A comparison of methods for estimating raccoon abundance: Implications for disease vaccination programs

Accurate estimates of demographic parameters are critical to the management of wildlife populations, including management programs focused on controlling the spread of zoonotic diseases. Rabies managers in the United States Department of Agriculture (USDA) have applied a simple raccoon (Procyon lotor) abundance index (RAI) based on cumulative catch of unique raccoons per unit area to determine vaccine-bait distribution densities. This approach was designed to allow for both the collection of biological samples and to index raccoon abundance to determine bait densities for oral rabies programs. However, post-baiting surveillance data indicate that, on average, only 30% of raccoons sampled have vaccine induced rabies antibody titers, suggesting that bait densities may not be well calibrated to raccoon densities. We trapped raccoons using both capture-mark-recapture (CMR) and the standard RAI to evaluate the accuracy of the current index-based methodology for estimating raccoon density. We then developed a resource selection function from spatial data collected from radio-collared raccoons to standardize trap placement within the existing RAI protocol, and evaluated the performance of this modified RAI approach relative to CMR for estimating raccoon population size. Both abundance and density estimates derived using the RAI consistently underestimated raccoon population sizes compared with CMR methods. Similarly, although the use of resource selection models to inform trap placement appeared to improve the accuracy of the RAI, the effectiveness of this method was inconsistent because of an inability to account for variance in detection probabilities. Despite the logistical advantages of using indices to estimate population parameters to determine vaccine bait distribution densities, our results suggest that adjustments may be necessary to more accurately quantify raccoon abundance, which should improve the effectiveness of rabies management in the United States. In particular, estimates of detection probabilities are needed to more precisely quantify abundance estimates and ensure appropriate vaccine coverage rates. © 2012 The Wildlife Society.     

Spatial patterns of neutral and functional genetic variations reveal patterns of local adaptation in raccoon (Procyon lotor) populations exposed to raccoon rabies

Local adaptation is necessary for population survival and depends on the interplay between responses to selective forces and demographic processes that introduce or retain adaptive and maladaptive attributes. Host–parasite systems are dynamic, varying in space and time, where both host and parasites must adapt to their ever‐changing environment in order to survive. We investigated patterns of local adaptation in raccoon populations with varying temporal exposure to the raccoon rabies virus (RRV). RRV infects approximately 85% of the population when epizootic and has been presumed to be completely lethal once contracted; however, disease challenge experiments and varying spatial patterns of RRV spread suggest some level of immunity may exist. We first assessed patterns of local adaptation in raccoon populations along the eastern seaboard of North America by contrasting spatial patterns of neutral (microsatellite loci) and functional, major histocompatibility complex (MHC) genetic diversity and structure. We explored variation of MHC allele frequencies in the light of temporal population exposure to RRV (0–60 years) and specific RRV strains in infected raccoons. Our results revealed high levels of MHC variation (66 DRB exon 2 alleles) and pronounced genetic structure relative to neutral microsatellite loci, indicative of local adaptation. We found a positive association linking MHC genetic diversity and temporal RRV exposure, but no association with susceptibility and resistance to RRV strains. These results have implications for landscape epidemiology studies seeking to predict the spread of RRV and present an example of how population demographics influence the degree to which populations adapt to local selective pressures.     

Determining natal dispersal patterns in a population of North American pikas (Ochotona princeps) using direct mark-resight and indirect genetic methods

A combination of direct (mark-resight) and indirect geneticmethods were used to investigate natal dispersal patterns andgenetic population structure in a population of North Americanpikas, Ochotona princeps. Pikas are small lagomorphs found intalus habitat of alpine areas throughout western North America.Adult pikas are individually territorial and rarely disperse.I used multilocus DNA fingerprinting to identify the parentsof juvenile animals. The settlement pattern of marked juvenilesand the pattern of relatedness of pikas across the study sitewas then examined within the study area. Although juvenilesborn at the study site exhibited a philopatric settlement pattern,an isolation-by-distance analysis did not reveal clusters ofhighly related individuals within the population. The F_ST estimatesuggests little genetic differentiation between populations2 km apart, and average DNA fingerprinting band-sharing amongadults was similar to values reported for outbred species. Anaverage of 34% of the adult population was replaced each winterby immigrants. DNA fingerprinting band-sharing analysis suggeststhat these immigrants had dispersed short, intermediate, andlong distances. These findings differ from earlier studies whichused observations of marked animals only to characterize dispersalpatterns. Direct observations of marked juveniles had documenteda philopatric settlement pattern, little or no dispersal outof natal populations, and no direct evidence of long distancemovement. Of the three major hypotheses proposed to explainthe evolution of dispersal in birds and mammals, competitionfor resources, competition for mates, and inbreeding avoidance,the results of this study support a competition for resourceshypothesis, where the key resource is territory     

Spatial Ecology of Raccoons Related to Cattle and Bovine Tuberculosis in Northeastern Michigan

ABSTRACT In 1995, Mycobacterium bovis, the causative bacterium of bovine tuberculosis (bTB), was detected in 5 beef cattle operations in Alcona County, Michigan, USA. In accordance with Federal law, the operations were depopulated to prevent the spread of bTB. Subsequent wildlife surveillance programs identified high prevalence of M. bovis in mesocarnivores, including raccoons (Procyon lotor), which suggested that raccoons may be complicit in vectoring the pathogen among livestock operations. Our goal was to develop an empirical basis for generating hypotheses about the likelihood for raccoons to mediate the transmission of bTB to livestock. We found intersexual differences in scale-dependent resource selection and probability of spatial interaction that, under certain circumstances, may form the foundation for a sex-bias in disease transmission. Spatial dispersion of mixed-forest patches facilitated overlap of adjacent males, whereas female overlap zones included pastures. Within overlap zones, probabilities of interaction for male-male and male-female dyads were greater than for female-female dyads, although we documented an elevated likelihood of spatial interaction between raccoons and livestock around cattle-feeding troughs and water sources, regardless of sex. Partial regressions generated by linear models indicated that distance between nearest-neighbor mixed-forest patches explained most of this observed variation. These results supported our prediction that forest patches juxtaposed with anthropogenic features fostered social tolerance between males and, thus, facilitated spatial interaction and exploitation of anthropogenic features. In raccoons, sex and landscape composition influenced pathogen transmission potential. We suggest that livestock producers locate livestock feeding and watering features away from forest patches to mitigate future outbreaks of bTB in endemic areas.     

Extensive seed and pollen dispersal and assortative mating in the rain forest tree Entandrophragma cylindricum (Meliaceae) inferred from indirect and direct analyses

Pollen and seed dispersal are key processes affecting the demographic and evolutionary dynamics of plant species and are also important considerations for the sustainable management of timber trees. Through direct and indirect genetic analyses, we studied the mating system and the extent of pollen and seed dispersal in an economically important timber species, Entandrophragma cylindricum (Meliaceae). We genotyped adult trees, seeds and saplings from a 400‐ha study plot in a natural forest from East Cameroon using eight nuclear microsatellite markers. The species is mainly outcrossed (t = 0.92), but seeds from the same fruit are often pollinated by the same father (correlated paternity, r_p = 0.77). An average of 4.76 effective pollen donors (N_ep) per seed tree contributes to the pollination. Seed dispersal was as extensive as pollen dispersal, with a mean dispersal distance in the study plot approaching 600 m, and immigration rates from outside the plot to the central part of the plot reaching 40% for both pollen and seeds. Extensive pollen‐ and seed‐mediated gene flow is further supported by the weak, fine‐scale spatial genetic structure (Sp statistic = 0.0058), corresponding to historical gene dispersal distances (σ_g) reaching approximately 1,500 m. Using an original approach, we showed that the relatedness between mating individuals (F_ij = 0.06) was higher than expected by chance, given the extent of pollen dispersal distances (expected F_ij = 0.02 according to simulations). This remarkable pattern of assortative mating could be a phenomenon of potentially consequential evolutionary and management significance that deserves to be studied in other plant populations.     

Long‐distance dispersal in a fire‐ and livestock‐protected savanna

Savannas are highly diverse and dynamic environments that can shift to forest formations due to protection policies. Long‐distance dispersal may shape the genetic structure of these new closed forest formations. We analyzed eight microsatellite loci using a single‐time approach to understand contemporary pollen and effective seed dispersal of the tropical tree, Copaifera langsdorffii Desf. (Fabaceae), occurring in a Brazilian fire‐ and livestock‐protected savanna. We sampled all adult trees found within a 10.24 ha permanent plot, young trees within a subplot of 1.44 ha and open‐pollinated seeds. We detected a very high level of genetic diversity among the three generations in the studied plot. Parentage analysis revealed high pollen immigration rate (0.64) and a mean contemporary pollen dispersal distance of 74 m. In addition, half‐sib production was 1.8 times higher than full‐sibs in significant higher distances, indicating foraging activity preference for different trees at long distances. There was a significant and negative correlation between diameter at breast height (DBH) of the pollen donor with the number of seeds (r = ?0.640, P‐value = 0.032), suggesting that pollen donor trees with a higher DBH produce less seeds. The mean distance of realized seed dispersal (recruitment kernel) was 135 m due to the large home range dispersers (birds and mammals) in the area. The small magnitude of spatial genetic structure found in young trees may be a consequence of overlapping seed shadows and increased tree density. Our results show the positive side of closed canopy expansion, where animal activities regarding pollination and seed dispersal are extremely high.     

Fine-scale genetic structure and gene dispersal inferences in 10 neotropical tree species

The extent of gene dispersal is a fundamental factor of the population and evolutionary dynamics of tropical tree species, but directly monitoring seed and pollen movement is a difficult task. However, indirect estimates of historical gene dispersal can be obtained from the fine-scale spatial genetic structure of populations at drift-dispersal equilibrium. Using an approach that is based on the slope of the regression of pairwise kinship coefficients on spatial distance and estimates of the effective population density, we compare indirect gene dispersal estimates of sympatric populations of 10 tropical tree species. We re-analysed 26 data sets consisting of mapped allozyme, SSR (simple sequence repeat), RAPD (random amplified polymorphic DNA) or AFLP (amplified fragment length polymorphism) genotypes from two rainforest sites in French Guiana. Gene dispersal estimates were obtained for at least one marker in each species, although the estimation procedure failed under insufficient marker polymorphism, limited sample size, or inappropriate sampling area. Estimates generally suffered low precision and were affected by assumptions regarding the effective population density. Averaging estimates over data sets, the extent of gene dispersal ranged from 150 m to 1200 m according to species. Smaller gene dispersal estimates were obtained in species with heavy diaspores, which are presumably not well dispersed, and in populations with high local adult density. We suggest that limited seed dispersal could indirectly limit effective pollen dispersal by creating higher local tree densities, thereby increasing the positive correlation between pollen and seed dispersal distances. We discuss the potential and limitations of our indirect estimation procedure and suggest guidelines for future studies.     

Environmental conditions affect spatial genetic structures and dispersal patterns in a solitary rodent

The study of the spatial distribution of relatives in a population under contrasted environmental conditions provides critical insights into the flexibility of dispersal behaviour and the role of environmental conditions in shaping population relatedness and social structure. Yet few studies have evaluated the effects of fluctuating environmental conditions on relatedness structure of solitary species in the wild. The aim of this study was to determine the impact of interannual variations in environmental conditions on the spatial distribution of relatives [spatial genetic structure (SGS)] and dispersal patterns of a wild population of eastern chipmunks (Tamias striatus), a solitary rodent of North America. Eastern chipmunks depend on the seed of masting trees for reproduction and survival. Here, we combined the analysis of the SGS of adults with direct estimates of juvenile dispersal distance during six contrasted years with different dispersal seasons, population sizes and seed production. We found that environmental conditions influences the dispersal distances of juveniles and that male juveniles dispersed farther than females. The extent of the SGS of adult females varied between years and matched the variation in environmental conditions. In contrast, the SGS of males did not vary between years. We also found a difference in SGS between males and females that was consistent with male‐biased dispersal. This study suggests that both the dispersal behaviour and the relatedness structure in a population of a solitary species can be relatively labile and change according to environmental conditions.     

Pollen dispersal and genetic structure of the tropical tree Dipteryx panamensis in a fragmented Costa Rican landscape

In the face of widespread deforestation, the conservation of rainforest trees relies increasingly on their ability to maintain reproductive processes in fragmented landscapes. Here, we analysed nine microsatellite loci for 218 adults and 325 progeny of the tree Dipteryx panamensis in Costa Rica. Pollen dispersal distances, genetic diversity, genetic structure and spatial autocorrelation were determined for populations in four habitats: continuous forest, forest fragments, pastures adjacent to fragments and isolated pastures. We predicted longer but less frequent pollen movements among increasingly isolated trees. This pattern would lead to lower outcrossing rates for pasture trees, as well as lower genetic diversity and increased structure and spatial autocorrelation among their progeny. Results generally followed these expectations, with the shortest pollen dispersal among continuous forest trees (240 m), moderate distances for fragment (343 m) and adjacent pasture (317 m) populations, and distances of up to 2.3 km in isolated pastures (mean: 557 m). Variance around pollen dispersal estimates also increased with fragmentation, suggesting altered pollination conditions. Outcrossing rates were lower for pasture trees and we found greater spatial autocorrelation and genetic structure among their progeny, as well as a trend towards lower heterozygosity. Paternal reproductive dominance, the pollen contributions from individual fathers, did not vary among habitats, but we did document asymmetric pollen flow between pasture and adjacent fragment populations. We conclude that long-distance pollen dispersal helps maintain gene flow for D. panamensis in this fragmented landscape, but pasture and isolated pasture populations are still at risk of long-term genetic erosion.     

Assessment of spatial discordance of primary and effective seed dispersal of European beech (Fagus sylvatica L.) by ecological and genetic methods

Spatial discordance between primary and effective dispersal in plant populations indicates that postdispersal processes erase the seed rain signal in recruitment patterns. Five different models were used to test the spatial concordance of the primary and effective dispersal patterns in a European beech (Fagus sylvatica) population from central Spain. An ecological method was based on classical inverse modelling (SSS), using the number of seed/seedlings as input data. Genetic models were based on direct kernel fitting of mother‐to‐offspring distances estimated by a parentage analysis or were spatially explicit models based on the genotype frequencies of offspring (competing sources model and Moran‐Clark's Model). A fully integrated mixed model was based on inverse modelling, but used the number of genotypes as input data (gene shadow model). The potential sources of error and limitations of each seed dispersal estimation method are discussed. The mean dispersal distances for seeds and saplings estimated with these five methods were higher than those obtained by previous estimations for European beech forests. All the methods show strong discordance between primary and effective dispersal kernel parameters, and for dispersal directionality. While seed rain was released mostly under the canopy, saplings were established far from mother trees. This discordant pattern may be the result of the action of secondary dispersal by animals or density‐dependent effects; that is, the Janzen‐Connell effect.     

Consequences of frugivore-mediated seed dispersal for the spatial and genetic structures of a neotropical palm

The idiosyncratic behaviours of seed dispersers are important contributors to plant spatial associations and genetic structures. In this study, we used a combination of field, molecular and spatial studies to examine the connections between seed dispersal and the spatial and genetic structures of a dominant neotropical palm Attalea phalerata. Field observation and genetic parentage analysis both indicated that the majority of A. phalerata seeds were dispersed locally over short distances (<30 m from the maternal tree). Spatial and genetic structures between adults and seedlings were consistent with localized and short-distance seed dispersal. Dispersal contributed to spatial associations among maternal sibling seedlings and strong spatial and genetic structures in both seedlings dispersed near (<10 m) and away (>10 m) from maternal palms. Seedlings were also spatially aggregated with juveniles. These patterns are probably associated with the dispersal of seeds by rodents and the survival of recruits at specific microsites or neighbourhoods over successive fruiting periods. Our cross-cohort analyses found palms in older cohorts and cohort pairs were associated with a lower proportion of offspring and sibling neighbours and exhibited weaker spatial and genetic structures. Such patterns are consistent with increased distance- and density-dependent mortality over time among palms dispersed near maternal palms or siblings. The integrative approaches used for this study allowed us to infer the importance of seed dispersal activities in maintaining the aggregated distribution and significant genetic structures among A. phalerata palms. We further conclude that distance- and density-dependent mortality is a key postdispersal process regulating this palm population.     

Population genetic structure and direct observations reveal sex‐reversed patterns of dispersal in a cooperative bird

Sex‐biased dispersal is pervasive and has diverse evolutionary implications, but the fundamental drivers of dispersal sex biases remain unresolved. This is due in part to limited diversity within taxonomic groups in the direction of dispersal sex biases, which leaves hypothesis testing critically dependent upon identifying rare reversals of taxonomic norms. Here, we use a combination of observational and genetic data to demonstrate a rare reversal of the avian sex bias in dispersal in the cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali). Direct observations revealed that (i) natal philopatry was rare, with both sexes typically dispersing locally to breed, and (ii), unusually for birds, males bred at significantly greater distances from their natal group than females. Population genetic analyses confirmed these patterns, as (i) corrected Assignment index (AIc), F_ST tests and isolation‐by‐distance metrics were all indicative of longer dispersal distances among males than females, and (ii) spatial autocorrelation analysis indicated stronger within‐group genetic structure among females than males. Examining the spatial scale of extra‐group mating highlighted that the resulting ‘sperm dispersal’ could have acted in concert with individual dispersal to generate these genetic patterns, but gamete dispersal alone cannot account entirely for the sex differences in genetic structure observed. That leading hypotheses for the evolution of dispersal sex biases cannot readily account for these sex‐reversed patterns of dispersal in white‐browed sparrow weavers highlights the continued need for attention to alternative explanations for this enigmatic phenomenon. We highlight the potential importance of sex differences in the distances over which dispersal opportunities can be detected.     

Pollen and seed flow patterns of Carapa guianensis Aublet. (Meliaceae) in two types of Amazonian forest

Various factors affect spatial genetic structure in plant populations, including adult density and primary and secondary seed dispersal mechanisms. We evaluated pollen and seed dispersal distances and spatial genetic structure of Carapa guianensis Aublet. (Meliaceae) in occasionally inundated and terra firme forest environments that differed in tree densities and secondary seed dispersal agents. We used parentage analysis to obtain contemporary gene flow estimates and assessed the spatial genetic structure of adults and juveniles. Despite the higher density of adults (diameter at breast height ≥ 25 cm) and spatial aggregation in occasionally inundated forest, the average pollen dispersal distance was similar in both types of forest (195 ± 106 m in terra firme and 175 ± 87 m in occasionally inundated plots). Higher seed flow rates (36.7% of juveniles were from outside the plot) and distances (155 ± 84 m) were found in terra firme compared to the occasionally inundated plot (25.4% and 114 ± 69 m). There was a weak spatial genetic structure in juveniles and in terra firme adults. These results indicate that inundation may not have had a significant role in seed dispersal in the occasionally inundated plot, probably because of the higher levels of seedling mortality.     

Demographic and genetic connectivity: the role and consequences of reproduction,dispersal and recruitment in seagrasses

Accurate estimation of connectivity among populations is fundamental for determining the drivers of population resilience, genetic diversity, adaptation and speciation. However the separation and quantification of contemporary versus historical connectivity remains a major challenge. This review focuses on marine angiosperms, seagrasses, that are fundamental to the health and productivity of temperate and tropical coastal marine environments globally. Our objective is to understand better the role of sexual reproduction and recruitment in influencing demographic and genetic connectivity among seagrass populations through an integrated multidisciplinary assessment of our present ecological, genetic, and demographic understanding, with hydrodynamic modelling of transport. We investigate (i) the demographic consequences of sexual reproduction, dispersal and recruitment in seagrasses, (ii) contemporary transport of seagrass pollen, fruits and seed, and vegetative fragments with a focus on hydrodynamic and particle transport models, and (iii) contemporary genetic connectivity among seagrass meadows as inferred through the application of genetic markers. New approaches are reviewed, followed by a summary outlining future directions for research: integrating seascape genetic approaches; incorporating hydrodynamic modelling for dispersal of pollen, seeds and vegetative fragments; integrating studies across broader geographic ranges; and incorporating non‐equilibrium modelling. These approaches will lead to a more integrated understanding of the role of contemporary dispersal and recruitment in the persistence and evolution of seagrasses.     

Gene dispersal inference across forest patches in an endangered medicinal tree: comparison of model‐based approaches

Propagule dispersal in plants is a fundamental mechanism for colonizing new sites and adapting to changing climates, as well as for maintaining genetic diversity. Contrasting past and current gene dispersal can provide useful insights to gauge the extent of recent human disturbances and guide management strategies. However, research on gene dispersal of plants is not yet exhaustive because evolutionary or environmental impacts are often species‐specific and most existing studies have focused on analysis of dispersal at a single site, which may not be helpful for landscape‐level inferences and management interventions. In the present study, we assessed whether current gene or propagule dispersal would be more restricted than past gene dispersal at multiple patches of the endangered medicinal tree, Prunus africana. We employed eight highly polymorphic microsatellite markers in conjunction with isolation‐by‐distance, spatial genetic structure (SGS), and parentage assignment models to estimate gene dispersal distance in a spatial extent of approximately 400 km². There was no significant difference between gene dispersal distances across the different models (Friedman chi‐squared = 7.286, d.f. = 5, P = 0.2002). Estimates of current gene dispersal distance were comparable to dispersal in the last few generations. However, gene dispersal distance was much shorter in smaller than bigger forest patches. Further, significant (P < 0.05) SGS was detected in most forest patches, with the extent of SGS among adults being stronger in the smaller than bigger patches. These results suggest the need for practicing enrichment plantings in most forest patches, particularly in the smaller ones, to assist gene exchange among individuals and patches. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 887–904.     

Molecular approaches reveal weak sibship aggregation and a high dispersal propensity in a non‐native fish parasite

Inferring parameters related to the aggregation pattern of parasites and to their dispersal propensity are important for predicting their ecological consequences and evolutionary potential. Nonetheless, it is notoriously difficult to infer these parameters from wildlife parasites given the difficulty in tracking these organisms. Molecular‐based inferences constitute a promising approach that has yet rarely been applied in the wild. Here, we combined several population genetic analyses including sibship reconstruction to document the genetic structure, patterns of sibship aggregation, and the dispersal dynamics of a non‐native parasite of fish, the freshwater copepod ectoparasite Tracheliastes polycolpus. We collected parasites according to a hierarchical sampling design, with the sampling of all parasites from all host individuals captured in eight sites spread along an upstream–downstream river gradient. Individual multilocus genotypes were obtained from 14 microsatellite markers, and used to assign parasites to full‐sib families and to investigate the genetic structure of T. polycolpus among both hosts and sampling sites. The distribution of full‐sibs obtained among the sampling sites was used to estimate individual dispersal distances within families. Our results showed that T. polycolpus sibs tend to be aggregated within sites but not within host individuals. We detected important upstream‐to‐downstream dispersal events of T. polycolpus between sites (modal distance: 25.4 km; 95% CI [22.9, 27.7]), becoming scarcer as the geographic distance from their family core location increases. Such a dispersal pattern likely contributes to the strong isolation‐by‐distance observed at the river scale. We also detected some downstream‐to‐upstream dispersal events (modal distance: 2.6 km; 95% CI [2.2–23.3]) that likely result from movements of infected hosts. Within each site, the dispersal of free‐living infective larvae among hosts likely contributes to increasing genetic diversity on hosts, possibly fostering the evolutionary potential of T. polycolpus.     

Population history and gene dispersal inferred from spatial genetic structure of a Central African timber tree,Distemonanthus benthamianus (Caesalpinioideae)

African rainforests have undergone major distribution range shifts during the Quaternary, but few studies have investigated their impact on the genetic diversity of plant species and we lack knowledge on the extent of gene flow to predict how plant species can cope with such environmental changes. Analysis of the spatial genetic structure (SGS) of a species is an effective method to determine major directions of the demographic history of its populations and to estimate the extent of gene dispersal. This study characterises the SGS of an African tropical timber tree species, Distemonanthus benthamianus, at various spatial scales in Cameroon and Gabon. Displaying a large continuous distribution in the Lower Guinea domain, this is a model species to detect signs of past population fragmentation and recolonization, and to estimate the extent of gene dispersal. Ten microsatellite loci were used to genotype 295 adult trees sampled from eight populations. Three clearly differentiated gene pools were resolved at this regional scale and could be linked to the biogeographical history of the region, rather than to physical barriers to gene flow. A comparison with the distribution of gene pools observed for two other tree species living in the same region invalidates the basic assumption that all species share the same Quaternary refuges and recolonization pathways. In four populations, significant and similar patterns of SGS were detected. Indirect estimates of gene dispersal distances (sigma) obtained for three populations ranged from 400 to 1200 m, whereas neighbourhood size estimates ranged from 50 to 110.