Haemosporidian parasites may impact avian health and are subject to shifts in distribution and abundance with changing ecologic conditions. Therefore, understanding variation in parasite prevalence is important for evaluating biologically meaningful changes in infection patterns and associated population level impacts. Previous research in western Alaska, US, indicated a possible increase in Leucocytozoon spp. infection between Emperor Geese (Anser canagicus) sampled in 1996 (<1%, n=134) and during 2011–12 (19.9%, 95% confidence interval [CI]: 3.0–36.8%, n=77); however, different detection methods were used for these estimates. Prior research in this same region identified a lack of Leucocytozoon spp. parasites (0%, n=117) in sympatrically breeding Cackling Geese (Branta hutchinsii minima) in 2011. We molecularly screened blood samples collected from sympatrically breeding Emperor and Cackling Geese in western Alaska during additional breeding seasons to better assess temporal and species-specific variation in the prevalence of blood parasites. We found similar prevalence estimates for Leucocytozoon spp. parasites in Emperor Goose blood samples collected in 1998 and 2014, suggesting consistent infection of Emperor Geese with blood parasites at these time points. Using samples from sympatric geese sampled during 2014, we found evidence for a higher incidence of parasites among Emperor Geese (20.3%, 95% CI: 11.8–32.7%) compared to Cackling Geese (3.6%, 95% CI: 1.1–11.0%), reinforcing the previous finding of species-specific differences in infection. Furthermore, we detected Leucocytozoon, Haemoproteus, and Plasmodium spp. blood parasites in unflighted goslings of both species, supporting the possible transmission of these parasites at western Alaska breeding grounds. Our results help to clarify that prevalence of Leucocytozoon spp. parasites have probably remained consistent among Emperor Geese breeding in western Alaska since the late 1990s and that this species may disproportionally harbor Leucocytozoon spp. compared to sympatrically breeding Cackling Geese.

Haemosporidians are a diverse group of single-celled, intracellular parasites that affect a wide range of vertebrates (Atkinson and van Riper 1991). Avian hosts are commonly affected by haemosporidians of the genera Leucocytozoon, Haemoproteus, and Plasmodium. These parasites are transmitted by dipteran insect vectors, with Leucocytozoon spp. being primarily transmitted by black flies, Haemoproteus spp. by mosquitoes and biting midges, and Plasmodium spp. by mosquitoes (Atkinson and van Riper 1991; Valkiunas 2005). Consequences of infection with these parasites reported in birds range from seemingly benign (Kilpatrick et al. 2006; Bensch et al. 2007; LaPointe et al. 2012) to impacts on reproductive fitness (Merino et al. 2000; Marzal et al. 2005; Asghar et al. 2015) and survival (Herman et al. 1975; Atkinson et al. 2000; Asghar et al. 2015).

Although haemosporidian infection in birds is common (Clark et al. 2018; Ellis et al. 2019), novel introductions of such parasites into naive avian populations have been documented and may be associated with population-level impacts (Warner 1968; van Riper et al. 1986). Thus, global climate change has the potential to facilitate future biologically consequential introductions of haemosporidian parasites into naive avian populations, through shifts in the ranges of parasites and their vectors to higher latitudes and elevations (Sekercioglu et al. 2008; Chen et al. 2011; Fecchio et al. 2019), lengthened breeding seasons of arthropod vectors, and improved conditions for parasite reproduction (LaPointe et al. 2010; Zamora-Vilchis et al. 2012; Loiseau et al. 2013). Additionally, changes in environmental conditions may alter the abundance of parasites at locations where they are currently uncommon (Brooks and Hoberg 2007). Such events may be more likely to occur in high-latitude regions, where the effects of climate change have been most pronounced (Kutz et al. 2009).

The Yukon-Kuskokwim Delta (YKD), a globally important wetland complex where more than a million geese congregate annually to breed, lies in one such high-latitude region within western Alaska, US. Three species of geese sympatrically breeding on the YKD have previously been sampled for haemosporidian parasites: Emperor Geese (Anser canagicus), Cackling Geese (Branta hutchinsii minima), and Black Brant (Branta bernicla nigricans). A single Leucocytozoon spp. infection was identified from 134 Emperor Goose (<1%) blood smears collected on the YKD in 1996 (Hollmén et al. 1998) in contrast to a higher prevalence estimate (19.9%, 95% confidence interval [CI]: 3.0–36.8%) for parasite infections in this same species and location, as inferred from molecular screening of whole blood samples collected during 2011–12 (n=77; Ramey et al. 2014). In the same investigation using molecular techniques, Leucocytozoon spp. infections were also detected in Black Brant (11.1%, 95% CI: 0–29.5%) sampled on the YKD during 2011–12 (n=49) but not in Cackling Geese sampled at this same locale in 2011 (n=117). Thus, previous sampling of geese on the YKD for haemosporidian parasites suggests that there may be considerable variation in prevalence among sympatrically nesting geese.

In this study, we further assessed the detection and prevalence of avian haemosporidian parasites in Emperor and Cackling Geese breeding on the YKD. Specifically, we used consistent methods to examine whether: 1) Emperor Geese sampled in 1998 had a different incidence of haemosporidian parasitic infections compared to those sampled in 2014, 2) Emperor Geese harbor a higher prevalence of haemosporidian parasites than do Cackling Geese raising broods in the same geographic area, and 3) transmission is potentially occurring within the YKD. Results of this study help to elucidate variation in haemosporidian parasite prevalence among sympatrically breeding geese on the YKD, which may inform future assessments of change in parasite distribution and abundance.

We obtained blood samples from Emperor Geese during incubation and brood rearing in 1998 and 2014, and from Cackling Geese during brood rearing in 2014, at locations adjacent to the Manokinak River (approx. 61°N, 165°W) on the YKD. Bow nets or mist nets were used to capture incubating adult female Emperor Geese. Flightless hatch year and adult geese were captured during brood rearing by herding birds into corrals. Capture and handling protocols were reviewed by the Animal Care and Use Committee at the US Geological Survey (USGS) Alaska Science Center and authorized under USGS federal bird banding permit no. 20022. Sex and age class (hatch year vs. adult) for both species were determined by plumage and cloacal examination. Whole blood was collected via jugular venipuncture and stored in Longmire buffer. Samples were kept at ambient temperature for up to ∼12 h before freezing, then remained frozen until molecular analysis.

We extracted DNA from whole blood using a DNeasy Blood and Tissue kit (Qiagen, Valencia, California, USA) following the manufacturer's protocol. To confirm successful DNA extraction, a 481-base pair fragment of the mitochondrial DNA (mtDNA) cytochrome oxidase I gene of the avian host was amplified using primers previously published in Ramey et al. (2014) and thermal-cycling conditions reported by Kerr et al. (2007). Each DNA extraction was screened three times for the presence of haematozoa using a nested PCR protocol described by Hellgren et al. (2004). A minimum of one negative control for every 24 wells was incorporated into each set of PCRs. Reactions were conducted in eight-well strip tubes with individual caps that remained closed except while loading template and reagents to prevent cross contamination. Primer sequences and amplification protocols are briefly summarized in Supplementary Material File S1. Amplicons were visualized on 0.8% agarose gels stained with Gel Red Nucleic Acid Gel Stain (Biotium, Hayward, California, USA).

Products from the PCR appearing to represent the 479-base pair cytochrome b (cyt b) mtDNA target were treated with ExoSap-IT (USB Inc., Cleveland, Ohio, USA) and sequenced with identical primers used for the PCR and with BigDye Terminator version 3.1 mix (Applied Biosystems, Foster City, California, USA) on an Applied Biosystems 3730xl automated DNA sequencer. Sequence data were cleaned and edited using DNA Dynamo (Blue Tractor Software Ltd., North Wales, UK). Sequences were then assigned to haemosporidian parasites of three genera (Leucocytozoon, Haemoproteus, or Plasmodium) using the nucleotide BLAST function available through the National Center for Biotechnology Information (NCBI; 2021). Assignment was based on the top NCBI BLAST result with a minimum max identity score of 90%. A sample was identified as positive for Leucocytozoon, Haemoproteus, or Plasmodium spp. parasites if any of the three replicate PCRs resulted in a bidirectional double-stranded target product that was verified through genetic sequencing. Samples from which single-stranded or otherwise ambiguous products resulted were considered negative. Information on cyt b mtDNA haplotypes are available in Reed et al. (2021) and NCBI GenBank (accession nos. MW574916–MW574929).

Given imperfect parasite detection (i.e., sensitivity) using our PCR-based approach, we employed occupancy modeling (MacKenzie et al. 2017) to provide estimates of detection and prevalence. We used the program MARK (White and Burnham 1999) through the RMARK package (Laake 2013) in the program R (version 4.0.2; R Core Team 2020) to build models and address the two primary study objectives (i.e., assessing temporal variation and differences between sympatric species in detection and prevalence of parasites) with separate analyses. Due to small sample size, we limited our model sets to all additive combinations of variables for prevalence (Ψ) while holding detection (ρ) to a single variable or constant. To be conservative in our inference, we did not include interactions between variables influencing prevalence (see Supplementary Material Tables S1, S2).

First, we focused on comparing results for Emperor Geese sampled in 1998 versus 2014. We assessed temporal variation in parasite detection and prevalence in Emperor Geese through a series of models incorporating covariates for age class (hatch year vs. adult), breeding stage (nesting vs. brood rearing), and year (1998 and 2014). Next, we compared results between Emperor Geese and Cackling Geese sampled in 2014. We assessed species-specific variation in detection and prevalence through a series of models incorporating covariates for species, age class, and sex. In both analyses, model fit was assessed to inform which model structures best fit the observed data. We used the Fletcher's c-hat values for the most general models in each analysis to evaluate goodness of fit and quantify appropriate variance inflation factors. These inflation values were used to create quasi-likelihood Akaike's information criterion corrected for small sample size (QAICC) for model selection. An information theoretic approach was used to determine influences on parasite prevalence and detection. Models were ranked by ΔQAICC scores and quasi-Akaike weights. The ΔQAICc scores were calculated as the difference between each model and the most parsimonious model. Detection and prevalence estimates were obtained by interpreting the most parsimonious model, unless one did not emerge, then model averaging was used to obtain unbiased point estimates and confidence intervals.

We extracted DNA from 307 blood samples collected from geese at sites on the YKD during 1998 (n=72 Emperor Geese) and 2014 (n=125 Emperor Geese, n=110 Cackling Geese) and molecularly detected Leucocytozoon, Haemoproteus, and Plasmodium spp. parasites (Table 1). Parasites of all three genera were identified in hatch year birds captured during brood drives (Table 1). The majority (45/57, 79%) of haemosporidian infections molecularly identified were assigned to the genus Leucocytozoon; therefore, the small numbers of Haemoproteus (n=7) and Plasmodium (n=6) detections were excluded from modeling efforts.

Table 1

Summary of molecular screening of whole blood samples collected from Emperor and Cackling Geese (Anser canagicus and Branta hutchinsii minima) breeding on the Yukon-Kuskokwim Delta of Alaska, USA in 1998 and 2014 for haemosporidian parasites of the genera Leucocytozoon, Haemoproteus, and Plasmodium by year, breeding stage, age class, and sex class.a

Summary of molecular screening of whole blood samples collected from Emperor and Cackling Geese (Anser canagicus and Branta hutchinsii minima) breeding on the Yukon-Kuskokwim Delta of Alaska, USA in 1998 and 2014 for haemosporidian parasites of the genera Leucocytozoon, Haemoproteus, and Plasmodium by year, breeding stage, age class, and sex class.a
Summary of molecular screening of whole blood samples collected from Emperor and Cackling Geese (Anser canagicus and Branta hutchinsii minima) breeding on the Yukon-Kuskokwim Delta of Alaska, USA in 1998 and 2014 for haemosporidian parasites of the genera Leucocytozoon, Haemoproteus, and Plasmodium by year, breeding stage, age class, and sex class.a

In our first analysis to assess temporal variation in parasite detection and prevalence between Emperor Geese sampled in 1998 and 2014, we detected moderate lack of fit in the most general model incorporating covariates for detection by sample year and for prevalence by sample year, breeding stage, and age class (Table S1). Therefore, a variance inflation factor of 1.67 was applied to the entire set of models and parameter estimation. Given the absence of a clear top model (Table S1), we used model averaging to attain unbiased point estimates and confidence intervals. Using this approach, we found model averaged point estimates of Leucocytozoon prevalence ranging from 17.8% (95% CI: 9.4–31.1%) for goslings in 2014, to 26.9% (95% CI: 14.0–45.3%) for incubating females in 1998 (Fig. 1). We also found little support for differences in the detection of Leucocytozoon parasites in Emperor Geese sampled in 1998 versus those sampled in 2014, or for variation in parasite detection and prevalence by breeding stage and age class (Fig. 1 and Table S1). Estimates of detection probability ranged between 0.72–0.77 (95% CI: 0.53–0.88) per PCR run or 0.90–>0.99 per sample when run in triplicate.

Figure 1

Detection (per replicate PCR run) and prevalence estimates with 95% confidence intervals for Leucocytozoon spp. parasites in: A. Emperor Geese (Anser canagicus) breeding on the Yukon-Kuskokwim Delta of Alaska, USA sampled during the incubation and brood-rearing periods in 1998 and 2014; and B. Emperor (EMGO) and Cackling (CACG) Geese (Branta hutchinsii minima) sympatrically breeding on the Yukon-Kuskokwim Delta sampled during the brood-rearing period in 2014 only.

Figure 1

Detection (per replicate PCR run) and prevalence estimates with 95% confidence intervals for Leucocytozoon spp. parasites in: A. Emperor Geese (Anser canagicus) breeding on the Yukon-Kuskokwim Delta of Alaska, USA sampled during the incubation and brood-rearing periods in 1998 and 2014; and B. Emperor (EMGO) and Cackling (CACG) Geese (Branta hutchinsii minima) sympatrically breeding on the Yukon-Kuskokwim Delta sampled during the brood-rearing period in 2014 only.

Close modal

In the second analysis, to examine species-specific variation in parasite detection and prevalence, we again detected moderate lack of fit in the most general model incorporating covariates for detection by species and prevalence by species, age class, and sex (Table S2). Therefore, a variance inflation factor of 1.58 was applied to the entire set of models and parameter estimation. However, model averaging was not necessary in this analysis to obtain point estimates and confidence intervals because a clear best model was identified, incorporating covariates for detection by age class and prevalence by species (QAICc weight = 0.41; Table S2). This top model received approximately three times the weight of the next-best ranked model. Furthermore, models including species as a covariate for prevalence received over 80% of total model weight in the candidate set. The prevalence estimates from our top model were 20.3% (95% CI: 11.8–32.7%) for Emperor Geese and 3.6% (95% CI: 1.1–11.0%) for Cackling Geese (Fig. 1). We found covariates for age class and sex to be uninformative for prevalence. However, four of the five top models (>75% of model weight in the set) included age class as a detection covariate (Table S2). The detection estimates from our top model were 0.85 (95% CI: 0.67–0.94) for adult geese and 0.24 (95% CI: 0.10–0.80) for goslings per PCR run (Fig. 1). This equates to estimated detection probabilities of >0.99 and 0.56 for samples from adult and hatch year geese, respectively, when run in triplicate.

Results of our investigation provide important insights regarding variation in the detection and prevalence of blood parasites among sympatrically breeding geese on the YKD in western Alaska. Specifically, our results provide evidence that Emperor Geese have probably consistently harbored Leucocytozoon spp. infections through recent time; that sympatrically breeding Emperor Geese and Cackling Geese may differentially harbor Leucocytozoon spp. infections; and that hatch year geese on the YKD may harbor a diversity of haemosporidian parasite infections that may not be as readily detected using PCR as they are in adult birds. These findings help to establish an important baseline for future assessments of changes in parasite prevalence and potential population-level effects in response to predicted ecologic change.

Using blood samples obtained from additional breeding seasons, our data are congruent with previous molecular screening efforts that support the consistent infection of Emperor Geese breeding on the YKD with Leucocytozoon spp. at a prevalence of around 20% (Ramey et al. 2014). We note that slight (nonsignificant) differences in point estimates of Leucocytozoon spp. prevalence for Emper- or Geese in 2014 in two analyses as part of this study are due to model averaging in the first analysis, using Emperor Goose samples collected in 1998 and 2014. In our second analysis, we included only samples collected in 2014 from both Emperor and Cackling Geese. Given relatively consistent evidence for the prevalence of Leucocytozoon spp. among Emperor Geese at all time points assessed using molecular methods (this study and Ramey et al. 2014), we infer that the apparent increase in Leucocytozoon spp. prevalence since the first record by Hollmén et al. (1998) in 1996 is most likely a function of methodology. In this case, the increased sensitivity of modern molecular methods probably accounted for the higher Leucocytozoon spp. prevalence estimates in recent investigations as opposed to an actual increase in parasite prevalence since 1996. Conclusions regarding trends of infection through time could be strengthened through testing of Emperor Goose blood samples from additional years.

Also consistent with a previous report (Ramey et al. 2014), we found evidence that Emperor Geese may indeed differentially harbor Leucocytozoon spp. infections compared to sympatrically breeding Cackling Geese. In our analysis, the prevalence of Leucocytozoon spp. infections in Emperor Geese was estimated to be more than five times that of Cackling Geese sampled on the YKD, despite these species nesting and rearing broods in the same geographic area. Differential parasite prevalence among sympatrically breeding species has also been observed in other systems where closely related taxa inhabit different wintering areas (Yohannes et al. 2009; Emmenegger et al. 2018). In the case of geese inhabiting the YKD, Cackling Geese tend to use agricultural fields within temperate lower latitudes during the nonbreeding season (Bogiatto et al. 2009) as opposed to Emperor Geese, which are dependent on natural food sources within subarctic high-latitude locations throughout the wintering period (Hupp et al. 2008; Uher-Koch et al. 2021). Consequently, Cackling Geese may more readily procure food resources and attain better physical condition prior to the onset of breeding; this might facilitate a robust immune response sufficient to quickly resolve haemosporidian infections (Arriero et al. 2018). In contrast, Emperor Geese may not arrive on the YKD with ample energetic reserves to meet the combined physiologic demands of breeding (i.e., egg laying and incubation) and mounting a sufficient immune response to suppress parasitic infections to undetectable levels. Alternatively or additionally, geographic variation in environmental conditions (Fecchio et al. 2020), or some degree of host specificity of parasites or vector preferences of biting insects (Hellgren et al. 2004), may play a role in parasite epidemiology on the YKD. Regardless of the underlying mechanism(s), our results suggest that avian haemosporidian parasites have the potential to disproportionally affect Emperor Geese breeding on the YKD; therefore, research to assess detrimental effects of Leucocytozoon spp. infections in this species is warranted.

The molecular identification of Leucocytozoon, Haemoproteus, and Plasmodium spp. parasites in unflighted goslings on the YKD provides important baseline information for future assessments of ecologic change, as this finding supports contemporary transmission of all three parasite genera at this locale. The finding of few Haemoproteus and Plasmodium spp. detections in waterfowl inhabiting the YKD is consistent with prior reports (Ramey et al. 2014; Ramey et al. 2015) and the premise that parasites of these genera may be temperature limited in high-latitude regions (Clark et al. 2020). Support for a difference in the estimated molecular detection of Leucocytozoon spp. in adult versus gosling Emperor Geese in our second analysis was unexpected, particularly given that this detection difference was not clearly implicated in our first analysis focused on Emperor Geese nor in previous models assessing haemosporidian parasite detection in samples collected from geese (Ramey et al. 2014), ducks (Ramey et al. 2015), and crows (Van Hemert et al. 2019) inhabiting Alaska. It is possible that the difference in detection we found in our analysis may have been due to unidentified sampling artifacts (e.g., disproportional sampling of birds exhibiting low parasitemia) among the relatively small sample size of Leucocytozoon spp.-positive hatch year birds assessed in our analytical framework (n=7). We encourage future investigations to incorporate age as a covariate when assessing variance in parasite detection until biologic significance is resolved.

In summary, our investigation establishes important baseline information regarding variation in the detection and prevalence of blood parasites that will be useful for informing future assessments of parasite prevalence in geese breeding in western Alaska and for evaluating potential ecologic effects in response to predicted environmental change. For example, our investigation provides additional support that Leucocytozoon spp. have clearly been established in geese breeding in western Alaska for at least 2 decades and therefore do not represent an emergent parasitic threat in the region. However, it is still unclear if haemosporidians are causing biologically significant effects in geese breeding on the YKD at the population level, which is worthy of future assessment. Furthermore, our study supports the previous finding that Haemoproteus and Plasmodium spp. parasites are uncommon among breeding waterfowl on the YKD but are transmitted within this region. Therefore, these presumably temperature-limited parasites may represent valuable targets for assessing future ecologic change within the YKD.

We appreciate help with sample collection provided by J. Barth, L. Bonczek, J. M. Duke, J. R. Duke, C. Gibson, D. Gerik, N. Graff, C. Gibson, S. Granroth, S. Hoepfner, C. Lalonde, C. Moore, A. Ortega, J. Pruszenski, and E. Watford. We thank the Matchian and Ayulik families and Mark Agimuk for safe transport of crews across the bays and rivers of the Yukon-Kuskokwim Delta. We would also like to thank the Yukon Delta National Wildlife Refuge for supporting work on this project and others over many years. We appreciate reviews on prior drafts of this product provided by J. Pearce, M. Smith, and three anonymous reviewers. This research was funded by the USGS Wildlife Program of the Ecosystems Mission area. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government.

Supplementary material for this article is online at http://dx.doi.org/10.7589/JWD-D-20-00159.

Arriero
E,
Pérez-Tris
J,
Ramírez
A,
Remacha
C.
2018
.
Trade-off between tolerance and resistance to infections: An experimental approach with malaria parasites in a passerine bird.
Oecologia
188
:
1001
1010
.
Asghar
M,
Hasselquist
D,
Hansson
B,
Zehtindjiev
P,
Westerdahl
H,
Bensch
S.
2015
.
Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds.
Science
347
:
436
438
.
Atkinson
CT,
Dusek
RJ,
Woods
KL,
Iko
WM.
2000
.
Pathogenicity of avian malaria in experimentally infected Hawaii Amakihi.
J Wildl Dis
36
:
197
204
.
Atkinson
CT,
van Riper
C
III.
1991
.
Pathogenicity and epizootiology of avian haemoatozoa: Plasmodium, Leucocytozoon, and Haemoproteus.
In:
Bird–parasite interactions: Ecology, evolution and behavior
,
Loye
JE,
Zuk
M,
editors.
Oxford University Press
,
New York, New York
, pp.
19
48
.
Bensch
S,
Waldenström
J,
Jonzén
N,
Westerdahl
H,
Hansson
B,
Sejberg
D,
Hasselquist
D.
2007
.
Temporal dynamics and diversity of avian malaria parasites in a single host species.
J Anim Ecol
76
:
112
122
.
Bogiatto
RJ,
Wright-Myers
SM,
Kraus
SH,
Moore
JL,
Hunt
JW.
2009
.
The use of eastern Sacramento Valley vernal pool habitats by geese and swans.
Calif Fish Game
95
:
175
187
.
Brooks
DR,
Hoberg
EP.
2007
.
How will global climate change affect parasite–host assemblages?
Trends Parasitol
23
:
571
574
.
Chen
I-C,
Hill
JK,
Ohlemüller
R,
Roy
DB,
Thomas
CD.
2011
.
Rapid range shifts of species associated with high levels of climate warming.
Science
333
:
1024
1026
.
Clark
NJ,
Clegg
SM,
Sam
K,
Goulding
W,
Koane
B,
Wells
K.
2018
.
Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly.
Diversity and Distributions
24
:
13
23
.
Clark
NJ,
Drovetski
SV,
Voelker
G.
2020
.
Robust geographical determinants of infection prevalence and a contrasting latitudinal diversity gradient for haemosporidian parasites in western Palearctic birds.
Mol Ecol
29
:
3131
3143
.
Ellis
VA,
Sari
EHR,
Rubenstein
DR,
Dickerson
RC,
Bensch
S,
Ricklefs
RE.
2019
.
The global biogeography of avian haemosporidian parasites is characterized by local diversification and intercontinental dispersal.
Parasitology
146
:
213
219
.
Emmenegger
T,
Bauer
S,
Dimitrov
D,
Olano Marin
J,
Zehtindjiev
P,
Hahn
S.
2018
.
Host migration strategy and blood parasite infections of three sparrow species sympatrically breeding in southeast Europe.
Parasitol Res
117
:
3733
3741
.
Fecchio
A,
Bell
JA,
Bosholn
M,
Vaughan
JA,
Tkach
VV,
Lutz
HL,
Cueto
VR,
Gorosito
CA,
González-Acuña
D,
Stromlund
C,
et al.
2020
.
An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds.
J Anim Ecol
89
:
423
435
.
Fecchio
A,
Wells
K,
Bell
JA,
Tkach
VV,
Lutz
HL,
Weckstein
JD,
Clegg
SM,
Clark
NJ.
2019
.
Climate variation influences host specificity in avian malaria parasites.
Ecol Lett
22
:
547
557
.
Hellgren
O,
Waldenström
J,
Bensch
S.
2004
.
A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood.
J Parasitol
90
:
797
802
.
Herman
CM,
Barrow
JH
Jr,
Tarshis
IB.
1975
.
Leucocytozoonosis in Canada geese at the Seney National Wildlife Refuge.
J Wildl Dis
11
:
404
411
.
Hollmén
TE,
Franson
JC,
Creekmore
LH,
Schmutz
JA,
Fowler
AC.
1998
.
Leucocytozoon simondi in emperor geese from the Yukon-Kuskokwim Delta in Alaska.
The Condor
100
:
402
404
.
Hupp
JW,
Schmutz
JA,
Ely
CR.
2008
.
The annual migration cycle of emperor geese in western Alaska.
Arctic
61
:
23
34
.
Kerr
KCR,
Stoeckle
MY,
Dove
CJ,
Weigt
LA,
Francis
CM,
Hebert
PDN.
2007
.
Comprehensive DNA barcode coverage of North American birds.
Mol Ecol Notes
7
:
535
543
.
Kilpatrick
AM,
LaPointe
DA,
Atkinson
CT,
Woodworth
BL,
Lease
JK,
Reiter
ME,
Gross
K.
2006
.
Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii amakihi (Hemignathus virens).
The Auk
123
:
764
774
.
Kutz
SJ,
Jenkins
EJ,
Veitch
AM,
Ducrocq
J,
Polley
L,
Elkin
B,
Lair
S.
2009
.
The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host–parasite interactions.
Vet Parasitol
163
:
217
228
.
Laake
JL.
2013
.
RMark: An R interface for analysis of capture–recapture data with MARK.
AFSC Processed Report 2013-01
,
Alaska Fisheries Science Center, National Marine Fisheries Service
,
Seattle, Washington
,
25
pp.
LaPointe
DA,
Atkinson
CT,
Samuel
MD.
2012
.
Ecology and conservation biology of avian malaria.
Ann NY Acad Sci
1249
:
211
226
.
LaPointe
DA,
Goff
ML,
Atkinson
CT.
2010
.
Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai‘i.
J Parasitol
96
:
318
324
.
Loiseau
C,
Harrigan
RJ,
Bichet
C,
Julliard
R,
Garnier
S,
Lendvai
AZ,
Chastel
O,
Sorci
G.
2013
.
Predictions of avian Plasmodium expansion under climate change.
Sci Rep
3
:
1126
.
MacKenzie
DI,
Nichols
JD,
Royle
JA,
Pollock
KH,
Bailey
L,
Hines
JE.
2017
.
Occupancy estimation and modeling: Inferring patterns and dynamics of species occurrence.
2nd Ed.
Academic Press
,
Cambridge, Massachusetts
,
648
pp.
Marzal
A,
de Lope
F,
Navarro
C,
Møller
AP.
2005
.
Malarial parasites decrease reproductive success: An experimental study in a passerine bird.
Oecologia
142
:
541
545
.
Merino
S,
Moreno
J,
Sanz
JJ,
Arriero
E.
2000
.
Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus).
Proc Biol Sci
267
:
2507
2510
.
NCBI.
2021
.
Basic local alignment search tool.
R Core Team.
2020
.
R: A language and environment for statistical computing.
R Foundation for Statistical Computing
,
Vienna, Austria
.
https://www.R-project.org/. Accessed March 2021.
Ramey
AM,
Reed
JA,
Schmutz
JA,
Fondell
TF,
Meixell
BW,
Hupp
JW,
Ward
DH,
Terenzi
J,
Ely
CR.
2014
.
Prevalence, transmission, and genetic diversity of blood parasites infecting tundra-nesting geese in Alaska.
Can J Zool
92
:
699
706
.
Ramey
AM,
Schmutz
JA,
Reed
JA,
Fujita
G,
Scotton
BD,
Casler
B,
Fleskes
JP,
Konishi
K,
Uchida
K,
Yabsley
MJ.
2015
.
Evidence for intercontinental parasite exchange through molecular detection and characterization of haematozoa in northern pintails (Anas acuta) sampled throughout the North Pacific Basin.
Int J Parasitol Parasites Wildl
4
:
11
21
.
Reed
JA,
Buchheit
RM,
Schmutz
JA,
Uher-Koch
B,
Ramey
AM.
2021
.
Blood parasite infection data from emperor geese (Anser canagicus) and cackling geese (Branta hutchinsii minima), Yukon-Kuskokwim Delta, Alaska, 1998–2014.
US Geological Survey data release
,
Reston, Virginia
.
https://doi.org/10.5066/P9F7LD2I. Accessed March 2021.
Sekercioglu
CH,
Schneider
SH,
Fay
JP,
Loarie
SR.
2008
.
Climate change, elevational range shifts, and bird extinctions.
Conserv Biol
22
:
140
150
.
Uher-Koch
BD,
Buchheit
RM,
Eldermire
CR,
Wilson
HM,
Schmutz
JA.
2021
.
Shifts in the wintering distribution and abundance of emperor geese in Alaska.
Glob Ecol Conserv
25
:
e01397
.
Valkiunas
G.
2005
.
Avian malaria parasites and other haemosporidia.
CRC Press
,
Boca Raton, Florida
,
946
pp.
Van Hemert
C,
Meixell
BW,
Smith
MM,
Handel
CM.
2019
.
Prevalence and diversity of avian blood parasites in a resident northern passerine.
Parasit Vectors
12
:
292
.
van Riper
C
III,
van Riper
SG,
Goff
ML,
Laird
M.
1986
.
The epizootiology and ecological significance of malaria in Hawaiian land birds.
Ecol Monogr
56
:
327
344
.
Warner
RE.
1968
.
The role of introduced diseases in the extinction of the endemic Hawaiian avifauna.
The Condor
70
:
101
120
.
White
GC,
Burnham
KP.
1999
.
Program MARK: Survival estimation from populations of marked animals.
Bird Study
46
(
Suppl
):
S120
S139
.
Yohannes
E,
Križanauskienė
A,
Valcu
M,
Bensch
S,
Kempenaers
B.
2009
.
Prevalence of malaria and related haemosporidian parasites in two shorebird species with different winter habitat distribution.
J Ornithol
150
:
287
291
.
Zamora-Vilchis
I,
Williams
SE,
Johnson
CN.
2012
.
Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: Implications for disease in a warming climate.
PLoS One
7
:
e39208
.

Supplementary data