The central aim of conservation biology is to understand and mitigate the effects of human activities on biodiversity. To successfully achieve this objective, researchers must take an interdisciplinary approach that fully considers the effects, both direct and indirect, of anthropogenic disturbances on wildlife physiology and health. A recent surge in research has revealed that host-associated microbiota—the archaeal, bacterial, fungal and viral communities residing on and inside organisms—profoundly influence animal health, and that these microbial communities can be drastically altered by anthropogenic activities. Therefore, conservation practitioners should consider the disruption of host-associated microbial diversity as a serious threat to wildlife populations. Despite the tremendous potential for microbiome research to improve conservation outcomes, few efforts have been made to truly integrate these fields. In this review, we call for the microbial renaissance of conservation biology, where biodiversity of host-associated microbiota is recognized as an essential component of wildlife management practices. Using evidence from the existing literature, we will examine the known effects of anthropogenic activities on the diversity of host-associated microbial communities and integrate approaches for maintaining microbial diversity to successfully achieve conservation objectives.
In numerous animal clades, the evolutionary history of host species drives patterns of gut microbial community structure, resulting in more divergent microbiota with increasing phylogenetic distance between hosts. This phenomenon, termed phylosymbiosis, has been observed in diverse evolutionary lineages, but has been difficult to detect in birds. Previous tests of phylosymbiosis among birds have been conducted using wild individuals, and thus interspecific differences in diet and environment may have masked a phylogenetic signal. Therefore, we tested for phylosymbiosis among all 15 species of cranes (family Gruidae) housed in the same captive environment and maintained on identical diets. 16S rRNA sequencing revealed that crane species harbour distinct gut microbiota. Overall, we detected marginally significant patterns of phylosymbiosis, the strength of which was increased when including the estimates of absolute microbial abundance (rather than relative abundance) derived from microbial densities determined by flow cytometry. Using this approach, we detected the statistically significant signatures of phylosymbiosis only after removing male cranes from our analysis, suggesting that using mixed-sex animal cohorts may prevent the detection of phylosymbiosis. Though weak compared with mammals (and especially insects), these results provide evidence of phylosymbiosis in birds. We discuss the potential differences between birds and mammals, such as transmission routes and host filtering, that may underlie the differences in the strength of phylosymbiosis.
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.
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 Ͻ 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.
Exertional myopathy developed in three whooping cranes (Grus americana) secondary to routine capture, handling, and trauma. Presumptive diagnosis of exertional myopathy was based on history of recent capture or trauma, clinical signs, and elevation of aspartate aminotransferase, alanine aminotransferase, creatine kinase, lactate dehydrogenase, and serum potassium. Treatments were attempted in each case, but ultimately were not successful. Gross and microscopic lesions at necropsy confirmed the diagnosis in each case, with the leg musculature most severely affected. Guidelines for determining prognosis of exertional myopathy in cranes have been included based on the analysis of these cases and others in the literature. As treatment is largely unrewarding, prevention remains the key in controlling exertional myopathy. Identification of predisposing factors and proper handling, immobilization, and transportation techniques can help prevent development of exertional myopathy in cranes.
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.
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