Rabies as a Potential Cause of Mass Mortality Events in North American Bat Species

The emergence of zoonotic diseases in wildlife threatens global public health and biodiversity (Daszak et al. 2000). Bats, order Chiroptera, are found nearly worldwide (Wong et al. 2007) and are unique among mammals in their ability to fly. Bats often gather in large social groups and are associated with a number of emerging diseases (Luis et al. 2013; Mollentze et al. 2020). Habitat loss and environmental changes from human development may contribute to the increasingly common finding of colonial bat species roosting in buildings, bridges, and other man-made structures (Jackson et al. 2008; Streicker et al. 2013). Bats living in close proximity to humans increase risks for zoonotic disease transmission, which in the Americas includes rabies virus.

Rabies virus (Lyssavirus) causes fatal encephalitis in mammals. Most human rabies cases in the US are caused by viral variants from insectivorous bats (Patyk et al. 2012; Pieracci et al. 2019). Despite the vast body of research on the bat–rabies relationship, a lack of literature exists on bat mortality events caused by rabies virus (O'Shea et al. 2016); therefore guidance is limited for predicting, monitoring, and responding to these events.

National Park Service (NPS) units provide excellent natural and man-made roosting habitat for bats, and host ∼300 million human visits annually. Consequently, opportunities exist for human–bat interactions and potential rabies exposure in parks. We describe three unique multibat mortality events caused by rabies virus that occurred within different NPS units (Table 1).

Casa Grande Ruins National Monument (CGRNM) in Arizona features the Great House (GH), an ancient Native American structure visited daily by tourists and staff. A colony of Western pipistrelle bats (Parastrellus hesperus) and Yuma myotis (Myotis yumanensis) of ∼50 individuals has historically roosted in the GH. A locally dispersing colony of Mexican free-tailed bats (Tadarida brasiliensis; TABR) numbering ∼1,000 individuals began roosting in the GH in 2010.

Two consecutive mortality events caused by rabies virus occurred at the GH in 2011 and 2012. A total of 28 TABR were found dead. Whole carcasses were collected in plastic bags and shipped on ice to the NPS Wildlife Veterinary Diagnostic Service. Rabies was detected by fluorescent antibody test (FAT) in 13/14 (93%) TABR tested in 2011 and 8/9 (89%) tested in 2012 (data not shown). Brain samples from four rabies-positive bats were sent to the US Centers for Disease Control and Prevention (CDC) for rabies strain typing using monoclonal antibodies to the rabies virus nucleoprotein. Virus was consistent with the variant circulating in TABR.

At Point Reyes National Seashore (PRNS) in California, Barn A is a historic barn closed to the public and used for storage by park staff. A maternity colony of Myotis bats (species unidentified) has been present there for decades with an estimated seasonally varying population of 300–500; TABR were not known to roost in that site, but their absence could not be confirmed. In 2014, 11 bats, California myotis (Myotis californicus) and/or little brown bats (M. lucifigus), were found dead at Barn A. Rabies was detected by FAT in 9/10 (90%) bats tested. Brain samples from four rabies-positive bats were submitted to CDC for reverse transcriptase–PCR analysis and sequencing, which revealed rabies virus variants consistent with those circulating in TABR.

There are no previous published reports of mortality events in free-living bat colonies attributed to a rabies virus strain circulating in a different bat species before this event at PRNS in 2014. It involved crossover of the TABR rabies variant into Myotis bats. At least 25 bats within the colony died during this mortality event. No previous mortality events of bats at the barn or elsewhere in the park were reported by PRNS staff, and no additional bat mortality events have been observed in the park since 2014.

At Gettysburg National Military Park (GNMP) in Pennsylvania, House A is a Civil War–era farmhouse used as a residence for employees and located next to a large barn and several smaller outbuildings. Park biologists have estimated that 10–15 bats (probably Eptesicus fuscus, based on local ecology and behaviors of these bats) are regularly seen year-round emerging from buildings to forage. In July 2016, seven bats were found dead during 1 wk at House A. Five of the bats were collected and identified as big brown bats (E. fuscus). Rabies virus was detected by FAT in 2/5 (40%) bats. Brain tissue from the two rabies-positive bats sent to CDC for strain typing revealed a strain consistent with those circulating in big brown bats. Bats (live or dead) have not been observed at House A since the mortality event.

Historically, rabies has not commonly been included as a differential diagnosis for mass mortality events of bats. We report three separate events of bat mass mortalities attributed to rabies. Further, evidence of a species-specific strain crossover event indicates potential for a rabies virus strain to result in a mortality event and sustained transmission in a nonadapted species (Mollentze et al. 2020). The annual national average of rabid bats of those submitted for testing to CDC from 2009 to 2014 was ∼6.0% (Monroe et al. 2016; Pieracci et al. 2020). In the cases we report, the percentage of rabid bats of those tested were significantly higher than the national average at 91% (CGRNM), 90% (PRNS), and 40% (GNMP).

Our study was limited by a lack of historical knowledge of bat roost size, species diversity, and expected mortality. Wildlife mortality is difficult to capture fully because of carcass scavenging and the myriad of remote locations where wildlife die. It is likely that rabies has caused mass mortality events of bats and crossed species more commonly than has been previously reported, due to a lack of testing or underreporting. Alternatively, these events may be new phenomena indicating recent changes in rabies ecology among bat populations. We suggest rabies should be included as a differential diagnosis in future mass bat mortality events, and more work is needed to understand cross-species transmission of rabies variants and virulence in nonadapted species.

Given the role of bats as the primary source of human rabies in the US, the potential for rabies exposure in humans should be considered when multiple bats are found sick or dead in close proximity to humans. The NPS continues to expand its training and education for staff on safe work practices around wildlife and information on how to investigate wildlife mortality events. Improved understanding of bat behavior and rabies ecology in synanthropic bat species may help reduce risks of bat–human interactions and zoonotic disease transmission near anthropogenic structures and promote safer environments for both bats and people.

This work was supported by the National Park Service's Wildlife Health Branch (Fort Collins, Colorado) with special assistance from Tegwin Taylor, Elizabeth Wheeler, Jenny Powers, Margaret Wild, and Scott Ratchford. Sincere thanks are expressed to Dave Press (Point Reyes National Seashore), Karl Cordova (Casa Grande Ruins National Monument), and Dafna Reiner (Gettysburg National Military Park) for their contributions and discussions related to their respective bat-rabies case reports. Thank you to the Colorado State University Veterinary Diagnostic Laboratory for assistance with diagnostic testing and analysis of specimens involved in this report and the Centers for Disease Control and Prevention's Rabies Branch for strain typing analysis and exceptional assistance in interpreting these results.