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We describe a wing abnormality present in a wild-hatched Whooping Crane (Grus americana) chick from the reintroduced Louisiana nonmigratory population. Despite its compromised flight ability, the chick fledged, reached independence, and lived until 13 months of age. Necropsy revealed a healed fracture near the left carpus likely resulting from trauma.
An outbreak of rabies occurred in a captive colony of wild-caught big brown bats ( Eptesicus fuscus ). Five of 27 bats exhibited signs of rabies virus infection 22–51 d after capture or 18–22 d after contact with the index case. Rabid bats showed weight loss, aggression, increased vocalization, hypersalivation, and refusal of food. Antigenic typing and virus sequencing confirmed that all five bats were infected with an identical rabies virus variant that circulates in E. fuscus in the United States. Two bats with no signs of rabies virus infection were seropositive for rabies virus-neutralizing antibodies; the brains of these bats had no detectable viral proteins by the direct fluorescence antibody test. We suspect bat-to-bat transmission of rabies virus occurred among our bats because all rabies-infected bats were confined to the cage housing the index case and were infected with viruses having identical sequences of the entire rabies nucleoprotein gene. This outbreak illustrated the risk of rabies virus infection in captive bats and highlights the need for researchers using bats to assume that all wild bats could be infected with rabies virus.
During 2014, highly pathogenic (HP) influenza A viruses (IAVs) of the A/Goose/Guangdong/1/1996 lineage (GsGD-HP-H5), originating from Asia, were detected in domestic poultry and wild birds in Canada and the US. These clade 2.3.4.4 GsGD-HP-H5 viruses included reassortants possessing North American lineage gene segments; were detected in wild birds in the Pacific, Central, and Mississippi flyways; and caused the largest HP IAV outbreak in poultry in US history. To determine if an antibody response indicative of previous infection with clade 2.3.4.4 GsGD-HP-H5 IAV could be detected in North American wild waterfowl sampled before, during, and after the 2014–15 outbreak, sera from 2,793 geese and 3,715 ducks were tested by blocking enzyme-linked immunosorbent assay and hemagglutination inhibition (HI) tests using both clade 2.3.4.4 GsGD-HPH5 and North American lineage low pathogenic (LP) H5 IAV antigens. We detected an antibody response meeting a comparative titer-based criteria (HI titer observed with 2.3.4.4 GsGD-HP-H5 antigens exceeded the titer observed for LP H5 antigen by two or more dilutions) for previous infection with clade 2.3.4.4 GsGD-HP-H5 IAV in only five birds, one Blue-winged Teal ( Spatula discors ) sampled during the outbreak and three Mallards ( Anas platyrhynchos ) and one Canada Goose ( Branta canadensis ) sampled during the post-outbreak period. These serologic results are consistent with the spatiotemporal extent of the outbreak in wild birds in North America during 2014 and 2015 and limited exposure of waterfowl to GsGD-HP-H5 IAV, particularly in the central and eastern US.
The proliferation of antibiotic resistant bacteria in the environment has potential negative economic and health consequences. Thus, previous investigations have targeted wild animals to understand the occurrence of antibiotic resistance in diverse environmental sources. In this critical review and synthesis, we summarize important concepts learned through the sampling of wildlife for antibiotic resistant indicator bacteria. These concepts are helpful for understanding dissemination of resistance through environmental pathways and helping to guide future research efforts. Our review is comprised of six sections. The first section briefly introduces antibiotic resistance as it pertains to bacteria harbored in environmental sources such as wild animals. Next, we differentiate wildlife from other animals in the context of how diverse taxa provide different information on antibiotic resistance in the environment. In the third section, we identify representative research and seminal works that illustrate important associations between the occurrence of antibiotic resistant bacteria in wildlife and anthropogenic inputs into the environment. For example, we highlight numerous investigations that support the premise that anthropogenic inputs into the environment drive the occurrence of antibiotic resistance in bacteria harbored by free-ranging wildlife. Additionally, we summarize previous research demonstrating foraging as a mechanism by which wildlife may be exposed to anthropogenic antibiotic resistance contamination in the environment. In the fourth section of our review, we summarize molecular evidence for the acquisition and dissemination of resistance among bacteria harbored by wildlife. In the fifth section, we identify what we believe to be important data gaps and potential future directions that other researchers may find useful towards the development of efficient, informative, and impactful investigations of antibiotic resistant bacteria in wildlife. Finally, we conclude our review by highlighting the need to move from surveys that simply identify antibiotic resistant bacteria in wildlife towards hypothesis-driven investigations that: (1) identify point sources of antibiotic resistance; (2) provide information on risk to human and animal health; (3) identify interventions that may interrupt environmentally mediated pathways of antibiotic resistance acquisition/transmission; and (4) evaluate whether management practices are leading to desirable outcomes.
We reviewed necropsy records of 124 Whooping Cranes ( Grus americana ) recovered following reintroduction of 268 individuals from 2001 to 2016 in the eastern US. Causes of death were determined in 62% (77/124) of cases facilitated by active monitoring that limited decomposition and scavenging artifact. The greatest proportions of mortality were caused by predation (0.468; 95% confidence interval 0.356–0.580; 36/77), collision with power lines or vehicles (0.260; 0.162–0.358; 20/77), and gunshot (0.169; 0.085–0.253; 13/77). Six deaths were attributed to infection (0.078; 0.018–0.138; 6/77), including bacterial and fungal etiologies. Lead analysis of 50 liver samples yielded two results with elevated concentrations (3.65 and 10.97 ppm wet weight), and 10 bone samples from partial carcasses lacking suitable liver tissue resulted in one elevated result (48.82 ppm dry weight). These data indicate that underlying subclinical or clinical lead toxicosis may be a factor in up to 5% of deaths attributed to predation or impact trauma. Brain cholinesterase activity testing indicated no exposure to organophosphate or carbamate pesticides (mean±SD=17.32±2.90 µmol/min/g, 31/71). The causes of death and potential underlying factors summarized in this study constitute the first definitive mortality survey of migratory Whooping Cranes based on a high carcass recovery rate. Causes of death by infectious etiologies remained comparatively rare in this study, and occurred as single cases with no evidence of sustained transmission among reintroduced Whooping Cranes.
We tested coyote ( Canis latrans ), fox ( Urocyon cinereoargenteus , Vulpes vulpes ), and raccoon ( Procyon lotor ) sera for influenza A virus (IAV) exposure. We found 2/139 samples (1 coyote, 1 raccoon) had IAV antibodies and hemagglutination inhibition assays revealed the antibodies to the 2009/2010 H1N1 human pandemic virus or to the 2007 human seasonal H1N1 virus.
Between 2014 and 2017, widespread seabird mortality events were documented annually in the Bering and Chukchi seas, concurrent with dramatic reductions of sea ice, warmer than average ocean temperatures, and rapid shifts in marine ecosystems. Among other changes in the marine environment, harmful algal blooms (HABs) that produce the neurotoxins saxitoxin (STX) and domoic acid (DA) have been identified as a growing concern in this region. Although STX and DA have been documented in Alaska (US) for decades, current projections suggest that the incidence of HABs is likely to increase with climate warming and may pose a threat to marine birds and other wildlife. In 2017, a multispecies die-off consisting of primarily Northern Fulmars ( Fulmarus glacialis ) and Short-tailed Shearwaters ( Ardenna tenuirostris ) occurred in the Bering and Chukchi seas. To evaluate whether algal toxins may have contributed to bird mortality, we tested carcasses collected from multiple locations in western and northern Alaska for STX and DA. We did not detect DA in any samples, but STX was present in 60% of all individuals tested and in 88% of Northern Fulmars. Toxin concentrations in Northern Fulmars were within the range of those reported from other STX-induced bird die-offs, suggesting that STX may have contributed to mortalities. However, direct neurotoxic action by STX could not be confirmed and starvation appeared to be the proximate cause of death among birds examined in this study.
Invasive rodents on islands have adverse effects on native birds in island ecosystems, and rats are the most common culprits. Recently, house mice ( Mus musculus ) in the South Atlantic were found preying on three species of albatross chicks. Here, we show that house mice can also prey on nesting adult Laysan Albatross ( Phoebastria immutabilis ) on Midway Atoll National Wildlife Refuge (US). In contrast to mouse attacks on albatross in the South Atlantic, where mice targeted the rump and crown of chicks, on Midway, mice targeted nesting adults mainly on the back. For both regions, the outcome was similar with reduced nesting success. In the case of Midway, reduced nesting success was due to nest abandonment or mortality of one or both parents because of secondary bacterial infections. Mouse-induced mortality of adult albatross has the potential to have a more potent demographic effect because of their much higher natural survivorship once they reach adulthood.
Haemosporidian parasites may impact avian health and are subject to shifts in distribution and abundance with changing ecologic conditions. Therefore, understanding variation in parasite prevalence is important for evaluating biologically meaningful changes in infection patterns and associated population level impacts. Previous research in western Alaska, US, indicated a possible increase in Leucocytozoon spp. infection between Emperor Geese ( Anser canagicus ) sampled in 1996 (<1%, n =134) and during 2011–12 (19.9%, 95% confidence interval [CI]: 3.0–36.8%, n =77); however, different detection methods were used for these estimates. Prior research in this same region identified a lack of Leucocytozoon spp. parasites (0%, n =117) in sympatrically breeding Cackling Geese ( Branta hutchinsii minima ) in 2011. We molecularly screened blood samples collected from sympatrically breeding Emperor and Cackling Geese in western Alaska during additional breeding seasons to better assess temporal and species-specific variation in the prevalence of blood parasites. We found similar prevalence estimates for Leucocytozoon spp. parasites in Emperor Goose blood samples collected in 1998 and 2014, suggesting consistent infection of Emperor Geese with blood parasites at these time points. Using samples from sympatric geese sampled during 2014, we found evidence for a higher incidence of parasites among Emperor Geese (20.3%, 95% CI: 11.8–32.7%) compared to Cackling Geese (3.6%, 95% CI: 1.1–11.0%), reinforcing the previous finding of species-specific differences in infection. Furthermore, we detected Leucocytozoon , Haemoproteus , and Plasmodium spp. blood parasites in unflighted goslings of both species, supporting the possible transmission of these parasites at western Alaska breeding grounds. Our results help to clarify that prevalence of Leucocytozoon spp. parasites have probably remained consistent among Emperor Geese breeding in western Alaska since the late 1990s and that this species may disproportionally harbor Leucocytozoon spp. compared to sympatrically breeding Cackling Geese.
Oil spills represent a continued threat to marine wildlife. Although the public expects, and the State of California, US requires, oiled animals to be rescued for rehabilitation and release, scientists have questioned the welfare and conservation value of capture and rehabilitation of oiled wildlife, based on poor postrelease survival documented in the few available studies. In May 2015, Plains Pipeline 901 spilled >100,000 gallons of oil near Refugio State Beach, California. Many California Brown Pelicans ( Pelecanus occidentalis californicus ) were oiled; capture and rehabilitation efforts began within 1 d. Ultimately, 65 live birds were captured, including 50 pelicans. Forty-six pelicans survived and were released. Of these, 12 adults (six male, six female) were fitted with solar-powered GPS satellite Platform Terminal Transmitters (PTT) and released in June 2015. In early July, we captured eight adult (three male, four female, one unknown), unoiled pelicans from the Ventura, California area. These control birds were similarly instrumented and released immediately. At 6 mo after release, PTTs from nine of 12 oiled pelicans and six of eight control pelicans were still transmitting; at 1 yr, those numbers decreased to two of 12 and two of eight, respectively. Survival analysis revealed no difference in survival between oiled and control birds. Although our sample size is limited, these data demonstrate that most oiled and rehabilitated pelicans can survive for 6 mo following release, and some individuals can survive over 1 yr.
We calculated reference intervals for 48 blood parameters from 120 wild American alligators ( Alligator mississippiensis ) in South Florida, US. Although previously reported by others, this study includes additional parameters not yet reported in wild populations. Most previously reported blood parameter values were similar to ours and fell within our reference intervals.
Only one virus, Avipox, has been documented previously in wild birds in Hawaii. Using immunohistochemistry and PCR, we found that two native threatened Hawaiian Geese ( Branta sandvicensis ), one with multicentric histiocytoma and the other with toxoplasmosis, and one Laysan Albatross ( Phoebastria immutabilis ) with avian pox were infected with reticuloendotheliosis virus (REV). The virus was isolated from one of the geese by cell culture. Surveys of other Hawaiian geese with various pathologies, avian pox cases, and pox viral isolates using PCR failed to reveal REV, suggesting that the virus is uncommon, at least in samples examined. The full genome of the Gag, Pol, and Env genes were sequenced for all three infected birds and revealed geographic divergence of the Pol gene, suggesting it to be under strong selective pressure. Our finding of REV in Hawaii makes this only the second virus documented in native Hawaiian birds associated with pathology. Moreover, the presence of REV in a pelagic seabird is unusual. Future surveys should seek the reservoir of the virus in efforts to trace its origins.
Chemical immobilization agents that provide rapid induction time, short duration of action, wide margin of safety, and postreversal recovery are important attributes to the handling process of immobilized animals. We evaluated differences in induction, recovery, and physiologic parameters in 23 (13 female, nine adults and four yearlings; 10 male, nine adults and one yearling) free-ranging bobcats ( Lynx rufus ) chemically immobilized with an intramuscular combination of ketamine (10 mg/kg) and xylazine (KX; 1.5 mg/kg; n =11) or a combination of butorphanol (0.8 mg/ kg), azaperone (0.27 mg/kg), and medetomidine (BAM; 0.32 mg/kg; n =12). Induction parameters, time to first effect, hemoglobin oxygen saturation, and anesthesia between bobcats administered KX and BAM were similar. Pulse rate was significantly higher for KX than for BAM. Time to standing and full recovery after reversal were faster for bobcats administered BAM than KX. Six of 11 (55%) bobcats given KX were effectively immobilized with a single injection, and five required additional drugs to allow adequate time for processing. Of 12 bobcats given BAM, six (50%) were effectively immobilized with a single injection, three (25%) individuals were not completely immobilized and required additional doses to allow adequate time for processing, and three (25%) required additional doses after complete arousal during processing. We found that BAM provided reduced sedation and processing times (<30 min), whereas KX provided extended sedation and processing times beyond 30 min. We suggest that researchers increase initial BAM drug volumes for yearling and adult bobcats at time of processing and consider taking appropriate safety precautions when handling free-ranging bobcats.
The protistan genus Epistylis contains freshwater colonial species that attach to aquatic organisms in an epibiotic or parasitic relationship. They are known to attach to the epidermis and shells of aquatic turtles, but have not been reported to cause heavy infestations or morbidity in turtles. We documented heavy infestations of Epistylis spp. in several populations of Sonoran mud turtles ( Kinosternon sonoriense ) inhabiting livestock ponds in Arizona, USA, and rough-footed mud turtles ( Kinosternon hirtipes ) from livestock ponds in Texas, USA, over the course of several years. Severe Epistylis spp. infestations on mud turtles appeared to alter diving and swimming behavior when compared to uninfested conspecifics. Infestations were cleared in captivity using tap water or a 10% salt solution, and the turtles had no permanent damage to their shell or epidermis upon clearing. While several of the mud turtles we observed had poor body condition, it is possible that the severe infestations we observed were caused by a comorbidity associated with a pathogen, parasite, or poor habitat quality that made the turtles more susceptible to the Epistylis spp. infestation. Further research on causes for these severe infestations are warranted because they contribute to changes in behavior of the heavily infested turtles and may contribute to morbidity in Kinosternon spp. when mud turtles inhabit extremely warm, shallow, eutrophic aquatic habitats, such as livestock ponds.
To assess infection with or exposure to endo- and ectoparasites in Alaska brown bears ( Ursus arctos ), blood and fecal samples were collected during 2013–17 from five locations: Gates of the Arctic National Park and Preserve; Katmai National Park; Lake Clark National Park and Preserve; Yakutat Forelands; and Kodiak Island. Standard fecal centrifugal flotation was used to screen for gastrointestinal parasites, molecular techniques were used to test blood for the presence of Bartonella and Babesia spp., and an ELISA was used to detect antibodies to Sarcoptes scabiei , a species of mite recently associated with mange in American black bears ( Ursus americanus ). From fecal flotations ( n =160), we identified the following helminth eggs: Uncinaria sp. ( n =16, 10.0%), Baylisascaris sp. ( n =5, 3.1%), Dibothriocephalus sp. ( n =2, 1.2%), and taeniid-type eggs ( n =1, 0.6%). Molecular screening for intraerythrocytic parasites ( Babesia spp.) and intracellular bacteria ( Bartonella spp.) was negative for all bears tested. We detected antibodies to S. scabiei in six of 59 (10.2%) individuals. The relatively low level of parasite detection in this study meets expectations for brown bear populations living in large, relatively undisturbed habitats near the northern edge of the range. These results provide a contemporary understanding of parasites in Alaska brown bears and establish baseline levels of parasite presence to monitor for changes over time and relative to ecologic alterations.
Plague, caused by Yersinia pestis , is a widespread threat to endangered black-footed ferrets ( Mustela nigripes ) and their primary prey, prairie dogs ( Cynomys spp.). Wildlife biologists most commonly manage plague using insecticides to control fleas, the primary vectors of Y. pestis . We tested edible baits containing the insecticides lufenuron and/or nitenpyram in prairie dogs. During a laboratory study, we treated 26 white-tailed prairie dogs ( Cynomys leucurus ) with lufenuron at 300 mg/kg body mass. All animals remained clinically healthy over the 9 wk monitoring period. Although serum lufenuron concentrations were >130 ppb in two treatment groups at week 1, concentrations declined to ≤60 ppb after 3 wk in non-torpid prairie dogs and after 7 wk in torpid prairie dogs. In a field experiment, we tested baits containing a combination of 75 mg lufenuron and 6 mg nitenpyram, respectively, in black-tailed prairie dogs ( Cynomys ludovicianus ). We uniformly distributed baits at 125 baits/ha on two plots (treated once) and 250 baits/ha on two plots (each treated twice 4.4 wk apart). Following treatments, flea abundance increased on prairie dogs and remained stable in burrows. Our findings indicate that baits containing lufenuron and nitenpyram, at the reported treatment rates, are ineffective tools for flea control on prairie dogs. Future experiments might evaluate efficacy of higher doses of lufenuron and nitenpyram, and repetitive treatments at differing intervals over time to evaluate potentially therapeutic treatments.
We evaluated a combination of nalbuphine HCl (40 mg/mL), azaperone tartrate (10 mg/mL), and medetomidine HCl (10 mg/mL), a combination known as NAM or NalMed-A, in 23 ringtails ( Bassariscus astutus ) during 29 handling events for a radio-collaring study in southern Oregon, US, from August 2020 to March 2022. The combination was delivered to ringtails by hand injection at 0.075 mL NAM per estimated 1 kg body mass. The mean (± standard deviation, SD) dosage calculated post hoc was 3.366 (±0.724) mg/kg nalbuphine, 0.841 (±0.181) mg/kg medetomidine, and 0.841 (±0.181) mg/kg azaperone. All captured ringtails were effectively immobilized with a mean (SD) induction time of 13.24 (±3.57) min. The medetomidine and nalbuphine components were antagonized with a combination of atipamezole and naltrexone HCl with a mean (SD) recovery time of 2.48 (±1.94) min. This combination appeared to be safe and effective for immobilizing ringtails with a low volume dose, smooth antagonism, and rapid recovery. In addition, NAM does not contain any drugs that are US Drug Enforcement scheduled, which makes it useful for immobilization procedures by wildlife professionals in the US.
Chemical immobilization is commonly used to capture and handle free-ranging elk ( Cervus canadensis ). Butorphanol-azaperone-medetomidine (BAM) and nalbuphine-medetomidine-azaperone (NalMed-A) are compounded drug combinations that are lower-scheduled in the US than drugs historically used for elk immobilizations. We compared BAM and NalMed-A for immobilization of free-ranging elk using free-darting and Clover trapping. From January 2020 to April 2022, 196 female elk were immobilized in Pennsylvania, USA. We report vital rates, induction and recovery times, and the need for supplemental drugs. We built mixed-effects logistic regression models to describe differences between drug choice based on induction and recovery times, capture method, and individual variation. Several models were competing, including our null model, which suggests that BAM and NalMed-A are comparable based on the parameters we evaluated. Supplemental drug administration was more frequently needed in NalMed-A immobilizations (21.2%) than in BAM immobilizations (9.0%). Overall, we found minor differences between BAM and NalMed-A, both of which appear to be effective for immobilizing elk in both free-darting and Clover trapping scenarios when performing moderately invasive, minimally painful procedures on free-ranging elk.