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Determinants of vector-borne avian pathogen occurrence in a mosaic of habitat fragmentation in California

Parasites & Vectors volume 18, Article number: 110 (2025) Cite this article

Abstract

Background

As habitat fragmentation increases, ecological processes, including patterns of vector-borne pathogen prevalence, will likely be disrupted, but ongoing investigations are necessary to examine this relationship. Here, we report the differences in the prevalence of Lyme disease (Borrelia burgdorferi sensu lato, s.l.) and haemoproteosis (Haemoproteus spp.) pathogens in avian populations of a fragmented habitat. B. burgdorferi s.l. is a generalist pathogen that is transmitted by Ixodes pacificus vectors in California, and Haemoproteus is an avian parasite transmitted by Culicoides vectors.

Methods

To determine whether biotic (avian and mammalian abundance) or abiotic characteristics (patch size and water availability) correlated with infection prevalence change, we screened 176 birds sampled across seven sites in oak woodland habitat in northern California.

Results

While biotic factors correlated with an increase in both pathogens, infection prevalence of Haemoproteus spp. was only associated with individual-level traits, specifically foraging substrate and diet, and B. burgdorferi s.l. was associated with community-level characteristics, both total mammal and, specifically, rodent abundance. Proximity to water was the only abiotic factor found to be significant for both pathogens and reinforces the importance of water availability for transmission cycles. Larger patch sizes did not significantly affect infection prevalence of Haemoproteus, but did increase the prevalence of B. burgdorferi.

Conclusions

These results highlight that while environmental factors (specifically habitat fragmentation) have a limited role in vector-borne pathogen prevalence, the indirect impact to biotic factors (community composition) can have consequences for both Haemoproteus and B. burgdorferi prevalence in birds. Given the pervasiveness of habitat fragmentation, our results are of broad significance.

Graphical abstract

Background

Urban planning has led to increased habitat fragmentation, creating a mosaic of disturbance patch sizes, with impacts on ecosystem functions [1, 2]. For avian communities, these land-use changes have contributed to a global decline of biodiversity and a shift towards increasingly homogeneous communities, either through the increased presence of cosmopolitan, disturbance-associated species or a widespread distribution of select native species [3,4,5,6,7,8]. This means the impact of land-use changes can be particularly concerning for biodiversity hotspots, such as the California Floristic Province [9]. Despite these concerns, the loss of avian biodiversity is likely to continue as expanding urbanization results in greater habitat fragmentation [3, 10]. Of course, while this emphasizes the role of landscape reconfiguration on the spatiotemporal dynamics of a local population, there are other not-readily-evident factors that may have more subtle population regulatory roles.

Diseases represent one such subtle factor that can have a significant regulatory role in a community. This was most dramatically exemplified when naïve Hawaiian populations of birds were decimated following the introduction of avian malaria [11,12,13]. Our research aims to examine the effects of habitat fragmentation, and resulting landscape mosaic, on avian disease prevalence in a global biodiversity hotspot. Through this work, we hope to contribute to our understanding of the potential risks encountered by avian communities in our increasingly human-dominated landscapes.

To effectively monitor the avian disease ecology of urban environments, it is necessary to understand small-scale habitat variations that reflect nuanced landscape heterogeneity. This relationship between habitat variation and disease ecology is directly studied through individual capture methods in tandem with blood sample analysis, but this method requires considerable effort and may pose ethical complications when studying endangered species. An alternative approach could be to focus on identifying and mapping infection likelihood on the basis of relevant ecological characteristics. Ecological characteristics include extrinsic abiotic variables (e.g., water availability and elevation) and biotic variables, including life histories, host susceptibility, disease transmissibility, and current pathogen distribution. Once identified, pathogen-specific ecological characteristics can be reliably used as a less invasive approach to assess pathogen communities and disease risks.

An increase in habitat fragmentation is expected to affect disease systems, including those caused by avian haemosporidians infections such as Haemoproteus, the causative agent of haemoproteosis, among other pathogens [14]. Avian haemosporidians can be more prevalent and result in greater severity of infections in fragmented, urban habitats compared with the prevalence and impact observed in larger, more rural environments [15, 16]. The few available studies exploring the relationship between avian haemosporidians, host community composition, and abiotic environmental conditions have found that greater diversity of birds and proximity to water are positively correlated with infection prevalence [17,18,19,20]. This relationship is likely due to the haemosporidian vectors, biting midges, and their need for water to complete their life cycles [14, 21, 22]. Therefore, as both community composition and presence of water can be affected by habitat fragmentation, we expect that there are also implications for prevalence of avian haemosporidian pathogens.

In contrast to haemosporidians, B. burgdorferi sensu lato (s.l.), the causative agent of Lyme disease, can involve complex interactions with a greater diversity of hosts [23]. Local host communities, encompassing avian, non-avian, and vector community composition, can contribute to the maintenance of B. burgdorferi s.l. infections [23,24,25]. In particular, the role of birds in the transmission and maintenance of B. burgdorferi s.l. is still relatively understudied [23]. The vectors responsible for transmitting B. burgdorferi s.l. in California are ticks (e.g., Ixodes pacificus). A generalist vector, I. pacificus is capable of feeding and transmitting B. burgdorferi s.l. infections to various hosts including mammals and birds [26]. Vectors and hosts are known to be affected by habitat disturbance [27,28,29], underscoring the importance of community composition for this pathogen within landscape mosaics. Ticks are also sensitive to desiccation, suggesting that water availability through associated humidity could be equally important for B. burgdorferi s.l. infections as it is for avian haemosporidians [30]. The degree to which habitat fragmentation, water availability, and overall community composition shape local B. borrelia s.l. prevalence in birds could provide valuable insight on an understudied disease that is prevalent in both mammals and birds [23,24,25, 31].

Here, we assess commonalities between two avian-associated pathogens with dissimilar life histories and vectors to determine if there are consistent habitat-mediated patterns of infection prevalence. We detected differences in host susceptibility and transmission likelihood between specialist and generalist pathogens across landscape characteristics in live bird captures. We were specifically interested in understanding whether differences in the community composition of birds and abundance of co-occurring mammal species, as well as landscape characteristics, including patch sizes and water availability, are related to the prevalence of the two pathogens. We hypothesized that (1) infection prevalence of host-specialist parasites in the genus Haemoproteus would be correlated with birds, but not mammals, and (2) water availability would be the only landscape variable expected to affect susceptibility of birds to Haemoproteus pathogens. For the generalist pathogen B. burgdorferi s.l., (3) infections would increase in response to the proportion of susceptible hosts, including mammalian and avian, and (4) in addition to water availability, larger habitat size would also affect the susceptibility of birds to B. burgdorferi s.l. Although we screened for additional pathogens, including Plasmodium, the infection prevalence was too low in our study sites for proper analysis. Our reported results highlight the potential for developing low-cost, fine-scale pathogen monitoring across fragmented environments while minimizing human–animal interactions. Although the exact health impact of Haemoproteus and B. burgdorferi s.l. on birds in California is understudied, general studies have reported host mortality following severe, acute infections as well as low, chronic infections increasing the potential for certain bird species to serve as reservoir hosts for both pathogens [14, 32,33,34]. This work is of broad significance, given the increasingly evident relationship between avian conservation and public health globally.

Methods

Study site

This study was conducted on seven sites across the San Francisco Bay Area of California, USA, which is part of the California Floristic Province global biodiversity hotspot [9]. This region has a high degree of urbanization and supports nearly eight million people, a number that has grown by 8% in the last decade (www.vitalsigns.mtc.ca.gov/). On the basis of the Public Review Draft Environmental Impact Report published by Plan Bay Area 2040, 28% of the Bay Area’s land cover is identified as protected open space. These designated parks differ in size but occur within a Mediterranean climate with cool, wet winters and warm, dry summers that experience unique microclimates [35]. At each site, we delineated three separate 10 m radius vegetation sampling plots. The center of each plot was selected from a randomized compass bearing and located 15 m from one of the ten mist nets that were used during this study to capture birds. Within each plot, we surveyed tree stem density (here a tree was defined as anything larger than 10 cm DBH), canopy cover percentage (measured using a spherical crown densitometer at the center point of each plot), and understory density (measured using a 2 m cover pole and defined as the percent cover of vegetation obscuring this pole from an observation point 5 m away at a randomized compass bearing). As these results showed, within site habitat was comparable, consistent with a previous report that found all sites were similar in both vegetation and climatic conditions [28]. Owing to these similarities, we only examined the larger-scale landscape characteristics of habitat fragmentation and proximity to water. Additional file 1: Table S1 lists all survey data.

A total of seven study sites were selected because of their use in other long-term studies focused on the relationship between shifting mammal communities and B. burgdorferi s.l. distribution (Fig. 1). Previous studies on mammalian communities have been published for our study sites [28, 36], and our own previous research [24] provides details on the avian community as well. These sites include three located in San Mateo County, CA, USA [Junipero Serra County Park (JSP, 37.607917, −122.424111), Windy Hill Open Space Preserve (WHO, 37.36455, −122.22108), and Pulgas Ridge Preserve (PRO, 37.474749, −122.28512)]; two sites in Marin County, CA, USA (CCP, China Camp State Park (38.00843, −122.49703) and Tiburon Uplands Nature Preserve [TUP,37.889306, −122.450861)]; one site in Contra Costa County, CA, USA [Lafayette Reservoir Nature Area (LFY, 37.88394, −122.13472)]; and one site in Sonoma County, CA, USA [SLP, Spring Lake Regional Park (38.45225, −122.64833)]. Although some study sites are relatively close, our net placements exceeded the expected territory sizes and movement for the focal species (50–100 m) [37]. All sites are within an oak woodland habitat, and the dominant tree communities at all sites include Quercus kelloggii and Quercus agrifolia. The US Geological Survey (USGS) landcover database was used to assess habitat fragmentation, referring to the largest area within a site that is completely bounded by human infrastructure (https://www.usgs.gov/centers/eros/science/annual-national-land-cover-database). The National Water Dashboard was used to measure the distance to the nearest permanent water source on the basis of the Hydrologic Unit Code 12. Size and seasonal fluctuations were not accounted for within our approach.

Fig. 1
figure 1

Site locations across northern California, USA. List of sites: Spring Lake Regional Park (SLP), China Camp State Park (CCP), Tiburon Uplands National Preserve (TUP), Lafayette Reservoir (LFY), Junipero Serra Park (JSP), Pulgas Ridge Open Space Preserve (PRO), and Windy Hill Open Space Preserve (WHO)

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Field methods

Birds were captured during the breeding season at each site over two consecutive days between June and September in 2019 and 2020. Transects consisted of ten mist nets, each 12 × 2.5 m, opened at sunrise (06:00 h) for 5 h. This translated into 120 m of net coverage active for 20 h at each field site (680 m active for 80 h across the entire study). Birds were banded using appropriately sized federal aluminum bands. Morphometrics, body condition, bird taxonomy, age, and sex were determined on the basis of published characteristics [38]. Blood was collected from every bird via brachial venipuncture conducted with a 30 ga needle. Between 50 and 100 μL of blood were transferred via heparinized-microhematocrit capillary tubes into cryotubes containing 750 μL of lysis buffer [10 mM Tris pH 8.0, 100 mM etheylenediaminetetraacetic acid (EDTA), 2% sodium dodecyl sulfate (SDS)] for subsequent molecular analysis [39]. Two blood films were prepared for each bird and air-dried within 5–10 s after preparation. Slides were immediately fixed in methanol in the field and subsequently stained using 1:10 Giemsa: phosphate buffer (0.005 M KH2PO4 and 0.007 M Na2HPO4) at pH 7.2 [14] within 30 days. Slides were examined, but the low parasitemia proved too challenging to obtain sufficient observations and limited our ability to describe the morphospecies of the two novel lineages of haemosporidians; therefore, results were not included in our study. However, slides are available for future use.

Pathogen screening and identification

Genomic DNA was preserved in the lysis buffer and stored at room temperature prior to freezing at −80 °C for long-term storage. Blood extraction was performed using Wizard SV Genomic DNA Purification System (Promega Corporation, Madison, WI, USA) following the manufacturer’s protocol. All subsequent polymerase chain reactions (PCRs) were conducted using GoTaq Flexi DNA Polymerase (Promega Corporation, Madison, WI, USA). DNA extraction quality was assessed by initial PCR amplification of the avian brain-derived neurotrophic factor gene to ensure the presence of amplifiable DNA [40]. Following verification of DNA extraction, nested PCR was used to test for Haemoproteus or Plasmodium by targeting the cytochrome b gene of the parasite’s mitochondria [41]. A nested PCR was used to screen for B. burgdorferi s.l. by targeting the B. burgdorferi s.l.-specific 5S-23S rRNA intergenic spacer region [24, 42, 43]. Nested PCR products were submitted for Sanger sequencing at ElimBio (CA, USA). Sequences were used to identify the parasite genus by comparing against the MalAvi and NCBI BLAST databases. Any haemosporidian sequence from our study that differed from a published sequence by over 1% or 4 bp was considered novel. Additional phylogenetic analysis will be reported elsewhere. A subset of birds was screened for the presence of Trypanosoma, Leucocytozoon, or avian pox, but owing to low infection prevalence of each, these were excluded from subsequent analyses [39, 44, 45]. Confidence intervals (95%) for infection prevalences were calculated using the methods listed in ref. [46]. In short, the qbeta function was run using base R version 1.2.5033 (RStudio Team 2019) with the shape one parameter set to the number of positive samples + 1 and the shape two parameter set to total sample size—positive samples + 1.

Statistical analysis

A series of independent models were conducted for each genus of pathogen. The infection prevalence of Haemoproteus and B. burgdorferi s.l. was set as the dependent variable in their respective sets of models. We applied binomial logistic regressions to infection data derived from avian blood samples using the package stats in R 4.1.2. To avoid overparameterization, each series consisted of three separate models (six models total—three per focal pathogen) comparing different potential determinants of infection prevalence. We only report on the best explanatory factors, but other variables including rodent abundances were also initially examined. The first was the site characteristic model (SCM) examining the effect of site identity, the area of contiguous habitat cover, and the distance to the nearest permanent water source (the latter two parameters determined using USGS land cover maps). The second model was the total community model (TCM), which included the abundance and diversity of rodents, non-rodent mammals, and birds at each site determined either from previously published data or from avian sampling conducted as part of this study. All surveys of mammal community metrics were completed using both live trapping (with Sherman traps) and camera trapping methods. The final model was the avian community model (ACM), which included the effects of bird sex, mass, and age, determined in the field, as well as diet guild, foraging guild, and nesting guild, which were categorized using data published by the Birds of the World Handbook (http://www.birdsoftheworld.org/) and related publications [47,48,49]. Models are outlined in Table 1. These three models were selected to approximate the effects of variance on host-specificity, driven by differences in avian community composition (the ACM), and transmissibility driven by differences in broader community composition (the TCM) or environmental characteristics (the SCM). Statistical significance of variables in each model was calculated using the likelihood-ratio test.

Table 1 Models of avian host infection prevalence as a response to abiotic and biotic factors
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Results

Pathogen prevalence

In the 2019 and 2020 breeding seasons, 218 individuals, corresponding to 22 distinct species of birds, were captured using mist nets, and samples were successfully collected from 176 individuals and screened for parasitic infections. A detailed list of all samples is available (Additional file 1: Table S2). Parasite lineages were diverse, but because abundance was relatively low, infections will be discussed at the genus level unless otherwise stated. Using PCR-based detection methods, 18.2% (confidence intervals, CI 13.2–24.6%) of birds were found to have Haemoproteus infections, 1.7% (CI 0.6–4.9%) had Leucocytozoon infections, and 1.1% (CI 0.4–4.0%) had Plasmodium infections. A total of 14.8% (CI 10.3–20.8%) B. burgdorferi s.l. infections were detected. Only one dark-eyed junco (Junco hyemalis) from WHO was found to be infected with Borrelia bissettiae, corresponding to 0.6% (CI 0.1–3.1%) of all samples. The most abundant bird species, dark-eyed junco, had high prevalence of both Haemoproteus (30.4%, CI 21.3–41.3%) and B. burgdorferi s.l. (15.2%, CI 8.9–24.7%) infections, but sample sizes were still too low for species-specific analyses. Coinfections of Haemoproteus and B. burgdorferi s.l. were detected in 4.0% (CI 2.0–8%%) of samples. These coinfections include the single dark-eyed junco infected with B. bissettiae also being infected with Haemoproteus spp. JUNHYE3.

The majority of species studied were represented by fewer than five individuals. Therefore, our analysis focused on guilds (granivores, insectivores, or omnivores) rather than species. Infection prevalence of Haemoproteus was highest in granivores (29.7%, CI 21.3–39.8%) while the prevalence of B. burgdorferi s.l. was highest in omnivores (18.2%, CI 5.5–48.4%). Plasmodium infections were uncommon (omnivores: 0%, CI 0.2–26.5%; granivores: 1.1%, CI 0.3–5.9%; and insectivores: 1.4%, CI 0.3–7.2%). Specific details about infection prevalence per individual and across sites are included in Additional File 1: Table S2.

Both pathogens showed a correlation with site characteristics (Table 1). Borrelia burgdorferi s.l. showed a response to all parameters including site identity, was positively correlated with habitat patch size, and negatively correlated with proximity to water (Fig. 2a and b), Similarly, Haemoproteus infection prevalence increased when in closer proximity to water (Fig. 2b) but was statistically independent of fragment size. Model coefficients are provided in Additional File 1: Table S3.

Fig. 2
figure 2

Plots of significant model predictors. Line plots show response of infection prevalence of B. burgdorferi s.l. (orange) and Haemoproteus (blue) to geographic and biotic environmental characteristics. SCM includes a habitat size and b proximity to fresh water. ACM includes c diet guild and d foraging substrate. TCM includes e diversity of non-rodent communities, and f diversity of rodent communities

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Total community composition did not change Haemoproteus infection prevalence, but B. burgdorferi s.l. infections were significantly correlated with mammal communities (Table 1, TCM). Both rodent species richness (Fig. 2e) and non-rodent mammal species richness (Fig. 2f) were positively correlated with B. burgdorferi s.l. infection prevalence. Avian community richness did not correlate with infection prevalence of either pathogen.

Only Haemoproteus infection prevalence was strongly affected by individual avian characteristics (Table 1, ACM). To determine individual susceptibility of the different bird species sampled, an initial model was run to determine if the probability of infection prevalence changed when considering sex, age, body condition, nesting substrate, foraging substrate, and primary diet composition. Of these, sex, diet (Fig. 2c), and foraging substrate (Fig. 2d) were significant and were shown to contribute to risk of Haemoproteus infections. Borrelia burgdorferi s.l. infection prevalence did not correspond with any of the examined host characteristics.

Pathogen lineage diversity

Across all sites, there were a total of 13 unique lineages (determined by a difference > 4 bp in the cyt b gene sequence) of haemosporidian parasites. Eleven of these lineages have sequences previously recorded and are presented with previously listed lineage names and accession numbers (Additional file 1: Table S2). The remaining two lineages differ from recorded lineages by over 1% or 4 bp, suggesting these could represent novel lineages. These include Haemoproteus spp. SPIPSA01 (GenBank accession number: PQ765730), found in a lesser goldfinch (Spinus psaltria) and Haemoproteus spp. JUHYE26 (GenBank accession number: PQ765731), found in a dark-eyed junco. B. burgdorferi species in this study primarily consist of B. burgdorferi sensu stricto and one confirmed B. bissettiae infection detected. Four hosts were confirmed to be infected with B. burgdorferi s.l. but species identification could not be performed.

Discussion

Disease prevalence is, in part, the result of how pathogens respond to environmental changes. In the case of vector-borne pathogens, infection prevalence should vary when pathogens demonstrate unique life histories. To this end, our study focused on determining what site characteristics are most likely to result in infection hotspots. We compared the prevalence of two unrelated vector-borne pathogens, B. burgdorferi s.l. and Haemoproteus, within the avian community in northern California. While some site characteristics correlated with differences in infection prevalence for both pathogens, community composition showed pathogen-specific variation.

For Haemoproteus spp., infections with these pathogens are transmitted within the avian hosts, Culicoides vector complex [50,51,52]. Given the relative specialization of the Haemoproteus-avian disease system, we expected to see infection prevalence respond to the avian host community composition. This was partially consistent with our results, as infection prevalence was higher in specific guilds and differed on the basis of diets (Fig. 2C, D). Ground foragers and granivorous species had the highest infection prevalence, likely the result of increased accessibility of these birds to the vectors compared with other guilds [53, 54]. However, it should be noted that avian species richness within a habitat was not predictive of Haemoproteus infection prevalence. This suggests that the ecological niche of a bird, rather than overall community composition, is more important for predicting whether birds become infected. This conclusion is consistent with results reported in other systems [17, 53, 55, 56].

The infection prevalence of Haemoproteus was positively correlated with proximity to water. This was consistent with our initial hypothesis, in which we expected areas closest to water would have the highest Haemoproteus infection prevalence. As water availability is necessary for the biting midge life cycle [21], we expected that proximity to water would increase vector abundance and subsequently increase Haemoproteus infection prevalence.

Environmental factors that affect host communities had a weaker impact on Haemoproteus infection prevalence. We did not find a connection between habitat size and Haemoproteus infection prevalence. This was expected as habitat size should impact host communities, specifically host species richness, not necessarily vector abundance [27]. When evaluating Haemoproteus lineages, many were previously reported in a study conducted in Alaska [57]. The significant environmental differences between California and Alaska highlight that the distribution of Haemoproteus pathogens is more likely regulated by host species rather than by broader environmental conditions. Collectively, our results suggest that Haemoproteus infection prevalence is regulated by host species and potentially vector communities rather than abiotic characteristics or community-level variations.

Our second pathogen of interest was B. burgdorferi s.l. This bacterial pathogen is locally transmitted by several ixodid ticks, notably I. pacificus, that feed on a wide range of blood meal hosts [26, 58]. With this large pool of susceptible hosts, we expected to observe a positive correlation between B. burgdorferi s.l. and host community composition. We did find that infection prevalence was positively correlated with mammalian species richness, for both rodent and non-rodent community richness. However, there was no correlation with avian community composition. The lack of correlation between avian community composition and B. burgdorferi s.l. supports the idea that birds have a relatively marginal role in Lyme disease transmission within this habitat [59]. Unlike mammals, and especially rodents, birds are not primary reservoirs of B. burgdorferi s.l.; therefore, even as bird communities composition changes, infection prevalence is expected to remain consistent [26, 60, 61].

When examining abiotic habitat characteristics, we expected infection prevalence of B. burgdorferi s.l. to increase in higher quality habitats. This hypothesis was supported, as we found that birds sampled from larger habitats and habitats near water had a higher prevalence of B. burgdorferi s.l. Although it is difficult to disentangle the effects of habitat disturbance from the effects on community composition, we can provide some insight on the basis of our results. We propose that the increase in B. burgdorferi s.l. infection prevalence in response to proximity to water is most likely related to the dependence of I. pacificus on specific humidity. However, a future study could determine if the presence of water correlates with behavioral changes in birds [62, 63] and whether this alters pathogen transmission. The role of habitat patch size is especially complex owing to its impacts on species diversity, abundance, and interactions [27, 28]. Of these, we could only examine diversity and abundance, and we found that species abundance, whether avian or mammalian, was not significantly correlated with B. burgdorferi s.l. infection prevalence in birds.

Although additional studies are necessary, previous literature suggests that increased biodiversity can have a nuanced role in maintaining B. burgdorferi s.l. within this system [36, 64]. One prevailing hypothesis known as the “dilution effect” posits that increased species diversity may decrease pathogen infection prevalence by increasing the proportion of noncompetent reservoir hosts and decreasing the proportion of highly competent reservoir hosts [65, 66]. Nevertheless, there is mixed empirical evidence across systems regarding the role of diversity in pathogen transmission [67]. While the original idea of the dilution effect was first proposed in the Lyme disease system in the northeastern USA [65, 68], other studies that involved highly fragmented landscapes in the eastern [69] and western USA [36] have found a positive relationship between increasing mammalian diversity and Lyme disease risk. This variability and the differing community assemblies in regional Lyme disease systems could explain the results found in our study. These results emphasize the complexity of studying Lyme disease and highlight the need for ongoing studies into this zoonotic pathogen.

Our study was based on a relatively small sample size that consisted of various bird species. To account for this limitation, we analyzed the data with a focus on one of three broad categories: site, bird characteristics, and community composition. However, many of the variables within these categories were highly correlated and could have obscured some of the mechanisms driving the patterns. Of these categories, only the result of our SCM was relatively robust, showing the same result when a negative binomial model was performed (SI Table 3). With future studies, it can be possible to verify and expand on these initial findings.

The lack of information on haemosporidian vectors is critical, but particularly challenging to obtain. Studies on the specific vectors in California that transmit Haemoproteus are sparse but based on broader studies, and the general life history of biting midges (genus: Culicoides) has suggested that water is necessary to maintain the larval stages and could subsequently be responsible for the increase in Haemoproteus infection prevalence [21, 51, 70,71,72,73]. Fully determining whether the correlation between water and Haemoproteus infection prevalence is the result of an increase in vector populations or due to increased concentration of hosts around a body of water requires further examination. In the case of B. burgdorferi s.l., abundance of infected nymphal ticks was found to correlate with infection prevalence, further emphasizing the importance of data on vectors for these disease systems [24]. Clearly, the role of vectors is an aspect that warrants further research.

An important distinction is that our study examines infection prevalence, but not transmission. While age was included as one of the factors in our model, the low parasitemia observed and low likelihood of obtaining wild birds during the acute infection stage [14] suggests that many birds were previously infected. This distinction is especially relevant for Haemoproteus, as the B. burgdorferi s.l. infections are likely locally acquired [24, 74]. A related concern is that birds are highly mobile, which can complicate determination of where infections are acquired. While connectivity between sites by movement was not directly assessed within our study, there were no instances of recapturing birds across study sites, but this does not discount the possibility of annual movement between sites. In the case of our most commonly captured bird, the dark-eyed junco, the distance between sites exceeded the projected home range sizes 7.97 ha during the breeding season [37]. Bird behaviors, such as feeding and general proximity to the ground, may play a role in infection probability. Additionally, while mobility could impact our results, these should result in increased homogenization that would have reduced our ability to detect differences between sites. Last, while our results captured the locations of bodies of water during the study, further research should examine possible effects of seasonal fluctuations in water availability.

Conclusions

Human-mediated habitat changes are increasing and, as a result, we are observing downstream consequences that are altering ecological communities. Although these habitat changes are expected to increase the homogeneity of bird communities, landscape mosaics present intrinsic and extrinsic factors that inform prevalence patterns of other wildlife and vector populations. Such combined effects are expected to have cascading effects on the dynamics of avian diseases. For example, we determined that Haemoproteus was impacted by avian host communities and water availability, consistent with other studies. In addition, as one of the few studies exploring the relationship between local bird communities and B. burgdorferi s.l., we found that mammal communities and habitat quality are important for the maintenance of this pathogen. Additionally, the observed differences in predictors between pathogens highlights that blanket vector mediation strategies may not be sufficient to regulate unique pathogens. Whether these hosts and pathogens continue to maintain their current patterns or manage to evolve in response to habitat changes could prove vital for both human and ecological health, but by prioritizing regions that are likely to be hotspots, we can monitor and prepare for these changes.

Availability of data and materials

The datasets supporting the conclusions of this article are included within the article and its additional files.

Abbreviations

B. burgdorferi s.l.:

Borrelia burgdorferi sensu lato

SCM:

Site characteristics model

ACM:

Avian community model

TCM:

Total community model

References

  1. Pérez-Rodríguez A, Khimoun A, Ollivier A, Eraud C, Faivre B, Garnier S. Habitat fragmentation, not habitat loss, drives the prevalence of blood parasites in a Caribbean passerine. Ecography. 2018;41:1835–49.

    Article  Google Scholar 

  2. Li D, Yang Y, Xia F, Sun W, Li X, Xie Y. Exploring the influences of different processes of habitat fragmentation on ecosystem services. Landsc Urban Plan. 2022;227:104544.

    Article  Google Scholar 

  3. Aronson MFJ, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, et al. A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc R Soc B. 2014;281:20133330.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Sandström UG, Angelstam P, Mikusiński G. Ecological diversity of birds in relation to the structure of urban green space. Landsc Urban Plan. 2006;77:39–53.

    Article  Google Scholar 

  5. Ortega-Álvarez R, MacGregor-Fors I. Living in the big city: effects of urban land-use on bird community structure, diversity, and composition. Landsc Urban Plan. 2009;90:189–95.

    Article  Google Scholar 

  6. Imai H, Nakashizuka T. Environmental factors affecting the composition and diversity of avian community in mid-to-late breeding season in urban parks and green spaces. Landsc Urban Plan. 2010;96:183–94.

    Article  Google Scholar 

  7. Rosenberg KV, Dokter AM, Blancher PJ, Sauer JR, Smith AC, Smith PA, et al. Decline of the North American avifauna. Science. 2019;366:120–4.

    Article  PubMed  Google Scholar 

  8. McKinney ML. Urbanization as a major cause of biotic homogenization. Biol Conserv. 2006;127:247–60.

    Article  Google Scholar 

  9. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403:853–8.

    Article  PubMed  Google Scholar 

  10. Dobson AP, Rodriguez JP, Roberts WM, Wilcove DS. Geographic distribution of endangered species in the United States. Science. 1997;275:550–3.

    Article  PubMed  Google Scholar 

  11. Warner RE. The role of introduced diseases in the extinction of the endemic Hawaiian Avifauna. The Condor. 1968;70:101–20.

    Article  Google Scholar 

  12. Atkinson CT, Utzurrum RB, Lapointe DA, Camp RJ, Crampton LH, Foster JT, et al. Changing climate and the altitudinal range of avian malaria in the Hawaiian Islands—An ongoing conservation crisis on the island of Kaua’i. Glob Change Biol. 2014;20:2426–36.

    Article  Google Scholar 

  13. Liao W, Atkinson CT, LaPointe DA, Samuel MD. Mitigating future avian malaria threats to hawaiian forest birds from climate change. PLoS ONE. 2017;12:e0168880.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Valkiūnas G. Avian malaria parasites and other haemosporidia. Boca Raton: CRC Press; 2005. p. 932.

    Google Scholar 

  15. Hernández-Lara C, González-García F, Santiago-Alarcon D. Spatial and seasonal variation of avian malaria infections in five different land use types within a neotropical montane forest matrix. Landsc Urban Plan. 2017;157:151–60.

    Article  Google Scholar 

  16. Hernández-Lara C, Carbó-Ramírez P, Santiago-Alarcon D. Effects of land use change (rural-urban) on the diversity and epizootiological parameters of avian Haemosporida in a widespread neotropical bird. Acta Trop. 2020;209:105542.

    Article  PubMed  Google Scholar 

  17. Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, et al. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region: host-specificity of Avian Haematozoa. Mol Ecol. 2004;13:3829–44.

    Article  PubMed  Google Scholar 

  18. Sehgal RNM, Buermann W, Harrigan RJ, Bonneaud C, Loiseau C, Chasar A, et al. Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird. Proc R Soc B. 2011;278:1025–33.

    Article  PubMed  Google Scholar 

  19. Gonzalez-Quevedo C, Davies RG, Richardson DS. Predictors of malaria infection in a wild bird population: landscape-level analyses reveal climatic and anthropogenic factors. J Anim Ecol. 2014;83:1091–102.

    Article  PubMed  Google Scholar 

  20. Ferraguti M, Martínez-de la Puente J, Bensch S, Roiz D, Ruiz S, Viana DS, et al. Ecological determinants of avian malaria infections: an integrative analysis at landscape, mosquito and vertebrate community levels. J Anim Ecol. 2018;87:727–40.

    Article  PubMed  Google Scholar 

  21. Pfannenstiel RS, Mullens BA, Ruder MG, Zurek L, Cohnstaedt LW, Nayduch D. Management of North American Culicoides biting midges: current knowledge and research needs. Vector Borne Zoonotic Dis. 2015;15:374–84.

    Article  PubMed  Google Scholar 

  22. Bukauskaitė D, Iezhova TA, Ilgūnas M, Valkiūnas G. High susceptibility of the laboratory-reared biting midges Culicoides nubeculosus to Haemoproteus infections, with review on Culicoides species that transmit avian haemoproteids. Parasitology. 2019;146:333–41.

    Article  PubMed  Google Scholar 

  23. Newman EA, Eisen L, Eisen RJ, Fedorova N, Hasty JM, Vaughn C, et al. Borrelia burgdorferi sensu lato spirochetes in wild birds in Northwestern California: associations with ecological factors, bird behavior and tick infestation. PLoS ONE. 2015;10:e0118146.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Lilly M, Amaya-Mejia W, Pavan L, Peng C, Crews A, Tran N, et al. Local community composition drives avian Borrelia burgdorferi infection and tick infestation. Vet Sci. 2022;9:55.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Slowik TJ, Lane RS. Birds and their ticks in Northerwestern California: minimal contribution to Borrelia burgdorferi enzootiology. Parasitol. 2001;87:755–61.

    Article  Google Scholar 

  26. Castro MB, Wright SA. Vertebrate hosts of Ixodes pacificus (Acari: Ixodidae) in California. J Vector Ecol. 2007;32:140–9.

    Article  PubMed  Google Scholar 

  27. Crooks KR, Suarez AV, Bolger DT. Avian assemblages along a gradient of urbanization in a highly fragmented landscape. Biol Conserv. 2004;115:451–62.

    Article  Google Scholar 

  28. Lawrence A, O’Connor K, Haroutounian V, Swei A. Patterns of diversity along a habitat size gradient in a biodiversity hotspot. Ecosphere. 2018;9:e02183.

    Article  Google Scholar 

  29. Guo F, Bonebrake TC, Gibson L. Land-use change alters host and vector communities and may elevate disease risk. EcoHealth. 2019;16:647–58.

    Article  PubMed  Google Scholar 

  30. Troughton DR, Levin ML. Life cycles of seven Ixodid tick species (Acari: Ixodidae) under standardized laboratory conditions. J Med Entomol. 2007;44:732–40.

    Article  PubMed  Google Scholar 

  31. Šujanová A, Čužiová Z, Václav R. The infection rate of bird-feeding Ixodes ricinus ticks with Borrelia garinii and B. valaisiana varies with host haemosporidian infection status. Microorganisms. 2022;11:60.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Heylen D, Matthysen E, Fonville M, Sprong H. Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes rinicus ticks. Environ Microbiol. 2014;16:2859–68.

    Article  PubMed  Google Scholar 

  33. Heylen DJA, Müller W, Vermeulen A, Sprong H, Matthysen E. Virulence of recurrent infestations with Borrelia-infected ticks in a Borrelia-amplifying bird. Sci Rep. 2015;5:16150.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Groff TC, Lorenz TJ, Crespo R, Iezhova T, Valkiūnas G, Sehgal RNM. Haemoproteosis lethality in a woodpecker, with molecular and morphological characterization of Haemoproteus velans (Haemosporida, Haemoproteidae). IJP:PAW. 2019;10:93–100.

    PubMed  PubMed Central  Google Scholar 

  35. Swei A, Meentemeyer R, Briggs CJ. Influence of abiotic and environmental factors on the density and infection prevalence of Ixodes pacificus (Acari: Ixodidae) with Borrelia burgdorferi. J Med Entomol. 2011;48:20–8.

    Article  PubMed  Google Scholar 

  36. Shaw G, Lilly M, Mai V, Clark J, Summers S, Slater K, et al. The roles of habitat isolation, landscape connectivity and host community in tick-borne pathogen ecology. R Soc Open Sci. 2024;11:240837.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Chandler CR, Ketterson ED, Nolan V, Ziegenfus C. Effects of testosterone on spatial activity in free-ranging male dark-eyed juncos, Junco hyemalis. Anim Behav. 1994;47:1445–55.

    Article  Google Scholar 

  38. Pyle P, Howe SNG, Ruck S. Identification guide to North American birds: a compendium of information on identifying, ageing, and sexing “near-passerines” and passerines in the hand. Bolinas: Slate Creek Press; 1997.

    Google Scholar 

  39. Sehgal RNM, Jones HI, Smith TB. Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Mol Ecol. 2001;10:2319–27.

    Article  PubMed  Google Scholar 

  40. Sehgal RNM, Lovette IJ. Molecular evolution of three avian neurotrophin genes: implications for proregion functional constraints. J Mol Evol. 2003;57:335–42.

    Article  PubMed  Google Scholar 

  41. Waldenström J, Bensch S, Hasselquist D, Östman Ö. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parastiol. 2004;90:191–4.

    Article  Google Scholar 

  42. Postic D, Assous MV, Grimont PAD, Baranton G. Diversity of Borrelia burgdorfeii sensu lato evidenced by restriction fragment length polymorphism of njf (5S)-rrl (23s) intergenic spacer amplicons. Int J Syst Bacteriol. 1994;44:743–52.

    Article  PubMed  Google Scholar 

  43. Lane RS, Steinlein DB, Mun J. Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest. J Med Entomol. 2004;41:239–48.

    Article  PubMed  Google Scholar 

  44. Lee LH, Lee KH. Application of the polymerase chain reaction for the diagnosis of fowl poxvirus infection. J Virol Methods. 1997;63:113–9.

    Article  Google Scholar 

  45. Hellgren O, Waldenström J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802.

    Article  PubMed  Google Scholar 

  46. Walther EL, Carlson JS, Cornel A, Morris BK, Sehgal RNM. First molecular study of prevalence and diversity of avian haemosporidia in a Central California songbird community. J Ornithol. 2016;157:549–64.

    Article  Google Scholar 

  47. O’Connell TJ, Jackson LE, Brooks RP. Bird guilds as indicators of ecological condition in the central Appalachians. Ecol Appl. 2000;10:1706–21.

    Article  Google Scholar 

  48. González-Salazar C, Martínez-Meyer E, López-Santiago G. A hierarchical classification of trophic guilds for North American birds and mammals. Rev Mexicana Biodivers. 2014;85:931–41.

    Article  Google Scholar 

  49. Billerman SM, Keeny BK, Rodewald PG. Birds of the world. Ithaca: Cornell Laboratory of Ornithology; 2020.

    Book  Google Scholar 

  50. Videvall E, Bensch S, Ander M, Chirico J, Sigvald R, Ignell R. Molecular identification of bloodmeals and species composition in Culicoides biting midges. Med Vet Entomol. 2013;27:104–12.

    Article  PubMed  Google Scholar 

  51. Tomazatos A, Jöst H, Schulze J, Spînu M, Schmidt-Chanasit J, Cadar D, et al. Blood-meal analysis of Culicoides (Diptera: Ceratopogonidae) reveals a broad host range and new species records for Romania. Parasit Vectors. 2020;13:79.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Santiago-Alarcon D, Havelka P, Pineda E, Segelbacher G, Schaefer HM. Urban forests as hubs for novel zoonosis: blood meal analysis, seasonal variation in Culicoides (Diptera: Ceratopogonidae) vectors, and avian haemosporidians. Parasitology. 2013;140:1799–810.

    Article  PubMed  Google Scholar 

  53. Hellard E, Cumming GS, Caron A, Coe E, Peters JL. Testing epidemiological functional groups as predictors of avian haemosporidia patterns in southern Africa. Ecosphere. 2016;7:e01225.

    Article  Google Scholar 

  54. Gupta P, Vishnudas CK, Robin VV, Dharmarajan G. Host phylogeny matters: examining sources of variation in infection risk by blood parasites across a tropical montane bird community in India. Parasit Vectors. 2020;13:536.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Clark NJ, Clegg SM, Lima MR. A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. Int J Parasitol. 2014;44:329–38.

    Article  PubMed  Google Scholar 

  56. Olsson-Pons S, Clark NJ, Ishtiaq F, Clegg SM. Differences in host species relationships and biogeographic influences produce contrasting patterns of prevalence, community composition and genetic structure in two genera of avian malaria parasites in southern Melanesia. J Anim Ecol. 2015;84:985–98.

    Article  PubMed  Google Scholar 

  57. Oakgrove KS, Harrigan RJ, Loiseau C, Guers S, Guers B, Sehgal RNM. Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. Int J Parasitol. 2014;44:717–27. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.ijpara.2014.04.011.

    Article  PubMed  Google Scholar 

  58. Brown RN, Lane RS. Lyme disease in California: a novel enzootic transmission cycle of Borrelia burgdorferi. Science. 1992;256:1439–42.

    Article  PubMed  Google Scholar 

  59. Wright SA, Tucker JR, Donohue AM, Castro MB, Kelley KL, Novak MG, et al. Avian hosts of Ixodes pacificus (Acari: Ixodidae) and the detection of Borrelia burgdorferi in larvae feeding on the oregon junco. J Med Entomol. 2011;48:852–9.

    Article  PubMed  Google Scholar 

  60. Norte AC, Lobato DNC, Braga EM, Antonini Y, Lacorte G, Gonçalves M, et al. Do ticks and Borrelia burgdorferi s.l. constitute a burden to birds? Parasitol Res. 2013;112:1903–12.

    Article  PubMed  Google Scholar 

  61. Dizon C, Lysyk TJ, Couloigner I, Cork SC. Ecology and epidemiology of Lyme disease in western North America. Zoonotic Dis. 2023;3:20–37.

    Article  Google Scholar 

  62. Mayer M, Natusch D, Frank S. Water body type and group size affect the flight initiation distance of European waterbirds. PLoS ONE. 2019;14:e0219845.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Barbosa KVDC, Rodewald AD, Ribeiro MC, Jahn AE. Noise level and water distance drive resident and migratory bird species richness within a Neotropical megacity. Landsc Urban Plan. 2020;197:103769.

    Article  Google Scholar 

  64. Swei A, Ostfeld RS, Lane RS, Briggs CJ. Impact of the experimental removal of lizards on Lyme disease risk. Proc R Soc B. 2011;278:2970–8.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Schmidt KA, Ostfeld RS. Biodiversity and the dilution effect in disease ecology. Ecology. 2001;82:609–19.

    Article  Google Scholar 

  66. Keesing F, Ostfeld RS. Dilution effects in disease ecology. Ecol Lett. 2021;24:2490–505.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Rohr JR, Civitello DJ, Halliday FW, Hudson PJ, Lafferty KD, Wood CL, et al. Towards common ground in the biodiversity–disease debate. Nat Ecol Evol. 2019;4:24–33.

    Article  PubMed  PubMed Central  Google Scholar 

  68. LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. PNAS. 2003;100:567–71.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Bastard J, Gregory N, Fernandez P, Mincone M, Card O, VanAcker MC, et al. Cascading effects of mammal host community composition on tick vector occurrence at the urban human–wildlife interface. Ecosphere. 2024;15:e4957.

    Article  Google Scholar 

  70. Holbrook FR, Tabachnick WJ. Culicoides variipennis (Diptera: Ceratopogonidae) complex in California. J Med Entomol. 1995;32:413–9.

    Article  PubMed  Google Scholar 

  71. Bernotienė R, Žiegytė R, Vaitkutė G, Valkiūnas G. Identification of a new vector species of avian haemoproteids, with a description of methodology for the determination of natural vectors of haemosporidian parasites. Parasit Vectors. 2019;12:307.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Martin E, Chu E, Shults P, Golnar A, Swanson DA, Benn J, et al. Culicoides species community composition and infection status with parasites in an urban environment of east central Texas, USA. Parasit Vectors. 2019;12:39.

    Article  PubMed  PubMed Central  Google Scholar 

  73. McGregor BL, Shults PT, McDermott EG. A review of the vector status of North American Culicoides (Diptera: Ceratopogonidae) for bluetongue virus, epizootic hemorrhagic disease virus, and other arboviruses of concern. Curr Trop Med Rep. 2022;9:130–9.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Asghar M, Hasselquist D, Bensch S. Are chronic avian haemosporidian infections costly in wild birds? J Avian Biol. 2011;42:530–7.

    Article  Google Scholar 

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Acknowledgements

We thank and acknowledge the contributions of various members of the Sehgal and Swei labs for their assistance in conducting data collection. Graphical abstract was created in BioRender. Amaya-Mejia (2025) https://BioRender.com/q13e545.

Funding

This research was funded by the National Science Foundation grant numbers 175037 and 1745411; National Science Foundation Graduate Research Fellowship under grant number 10328000, and the Genentech Foundation Scholarship. L.P. and R.D. were supported by Stanford University’s unrestricted funds.

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Author notes

  1. Wilmer Amaya-Mejia and Lucas Pavan have contributed equally to this work.

Authors and Affiliations

  1. University of California, Los Angeles, California, USA

    Wilmer Amaya-Mejia

  2. Stanford University, Stanford, California, USA

    Lucas Pavan & Rodolfo Dirzo

  3. Columbia University, New York, New York, USA

    Marie Lilly

  4. San Francisco State University, San Francisco, California, USA

    Wilmer Amaya-Mejia, Marie Lilly, Andrea Swei & Ravinder N. M. Sehgal

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  1. Wilmer Amaya-Mejia
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  6. Ravinder N. M. Sehgal
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Contributions

W.A.M. and L.P. contributed to data collection, including field work, laboratory data analysis, and writing of the manuscript. M.L. contributed to data collection. R.D., A.S., and R.S. provided guidance throughout the preparation, conceptualization of the project, providing funding, permits, and data availability and assisted with writing and editing the manuscript.

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Correspondence to Wilmer Amaya-Mejia or Lucas Pavan.

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The study was conducted with approval by the Institutional Review Board of San Francisco State University IACUC protocol code AU19-01R2 and by the Institutional Review Board of Stanford University IACUC protocol code 337733.

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Supplementary Information

13071_2025_6742_MOESM1_ESM.xlsx

Additional file 1: Table S1. Site vegetation survey summary. Table S2. Detailed individual-level infection, morphological, and guild characteristics. Table S3. Detailed model coefficients and negative binomial regression output

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Amaya-Mejia, W., Pavan, L., Lilly, M. et al. Determinants of vector-borne avian pathogen occurrence in a mosaic of habitat fragmentation in California. Parasites Vectors 18, 110 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13071-025-06742-x

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Parasites & Vectors

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