Abstract
Turnover in species composition between sites, or beta diversity, is a critical component of species diversity that is typically influenced by geography, environment, and biotic interactions. Quantifying turnover is particularly challenging, however, in multi-host, multi-parasite assemblages where undersampling is unavoidable, resulting in inflated estimates of turnover and uncertainty about its spatial scale. We developed and implemented a framework using null models to test for community turnover in avian haemosporidian communities of three sky islands in the southwestern United States. We screened 776 birds for haemosporidian parasites from three genera (Parahaemoproteus, Plasmodium, and Leucocytozoon) by amplifying and sequencing a mitochondrial DNA barcode. We detected infections in 280 birds (36.1%), sequenced 357 infections, and found a total of 99 parasite haplotypes. When compared to communities simulated from a regional pool, we observed more unique, single-mountain haplotypes and fewer haplotypes shared among three mountain ranges than expected, indicating that haemosporidian communities differ to some degree among adjacent mountain ranges. These results were robust even after pruning datasets to include only identical sets of host species, and they were consistent for two of the three haemosporidian genera. The two more distant mountain ranges were more similar to each other than the one located centrally, suggesting that the differences we detected were due to stochastic colonization–extirpation dynamics. These results demonstrate that avian haemosporidian communities of temperate-zone forests differ on relatively fine spatial scales between adjacent sky islands. Null models are essential tools for testing the spatial scale of turnover in complex, undersampled, and poorly known systems.
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References
Anderson MJ, Crist TO, Chase JM et al (2011) Navigating the multiple meanings of beta diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28. https://doi.org/10.1111/j.1461-0248.2010.01552.x
Asghar M, Hasselquist D, Hansson B et al (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347:436–438. https://doi.org/10.1126/science.1261121
Atkinson CT, LaPointe DA (2009) Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. J Avian Med Surg 23:53–63. https://doi.org/10.1647/2008-059.1
Barrow LN, McNew SM, Mitchell N et al (2019) Deeply conserved susceptibility in a multi-host, multi-parasite system. Ecol Lett 22:987–998. https://doi.org/10.1111/ele.13263
Beck J, Holloway JD, Schwanghart W (2013) Undersampling and the measurement of beta diversity. Methods Ecol Evol 4:370–382. https://doi.org/10.1111/2041-210x.12023
Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x
Betancourt JL, Van Devender TR, Martin PS (1990) Packrat middens: the last 40,000 years of biotic change. University of Arizona Press, Tucson
Biesmeijer JC, Roberts SPM, Reemer M et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354. https://doi.org/10.1126/science.1127863
Borner J, Pick C, Thiede J et al (2016) Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Mol Phylogenet Evol 94:221–231. https://doi.org/10.1016/j.ympev.2015.09.003
Bouckaert R, Heled J, Kuhnert D et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Brooks DR, Hoberg EP (2007) How will global climate change affect parasite-host assemblages? Trends Parasitol 23:571–574. https://doi.org/10.1016/j.pt.2007.08.016
Brooks DR, León-Règagnon V, Mclennan DA, Zelmer D (2006) Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87:S76–S85
Buckley LB, Jetz W (2008) Linking global turnover of species and environments. Proc Natl Acad Sci 105:17836–17841. https://doi.org/10.1073/pnas.0803524105
Cardoso P, Borges PAV, Veech JA (2009) Testing the performance of beta diversity measures based on incidence data: the robustness to undersampling. Divers Distrib 15:1081–1090. https://doi.org/10.1111/j.1472-4642.2009.00607.x
Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159. https://doi.org/10.1111/j.1461-0248.2004.00707.x
Chao A, Chazdon RL, Colwell RK, Shen TJ (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371. https://doi.org/10.1111/j.1541-0420.2005.00489.x
Clark NJ (2018) Phylogenetic uniqueness, not latitude, explains the diversity of avian blood parasite communities worldwide. Glob Ecol Biogeogr 27:744–755. https://doi.org/10.1111/geb.12741
Clark NJ, Clegg SM (2017) Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity. Mol Ecol 26:3074–3086. https://doi.org/10.1111/mec.14101
Clark NJ, Clegg SM, Sam K et al (2018) Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly. Divers Distrib 24:13–23. https://doi.org/10.1111/ddi.12661
Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. http://purl.oclc.org/estimates
Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc B Biol Sci 345:101–118
Colwell RK, Chao A, Gotelli NJ et al (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21. https://doi.org/10.1093/jpe/rtr044
Dallas T, Cornelius E (2015) Co-extinction in a host-parasite network: identifying key hosts for network stability. Sci Rep 5:1–10. https://doi.org/10.1038/srep13185
Dornelas M, Gotelli NJ, McGill B et al (2014) Assemblage time series reveal biodiversity change but not systematic loss. Science 344:296–299. https://doi.org/10.1126/science.1248484
Ellis VA, Collins MD, Medeiros MCI et al (2015) Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites. Proc Natl Acad Sci 112:11294–11299. https://doi.org/10.1073/pnas.1515309112
Fallon SM, Bermingham E, Ricklefs RE (2003) Island and taxon effects in parasitism revisited: Avian malaria in the Lesser Antilles. Evolution 57:606–615. https://doi.org/10.1554/0014-3820(2003)057[0606:IATEIP]2.0.CO;2
Fallon SM, Ricklefs RE, Latta SC, Bermingham E (2004) Temporal stability of insular avian malarial parasite communities. Proc R Soc B Biol Sci 271:493–500. https://doi.org/10.1098/rspb.2003.2621
Fallon SM, Bermingham E, Ricklefs RE (2005) Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. Am Nat 165:466–480. https://doi.org/10.1086/428430
Fecchio A, Pinheiro R, Felix G et al (2017) Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds. Ecography 41:505–515. https://doi.org/10.1111/ecog.03058
Fecchio A, Bell JA, Pinheiro RBP et al (2019) Avian host composition, local speciation, and dispersal drive the regional assembly of avian malaria parasites in South American birds. Mol Ecol 28:2681–2693. https://doi.org/10.1111/mec.15094
Fecchio A, Bell JA, Bosholn M 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. https://doi.org/10.1111/1365-2656.13117
Fitzpatrick MC, Sanders NJ, Normand S et al (2013) Environmental and historical imprints on beta diversity: insights from variation in rates of species turnover along gradients. Proc R Soc B Biol Sci 280:20131201. https://doi.org/10.1098/rspb.2013.1201
Galen SC, Witt CC (2014) Diverse avian malaria and other haemosporidian parasites in Andean house wrens: Evidence for regional co-diversification by host-switching. J Avian Biol 45:374–386. https://doi.org/10.1111/jav.00375
Galen SC, Borner J, Martinsen ES et al (2018) The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. R Soc Open Sci 5:171780. https://doi.org/10.1098/rsos.171780
Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621
Gotelli NJ, Ulrich W (2012) Statistical challenges in null model analysis. Oikos 121:171–180. https://doi.org/10.1111/j.1600-0706.2011.20301.x
Gupta P, Vishnudas CK, Ramakrishnan U et al (2019) Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago. Proc R Soc B Biol Sci 286:20190439. https://doi.org/10.1098/rspb.2019.0439
Hackett SJ, Kimball RT, Reddy S et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science (New York, NY) 320:1763–1768. https://doi.org/10.1126/science.1157704
Harrigan RJ, Sedano R, Chasar AC et al (2014) New host and lineage diversity of avian haemosporidia in the northern andes. Evol Appl 7:799–811. https://doi.org/10.1111/eva.12176
Harrison S, Ross SJ, Lawton JH (1992) Beta diversity on geographic gradients in Britain. J Anim Ecol 61:151–158
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. https://doi.org/10.1645/GE-184R1
Hellgren O, Waldenström J, Peréz-Tris J et al (2007) Detecting shifts of transmission areas in avian blood parasites—a phylogenetic approach. Mol Ecol 16:1281–1290. https://doi.org/10.1111/j.1365-294X.2007.03227.x
Hellgren O, Pérez-Tris J, Bensch S (2009) A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90:2840–2849. https://doi.org/10.1890/08-1059.1
Hellgren O, Atkinson CT, Bensch S et al (2015) Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography 38:842–850. https://doi.org/10.1111/ecog.01158
Holmgren CA, Betancourt JL, Rylander KA (2006) A 36,000-yr vegetation history from the Peloncillo Mountains, southeastern Arizona, USA. Palaeogeogr Palaeoclimatol Palaeoecol 240:405–422. https://doi.org/10.1016/j.palaeo.2006.02.017
Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67:4399–4406. https://doi.org/10.1128/AEM.67.10.4399
Ishtiaq F, Clegg SM, Phillimore AB et al (2010) Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. J Biogeogr 37:120–132. https://doi.org/10.1111/j.1365-2699.2009.02189.x
Jarvis A, Reuter HI, Nelson A, Guevara E (2008) Hole-filled seamless SRTM data V4. International Centre for Tropical Agriculture (CIAT) available from http://srtm.csi.cgiar.org
Jetz W, Thomas GH, Joy JB et al (2012) The global diversity of birds in space and time. Nature 491:444–448. https://doi.org/10.1038/nature11631
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Knowles LL (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshopprers. Mol Ecol 10:691–701. https://doi.org/10.1046/j.1365-294X.2001.01206.x
Knowles SCL, Palinauskas V, Sheldon BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J Evol Biol 23:557–569. https://doi.org/10.1111/j.1420-9101.2009.01920.x
Krasnov BR, Stanko M, Khokhlova IS et al (2011) Nestedness and β-diversity in ectoparasite assemblages of small mammalian hosts: effects of parasite affinity, host biology and scale. Oikos 120:630–639. https://doi.org/10.1111/j.1600-0706.2010.19072.x
Lanfear R, Frandsen PB, Wright AM et al (2017) Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773. https://doi.org/10.1093/molbev/msw260
LaPointe DA, Goff ML, Atkinson CT (2010) Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodiumrelictum in Hawai’i. J Parasitol 96:318–324. https://doi.org/10.1645/GE-2290.1
Latta RG, Mitton JB (1999) Historical separation and present gene flow through a zone of secondary contact in ponderosa pine. Evolution 53:769–776. https://doi.org/10.1111/j.1558-5646.1999.tb05371.x
Loiseau C, Harrigan RJ, Robert A et al (2012) Host and habitat specialization of avian malaria in Africa. Mol Ecol 21:431–441. https://doi.org/10.1111/j.1365-294X.2011.05341.x
Marroquin-Flores RA, Williamson JL, Chavez AN et al (2017) Diversity, abundance, and host relationships in the avian malaria community of New Mexico pine forests. PeerJ 5:e3700. https://doi.org/10.7717/peerj.3700
Marzal A, Bensch S, Reviriego M et al (2008) Effects of malaria double infection in birds: one plus one is not two. J Evol Biol 21:979–987. https://doi.org/10.1111/j.1420-9101.2008.01545.x
McCormack JE, Bowen BS, Smith TB (2008) Integrating paleoecology and genetics of bird populations in two sky island archipelagos. BMC Biol 6:1–12. https://doi.org/10.1186/1741-7007-6-28
Moens MAJ, Valkiūnas G, Paca A et al (2016) Parasite specialization in a unique habitat: hummingbirds as reservoirs of generalist blood parasites of Andean birds. J Anim Ecol 85:1234–1245. https://doi.org/10.1111/1365-2656.12550
Oksanen J, Blanchet FG, Friendly M et al (2018) vegan: Community Ecology Package. Version 2.5–2. https://CRAN.R-project.org/package=vegan.
Olias P, Wegelin M, Zenker W et al (2011) Avian malaria deaths in parrots, Europe. Emerg Infect Dis 17:950–952. https://doi.org/10.1086/605025
Olsson-Pons S, Clark NJ, Ishtiaq F, Clegg SM (2015) 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 84:985–998. https://doi.org/10.1111/1365-2656.12354
Poulin R (1997) Species richness of parasite assemblages: evolution and patterns. Annu Rev Ecol Syst 28:341–358. https://doi.org/10.1146/annurev.ecolsys.28.1.341
Poulin R (1999) The functional importance of parasites in animal communities: many roles at many levels? Int J Parasitol 29:903–914
Poulin R (2003) The decay of similarity with geographical distance in parasite communities of vertebrate hosts. J Biogeogr 30:1609–1615
Poulin R (2014) Parasite biodiversity revisited: frontiers and constraints. Int J Parasitol 44:581–589. https://doi.org/10.1016/j.ijpara.2014.02.003
R Core Team (2016) R: a language and environment for statistical computing. https://www.R-project.org/
Rambaut A, Drummond AJ, Xie D et al (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Ricklefs RE (1992) Embryonic development period and the prevalence of avian blood parasites. Proc Natl Acad Sci 89:4722–4725. https://doi.org/10.1073/pnas.89.10.4722
Ricklefs R, Bermingham E (2008) The West Indies as a laboratory of biogeography and evolution. Philos Trans R Soc B Biol Sci 363:2393–2413. https://doi.org/10.1098/rstb.2007.2068
Ricklefs RE, Swanson BL, Fallon SM et al (2005) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75:543–559. https://doi.org/10.1890/04-1820
Ricklefs RE, Dodge Gray J, Latta SC, Svensson-Coelho M (2011) Distribution anomalies in avian haemosporidian parasites in the southern Lesser Antilles. J Avian Biol 42:570–584. https://doi.org/10.1111/j.1600-048X.2011.05404.x
Ricklefs RE, Outlaw DC, Svensson-Coelho M et al (2014) Species formation by host shifting in avian malaria parasites. Proc Natl Acad Sci USA 111:14816–14821. https://doi.org/10.1073/pnas.1416356111
Ricklefs RE, Medeiros M, Ellis VA et al (2017) Avian migration and the distribution of malaria parasites in New World passerine birds. J Biogeogr 44:1113–1123. https://doi.org/10.1111/jbi.12928
Roden VJ, Kocsis ÁT, Zuschin M, Kiessling W (2018) Reliable estimates of beta diversity with incomplete sampling. Ecology 99:1051–1062. https://doi.org/10.1002/ecy.2201
Scaglione FE, Cannizzo FT, Pregel P et al (2016) Blood parasites in hooded crows (Corvus corone cornix) in Northwest Italy. Veterinaria Italiana 52:111–116. https://doi.org/10.12834/VetIt.110.307.2
Schmid S, Fachet K, Dinkel A et al (2017) Carrion crows (Corvuscorone) of southwest Germany: important hosts for haemosporidian parasites. Malaria J 16:1–12. https://doi.org/10.1186/s12936-017-2023-5
Scordato ESC, Kardish MR (2014) Prevalence and beta diversity in avian malaria communities: Host species is a better predictor than geography. J Anim Ecol 83:1387–1397. https://doi.org/10.1111/1365-2656.12246
Soares L, Latta SC, Ricklefs RE (2017) Dynamics of avian haemosporidian assemblages through millennial time scales inferred from insular biotas of the West Indies. Proc Natl Acad Sci 114:6635–6640. https://doi.org/10.1073/pnas.1702512114
Soares L, Latta SC, Ricklefs RE (2020a) Neotropical migratory and resident birds occurring in sympatry during winter have distinct haemosporidian parasite assemblages. J Biogeogr 47:748–759. https://doi.org/10.1111/jbi.13760
Soares L, Young EI, Ricklefs RE (2020b) Haemosporidian parasites of resident and wintering migratory birds in The Bahamas. Parasitol Res 119:1563–1572. https://doi.org/10.1007/s00436-020-06646-y
Socolar JB, Gilroy JJ, Kunin WE, Edwards DP (2016) How should beta-diversity inform biodiversity conservation? Trends Ecol Evol 31:67–80. https://doi.org/10.1016/j.tree.2015.11.005
Spellman GM, Klicka J (2006) Testing hypotheses of Pleistocene population history using coalescent simulations: phylogeography of the pygmy nuthatch (Sitta pygmaea). Proc R Soc B Biol Sci 273:3057–3063. https://doi.org/10.1098/rspb.2006.3682
Stier AC, Bolker BM, Osenberg CW (2016) Using rarefaction to isolate the effects of patch size and sampling effort on beta diversity. Ecosphere 7:e01612. https://doi.org/10.1002/ecs2.1612
Svensson-Coelho M, Ricklefs RE (2011) Host phylogeography and beta diversity in avian haemosporidian (Plasmodiidae) assemblages of the Lesser Antilles. J Anim Ecol 80:938–946. https://doi.org/10.1111/j.1365-2656.2011.01837.x
Svensson-Coelho M, Blake JG, Loiselle BA et al (2013) Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a Western Amazon assemblage. Ornithol Monogr 76:1–47. https://doi.org/10.1525/om.2013.76.1.1.1
Svensson-Coelho M, Silva GT, Santos SS et al (2016) Lower detection probability of avian plasmodium in blood compared to other tissues. J Parasitol 102:559–561. https://doi.org/10.1645/16-8
Thieltges DW, Ferguson MAD, Jones CS et al (2009) Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160:163–173. https://doi.org/10.1007/s00442-009-1276-2
Thornhill R, Fincher CL (2013) The parasite-driven-wedge model of parapatric speciation. J Zool 291:23–33. https://doi.org/10.1111/jzo.12070
Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton
van Riper C, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344. https://doi.org/10.2307/1942550
van Rooyen J, Lalubin F, Glaizot O, Christe P (2013) Altitudinal variation in haemosporidian parasite distribution in great tit populations. Paras Vect 6:1–10. https://doi.org/10.1186/1756-3305-6-139
Waldenström J, Bensch S, Hasselquist D, Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90:191–194. https://doi.org/10.1645/GE-3221RN
Walther EL, Carlson JS, Cornel A et al (2016) First molecular study of prevalence and diversity of avian haemosporidia in a central California songbird community. J Ornithol 157:549–564. https://doi.org/10.1007/s10336-015-1301-7
Warburton EM, Kohler SL, Vonhof MJ (2016) Patterns of parasite community dissimilarity: the significant role of land use and lack of distance-decay in a bat-helminth system. Oikos 125:374–385. https://doi.org/10.1111/oik.02313
Warner RE (1968) The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70:101–120. https://doi.org/10.2307/1365954
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279–338. https://doi.org/10.2307/1943563
Whittaker RH (1972) Evolution and the measurement of species diversity. Taxon 21:213–251
Williams PH (1996) Mapping variations in the strength and breadth of biogeographic transition zones using species turnover. Proc R Soc B Biol Sci 263:579–588. https://doi.org/10.1098/rspb.1996.0087
Williamson JL, Wolf CJ, Barrow LN et al (2019) Ecology, not distance, explains community composition in parasites of sky-island Audubon’s Warblers. Int J Parasitol 49:437–448. https://doi.org/10.1016/j.ijpara.2018.11.012
Woolhouse M, Gaunt E (2007) Ecological origins of novel human pathogens. Crit Rev Microbiol 33:231–242. https://doi.org/10.1080/10408410701647560
Zhou J, Jiang Y-H, Deng Y et al (2013) Random sampling process leads to overestimation of Beta diversity of microbial communities. mBio 4:e00324-e413. https://doi.org/10.1128/mBio.00324-13.Editor
Acknowledgements
We thank Michael Andersen, Sara Brant, Mariel Campbell, Joseph Manthey, Moses Michelsohn, and George Rosenberg. This work was supported by the Bureau of Land Management Rio Puerco Field Office (via the Colorado Plateau Cooperative Ecosystems Studies Unit agreement) and NSF DEB-1146491. SMB, RMF, and TEM were supported by PREP/FlyBase Fellowships (NIH 5R25HG007630) and LNB was supported by an NSF Postdoctoral Research Fellowship in Biology (NSF DBI-1611710).
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LNB, SMB, and CCW conceived the ideas; LNB, SMB, JLW, JEF, MJB, SSB, ANC, CRG, SCG, ABJ, XMM, RMF, TEM, JMM, and CCW conducted fieldwork and generated data; LNB, SMB, PAC, JLW, DLW, JEF, RMF, and JEM conducted molecular work and microscopy; LNB, SMB, PAC, and JLW analyzed the data, and LNB and CCW wrote the manuscript.
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Barrow, L.N., Bauernfeind, S.M., Cruz, P.A. et al. Detecting turnover among complex communities using null models: a case study with sky-island haemosporidian parasites. Oecologia 195, 435–451 (2021). https://doi.org/10.1007/s00442-021-04854-6
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DOI: https://doi.org/10.1007/s00442-021-04854-6