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

Abstract

b s t r a c tThe 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.

Genetic characterization of oropharyngeal trichomonad isolates from wild birds indicates that genotype is associated with host species, diet and presence of pathognomonic lesions

“…These findings show that this genotype is found among many species, including raptors, columbids and other avian species like corvids and finches over the world. Actually, this is the most frequently isolated genotype from birds with clinical signs and seems to be much more related to the presence of pathognomonic lesions than the others, as previous studies have reported (Sansano-Maestre et al, 2009;Chi et al, 2013;Girard et al, 2014b). On the other hand, the absence of oropharyngeal lesions might be explained either because some samples could have been taken at an early time in the infection and the clinical signs had not developed yet or because birds could have been immunized previously and be asymptomatic carriers of the parasite for a certain time (revised in Forrester & Foster, 2008), as occurs in other trichomonad infections (Trichomonas foetus infections in cattle, as an example).…”

“…isolate from a dog (AJ784785) and T. canistomae (AY244652), in comparison with other T. gallinae isolates. Girard et al (2014b) also reported T. vaginalis-like genotypes that were present only in some species and not in others, suggesting a restricted host range or the possibility of more recently evolved organisms. Genotype ITS-OBT-Tvl-5 is another newly described genotype in Spain, and to our knowledge the first detection of this genotype in the Egyptian vulture.…”

“…Previous studies carried out in Spain and the UK, employing sequencing of the ITS1/5.8S/ITS2 region, have shown a relationship between the genetic variant and the presence of pathognomonic lesions (Sansano-Maestre et al, 2009;Lawson et al, 2011a;Chi et al, 2013;Girard et al, 2014b). In fact, only one clonal strain was detected in the British outbreaks, where it was estimated that 500,000 birds died directly from trichomonosis (Robinson et al, 2010;Lawson et al, 2011a).…”

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

“…Genetic typing of the protozoan parasites is accomplished using PCR, identifying 15 different internal transcribed spacer (ITS) subtypes of T. gallinae isolated from a diversity of avian species, with some subtypes more commonly found in certain species (Gerhold et al., 2008, Grabensteiner et al., 2010, Sansano-Maestre et al., 2009). These subtypes have been further classified by sequencing the hydrogenosomal Fe-hydrogenase gene, of which two predominant subtypes exist, delineated A1 and A2 (Girard et al., 2014b, Lawson et al., 2011). Generally, subtype A1 is isolated from songbirds, columbids, and raptors in Europe while A2 is less commonly isolated and was recently found to be the predominant subtype isolated from Pacific Coast band-tailed pigeons ( Patagioenas fasciata monolis ) in California, USA (Girard et al., 2014b).…”

“…These subtypes have been further classified by sequencing the hydrogenosomal Fe-hydrogenase gene, of which two predominant subtypes exist, delineated A1 and A2 (Girard et al., 2014b, Lawson et al., 2011). Generally, subtype A1 is isolated from songbirds, columbids, and raptors in Europe while A2 is less commonly isolated and was recently found to be the predominant subtype isolated from Pacific Coast band-tailed pigeons ( Patagioenas fasciata monolis ) in California, USA (Girard et al., 2014b). Genetic evaluation of the parasite gives us insight into the ecology and epidemiology of avian trichomonosis and refines our understanding of host associations, cross-species transmission, and spillover events.…”