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Effect of climate change on disease spread in wildlife

A growing body of evidence indicates that climate change alone, or acting synergistically with current anthropogenic threats, is affecting the health of wild populations of aquatic and terrestrial wildlife. Measurable by-products of climate change include elevated atmospheric concentrations of greenhouse gases, higher average global temperatures; variations in global precipitation patterns, rising and warming oceans, altered hydrographs of rivers, and increased mid-continental drying during summer. These consequences affect the terrestrial environment through shifts in phenology, vegetation cover, and fire regimes. Warmer ocean temperatures, increased acidification, rise in sea levels, and reduction in sea ice cover are also leading to widespread ecological changes in marine systems. Wildlife populations face a variety of climate-related pressures, such as changes in animal distribution or density, limitation of food resources, and alteration to critical habitats. The increased potential for emergence and resurgence of diseases that are responsive to environmental conditions also has implications for wildlife populations. Shifts in temperature or other climatic factors may directly affect the incidence of disease in wildlife by altering host-pathogen interactions, promoting vector populations or allowing new ranges for vectors, or reducing development times for parasites. A number of examples from both field and laboratory studies have demonstrated a clear link between warming environments and disease spread. Many climate-related environmental changes also influence wildlife health indirectly. For example, increasing temperatures, in combination with shifts in rainfall and humidity, may aggravate current trends for water resource limitation and habitat degradation or destruction and lead to increased crowding of animal populations, thereby promoting transmission opportunities of pathogens within populations or across species. Although it may be difficult to disentangle the influences of other anthropogenic changes from the direct effects of warming, some ecosystems provide especially useful models for studying climate-related disease spread in wildlife. For example, the effects of climate change on parasite dynamics may be easily observed in the Arctic, where environmental changes are occurring rapidly, anthropogenic influences are relatively limited, and biodiversity is generally low. Marine ecosystems are also undergoing rapid rates of change and may be vulnerable to a variety of natural and anthropogenic perturbations. Although many factors affect the health of organisms in ocean environments, temperature has been clearly linked to an increase in disease prevalence among sessile organisms such as corals. In this chapter, we discuss observed and predicted changes to wildlife health resulting from climate change. Our review will not include all aspects of wildlife health, but will instead focus on established or suspected links between climate drivers and disease spread and discuss examples from the current literature. Here, we define disease spread to include: 1) change in geographical or altitudinal distribution of pathogens, parasites, and vectors and the diseases they cause; 2) change in prevalence or severity of disease; and 3) emergence of novel diseases. Additionally, because wildlife species serve as reservoirs for zoonotic diseases that affect both animals and humans, we include select examples of the effect of climate change on the capacity of wildlife to harbor and spread these disease agents.

Book chapter

Ecological divergence of wild birds drives avian influenza spillover and global spread

The diversity of influenza A viruses (IAV) is primarily hosted by two highly divergent avian orders: Anseriformes (ducks, swans and geese) and Charadriiformes (gulls, terns and shorebirds). Studies of IAV have historically focused on Anseriformes, specifically dabbling ducks, overlooking the diversity of hosts in nature, including gull and goose species that have successfully adapted to human habitats. This study sought to address this imbalance by characterizing spillover dynamics and global transmission patterns of IAV over 10 years at greater taxonomic resolution than previously considered. Furthermore, the circulation of viral subtypes in birds that are either host-adapted (low pathogenic H13, H16) or host-generalist (highly pathogenic avian influenza—HPAI H5) provided a unique opportunity to test and extend models of viral evolution. Using Bayesian phylodynamic modelling we uncovered a complex transmission network that relied on ecologically divergent bird hosts. The generalist subtype, HPAI H5 was driven largely by wild geese and swans that acted as a source for wild ducks, gulls, land birds, and domestic geese. Gulls were responsible for moving HPAI H5 more rapidly than any other host, a finding that may reflect their long-distance, pelagic movements and their immuno-naïve status against this subtype. Wild ducks, long viewed as primary hosts for spillover, occupied an optimal space for viral transmission, contributing to geographic expansion and rapid dispersal of HPAI H5. Evidence of inter-hemispheric dispersal via both the Pacific and Atlantic Rims was detected, supporting surveillance at high latitudes along continental margins to achieve early detection. Both neutral (geographic expansion) and non-neutral (antigenic selection) evolutionary processes were found to shape subtype evolution which manifested as unique geographic hotspots for each subtype at the global scale. This study reveals how a diversity of avian hosts contribute to viral spread and spillover with the potential to improve surveillance in an era of rapid global change.

PLoS Pathogens

Virulence evolution of a salmonid virus following a host jump

Emergent viral diseases remain a critical obstacle to welfare across landscapes and species, encompassing humans, wildlife, and agriculture. Following a jump to a novel host, the severity of disease resulting from infection is a critical determinant of the overall emergent pathogen threat. Conventional wisdom posits that virulence, defined here as host mortality, attenuates to intermediate levels as a pathogen adapts to a novel host, but this is largely based on data from just one system, myxoma virus, which was intentionally introduced as a biocontrol agent in rabbits ( Oryctolagus cuniculus ) in mid-1900s Australia. In this study, we demonstrate that infectious hematopoietic necrosis virus (IHNV), which made a host jump from sockeye salmon ( Oncorhynchus nerka , ancestral host) to rainbow trout ( O. mykiss , novel host), has not conformed to classical theory. We quantified virulence in the ancestral and novel hosts using common garden in vivo experiments with 16 archival IHNV isolates collected from 1972-2017, which span the period from shortly after the host jump and the subsequent 45 years of host adaptation. These virus isolates also represent two distinct phylogenetic genogroups, each associated with either the ancestral or novel host. The experiments were replicated across two research facilities, two challenges dosages, and two temperatures. While isolates from the ancestral genogroup showed no temporal change in virulence in either host, isolates from the novel viral genogroup displayed a significant increase in virulence over time in the novel host. Some possible indication of a virus temperature adaption after the host jump was also present. Potential drivers of virulence evolution are discussed. This represents one of only a handful of systems in which the evolution of increased virulence has been empirically characterized after a host jump and subsequent adaptation. It contributes to a growing body of evidence that contradicts the classical case study of myxoma virus attenuation after adaptation.

PLoS Pathogens

Evidence for the use of mucus swabs to detect Renibacterium salmoninarum in brook trout

Efforts to advance fish health diagnostics have been highlighted in many studies to improve the detection of pathogens in aquaculture facilities and wild fish populations. Typically, the detection of a pathogen has required sacrificing fish; however, many hatcheries have valuable and sometimes irreplaceable broodstocks, and lethal sampling is undesirable. Therefore, the development of non-lethal detection methods is a high priority. The goal of our study was to compare non-lethal sampling methods with standardized lethal kidney tissue sampling that is used to detect Renibacterium salmoninarum infections in salmonids. We collected anal, buccal, and mucus swabs (non-lethal qPCR) and kidney tissue samples (lethal DFAT) from 72 adult brook trout ( Salvelinus fontinalis ) reared at the Colorado Parks and Wildlife Pitkin Brood Unit and tested each sample to assess R. salmoninarum infections. Standard kidney tissue detected R. salmoninarum 1.59 times more often than mucus swabs, compared to 10.43 and 13.16 times more often than buccal or anal swabs, respectively, indicating mucus swabs were the most effective and may be a useful non-lethal method. Our study highlights the potential of non-lethal mucus swabs to sample for R. salmoninarum and suggests future studies are needed to refine this technique for use in aquaculture facilities and wild populations of inland salmonids.

Pathogens

Factors affecting post-challenge survival of Flavobacterium psychrophilum in susceptible rainbow trout from the literature

Infectious bacterial pathogens are a concern for aquaculture as estimates suggest that billions of US dollars are lost annually in aquaculture due to disease. One of the most prevalent salmonid pathogens is the bacterium Flavobacterium psychrophilum that causes bacterial coldwater disease. We reviewed the published F. psychrophilum literature and conducted a Bayesian analysis to examine large-scale patterns in rainbow trout ( Oncorhynchus mykiss ) mortality associated with laboratory challenge. We incorporated factors that were common across a majority of the laboratory exposure studies and these included bacterial dose, culture time, exposure method, bacterial isolate, experimental duration, and fish weight. The comparison showed that injection as the exposure method produced higher mortality than bath immersion, bacterial isolates differed in their effect on mortality, and bacterial dose has an interactive effect with fish weight and exposure method. Our comparison allows for inference on factors affecting rainbow trout mortality due to exposure to F. psychrophilum and suggests avenues to further optimize research protocols to better reach study goals.

Pathogens

Nocardia cyriacigeorgica in a Mallard (Anas platyrhynchos) from Arizona, USA

Nocardia spp. are opportunistic pathogens of humans, domestic animals, and wildlife that can cause high levels of morbidity and mortality. Here, we present a unique case of nocardial airsacculitis in a free-ranging mallard ( Anas platyrhynchos ) from Arizona, USA, and compare it to the hosts, geographic distribution, diagnostic methodology, and infection site of known nocardiosis cases in birds. A gross necropsy, histopathology, and bacterial culture were performed. There were no gross findings associated with the nocardiosis. Histopathology showed multiple granulomas expanding the air sac with intralesional filamentous bacteria that were Grocott’s methenamine silver-positive, Fite–Faraco and Ziehl–Neelsen acid-fast, positive with the Periodic acid–Schiff reaction, and variably Gram-positive. The organism was isolated in culture and identified as Nocardia cyriacigeorgica based on the sequencing of a 463 bp portion of the 16S rRNA gene. While reports of nocardiosis in the class Aves are rare and some are possibly misdiagnosed due to limited diagnostics, cases are reported globally, sometimes resulting in epizootics. More information is needed to understand whether immunosuppression plays a role in disease development in birds. Known to be an emerging pathogen in humans, N. cyriacigeorgica can be considered as a differential diagnosis for pulmonary and potentially cutaneous or disseminated infections in birds.

Arizona

Animal migration and risk of spread of viral infections

The potential contribution of migration towards the spread of disease is as varied as the ecology of the pathogens themselves and their host populations. This chapter outlines multiple examples of viral diseases in animal populations and their mechanisms of viral spread. Many species of insects, mammals, fish, and birds exhibit migratory behavior and have the potential to disperse diseases over long distances. The majority of studies available on viral zoonoses have focused on birds and bats, due to their highly migratory life histories. A number of studies have reported evidence of changes in the timing of animal migrations in response to climate change. The majority indicate an advancement of spring migration, with few or inconclusive results for fall migration. Predicting the combined effects of climate change on migratory patterns of host species and epidemiology of viral pathogens is complex and not fully realistic.

Book chapter

Survival of whirling disease resistant rainbow trout fry in the wild: A comparison of two strains

Introduced pathogens can affect fish populations, and three main factors affect disease occurrence: the environment, host, and pathogen. Manipulating at least one of these factors is necessary for controlling disease. Myxobolus cerebralis , the parasite responsible for salmonid whirling disease, became established in Colorado during the 1990s and caused significant declines in wild Rainbow Trout Oncorhynchus mykiss populations. Attempts to re-establish Rainbow Trout have focused on manipulating salmonid host resistance. A Rainbow Trout strain known as GR × CRR was developed for stocking in Colorado by crossing a whirling-disease-resistant strain known as the German Rainbow Trout (GR) with the Colorado River Rainbow Trout (CRR). The GR × CRR fish exhibit resistance similar to that shown by GR, and survival and reproduction were expected to be similar to those of CRR. One disadvantage of stocking GR × CRR is that outcrossing and backcrossing could decrease resistance, and laboratory studies have indicated that this can occur. A potential disadvantage of stocking pure GR is lower survival due to domestication. To compare fry survival between the strains, a field experiment was conducted in 1.6-km reaches of nine Colorado streams. Each stream was stocked in August 2014 with 5,000 GR × CRR and 5,000 GR individuals. In October 2014, April 2015, and August 2015, apparent survival was assessed. Two laboratory predation experiments were also conducted. The field experiment revealed that short-term apparent survival was influenced by stream, and growth rate was influenced by strain and stream. However, after 12 months, there was no difference in apparent survival or growth rate between the GR and GR × CRR strains. Laboratory experiments showed that survival did not differ between the strains when confronted with Brown Trout Salmo trutta predation. Our results indicate that the GR strain is a viable option for stocking in streams where M. cerebralis is enzootic. Further evaluation is needed to determine whether GR fish will survive to maturity and reproduce.

Journal of Aquatic Animal Health

Evaluation of Francisella orientalis ΔpdpA as a live attenuated vaccine against piscine Francisellosis in Nile tilapia

Francisella orientalis is an important bacterial pathogen of marine and freshwater fish with worldwide distribution. Fish francisellosis is a severe subacute to chronic granulomatous disease, with high mortalities and high infectivity rates in cultured and wild fish. To date, there is no approved vaccine for this disease. In this study, we evaluated the efficacy of a defined F. orientalis pathogenicity determinant protein A ( pdpA ) mutant (Δ pdpA ) as a live attenuated immersion vaccine against subsequent immersion challenge with the wild-type organism. Immunized Nile tilapia Oreochromis niloticus were protected (45% relative percent survival) from the lethal challenges and presented significantly lower mortality than nonvaccinated and challenged treatments. Although serum IgM was significantly higher in immunized fish, similar bacterial loads were detected in vaccinated and nonvaccinated survivors. In conclusion, although the F. orientalis Δ pdpA is attenuated and effectively stimulated an adaptive immune response, the low relative percent survival and high bacterial persistence in survivors of immunized and challenged treatments indicates low suitability of Δ pdpA as a mucosal vaccine for tilapia under conditions used in this study.

Journal of Aquatic Animal Health

Susceptibility of Pallid Sturgeon to viral hemorrhagic septicemia virus genotype IVb

Objective Viral hemorrhagic septicemia virus (VHSV) is an aquatic rhabdovirus causing severe disease in freshwater and saltwater fish species. The susceptibility of endangered Pallid Sturgeon Scaphirhynchus albus to VHSV genotype IVb (VHSV-IVb) infection was investigated. Methods An in vitro assessment using two Pallid Sturgeon cell lines derived from skin and spleen tissue and in vivo evaluation of juvenile Pallid Sturgeon after exposure to VHSV-IVb were performed. Result Plaque assay and RT-PCR results confirmed VHSV-IVb replication in Pallid Sturgeon cell lines. Sturgeon were also susceptible to VHSV-IVb infection after immersion and injection exposures during laboratory experiments. However, after widespread mortality occurred in all treatment groups, including negative control fish, it was determined that the Pallid Sturgeon stock fish were infected with Missouri River sturgeon iridovirus (MRSIV) prior to experimental challenge. Nevertheless, mortalities were equal or higher among VHSV-exposed fish than among negative controls (MRSIV infected), and histopathological assessments indicated reduced hematopoietic cells in spleen and kidney tissues and hemorrhage in the gastrointestinal organs only in fish from the VHSV treatment. Conclusion These results indicate that Pallid Sturgeon is a susceptible host for VHSV-IVb, but the degree of pathogenicity was confounded by the underlying MRSIV infection. Research comparing susceptibility of specific pathogen-free and MRSIV-infected fish to VHSV-IVb is needed to accurately assess the vulnerability of Pallid Sturgeon to VHSV-IVb.

Journal of Aquatic Animal Health

A pesticide paradox: Fungicides indirectly increase fungal infections

There are many examples where the use of chemicals have had profound unintended consequences, such as fertilizers reducing crop yields (paradox of enrichment) and insecticides increasing insect pests (by reducing natural biocontrol). Recently, the application of agrochemicals, such as agricultural disinfectants and fungicides, has been explored as an approach to curb the pathogenic fungus, Batrachochytrium dendrobatidis ( Bd ), which is associated with worldwide amphibian declines. However, the long-term, net effects of early-life exposure to these chemicals on amphibian disease risk have not been thoroughly investigated. Using a combination of laboratory experiments and analysis of data from the literature, we explored the effects of fungicide exposure on Bd infections in two frog species. Extremely low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture. However, estimated environmental concentrations of the fungicides did not reduce Bd on Cuban tree frog ( Osteopilus septentrionalis ) tadpoles exposed simultaneously to any of these fungicides and Bd , and fungicide exposure actually increased Bd -induced mortality. Additionally, exposure to any of these fungicides as tadpoles resulted in higher Bd abundance and greater Bd -induced mortality when challenged with Bd post-metamorphosis, an average of 71 d after their last fungicide exposure. Analysis of data from the literature revealed that previous exposure to the fungicide itraconazole, which is commonly used to clear Bd infections, made the critically endangered booroolong frog ( Litoria booroolongensis ) more susceptible to Bd . Finally, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. Although fungicides show promise for controlling Bd , these results suggest that, if fungicides do not completely eliminate Bd or if Bd recolonizes, exposure to fungicides has the potential to do more harm than good. To ensure that fungicide applications have the intended consequence of curbing amphibian declines, researchers must identify which fungicides do not compromise the pathogen resistance mechanisms of amphibians.

Ecological Applications

Waterfowl show spatiotemporal trends in influenza A H5 and H7 infections but limited taxonomic variation

Influenza A viruses in wild birds pose threats to the poultry industry, wild birds, and human health under certain conditions. Of particular importance are wild waterfowl, which are the primary reservoir of low pathogenicity influenza viruses that ultimately cause high pathogenicity outbreaks in poultry farms. Despite much work on the drivers of influenza A virus prevalence, the underlying viral subtype dynamics are still mostly unexplored. Nevertheless, understanding these dynamics, particularly for the agriculturally significant H5 and H7 subtypes, is important for mitigating the risk of outbreaks in domestic poultry farms. Here, using an expansive surveillance database, we take a large-scale look at the spatial, temporal, and taxonomic drivers in the prevalence of these two subtypes among influenza A positive wild waterfowl. We document spatiotemporal trends that are consistent with past work, particularly an uptick in H5 viruses in late autumn and H7 viruses in spring. Interestingly, despite large species differences in temporal trends in overall influenza A virus prevalence, we document only modest differences in the relative abundance of these two subtypes and little, if any, temporal differences among species. As such, it appears that differences in species' phenology, physiology, and behaviors that influence overall susceptibility to influenza A viruses play a much lesser role in relative susceptibility to different subtypes. Instead, species likely freely pass viruses among each other regardless of subtype. Importantly, despite the similarities among species documented here, individual species still may play important roles in moving viruses across large geographic areas or sustaining local outbreaks through their different migratory behaviors.

Ecological Applications

Growth, drought response, and climate-associated genomic structure in whitebark pine in the Sierra Nevada of California

Whitebark pine ( Pinus albicaulis Engelm.) has experienced rapid population declines and is listed as threatened under the Endangered Species Act in the United States. Whitebark pine in the Sierra Nevada of California represents the southernmost end of the species' distribution and, like other portions of its range, faces threats from an introduced pathogen, native bark beetles, and a rapidly warming climate. Beyond these chronic stressors, there is also concern about how this species will respond to acute stressors, such as drought. We present patterns of stem growth from 766 large (average diameter at breast height >25 cm), disease-free whitebark pine across the Sierra Nevada before and during a recent period of drought. We contextualize growth patterns using population genomic diversity and structure from a subset of 327 trees. Sampled whitebark pine generally had positive to neutral stem growth trends from 1970 to 2011, which was positively correlated with minimum temperature and precipitation. Indices of stem growth during drought years (2012 to 2015) relative to a predrought interval were mostly positive to neutral at our sampled sites. Individual tree growth response phenotypes appeared to be linked to genotypic variation in climate-associated loci, suggesting that some genotypes can take better advantage of local climatic conditions than others. We speculate that reduced snowpack during the 2012 to 2015 drought years may have lengthened the growing season while retaining sufficient moisture to maintain growth at most study sites. Growth responses may differ under future warming, however, particularly if drought severity increases and modifies interactions with pests and pathogens.

California, Nevada

Root endophytes and invasiveness: no difference between native and non‐native Phragmites in the Great Lakes Region

Microbial interactions could play an important role in plant invasions. If invasive plants associate with relatively more mutualists or fewer pathogens than their native counterparts, then microbial communities could foster plant invasiveness. Studies examining the effects of microbes on invasive plants commonly focus on a single microbial group (e.g., bacteria) or measure only plant response to microbes, not documenting the specific taxa associating with invaders. We surveyed root microbial communities associated with co‐occurring native and non‐native lineages of Phragmites australis, across Michigan, USA. Our aim was to determine whether (1) plant lineage was a stronger predictor of root microbial community composition than environmental variables and (2) the non‐native lineage associated with more mutualistic and/or fewer pathogenic microbes than the native lineage. We used microscopy and culture‐independent molecular methods to examine fungal colonization rate and community composition in three major microbial groups (bacteria, fungi, and oomycetes) within roots. We also used microbial functional databases to assess putative functions of the observed microbial taxa. While fungal colonization of roots was significantly higher in non‐native Phragmites than the native lineage, we found no differences in root microbial community composition or potential function between the two Phragmites lineages. Community composition did differ significantly by site, with soil saturation playing a significant role in structuring communities in all three microbial groups. The relative abundance of some specific bacterial taxa did differ between Phragmites lineages at the phylum and genus level (e.g., Proteobacteria, Firmicutes ). Purported function of root fungi and respiratory mode of root bacteria also did not differ between native and non‐native Phragmites . We found no evidence that native and non‐native Phragmites harbored distinct root microbial communities; nor did those communities differ functionally. Therefore, if the trends revealed at our sites are widespread, it is unlikely that total root microbial communities are driving invasion by non‐native Phragmites plants.

Ecosphere

Western bumble bee: Declines in United States and range-wide information gaps

In recent decades, many bumble bee species have declined due to changes in habitat, climate, and pressures from pathogens, pesticides, and introduced species. The western bumble bee ( Bombus occidentalis ), once common throughout western North America, is a species of concern and will be considered for listing by the U.S. Fish and Wildlife Service (USFWS) under the Endangered Species Act (ESA). We attempt to improve alignment of data collection and research with USFWS needs to consider redundancy, resiliency, and representation in the upcoming species status assessment. We reviewed existing data and literature on B. occidentalis , highlighting information gaps and priority topics for research. Priorities include increased knowledge of trends, basic information on several life‐history stages, and improved understanding of the relative and interacting effects of stressors on population trends, especially the effects of pathogens, pesticides, climate change, and habitat loss. An understanding of how and where geographic range extent has changed for the two subspecies of B. occidentalis is also needed. We outline data that could be easily collected in other research projects that would increase their utility for understanding range‐wide trends of bumble bees. We modeled the overall trend in occupancy from 1998 to 2018 of Bombus occidentalis within the continental United States using existing data. The probability of local occupancy declined by 93% over 21 yr from 0.81 (95% CRI = 0.43, 0.98) in 1998 to 0.06 (95% CRI = 0.02, 0.16) in 2018. The decline in occupancy varied spatially by landcover and other environmental factors. Detection rates vary in both space and time, but peak detection across the continental United States occurs in mid‐July. We found considerable spatial gaps in recent sampling, with limited sampling in many regions, including most of Alaska, northwestern Canada, and the southwestern United States. We therefore propose a sampling design to address these gaps to best inform the ESA species status assessment through improved assessment of how the spatial distribution of stressors influences occupancy changes. Finally, we request involvement via data sharing, participation in occupancy sampling with repeated visits to distributed survey sites, and complementary research to address priorities outlined in this paper.

Ecosphere

Compounding effects of white pine blister rust, mountain pine beetle, and fire threaten four white pine species

Invasive pathogens and bark beetles have caused precipitous declines of various tree species around the globe. Here, we characterized long‐term patterns of mountain pine beetle ( Dendroctonus ponderosae ; MPB) attacks and white pine blister rust, an infectious tree disease caused by the pathogen, Cronartium ribicola . We focused on four dominant white pine host species in Sequoia and Kings Canyon National Parks (SEKI), including sugar pine ( Pinus lambertiana ), western white pine ( P. monticola ), whitebark pine ( P. albicaulis ), and foxtail pine ( P. balfouriana ). Between 2013 and 2017, we resurveyed 152 long‐term monitoring plots that were first surveyed and established between 1995 and 1999. Overall extent (plots with at least one infected tree) of white pine blister rust (blister rust) increased from 20% to 33%. However, the infection rate across all species decreased from 5.3% to 4.2%. Blister rust dynamics varied greatly by species, as infection rate decreased from 19.1% to 6.4% in sugar pine, but increased in western white pine from 3.0% to 8.7%. For the first time, blister rust was recorded in whitebark pine, but not foxtail pine plots. MPB attacks were highest in sugar pines and decreased in the higher elevation white pine species, whitebark and foxtail pine. Both blister rust and MPB were important factors associated with elevated mortality in sugar pines. We did not, however, find a relationship between previous fires and blister rust occurrence. In addition, multiple mortality agents, including blister rust, fire, and MPB, contributed to major declines in sugar pine and western white pine; recruitment rates were much lower than mortality rates for both species. Our results highlighted that sugar pine has been declining much faster in SEKI than previously documented. If blister rust and MPB trends persist, western white pine may follow similar patterns of decline in the future. Given current spread patterns, blister rust will likely continue to increase in higher elevations, threatening subalpine white pines in the southern Sierra Nevada. More frequent long‐term monitoring efforts could inform ongoing restoration and policy focused on threats to these highly valuable and diverse white pines.

California

Why do trees die? Characterizing the drivers of background tree mortality

The drivers of background tree mortality rates—the typical low rates of tree mortality found in forests in the absence of acute stresses like drought—are central to our understanding of forest dynamics, the effects of ongoing environmental changes on forests, and the causes and consequences of geographical gradients in the nature and strength of biotic interactions. To shed light on factors contributing to background tree mortality, we analyzed detailed pathological data from 200,668 tree-years of observation and 3,729 individual tree deaths, recorded over a 13-yr period in a network of old-growth forest plots in California's Sierra Nevada mountain range. We found that: (1) Biotic mortality factors (mostly insects and pathogens) dominated (58%), particularly in larger trees (86%). Bark beetles were the most prevalent (40%), even though there were no outbreaks during the study period; in contrast, the contribution of defoliators was negligible. (2) Relative occurrences of broad classes of mortality factors (biotic, 58%; suppression, 51%; and mechanical, 25%) are similar among tree taxa, but may vary with tree size and growth rate. (3) We found little evidence of distinct groups of mortality factors that predictably occur together on trees. Our results have at least three sets of implications. First, rather than being driven by abiotic factors such as lightning or windstorms, the “ambient” or “random” background mortality that many forest models presume to be independent of tree growth rate is instead dominated by biotic agents of tree mortality, with potentially critical implications for forecasting future mortality. Mechanistic models of background mortality, even for healthy, rapidly growing trees, must therefore include the insects and pathogens that kill trees. Second, the biotic agents of tree mortality, instead of occurring in a few predictable combinations, may generally act opportunistically and with a relatively large degree of independence from one another. Finally, beyond the current emphasis on folivory and leaf defenses, studies of broad-scale gradients in the nature and strength of biotic interactions should also include biotic attacks on, and defenses of, tree stems and roots.

Ecology

Disease introduction is associated with a phase transition in bighorn sheep demographics

Ecological theory suggests that pathogens are capable of regulating or limiting host population dynamics, and this relationship has been empirically established in several settings. However, although studies of childhood diseases were integral to the development of disease ecology, few studies show population limitation by a disease affecting juveniles. Here, we present empirical evidence that disease in lambs constrains population growth in bighorn sheep ( Ovis canadensis ) based on 45 years of population-level and 18 years of individual-level monitoring across 12 populations. While populations generally increased (λ = 1.11) prior to disease introduction, most of these same populations experienced an abrupt change in trajectory at the time of disease invasion, usually followed by stagnant-to-declining growth rates (λ = 0.98) over the next 20 years. Disease-induced juvenile mortality imposed strong constraints on population growth that were not observed prior to disease introduction, even as adult survival returned to pre-invasion levels. Simulations suggested that models including persistent disease-induced mortality in juveniles qualitatively matched observed population trajectories, whereas models that only incorporated all-age disease events did not. We use these results to argue that pathogen persistence may pose a lasting, but under-recognized, threat to host populations, particularly in cases where clinical disease manifests primarily in juveniles.

Ecology