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Human density is associated with the increased prevalence of a generalist zoonotic parasite in mammalian wildlife

Authors:
  • Environment and Climate Change Canada

Abstract

Macroecological approaches can provide valuable insight into the epidemiology of globally distributed, multi-host pathogens. Toxoplasma gondii is a zoonotic protozoan that infects any warm-blooded animal, including humans, in almost every ecosystem worldwide. There is substantial geographical variation in T. gondii prevalence in wildlife populations and the mechanisms driving this variation are poorly understood. We implemented Bayesian phylogenetic mixed models to determine the association between species’ ecology, phylogeny and climatic and anthropogenic factors on T. gondii prevalence. Toxoplasma gondii prevalence data were compiled for free-ranging wild mammal species from 202 published studies, encompassing 45 079 individuals from 54 taxonomic families and 238 species.We found that T. gondii prevalence was positively associated with human population density and warmer temperatures at the sampling location. Terrestrial species had a lower overall prevalence, but there were no consistent patterns between trophic level and prevalence. The relationship between human density and T. gondii prevalence is probably mediated by higher domestic cat abundance and landscape degradation leading to increased environmental oocyst contamination. Landscape restoration and limiting freeroaming in domestic cats could synergistically increase the resiliency of wildlife populations and reduce wildlife and human infection risks from one of the world’s most common parasitic infections.
royalsocietypublishing.org/journal/rspb
Research
Cite this article: Wilson AG, Wilson S, Alavi
N, Lapen DR. 2021 Human density is
associated with the increased prevalence of a
generalist zoonotic parasite in mammalian
wildlife. Proc. R. Soc. B 288: 20211724.
https://doi.org/10.1098/rspb.2021.1724
Received: 31 July 2021
Accepted: 23 September 2021
Subject Category:
Global change and conservation
Subject Areas:
health and disease and epidemiology, ecology
Keywords:
wildlife disease, Toxoplasma gondii,
anthropogenic pressure, free-roaming cats,
one health
Author for correspondence:
Amy G. Wilson
e-mail: amy.wilson@ubc.ca
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.5662210.
Human density is associated with the
increased prevalence of a generalist
zoonotic parasite in mammalian wildlife
Amy G. Wilson
1,2
, Scott Wilson
1,3
, Niloofar Alavi
4
and David R. Lapen
5
1
Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, British Columbia,
Canada V6T 1Z4
2
Canadian Wildlife Health Cooperative, Abbotsford, British Columbia, Canada V3G 2M3
3
Environment and Climate Change Canada, Delta, British Columbia, Canada V4 K 3N2 0H3
4
Environment and Climate Change Canada, Ottawa, Ontario, Canada K1S 5B6
5
Ottawa Research Development Centre, Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada K1A 0C6
AGW, 0000-0003-2789-0480; SW, 0000-0002-1210-8727
Macroecological approaches can provide valuable insight into the epide-
miology of globally distributed, multi-host pathogens. Toxoplasma gondii is
a zoonotic protozoan that infects any warm-blooded animal, including
humans, in almost every ecosystem worldwide. There is substantial geo-
graphical variation in T. gondii prevalence in wildlife populations and the
mechanisms driving this variation are poorly understood. We implemented
Bayesian phylogenetic mixed models to determine the association between
speciesecology, phylogeny and climatic and anthropogenic factors on
T. gondii prevalence. Toxoplasma gondii prevalence data were compiled for
free-ranging wild mammal species from 202 published studies, encompass-
ing 45 079 individuals from 54 taxonomic families and 238 species. We found
that T. gondii prevalence was positively associated with human population
density and warmer temperatures at the sampling location. Terrestrial
species had a lower overall prevalence, but there were no consistent patterns
between trophic level and prevalence. The relationship between human
density and T. gondii prevalence is probably mediated by higher domestic
cat abundance and landscape degradation leading to increased environ-
mental oocyst contamination. Landscape restoration and limiting free-
roaming in domestic cats could synergistically increase the resiliency of
wildlife populations and reduce wildlife and human infection risks from
one of the worlds most common parasitic infections.
1. Background
Anthropogenic pressures can promote the emergence of novel pathogens or
worsen the disease burden of endemic pathogens [1,2]. Examples of anthropo-
genic mechanisms creating these conditions include altering host community
structure [1,3], reducing host health and immunity [4], disrupting ecosystem
services capable of regulating pathogen transmission [5] and introducing
invasive species and associated pathogens [6]. Human development and associ-
ated land-use changes can further amplify transmission risks by creating large,
high-density populations of domestic animals that transmit pathogens to
wildlife and humans across humandomestic animalwildlife interfaces [1].
Although wildlife populations have increased pathogen richness, it is domesti-
cated animals that have a more central role in sharing generalist pathogens with
both humans and wildlife, ranging from viruses [7] to helminths [8] and
ectoparasites [9]. Understanding how anthropogenic drivers influence the
epidemiology of generalist pathogens is essential because they are more likely
to be zoonotic, classified as emerging or reemerging diseases [10] and be of
conservation concern [11].
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Toxoplasma gondii is a model pathogen for examining how
anthropogenic factors influence disease risk in wildlife popu-
lations across a range of taxonomic and geographical
gradients. Toxoplasma gondii is a generalist protozoal parasite
that is thought to be able to infect any endothermic animal,
including humans, with a global human infection rate of 30
50% [12]. In addition to a broad host and geographical
range, T. gondii has other key epidemiological traits such as
using a domestic species as a definitive host, multiple trans-
mission routes and extended persistence within hosts and
the environment. Toxoplasma gondii infects hosts through
fecaloral exposure of a free-living, passively dispersed
oocyst or carnivory of tissue cysts.
Domestic cats and wild felids serve as the definitive hosts
in the domestic and wild cycles, respectively. Infected felids
episodically excrete millions of environmentally robust
oocysts in their faeces when they are exposed or re-exposed
to infected prey or are immunosuppressed [13,14]. These
oocysts can remain infectious for years in soil or water, pas-
sively dispersing through the soil matrix and contaminating
aquatic ecosystems via surface runoff [15]. Infection occurs
when animals or humans ingest oocysts in contaminated
water, food or inadvertent surface contact. Toxoplasma gondii
will permanently encyst within neurological and muscular
tissue of infected hosts, with these tissue cysts being
infectious to any carnivore that consumes that host. Trans-
mission between intermediate hosts is a trait unique to
T. gondii, enabling it to persist in the food chain, potentially
circumventing what could have been a dead-end host [16].
Toxoplasma gondii infections can be fatal for immuncom-
promised humans or animals [17]. Multiple wildlife taxa
are highly susceptible to T. gondii infections, such as marine
mammals, Australian marsupials and New World monkeys,
with reported mortalities in numerous endangered and ende-
mic species [17]. However, even for healthy or insensitive
hosts, latent T. gondii tissue cysts within host tissues can
cause subclinical effects for the hosts lifespan [17]. In
humans, latent toxoplasmosis has associations with mental
disorders (e.g. schizophrenia), epilepsy, autism, cognitive
and vision deficits, cancers, traffic accidents and increased
severity of other accompanying diseases [12].
Infected hosts can also have subtle behavioural changes
affecting survival, such as reduced vigilance or even an
attraction to felids, which for felid prey species would serve
to complete the sexual life cycle of the parasite. These behav-
ioural changes have been documented in species ranging
from rats [18] to chimpanzees [19]. Although poorly under-
stood, latent T. gondii infections in wildlife have been
associated with reduced population fitness through altered
fetal development [20] and increased mortality due to auto-
mobile collisions [21], cold weather [22] and concurrent
parasitic infections [23]. Given these acute and chronic
health impacts of T. gondii for such large numbers of individ-
uals, identifying specific environmental risk factors that are
amenable to mitigation, such as anthropogenic landscape
changes and domestic animal management, would benefit
public and wildlife health initiatives.
Due to the public and wildlife health burden of T. gondii,
considerable research has been directed towards measuring
prevalence in wildlife, with data now available for tens of
thousands of individuals from hundreds of wild animal
species worldwide. However, characterizing the probable dri-
vers of these prevalence patterns has received less attention.
Since T. gondii prevalence data have been collected across a
range of geographical gradients for diverse taxonomic
groups, it is possible to integrate information from across
studies to untangle specific climatic, anthropogenic, ecologi-
cal and phylogenetic correlations with T. gondii prevalence.
Moreover, the broad host range, coupled with global data
richness, enables a global perspective that is rarely possible
for other individual wildlife pathogens.
In this paper, we test three sets of hypotheses related to
the ecological, climatic and anthropogenic correlates of
T. gondii prevalence in mammalian wildlife. We first tested
the hypothesis that species-specific ecological traits related
to ecosystem and trophic level would lead to different
exposure rates to T. gondii through oocysts and tissue cysts.
Species living in aquatic ecosystems are expected to have
increased oocyst exposure risks due to the potential for sub-
stantial and localized oocyst influxes through runoff and
increased exposure area through suspension through the
water column. Aquatic avian wildlife has an increased preva-
lence of T. gondii relative to terrestrial species [24], and we
predicted this pattern would also be evident at a global
scale in mammals. Trophic level influences exposure risk
because carnivores of endothermic vertebrates will be
exposed to increased infection risks through the tissue-cyst
transmission route. Similarly, studies have reported a consist-
ent positive relationship between T. gondii prevalence and
trophic levels [24,25]; therefore, we predicted that prevalence
would be higher among carnivorous taxa.
Our second set of hypotheses considered climatic factors
since temperature and precipitation affect oocyst survival
and transport in the environment and domestic cat abun-
dance and free-roaming activity [26]. Extreme temperatures
can reduce oocyst survival [27], while heavy precipitation
facilitates oocyst transport in terrestrial and aquatic ecosys-
tems [28]. Therefore, we predicted a positive association
between T. gondii prevalence in mammals and the average
air temperature and precipitation at the locations where
they were surveyed.
Finally, our last and most important hypotheses examined
the relationship between T. gondii prevalence and anthropo-
genic factors. Mammals in more anthropized locations may
have a higher T. gondii prevalence because of land conversion
(e.g. impervious surfaces and losses of wetlands [5,29]) effects
on oocyst transport and survival and increased exposure to
higher densities of free-roaming domestic cats [30], which
are the most consequential definitive host species compared
to wild felids [28]. To measure the relationship between
T. gondii and prevalence in mammals in anthropogenic
environments, we selected three spatial layers (i) human den-
sity representing urbanization, (ii) crop coverage representing
agricultural environments and (iii) the human footprint index
(HFI) as a composite measure of multiple human pressures.
We predicted a positive relationship between T. gondii
prevalence and these three measures of human impact.
2. Methods
(a) Literature search
Our analyses focused on studies reporting on the prevalence of
T. gondii in free-ranging wild mammal populations. We searched
for studies using Web of Science Core Collection and PubMed
using search terms: wild*and toxoplasmosisor toxoplasma.
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We located additional studies from the reference lists of these
studies, citations of these works and comprehensive review
articles [17]. As we were interested in the geographical variables
at the sampling site, we only included studies that provided
specific location information or where the sampling locations
could be estimated within a 50 km distance. For our analyses,
we selected a 50 km threshold in order to reflect the average
precision of sampling information provided by authors and to
more realistically capture the geographical gradients experienced
by individuals.Of the 238 species in this study, a subset of 142
had species-specific home range estimates available [31]. The
home range estimates were much smaller than 50 km for 127 of
these species, with individuals from these taxa constituting
78% of the full dataset and 93% of the subset of taxa with esti-
mated home ranges (electronic supplementary material, table
S1).We excluded pelagic marine mammals due to their propen-
sity for long-distance movements, which introduces uncertainty
regarding the geographical characteristics of their likely exposure
location. We also excluded studies that reported only seroposi-
tive cases, provided only genus level identifiers or were from
captive or farmed wild animals. The complete list of included
studies is provided in electronic supplementary material, table
S2, and the study inclusion path is provided in electronic
supplementary material, figure S1.
From each study, we extracted data on the number of positive
and negative animals, the total number of individuals tested, the
species tested, method of detection (serology or isolation) and geo-
graphical information of the sampling location. For each species,
we then compiled species-specific ecological traits. To account
for ecological correlates of T. gondii prevalence in mammals, we
collected information on species ecosystem type (terrestrial or
aquatic) from the IUCN Red List [32]. The trophic level of a species
was based on the proportion of a speciess diet consisting of fruit,
nectar, seeds, invertebrates and vertebrate prey as provided in
EltonTraits 1.0 [33]. We reclassified these proportions into four cat-
egories: herbivores, invertivores, omnivores and carnivores.
Herbivores and invertivores were species where greater than
50% of the diet was vegetation and invertebrate prey, respectively.
We defined omnivores as species where the primary diet could be
vegetation or invertebrates but included less than 50% vertebrates.
Carnivores were species that primarily consumed greater than
50% live vertebrate prey or carrion. Species-specific dietary com-
positions and resulting classifications are provided in electronic
supplementary material, table S1.
For all sampling groups within each study, we extracted
location-specific climatic data from the WorldClim 2.0 database
[34], human population density data from the Center for
International Earth Science Information Network (CIESIN) [35],
land coverage from the European Space Agency Climate Change
Initiative Land Cover maps (CCILC) [36] and a composite measure
of anthropogenic pressure from the HFI database [37]. For the
WorldClim database, we obtained spatial data for interpolated
estimates of average annual temperature and precipitation
(19702000) at a 10 km resolution. The average, maximum
and minimum temperatures were highly correlated, and explora-
tory analyses showed that average temperature was a stronger
predictor of T. gondii prevalence than the maximum or minimum
temperature; therefore, we retained average temperature for
all analyses.
We obtained spatial data on human population density
(people per km
2
) from the CIESIN, using the 1 km resolution
maps. Land cover data were obtained from the CCILC database
with a 300 m resolution. For both the human density and land
cover maps, we obtained data for 2000, 2005, 2010, 2015 and
2019 and for each study, we used the time period for those vari-
ables that most closely corresponded to the sampling dates of the
study. Site-specific cropland coverage was calculated from the 22
land cover classes provided in the ESA CCILC database, where
we included the four cropland cover classes of rainfed cropland,
irrigated or post-flooding cropland, mosaic cropland and mosaic
natural vegetation. A composite measure of anthropogenic press-
ures was obtained from the 2009 Human Footprint map, which is
a 1 km resolution map of the cumulative anthropogenic press-
ures arising from human density, built environments, electric
infrastructure, croplands, pasture lands, transport routes (road,
railways and navigable waterways) [37] termed as the HFI.
We extracted the average annual temperature and precipi-
tation, human density and HFI for each sampling location
averaged over a 50 km buffer around the sampling point using
the R package raster [38], with a World Geodetic System 1984
projection. Using ArcGIS [39], cropland was calculated as the pro-
portion of the 50 km buffer area that contained any of the four
CCILC cropland types. The buffers were transformed to the local
UTM coordinate system of each site to minimize area distortion,
especially for the sites in the higher latitudes. A 25 km buffer
was also calculated to determine comparability. All geographical
fixed-effect variables were standardized before analysis to place
them on the same scale, and we calculated Pearson correlation
coefficients between standardized fixed variables prior to testing
(electronic supplementary material, table S3). There were no vari-
ables appearing in the same model with a mean correlation above
0.7. For temperature and cropland, which had a correlation of 0.69,
we compared all model coefficients when the two variables were
included together and separate. There were only small differences
in the coefficients for the two scenarios, and therefore we did not
exclude these correlated variables from appearing in the same
model. The sampling representation across the climatic and
anthropogenic variables is provided in electronic supplementary
material, figure S2.
(b) Statistical analysis
We tested our hypotheses using Bayesian phylogenetic general-
ized linear mixed models as implemented in the R package
MCMCglmm [40], following the methods of Barrow et al. [72].
These models enable the incorporation of phylogenetic distance
to accommodate for non-independence due to shared ancestry.
Phylogenetic variance was included as a random effect with the
phylogenetic covariance matrix for mammalian taxa based on
1000 birthdeath node-dated trees [41], with the R package ape
[42]. Prevalence data were modelled as counts of positive individ-
uals and negative individuals with an assumed multinomial
distribution. We took a hypothesis testing approach and evaluated
the relative support for an association between T. gondii prevalence
and ecological, climatic and anthropogenic factors. Because our
expectations were for linear relationships between the predictor
variables and prevalence, we did not test curvilinear relationships,
nor did we include interactions among the predictor variables.
Model support was evaluated based on the deviance information
criterion (DIC), where a difference in DIC (ΔDIC) of greater than
37 would be indicative of less model support [43]. Fixed-effect
predictors were considered to be significant if the 95% credible
interval (CI) did not overlap with zero.
Model selection started with an intercept-only model that was
used to evaluate support for a mixed-effects base model with
study, species and phylogeny as random effects and detection
method (serology versus isolation) as a fixed effect. This mixed-
effects base model had substantial support over the intercept-
only model (ΔDIC = 366.35) and was therefore included in all
subsequent model testing. The analyses to test our three main
hypotheses first assessed an ecological traits-only model, evaluat-
ing the support for an association of ecosystem or diet, separately
or combined on T. gondii prevalence. Similarly, a climate-only
model was tested, where we examined the relative relationship
between T. gondii prevalence and annual average precipitation
and temperature. For both of these model comparisons, the
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statistically significant predictors were then retained in models
testing the relative correlation of T. gondii prevalence with anthro-
pogenic variables. Using the mixed-effects base model and
including influential ecological and climatic variables, we com-
pared model support and mean effects for human population
density, crop coverage and HFI (table 1). The top selected model
was used to estimate mean effects of all fixed-effect variables
and the relative contribution of phylogenetic and non-
phylogenetic specieseffects to the total random variation, which
approximates the phylogenetic signal (termed lambda, λ).
All models assumed a multinomial distribution and were run
for 400 000 iterations with a burn-in of 100 000 and a thinning
interval of 100. For the random effects, we used the priors as
implemented in MCMCglmm (V= 1 and ν= 0.02). All variables
had effective sample sizes exceeding 2500, Gelman statistics
approximating 1.0 and consistent trace plots, all of which indi-
cate MCMC convergence [44]. The R package epiR [45] was
used to calculate T. gondii prevalence at the taxonomic family
level (electronic supplementary material, table S4).
3. Results
Our literature search produced 202 T. gondii prevalence
studies representing 238 species from 54 taxonomic families
and 45 079 tested individuals. Collectively, these studies
sampled individuals from 981 locations across the globe
(figure 1). There were notable study gaps in Asia (i.e.
Russia, China, India), but similar absolute latitudinal gradi-
ents were captured in North and South America and from
northern Scandinavia to equatorial Africa. The number of
sampled individuals from different dietary-ecosystem
groups were as follows: aquatic herbivore (n= 1433), aquatic
omnivore (n= 25), aquatic carnivore (n= 1443), terrestrial her-
bivore (n= 24 678), terrestrial invertivore (n= 1522), terrestrial
omnivore (n= 13 423), terrestrial carnivore (n= 2555).
Compared to an intercept-only model, the addition
of study, species and phylogeny as random effects led to signifi-
cant model improvement (ΔDIC = 366.35). For the ecological
trait-only (ecosystem and diet) and climatic factor-only (temp-
erature and precipitation) models, only ecosystem type and
temperature were significant, both improving model support
over the base model with their inclusion (ΔDIC = 8.42).
Among the anthropogenic variables, the inclusion of human
density resulted in the greatest improvement in model support
(ΔDIC = 23.97), followed by the inclusion of HFI (ΔDIC =
17.73). By contrast, the inclusion of crop coverage did not
improve model support over a reduced model (table 1). The
top model containing human density, temperature and ecosys-
tem (table 1), showed a significant and positive effect of human
density (β= 0.71; 95% CI: 0.411.03) and average temperature
(β= 0.43; 95% CI: 0.230.63) on T. gondii prevalence. Mamma-
lian species in terrestrial ecosystems had a lower average
prevalence than species in aquatic ecosystems (β=0.96; 95%
CI: 1.69 to 0.25; figure 2). Results for model selection and
mean effect coefficients were comparable if a 25 km buffer
was used (electronic supplementary material, table S5). We
found a significant phylogenetic signal for T. gondii prevalence,
where phylogenetic variation (λ) accounted for 48% of the
random variation (95% CI: 0.250.68), while the variation
attributed to species as a random variable accounted for
approximately 3.9% of total variation (95% CI: 0.000.14).
4. Discussion
Our global analysis supported our hypotheses that T. gondii
prevalence would be associated with human density,
temperature and ecosystem type across a diversity of mamma-
lian taxa and a broad geographical range. The most compelling
result was strong support for our hypothesis that T. gondii
infections in wildlife would be greater in areas of higher
human density. This finding is consistent with previous finer
geographical-scale studies that have documented increases in
T. gondii prevalence in wildlife with increasing anthropogenic
pressures [4649]. Increased human density (rural and urban
development) is connected with multiple landscape alterations
that could influence the epidemiology of T. gondii, the most
intuitive being the abundance of owned and unowned free-
roaming domestic cats [50]. Although such a direct association
between cat density and T. gondii prevalence cannot be made at
Table 1. Deviance information criterion (DIC) model selection results for testing hypotheses for ecological (eco and habitat), climatic (temp and precip) and
anthropogenic (human, crop and HFI) risk factors associated with Toxoplasma gondii prevalence patterns in free-ranging mammalian wildlife. ΔDIC = change in
DIC relative to the top model in each hypothesis. Predictor xed effects: eco = aquatic or terrestrial; diet = herbivore, invertivore, omnivore or carnivore; temp =
average annual temperature; precip = average annual precipitation; HFI = human footprint; crop = cropland coverage; human = human density. The base model
(base) includes detection method as a xed effect and random effects for phylogeny, species and study (DIC = 30 584.59). See Methods for further details.
DIC ΔDIC
1. ecological variablesecosystem and diet
ecosystem only eco + base 30 583.9 0
ecosystem and diet only eco + diet + base 30 586.21 2.31
2. climatic variablesprecipitation and average temperature
temperature only temp + base 30 576.73 0
temperature and precipitation temp + precip + base 30 618.58 41.85
3. anthropogenic variableshuman density, HFI, cropland coverage
human density eco + temp + human + base 30 552.19 0
HFI eco + temp + HFI + base 30 569.93 17.73
ecosystem and temperature eco + temp + base 30 576.17 23.97
cropland eco + temp + crop + base 30 576.94 24.75
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the global scale due to a lack of cat abundance data, this
association has been made at local scales [21,51,52].
There are an estimated 600 million domestic cats globally
[53], which is several orders of magnitude larger than the com-
bined abundance of all wild felid species [32]. Consequently,
although multiple species of felids are known definitive hosts
for T. gondii, this significant disparity in population size, and
the positive association between T. gondii prevalence and
human density in this present study, provide additional sup-
port for domestic cats being the most consequential definitive
host for wildlife T. gondii infections [28]. Wildlife populations
in pristine environments with exposure only to wild felids
have a lower T. gondii prevalence than populations with
increased exposure to domestic cats [21,52]. Therefore,
T. gondii transfer from domestic cats into wildlife populations
likely elevates infection rates above more naturalized endemic
levels and introduces domestic strains into the wildlife cycle.
The transfer of T. gondii strains between wildlife and domestic
cats is consequential because strains predominating in dom-
estic cats versus wild felids differ in virulence, shedding
behaviour and oocyst and tissue-cyst infectivity [16]. Com-
pared to wild-type strains, domestic cat strains have evolved
increased tissue-cyst infectivity [16] and induce more prolific
oocyst shedding in domestic cats [54]. These traits of domestic
strains could further increase the prevalence and persistence of
T. gondii in exposed wildlife populations.
Increases in human density also impact the severity and
spatial scale of T. gondii contamination by removing ecosys-
tem services that reduce oocyst spread and limit the size of
free-roaming cat populations. For example, wetlands and
other naturalized features can help impede lateral oocyst
spread via terrestrially based runoff into aquatic systems
[5], functions which are crippled in landscapes dominated
by impervious surfaces [29]. Intact ecosystems are also
associated with higher abundances of native predators such
as coyotes that limit the infiltration of free-roaming cats into
important wildlife areas [55]. This protective role of native
predators was demonstrated when population declines of
Tasmanian devils (Sarcophilus harrisii) were correlated with
both an increase in the numbers of feral cats and T. gondii
prevalence in native wildlife [21].
Due to the significant landscape and hydrological altera-
tions associated with agricultural intensification, we had
predicted that T. gondii prevalence in wildlife would be posi-
tively associated with cropland cover. However, we did not
find a consistent association with cropland coverage. Native
habitat retention within agricultural landscapes has been
associated with lower risks of pathogen transfer from dom-
estic animals into wildlife [56]. However, domestic cat
densities frequently show a reduced [57] but unequal distri-
bution across rural habitat types [50], and this may
complicate attempts to elucidate a broad-scale pattern using
available land cover metrics.
We also found support that T. gondii prevalence is
influenced by climate. Specifically, we found that T. gondii
prevalence increased in warmer locations. Temperature may
influence prevalence through both variation in oocyst survi-
val and host distribution [58]. Oocyst viability declines at
temperatures below 20°C [27], but colder regions could also
have smaller free-roaming domestic cat populations due to
decreased overwinter survival of feral cats and owned cats
being limited to free-roaming only during warmer seasons.
Although precipitation has been demonstrated to increase
T. gondii transmission to the aquatic ecosystem [59,60], we
had anticipated increased precipitation would also be associ-
ated with increased exposure within terrestrial ecosystems.
Contrary to our predictions, precipitation lacked a significant
association with T. gondii prevalence. The role of precipitation
Figure 1. Distribution of study sites included in the global analysis of Toxoplasma gondii prevalence data for free-ranging wild mammal populations. (Online version
in colour.)
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in the fate and transport of oocysts would be impacted by local
hydrological governing factors, such as soil and topography,
dilution effects, seasonality and the nature and degree of pre-
cipitation intensity and antecedent soil moisture conditions
[59,60].
Waterborne toxoplasmosis via oocysts is an important
route of infection for humans and wildlife [15,24], and we
did find that aquatic mammals had an increased T. gondii
prevalence compared to terrestrial species. Because there is
no known aquatic definitive host for T. gondii, aquatic ani-
mals are likely exposed to oocysts transferred from felids in
terrestrial ecosystems [28]. Studies of California sea otters
(Enhydra lutris) [60] and beluga whales (Delphinapterus
leucas) [61] reported increased T. gondii prevalence under con-
ditions of higher terrestrial runoff. Further evidence of
anthropogenic oocyst loading of freshwater comes from the
higher prevalence of T. gondii in muskrats (Ondatra zibethicus)
exposed to wastewater [62] or watersheds subject to larger
amounts of terrestrial runoff [63], compared to the absence
of seropositive muskrats in pristine watersheds [64]. Com-
pared to terrestrial ecosystems, there may also be increased
oocyst accumulation and persistence within aquatic ecosys-
tems due to oocyst adherence to biofilms on aquatic
vegetation [65] and bioaccumulation within aquatic microor-
ganisms [66] and larger-bodied filter-feeding transport hosts
[67]. This bioaccumulation of waterborne pathogens has been
leveraged in novel surveillance programmes for both marine
[68] and freshwater ecosystems [69].
By contrast to comparative studies of sympatric taxa [25],
we did not find a significant effect of a speciestrophic level,
suggesting that environmental exposure (oocyst-associated)
may be more globally significant than trophic transmission
(tissue-cyst-associated). Tissue cysts could have an inherently
lower transmission rate because infections require that a
predator ingest viable tissue cysts, which may infrequently
occur unless the entire body of the prey is freshly consumed.
Results from this study and other large-scale analyses [4]
highlight how geographical factors such as anthropogenic
pressures in an individuals ecosystem may be more
predictive of disease risk than generalized species-specific
ecological traits. For example, within this dataset, black
bears (Ursus americanus) had double the prevalence (58%) of
the less synanthropic, but similarly omnivorous, grizzly
bears (U. arctos, 24%). Similarly, insectivorous bats (Miniopterus
schreibersii), which would be expected to be a low-risk ecologi-
cal guild for T. gondii exposure, had a significantly higher
prevalence in southern Myanmar compared to conspecific
populations in China, again demonstrating the strong
influence of geographical factors [70,71].
Despite the variable impact of species ecology on T. gondii
prevalence, we detected a notable phylogenetic signal.
Although few studies have quantified a phylogenetic signal
for wildlife diseases, which limits comparison, the signal
for T. gondii was higher than that reported for a smaller
scale study focused on avian malaria among multiple
orders of Andean birds (λ: 0.130.35 [72]). The phylogenetic
signal for a generalist pathogen such as T. gondii probably
reflects evolutionarily conserved ecological or physiological
host traits that influence prevalence but were not included
in our analysis. For example, the evolutionarily distant
families, Didelphidae and Procyonidae, are both synanthro-
pic, terrestrial omnivores, but the former has half the mean
prevalence, suggesting the presence of other unaccounted
for drivers. Additionally, the clinical severity of T. gondii
infections varies among taxonomic groups, with related
taxa showing similar patterns of susceptibility, which
would also contribute towards a phylogenetic signal in this
dataset [72].
We acknowledge several important caveats in our study.
First, as we noted earlier, although a large amount of
T. gondii prevalence data were available, there are key areas
such as central Eurasia and east-central Africa that had mini-
mal representation, which is unfortunate given that countries
on these continents have relatively high human T. gondii
prevalence [12]. Furthermore, we broadly categorized ecosys-
tem types as terrestrial or aquatic, and sampling efforts are
unlikely to be uniform across different environments and
habitats within these ecosystems. Therefore, the associations
1
0
–1
–2
Herb Invert Omniv Terr cropland HFI human density Precip Temp (°C)
diet ecosystem anthropogenic climate
ecological geographical
effect on prevalence (b)
Figure 2. Posterior mean effects (95% credible intervals shown) for fixed variables in a top model containing the ecological, climatic and anthropogenic factors
tested for an association with Toxoplasma gondii prevalence in global free-ranging wild mammal populations. The ecological species-specific variables shown in the
left facet are the effect on prevalence for mammals that have primarily a herbivore (Herb), invertivore (Invert) and omnivore (Omniv) diet relative to a carnivore diet
and live in a terrestrial (Terr) relative to an aquatic ecosystem. The geographical variables in the right facet are cropland coverage, human footprint (HFI), human
population density, annual precipitation (Precip) and average annual temperature °C (Temp).
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 288: 20211724
6
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found in the present analysis may differ from those present in
wildlife populations from data-deficient regions or environ-
ments. An emphasis on georeferencing data and passive
surveillance of wildlife populations for underrepresented
taxa, regions and ecosystems would enable a more refined
analysis for additional ecological and geographical variables
that may be associated with T. gondii prevalence.
Second, while our model can help identify prospective
higher risk areas for T. gondii associated with climate and
human densities, we acknowledge that the identification of
cause and effect mechanisms, such as domestic cat abun-
dance, can only be deduced in a general manner at a global
spatial scale. Molecular epidemiological methods are well
suited to address these knowledge gaps with increasingly
sensitive assays for detecting T. gondii DNA in environmental
samples [15]. Moreover, these studies can genotype T. gondii
isolates and identify them as strains most likely to originate
from wild or domestic cycles [73]. Even in the absence of
mechanistic cause and effect evidence herein, the presence
of a significant relationship between human density and
T. gondii prevalence in wildlife at a global scale suggests
that proactively targeting pathogen pollution from domestic
cats would be the most pragmatic and impactful intervention
for decreasing wildlife infections. Approaches targeting inter-
mediate hosts fail to address the significant role of oocyst-
associated infections in T. gondii epidemiology. For example,
focusing management efforts on removing pathogen inputs
from the domestic pig definitive host led to a significant
reduction in Trichinella spiralis prevalence in European
wildlife in less than a decade [74].
Adopting an ecosystem-based approach for managing
zoonotic diseases can be more economically efficient than
reactionary interventions to single pathogens [75], with
synergistic health and conservation benefits. Addressing eco-
system health may be particularly efficacious for T. gondii
prevention. Free-roaming domestic cats depredate tens of bil-
lions of wild animals each year [76], with additional wildlife
and public health impacts through the transmission of
T. gondii and other pathogens [77]. Mitigating these influences
through landscape restoration and effective population man-
agement of free-roaming cats would simultaneously benefit
wildlife through reduced predation mortality, disease and
increased population resiliency. Furthermore, because wildlife
are reliable sentinels for human exposure risk to T. gondii, these
actions could also contribute towards decreasing the human
health burden of one of the most common global human
parasitic zoonoses.
Data accessibility. Master dataset used for analysis have been included as
electronic supplementary material. The data are provided in the elec-
tronic supplementary material [78].
Authorscontributions. A.G.W.: conceptualization, data curation, formal
analysis, investigation, methodology, validation, visualization,
writingoriginal draft, writingreview and editing; S.W.: conceptu-
alization, formal analysis, investigation, writingoriginal draft,
writingreview and editing; N.A.: formal analysis; D.R.L.: conceptu-
alization, formal analysis, funding acquisition, investigation,
writingoriginal draft, writingreview and editing. All authors
gave final approval for publication and agreed to be held accountable
for the work performed therein.
Competing interests. We declare we have no competing interests.
Funding. This work was financially supported by Agriculture and
Agri-Food Canada Project J-002305, Environmental Change One
Health Observatory (ECO
2
).
Acknowledgements. We gratefully acknowledge the efforts of all authors
whose published work form the basis of our global analysis. We also
thank the anonymous reviewers whose comments and suggestions
greatly improved this manuscript.
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... Disease transmission risk increases when ecosystem degradation reduces the disease resiliency of wildlife [6], and habitat encroachment places wildlife in abnormal contact situations such as live animal markets [7] or through frequent interactions with domestic animals. Frequent close contact between wildlife and free-roaming domestic animals increases the opportunity for bidirectional disease transfer [8]. ...
... Domestic cats are a particular concern for conservation, welfare and public health in many regions because they are often allowed to roam free without supervision and, as a result, frequently interact with and kill wildlife. Freeroaming cats not only present a risk for transmitting viral, parasitic and bacterial diseases to wildlife [4,8,[11][12][13], but also contracting and transporting diseases from wildlife that can be then passed on to humans [11]. ...
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Free-ranging domestic cats are a detriment to wildlife and humans by preying on native species and transmitting disease. As a result, removing free-ranging cats from the landscape has become a conservation and public health priority. Estimating cat population size with an unbiased sampling design, however, especially in human-dominated areas, is logistically challenging and rarely done. The lack of robust cat population sampling limits our understanding of where cats pose risks, which is important for evaluating management strategies, such as trap-remove or trap-neuter-return. We hypothesized that cat abundance and activity both depend on human land use and demographics. Using a network of sites participating in a community science program, we conducted transect and camera trap surveys to test predictions of cat population abundance and activity across a gradient of residential land use intensity. Both sampling methods determined that cat abundance was greatest in areas with intermediate human population density and lower educational attainment. Transect data also provided evidence that cat abundance was greatest at intermediate levels of impervious surface cover (e.g., road and buildings), while data from camera traps also showed that cat abundance was positively associated with household income. Using counts of cats observed on cameras, we found that the timing of cat activity varied depending on the degree of urban intensity. Cats were more strictly nocturnal in medium and high intensity residential land-use areas, possibly because a greater proportion of these cats are unowned or because they avoid human activity. These results suggest that transect surveys conducted during the day may undercount cats in urban environments where unowned free-ranging cats predominate. Taken together, our results highlight the importance of incorporating human demographics, land use patterns, and urban context in estimating the abundance of free-ranging cats to better inform management decisions and improve conservation outcomes.
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Agricultural intensification and simplification are key drivers of recent declines in wild bird populations, heightening the need to better balance conservation with food production. This is hindered, however, by perceptions that birds threaten food safety. While birds are known reservoirs of foodborne pathogens, there remains uncertainty about the links between landscape context, farming practices, and actual crop contamination by birds. Here, we examine relationships between landscape context, farming practices, and pathogen contamination by birds using a barrier‐to‐spillover approach. First, we censused bird communities using point count surveys. Second, we collected 2,024 faecal samples from captured birds alongside 1,215 faecal samples from brassica fields and food processing areas across 50 farms spanning the USA West Coast. We then estimated the prevalence of three foodborne pathogens across landscape and livestock intensification gradients. Finally, we quantified the number of plants with faeces. Campylobacter spp. were detected in 10.2% of faeces from captured birds and 13.1% of faeces from production areas. Non‐native birds were 4.1 times more likely to have Campylobacter spp. than native birds. Salmonella spp. were detected in 0.2% of faeces from production areas and were never detected in captured birds. We detected evidence of Shiga toxigenic E. coli in one sample across the >3,200 tested. Campylobacter spp. prevalence in faeces from production areas increased with increasing mammalian livestock densities in the landscape but decreased with increasing amounts of natural habitat. We encountered bird faeces on 3.3% of plants examined. Despite the impact on pathogen prevalence, amount of natural habitat in the landscape did not increase the number of plants with bird faeces, although on‐farm mammalian livestock density slightly did. Synthesis and applications. Food safety and wildlife conservation are often thought to be in conflict. However, our findings suggest that natural habitat around farms may reduce crop contamination rates by birds. This is perhaps because natural habitat can promote native birds that are less likely to harbour foodborne pathogens or because it decreases contact with livestock waste. Our results suggest that preservation of natural habitats around farms could benefit both conservation and food safety, contrary to current standards for ‘best practices’. Food safety and wildlife conservation are often thought to be in conflict. However, our findings suggest that natural habitat around farms may reduce crop contamination rates by birds. This is perhaps because natural habitat can promote native birds that are less likely to harbour foodborne pathogens or because it decreases contact with livestock waste. Our results suggest that preservation of natural habitats around farms could benefit both conservation and food safety, contrary to current standards for ‘best practices’.
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Land use change—for example, the conversion of natural habitats to agricultural or urban ecosystems—is widely recognized to influence the risk and emergence of zoonotic disease in humans1,2. However, whether such changes in risk are underpinned by predictable ecological changes remains unclear. It has been suggested that habitat disturbance might cause predictable changes in the local diversity and taxonomic composition of potential reservoir hosts, owing to systematic, trait-mediated differences in species resilience to human pressures3,4. Here we analyse 6,801 ecological assemblages and 376 host species worldwide, controlling for research effort, and show that land use has global and systematic effects on local zoonotic host communities. Known wildlife hosts of human-shared pathogens and parasites overall comprise a greater proportion of local species richness (18–72% higher) and total abundance (21–144% higher) in sites under substantial human use (secondary, agricultural and urban ecosystems) compared with nearby undisturbed habitats. The magnitude of this effect varies taxonomically and is strongest for rodent, bat and passerine bird zoonotic host species, which may be one factor that underpins the global importance of these taxa as zoonotic reservoirs. We further show that mammal species that harbour more pathogens overall (either human-shared or non-human-shared) are more likely to occur in human-managed ecosystems, suggesting that these trends may be mediated by ecological or life-history traits that influence both host status and tolerance to human disturbance5,6. Our results suggest that global changes in the mode and the intensity of land use are creating expanding hazardous interfaces between people, livestock and wildlife reservoirs of zoonotic disease.
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Aim Free‐ranging wildlife are valuable sentinels for zoonotic, multi‐host pathogens, and new insight into parasite transmission patterns is possible through a macroecological approach. Toxoplasma gondii is a protozoan capable of infecting all warm‐blooded animals, including humans, primarily through a free‐living oocyst and/or tissue cyst life stage. Anthropogenic disturbance is facilitating the spread of T. gondii, making it crucial to understand the general ecological and life‐history drivers of T. gondii infections in wild birds, which are important intermediate hosts. Our goal was to determine how habitat (terrestrial versus aquatic), dietary trophic level and scavenging behaviour influence the prevalence of T. gondii infection in wild birds at a global scale. Location Global. Time period 1952–2017. Major taxa studied Birds. Methods Our analysis used the serological, bioassay and molecular prevalence data of T. gondii in avian species compiled from 81 studies conducted worldwide and encompassing 24,344 individuals from 393 avian species from 84 families. Results We showed that at a global scale, trophic level and habitat interacted significantly to influence T. gondii prevalence in avian intermediate hosts. In the terrestrial environment, T. gondii prevalence increased with trophic level, consistent with predominant tissue cyst transmission. The highest prevalence was in terrestrial omnivores, which might reflect their synanthropic foraging behaviour. In aquatic species, prevalence was more consistent across trophic levels, but high prevalence in aquatic herbivores and insectivores reflects significant waterborne exposure to oocysts. Contrary to our predictions, generalized scavenging per se was not associated with increased prevalence. Main conclusions This study highlights the value of comparing pathogen prevalence among multiple ecological guilds and ecosystem types for a more comprehensive understanding of the epidemiology of generalist pathogens, such as T. gondii. Increased effort is needed to reduce T. gondii spillover from the domestic cat cycle into wildlife populations.
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Waterborne transmission of Toxoplasma gondii is assumed to be enhanced in areas with human-altered landscapes (e.g., urbanization, agriculture) and increased populations of non-native domestic and feral cats (Felis catus). However, little is known concerning T. gondii exposure risks in more natural watersheds (e.g., reduced human footprint, no domestic or feral cats) to establish a baseline for comparisons. In this study, muskrats (Ondatra zibethicus) were used as sentinels to assess baseline T. gondii exposure in a relatively pristine watershed in the Greater Voyageurs Ecosystem, northern Minnesota during the summers of 2018-2019. Toxoplasma gondii antibodies were assayed in sera of live-trapped muskrats (n = 70) using a modified agglutination test. None of our samples were positive for T. gondii antibodies (p = 0.00, 95% Wald Score Interval Confidence Interval = 0.00 - 0.05). This study establishes a baseline to compare T. gondii waterborne transmission risks in other human-modified watersheds.