Pieter Johnson

• PhD
• Professor (Associate) at University of Colorado Boulder

Trematodes in the genus Clinostomum develop into large metacercariae that can sometimes achieve high intensity in their second intermediate hosts, potentially causing pathology. Here, we characterize a morbidity event in tiger salamanders (Ambystoma tigrinum) from a freshwater pond in Boulder, Colorado, USA, linked to extreme clinostomid infection....

Most hosts contain few parasites, whereas few hosts contain many. This pattern, known as aggregation, is well-documented in macroparasites where parasite intensity distribution among hosts affects host–parasite dynamics. Infection intensity also drives fungal disease dynamics, but we lack a basic understanding of host–fungal aggregation patterns, h...

Despite evidence that certain diseases of marine wildlife are increasing, long-term infection data are often lacking. Archived samples of hosts from natural history collections offer a powerful tool for evaluating temporal changes in parasitism. Using vouchered fish collections from the Southern Caribbean, we investigated long-term (1905–2022) shif...

Batrachochytrium dendrobatidis (Bd), an aquatic pathogenic fungus, is responsible for the decline of hundreds of amphibian species worldwide and negatively impacts biodiversity globally. Prophylactic exposure to the metabolites produced by Bd can provide protection for naïve tree frogs and reduce subsequent Bd infection intensity. Here, we used a r...

The detection of severe limb malformations in metamorphosing northern leopard frogs (Rana pipiens) from a Colorado pond in August 2022 prompted questions about the cause(s) and concern over the implications. Northern leopard frogs, which are a Tier 1 Species of Greatest Conservation Need in Colorado, have declined over much of their range in the st...

Members of the genus Scaphanocephalus mature in accipitrids, particularly osprey, Pandion haliaetus, with metacercaria causing Black Spot Syndrome in reef fishes. In most of the world, only the type species, Scaphanocephalus expansus (Creplin, 1842) has been reported. Recent molecular studies in the Western Atlantic, Mediterranean and Persian Gulf...

The naïve host syndrome hypothesis suggests that pathogens are able to easily invade and become deadly to novel hosts because of a lack of co‐evolutionary history, whereas the local adaptation hypothesis suggests that pathogens are better able to invade local hosts because of their co‐evolutionary history, but rarely do studies on these two hypothe...

Landscapes of fear can determine the dynamics of entire ecosystems. In response to perceived predation risk, prey can show physiological, behavioral, or morphological trait changes to avoid predation. This in turn can indirectly affect other species by modifying species interactions (e.g., altered feeding), with knock-on effects, such as trophic ca...

Landscapes of fear can determine the dynamics of entire ecosystems. In response to perceived predation risk, prey can show physiological, behavioral, or morphological trait changes to avoid predation. This in turn can indirectly affect other species by modifying species interactions (e.g., altered feeding), with knock‐on effects, such as trophic ca...

Parasites represent a critically understudied component of reef communities—a knowledge gap that has become more evident as infectious diseases emerge. Here, we test the roles of competing ecological and evolutionary factors in driving infections by an emerging infectious phenomenon: Black spot syndrome (BSS) in Caribbean reef fishes. BSS, a condit...

Despite the importance of virulence in epidemiological theory, the relative contributions of host and parasite to virulence outcomes remain poorly understood. Here, we use reciprocal cross experiments to disentangle the influence of host and parasite on core virulence components—infection and pathology—and understand dramatic differences in parasit...

The location of parasites within individual hosts is often treated as a static trait, yet many parasite species can occur in multiple locations or organs within their hosts. Here, we apply distributional heat maps to study the within- and between-host infection patterns for four trematodes ( Alaria marcianae, Cephalogonimus americanus, Echinostoma...

Losses in biodiversity can alter disease risk through changes in host species composition. Host species vary in pathogen susceptibility and competence, yet how changes in diversity alter host–pathogen dynamics remains unclear in many systems, particularly with respect to generalist pathogens. Amphibians are experiencing worldwide population decline...

Understanding parasite transmission in communities requires knowledge of each species' capacity to support transmission. This property, ‘competence’, is a critical currency for modelling transmission under community change and for testing diversity–disease theory. Despite the central role of competence in disease ecology, we lack a clear understand...

The need for efficient, accurate biodiversity monitoring is growing, especially for globally imperiled taxa, such as amphibians. Environmental DNA (eDNA) analysis holds enormous potential for enhancing monitoring programs, but as this tool is increasingly adopted, it is imperative for users to understand its potential benefits and shortcomings. We...

The increasing frequency and severity of drought may exacerbate ongoing global amphibian declines. However, interactions between drought and coincident stressors, coupled with high interannual variability in amphibian abundances, can mask the extent and underlying mechanisms of drought impacts. We synthesized a decade (2009–2019) of regional-scale...

Predation on parasites is a common interaction with multiple, concurrent outcomes. Free‐living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While...

Parasites are important players in ecological communities that can shape community structure and influence ecosystem energy flow. Yet beyond their effects on hosts, parasites can also function as an important prey resource for predators. Predators that consume infectious stages in the environment can benefit from a nutrient-rich prey item while con...

Ecosystems across the United States are changing in complex and surprising ways. Ongoing demand for critical ecosystem services requires an understanding of the populations and communities in these ecosystems in the future. This paper represents a synthesis effort of the U.S. National Science Foundation‐funded Long‐Term Ecological Research (LTER) n...

Abstract Despite long‐term analyses of lake ice phenology globally, comparatively little is known about high‐elevation lakes, for which climate shifts are thought to be occurring faster than at lower elevations. Using a 36‐yr dataset (1983–2018) on alpine lakes (> 3000 m ASL) from the Green Lakes Valley, Colorado (GLV), we found that ice‐cover dura...

The prolonged ice cover inherent to alpine lakes incurs unique challenges for aquatic life, which are compounded by recent shifts in the timing and duration of ice cover. To understand the responses of alpine zooplankton, we analyzed a decade (2009–2019) of open-water samples of Daphnia pulicaria and Hesperodiaptomus shoshone for growth, reproducti...

Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifying β‐diversity across scales and over time additionally offers m...

Free-living parasite infectious stages, such as motile cercariae of trematodes (flatworms), can constitute substantial biomass within aquatic ecosystems and are frequently eaten by various consumers, potentially serving as an important source of nutrients and energy. However, quantitative data on their nutritional value (e.g., essential fatty acids...

A key challenge surrounding ongoing climate shifts is to identify how they alter species interactions, including those between hosts and parasites. Because transmission often occurs during critical time windows, shifts in the phenology of either taxa can alter the likelihood of interaction or the resulting pathology. We quantified how phenological...

Two widespread drivers of change in high-elevation lakes are climate warming and atmospheric nitrogen deposition, which may have interactive effects on aquatic ecosystems. Using an outdoor mesocosm experiment at 2900 m above-sea level along the Colorado Front Range, we investigated the individual and combined effects of realistic increases in tempe...

Recently, observations of black spot syndrome (BSS) in Caribbean fishes have been linked to infection by a digenean trematode parasite, Scaphanocephalus expansus. Recently, This study examined the distribution of BSS over multiple spatial and temporal scales: at the island scale in Bonaire, Dutch Caribbean, using field surveys of 4885 fish belongin...

Despite the evidence that diseases have increased in marine taxa, parasites remain underrepresented in studies of marine ecology. Recently, observations of black-spot syndrome (BSS) in Caribbean fishes, especially ocean surgeonfishes, Acanthurus tractus (Poey, 1860), have been reported, although its cause(s) has remained conjectural. We investigate...

Debates over the relationship between biodiversity and disease dynamics underscore the need for a more mechanistic understanding of how changes in host community composition influence parasite transmission. Focusing on interactions between larval amphibians and trematode parasites, we experimentally contrasted the effects of host richness and speci...

Ongoing debate over the relationship between biodiversity and disease risk underscores the need to develop a more mechanistic understanding of how changes in host community composition influence parasite transmission, particularly in complex communities with multiple hosts. A key challenge involves determining how motile parasites select among pote...

In nature, multiple waves of exposure to the same parasite are likely, making it important to understand how initial exposure or infection affects subsequent host infections, including the underlying physiological pathways involved. We tested whether experimental exposure to trematodes (Echinostoma trivolvis or Ribeiroia ondatrae) affected the stre...

Promoting health equity is a fundamental public health objective, yet health disparities remain largely overlooked in studies of vectorborne diseases, especially those transmitted by ticks. We sought to identify health disparities associated with Lyme disease and human monocytic ehrlichiosis, two of the most pervasive tickborne diseases within the...

Results of county-level post hoc analyses using general linear mixed modeling to quantify associations between the incidence of Lyme disease and human monocytic ehrlichiosis with four housing vacancy type variables. For each disease, results of the non-reduced multivariable model including all four housing vacancy type variables together are shown....

Results of county-level subset analyses using general linear mixed modeling to quantify associations between the incidence of Lyme disease (LD) and human monocytic ehrlichiosis (HME) with six racial/ethnic and socioeconomic variables (socioeconomic variables) and two ecological variables. For each disease, subset analyses were limited to the subset...

Results of county-level analyses using general linear mixed modeling to quantify associations between the incidence of Lyme disease with six racial/ethnic and socioeconomic variables (socioeconomic variables) and two ecological variables. Results of univariable models (each socioeconomic variable individually), the final (reduced) multivariable mod...

Results of county-level analyses using general linear mixed modeling to quantify associations between the incidence of human monocytic ehrlichiosis with six racial/ethnic and socioeconomic variables (socioeconomic variables) and two ecological variables. Results of univariable models (each socioeconomic variable individually), the final (reduced) m...

Results of county-level subset analyses using general linear mixed modeling to quantify associations between the incidence of human monocytic ehrlichiosis with six racial/ethnic and socioeconomic variables (socioeconomic variables) and two ecological variables. Subset analyses were limited to the subset of the 2,695 counties included in the full an...

Microsoft Excel file containing all raw data used in the analyses. (XLSX)

Map of the boundaries of geographic regions used in the analyses and based on the standard federal regions established by the United States Office of Management and Budget. Upper Northeast and Lower Northeast standard federal regions (regions I and II, respectively) are combined into the Northeast geographic region; Central Mountain and Upper Midwe...

Summary information for variables included in the analyses. Qualitative summary information includes variable type, name, definition and data source(s). Quantitative summary information includes the county-level mean (±95% confidence interval), median, and range of values for each variable among the 2,695 counties included in primary and secondary...

Results of county-level analyses using general linear mixed modeling to quantify associations between disease (Lyme disease, human monocytic ehrlichiosis), six racial/ethnic and socioeconomic variables (socioeconomic variables), and their interaction in predicting disease incidence. HME was used as the reference category. Incidence was modeled usin...

Results of county-level subset analyses using general linear mixed modeling to quantify associations between the incidence of Lyme disease with six racial/ethnic and socioeconomic variables (socioeconomic variables) and two ecological variables. Subset analyses were limited to the subset of the 2,695 counties included in the full analyses in which...

• Identifying ecological niche filters that shape species community composition is a critical first step in understanding the relative contributions of deterministic and stochastic processes in structuring communities. Systems with harsh ecological filters often have a more deterministic basis to community structure. Although these filters are ofte...

Species invasions increasingly occur alongside other forms of ecosystem change, highlighting the need to understand how invasion outcomes are influenced by environmental factors. Within freshwaters, two of the most widespread drivers of change are introduced fishes and nutrient loading, yet it remains difficult to predict how interactions between t...

Classical research on animal toxicity has focused on the role of toxins in protection against predators, but recent studies suggest these same compounds can offer a powerful defense against parasites and infectious diseases. Newts in the genus Taricha are brightly coloured and contain the potent neurotoxin, tetrodotoxin ( TTX ), which is hypothesiz...

Abstract: Freshwater environments are threatened by nonnative species introductions, often involving fishes. Parasites and pathogens introduced with fishes have the potential to infect native taxa and should be investigated. We examined 726 fishes representing 6 invasive species from 27 ponds in California to evaluate how parasite richness, infecti...

Circadian rhythms of parasites and their hosts can influence processes such as transmission, pathology and life cycle evolution. For trematode parasites that depend on free-living infectious stages (i.e. cercariae) to move among host species, the timing of parasite release is hypothesized to increase the likelihood of contacting a host. Yet, a pers...

Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of transmission remain rare, and those experiments that are conducted are often not designed to test the full range of possible forms. To differentiate among 10 candidate transmission functions, w...

Widespread observations of malformed amphibians across North America have generated both concern and controversy. Debates over the causes of such malformations—which can affect >50% of animals in a population—have continued, likely due to involvement of multiple causal factors. Here, we used a 13-year dataset encompassing 53,880 frogs and toads fro...

Almost all macroparasites show over-dispersed infections within natural host populations such that most parasites are distributed among a few heavily-infected individuals. Despite the importance of parasite aggregation for understanding system stability, the potential for population regulation, and super-spreading events, many questions persist abo...

• The ecological consequences of species invasions can vary in time and space, complicating efforts to generalise invader impacts across ecosystems. This challenge is particularly relevant when using small‐scale experiments to derive predictions for freshwater ecosystems. In this study, our aims were to document the effects of a controlled fish int...

Symbiont occurrence is influenced by host occurrence and vice versa, which leads to correlations in host-symbiont distributions at multiple levels. Interactions between co-infecting symbionts within host individuals can cause correlations in the abundance of two symbiont species across individual hosts. Similarly, interactions between symbiont tran...

This supplement includes all code and data required to replicate our analysis. The analysis.R file will read and process the data from host_data.csv and parasite_data.csv, compile the Stan model (mod.stan), then estimate the parameters and recreate the figures. (ZIP)

Growing evidence indicates that parasites—when considered—can play influential roles in ecosystem structure and function, highlighting the need to integrate disease ecology and ecosystem science. To strengthen links between these traditionally disparate fields, we identified mechanisms through which parasites can affect ecosystems and used empirica...

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune inve...

Many fields in the biological sciences have witnessed a shift away from organism- or taxon-focused research and teaching in favor of more conceptual and process-driven paradigms. The field of parasitology is no exception, despite the diversity of topics and taxa it encompasses. Concurrently, however, interest in disease ecology has increased dramat...

Despite a century of research into the factors that generate and maintain biodiversity, we know remarkably little about the drivers of parasite diversity. To identify the mechanisms governing parasite diversity, we combined surveys of 8100 amphibian hosts with an outdoor experiment that tested theory developed for free-living species. Our analyses...

High-elevation aquatic ecosystems are highly vulnerable to climate change, yet relatively few records are available to characterize shifts in ecosystem structure or their underlying mechanisms. Using a long-term data set on seven alpine lakes (3126 to 3620m) in Colorado, USA, we show that ice-off dates have shifted 7days earlier over the past 33yea...

Global climate change is expected to alter patterns of temperature variability, which could influence species interactions including parasitism. Species interactions can be difficult to predict in variable‐temperature environments because of thermal acclimation responses, i.e. physiological changes that allow organisms to adjust to a new temperatur...

Despite growing evidence that parasites often alter nutrient flows through their hosts and can comprise a substantial amount of biomass in many systems, whether endemic parasites influence ecosystem nutrient cycling, and which nutrient pathways may be important, remains conjectural. A framework to evaluate how endemic parasites alter nutrient cycli...

Antimicrobial peptides (AMPs) contribute to the immune defenses of many vertebrates, including amphibians. As larvae, amphibians are often exposed to the infectious stages of trematode parasites, many of which must penetrate the host's skin, potentially interacting with host AMPs. We tested the effects of the natural AMPs repertoires on both the su...

Understanding the drivers of species occurrence is a fundamental goal in basic and applied ecology. Occupancy models have emerged as a popular approach for inferring species occurrence because they account for problems associated with imperfect detection in field surveys. Current models, however, are limited because they assume covariates are indep...

The life history characteristics of hosts often influence patterns of parasite infection either by affecting the likelihood of parasite exposure or the probability of infection following exposure. In birds, migratory behavior has been suggested to affect both the composition and abundance of parasites within a host, although whether migratory birds...

Understanding the drivers of species occurrence is a fundamental goal in basic and applied ecology. Occupancy models have emerged as a popular approach for inferring species occurrence because they account for problems associated with imperfect detection in field surveys. Current models, however, are limited because they assume covariates are indep...

Infections by the digenetic trematode, Ribeiroia ondatrae , cause severe limb malformations in many North American amphibians. Ribeiroia ondatrae also infects fishes as second intermediate hosts, but less is known about the pathology and immune responses initiated in infected fish, even though reports of infected fish date back to early 1900s. To t...

Parasites have historically been considered a scourge, deserving of annihilation. Although parasite eradications rank among humanity's greatest achievements, new research is shedding light on the collateral effects of parasite loss. Here, we explore a "world without parasites": A thought experiment for illuminating the ecological roles that parasit...

Infectious diseases often emerge from interactions among multiple species and across nested levels of biological organization. Threats as diverse as Ebola virus, human malaria, and bat white-nose syndrome illustrate the need for a mechanistic understanding of the ecological interactions underlying emerging infections. We describe how recent advance...

Global losses of biodiversity have galvanised efforts to understand how changes to communities affect ecological processes, including transmission of infectious pathogens. Here, we review recent research on diversity-disease relationships and identify future priorities. Growing evidence from experimental, observational and modelling studies indicat...

Approaches based on organismal DNA found in the environment (eDNA) have become increasingly utilized for ecological studies and biodiversity inventories as an alternative to traditional field survey methods. Such DNA-based techniques have been largely used to establish the presence of free-living organisms, but have much potential for detecting and...

Preventing the arrival of invasive species is the most effective way of controlling their impact. Preventative strategies may be ‘offensive’ aimed at preventing the invader leaving colonised locations or ‘defensive’ aimed at preventing its arrival at uninvaded locations. The limited resources for invasive species control must be prioritized, partic...

Understanding the effects of predation on disease dynamics is increasingly important in light of the role ecological communities can play in host-parasite interactions. Surprisingly, however, few studies have characterized direct predation of parasites. Here we used an experimental approach to show that consumption of free-living parasite stages is...

Two of the most prominent frameworks to develop in ecology over the past decade are metacommunity ecology, which seeks to characterize multispecies distributions across space, and occupancy modeling, which corrects for imperfect detection in an effort to better understand species occurrence patterns Although their goals are complementary, metacommu...

Abstract Background: Commonplace biodiversity labs in introductory undergraduate biology typically emphasize declarative knowledge. We contend that shifting these labs to emphasize evolution, higher-order cognition, and science reasoning would benefit student learning. Four factors that likely make evolution-based higher-order learning goals diffic...

Changes in the magnitude and frequency of temperature shifts with climate change will influence species interactions if species have differential acclimation responses. For example, if parasites acclimate to temperature shifts faster than their hosts, as might be expected due to their smaller sizes and faster metabolisms, temperature variability co...

Background/Question/Methods Pattern-based metacommunity approaches use observed species incidence data to determine how a metacommunity is structured and subsequently to infer structuring processes. However, this type of community data suffers inherently from imperfect detection, and false absences could bias the methods used to assign metacommun...

Background/Question/Methods The effect of biodiversity loss on parasite transmission has caused heated controversy lately, partly due to confusion over how transmission rates and parasite diversity relate to disease risk. For instance, while empirical evidence suggests that host biodiversity can limit the transmission of multi-host parasites, evi...

Background/Question/Methods One of the most fundamental challenges facing contemporary disease ecology involves understanding host-parasite interactions within complex communities composed of multiple host species, coinfecting parasites, and a suite of non-host species. Although interest in applying ecological approaches to disease research has g...

Background/Question/Methods Parasites represent one of the most conspicuous gaps in our understanding of life’s diversity. This ignorance is a liability when considered in light of the increasingly important role that parasites play in human and wildlife health. Especially troubling are indications that anthropogenic biodiversity loss could incre...

Growing interest in unifying the field of natural enemy ecology has revealed similarities between predation and parasitism. In parallel with predation, parasite infection – and even the threat of infection – can alter host traits and indirectly affect community interactions. Nonetheless, few studies have considered multiple mechanisms of natural en...

Hydroperiod strongly influences the breeding period and development time of many amphibians, and larvae of various species display developmental plasticity in response to habitat drying. Hydrologic alterations associated with anthropogenic activities potentially can influence host–parasite interactions in humans and wildlife, but few investigators...

Despite the ubiquity of bilateral symmetry among animals, a long-standing mystery centers on why parasites that infect paired organs often do so non-randomly. Examples from diverse host and parasite taxa continue to accumulate, yet little is known about their causes or implications for host–parasite fitness. We combined field surveys, experimental...

Infection heterogeneity is one of the most fundamental patterns in disease ecology, yet surprisingly few studies have experimentally explored its underlying drivers. Here, we used large‐scale field assessments to evaluate the degree of parasite aggregation within amphibian host populations followed by a novel experimental approach to assess the pot...

Predators can directly and indirectly influence host–parasite interactions by consuming infected individuals, by removing infectious parasite stages and by changing host traits (e.g. behaviour). Because such effects can affect infection positively or negatively, understanding the net effects of predation on pathogen transmission under natural condi...

Multi-species experiments are critical for identifying the mechanisms through which climate change influences population dynamics and community interactions within ecological systems, including infectious diseases. Using a host-parasite system involving freshwater snails, amphibians and trematode parasites, we conducted a year-long, outdoor experim...

Most food webs use taxonomic or trophic species as building blocks, thereby collapsing variability in feeding linkages that occurs during the growth and development of individuals. This issue is particularly relevant to integrating parasites into food webs because parasites often undergo extreme ontogenetic niche shifts. Here, we used three version...

Amphibians with missing, misshapen, and extra limbs have garnered public and scientific attention for two decades, yet the extent of the phenomenon remains poorly understood. Despite progress in identifying the causes of abnormalities in some regions, a lack of knowledge about their broader spatial distribution and temporal dynamics has hindered ef...

Clarifying how species move across and utilize human-modified landscapes is key to the conservation of declining populations, as well as to the management and control of invasive species. The North American bullfrog (Lithobates catesbeianus) is a globally distributed invasive amphibian that has been implicated in the decline of native amphibians ac...

Significance Ongoing losses of biodiversity underscore the need to understand how species loss affects infectious diseases. Recognizing that most communities include multiple hosts and pathogens, we tested how variation in host and parasite diversity influenced disease risk. By combining field surveys and experiments involving amphibian hosts and t...

Background/Question/Methods Ribeiroia ondatrae, a trematode from the Psilostomatidae family, is one of the major contributors to amphibian malformations. Infection with Ribeiroia during limb development may result in the amphibian developing deformities such as multiple limbs, skin webbing, missing limbs and total suppression of limb development....