Neotoma Fuscipes Research Articles

Asymmetrical predation intensity produces divergent antipredator behaviours in primary and secondary prey.

It is widely recognized that predators can influence prey through both direct consumption and by inducing costly antipredator behaviours, the latter of which can produce nonconsumptive effects that cascade through trophic systems. Yet, determining how particular prey manage risk in natural settings remains challenging as empirical studies disproportionately focus on single predator-prey dyads. Here, we contrast foraging strategies within the context of a primary and secondary prey to explore how antipredator behaviours emerge as a product of predation intensity as well as the setting in which an encounter takes place. We studied the effects of spotted owls (Strix occidentalis) on two species experiencing asymmetrical risk: dusky-footed woodrats (Neotoma fuscipes; primary prey) and deer mice (Peromyscus spp.; alternative prey). Woodrats are most abundant within young forests, but predominantly captured by owls foraging within mature forests; in contrast, deer mice occur in high densities across forest types and seral stages and are consumed at lower per-capita rates overall. We deployed experimental foraging patches within areas of high and low spotted owl activity, created artificial risky and safe refuge treatments, and monitored behaviour throughout the entirety of prey foraging bouts. Woodrats were more vigilant and foraged less within mature forests and at riskier patches, although the effect of refuge treatment was contingent upon forest type. In contrast, deer mice only demonstrated consistent behavioural responses to riskier refuge treatments; forest type had little effect on perceived risk or the relative importance of refuge treatment. Thus, habitat can interact with predator activity to structure antipredator responses differently for primary versus secondary prey. Our findings show that asymmetrical predation can modulate both the magnitude of perceived risk and the strategies used to manage it, thus highlighting an important and understudied contingency in risk effects research. Evaluating the direct and indirect effects of predation through the paradigm of primary and secondary prey may improve our understanding of how nonconsumptive effects can extend to population- and community-level responses.

Landscape heterogeneity provides co-benefits to predator and prey.

Predator populations are imperiled globally, due in part to changing habitat and trophic interactions. Theoretical and laboratory studies suggest that heterogeneous landscapes containing prey refuges acting as source habitats can benefit both predator and prey populations, although the importance of heterogeneity in natural systems is uncertain. Here, we tested the hypothesis that landscape heterogeneity mediates predator-prey interactions between the California spotted owl (Strix occidentalis occidentalis)-a mature forest species-and one of its principal prey, the dusky-footed woodrat (Neotoma fuscipes)-a younger forest species-to the benefit of both. We did so by combining estimates of woodrat density and survival from live trapping and very high frequency tracking with direct observations of prey deliveries to dependent young by owls in both heterogeneous and homogeneous home ranges. Woodrat abundance was ~2.5 times higher in owl home ranges (14.12 km2 ) featuring greater heterogeneity in vegetation types (1805.0 ± 50.2 SE) compared to those dominated by mature forest (727.3 ± 51.9 SE), in large part because of high densities in young forests appearing to act as sources promoting woodrat densities in nearby mature forests. Woodrat mortality rates were low across vegetation types and did not differ between heterogeneous and homogeneous home ranges, yet all observed predation by owls occurred within mature forests, suggesting young forests may act as woodrat refuges. Owls exhibited a type 1 functional response, consuming ~2.5 times more woodrats in heterogeneous (31.1/month ± 5.2 SE) versus homogeneous (12.7/month ± 3.7 SE) home ranges. While consumption of smaller-bodied alternative prey partially compensated for lower woodrat consumption in homogeneous home ranges, owls nevertheless consumed 30% more biomass in heterogeneous home ranges-approximately equivalent to the energetic needs of producing one additional offspring. Thus, a mosaic of vegetation types including young forest patches increased woodrat abundance and availability that, in turn, provided energetic and potentially reproductive benefits to mature forest-associated spotted owls. More broadly, our findings provide strong empirical evidence that heterogeneous landscapes containing prey refuges can benefit both predator and prey populations. As anthropogenic activities continue to homogenize landscapes globally, promoting heterogeneous systems with prey refuges may benefit imperiled predators.

Food and cover resources for small mammals on an industrially logged landscape in the Sierra Nevada of California

The presence and abundance of organisms within an ecosystem often correlate with habitat variables that may have few, or unknown, functional values. Understanding the functional role of these variables is especially important for organisms occupying landscapes managed for timber production and containing diverse habitat patches of different quantities and structures of vegetation. We investigated the strength of associations reported in the literature between small mammal generalists and vegetation. On an industrially logged landscape in northern CA, we used occupancy and mark-recapture analyses across three years to estimate the presence and total numbers for woodrats ( Neotoma fuscipes Baird, 1858) and deer mice ( Peromyscus maniculatus (Wagner, 1845)) related to vegetative attributes on coniferous and non-coniferous sites. Abundances of the small mammals correlated positively with shrub cover and hardwoods for woodrats and with shrubs and masting species for deer mice. Indices describing the value of vegetation features for both food and cover, but not these resources independently, described both species’ presence and abundances best. We demonstrated that shrubs and non-coniferous trees are particularly important for small mammals and should be of particular focus to forest managers in the Sierras and mountains with similar forest structures.

Linking Lyme disease ecology and epidemiology: reservoir host identity, not richness, determines tick infection and human disease in California

Understanding the community ecology of vector-borne and zoonotic diseases, and how it may shift transmission risk as it responds to environmental change, has become a central focus in disease ecology. Yet, it has been challenging to link the ecology of disease with reported human incidence. Here, we bridge the gap between local-scale community ecology and large-scale disease epidemiology, drawing from a priori knowledge of tick-pathogen-host ecology to model spatially-explicit Lyme disease (LD) risk, and human Lyme disease incidence (LDI) in California. We first use a species distribution modeling approach to model disease risk with variables capturing climate, vegetation, and ecology of key reservoir host species, and host species richness. We then use our modeled disease risk to predict human disease incidence at the zip code level across California. Our results suggest the ecology of key reservoir hosts—particularly dusky-footed woodrats—is central to disease risk posed by ticks, but that host community richness is not strongly associated with tick infection. Predicted disease risk, which is most strongly influenced by the ecology of dusky-footed woodrats, in turn is a strong predictor of human LDI. This relationship holds in the Wildland-Urban Interface, but not in open access public lands, and is stronger in northern California than in the state as a whole. This suggests peridomestic exposure to infected ticks may be more important to LD epidemiology in California than recreational exposure, and underlines the importance of the community ecology of LD in determining human transmission risk throughout this LD endemic region of far western North America. More targeted tick and pathogen surveillance, coupled with studies of human and tick behavior could improve understanding of key risk factors and inform public health interventions. Moreover, longitudinal surveillance data could further improve forecasts of disease risk in response to global environmental change.

Large trees and forest heterogeneity facilitate prey capture by California Spotted Owls

Abstract Predators are among the most threatened animal groups globally, with prey declines contributing to their endangerment. However, assessments of the habitat conditions that influence the successful capture of different prey species are rare, especially for small, cryptic predators. Accordingly, most predator conservation plans are based on the relative importance of habitats inferred from coarse-scale studies that do not consider habitat features contributing to hunting success, which can vary among prey species. To address this limitation, we integrated high-resolution global positioning system tracking and nest video monitoring to characterize habitat features at prey capture locations during the nestling provisioning stage for the Spotted Owl (Strix occidentalis) a small, cryptic predator that has been at the center of a decades-long forest management conflict in western North America. When all prey species were considered collectively, males provisioning nests tended to capture prey: (1) in areas with more large-tree forest, (2) in areas with more medium trees/medium canopy forest, and (3) at edges between conifer and hardwood forests. However, when we considered the owl’s two key prey species separately, males captured woodrats (Neotoma fuscipes) and Humboldt flying squirrels (Glaucomys oregonensis) in areas with markedly different habitat features. Our study provides clarity for forest management in mixed-ownership landscapes because different prey species achieve high densities in different habitat types. Specifically, our results suggest that promoting large trees, increasing forest heterogeneity, and creating canopy gaps in forests with medium trees/high canopy cover could benefit Spotted Owls and their prey, which has the ancillary benefit of enhancing forest resilience. Combining high-resolution global positioning system tagging with video-based information on prey deliveries to breeding sites can strengthen conservation planning for small predators by more rigorously defining those habitat features that are associated with successful prey acquisition.

Host infection and community composition predict vector burden.

Lyme disease is the most prevalent vector-borne disease in the United States, yet critical gaps remain in our understanding of tick and host interactions that shape disease dynamics. Rodents such as deer mice (Peromyscus spp.) and dusky-footed woodrats (Neotoma fuscipes) are key reservoirs for Borrelia burgdorferi, the etiological bacterium of Lyme disease, and can vary greatly in abundance between habitats. The aggregation of Ixodes pacificus, the western black-legged tick, on rodent hosts is often assumed to be constant across various habitats and not dependent on the rodent or predator communities; however, this is rarely tested. The factors that determine tick burdens on key reservoir hosts are important in estimating Lyme disease risk because larger tick burdens can amplify pathogen transmission. This study is the first to empirically measure I. pacificus larval burdens on competent reservoir hosts as a function of community factors such as rodent diversity, predator diversity, and questing tick abundance. Rodents were live trapped at oak woodland sites to collect tick burdens and tissue samples to test for infection with Borrelia burgdorferi sensu lato. We found that N. fuscipes tick burdens were negatively correlated with predator diversity, but positively correlated with questing I. pacificus larvae. In addition, rodent hosts that were infected with B. burgdorferi sensu lato tend to have higher burdens of larval ticks. These results demonstrate that tick burdens can be shaped by variability between individuals, species, and the broader host community with consequences for transmission and prevalence of tick-borne pathogens.

Genome-wide genetic variation coupled with demographic and ecological niche modeling of the dusky-footed woodrat (Neotoma fuscipes) reveal patterns of deep divergence and widespread Holocene expansion across northern California.

Understanding how species have responded to past climate change may help refine projections of how species and biotic communities will respond to future change. Here, we integrate estimates of genome-wide genetic variation with demographic and niche modeling to investigate the historical biogeography of an important ecological engineer: the dusky-footed woodrat, Neotoma fuscipes. We use RADseq to generate a genome-wide dataset for 71 individuals from across the geographic distribution of the species in California. We estimate population structure using several model-based methods and infer the demographic history of regional populations using a site frequency spectrum-based approach. Additionally, we use ecological niche modeling to infer current and past (Last Glacial Maximum) environmental suitability across the species' distribution. Finally, we estimate the directionality and possible spatial origins of regional population expansions. Our analyses indicate this species is subdivided into three regionally distinct populations, with the deepest divergence occurring ~1.7 million years ago across the modern-day San Francisco-Bay Delta region; a common biogeographic barrier for the flora and fauna of California. Our models of environmental suitability through time coincide with our estimates of population expansion, with relative long-term stability in the southern portion of the range, and more recent expansion into the northern end of the range. Our study illustrates how the integration of genome-wide data with spatial and demographic modeling can reveal the timing and spatial extent of historic events that determine patterns of biotic diversity and may help predict biotic response to future change.

FIRST RECORD OF THE DUSKY-FOOTED WOODRAT, NEOTOMA FUSCIPES, IN NORTHERN NEVADA

On 3 August 2018, a single specimen of the Dusky-footed Woodrat, Neotoma fuscipes, was collected as the 1st occurrence of the species in Nevada.

Borrelia burgdorferi and Anaplasma phagocytophilum Genospecies in Northern California.

The sensu lato (s.l.) complexes of Borrelia burgdorferi and Anaplasma phagocytophilum include pathogenic genospecies each with distinct ecologies in northern California, yet, most work conflates the genospecies of each pathogen into one sensu lato species. Detailed understanding of the differences in geographic distributions and ecology among genospecies is lacking. We aimed to evaluate whether two B. burgdorferi and two A. phagocytophilum genospecies in high-risk locations in coastal northern California were spatially clustered and if presence of a particular genospecies was associated with geographical site, host species, or other demographic or ecological variables. DNA sequencing was performed to differentiate genospecies of Borreliae and Anaplasma from PCR-positive dusky-footed woodrats (Neotoma fuscipes) and sciurids (chipmunks, Tamias spp., and Douglas squirrels, Tamiasciurus douglasii) at four sites in northwestern California. Logistic regression was performed to assess associations of genospecies with the predictor variables host species, host sex, site, season, and year. Spatial clustering was assessed using a Poisson spatial scan statistic in SaTScan. Host species was a significant predictor for Borrelia bissettiae, B. burgdorferi sensu stricto (s.s.), A. phagocytophilum s.s., and the DU1 Anaplasma genospecies. Woodrats were significantly more likely to be PCR-positive for B. bissettiae and A. phagocytophilum DU1 genospecies, while A. phagocytophilum s.s. and B. burgdorferi s.s. were significantly associated with sciurids. We report a single Borrelia lanei in an Allen's chipmunk (Tamias senex) from the Hoopa Valley Tribal Reservation. A significant spatial cluster of A. phagocytophilum s.s. was detected at Hendy Woods State Park in Mendocino County. These results highlight the need to better understand genospecies partitioning according to host species to further assess human risks, aid in future surveillance, and inform targeted research.

Borrelia miyamotoi Infections in Small Mammals, California, USA.

Surveillance to investigate the wildlife–vector transmission cycle of the human pathogen Borrelia miyamotoi in California, USA, revealed infections in dusky-footed woodrats, brush mice, and California mice. Phylogenetic analyses suggest a single, well-supported clade of B. miyamotoi is circulating in California.

Spatial clustering of Borrelia burgdorferi sensu lato within populations of Allen's chipmunks and dusky-footed woodrats in northwestern California.

The ecology of Lyme borreliosis is complex in northwestern California, with several potential reservoir hosts, tick vectors, and genospecies of Borrelia burgdorferi sensu lato. The primary objective of this study was to determine the fine-scale spatial distribution of different genospecies in four rodent species, the California ground squirrel (Otospermophilus beecheyi), northern flying squirrel (Glaucomys sabrinus), dusky-footed woodrat (Neotoma fuscipes), and Allen’s chipmunk (Neotamias senex). Rodents were live-trapped between June 2004 and May 2005 at the Hoopa Valley Tribal Reservation (HVTR) in Humboldt County, California. Ear-punch biopsies obtained from each rodent were tested by polymerase chain reaction (PCR) and sequencing analysis. The programs ArcGIS and SaTScan were used to examine the spatial distribution of genospecies. Multinomial log-linear models were used to model habitat and host-specific characteristics and their effect on the presence of each borrelial genospecies. The Akaike information criterion (AICc) was used to compare models and determine model fit. Borrelia burgdorferi sensu stricto was primarily associated with chipmunks and B. bissettiae largely with woodrats. The top model included the variables “host species”, “month”, and “elevation” (weight = 0.84). Spatial clustering of B. bissettiae was detected in the northwestern section of the HVTR, whereas B. burgdorferi sensu stricto was clustered in the southeastern section. We conclude that the spatial distribution of these borreliae are driven at least in part by host species, time-of-year, and elevation.

Differential Effects of Climate on Survival Rates Drive Hybrid Zone Movement

Climate change has been implicated as driving shifts of hybridizing species' range limits [1, 2]. Whether and how much hybrid zones move depends on the relative fitness of hybridzing species under changing conditions [3, 4]. However, fitness is rarely linked to both climatic conditions and movement of hybrid zones, such that the relationship between climate change and hybrid zone dynamics remains tenuous [5]. Here we report how interactions between climate (seasonal precipitation) and competitor densities result in steep differentials in survival, which in turndrive hybrid zone movement for two woodrat species (Neotoma fuscipes and N.macrotis) in central California, USA. Using 6 years of capture-mark-recapture data, we found that the smaller-bodied species, N.macrotis, and hybrids had survival advantages over the larger-bodied N.fuscipes in the contact region during dry winters and wet springs. This pattern of differential survival, with N.macrotis having a consistent advantage over N.fuscipes during our study period, matched the spatial dynamics of the hybrid zone, which moved steadily north into N.fuscipes territory, with its estimated center moving ∼150m north in 6 years. Our findings provide a unique demonstration of range movements emerging from a complex interplay between climate and competition. Although all studysite areas experienced the same climatic conditions, competitive effects created a complex spatial pattern of survival differentials, which in turn influenced hybrid zone movement. Characterization of fitness differentials derived from replicated demographic studies of contact regions between competitors should greatly improve our ability to understand and forecast climate-driven range dynamics.

The complete mitochondrial genome of northern grasshopper mouse (Onychomys leucogaster)

In this study, we presented the complete mitochondrial genome of northern grasshopper mouse (Onychomys leucogaster). The circular genome is 16,370 bp in length and contains 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, 2 ribosome RNA genes, and 1 D-loop control regions. The overall nucleotide composition is: 31.2% A, 25.2% T, 29.9% C, and 13.6% G, with a total G + C content of 43.53%. The phylogenetic tree was constructed to validate the taxonomic status of Onychomys leucogaster, exhibiting a closest relationship with Neotoma fuscipes.

Speciation along a shared evolutionary trajectory.

Groups of organisms—whether multiple species or populations of a single species—can differ in several non-exclusive ways. For example, groups may have diverged phenotypically, genetically, or in the evolutionary responses available to them. We tested for the latter of these—response divergence—between 2 species of woodrats: Neotoma fuscipes and Neotoma macrotis. Based on random skewers analyses we found that, despite being well differentiated both phenotypically and genetically, N. fuscipes and N. macrotis appear to be diverging along a shared evolutionary trajectory (r° = 0.895, P = 0.114). Because these species are currently in secondary contact, their phenotypic evolution being along a shared evolutionary axis has important implications. In particular, that their response to selection arising from interspecific interactions will be constrained along the same evolutionary trajectory may reduce the potential for reinforcing selection to maintain species boundaries.

Borrelia bissettiae sp. nov. and Borrelia californiensis sp. nov. prevail in diverse enzootic transmission cycles.

Two species of the genus Borrelia, Borrelia bissettiae sp. nov. and Borrelia californiensis sp. nov., were first described by Postic and co-workers on the basis of genetic analyses of several loci. Multilocus sequence analysis of eight housekeeping loci confirmed that these two Borrelia genomospecies are distinct members of the Borrelia burgdorferi sensu lato complex. B. bissettiae sp. nov. was initially described in transmission cycles involving Neotoma fuscipes wood rats and Ixodes pacificus ticks in California, and Neotoma mexicana and Ixodes spinipalpis in Colorado. The preferred host of B. californiensis sp. nov. appears to be the California kangaroo rat, Dipodomys californicus; Ixodes jellisoni, I. spinipalipis and I. pacificus ticks are naturally infected with it. Thus, the ecological associations of the two genomospecies and their genetic distance from all other known Borrelia genomospecies species justify their description as separate genomospecies: B. bissettiae sp. nov. (type strain DN127T = DSM 17990T = CIP 109136T) and B. californiensis (type strain CA446T = DSM 17989T = ATCC BAA-2689T).

The complete mitochondrial genome of the dusky-footed woodrat(Neotoma fuscipes) (Rodentia, Cricetidae)

The dusky-footed woodrat (Neotoma fuscipes) is an endemic North American rodent belonging to the family Cricetidae. We present here the first complete mitogenome within the Neotoma genus. The mitogenome is 16,199 bp in length, and has a structure and gene organization similar to other rodent species (e.g. Mus musculus, Peromyscus maniculatus and Microtus fortis calamorum). The overall base composition is A (35.2%), C (25.5%), G (12.3%), T (27.0%), with a GC content of 37.8%, similar to other rodents. This mitogenome serves as a foundation for future phylogenetic, phylogeographic and population genetic studies.

Fine-scale genetic structure of woodrat populations (Genus: Neotoma) and the spatial distribution of their tick-borne pathogens

Dusky-footed woodrats are territorial cricetid rodents that individually occupy large stick houses from which they foray to gather food, find mates, and engage in other activities. These rodents are often bitten by Ixodes spp. ticks and are reservoirs of some strains of tick-borne bacterial pathogens such as Anaplasma phagocytophilum and Borrelia burgdorferi. Limited dispersal by hosts and vectors could create fine-scale population structure where related hosts and pathogen exposure are co-distributed in space. To quantify population genetic structure and infection status, we genotyped 167 woodrats using a panel of 15 microsatellite loci from three northern California study sites: Soquel (SD), Cold Canyon (CC), and Quail Ridge (QR). We used quantitative PCR and serology to test for infection with A. phagocytophilum and B. burgdorferi. All three populations maintained similar, moderately high levels of genetic variation. For A. phagocytophilum, the PCR-prevalence was higher at SD (30.0%) than CC (13%) and QR (7%) whereas the seroprevalence was similar at all three sites (13–18%). The B. burgdorferi PCR-prevalence at CC was 11%, no woodrats were PCR-positive at QR, and none were tested at SD. We found a negative correlation between pairwise genetic relatedness and spatial distance with the majority of highest order relatives occurring within 200m of one another. Related dyads were more likely to be adult females than males, suggesting that adult female residents are the primary source of spatially proximate, high-order relatives in woodrat populations. Despite spatial genetic clustering of hosts, our spatial window test found no significant clustering of pathogens. Woodrats that were seropositive for A. phagocytophilum had higher heterozygosity than seronegative woodrats, which could be consistent with genetically diverse individuals having greater capacity to mount an immune response. Overall, our analyses show that limited dispersal of individual woodrats leads to fine-scale genetic structure within populations. Genetic structure, coupled with the limited dispersal of I. pacificus ticks could result in disease dynamics that are uniquely restricted to small spatial scales. By combining host genetic and disease studies we are able to infer limited dispersal and structured populations among hosts which affect infectious disease clustering and dynamics.

Microhabitat and House Use by Dusky-Footed Woodrats (Neotoma fuscipes) in Northwestern California: Insight from Trapping Data

Abstract. Capture data differed at woodrat houses associated with selected microhabitats in a chaparral-oak woodland site in the foothills of northwestern California. Mean trapping success was significantly higher at houses located under dense tree canopy (and in low scrub cover) compared with houses in high scrub cover (and under less tree canopy), as was trapping success at houses found in non-edge versus edge habitat. Woodrats trapped at houses under dense canopy also were significantly heavier than those captured in high scrub cover; however, mean body masses at edge- and non-edge houses were similar. Broadly, our results mirror existing research but indicate the need for more study of the specific microhabitat factors that influence woodrat house use in chaparral-oak habitat.

Dispatches

Dispatches

Hybridization and asymmetric introgression across a narrow zone of contact betweenNeotoma fuscipesandN. macrotis(Rodentia: Cricetidae)

When lineages diverge in allopatry and come into secondary contact, we have a unique opportunity to examine the degree to which they have become reproductively isolated from one another and the mechanisms that contribute to rates of interspecific gene flow. If hybridization and introgression have occurred in the past or are ongoing, examining patterns of variation in differentially inherited genetic markers can provide insight into underlying mechanisms determining interspecific reproductive interactions. We investigated genetic variation in a recently discovered contact zone between two species of woodrats (Neotoma fuscipes and N. macrotis) in central coastal California. Previous studies have found evidence of historic hybridization between these species, but an active site of sympatry had yet to be discovered. Here, we describe the first known area of sympatry between the two species and present evidence of ongoing hybridization at this site. We intensively sampled throughout the narrow area of interspecific contact and continuously into the adjacent areas where each taxon existed largely in isolation of the other. We genotyped 851 individuals sampled in a single year at 15 nuclear microsatellite loci and sequenced a portion of the cytochrome b gene in a subset of these to examine patterns of introgression. We find that the area of sympatry is less than 1 km in length, but hybridization appeared to be fairly common, with 15% of the woodrats being of hybrid origin. At least some hybrids are fertile because introgression was evident. However, introgression appeared to be asymmetric with backcrosses toward N. macrotis being more common, a pattern we suspect is due in part to directional mate choice related to differential body size. This study adds to our growing understanding of the nature of species boundaries, especially between lineages that are far along the continuum towards speciation. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 162–172.