Krysta H. Rogers

Trichomonas stableri n. sp., an agent of trichomonosis in Pacific Coast band-tailed pigeons (Patagioenas fasciata monilis)

Graphical abstract

Dual-pathogen etiology of avian trichomonosis in a declining band-tailed pigeon population

The Pacific Coast band-tailed pigeon (Patagioenas fasciata monilis) is a migratory game bird of North America that is at risk for population decline. Epidemics of avian trichomonosis caused by upper digestive tract infection with Trichomonas spp. protozoa in these and other doves and pigeons of the United States are sporadic, but can involve tens of thousands of birds in a single event. Herein, we analyze the role of trichomonosis in band-tailed pigeon mortality and relate spatial, temporal and demographic patterns of parasite transmission to the genetic background of the infecting organism. Infections were most common in adult birds and prevalence was high in band-tailed pigeons sampled at mortality events (96%) and rehabilitation centers (36%) compared to those that were hunter-killed (11%) or live-caught (4%). During non-epidemic periods, animals were primarily infected with T. gallinae Fe-hydrogenase subtype A2, and were less often infected with either T. gallinae subtype A1 (the British finch epidemic strain), T. stableri n. sp. (a T. vaginalis-like species), or Tritrichomonas blagburni n. sp.-like organisms. Birds sampled during multiple epidemics in California were only infected with T. gallinae subtype A2 and T. stableri. The non-clonal etiology of avian trichomonosis outbreaks in band-tailed pigeons and the risk of spill-over to raptor and passerine species highlights the need for additional studies that clarify the host range and evolutionary relationships between strains of Trichomonas spp. in regions of trichomonosis endemicity.

Ecologic drivers and population impacts of avian trichomonosis mortality events in band-tailed pigeons (Patagioenas fasciata) in California, USA

Abstract:   Avian trichomonosis, a disease typically caused by the protozoan parasite Trichomonas gallinae, is a well recognized cause of death in many avian species. In California, US, trichomonosis has caused periodic epidemics in Pacific Coast Band-tailed Pigeons (Patagioenas fasciata monilis). We summarize reported mortality events and investigate ecologic drivers and population impacts associated with epidemic mortality due to trichomonosis in Band-tailed Pigeons. Between 1945 and 2014, 59 mortality events involving Band-tailed Pigeons were reported in California with the number of reported events increasing over time. Estimated mortality for these events was variable, ranging between 10 and 10,000 pigeons. Events were most-frequently reported in Monterey (19%; 11/59) and San Luis Obispo (8%; 5/59) counties. Events often started in January (32%; 9/28) and February (50%; 14/28) and lasted 5–68 d. Impacts of mortality events on pigeon populations were indicated by Breeding Bird Survey and Christmas Bird Count abundance indices, which showed a decline in outbreak years compared to nonoutbreak years. Environmental conditions most associated with outbreak years included higher average temperatures between January and March, the period most associated with mortality events, and lower average precipitation in December just prior to mortality events. In Monterey County, events tended to occur in winters following higher acorn production of coast live oaks (Quercus agrifolia) in the fall. Weather and food abundance could be related to increased transmission or enhanced viability of Trichomonas spp. Although estimated mortality due to avian trichomonosis was highly variable across years, cumulative losses were substantial and likely to have a negative impact on population size.

Avian trichomonosis in spotted owls (Strix occidentalis): Indication of opportunistic spillover from prey

Avian trichomonosis, caused by the flagellated protozoan parasite Trichomonas gallinae, has variable pathogenicity among bird species ranging from asymptomatic infections to severe disease periodically manifesting in epidemic mortality. Traditionally, columbids are identified as highly susceptible to infection with occasional spillover into raptors that prey on infected birds. We identified avian trichomonosis in two dead California spotted owls (Strix occidentalis occidentalis) and three dead northern spotted owls (S. o. caurina) in California during 2011–2015; infection was confirmed in four owls by PCR. Pathologic lesions associated with trichomonosis in the owls included caseonecrotic lesions of the upper palate accompanied by oropharyngitis, cellulitis, myositis, and/or sinusitis. Spotted owls are known to mainly feed on small mammals; therefore, the source of infection as well as the significance of the disease in spotted owls is unclear. These owl trichomonosis cases coincided temporally and spatially with three trichomonosis epidemics in band-tailed pigeons (Patagioenas fasciata monilis). The same parasite, T. gallinae subtype A2, was isolated from the spotted owls and band-tailed pigeons, suggesting the owls became infected when opportunistically feeding on pigeons during mortality events. Avian trichomonosis is an important factor in the decline of the Pacific Coast band-tailed pigeon population with near-annual mortality events during the last 10 years and could have conservation implications for raptor species at risk, particularly those that are facing multiple threats.

Mange Caused by a Novel Micnemidocoptes Mite in a Golden Eagle ( Aquila chrysaetos ).

Abstract: A second-year, female golden eagle (Aquila chrysaetos) was live trapped in northern California because of severe feather loss and crusting of the skin on the head and legs. On physical examination, the bird was lethargic, dehydrated, and thin, with severe feather loss and diffuse hyperemia and crusting on the head, ventral wings, ventrum, dorsum, and pelvic limbs. Mites morphologically similar to Micnemidocoptes derooi were identified with scanning electron microscopy. The eagle was treated with ivermectin (0.4 mg/kg) once weekly for 7 weeks, as well as pyrethrin, meloxicam, ceftiofur crystalline free acid, and voriconazole. Although the eagles condition improved, and live mites or eggs were not evident on skin scrapings at the time of completion of ivermectin treatment, evidence of dead mites and mite feces were present after the last dose of ivermectin. Two additional doses of ivermectin and 2 doses of topical selamectin (23 mg/kg) were administered 2 and 4 weeks apart, respectively. No mite eggs, feces, or adults were evident after treatment was completed. A second golden eagle found in the same region was also affected with this mite but died soon after presentation. This is the first report, to our knowledge, of successful treatment, as well as treatment with selamectin, of mites consistent with Micnemidocoptes species in any raptorial species.

Knemidocoptic mange in wild golden eagles, California, USA

During 2012–2013 in California, USA, 3 wild golden eagles were found with severe skin disease; 2 died. The cause was a rare mite, most closely related to Knemidocoptes derooi mites. Cautionary monitoring of eagle populations, habitats, and diseases is warranted.

Polymelia and Syndactyly in a Swainson’s Hawk (Buteo swainsoni)

Abstract A hatch-year Swainson’s Hawk (Buteo swainsoni) recovered from Modoc County, California, US, on 12 August 2012 had malformations of the rear limbs consisting of bilateral polymelia and syndactyly. We describe the malformations and evaluate potential causes. Postmortem examination revealed varus rotation of both femurs and abnormal appendages originating from the distal medial surface of the tibiotarsi with two nonfunctional digits on the right leg and one digit on the left leg. There was syndactyly between digits III and IV of both feet. Avian pox viral dermatitis was present on the skin of the ventral abdomen. A definitive cause of the skeletal malformations was not identified.

Sarcocystis calchasi Outbreak in Feral Rock Pigeons (Columba livia) in California

Twenty-two feral rock pigeons (Columba livia) from 10 counties in California with ataxia, torticollis, and difficulty standing and flying were admitted to rehabilitation centers in late winter and spring of 2017 and died or were euthanized. Common necropsy findings included thin body condition, generalized deep red discoloration of organs, and hemorrhagic subcutaneous neck tissues. Meningoencephalitis was observed microscopically in 16 pigeons, and 3 also had protozoal schizonts in the brain. The most consistently affected regions of the brain were cerebellum and brainstem. Skeletal muscles, and less frequently the heart, contained large intrasarcoplasmic bradyzoites typically without inflammation. Fifteen of the 22 birds tested positive using pan-Sarcocystis polymerase chain reaction. The sequence of the amplicon was most closely related to S. calchasi, and the 8 subtyped sequences had 100% homology with S. calchasi. This investigation demonstrated the transcontinental and North American spread of S. calchasi causing a disease outbreak in free-ranging rock pigeons, thus warranting increased surveillance in susceptible native columbids.

Mycoplasmosis of House Finches (Haemorhous mexicanus) and California Scrub-Jays (Aphelocoma californica) in a Wildlife Rehabilitation Facility with Probable Nosocomial Transmission

Abstract: We describe an investigation of an outbreak of conjunctivitis in juvenile House Finches (Haemorhous mexicanus) and California Scrub-jays (Aphelocoma californica) at a central California, US wildlife rehabilitation facility. In late May 2015, the facility began admitting juvenile finches, the majority with normal eyes at intake. In June, with juvenile finches already present, the facility admitted juvenile scrub-jays, all with normal eyes at intake. In July, after conjunctivitis was observed in increasing numbers of juvenile finches and scrub-jays, carcasses were submitted for postmortem examination. Histopathology of five finches and three scrub-jays identified lymphocytic infiltrates in the ocular tissues. Conjunctival swabs from 87% (13/15) finches and 33% (4/12) scrub-jays were PCR-positive for Mycoplasma gallisepticum. One finch and two scrub-jays were PCR-positive for Mycoplasma synoviae. Additionally, gene sequencing (16S ribosomal RNA and 16S-23S intergenic spacer region) identified Mycoplasma sturni from 33% (3/9) scrub-jays. This outbreak of conjunctivitis suggested that M. gallisepticum-infected juvenile finches admitted to and maintained in a multispecies nursery likely resulted in transmission within the facility to healthy juvenile finches and scrub-jays. Evidence of other Mycoplasma spp. in finches and scrub-jays indicates that these species are susceptible to infection and may act as carriers. This outbreak highlighted the need for effective triage and biosecurity measures within wildlife rehabilitation facilities.

Avian trichomonosis mortality events in band-tailed pigeons (Patagioenas fasciata) in California during winter 2014–2015

Avian trichomonosis is an upper digestive tract disease of birds typically caused by the protozoan parasite Trichomonas gallinae. In California (U.S.A), trichomonosis is known to cause periodic epidemics in the Pacific Coast band-tailed pigeon (Patagioenas fasciata monolis), a migratory upland game bird. We summarize the mortality events that occurred during winter 2014–2015 including the duration, estimated mortality, pathology, and genetic identity of infecting parasites. Increased mortality was reported from locations in 25 counties between November 2014 and June 2015. Based on reports, carcasses received, wildlife rehabilitation center admissions, site visits, and regular monitoring by local personnel, total mortality was estimated at 18,440. At necropsy, birds had multiple coalescing lesions in the oral cavity involving the upper palate and/or around the tongue and glottis, esophagus, crop, and/or proventriculus. Birds collected from Contra Costa (63.9%; 30/47); Marin (75.0%; 6/8), San Mateo (46.7%; 14/30), and Santa Clara (35.0%; 37/106) counties were more likely to have lesions extending into their head involving muscle, sinuses, ear canals, eye sockets, and bone (χ2 = 62.9; df = 11; P < 0.001). Histopathologic findings included pharyngitis, esophagitis, myositis, and air sacculitis of the pneumatic bone of the skull. Mixed bacterial colonies were found multifocally at the fronts of the necrosis in six of the eleven birds examined histologically. Infecting trichomonads included T. gallinae subtype A2 (n = 5), un-typed T. gallinae (n = 4), mixed infection with T. gallinae subtype A2 and T. stableri (n = 1), and mixed infection with un-typed T. gallinae and T. stableri (n = 1). The winter 2014–2015 epidemic was the largest on record in terms of duration, locations, and birds affected. Infection dynamics may have been exacerbated by the drought in California. Increased monitoring of band-tailed pigeons is needed to understand the long-term impacts of large-scale mortality events on their population.