Take care with reintroductions

I recently came across an item in Science Daily describing an article¹ in Current Biology about the introduction of a notorious pathogen to an endangered animal population by reintroductions from a captive breeding programme. The Mallorcan Midwife Toad, Alytes muletensis, classified as Vulnerable by the IUCN, has been found to be infected with the fungus Batrachochytrium dendrobatidis, which is thought to be one of the main causes of the severe declines in amphibian populations observed in different parts of the world (it kills them by disrupting epidermal function, leading to osmotic imbalance²). When the genotypes of B. dendrobatidis from midwife toads in Mallorca, from other parts of Europe and from other amphibians housed in the same captive breeding facility were compared, it was concluded that the latter were the source of the infection in Mallorca.

Fortunately it appears that the disease has not had a serious effect in this case; three of the four populations in which the fungus was found are doing well, and the reintroduction programme as a whole has been very successful. This is not necessarily surprising, as it is known that different amphibian species (or different populations of the same species) can vary in their susceptibility to infection. One variable affecting susceptibility is the presence of antifungal peptides in the skin³; other factors that I found mentioned in records in CAB Abstracts included behaviour (which can affect transmission⁴), environmental temperature⁵ and the presence of symbiotic bacteria⁶. It is interesting to note that a closely related species just across the sea in mainland Spain has been adversely affected by chytridiomycosis⁷.

Reintroduction after captive breeding is of course not the only way, or even the main way, in which human activity can spread the disease. Trade in amphibians, (for example for restaurants⁸ or the pet trade⁹) is on a much larger scale, and there is strong evidence that it is contributing to the spread of chytridiomycosis¹⁰. However this case does suggest that efforts to help endangered species risk doing more harm than good if the possibility of introducing diseases is not taken sufficiently into account.

Known diseases can be dealt with -- screening for B. dendrobatidis was introduced as soon as it was discovered in the late 1990s, and it is now covered by OIE regulations -- but there is always the possibility of unknown diseases. Presumably good hygiene and avoiding unnecessary contact between different groups of animals will go some way towards preventing their spread. A quick database search revealed a number of articles about diseases in captive or reintroduced animals, but none about the introduction of diseases to wild populations as a result of reintroductions; I hope this indicates that the problem is rare rather than large and unknown.

A related issue is raised in another Science Daily item; one of the authors of the article¹¹ about disease resistance in frogs to which it refers suggests selective breeding of captive frogs to maintain or improve disease resistance. To me as a non-expert it seems a novel idea to breed zoo animals selectively as one would domestic ones (although I was aware of the need to maintain genetic diversity and avoid inadvertently selecting for traits that were beneficial only in captivity), and it wouldn't surprise me if some people objected to manipulating wild animals in this way; but if it's the best way to avoid extinctions it's probably worth considering.

 

1: Walker, S.F. et al.: Invasive pathogens threaten species recovery programs. Current Biology (2008) 18 (18), pp. R853-R854. DOI:10.1016/j.cub.2008.07.033.   

2: Voyles, J. et al.: Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Diseases of Aquatic Organisms (2007) 77 (2), pp. 113-118. DOI:10.3354/dao01838

3: Woodhams, D.C. et al.: Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Animal Conservation (2007) 10 (4), pp. 409-417. DOI:10.1111/j.1469-1795.2007.00130.x.   

4: Rowley, J.J.L. and Alford, R.A.: Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Diseases of Aquatic Organisms (2007) 77 (1), pp. 1-9. DOI:10.3354/dao01830

5: Berger, L. et al.: Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal (2004) 82 (7), pp. 434-439. DOI:10.1111/j.1751-0813.2004.tb11137.x.

6: Woodhams, D.C. et al.: Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biological Conservation (2007) 138 (3/4), pp. 390-398. DOI:10.1016/j.biocon.2007.05.004.

7: Bosch, J. et al.: Evidence of a chytrid fungus infection involved in the decline of the common midwife toad Alytes obstetricans) in protected areas of central Spain. Biological Conservation (2001) 97 (3), pp. 331-337. DOI:10.1016/S0006-3207(00)00132-4 

8: Mazzoni, R.: Emerging pathogen of wild amphibians in frogs (Rana catesbeiana) farmed for international trade. Emerging Infectious Diseases  (2003) 9 (8), pp. 995-998.

9: Pasmans, F. et al.: Chytridiomycosis in the Central American bolitoglossine salamander (Bolitoglossa dofleini). Veterinary Record (2004) 154 (5), p. 153. 

10:Fisher, M.C. and Garner, T.W.J. The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews (2007) 21 (1) pp. 2-9. DOI:10.1016/j.fbr.2007.02.002.

11: Barribeau, S.M. et al.: Major histocompatibility complex based resistance to a common bacterial pathogen of amphibians. PloS One (2008) 3 (7), e2692. DOI:10.1371/journal.pone.0002692