Current trends in the application of non-invasive genetic sampling to study Neotropical birds: Uses, goals, and conservation potential

The non-invasive collection of biological samples has proven useful to study a diverse array of research topics worldwide. Here, we present a systematic bibliographical synthesis exploring how the non-invasive collection of genetic samples has been used to study avian populations in the Neotropics. We searched international online databases for scientific publications, spanning from 2007 to 2017, to describe the trends and identify the sample types used, species studied, and research questions addressed. The analysis of 21 articles showed that shed feathers were most frequently used (66.7% of articles), followed by carcasses (14.2%), eggs (9.5%), and non-invasively obtained blood (4.8%); one study used both feces and shed feathers. Most studies addressed population genetic issues (38.1%), followed by species identification (28.6%), phylogenetic questions (14.3%), molecular sexing (9.5%), and parentage analyses (9.5%). Brazil produced almost half (47.6%) of the publications retrieved. Despite an increasing interest in using non-invasive sampling to study Neotropical avifauna, its application is still largely concentrated in the most developed countries in this region and to explore a limited number of questions. A more regular use of non-invasive sampling would help advance the knowledge of ecological, behavioral, genetic, and evolutionary aspects of Neotropical birds. Investigating the extent of human–wildlife conflict, such as impact of road-kills, illegal traffic, and collision with aerial infrastructure or unmanned vehicles, is an underexplored avenue of research in which this method could be of much help. Non-invasive genetic sampling can help tackle conservation problems and pave the way to scientifically informed conservation policies in this avian biodiversity hotspot.

The sarolga: conservation implications of genetic and visual evidence for hybridization between the brolga Antigone rubicunda and the Australian sarus crane Antigone antigone gillae

To investigate the extent of suspected hybridization between the brolga Antigone rubicunda and the Australian sarus crane Antigone antigone gillae, first noted in the 1970s, we analysed the genetic diversity of 389 feathers collected from breeding and flocking areas in north Queensland, Australia. We compared these with 15 samples from birds of known identity, or that were phenotypically typical. Bayesian clustering based on 10 microsatellite loci identified nine admixed birds, confirming that Australian cranes hybridize in the wild. Four of these were backcrosses, also confirming that wild Australian crane hybrids are fertile. Genetic analyses identified 10 times more hybrids than our accompanying visual field observations. Our analyses also provide the first definitive evidence that both brolgas and sarus cranes migrate between the Gulf Plains, the principal breeding area for sarus cranes, and major non-breeding locations on the Atherton Tablelands. We suggest that genetic analysis of shed feathers could potentially offer a cost-effective means to provide ongoing monitoring of this migration. The first observations of hybrids coincided with significantly increased opportunities for interaction between the two species when foraging on agricultural crops, which have developed significantly in the Atherton Tablelands flocking area since the 1960s. As the sarus crane is declining in much of its Asian range, challenges to the genetic integrity of the Australian sarus crane populations have international conservation significance.

Genetic rescue, the greater prairie chicken and the problem of conservation reliance in the Anthropocene

A central question in conservation is how best to manage biodiversity, despite human domination of global processes (= Anthropocene). Common responses (i.e. translocations, genetic rescue) forestall potential extirpations, yet have an uncertain duration. A textbook example is the greater prairie chicken (GRPC: Tympanuchus cupido pinnatus ), where translocations (1992–1998) seemingly rescued genetically depauperate Illinois populations. We re-evaluated this situation after two decades by genotyping 21 microsatellite loci from 1831 shed feathers across six leks in two counties over 4 years (2010–2013). Low migration rates (less than 1%) established each county as demographically independent, but with declining-population estimates (4 year average N = 79). Leks were genetically similar and significantly bottlenecked, with low effective population sizes (average N e = 13.1; 4 year N e / N = 0.166). Genetic structure was defined by 12 significantly different family groups, with relatedness r = 0.31 > half-sib r = 0.25. Average heterozygosity, indicating short-term survival, did not differ among contemporary, pre- and post-translocated populations, whereas allelic diversity did. Our results, the natural history of GRPC (i.e. few leks, male dominance hierarchies) and its controlled immigration suggest demographic expansion rather than genetic rescue. Legal protection under the endangered species act (ESA) may enhance recovery, but could exacerbate political–economic concerns on how best to manage ‘conservation-reliant’ species, for which GRPC is now an exemplar.

Contemporary premature feather loss (PFL) among common tern chicks in Lake Ontario: the return of an enigmatic developmental anomaly

In July 2014, we observed premature feather loss (PFL) among non-sibling, common tern Sterna hirundo chicks between 2 and 4 weeks of age at Gull Island in northern Lake Ontario, Canada. Rarely observed in wild birds, to our knowledge PFL has not been recorded in terns since 1974, despite the banding of tens of thousands of tern chicks across North America since then. The prevalence (5% of chicks) and extent of feather loss was more extreme than in previous reports but was not accompanied by other aberrant developmental or physical deformities. Complete feather loss from all body areas (wing, tail, head and body) occurred over a period of a few days but all affected chicks appeared vigorous and quickly began to grow replacement feathers. All but one (recovered dead and submitted for post-mortem) most likely fledged 10-20 days after normal fledging age. Secondary covert feather samples were collected from PFL chicks (n=6; including shed feathers and re-growing live feathers) and normal individuals (n=8; plucked live feathers) and were analyzed for corticosterone concentrations. There was striking temporal association between the onset of PFL and persistent strong southwesterly winds that caused extensive mixing of near-shore surface water with cool, deep lake waters. We found no evidence of feather dystrophy, concurrent developmental abnormalities or nutritional shortfall among affected chicks. Thus, the PFL we observed among common terns in 2014 was largely of unknown origin but may have been caused by unidentified pathogens or toxins welling up from these deep waters along the shoreline. PFL was not observed among common terns at Gull Island in 2015, although we did observe similar feather loss in a herring gull Larus argentatus chick in that year. Comparison with sporadic records of PFL in other seabirds suggests that PFL may be a rare, but non-specific response to a range of potential stressors. Its reemergence in penguins, and now gulls and terns, may indicate widespread environmental changes that could lead to health risks for birds and other wildlife.

Contemporary premature feather loss (PFL) among common tern chicks in Lake Ontario: the return of an enigmatic developmental anomaly

In July 2014, we observed premature feather loss (PFL) among non-sibling, common tern Sterna hirundo chicks between 2 and 4 weeks of age at Gull Island in northern Lake Ontario, Canada. Rarely observed in wild birds, to our knowledge PFL has not been recorded in terns since 1974, despite the banding of tens of thousands of tern chicks across North America since then. The prevalence (5% of chicks) and extent of feather loss was more extreme than in previous reports but was not accompanied by other aberrant developmental or physical deformities. Complete feather loss from all body areas (wing, tail, head and body) occurred over a period of a few days but all affected chicks appeared vigorous and quickly began to grow replacement feathers. All but one (recovered dead and submitted for post-mortem) most likely fledged 10-20 days after normal fledging age. Secondary covert feather samples were collected from PFL chicks (n=6; including shed feathers and re-growing live feathers) and normal individuals (n=8; plucked live feathers) and were analyzed for corticosterone concentrations. There was striking temporal association between the onset of PFL and persistent strong southwesterly winds that caused extensive mixing of near-shore surface water with cool, deep lake waters. We found no evidence of feather dystrophy, concurrent developmental abnormalities or nutritional shortfall among affected chicks. Thus, the PFL we observed among common terns in 2014 was largely of unknown origin but may have been caused by unidentified pathogens or toxins welling up from these deep waters along the shoreline. PFL was not observed among common terns at Gull Island in 2015, although we did observe similar feather loss in a herring gull Larus argentatus chick in that year. Comparison with sporadic records of PFL in other seabirds suggests that PFL may be a rare, but non-specific response to a range of potential stressors. Its reemergence in penguins, and now gulls and terns, may indicate widespread environmental changes that could lead to health risks for birds and other wildlife.

Does contemporary premature feather loss among common tern chicks in Lake Ontario reflect persistent pollutants, enigmatic diseases or novel pathogens?

We observed premature feather loss (PFL) among common terns Sterna hirundo at a small colony in northern Lake Ontario, Canada in July 2014. This condition is characterized by affected chicks losing all their wing, tail, head and body feathers several weeks after hatching. Rarely observed in wild birds, to our knowledge PFL in terns has not been recorded since 1974 (despite the banding of tens of thousands of tern chicks across North America since then). In July 2014, we observed PFL in chicks at between 2 and 4 weeks of age. The extent of feather loss was more extreme than in previous reports but was not accompanied by other aberrant developmental or physical deformities. Complete feather loss occurred over a period of a few days but all affected chicks quickly began to grow replacement feathers and all but one most likely fledged 10-20 days after normal fledging age. Feather samples, both shed feathers and re-growing live feathers, were collected from both affected chicks and normal individuals. One subsequently dead PFL chick was collected. Samples are awaiting further analysis. There was striking temporal association between the onset of PFL and persistent strong southwesterly winds that caused extensive mixing of near-shore, surface water with cool, deep lake waters. To our current knowledge it seems most probable that the PFL we observed in 2014 was caused by pathogens (viruses, bacteria, algal toxins) welling up from these deep waters along the shoreline but a direct link has not yet been made. The re-emergence of PFL in common terns may indicate acute health risks for birds and other wildlife in the Lake Ontario region and may also have potential for human health risks.