Conservation biology

When an infection turns lethal

Losses in biodiversity and the emergence of new infectious diseases are among the greatest threats to life on the planet. The declines in amphibian populations lie at the interface between these issues.

It is estimated1 that roughly one-third of amphibian species are under threat of extinction and that more than 100 species may have become extinct since 1980. The reasons for the decline and extinction of amphibian populations are probably complex and multifactorial2. But growing evidence3 indicates that, in many cases, infectious disease is driving amphibian losses. In particular, the pathogenic fungus Batrachochytrium dendrobatidis has been linked to the decline of amphibian populations throughout the world. Two related papers published in Proceedings of the National Academy of Sciences, by Vredenburg et al.4 and Briggs et al.5, considerably improve our understanding of the dynamics of B. dendrobatidis infection.

This pathogen causes the often-lethal disease chytridiomycosis, which disrupts the function of epidermal structures such as the skin and teeth and the regulation of osmosis6 to varying degrees, depending on the amphibian species and its life stage7. Since its description in the late 1990s, B. dendrobatidis has been the subject of hundreds of studies by researchers from various disciplines. Nonetheless, many ecological questions remain. Why does B. dendrobatidis cause extinction of the host population (through inducing an epidemic) in some regions but persist in the population in an endemic state in other regions? In addition, how does this pathogen induce host losses without a concomitant decrease in its transmission (as would be expected to occur for a density-dependent parasite)? After all, as infected hosts die, one would expect the disease to decline in prevalence as well.

Vredenburg and colleagues4 and Briggs et al.5 carried out long-term, large-scale monitoring and sampling of amphibian populations in the Sierra Nevada in California, focusing on yellow-legged frogs — Rana muscosa and Rana sierrae — the populations of which have declined in recent decades. Previous studies focused exclusively on the prevalence of infection (that is, the proportion of infected hosts), ignoring the role of infection intensity (the amount of infection per individual host) in controlling host-population losses. Instead of simply cataloguing the presence or absence of B. dendrobatidis and its spread among host populations, these investigators4,5 identify a 'lethal threshold' of pathogen infection intensity, which may be the key to understanding how B. dendrobatidis epidemics can be controlled.

Vredenburg et al.4 carried out intensive sampling of 88 frog populations over 9–13 years. Among the lakes they studied, they found that, within three years of its arrival, B. dendrobatidis had spread in a wave-like pattern — that is, the area covered by the pathogen increased steadily in size over time — until nearly all of the frog populations at the lake were infected. The amphibian populations did not, however, collapse until a lethal threshold of about 10,000 zoospores of the fungus per frog was reached.

The existence of such an intensity threshold may help to explain how B. dendrobatidis causes almost complete losses of amphibian hosts. Because of this threshold, there is a time lag between exposure and mortality, so the pathogen can spread through much of the amphibian population before disease-driven reductions in host density negatively affect the transmission of B. dendrobatidis. Consequently, the pathogen can cause the loss and extinction of its host population, unlike the many other pathogens that disappear as their hosts decline in numbers.

Briggs et al.5 combine long-term field data with modelling analysis to investigate how some amphibian populations persist even though B. dendrobatidis is present in their habitat. The authors' intensive data — involving marking the animals and later recapturing them — show that, in populations that survive, infected yellow-legged frogs have fungal loads well below the lethal intensity threshold, and that these frogs have cleared fungal infection and become reinfected over the course of years, with no effect on their survival.

Previous studies suggested that genetic changes that alter host tolerance of the pathogen or pathogen virulence might explain how some amphibian populations persist in the presence of B. dendrobatidis. Briggs and colleagues' modelling efforts, however, hint that simple decreases in host density and the resultant reduction in pathogen transmission could account for such an outcome. This is particularly true when there are environmental reservoirs of B. dendrobatidis, including amphibian species or life stages (such as tadpoles) that can persist with the infection for long periods and spread it to more sensitive hosts.

This modelling work5, which was based on a variety of biological scenarios, offers insight into both the epidemic and endemic aspects of B. dendrobatidis dynamics. For instance, the study predicts that infection intensity builds up rapidly when frog populations are dense, as well as under conditions that promote reinfection. If B. dendrobatidis reaches its intensity threshold, the infected amphibian population can become extinct. By contrast, if some members of the host population survive, then a new endemic state develops, with persistent infection in the remaining frogs.

Intriguingly, both studies4,5 indicate that the traditional dichotomous classification of pathogens as either microparasites or macroparasites may be overly simplistic, as the dynamics of infection with B. dendrobatidis — a microparasite — strongly depend on infection intensity (which is usually considered only for macroparasites). This finding suggests that incorporating infection intensity into other microparasite disease models could provide insight into other host–pathogen systems.

The new papers4,5 markedly increase the understanding of a disease that affects many amphibian populations. In particular, the types of data presented — based on long-term, extensive monitoring that generates detailed records — are largely unprecedented for analyses of many wildlife disease systems.

Nevertheless, large gaps remain in the knowledge of B. dendrobatidis and in how the dynamics of chytridiomycosis vary between geographical regions. The populations that these researchers4,5 studied are from montane ecosystems that have low species diversity and relatively harsh winter conditions. Will the reported dynamics for B. dendrobatidis in this system explain the spread of this pathogen in, for example, lowland regions of Europe or in the tropics, where host-species density is substantially higher?

Moreover, it is still not clear precisely which vectors spread the infection, in which systems it is endemic and in which ones it is epidemic, and whether environmental changes can trigger the emergence of this pathogen. By focusing on infection intensity and the differences between epidemic and endemic states of B. dendrobatidis infection, Vredenburg et al. and Briggs et al. lay a valuable foundation for addressing questions such as how the intensity threshold of B. dendrobatidis varies across species or with environmental conditions, and what part is played by environmental cofactors such as climate change8 in affecting the dynamics of endemic infection.

How can this information be applied so as to slow, or even prevent, population declines? As the authors of both papers propose, interventions designed to prevent B. dendrobatidis infection from reaching the lethal-intensity threshold could reduce extinction events. Because it is unlikely that the pathogen will be completely eradicated, the only realistic option may be to manage sensitive amphibian populations in such a way as to create an endemic state of infection. For instance, as described in a News Feature in these pages last week9, reducing the density of susceptible frogs by capturing them before the infection wave, or by treating a subset of individuals with an antifungal agent, could reduce transmission of B. dendrobatidis and prevent infection intensities from becoming lethal.

References

  1. 1

    Stuart, S. N. et al. Science 306, 1783–1786 (2004).

    ADS  CAS  Article  Google Scholar 

  2. 2

    Blaustein, A. R. & Kiesecker, J. M. Ecol. Lett. 5, 597–608 (2002).

    Article  Google Scholar 

  3. 3

    Daszak, P., Cunningham, A. A. & Hyatt, A. D. Divers. Distrib. 9, 141–150 (2003).

    Article  Google Scholar 

  4. 4

    Vredenburg, V. T., Knapp, R. A., Tunstall, T. S. & Briggs, C. J. Proc. Natl Acad. Sci. USA 107, 9689–9694 (2010).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Briggs, C. J., Knapp, R. A. & Vredenburg, V. T. Proc. Natl Acad. Sci. USA 107, 9695–9700 (2010).

    ADS  CAS  Article  Google Scholar 

  6. 6

    Voyles, J. et al. Science 326, 582–585 (2009).

    ADS  CAS  Article  Google Scholar 

  7. 7

    Blaustein, A. R. et al. Conserv. Biol. 19, 1460–1468 (2005).

    Article  Google Scholar 

  8. 8

    Pounds, J. A. et al. Nature 439, 161–167 (2006).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Lubick, N. Nature 465, 680–681 (2010).

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Blaustein, A., Johnson, P. When an infection turns lethal. Nature 465, 881–882 (2010). https://doi.org/10.1038/465881a

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.