Respiratory Microbiome of Endangered Southern Resident Killer Whales and Microbiota of Surrounding Sea Surface Microlayer in the Eastern North Pacific

Stephen A Raverty,Caroline E Cameron,M Bradley Hanson,J Pete Schroeder,Erin Zabek,Azad Eshghi,Linda D Rhodes

doi:10.1038/s41598-017-00457-5

Abstract

In the Salish Sea, the endangered Southern Resident Killer Whale (SRKW) is a high trophic indicator of ecosystem health. Three major threats have been identified for this population: reduced prey availability, anthropogenic contaminants, and marine vessel disturbances. These perturbations can culminate in significant morbidity and mortality, usually associated with secondary infections that have a predilection to the respiratory system. To characterize the composition of the respiratory microbiota and identify recognized pathogens of SRKW, exhaled breath samples were collected between 2006–2009 and analyzed for bacteria, fungi and viruses using (1) culture-dependent, targeted PCR-based methodologies and (2) taxonomically broad, non-culture dependent PCR-based methodologies. Results were compared with sea surface microlayer (SML) samples to characterize the respective microbial constituents. An array of bacteria and fungi in breath and SML samples were identified, as well as microorganisms that exhibited resistance to multiple antimicrobial agents. The SML microbes and respiratory microbiota carry a pathogenic risk which we propose as an additional, fourth putative stressor (pathogens), which may adversely impact the endangered SRKW population.

Highlights

In the Salish Sea, the endangered Southern Resident Killer Whale (SRKW) is a high trophic indicator of ecosystem health
The surface microlayer (SML) microbes and respiratory microbiota carry a pathogenic risk which we propose as an additional, fourth putative stressor, which may adversely impact the endangered SRKW population
This study is the first to characterize the microbial contents of exhaled breath from a wild population of killer whales

Summary

Introduction

In the Salish Sea, the endangered Southern Resident Killer Whale (SRKW) is a high trophic indicator of ecosystem health. The ability to characterize the health status of live SRKW is restricted by public sentiment, law and logistics, relying on opportunistic and non-invasive sample collection The latter can be achieved by sampling the exhaled breath as an alternate means for acquiring samples indicative of the respiratory health of free-swimming whales. Respiratory adaptations in cetaceans have evolved to consist of prolonged breath holding during deep dives followed by short, rapid expirations and inhalations with a tidal volume of 70–85 percent, and exhalation of 0.3 seconds for smaller cetaceans and 1–2 seconds for larger whales[9] These respiratory patterns, coupled with a direct conduit from the blowhole to lungs, may facilitate inadvertent aspiration of small quantities of the sea surface microlayer (SML). An assessment of the composition of microorganisms within both exhaled breath samples and the SML could reveal a potential relationship between host respiratory and SML microbial flora

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