Wind and small mammals are complementary fungal dispersers.

Following a disturbance, dispersal shapes community composition as well as ecosystem structure and function. For fungi, dispersal is often wind or mammal facilitated, but it is unclear whether these pathways are complementary or redundant in the taxa they disperse and the ecosystem functions they provide. Here, we compare the diversity and morphology of fungi dispersed by wind and three rodent species in recently harvested forests using a combination of microscopy and Illumina sequencing. We demonstrate that fungal communities dispersed by wind and small mammals differ in richness and composition. Most wind-dispersed fungi are wood saprotrophs, litter saprotrophs, and plant pathogens, whereas fungi dispersed in mammal scat are primarily mycorrhizal, soil saprotrophs, and unspecified saprotrophs. We note substantial dispersal of truffles and agaricoid mushrooms by small mammals, and dispersal of agaricoid mushrooms, crusts, and polypores by wind. In addition, we find mammal-dispersed spores are larger than wind-dispersed spores. Our findings suggest that wind- and small-mammal-facilitated dispersal are complementary processes and highlight the role of small mammals in dispersing mycorrhizal fungi, particularly following disturbances such as timber harvest.

Small herbivores with big impacts: Tundra voles (Microtus oeconomus) alter post-fire ecosystem dynamics.

Fire is an important ecological disturbance that can reset ecosystems and initiate changes in plant community composition, ecosystem biogeochemistry, and primary productivity. As herbivores rely on primary producers for food, changes in vegetation may alter plant-herbivore interactions with important-but often unexplored-feedbacks to ecosystems. Here we examined the impact of post-fire changes in plant community composition and structure on habitat suitability and rodent herbivore activity in response to a large, severe, and unprecedented fire in northern Alaskan tundra. In moist acidic tundra where the fire occurred, tundra voles (Microtus oeconomus) are the dominant herbivore and rely on the tussock forming sedge Eriophorum vaginatum for both food and nesting material. Tundra voles were 10 times more abundant at the burned site compared with nearby unburned tundra 7-12 years after the fire. Fire increased the habitat suitability for voles by increasing plant productivity and biomass, food quality, and cover through both taller vegetation and increased microtopography. As a result of elevated vole abundance, Eriophorum mortality caused by vole herbivory was two orders of magnitude higher than natural mortality and approached the magnitude of the mortality rate resulting directly from the fire. These findings suggest that post-fire increases in herbivore pressure on Eriophorum could, in turn, disrupt graminoid recovery and enhance shrub encroachment. Tundra state transitions from graminoid to shrub dominated are also evident following other disturbances and fertilization experiments, suggesting that as Arctic temperatures rise, greater available nutrients and increased frequencies of large-scale disturbances may also alter plant-animal interactions with cascading impacts on plant communities and ecosystem function.

Model responses to CO2 and warming are underestimated without explicit representation of Arctic small-mammal grazing.

We use a simple model of coupled carbon and nitrogen cycles in terrestrial ecosystems to examine how "explicitly representing grazers" vs. "having grazer effects implicitly aggregated in with other biogeochemical processes in the model" alters predicted responses to elevated carbon dioxide and warming. The aggregated approach can affect model predictions because grazer-mediated processes can respond differently to changes in climate compared with the processes with which they are typically aggregated. We use small-mammal grazers in a tundra as an example and find that the typical three-to-four-year cycling frequency is too fast for the effects of cycle peaks and troughs to be fully manifested in the ecosystem biogeochemistry. We conclude that implicitly aggregating the effects of small-mammal grazers with other processes results in an underestimation of ecosystem response to climate change, relative to estimations in which the grazer effects are explicitly represented. The magnitude of this underestimation increases with grazer density. We therefore recommend that grazing effects be incorporated explicitly when applying models of ecosystem response to global change.

The underappreciated role of rodent generalists in fungal spore dispersal networks.

Animals are often the primary dispersers of seeds and fungal spores. Specialist species that consume fruits or fungal fruiting bodies (sporocarps) as their main food source are thought to play a more important role in dispersal networks compared to generalist species. However, dispersal networks are often based on occurrence data, overlooking the influence of animal abundance and dispersal effectiveness on network interactions. Using rodent-mycorrhizal fungi networks, we determined how diet specialization and abundance influence the role of rodent species in dispersing fungal spores in temperate forests of northern New Hampshire, USA. We tracked the interactions of five rodent species and 34 fungal taxa over a 3-yr period across hardwood, mixed, and softwood forest stands. We accounted for fluctuations in rodent abundance and differences in the number of spores dispersed in rodent scat. Myodes gapperi, a fungal specialist, dispersed a more diverse spore community than rodent generalists and was consistently the most important disperser in forest types with high fungal availability. Nevertheless, during years when generalist species such as Tamias striatus and Peromyscus maniculatus reached high abundance, their relative importance (species strength) in networks approached or even surpassed that of M. gapperi, particularly in forest types where M. gapperi was less common and fungal availability was low. Increased numbers of generalists enhanced network interaction diversity and the number of fungal taxa dispersed, the timing of which was coincident with seedling establishment following masting, a stage when inoculation by mycorrhizal fungi is critical for growth and survival. Our findings suggest that although specialists play key roles in dispersing mycorrhizal fungal spores, generalists play a heretofore underappreciated role.

Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions.

Many plant and fungal species use volatile organic compounds (VOCs) as chemical signals to convey information about the location or quality of their fruits or fruiting bodies to animal dispersers. Identifying the environmental factors and biotic interactions that shape fruit selection by animals is key to understanding the evolutionary processes that underpin chemical signaling. Using four Elaphomyces truffle species, we explored the role of fruiting depth, VOC emissions, and protein content in selection by five rodent species. We used stable isotope analysis of nitrogen (δ15 N) in truffles to estimate fruiting depth, proton-transfer-reaction mass spectrometry to determine volatile emission composition, and nitrogen concentrations to calculate digestible protein of truffles. We coupled field surveys of truffle availability with truffle spore loads in rodent scat to determine selection by rodents. Despite presumably easier access to the shallow fruiting species, E. americanus (0.5-cm depth) and E. verruculosus (2.5-cm depth), most rodents selected for truffles fruiting deeper in the soil, E. macrosporus (4.1-cm depth) and E. bartlettii (5.0-cm depth). The deeper fruiting species had distinct VOC profiles and produced significantly higher quantities of odiferous compounds. Myodes gapperi (southern red-backed vole), a fungal specialist, also selected for truffles with high levels of digestible protein, E. verruculosus and E. macrosporus. Our results highlight the importance of chemical signals in truffle selection by rodents and suggest that VOCs are under strong selective pressures relative to protein rewards. Strong chemical signals likely allow detection of truffles deep within the soil and reduce foraging effort by rodents. For rodents that depend on fungi as a major food source, protein content may also be important in selecting truffles.

Pulsed resource availability changes dietary niche breadth and partitioning between generalist rodent consumers.

Identifying the mechanisms that structure niche breadth and overlap between species is important for determining how species interact and assessing their functional role in an ecosystem. Without manipulative experiments, assessing the role of foraging ecology and interspecific competition in structuring diet is challenging. Systems with regular pulses of resources act as a natural experiment to investigate the factors that influence the dietary niches of consumers. We used natural pulses of mast-fruiting of American beech (Fagus grandifolia) to test whether optimal foraging or competition structure the dietary niche breadth and overlap between two congener rodent species (Peromyscus leucopus and P. maniculatus), both of which are generalist consumers. We reconstructed diets seasonally over a 2-year period using stable isotope analysis (δ13C, δ15N) of hair and of potential dietary items and measured niche dynamics using standard ellipse area calculated within a Bayesian framework. Changes in niche breadth were generally consistent with predictions of optimal foraging theory, with both species consuming more beechnuts (a high-quality food resource) and having a narrower niche breadth during masting seasons compared to nonmasting seasons when dietary niches expanded and more fungi (a low-quality food source) were consumed. In contrast, changes in dietary niche overlap were consistent with competition theory, with higher diet overlap during masting seasons than during nonmasting seasons. Overall, dietary niche dynamics were closely tied to beech masting, underscoring that food availability influences competition. Diet plasticity and niche partitioning between the two Peromyscus species may reflect differences in foraging strategies, thereby reducing competition when food availability is low. Such dietary shifts may have important implications for changes in ecosystem function, including the dispersal of fungal spores.

Emergent lineages of mumps virus suggest the need for a polyvalent vaccine.

Mumps outbreaks among vaccinated patients have become increasingly common in recent years. While there are multiple conditions driving this re-emergence, convention has suggested that these outbreaks are associated with waning immunity rather than vaccine escape. Molecular evidence from both the ongoing American and Dutch outbreaks in conjunction with recent structural biology studies challenge this convention, and suggest that emergent lineages of mumps virus exhibit key differences in antigenic epitopes from the vaccine strain employed: Jeryl-Lynn 5. The American and Dutch 2016-2017 outbreak lineages were examined using computational biology through the lens of diversity in immunogenic epitopes. Findings are discussed and the laboratory evidence indicating neutralization of heterologous mumps strains by serum from vaccinated individuals is reviewed. Taken together, it is concluded that the number of heterologous epitopes occurring in mumps virus in conjunction with waning immunity is facilitating small outbreaks in vaccinated patients, and that consideration of a polyvalent mumps vaccine is warranted.

Genotype-environment associations support a mosaic hybrid zone between two tidal marsh birds.

Local environmental features can shape hybrid zone dynamics when hybrids are bounded by ecotones or when patchily distributed habitat types lead to a corresponding mosaic of genotypes. We investigated the role of marsh-level characteristics in shaping a hybrid zone between two recently diverged avian taxa - Saltmarsh (Ammodramus caudacutus) and Nelson's (A. nelsoni) sparrows. These species occupy different niches where allopatric, with caudacutus restricted to coastal marshes and nelsoni found in a broader array of wetland and grassland habitats and co-occur in tidal marshes in sympatry. We determined the influence of habitat types on the distribution of pure and hybrid sparrows and assessed the degree of overlap in the ecological niche of each taxon. To do this, we sampled and genotyped 305 sparrows from 34 marshes across the hybrid zone and from adjacent regions. We used linear regression to test for associations between marsh characteristics and the distribution of pure and admixed sparrows. We found a positive correlation between genotype and environmental variables with a patchy distribution of genotypes and habitats across the hybrid zone. Ecological niche models suggest that the hybrid niche was more similar to that of A. nelsoni and habitat suitability was influenced strongly by distance from coastline. Our results support a mosaic model of hybrid zone maintenance, suggesting a role for local environmental features in shaping the distribution and frequency of pure species and hybrids across space.

Energy flow and functional compensation in Great Basin small mammals under natural and anthropogenic environmental change.

Research on the ecological impacts of environmental change has primarily focused at the species level, leaving the responses of ecosystem-level properties like energy flow poorly understood. This is especially so over millennial timescales inaccessible to direct observation. Here we examine how energy flow within a Great Basin small mammal community responded to climate-driven environmental change during the past 12,800 y, and use this baseline to evaluate responses observed during the past century. Our analyses reveal marked stability in energy flow during rapid climatic warming at the terminal Pleistocene despite dramatic turnover in the distribution of mammalian body sizes and habitat-associated functional groups. Functional group turnover was strongly correlated with climate-driven changes in regional vegetation, with climate and vegetation change preceding energetic shifts in the small mammal community. In contrast, the past century has witnessed a substantial reduction in energy flow caused by an increase in energetic dominance of small-bodied species with an affinity for closed grass habitats. This suggests that modern changes in land cover caused by anthropogenic activities--particularly the spread of nonnative annual grasslands--has led to a breakdown in the compensatory dynamics of energy flow. Human activities are thus modifying the small mammal community in ways that differ from climate-driven expectations, resulting in an energetically novel ecosystem. Our study illustrates the need to integrate across ecological and temporal scales to provide robust insights for long-term conservation and management.

Environmental change and declining resource availability for small-mammal communities in the Great Basin.

Changes in climate and land use can impact natural systems across all levels of ecological organization. Most documented and anticipated effects consider species' properties, including phenologies, geographic distributions, and abundances. Responses of higher-level aggregate community or ecosystem properties have not been considered as they are assumed to be relatively stable due to compensatory dynamics and diversity-stability relationships. However, this assumption may not be as fundamental as previously thought. Here we assess stability in the aggregate properties of total abundance, biomass, and energy consumption for small-mammal communities in the Great Basin, using paired historical and modern survey data spanning nearly a century of environmental change. Results show marked declines in each aggregate property independent of spatial scale, elevation, or habitat type, and a reallocation of available biomass and energy favoring diet and habitat generalists. Because aggregate properties directly reflect resource availability, our findings indicate a regionwide decline in resources of 50% over the past century, which may signal a resource crisis. This work illustrates the power of using aggregate properties as indicators of ecological conditions and environmental change at broad spatial and temporal scales.

DNA interstrand cross-linking activity of (1-Chloroethenyl)oxirane, a metabolite of beta-chloroprene.

With the goal of elucidating the molecular and cellular mechanisms of chloroprene toxicity, we examined the potential DNA cross-linking of the bifunctional chloroprene metabolite, (1-chloroethenyl)oxirane (CEO). We used denaturing polyacrylamide gel electrophoresis to monitor the possible formation of interstrand cross-links by CEO within synthetic DNA duplexes. Our data suggest interstrand cross-linking at deoxyguanosine residues within 5'-GC and 5'-GGC sites, with the rate of cross-linking depending on pH (pH 5.0 > pH 6.0 > pH 7.0). A comparison of the cross-linking efficiencies of CEO and the structurally similar cross-linkers diepoxybutane (DEB) and epichlorohydrin (ECH) revealed that DEB > CEO > or = ECH. Furthermore, we found that cytotoxicity correlates with cross-linking efficiency, supporting a role for interstrand cross-links in the genotoxicology of chloroprene.

Legacies of land use and recent climatic change: the small mammal fauna in the mountains of Utah.

Climate warming will continue alongside human modification of the landscape. Therefore, studying systems modified by land use may highlight factors that mitigate or exacerbate predicted biological responses to ongoing climate warming. Using historical museum specimen records and recent field surveys, I examine temporal patterns in the ecological dynamics of the small mammal fauna on five mountain ranges in central Utah over time intervals of 27-53 years during the past century. This landscape was heavily modified by livestock grazing early in the twentieth century and since then has witnessed a steady decline in grazing intensity. In general, at regional and landscape scales, species preferring mesic habitats increased in percent abundance, rank abundance, and rank occurrence over time. This result is opposite that predicted from regional climate trends and probably represents the recovery of forest conditions following a release over time from earlier periods of severe overgrazing. Decreased grazing intensity may thus mitigate the predicted biological effects of climatically driven environmental change for small mammals. This work also illustrates that abundance data gleaned from natural history collections can be an appropriate tool for assessing temporal changes in composition, especially when comparisons are drawn using time- and space-averaged data sets.