Kevin T. Castle

Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats

White-nose syndrome (WNS) is a fatal disease of bats that hibernate. The etiologic agent of WNS is the fungus Geomyces destructans, which infects the skin and wing membranes. Over 1 million bats in six species in eastern North America have died from WNS since 2006, and as a result several species of bats may become endangered or extinct. Information is lacking on the pathogenesis of G. destructans and WNS, WNS transmission and maintenance, individual and site factors that contribute to the probability of an outbreak of WNS, and spatial dynamics of WNS spread in North America. We considered how descriptive and analytical epidemiology could be used to fill these information gaps, including a four-step (modified) outbreak investigation, application of a set of criteria (Hills) for assessing causation, compartment models of disease dynamics, and spatial modeling. We cataloged and critiqued adaptive-management options that have been either previously proposed for WNS or were helpful in addressing other emerging diseases of wild animals. These include an ongoing program of prospective surveillance of bats and hibernacula for WNS, treatment of individual bats, increasing population resistance to WNS (through vaccines, immunomodulators, or other methods), improving probability of survival from starvation and dehydration associated with WNS, modifying hibernacula environments to eliminate G. destructans, culling individuals or populations, controlling anthropogenic spread of WNS, conserving genetic diversity of bats, and educating the public about bats and bat conservation issues associated with WNS.

Electrolyte Depletion in White-nose Syndrome Bats

The emerging wildlife disease white-nose syndrome is causing widespread mortality in hibernating North American bats. White-nose syndrome occurs when the fungus Geomyces destructans infects the living skin of bats during hibernation, but links between infection and mortality are underexplored. We analyzed blood from hibernating bats and compared blood electrolyte levels to wing damage caused by the fungus. Sodium and chloride tended to decrease as wing damage increased in severity. Depletion of these electrolytes suggests that infected bats may become hypotonically dehydrated during winter. Although bats regularly arouse from hibernation to drink during winter, water available in hibernacula may not contain sufficient electrolytes to offset winter losses caused by disease. Damage to bat wings from G. destructans may cause life-threatening electrolyte imbalances.

Investigating and Managing the Rapid Emergence of White-Nose Syndrome, a Novel, Fatal, Infectious Disease of Hibernating Bats: White-Nose Syndrome in Bats

White-nose syndrome (WNS) is a fatal disease of bats that hibernate. The etiologic agent of WNS is the fungus Geomyces destructans, which infects the skin and wing membranes. Over 1 million bats in six species in eastern North America have died from WNS since 2006, and as a result several species of bats may become endangered or extinct. Information is lacking on the pathogenesis of G. destructans and WNS, WNS transmission and maintenance, individual and site factors that contribute to the probability of an outbreak of WNS, and spatial dynamics of WNS spread in North America. We considered how descriptive and analytical epidemiology could be used to fill these information gaps, including a four-step (modified) outbreak investigation, application of a set of criteria (Hills) for assessing causation, compartment models of disease dynamics, and spatial modeling. We cataloged and critiqued adaptive-management options that have been either previously proposed for WNS or were helpful in addressing other emerging diseases of wild animals. These include an ongoing program of prospective surveillance of bats and hibernacula for WNS, treatment of individual bats, increasing population resistance to WNS (through vaccines, immunomodulators, or other methods), improving probability of survival from starvation and dehydration associated with WNS, modifying hibernacula environments to eliminate G. destructans, culling individuals or populations, controlling anthropogenic spread of WNS, conserving genetic diversity of bats, and educating the public about bats and bat conservation issues associated with WNS.

First Direct Evidence of Long-distance Seasonal Movements and Hibernation in a Migratory Bat

Understanding of migration in small bats has been constrained by limitations of techniques that were labor-intensive, provided coarse levels of resolution, or were limited to population-level inferences. Knowledge of movements and behaviors of individual bats have been unknowable because of limitations in size of tracking devices and methods to attach them for long periods. We used sutures to attach miniature global positioning system (GPS) tags and data loggers that recorded light levels, activity, and temperature to male hoary bats (Lasiurus cinereus). Results from recovered GPS tags illustrated profound differences among movement patterns by individuals, including one that completed a >1000 km round-trip journey during October 2014. Data loggers allowed us to record sub-hourly patterns of activity and torpor use, in one case over a period of 224 days that spanned an entire winter. In this latter bat, we documented 5 torpor bouts that lasted ≥16 days and a flightless period that lasted 40 nights. These first uses of miniature tags on small bats allowed us to discover that male hoary bats can make multi-directional movements during the migratory season and sometimes hibernate for an entire winter.

Using sutures to attach miniature tracking tags to small bats for multimonth movement and behavioral studies.

Determining the detailed movements of individual animals often requires them to carry tracking devices, but tracking broad-scale movement of small bats (<30 g) has been limited by transmitter technology and long-term attachment methods. This limitation inhibits our understanding of bat dispersal and migration, particularly in the context of emerging conservation issues such as fatalities at wind turbines and diseases. We tested a novel method of attaching lightweight global positioning system (GPS) tags and geolocating data loggers to small bats. We used monofilament, synthetic, absorbable sutures to secure GPS tags and data loggers to the skin of anesthetized big brown bats (Eptesicus fuscus) in Colorado and hoary bats (Lasiurus cinereus) in California. GPS tags and data loggers were sutured to 17 bats in this study. Three tagged bats were recaptured 7 months after initial deployment, with tags still attached; none of these bats showed ill effects from the tag. No severe injuries were apparent upon recapture of 6 additional bats that carried tags up to 26 days after attachment; however, one of the bats exhibited skin chafing. Use of absorbable sutures to affix small tracking devices seems to be a safe, effective method for studying movements of bats over multiple months, although additional testing is warranted. This new attachment method has the potential to quickly advance our understanding of small bats, particularly as more sophisticated miniature tracking devices (e.g., satellite tags) become available.

COYOTE (CANIS LATRANS) AND DOMESTIC DOG (CANIS FAMILIARIS) MORTALITY AND MORBIDITY DUE TO A KARENIA BREVIS RED TIDE IN THE GULF OF MEXICO

Abstract In October 2009, during a Karenia brevis red tide along the Texas coast, millions of dead fish washed ashore along the 113-km length of Padre Island National Seashore (PAIS). Between November 2009 and January 2010, at least 12 coyotes (Canis latrans) and three domestic dogs (Canis familiaris) died or were euthanized at PAIS or local veterinary clinics because of illness suspected to be related to the red tide. Another red tide event occurred during autumn 2011 and, although fewer dead fish were observed relative to the 2009 event, coyotes again were affected. Staff at PAIS submitted carcasses of four coyotes and one domestic dog from November 2009 to February 2010 and six coyotes from October to November 2011 for necropsy and ancillary testing. High levels of brevetoxins (PbTxs) were measured by enzyme-linked immunosorbent assay in seven of the coyotes and the dog, with concentrations up to 634 ng PbTx-3 eq/g in stomach contents, 545 ng PbTx-3 eq/g in liver, 195 ng PbTx-3 eq/g in kidney, and 106 ng PbTx-3 eq/mL in urine samples. Based on red tide presence, clinical signs, and postmortem findings, brevetoxicosis caused by presumptive ingestion of toxic dead fish was the likely cause of canid deaths at PAIS. These findings represent the first confirmed report of terrestrial mammalian wildlife mortalities related to a K. brevis bloom. The implications for red tide impacts on terrestrial wildlife populations are a potentially significant but relatively undocumented phenomenon.