Is host tolerance to pathogens and herbivores is more beneficial than resistance in reintroduced populations?

In just about every set of reintroduction guidelines I’ve ever read, one of the primary recommendations is always to eradicate the threats that caused the extirpation of populations of the target species. However, dealing with threats that have an extensive impact are often impossible to eradicate or limit to a specific location.  In the paper summarised below, Matthew Venesky and his co-authors (Venesky et al. 2012) examine several lines of evidence to look at the incidence of pathogens and herbivores and how reintroductions can be optimised to cope with a threat that can’t easily be controlled.

The paper relies on three concepts to make their argument that particular traits are key to successful translocation of species threatened by non-native pathogens or herbivores: virulence, tolerance and resistance. Virulence is defined "as the per capita effects of a pathogen or herbivore". Host tolerance is expressed as the ability to withstand an attack with little loss of fitness. Resistance refers to the reduction of pathogen or herbivore impact through deterring infection or herbivory, or attacking the pests directly. Tolerance is thought to have a neutral or positive consequence for pest abundance whereas resistance has a negative impact on pathogen or herbivore abundance.

The main thesis is that the generation time of pathogens and herbivores (especially invertebrates) is shorter than that of their hosts and can therefore be subject to selection pressures that are exerted as a result of the negative influence of host resistance. This creates pest populations that evolve countermeasures against resistance mechanisms; the lag in the host response means that reintroduced populations suffer high mortality before developing adequate resistance. Hosts which exhibit tolerance rather than resistance do not place strong selection pressures causing increased virulence, and in some cases may even select for decreased impacts. As a result, captive breeding that selects for tolerant (rather than resistant) individuals for translocation, may maximise the chance that a reintroduction attempt will survive long enough to produce progeny.

The two case studies use examples of non-native organisms to explore how captive breeding might select for tolerance rather than resistance to cope with pathogens and herbivory. The first is the fungal pathogen Batrachochytrium dendrobatidis (Bd) that causes chytridiomycosis and has decimated amphibian populations across the world. Selection for resistance involves several suggested approaches including identifying indicators of infection but minimal loss in fitness.  The second example is the cactus moth (Cactoblastis cactorum) which was succesfully introduced to Australia to reduce the prevalence of non-native prickly pear (Opuntia spp.). Unfortunately, the cactus moth has exhibited similar voracity against two narrow endemic species of cactus in Florida. Selection for tolerant genotypes might involve identifying individuals that drop pads from the main plant when stressed by moth herbivory.

The final section of the paper adds some important caveats to the discussion that shifts in host tolerance may have unexpected consequences such as a trade-off for competitive abilities of the host and the existence of low levels of pathogens and herbivores that could act as a reservoir for invading non-tolerant communities. As a result, Venesky et al. (2012) recommend adaptive managment strategies and using an experimental approach to compare the survival of resistant and tolerant genotypes post translocation.

Venesky, M. D., Mendelson III, J. R., Sears, B. F., Stiling, P., & Rohr, J. R. (2012). Selecting for Tolerance against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation. Conservation biology, 26(4), 586–592. doi:10.1111/j.1523-1739.2012.01854.x