Application of modern coexistence theory to rare plant restoration provides early indication of restoration trajectories.

Restoration ecology commonly seeks to re-establish species of interest in degraded habitats. Despite a rich understanding of how succession influences re-establishment, there are several outstanding questions that remain unaddressed: are short-term abundances sufficient to determine long-term re-establishment success, and what factors contribute to unpredictable restorations outcomes? In other words, when restoration fails, is it because the restored habitat is substandard, because of strong competition with invasive species, or alternatively due to changing environmental conditions that would equally impact established populations? Here, we re-purpose tools developed from modern coexistence theory to address these questions, and apply them to an effort to restore the endangered Contra Costa goldfields (Lasthenia conjugens) in constructed ("restored") California vernal pools. Using 16 years of data, we construct a population model of L. conjugens, a species of conservation concern due primarily to habitat loss and invasion of exotic grasses. We show that initial, short-term appearances of restoration success from population abundances is misleading, as year-to-year fluctuations cause long-term population growth rates to fall below zero. The failure of constructed pools is driven by lower maximum growth rates compared with reference ("natural") pools, coupled with a stronger negative sensitivity to annual fluctuations in abiotic conditions that yield decreased maximum growth rates. Nonetheless, our modeling shows that fluctuations in competition (mainly with exotic grasses) benefit L. conjugens through periods of competitive release, especially in constructed pools of intermediate pool depth. We therefore show how reductions in invasives and seed addition in pools of particular depths could change the outcome of restoration for L. conjugens. By applying a largely theoretical framework to the urgent goal of ecological restoration, our study provides a blueprint for predicting restoration success, and identifies future actions to reverse species loss.

No evidence for enzootic plague within black-tailed prairie dog (Cynomys ludovicianus) populations.

Yersinia pestis, causative agent of plague, occurs throughout the western United States in rodent populations and periodically causes epizootics in susceptible species, including black-tailed prairie dogs (Cynomys ludovicianus). How Y. pestis persists long-term in the environment between these epizootics is poorly understood but multiple mechanisms have been proposed, including, among others, a separate enzootic transmission cycle that maintains Y. pestis without involvement of epizootic hosts and persistence of Y. pestis within epizootic host populations without causing high mortality within those populations. We live-trapped and collected fleas from black-tailed prairie dogs and other mammal species from sites with and without black-tailed prairie dogs in 2004 and 2005 and tested all fleas for presence of Y. pestis. Y. pestis was not detected in 2126 fleas collected in 2004 but was detected in 294 fleas collected from multiple sites in 2005, before and during a widespread epizootic that drastically reduced black-tailed prairie dog populations in the affected colonies. Temporal and spatial patterns of Y. pestis occurrence in fleas and genotyping of Y. pestis present in some infected fleas suggest Y. pestis was introduced multiple times from sources outside the study area and once introduced, was dispersed between several sites. We conclude Y. pestis likely was not present in these black-tailed prairie dog colonies prior to epizootic activity in these colonies. Although we did not identify likely enzootic hosts, we found evidence that deer mice (Peromyscus maniculatus) may serve as bridging hosts for Y. pestis between unknown enzootic hosts and black-tailed prairie dogs.

BioTIME: A database of biodiversity time series for the Anthropocene.

MOTIVATION: The BioTIME database contains raw data on species identities and abundances in ecological assemblages through time. These data enable users to calculate temporal trends in biodiversity within and amongst assemblages using a broad range of metrics. BioTIME is being developed as a community-led open-source database of biodiversity time series. Our goal is to accelerate and facilitate quantitative analysis of temporal patterns of biodiversity in the Anthropocene. MAIN TYPES OF VARIABLES INCLUDED: The database contains 8,777,413 species abundance records, from assemblages consistently sampled for a minimum of 2 years, which need not necessarily be consecutive. In addition, the database contains metadata relating to sampling methodology and contextual information about each record. SPATIAL LOCATION AND GRAIN: BioTIME is a global database of 547,161 unique sampling locations spanning the marine, freshwater and terrestrial realms. Grain size varies across datasets from 0.0000000158 km2 (158 cm2) to 100 km2 (1,000,000,000,000 cm2). TIME PERIOD AND GRAIN: BioTIME records span from 1874 to 2016. The minimal temporal grain across all datasets in BioTIME is a year. MAJOR TAXA AND LEVEL OF MEASUREMENT: BioTIME includes data from 44,440 species across the plant and animal kingdoms, ranging from plants, plankton and terrestrial invertebrates to small and large vertebrates. SOFTWARE FORMAT: .csv and .SQL.

Quantifying the dominance of local control and the sources of regional control in the assembly of a metacommunity.

To understand the relative roles of local and regional processes in structuring local communities, and to compare sources of dispersal, we studied plant species composition in the context of a field experiment in vernal pool community assembly. In 1999, we constructed 256 vernal pools in a grid surrounding a group of over 60 naturally occurring reference pools. Each constructed pool received a seeding or control treatment. Seeding treatments involved several "focal species" native to vernal pools in this region. Earlier analyses identified local habitat quality (pool depth) and pool history (seeding treatment) as strong predictors of local species composition. For the current analysis, we asked how connectivity among pools might enhance models of focal species presence and cover within pools, using long-term data from control pools and from unseeded transects within a stratified random sample of all constructed pools. We fitted connectivity models for each of four focal species, and compared the relative support for connectivity, seeding treatment, and pool depth as predictors of local species presence and cover. We modeled connectivity in several ways to quantify the relative importance of immigration (1) from constructed pools, (2) from reference pools within the study site, (3) from a cluster of natural pools off-site, and (4) along ephemeral waterways. We found strongest support for effects of connectivity with reference pools. Species presence in a target pool was usually well predicted by an exponential decline in connectivity with distance to source pools, and our fitted estimates of mean dispersal distance indicate strong dispersal limitation in this system. Effects of target and source pool size were also supported in some models, and long-term effects of seeding were supported for most species. However, pool depth was by far the strongest predictor of focal species presence, and depth rivaled connectivity with reference pools as a top predictor of cover after accounting for species presence. We conclude that local species composition was determined primarily by local processes in this system, and we encourage more widespread use of a straightforward method for weighing local vs. regional influences.

Do pathogens reduce genetic diversity of their hosts? Variable effects of sylvatic plague in black-tailed prairie dogs.

Introduced diseases can cause dramatic declines in-and even the loss of-natural populations. Extirpations may be followed by low recolonization rates, leading to inbreeding and a loss of genetic variation, with consequences on population viability. Conversely, extirpations may create vacant habitat patches that individuals from multiple source populations can colonize, potentially leading to an influx of variation. We tested these alternative hypotheses by sampling 15 colonies in a prairie dog metapopulation during 7 years that encompassed an outbreak of sylvatic plague, providing the opportunity to monitor genetic diversity before, during and after the outbreak. Analysis of nine microsatellite loci revealed that within the metapopulation, there was no change in diversity. However, within extirpated colonies, patterns varied: In half of the colonies, allelic richness after recovery was less than the preplague conditions, and in the other half, richness was greater than the preplague conditions. Finally, analysis of variation within individuals revealed that prairie dogs present in recolonized colonies had higher heterozygosity than those present before plague. We confirmed plague survivorship in six founders; these individuals had significantly higher heterozygosity than expected by chance. Collectively, our results suggest that high immigration rates can maintain genetic variation at a regional scale despite simultaneous extirpations in spatially proximate populations. Thus, virulent diseases may increase genetic diversity of host populations by creating vacant habitats that allow an influx of genetic diversity. Furthermore, even highly virulent diseases may not eliminate individuals randomly; rather, they may selectively remove the most inbred individuals.

Long-term dynamics of biotic and abiotic resistance to exotic species invasion in restored vernal pool plant communities.

Invasion of native ecosystems by exotic species can seriously threaten native biodiversity, alter ecosystem function, and inhibit conservation. Moreover, restoration of native plant communities is often impeded by competition from exotic species. Exotic species invasion may be limited by unfavorable abiotic conditions and by competition with native species, but the relative importance of biotic and abiotic factors remains controversial and may vary during the invasion process. We used a long-term experiment involving restored vernal pool plant communities to characterize the temporal dynamics of exotic species invasion, and to evaluate the relative support for biotic and abiotic factors affecting invasion resistance. Experimental pools (n=256) were divided among controls and several seeding treatments. In most treatments, native vernal pool species were initially more abundant than exotic species, and pools that initially received more native seeds exhibited lower frequencies of exotic species over time. However, even densely seeded pools were eventually dominated by exotic species, following extreme climatic events that reduced both native and exotic plant densities across the study site. By the sixth year of the experiment, most pools supported more exotics than native vernal pool species, regardless of seeding treatment or pool depth. Although deeper pools were less invaded by exotic species, two exotics (Hordeum marinum and Lolium multiflorum) were able to colonize deeper pools as soon as the cover of native species was reduced by climatic extremes. Based on an information-theoretic analysis, the best model of invasion resistance included a nonlinear effect of seeding treatment and both linear and nonlinear effects of pool depth. Pool depth received more support as a predictor of invasion resistance, but seeding intensity was also strongly supported in multivariate models of invasion, and was the best predictor of resistance to invasion by H. marinum and L. multilorum. We conclude that extreme climatic events can facilitate exotic species invasions by both reducing abiotic constraints and weakening biotic resistance to invasion.

Population genetic structure of the prairie dog flea and plague vector, Oropsylla hirsuta.

Oropsylla hirsuta is the primary flea of the black-tailed prairie dog and is a vector of the plague bacterium, Yersinia pestis. We examined the population genetic structure of O. hirsuta fleas collected from 11 prairie dog colonies, 7 of which had experienced a plague-associated die-off in 1994. In a sample of 332 O. hirsuta collected from 226 host individuals, we detected 24 unique haplotype sequences in a 480 nucleotide segment of the cytochrome oxidase II gene. We found significant overall population structure but we did not detect a signal of isolation by distance, suggesting that O. hirsuta may be able to disperse relatively quickly at the scale of this study. All 7 colonies that were recently decimated by plague showed signs of recent population expansion, whereas 3 of the 4 plague-negative colonies showed haplotype patterns consistent with stable populations. These results suggest that O. hirsuta populations are affected by plague-induced prairie dog die-offs and that flea dispersal among prairie dog colonies may not be dependent exclusively on dispersal of prairie dogs. Re-colonization following plague events from plague-free refugia may allow for rapid flea population expansion following plague epizootics.

Sin Nombre virus infection in field workers, Colorado, USA.

We report 2 cases of Sin Nombre virus (SNV) infection in field workers, possibly contracted through rodent bites. Screening for antibodies to SNV in rodents trapped in 2 seasons showed that 9.77% were seropositive. Quantitative real-time PCR showed that 2 of 79 deer mice had detectable titers of SNV RNA.

Disease limits populations: plague and black-tailed prairie dogs.

Plague is an exotic vector-borne disease caused by the bacterium Yersinia pestis that causes mortality rates approaching 100% in black-tailed prairie dogs (Cynomys ludovicianus). We mapped the perimeter of the active portions of black-tailed prairie dog colonies annually between 1999 and 2005 at four prairie dog colony complexes in areas with a history of plague, as well as at two complexes that were located outside the distribution of plague at the time of mapping and had therefore never been affected by the disease. We hypothesized that the presence of plague would significantly reduce overall black-tailed prairie dog colony area, reduce the sizes of colonies on these landscapes, and increase nearest-neighbor distances between colonies. Within the region historically affected by plague, individual colonies were smaller, nearest-neighbor distances were greater, and the proportion of potential habitat occupied by active prairie dog colonies was smaller than at plague-free sites. Populations that endured plague were composed of fewer large colonies (>100 ha) than populations that were historically plague free. We suggest that these differences among sites in colony size and isolation may slow recolonization after extirpation. At the same time, greater intercolony distances may also reduce intercolony transmission of pathogens. Reduced transmission among smaller and more distant colonies may ultimately enhance long-term prairie dog population persistence in areas where plague is present.

Rodent and flea abundance fail to predict a plague epizootic in black-tailed prairie dogs.

Small rodents are purported to be enzootic hosts of Yersinia pestis and may serve as sources of infection to prairie dogs or other epizootic hosts by direct or flea-mediated transmission. Recent research has shown that small rodent species composition and small rodent flea assemblages are influenced by the presence of prairie dogs, with higher relative abundance of both small rodents and fleas at prairie dog colony sites compared to grasslands without prairie dogs. However, it is unclear if increased rodent or flea abundance predisposes prairie dogs to infection with Y. pestis. We tracked rodent and flea occurrence for 3 years at a number of prairie dog colony sites in Boulder County, Colorado, before, during, and after a local plague epizootic to see if high rodent or flea abundance was associated with plague-affected colonies when compared to colonies that escaped infection. We found no difference in preepizootic rodent abundance or flea prevalence or abundance between plague-positive and plague-negative colonies. Further, we saw no significant before-plague/after-plague change in these metrics at either plague-positive or plague-negative sites. We did, however, find that small rodent species assemblages changed in the year following prairie dog die-offs at plague-affected colonies when compared to unaffected colonies. In light of previous research from this system that has shown that landscape features and proximity to recently plagued colonies are significant predictors of plague occurrence in prairie dogs, we suggest that landscape context is more important to local plague occurrence than are characteristics of rodent or flea species assemblages.

Are carnivores universally good sentinels of plague?

Sylvatic plague, caused by the bacterium Yersinia pestis, is a flea-borne disease that primarily affects rodents but has been detected in over 200 mammal species worldwide. Mammalian carnivores are routinely surveyed as sentinels of local plague activity, since they can present antibodies to Y. pestis infection but show few clinical signs. In Boulder County, Colorado, USA, plague epizootic events are episodic and occur in black-tailed prairie dogs. Enzootic hosts are unidentified as are plague foci. For three years, we systematically sampled carnivores in two distinct habitat types to determine whether carnivores may play a role in maintenance or transmission of Y. pestis and to identify habitats associated with increased plague prevalence. We sampled 83 individuals representing six carnivore species and found only two that had been exposed to Y. pestis. The low overall rate of plague exposure in carnivores suggests that plague may be ephemeral in this study system, and thus we cannot draw any conclusions regarding habitat-associated plague foci or temporal changes in plague activity. Plague epizootics involving prairie dogs were confirmed in this study system during two of the three years of this study, and we therefore suggest that the targeting carnivores to survey for plague may not be appropriate in all ecological systems.

Transient patterns in the assembly of vernal pool plant communities.

Community assembly theory asserts that the contemporary composition of ecological communities may depend critically on events that occur during the formation of the community; a phenomenon termed "historical contingence." We tested key aspects of this theory using plant communities in over 200 experimentally created vernal pools at a field site in central California, USA. The experiment was initiated in 1999 with construction of vernal pool basins into which different seeding treatments were imposed to evaluate the effects of dispersal limitation, order of colonization ("priority effects"), and frequency of colonization on plant community composition. We tracked the abundance and distribution of five focal species for seven years following seeding and observed strong but transient effects of seeding, as well as order and frequency of colonization. All five species occurred with higher frequency in seeded pools vs. unseeded control pools, demonstrating dispersal limitation. Three of four species exerted strong priority effects, with much higher abundance in pools in which they were seeded first compared to pools in which they were seeded in the second year of the study, one year after other species were seeded. We tested for effects of frequency of colonization using one species, the endangered Lasthenia conjugens, and observed much higher abundance in frequently vs. infrequently seeded pools for the first four years following seeding. Finally, we observed that the strength of priority effects varied significantly with water depth for one of the species groups, which demonstrates that abiotic context can strongly influence species interactions. We conclude that several aspects of historical contingence play key roles in the early formation of vernal pool plant communities. But we also observed reversals in community trajectories, suggesting that in this system historical effects may be lost within a decade.

Characterization of Bartonella strains isolated from black-tailed prairie dogs (Cynomys ludovicianus).

Thirty bartonella strains were isolated from the blood of black-tailed prairie dogs (Cynomys ludovicianus) from Boulder County, Colorado, USA. The bacteria appeared as small, fastidious, aerobic, Gram-negative rods. The partial sequences of the citrate synthase gene (gltA) demonstrated five unique genetic variants. Phylogenetic analysis based on sequences of gltA, 16S rRNA, rpoB, ftsZ, and ribC showed that the black-tailed prairie dog-related Bartonella variants comprise a distinct monophyletic clade that is closely related to Bartonella washoensis, a species isolated from a human patient and subsequently from ground squirrels. These variants, however, are grouped together in 100% of the bootstrapped trees. These variants were not found in other small mammals trapped during the same study, showing some evidence of host specificity. We believe that the group being described here is typical of the black-tailed prairie dog. We propose to name the bacteria Candidatus Bartonella washoensis subsp. cynomysii. The type strain is CL8606co(T)(=ATCC BAA-1342(T) = CCUG 53213(T)), which is the representative isolate of the dominant variant of the characterized group.

Acquisition of nonspecific Bartonella strains by the northern grasshopper mouse (Onychomys leucogaster).

Rodent-associated Bartonella species are generally host-specific parasites in North America. Here evidence that Bartonella species can 'jump' between host species is presented. Northern grasshopper mice and other rodents were trapped in the western USA. A study of Bartonella infection in grasshopper mice demonstrated a high prevalence that varied from 25% to 90% by location. Bartonella infection was detected in other rodent species with a high prevalence as well. Sequence analyses of gltA identified 29 Bartonella variants in rodents, 10 of which were obtained from grasshopper mice. Among these 10, only six variants were specific to grasshopper mice, whereas four were identical to variants specific to deer mice or 13-lined ground squirrels. Fourteen of 90 sequenced isolates obtained from grasshopper mice were strains found more commonly in other rodent species and were apparently acquired from these animals. The ecological behavior of grasshopper mice may explain the occurrence of Bartonella strains in occasional hosts. The observed rate at which Bartonella jumps from a donor host species to the grasshopper mouse was directly proportional to a metric of donor host density and to the prevalence of Bartonella in the donor host, and inversely proportional to the same parameters for the grasshopper mouse.

Abiotic constraints eclipse biotic resistance in determining invasibility along experimental vernal pool gradients.

Effective management of invasive species requires that we understand the mechanisms determining community invasibility. Successful invaders must tolerate abiotic conditions and overcome resistance from native species in invaded habitats. Biotic resistance to invasions may reflect the diversity, abundance, or identity of species in a community. Few studies, however, have examined the relative importance of abiotic and biotic factors determining community invasibility. In a greenhouse experiment, we simulated the abiotic and biotic gradients typically found in vernal pools to better understand their impacts on invasibility. Specifically, we invaded plant communities differing in richness, identity, and abundance of native plants (the "plant neighborhood") and depth of inundation to measure their effects on growth, reproduction, and survival of five exotic plant species. Inundation reduced growth, reproduction, and survival of the five exotic species more than did plant neighborhood. Inundation reduced survival of three species and growth and reproduction of all five species. Neighboring plants reduced growth and reproduction of three species but generally did not affect survival. Brassica rapa, Centaurea solstitialis, and Vicia villosa all suffered high mortality due to inundation but were generally unaffected by neighboring plants. In contrast, Hordeum marinum and Lolium multiflorum, whose survival was unaffected by inundation, were more impacted by neighboring plants. However, the four measures describing plant neighborhood differed in their effects. Neighbor abundance impacted growth and reproduction more than did neighbor richness or identity, with growth and reproduction generally decreasing with increasing density and mass of neighbors. Collectively, these results suggest that abiotic constraints play the dominant role in determining invasibility along vernal pool and similar gradients. By reducing survival, abiotic constraints allow only species with the appropriate morphological and physiological traits to invade. In contrast, biotic resistance reduces invasibility only in more benign environments and is best predicted by the abundance, rather than diversity, of neighbors. These results suggest that stressful environments are not likely to be invaded by most exotic species. However, species, such as H. marinum, that are able to invade these habitats require careful management, especially since these environments often harbor rare species and communities.

Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores.

We investigated the effects of genotype, habitat, and seasonal variation on production of the iridoid glycosides, aucubin and catalpol, in leaves of the common weed Plantago lanceolata. Two genotypes, one each from a lawn and an adjacent abandoned hayfield population, were clonally replicated in the greenhouse, and then planted back into the two habitats. One quarter of the plants from each treatment were harvested on each of four dates, at approximately two-week intervals. Over the course of the growing season, and in both habitats, we found a significant increase in the concentration of both aucubin and catalpol in P. lanceolata leaves. The genotypes differed in their response to environmental variation, both in time and between sites, as indicated by significant genotype x date and genotype x site interactions. Early in the season, habitat (lawn or field) had a greater effect on iridoid glycoside concentration than did plant genotype, but later in the season, plant genotype was more influential in determining the iridoid glycoside concentration. Thus, the relative palatability of Plantago genotypes to specialist and generalist herbivores may vary in time and space.