An Old Pathogen in a New Environment–Implications of Coxiella burnetii in Australian Fur Seals (Arctocephalus pusillus doriferus)

Abstract

The Australian fur seal (Arctocephalus pusillus doriferus) has experienced a slower than expected population recovery since the end of the commercial sealing era, with a high third trimester abortion rate. There is currently no known proximate cause. Coxiella burnetii (Cb) is a well-known cause of abortion in domestic and wildlife species and an important zoonotic pathogen. It has been recorded from a small number of northern hemisphere marine mammals and may be a potential contributory factor to decreasing populations of northern fur seals (Callorhinus ursinus) and Steller sealions (Eumetopias jubatus). It has not been recorded from marine mammals in the southern hemisphere but is well documented in ruminants and wildlife in Australia as a cause of reproductive failure. Third trimester aborted fetuses (n = 46) and full-term placentas (n = 66) from Australian fur seals, were collected on Kanowna Island and Seal Rocks in Bass Strait, south-eastern Australia. Utilizing routine hematoxylin and eosin histopathology, Cb immunohistochemistry and two different qPCR targets–htpAB and com1, Cb was identified. Routine histopathology and immunohistochemistry were insensitive for the detection of Cb. The detected Cb prevalence ranged from 10.6% for com1 up to 40.9% with htpAB. Coxiella burnetti was readily detected in full-term placentas but in aborted fetal material only in a single placenta associated with a still birth. The exact significance is currently unclear, but this highlights that Cb is present in Australian fur seals, breeding in Bass Strait. Bass Strait is in one of the world’s fastest warming oceanic regions and marine mammals breeding in the area are likely to be key indicators of marine ecosystem stressors. This first description of Cb in a marine mammal from the southern hemisphere, highlights the need to further investigate the potential risks this pathogen poses to Australian fur seals and sympatric marine mammals. Additionally, it is important to determine the zoonotic risk of this pathogen to persons working with, and in proximity of, Australian fur seal breeding colonies.

Understanding the zoonotic pathogen, Coxiella burnetii in Australian fur seal breeding colonies through environmental DNA and genotyping

“…The targets were the com1 and htpAB genes and the IS1111 insertion. The same qPCR technique was used as had been employed by researchers in the initial detection of C. burnetii in Australian fur seals (Gardner et al 2022) other than the addition of the IS1111 insertion as a marker. IS1111 markers are based on previously described techniques (Schneeberger et al 2010).…”

“…Although a common differential diagnosis for reproductive failure in terrestrial mammals (Agerholm 2013), it has only in recent years been associated with declining populations of two species of pinnipeds in the northern hemisphere (Minor et al 2013). It has only very recently been described in marine mammals in the southern hemisphere in Australian fur seals (Arctocephalus pusillus doriferus) (Gardner et al 2022).…”

“…The Australian fur seal has had a slower than expected recovery after a cessation of commercial harvest and has shown decreased pup numbers in some key breeding colonies (McIntosh et al 2022). A large percentage of Australian fur seal placentas from the third largest breeding colony for the species have both molecular and histopathological evidence of C. burnetii (Gardner et al 2022).…”

“…The Australian fur seal has had a slower than expected recovery after a cessation of commercial harvest and has shown decreased pup numbers in some key breeding colonies (McIntosh et al 2022). A large percentage of Australian fur seal placentas from the third largest breeding colony for the species have both molecular and histopathological evidence of C. burnetii (Gardner et al 2022). It is currently unknown whether this C. burnetii is related to a terrestrial spillover (Gardner et al 2022) or a unique marine mammal-adapted genotype as previously postulated for northern fur seals (Callorhinus ursinus) (Duncan et al 2013).…”

Pacific Gulls (Larus pacificus) as Potential Vectors of Coxiella burnetii in an Australian Fur Seal Breeding Colony

“…It is a known cause of reproductive failure in wildlife species [ 3 ] and in recent years has been associated with declining populations of northern fur seals ( Callorhinus ursinus ) and Steller sea lions ( Eumetopias jubatus ) [ 4 ]. It was first described in marine mammals in the southern hemisphere, in 2022, in Australian fur seals (AusFS, Arctocephalus pusillus doriferus ) breeding on Kanowna Island (KI) in the Bass Strait, southeastern Australia [ 5 ]. Australian fur seals have recently had decreased pup production, more obviously in their largest breeding colony at Seal Rocks [ 6 ].…”