Opportunistic bacteria and mass mortality in ungulates: lessons from an extreme event

Sarah Robinson, E. J. Milner-Gulland, Yuri Grachev, Albert Salemgareyev, Mukhit Orynbayev, Anna Lushchekina, Eric Morgan, Wendy Beauvais , Navinder Singh, Sergei Khomenko, Rosie Cammack and Richard Kock

In May of 2015 a Kazakh population of the saiga antelope was hit by an extreme mass mortality event, during which over 200,000 animals died.  Reporting in 2018, an international group of scientists lead by Prof. Richard Kock of the Royal Veterinary College identified the cause of death as haemorrhagic septicaemia, caused by a specific serotype (B) of the bacterium Pasteurella multocida. Documented in many animal species, this organism exhibits ‘commensal’ behaviour – living harmlessly on the surface of the throat or tonsils of its host for long periods of time. For reasons which are poorly understood, the bacteria may suddenly cross the mucosal barrier of the respiratory and gastrointestinal systems, entering the bloodstream and by this route infecting multiple organs and causing death in a few hours.

mass die off
  Saiga die-off, 2015 © The authors​​​​​​

The research group found statistical associations between warm and humid conditions and the occurrence of a number of such outbreaks in saiga over the last 40 years, suggesting that environmental factors may trigger pathogenic activity. However, many questions remained. Have mass mortality events caused by this pathogen and its relatives been recorded in other wild ungulates (hoofed mammals) and if so, how do these cases compare to those in saiga? What types of trigger cause the transformation from harmless commensal to deadly pathogen and do these differ between species?  In the journal Ecosphere, the group address some of these questions by examining case histories of disease in wild ungulates caused by Pasteurella multocida and related organisms.  The review covers published cases in multiple languages starting from the beginning of the 20th Century when these bacteria had only recently been described. The authors also explore examples of such ‘opportunistic’ responses by other types of commensal organisms implicated in mass mortality events.                                

The results confirm that the die-offs in saiga are unprecedented in scale. In none of the reviewed cases of haemorrhagic septicaemia did mortality levels even approach those recorded in saiga. However as in saiga, humidity, rainfall and temperature were commonly suggested external factors associated with outbreaks and some of these factors have been demonstrated to increase infection rates by related organisms under experimental conditions, although Pasteurella multocida has not been specifically investigated. The life history of the host species may also be significant— saigas are migratory and the largest outbreaks recorded in other ungulates also occurred in temperate migratory species. Deaths of migratory birds affected by a related syndrome caused by the same bacteria are regularly counted in tens of thousands. It is a fine balance between the physical stress of this lifestyle and the ability to escape the extremes of climate, reproduce en masse and forage optimally for food, and weather anomalies may tip the balance, making potential hosts vulnerable to this opportunistic response.

Mongolian gazelle 
Mongolian gazelle  © Anna Lushchekina

Die-offs associated with other opportunistic commensals in ungulates also killed only small number of individuals, and were associated with various factors, from nutritional or climatic stress to co-infection with other viruses or bacteria. Mechanisms favouring colonisation of an entire population by a commensal, followed by a synchronous shift to virulence causing close to one hundred percent mortality have been fully demonstrated only in molluscs. In this example both steps were shown experimentally to be caused by different sets of very specific weather conditions. Certainly in saiga, levels of colonisation must have been extremely high by spring of 2015, but studies of healthy animals suggest that this may be a semi-permanent state of affairs.

 

 

In the end, only laboratory experiments can demonstrate how environmental conditions affect the host and pathogen and reveal the molecular mechanisms behind the shift to virulence of commensals. If both triggers and their consequences can be demonstrated under controlled conditions, then our ability to predict such events will be greatly enhanced. A fast-changing global environment combined with increasingly small and vulnerable populations of wildlife means that such an ability will become of increasing importance in the future.

 Reindeer 
 Reindeer © Richard Kock