence, lower measures of immune function may not necessarily reflect a lower ability to respond to infectious agents if, for example, resources can be mobilized in response to infection. For this and other reasons, including the observation that correlations between assays of immunity and disease resistance are typically pathogen-specific and often weak and/or non-linear, Adamo (2004) strongly recommended that susceptibility to infectious agents inferred from reduced measures of immune function be confirmed through experimental challenge. However, to the best of my knowledge, such challenges have yet to be conducted for any wild bird population.
Despite this lack of proof, that reduced measures of immune function equate to increased susceptibility to infectious agents in wild bird populations, the likelihood of such a link (and its implications for population resilience and long-term species viability) is again sufficient to warrant concern in bottlenecked bird populations. For example, although Hale & Briskie (2007) found no correlation between ectoparasites and measures of immune function in their study of New Zealand robins, there are several diseases of concern to wild bird populations in New Zealand, such as aspergillosis, avian malaria, avian pox, coccidiosis and Salmonella (Alley, 2002; Tompkins & Gleeson, 2006), to which reduced immune function could potentially make both individuals and populations more vulnerable. Hence, in view of the current phase of disease emergence both within New Zealand and globally (Daszak, Cunningham & Hyatt, 2000; Tompkins & Poulin, 2006), and the fact that conducting experimental challenges for all potential bottlenecked bird species/infectious agent combinations is unfeasible, endangered species management needs to take into account the potential for increased susceptibility to infectious agents (and hence reduced viability) of populations of such species.
If there is indeed an issue, can it be addressed by management? Several management options are available to conservationists managing existing populations or founding new populations of endangered bird species. The first is to pre-empt potential losses of immune function by acting to prevent or, at least, reduce the sizes of bottlenecks that populations go through. As Hale & Briskie (2007) note, it is likely that bottlenecks, less severe than those for which reduced measures of immune function have been documented, will avoid these issues. This reasoning is based on the fact that threshold population sizes above which bottleneck effects generally appear to be avoided have been identified for other bird life-history variables (Briskie & Mackintosh, 2004). Similar exploration of a potential population threshold for immune function would likewise provide much-needed guidance to conservationists.
If reduced immune function in bottlenecked bird populations is shown to be transitory, management solely to prevent challenge by infectious agents of concern during the initial period post-bottleneck may be all that is required before populations are once again resilient enough to withstand such challenges. Management to this end may take the form of disease screening of individuals being translocated between populations, population isolation and habitat management to reduce either the abundance of disease vectors (such as mosquitoes or ticks), or other stress factors on bird populations (Tompkins & Poulin, 2006).
If reduced immune function in bottlenecked bird species is shown not to be transitory, management to restore such function would also be necessary; otherwise, control of infectious agents would always be required. Theoretically, if losses in immune function experienced when passing through population bottlenecks are caused by reductions in genetic variation, restoration of such variation through outbreeding (achieved by moving either gametes or individuals between populations) would reverse that loss. Although demonstrating such a reverse with wild populations of endangered birds is likely to be impractical, a proof of concept experiment involving captive individuals would provide much-needed information on whether such management of immune function is possible. Evidence that hybridization with closely related species improves immune function in relatively inbred wild bird populations suggests that such within-species management would indeed be successful (Tompkins et al., 2006).
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