George V. Kollias

Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches

Evidence is accumulating that genetic variation within individual hosts can influence their susceptibility to pathogens. However, there have been few opportunities to experimentally test this relationship, particularly within outbred populations of non-domestic vertebrates. We performed a standardized pathogen challenge in house finches (Carpodacus mexicanus) to test whether multilocus heterozygosity across 12 microsatellite loci predicts resistance to a recently emerged strain of the bacterial pathogen, Mycoplasma gallisepticum (MG). We simultaneously tested whether the relationship between heterozygosity and pathogen susceptibility is mediated by differences in cell-mediated or humoral immunocompetence. We inoculated 40 house finches with MG under identical conditions and assayed both humoral and cell-mediated components of the immune response. Heterozygous house finches developed less severe disease when infected with MG, and they mounted stronger cell-mediated immune responses to phytohaemagglutinin. Differences in cell-mediated immunocompetence may, therefore, partly explain why more heterozygous house finches show greater resistance to MG. Overall, our results underscore the importance of multilocus heterozygosity for individual pathogen resistance and immunity.

SEROPREVALENCE OF INFECTIOUS DISEASE AGENTS IN FREE-RANGING FLORIDA PANTHERS (FELIS CONCOLOR CORYI)

Serum samples obtained from 38 free-ranging Florida panthers (Felis concolor coryi) in southern Florida, March 1978 through February 1991, were tested for antibodies against eight bacterial, parasitic, and viral disease agents. Sera were positive for antibodies against feline panleukopenia virus (FPV) (78%), feline calicivirus (56%), feline immunodeficiency virus/puma lentivirus (37%), feline enteric coronavirus/feline infectious peritonitis virus (19%), and Toxoplasma gondii (9%). All samples were seronegative for Brucella spp., feline rhinotracheitis virus, and pseudorabies virus. In addition, all the animals tested were negative for feline leukemia virus p27 antigen as determined by enzyme-linked immunosorbent assay. Feline panleukopenia virus was considered to be a potentially significant disease agent; FPV antibodies occurred in the highest prevalences in older age classes (P = 0.027) and in panthers living in the dense mixed hardwood swamps in the western portion of their range compared to the open cypress and sawgrass prairies to the east (P = 0.096). Because <50 animals remain in this relict population and the probable resultant depression of genetic diversity and lowered disease resistance, FPV or other disease agents could contribute to the extinction of this endangered subspecies.

EXPERIMENTAL INFECTION OF HOUSE FINCHES WITH MYCOPLASMA GALLISEPTICUM

Mycoplasma gallisepticum (MG) has caused an endemic upper respiratory and ocular infection in the eastern house finch (Carpodacus mexicanus) after the epidemic first described in 1994. The disease has been studied by a number of investigators at a population level and reports describe experimental infection in group-housed MG-free house finches. Because detailed observation and evaluation of individual birds in group housed passerines is problematic, we studied individually housed house finches that were experimentally inoculated with the finch strain of MG in a controlled environment. To accomplish this, a study was conducted spanning the period of November 2001–April 2002 with 20 MG-free (confirmed by the rapid plate agglutination assay and polymerase chain reaction [PCR] assay) eastern house finches captured in the Cayuga Basin area of central New York (USA) in the summer of 2001. After a period of acclimatization and observation (12 wk), 20 finches were inoculated with a 0.05-ml aliquot of MG (3.24×105 colony-forming units/ml) via bilateral conjunctival sac instillations. Two additional finches acted as controls and were inoculated in the same manner with preservative-free sterile saline solution. After inoculation, all finches except the controls exhibited clinical signs of conjunctivitis within 2–6 days. The progression of the disease was evaluated by several methods, including PCR, behavioral observations, and physical examination including eye scoring, body weight, and body condition index. Over a period of 21 wk, MG-infected finches developed signs of disease and recovered (80%), developed signs of disease and progressed to become chronically infected (15%), or died (5%). We hypothesize that the high survival rate and recovery of these finches after infection was associated with the use of controlled environmental conditions, acclimatization, a high plane of nutrition, and low stocking (housing) density, all of which are factors documented to be important in the outcome of MG infections in domestic poultry and other species.

Mycoplasmal conjunctivitis in songbirds from New York.

A field study was conducted to determine the prevalence of conjunctivitis and Mycoplasma gallisepticum (MG) infections in house finches (Carpodacus mexicanus) and other songbirds common to bird feeders in Tompkins County (New York, USA). Eight hundred two individuals of 23 species and nine families of birds were captured and given physical examinations during the 14 mo study beginning in February 1998. Clinical conjunctivitis (eyelid or conjunctival swelling, erythema, and discharge) was observed in 10% (19/196) of house finches examined, and only in the winter months from November to March. Unilateral conjunctivitis was observed in 79% (15/19) of affected house finches; one case developed bilateral disease between 8 and 18 days following initial examination. Conjunctivitis was observed in a similar proportion of males and females sampled, and body condition scores and wing chord lengths were not significantly different between diseased and non-diseased house finches. Mycoplasma gallisepticum was isolated from 76% (13/17) of finches with conjunctivitis and 2% (3/168) of clinically normal house finches sampled during the study. DNA fingerprints of 11 MG isolates using random amplification of polymorphic DNA (RAPD) techniques showed no apparent differences in banding patterns over the course of the study, suggesting persistence of a single MG strain in the study population. The prevalence of conjunctivitis and MG infections declined in house finches between February/ March 1998 and February/March 1999 (23% to 6%, and 20% to 5%, respectively), but only the former was significant (P < 0.05). Conjunctivitis was also observed in four American goldfinches (Carduelis tristis) and one purple finch (Carpodacus purpureus). Mycoplasma gallisepticum infection was confirmed in the purple finch, the first documented case of MG-associated conjunctivitis in this species. The purple finch isolate was similar to house finch isolates from the study site by RAPD analysis. Positive plate agglutination (PA) tests were recorded in one other goldfinch and two purple finches, suggesting exposure of these individuals to MG. Positive PA tests were also obtained from two brown-headed cowbirds (Molothrus ater) and four tufted titmice (Parus bicolor), but MG infection could not be confirmed in these cases due to lack of samples. Based on these findings, the prevalence of MG infections in hosts other than house finches appear to be low in the population sampled. There is growing evidence, however, that songbird species other than house finches are susceptible to MG infection and disease.

HOST RANGE AND DYNAMICS OF MYCOPLASMAL CONJUNCTIVITIS AMONG BIRDS IN NORTH AMERICA

An epidemic of conjunctivitis among house finches (Carpodacus mexicanus) caused by Mycoplasma gallisepticum (MG) bacterial infections was first described in 1994. The disease exhibits high primary host specificity, but has been isolated from a limited number of secondary avian hosts at various times and locations. We used records from the House Finch Disease Survey, a continent-wide, volunteer monitoring project, to document the host range of conjunctivitis in birds at feeding stations and to investigate how disease in house finches might influence the spread of conjunctivitis to other hosts. Between 1994 and 1998, participants recorded 675 cases of conjunctivitis in 31 species other than house finches in eastern North America. Seventy five % of these cases were observed among three species: American goldfinches (Carduelis tristis), purple finches (Carpodacus purpureus) and house sparrows (Passer domesticus). The proportion of sites with diseased wintering populations of the three species increased over the 4 yr study and coincided with range expansion of conjunctivitis in house finches. Sites with diseased house finches present were significantly more likely to report conjunctivitis in each of the three species during the same month. These observations are most consistent with transmission of an infectious agent (presumably MG) from house finches to these secondary hosts via spillover of localized epidemics, rather than sustained interspecific transmission.

RISK FACTORS ASSOCIATED WITH MYCOPLASMAL CONJUNCTIVITIS IN HOUSE FINCHES

Observations from a citizen-based survey were used to identify potential risk factors associated with mycoplasmal conjunctivitis (Mycoplasma gallisepticum) in eastern house finches (Carpodacus mexicanus). Between November 1994 and October 1996, 778 volunteers provided 7,224 monthly observations at residential bird feeding sites across an eight state region in the eastern USA. Information collected by questionnaires included health status of house finches and four sympatric passerine species, types and number of bird feeders maintained, neighborhood housing locale and altitude of the observation site. Bivariate analyses revealed that house finches were 14 to 72 times as likely to be observed with conjunctivitis than the sympatric species studied. Year of the study, season, and the presence of platform, hopper, and tube type feeders were significantly associated with conjunctivitis in house finches. Multivariate analysis using a logistic regression model suggests that increased risk of conjunctivitis in house finches was associated with the second year of the study (the third year of the outbreak), the cooler non-breeding periods from September through March, and the presence of tube style feeders. In addition, the presence of raised platform type feeders may have been protective against conjunctivitis in house finches. Prevention of spread of this disease may include modifying bird feeding activities based on season and type of feeder.

DYNAMICS OF CONJUNCTIVITIS AND MYCOPLASMA GALLISEPTICUM INFECTIONS IN HOUSE FINCHES

Abstract Conjunctivitis, an infectious disease caused by Mycoplasma gallisepticum (MG), has produced a significant decline in eastern House Finches (Carpodacus mexicanus) of North America. In this paper, we present findings from two complementary studies designed to clarify annual and seasonal trends of MG infections in House Finches from the northeastern United States. The first was a field study of House Finches common to urban and residential habitat from Mercer County, New Jersey. We documented conjunctivitis in 11% (188/1,651) of the birds examined. Conjunctivitis prevalence in House Finches ranged from 0 to 43% per month, and exhibited marked seasonal fluctuation (elevations during fall and winter months and lower disease prevalence during the breeding season). There was excellent intermethod agreement on disease prevalence when measured by either presence of physical signs (conjunctivitis) or MG infection (kappa = 0.75). During the peak of the breeding season (April through June), conjunctivitis was present in a greater proportion of males lacking a cloacal protuberance than males with a cloacal protuberance (P < 0.01), but was similar between breeding and nonbreeding females. The second study, a volunteer survey, revealed the proportion of northeastern U.S. monitoring sites with at least one diseased House Finch each month ranged from a peak of 59% (August 1995) to a minimum of 12% (July 1999). Subsequent to the epidemic peak of disease in 1995, a series of recurring cycles occurred, with elevations in those proportions noted in late fall and winter and minima during the breeding season. Mycoplasmal conjunctivitis now appears endemic among House Finches of that region and demonstrates dynamics consistent with annual variation in host density.

Characterization of Experimental Mycoplasma gallisepticum Infection in Captive House Finch Flocks

Abstract The use of controlled, horizontal-transmission experiments provides detailed information on the spread of disease within fixed social groups, which informs our understanding of disease dynamics both in an empirical and theoretical context. For that reason, we characterized in 2002, horizontal transmission of Mycoplasma gallisepticum (MG) in two flocks of 11 wild-caught house finches housed in outdoor aviaries over a 6-mo period. All birds were initially free of MG by a polymerase chain reaction (PCR)-based test, rapid plate agglutination (RPA), and the scoring of physical signs. We inoculated one flock member bilaterally in the palpebral conjunctiva and reintroduced it into its cage. Index birds developed conjunctivitis within 3 to 5 days but died 13 and 20 days postinfection (PI) possibly because of very severe weather. The proportion of birds with physical signs increased gradually, reached 40% at 6 wk PI, and fluctuated around 40% until 21 wk PI. By the time our experiment ended at 24.5 wk PI, 28% of the birds still exhibited physical signs. Across both flocks, 80% of the birds developed unilateral or bilateral conjunctivitis, and several birds relapsed. The appearance of physical signs in new individuals occurred between 10 and 144 days PI (median 41 days PI). Physical signs lasted 1–172 days (median 42 days). Birds that became infected earlier during the experiment developed more severe conjunctivitis, and there was a tendency for birds that developed bilateral conjunctivitis to develop physical signs earlier. Most birds that developed physical signs of MG were also PCR- and RPA-positive, although we detected a single asymptomatic carrier and a single symptomatic false negative. No birds died as a result of secondary MG infection.

INFECTIOUS AND PARASITIC DISEASES AND CONTAMINANT-RELATED PROBLEMS OF NORTH AMERICAN RIVER OTTERS (LONTRA CANADENSIS): A REVIEW

Abstract The aquatic North American river otter (Lontra canadensis), a charismatic nonendangered mustelid, presently occupies a greatly reduced range. The species is common in zoos and has economic value as a furbearer. At least 17 states and one Canadian province have undertaken recent reintroduction programs. Nevertheless, little has been published on nonparasitic diseases of river otters, and little is known of the clinical significance of most of their parasitic infections. Records of environmental contaminant-related diseases and traumatic injuries in free-ranging North American river otters are also rare. This paper reviews present knowledge of North American river otter diseases, especially those with the greatest potential for impacting reintroduction programs.

SURGICAL TECHNIQUE FOR INTRA-ABDOMINAL RADIOTRANSMITTER PLACEMENT IN NORTH AMERICAN RIVER OTTERS (LONTRA CANADENSIS)

Abstract Twenty-two free-ranging North American river otters (Lontra canadensis) from northern and eastern New York were captured and surgically implanted with radiotransmitters as part of a relocation project. The surgical technique involved an incision in the paralumbar fossa and transection through the abdominal musculature to introduce a radiotransmitter into the abdominal cavity. Two complications were encountered. Excessive hemorrhage occurred during one procedure. The otter was treated for blood loss with fluids, and it recovered uneventfully. Surgical incision infection occurred in a second animal. The otter was treated with metronidazole and enrofloxacin, and the wound was cleaned daily with chlorhexidine. The otter recovered uneventfully. Otters were released in western New York state. Postrelease monitoring via radiotelemetry revealed that the otters became established in their new ranges. The intra-abdominal implants did not affect their survival or reproductive potential.