The impacts of increasing drought on forest dynamics, structure, and biodiversity in the United States.

We synthesize insights from current understanding of drought impacts at stand-to-biogeographic scales, including management options, and we identify challenges to be addressed with new research. Large stand-level shifts underway in western forests already are showing the importance of interactions involving drought, insects, and fire. Diebacks, changes in composition and structure, and shifting range limits are widely observed. In the eastern US, the effects of increasing drought are becoming better understood at the level of individual trees, but this knowledge cannot yet be confidently translated to predictions of changing structure and diversity of forest stands. While eastern forests have not experienced the types of changes seen in western forests in recent decades, they too are vulnerable to drought and could experience significant changes with increased severity, frequency, or duration in drought. Throughout the continental United States, the combination of projected large climate-induced shifts in suitable habitat from modeling studies and limited potential for the rapid migration of tree populations suggests that changing tree and forest biogeography could substantially lag habitat shifts already underway. Forest management practices can partially ameliorate drought impacts through reductions in stand density, selection of drought-tolerant species and genotypes, artificial regeneration, and the development of multistructured stands. However, silvicultural treatments also could exacerbate drought impacts unless implemented with careful attention to site and stand characteristics. Gaps in our understanding should motivate new research on the effects of interactions involving climate and other species at the stand scale and how interactions and multiple responses are represented in models. This assessment indicates that, without a stronger empirical basis for drought impacts at the stand scale, more complex models may provide limited guidance.

When is a parasite not a parasite? Effects of larval tick burdens on white-footed mouse survival.

Many animal species can carry considerable burdens of ectoparasites: parasites living on the outside of a host's body. Ectoparasite infestation can decrease host survival, but the magnitude and even direction of survival effects can vary depending on the type of ectoparasite and the nature and duration of the association. When ectoparasites also serve as vectors of pathogens, the effects of ectoparasite infestation on host survival have the potential to alter disease dynamics by regulating host populations and stabilizing transmission. We quantified the impact of larval Ixodes scapularis tick burdens on both within-season and overwinter survival of white-footed mice (Peromyscus leucopus) using a hierarchical Bayesian capture-mark-recapture model. I. scapularis and P. leucopus are, respectively, vectors and competent reservoirs for the causative agents of Lyme disease, anaplasmosis, and babesiosis. Using a data set of 5587 individual mouse capture histories over sixteen years, we found little evidence for any effect of tick burdens on either within-season or overwinter mouse survival probabilities. In male mice, tick burdens were positively correlated with within-season survival probabilities. Mean maximum tick burdens were also positively correlated with population rates of change during the concurrent breeding season. The apparent indifference of mice to high tick burdens may contribute to their effectiveness as reservoir hosts for several human zoonotic pathogens.

Reservoir competence of wildlife host species for Babesia microti.

Human babesiosis is an increasing health concern in the northeastern United States, where the causal agent, Babesia microti, is spread through the bite of infected Ixodes scapularis ticks. We sampled 10 mammal and 4 bird species within a vertebrate host community in southeastern New York to quantify reservoir competence (mean percentage of ticks infected by an individual host) using real-time PCR. We found reservoir competence levels >17% in white-footed mice (Peromyscus leucopus), raccoons (Procyon lotor), short-tailed shrews (Blarina brevicauda), and eastern chipmunks (Tamias striatus), and <6% but >0% in all other species, including all 4 bird species. Data on the relative contributions of multiple host species to tick infection with B. microti and level of genetic differentiation between B. microti strains transmitted by different hosts will help advance understanding of the spread of human babesiosis.

Reservoir competence of vertebrate hosts for Anaplasma phagocytophilum.

Fourteen vertebrate species (10 mammals and 4 birds) were assessed for their ability to transmit Anaplasma phagocytophilum, the bacterium that causes human granulocytic anaplasmosis, to uninfected feeding ixodid ticks. Small mammals were most likely to infect ticks but all species assessed were capable of transmitting the bacterium, in contrast to previous findings.

Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival.

Host-specific mortality driven by natural enemies is a widely discussed mechanism for explaining plant diversity. In principle, populations of plant species can be regulated by distinct host-specific natural enemies that have weak or nonexistent effects on heterospecific competitors, preventing any single species from becoming dominant and thus promoting diversity. Two of the first steps in exploring the role of natural enemies in diversity regulation are to (1) identify potential enemies and (2) evaluate their levels of host specificity by determining if interactions between any one host and its enemy have equivalent survival impacts on co-occurring host species. We developed a bioinformatics framework to evaluate impacts of potential pathogens on seedling survival, for both single and multiple infections. Importantly, we consider scenarios not only if there are specialist pathogens for each plant, but also when generalist pathogens have differential effects on multiple host species, and when co-infection has species-specific effects. We then applied this analytical framework to a field experiment using molecular techniques to detect potential fungal pathogens on co-occurring tree seedling hosts. Combinatorial complexity created by 160 plant-fungus interactions was reduced to eight combinations that affect seedling survival. Potential fungal pathogens had broad host ranges, but seedling species were each regulated by different combinations of fungi or by generalist fungi that had differential effects on multiple plant species. Soil moisture can have the potential to shift the nature of the interactions in some plant-fungal combinations from neutral to detrimental. Reassessing the assumption of single-enemy-single-host interactions broadens the mechanisms through which natural enemies can influence plant diversity.

Individual-scale variation, species-scale differences: inference needed to understand diversity.

As ecological data are usually analysed at a scale different from the one at which the process of interest operates, interpretations can be confusing and controversial. For example, hypothesised differences between species do not operate at the species level, but concern individuals responding to environmental variation, including competition with neighbours. Aggregated data from many individuals subject to spatio-temporal variation are used to produce species-level averages, which marginalise away the relevant (process-level) scale. Paradoxically, the higher the dimensionality, the more ways there are to differ, yet the more species appear the same. The aggregate becomes increasingly irrelevant and misleading. Standard analyses can make species look the same, reverse species rankings along niche axes, make the surprising prediction that a species decreases in abundance when a competitor is removed from a model, or simply preclude parameter estimation. Aggregation explains why niche differences hidden at the species level become apparent upon disaggregation to the individual level, why models suggest that individual-level variation has a minor impact on diversity when disaggregation shows it to be important, and why literature-based synthesis can be unfruitful. We show how to identify when aggregation is the problem, where it has caused controversy, and propose three ways to address it.

Community context for mechanisms of disease dilution: insights from linking epidemiology and plant-soil feedback theory.

In many natural systems, diverse host communities can reduce disease risk, though less is known about the mechanisms driving this "dilution effect." We relate feedback theory, which focuses on pathogen-mediated coexistence, to mechanisms of dilution derived from epidemiological models, with the central goal of gaining insights into host-pathogen interactions in a community context. We first compare the origin, structure, and application of epidemiological and feedback models. We then explore the mechanisms of dilution, which are grounded in single-pathogen, single-host epidemiological models, from the perspective of feedback theory. We also draw on feedback theory to examine how coinfecting pathogens, and pathogens that vary along a host specialist-generalist continuum, apply to dilution theory. By identifying synergies among the feedback and epidemiological approaches, we reveal ways in which organisms occupying different trophic levels contribute to diversity-disease relationships. Additionally, using feedbacks to distinguish dilution in disease incidence from dilution in the net effect of disease on host fitness allows us to articulate conditions under which definitions of dilution may not align. After ascribing dilution mechanisms to macro- or microorganisms, we propose ways in which each contributes to diversity-disease and productivity-diversity relationships. Our analyses lead to predictions that can guide future research efforts.

Co-infection of blacklegged ticks with Babesia microti and Borrelia burgdorferi is higher than expected and acquired from small mammal hosts.

Humans in the northeastern and midwestern United States are at increasing risk of acquiring tickborne diseases--not only Lyme disease, but also two emerging diseases, human granulocytic anaplasmosis and human babesiosis. Co-infection with two or more of these pathogens can increase the severity of health impacts. The risk of co-infection is intensified by the ecology of these three diseases because all three pathogens (Borrelia burgdorferi, Anaplasma phagocytophilum, and Babesia microti) are transmitted by the same vector, blacklegged ticks (Ixodes scapularis), and are carried by many of the same reservoir hosts. The risk of exposure to multiple pathogens from a single tick bite and the sources of co-infected ticks are not well understood. In this study, we quantify the risk of co-infection by measuring infection prevalence in 4,368 questing nymphs throughout an endemic region for all three diseases (Dutchess County, NY) to determine if co-infections occur at frequencies other than predicted by independent assortment of pathogens. Further, we identify sources of co-infection by quantifying rates of co-infection on 3,275 larval ticks fed on known hosts. We find significant deviations of levels of co-infection in questing nymphs, most notably 83% more co-infection with Babesia microti and Borrelia burgdorferi than predicted by chance alone. Further, this pattern of increased co-infection was observed in larval ticks that fed on small mammal hosts, but not on meso-mammal, sciurid, or avian hosts. Co-infections involving A. phagocytophilum were less common, and fewer co-infections of A. phagocytophilum and B. microti than predicted by chance were observed in both questing nymphs and larvae fed on small mammals. Medical practitioners should be aware of the elevated risk of B. microti/B. burgdorferi co-infection.

Pathogen regulation of plant diversity via effective specialization.

The Janzen-Connell (JC) hypothesis, one of the most influential hypotheses explaining forest diversity, is inconsistent with evidence that tree species share the same natural enemies. Through the discussion of seedling diseases from a pathogen-centered perspective, we expand the JC hypothesis to tie in host-pathogen-environment interactions at three levels: local adaptation, host specificity of the combined effect of multiple infections, and environmental modulation of disease. We present evidence from plant pathology, disease ecology, and host-parasite evolution relevant to (but not commonly associated with) forest species diversity maintenance. This expanded view of the JC hypothesis suggests ways to direct new experiments to integrate research on pathogen local adaptation, co-infection, and environmental effects on infection by using high-throughput molecular techniques and statistical models.

A predictive framework to understand forest responses to global change.

Forests are one of Earth's critical biomes. They have been shown to respond strongly to many of the drivers that are predicted to change natural systems over this century, including climate, introduced species, and other anthropogenic influences. Predicting how different tree species might respond to this complex of forces remains a daunting challenge for forest ecologists. Yet shifts in species composition and abundance can radically influence hydrological and atmospheric systems, plant and animal ranges, and human populations, making this challenge an important one to address. Forest ecologists have gathered a great deal of data over the past decades and are now using novel quantitative and computational tools to translate those data into predictions about the fate of forests. Here, after a brief review of the threats to forests over the next century, one of the more promising approaches to making ecological predictions is described: using hierarchical Bayesian methods to model forest demography and simulating future forests from those models. This approach captures complex processes, such as seed dispersal and mortality, and incorporates uncertainty due to unknown mechanisms, data problems, and parameter uncertainty. After describing the approach, an example by simulating drought for a southeastern forest is offered. Finally, there is a discussion of how this approach and others need to be cast within a framework of prediction that strives to answer the important questions posed to environmental scientists, but does so with a respect for the challenges inherent in predicting the future of a complex biological system.