Climate extremes promote fatal co-infections during canine distemper epidemics in African lions

Linda Munson, Karen A. Terio, Richard Kock, Titus Mlengeya, Melody E. Roelke, Edward Dubovi, Brian Summers, Anthony R E Sinclair, Craig Packer

Research output: Contribution to journalArticle

113 Citations (Scopus)

Abstract

Extreme climatic conditions may alter historic host-pathogen relationships and synchronize the temporal and spatial convergence of multiple infectious agents, triggering epidemics with far greater mortality than those due to single pathogens. Here we present the first data to clearly illustrate how climate extremes can promote a complex interplay between epidemic and endemic pathogens that are normally tolerated in isolation, but with co-infection, result in catastrophic mortality. A 1994 canine distemper virus (CDV) epidemic in Serengeti lions (Ponthera leo) coincided with the death of a third of the population, and a second high-mortality CDV epidemic struck the nearby Ngorongoro Crater lion population in 2001. The extent of adult mortalities was unusual for CDV and prompted an investigation into contributing factors. Serological analyses indicated that at least five "silent" CDV epidemics swept through the same two lion populations between 1976 and 2006 without clinical signs or measurable mortality, indicating that CDV was not necessarily fatal. Clinical and pathology findings suggested that hemoparsitism was a major contributing factor during fatal epidemics. Using quantitive real-time PCR, we measured the magnitude of hemoparasite infections in these populations over 22 years and demonstrated significantly higher levels of Babesia during the 1994 and 2001 epidemics. Babesia levels correlated with mortalities and extent of CDV exposure within prides. The common event preceding the two high mortality CDV outbreaks was extreme drought conditions with wide-spread herbivore die-offs, most notably of Cape buffalo (Syncerus caffer). As a consequence of high tick numbers after the resumption of rains and heavy tick infestations of starving buffalo, the lions were infected by unusually high numbers of Babesia, infections that were magnified by the immunosuppressive effects of coincindent CDV, leading to unprecedented mortality. Such mass mortality events may become increasingly common if climate extremes disrupt historic stable relationships between co-existing pathogens and their susceptible hosts.

Original languageEnglish (US)
Article numbere2545
JournalPLoS One
Volume3
Issue number6
DOIs
StatePublished - Jun 25 2008

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Distemper
Lions
canine distemper
Canine Distemper Virus
Panthera leo
Canine distemper virus
Climate
Coinfection
mixed infection
Viruses
climate
Mortality
Pathogens
Babesia
Buffaloes
Syncerus caffer
pathogens
Population
Tick Infestations
immunosuppressive agents

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Munson, L., Terio, K. A., Kock, R., Mlengeya, T., Roelke, M. E., Dubovi, E., ... Packer, C. (2008). Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. PLoS One, 3(6), [e2545]. https://doi.org/10.1371/journal.pone.0002545

Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. / Munson, Linda; Terio, Karen A.; Kock, Richard; Mlengeya, Titus; Roelke, Melody E.; Dubovi, Edward; Summers, Brian; Sinclair, Anthony R E; Packer, Craig.

In: PLoS One, Vol. 3, No. 6, e2545, 25.06.2008.

Research output: Contribution to journalArticle

Munson, L, Terio, KA, Kock, R, Mlengeya, T, Roelke, ME, Dubovi, E, Summers, B, Sinclair, ARE & Packer, C 2008, 'Climate extremes promote fatal co-infections during canine distemper epidemics in African lions', PLoS One, vol. 3, no. 6, e2545. https://doi.org/10.1371/journal.pone.0002545
Munson, Linda ; Terio, Karen A. ; Kock, Richard ; Mlengeya, Titus ; Roelke, Melody E. ; Dubovi, Edward ; Summers, Brian ; Sinclair, Anthony R E ; Packer, Craig. / Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. In: PLoS One. 2008 ; Vol. 3, No. 6.
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