skip to main content


Title: Global drivers of avian haemosporidian infections vary across zoogeographical regions
Abstract Aim

Macroecological analyses provide valuable insights into factors that influence how parasites are distributed across space and among hosts. Amid large uncertainties that arise when generalizing from local and regional findings, hierarchical approaches applied to global datasets are required to determine whether drivers of parasite infection patterns vary across scales. We assessed global patterns of haemosporidian infections across a broad diversity of avian host clades and zoogeographical realms to depict hotspots of prevalence and to identify possible underlying drivers.

Location

Global.

Time period

1994–2019.

Major taxa studied

Avian haemosporidian parasites (generaPlasmodium,Haemoproteus,LeucocytozoonandParahaemoproteus).

Methods

We amalgamated infection data from 53,669 individual birds representing 2,445 species world‐wide. Spatio‐phylogenetic hierarchical Bayesian models were built to disentangle potential landscape, climatic and biotic drivers of infection probability while accounting for spatial context and avian host phylogenetic relationships.

Results

Idiosyncratic responses of the three most common haemosporidian genera to climate, habitat, host relatedness and host ecological traits indicated marked variation in host infection rates from local to global scales. Notably, host ecological drivers, such as migration distance forPlasmodiumandParahaemoproteus, exhibited predominantly varying or even opposite effects on infection rates across regions, whereas climatic effects on infection rates were more consistent across realms. Moreover, infections in some low‐prevalence realms were disproportionately concentrated in a few local hotspots, suggesting that regional‐scale variation in habitat and microclimate might influence transmission, in addition to global drivers.

Main conclusions

Our hierarchical global analysis supports regional‐scale findings showing the synergistic effects of landscape, climate and host ecological traits on parasite transmission for a cosmopolitan and diverse group of avian parasites. Our results underscore the need to account for such interactions, in addition to possible variation in drivers across regions, to produce the robust inference required to predict changes in infection risk under future scenarios.

 
more » « less
Award ID(s):
2001213
NSF-PAR ID:
10360093
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  more » ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;   « less
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Global Ecology and Biogeography
Volume:
30
Issue:
12
ISSN:
1466-822X
Page Range / eLocation ID:
p. 2393-2406
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Aim

    Characterizing macroecological patterns in biodiversity is key to improve our understanding of community assembly. Global biodiversity for many taxa follows a latitudinal gradient, with increased diversity in tropical latitudes. Less is known about global parasite biodiversity, inhibiting our ability to predict how global change will impact parasitic disease emergence. Using distribution and phylogenetic data for 2,386 avian haemosporidian blood parasites (generaPlasmodium,HaemoproteusandLeucocytozoon), I assessed how contemporary and historical drivers influence the composition of parasite communities worldwide.

    Location

    Global.

    Time period

    Current.

    Major taxa studied

    Haemosporidian blood parasites.

    Methods

    Parasite distribution and cytochrome bsequence data were accessed from an open‐source database. Bayesian phylogenetic tree distributions were constructed for each parasite genus using two substitution models to capture uncertainty. Hierarchical regressions assessed effects of environmental variation, latitude and phylogenetic β‐diversity (βdiv; a proxy for phylogenetic uniqueness) on the diversity and asymmetry of parasite communities around the globe.

    Results

    I uncovered biodiversity hotspots and identified broad variation in global diversity patterns among parasite genera. Community diversity increased with increasing phylogenetic uniqueness for all three parasite genera; however, these diverse and unique regions did not consistently occur in the tropics. I found no evidence of a latitudinal diversity gradient, and support for a latitudinal gradient in community phylogenetic asymmetry was weak.

    Main conclusions

    Global variation in avian haemosporidian phylogenetic diversity does not reflect a latitudinal gradient. Instead, parasite biogeography may reflect fundamental differences in host‐switching tendencies or the timing of avian evolutionary radiations. Examining the interplay between shared evolutionary history and phylogenetic diversity can provide important insights into the drivers of parasite biodiversity at global scales.

     
    more » « less
  2. Abstract Aim

    We compared the parasite assemblages of over‐wintering migratory birds and permanent residents on the wintering grounds. We determined whether parasite sharing between migratory and resident birds is influenced by host phylogenetic relatedness. We then inferred whether migratory birds transport haemosporidian parasite lineages between the breeding and wintering grounds.

    Location

    Sierra de Bahoruco National Park, Dominican Republic, Hispaniola.

    Taxa

    Migratory and resident birds (primarily Aves: Passeriformes) and their haemosporidian parasites (order Haemosporida,Plasmodium,HaemoproteusandParahaemoproteus).

    Methods

    We used mist nets to capture birds in thorn scrub, broadleaf dry forests and pine forests during midwinter. We used molecular methods to recognize haemosporidian parasites in blood samples, and genotyped infections based on the nucleotide differences in a region of the parasite cytochromebgene.

    Results and Main Conclusion

    We identified 505 infections by 32 haemosporidian parasite lineages in 1,780 blood samples from 37 resident species, and in 901 blood samples from 14 overwintering migratory species, over five years at the same sites. Infection prevalence varied among migratory species from zero to 13%, whereas infection prevalence among resident species ranged up to 77%. Host relatedness did not predict parasite assemblage similarity. We discuss four hypotheses for the rarity of haemosporidian infections in migratory birds during winter, and for the infrequency of parasite sharing between migratory and resident birds: (a) relative abundance and host preferences of dipteran vectors lower parasite transmission to migratory birds; (b) parasite lineages adapted to infect endemic Caribbean hosts are unable to infect migratory species; (c) the physiology of migratory birds after migration and during winter reduces parasite survival; and (d) infected individuals suffer more pronounced mortality rates during migration. We highlight the link between host–parasite coevolution and the physiological adaptations associated with avian seasonal migration.

     
    more » « less
  3. Abstract Background

    The prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.

    Methods

    Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate the prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.

    Results

    We estimated the prevalence and diversity of avian Haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open-cup nesters have higherHaemoproteusprevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higherHaemoproteusprevalence compared to other host species.Plasmodiumprevalence was relatively low (5%), consistent with the idea that competent vectors may be rare at high altitudes.

    Conclusions

    Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host–parasite relationships of blood parasites and their avian hosts.

    Graphical Abstract 
    more » « less
  4. Abstract

    Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector‐transmitted parasites.

    Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity ofLeucocytozoon(an avian blood parasite) at site and species levels across the New World.

    To explore spatial patterns in infection probability and lineage diversity forLeucocytozoonparasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high‐resolution satellite remote‐sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly.

    Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence ofLeucocytozoonparasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected withLeucocytozoonincreased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes.

    Whereas temperature partially constrainsLeucocytozoondiversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, forLeucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector‐transmitted parasites. Unlike other vector‐transmitted diseases, our results show thatLeucocytozoondiversity and prevalence will likely decrease with warming temperatures.

     
    more » « less
  5. Abstract Aim

    The role of migratory birds in the spread of parasites is poorly known, in part because migratory strategies and behaviours potentially affecting transmission are not easy to study. We investigated the dynamics of infection by blood parasites through the annual cycle of a long‐distance Nearctic–Neotropical migratory songbird to examine the role of this species in dispersing parasites between continents.

    Location

    The Americas.

    Taxon

    Grey‐cheeked Thrush (Catharus minimus, Aves, Passeriformes, Turdidae), Birds.

    Methods

    We used molecular and microscopy screening of haemosporidian parasites (Plasmodium,Haemoproteus, andLeucocytozoon) to examine the prevalence, distribution, and diversity of lineages through the annual cycle (breeding, migration, and wintering) of the grey‐cheeked thrush in North and Central America, Santa Marta mountains, the Andes, and the Amazon. We aimed to identify transmission areas, to examine the degree of sharing of haemosporidian lineages with resident birds in various areas and to assess the potential role of immunologically naïve juvenile individuals in parasite transmission.

    Results

    Prevalence and lineage diversity of haemosporidians varied significantly over time, being higher during breeding and fall and spring migration, and declining during wintering. Grey‐cheeked thrush shared few parasite lineages with tropical resident birds and slightly more lineages with other migratory and resident boreal species. We detected gametocytes in blood during spring migration stopover, but these were of lineages not found in resident tropical birds, indicating relapses of parasites transmitted elsewhere. Transmission likely occurs mostly on the breeding grounds, where juveniles and adults carried lineages restricted to closely related species of thrushes and other species of boreal birds.

    Main conclusions

    Long‐distance migratory songbirds are likely not important dispersers of blood parasites because there are ecological and evolutionary barriers to the interchange of parasites across vastly separated areas. Further work with thorough spatial and temporal sampling across other species, and considering the role of vectors, is necessary to understand the ecological and evolutionary factors explaining the distribution of parasites over broad scales.

     
    more » « less