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Climate predictors and climate change projections for avian haemosporidian prevalence in Mexico

Published online by Cambridge University Press:  10 May 2022

Larissa Ortega-Guzmán
Affiliation:
Instituto Potosino de Investigación Científica y Tecnológica A.C., División de Ciencias Ambientales, Camino a la Presa San José 2055, Lomas 4a Sección, C.P., 78216, San Luis Potosí, México
Octavio Rojas-Soto
Affiliation:
Red de Biología Evolutiva, Instituto de Ecología A. C., Xalapa, Veracruz, México
Diego Santiago-Alarcon
Affiliation:
Department of Integrative Biology, University of South Florida, Tampa, FL 33620, USA
Elisabeth Huber-Sannwald
Affiliation:
Instituto Potosino de Investigación Científica y Tecnológica A.C., División de Ciencias Ambientales, Camino a la Presa San José 2055, Lomas 4a Sección, C.P., 78216, San Luis Potosí, México
Leonardo Chapa-Vargas*
Affiliation:
Instituto Potosino de Investigación Científica y Tecnológica A.C., División de Ciencias Ambientales, Camino a la Presa San José 2055, Lomas 4a Sección, C.P., 78216, San Luis Potosí, México
*
Author for correspondence: Leonardo Chapa-Vargas, E-mail: lchapa@ipicyt.edu.mx

Abstract

Long-term, inter-annual and seasonal variation in temperature and precipitation influence the distribution and prevalence of intraerythrocytic haemosporidian parasites. We characterized the climatic niche behind the prevalence of the three main haemosporidian genera (Haemoproteus, Plasmodium and Leucocytozoon) in central-eastern Mexico, to understand their main climate drivers. Then, we projected the influence of climate change over prevalence distribution in the region. Using the MaxEnt modelling algorithm, we assessed the relative contribution of bioclimatic predictor variables to identify those most influential to haemosporidian prevalence in different avian communities within the region. Two contrasting climate change scenarios for 2070 were used to create distribution models to explain spatial turnover in prevalence caused by climate change. We assigned our study sites into polygonal operational climatic units (OCUs) and used the general haemosporidian prevalence for each OCU to indirectly measure environmental suitability for these parasites. A high statistical association between global prevalence and the bioclimatic variables ‘mean diurnal temperature range’ and ‘annual temperature range’ was found. Climate change projections for 2070 showed a significant modification of the current distribution of suitable climate areas for haemosporidians in the study region.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Álvarez-Mendizábal, P, Villalobos, F, Rodríguez-Hernández, K, Hernández-Lara, C, Rico-Chávez, O, Suzán, G, Chapa-Vargas, L and Santiago-Alarcon, D (2021) Metacommunity structure reveals that temperature affects the landscape compositional patterns of avian malaria and related haemosporidian parasites across elevations. Acta Oecologica 113, https://doi.org/10.1016/j.actao.2021.103789CrossRefGoogle Scholar
Atkinson, CT (1999) Chapter 24: haemosporidiosis. In Friend, M and Franson, JC (eds), Field Manual of Wildlife Diseases. Washington, DC: USGS Biological Resources Division, pp. 193200.Google Scholar
Atkinson, CT, Utzurrum, RB, LaPointe, DA, Camp, RJ, Crampton, LH, Foster, JT and Giambelluca, TW (2014) Changing climate and the altitudinal range of avian malaria in the Hawaiian Islands – an ongoing conservation crisis on the island of Kaua'i. Global Change Biology 20, 24262436.CrossRefGoogle ScholarPubMed
Bates, D, Mächler, M, Bolker, BM and Walker, SC (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.10.18637/jss.v067.i01CrossRefGoogle Scholar
Beadell, JS, Gering, E, Austin, J, Dumbacher, JP, Peirce, MA, Pratt, TK, Atkinson, CT and Fleischer, RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology 13, 38293844.CrossRefGoogle ScholarPubMed
Bell, JA, Weckstein, JD, Fecchio, A and Tkach, VV (2015) A new real-time PCR protocol for detection of avian haemosporidians. Parasites & Vectors 8, 19.CrossRefGoogle ScholarPubMed
Bennett, GF, Aguirre, AA and Cook, RS (1991) Blood parasites of some birds from northeastern Mexico. Journal of Parasitology 77, 3841.CrossRefGoogle ScholarPubMed
Benning, TL, LaPointe, D, Atkinson, CT and Vitousek, PM (2002) Interactions of climate change with biological invasions and land use in the Hawaiian Islands: modeling the fate of endemic birds using a geographic information system. PNAS 99, 1424614249.10.1073/pnas.162372399CrossRefGoogle ScholarPubMed
Brooks, DR and Hoberg, EP (2007) How will global climate change affect parasite–host assemblages? Trends in Parasitology 23, 571574.CrossRefGoogle ScholarPubMed
Busse, P and Meissner, W (2015) Bird Ringing Station Manual. Warsaw, Berlin: De Gruyter Open Ltd.CrossRefGoogle Scholar
Carbó-Ramírez, P, Zuria, I, Schaefer, HM and Santiago-Alarcon, D (2017) Avian haemosporidians at three environmentally contrasting urban greenspaces. Journal of Urban Ecology 3, 111.10.1093/jue/juw011CrossRefGoogle Scholar
Cavazos, T, Salinas, JA, Martínez, B, Colorado, G, de Grau, P, Prieto González, R, Conde Álvarez, AC, Quintanar Isaías, A, Santana Sepúlveda, JS, Romero Centeno, R, Maya Magaña, ME, Rosario de La Cruz, JG, Ayala Enríquez, MdR, Carrillo Tlazazanatza, H, Santiesteban, O and Bravo, ME (2013) Actualización de Escenarios de Cambio Climático para México como Parte de los Productos de la Quinta Comunicación Nacional. Centro de Investigación Científica y de Educación Superior de Ensenada, B. C., Instituto Mexicano de Tecnología del Agua, Centro de Ciencias de la Atmosfera, UNAM. Mexico. 151pp.Google Scholar
Chapa-Vargas, L, Matta, NE and Merino, S (2020) Chapter 10: effects of ecological gradients on tropical avian hemoparasites. In Santiago-Alarcon, D and Marzal, A (eds), Avian Malaria and Related Parasites in the Tropics. Ecology, Evolution and Systematics. Switzerland AG: Springer, pp. 349378. https://doi.org/10.1007/978-3-030-51633-8.CrossRefGoogle Scholar
Clark, NJ (2018) Phylogenetic uniqueness, not latitude, explains the diversity of avian blood parasite communities worldwide. Global Ecology and Biogeography 27, 744755.CrossRefGoogle Scholar
Clark, NJ, Wells, K, Dimitrov, D and Clegg, SM (2016) Co-infections and environmental conditions drive the distributions of blood parasites in wild birds. Journal of Animal Ecology 85, 14611470.10.1111/1365-2656.12578CrossRefGoogle ScholarPubMed
Clark, NJ, Clegg, SM, Sam, K, Goulding, W, Koane, B and Wells, K (2018) Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly. Diversity and Distributions 24, 1323.CrossRefGoogle Scholar
Clarke, LE, Edmonds, JA, Jacoby, HD, Pitcher, HM, Reilly, JM and Richels, RG (2007) Scenarios of greenhouse gas emissions and atmospheric concentrations. Sub-report 2.1A of Synthesis and Assessment Product 2.1 by the U.S. Climate Change Science Program and the Subcommittee on Global Change Research. Department of Energy, Office of Biological & Environmental Research. Washington, D.C. 154pp. http://www.climatescience.gov/Library/sap/sap2-1/finalreport/default.htm.Google Scholar
Cobos, ME, Peterson, AT, Osorio-Olvera, L and Jiménez-García, D (2019) An exhaustive analysis of heuristic methods for variable selection in ecological niche modeling and species distribution modeling. Ecological Informatics 53, 100983. https://doi.org/10.1016/j.ecoinf.2019.100983.CrossRefGoogle Scholar
CONABIO (2008) Portal de Geoinformación. Sistema Nacional de Información sobre Biodiversidad. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Retrieved from: http://www.conabio.gob.mx/informacion/gis/.Google Scholar
Coon, CAC and Martin, LB (2013) Patterns of haemosporidian prevalence along a range expansion in introduced Kenyan house sparrows Passer domesticus. Journal of Avian Biology 45, 3442.CrossRefGoogle Scholar
Crosskey, RW (1993) Blackflies (Simuliidae). In Lane, RP and Crosskey, RW (eds), Medical Insects and Arachnids. Dordrecht: Springer, pp. 241287. https://doi.org/10.1007/978-94-011-1554-4_6.CrossRefGoogle Scholar
Escobar, LE, Lira-Noriega, A, Medina-Vogel, G and Peterson, AT (2014) Potential for spread of the white-nose fungus (Pseudogymnoascus destructans) in the Americas: use of Maxent and NicheA to assure strict model transference. Geospatial Health 9, 221229.CrossRefGoogle ScholarPubMed
Fecchio, A, Wells, K, Bell, JA, Tkach, VV, Lutz, HL, Weckstein, JD, Clegg, SM and Clark, NJ (2019a) Climate variation influences host specificity in avian malaria parasites. Ecology Letters 22, 547557.CrossRefGoogle Scholar
Fecchio, A, Bell, JA, Bosholn, M, Vaughan, JA, Tkach, VV, Lutz, HL, Cueto, VR, Gorosito, CA, González-Acuña, D, Stromlund, C, Kvasager, D, Comiche, KJM, Kirchgatter, K, Pinho, JB, Berv, J, Anciães, M, Fontana, CS, Zyskowski, K, Sampaio, S, Dispoto, JH, Galen, SC, Weckstein, JD and Clark, NJ (2019b) An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds. Journal of Animal Ecology 89, 423435.CrossRefGoogle Scholar
Fecchio, A, Clark, NJ, Bell, JA, Skeen, HR, Lutz, HL, De La Torre, GM, Vaughan, JA, Tkach, VV, Schunck, F, Ferreira, FC, Braga, ÉM, Lugarini, C, Wuamiti, W, Dispoto, JH, Galen, SC, Kirchgatter, K, Sagario, MC, Cueto, VR, González-Acuña, D, Inumaru, M, Sato, Y, Schumm, YR, Quillfeldt, P, Pellegrino, I, Dharmarajan, G, Gupta, P, Robin, VV, Ciloglu, A, Yildirim, A, Huang, X, Chapa-Vargas, L, Álvarez-Mendizábal, P, Santiago-Alarcon, D, Drovetski, SV, Hellgren, O, Voelker, G, Ricklefs, RE, Hackett, SJ, Collins, MD, Weckstein, JD and Wells, K (2021) Global drivers of avian haemosporidian infections vary across zoogeographical regions. Global Ecology and Biogeography 30, 23932406.CrossRefGoogle Scholar
Ferraguti, M, Martínez-de la Puente, J, Bensch, S, Roiz, D, Ruiz, S, Duarte, SV, Soriguer, RC and Figuerola, J (2018) Ecological determinants of avian malaria infections: an integrative analysis at landscape, mosquito and vertebrate community levels. Journal of Animal Ecology 87, 727740.CrossRefGoogle ScholarPubMed
Ferraguti, M, Hernández-Lara, C, Sehgal, RNM and Santiago-Alarcon, D (2020) Chapter 14: anthropogenic effects on avian haemosporidians and their vectors. In Santiago-Alarcon, D and Marzal, A (eds), Avian Malaria and Related Parasites in the Tropics. Ecology, Evolution and Systematics. Switzerland AG: Springer Nature, pp. 451485. https://doi.org/10.1007/978-3-030-51633-8.CrossRefGoogle Scholar
Ferreira, FC, Santiago-Alarcon, D and Braga, ÉM (2020) Chapter 6: Diptera vectors of avian haemosporidians: with emphasis on tropical regions. In Santiago-Alarcon, D and Marzal, A (eds), Avian Malaria and Related Parasites in the Tropics. Ecology, Evolution and Systematics. Switzerland AG: Springer, pp. 185250. https://doi.org/10.1007/978-3-030-51633-8.CrossRefGoogle Scholar
Forrester, DJ and Greiner, EC (2008) Chapter 4: leucocytozoonosis. In Atkinson, CT, Thomas, NJ and Hunter, DB (eds), Parasitic Diseases of Wild Birds. Ames, Iowa: Wiley-Blackwell, pp. 54107. https://doi.org/10.1002/9780813804620.ch4.Google Scholar
Friend, M and Franson, JC (1999) Field Manual of Wildlife Diseases: General Field Procedures and Diseases of Birds. Washington, DC: National Wildlife Health Center, p. 425.Google Scholar
Fuller, T, Bensch, S, Müller, I, Novembre, J, Pérez-Tris, J, Ricklefs, RE, Smith, TB and Waldenström, J (2012) The ecology of emerging infectious diseases in migratory birds: an assessment of the role of climate change and priorities for future research. EcoHealth 9, 8088.CrossRefGoogle ScholarPubMed
Galen, SC and Witt, CC (2014) Diverse avian malaria and other haemosporidian parasites in Andean house wrens: evidence for regional co-diversification by host-switching. Journal of Avian Biology 45, 374386.CrossRefGoogle Scholar
Garamszegi, LZ (2011) Climate change increases the risk of malaria in birds. Global Change Biology 17, 17511759.10.1111/j.1365-2486.2010.02346.xCrossRefGoogle Scholar
Gosling, SN, Dunn, R, Carrol, F, Christidis, N, Fullwood, J, de Gusmao, D, Golding, N, Good, L, Hall, T, Kendon, L, Kennedy, J, Lewis, K, McCarthy, R, McSweeney, C, Morice, C, Parker, D, Perry, M, Stott, P, Willett, K, Allen, M, Arnell, N, Bernie, D, Betts, R, Bowerman, N, Brak, B, Caesar, J, Challinor, A, Dankers, R, Hewer, F, Huntingford, C, Jenkins, A, Klingaman, N, Lewis, K, Lloyd-Hughes, B, Lowe, J, McCarthy, R, Miller, J, Nicholls, R, Noguer, M, Otto, F, van der Linden, P and Warren, R (2011) Climate: Observations, Projections and Impacts: Mexico. Devon, UK: Met Office Hadley Centre.Google Scholar
Grech, MG, Manzo, LM, Epele, LB, Laurito, M, Claverie, , Ludueña-Almeida, FF, Miserendino, ML and Almirón, WR (2019) Mosquito (Diptera: Culicidae) larval ecology in natural habitats in the cold temperate Patagonia region of Argentina. Parasites & Vectors 12, 114. https://doi.org/10.1186/s13071-019-3459-y.CrossRefGoogle ScholarPubMed
Ham-Dueñas, G, Chapa-Vargas, L, Stracey, CM and Huber-Sannwald, E (2017) Haemosporidian prevalence and parasitaemia in the Black-throated sparrow (Amphispiza bilineata) in central-Mexican dryland habitats. Parasitology Research 116, 25272537.CrossRefGoogle ScholarPubMed
Harrigan, RJ, Sedano, R, Chasar, AC, Chaves, JA, Nguyen, JT, Whitaker, A and Smith, TB (2014) New host and lineage diversity of avian haemosporidia in the northern Andes. Evolutionary Applications 7, 799811.CrossRefGoogle ScholarPubMed
Hellgren, O, Waldenström, J and Bensch, S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.10.1645/GE-184R1CrossRefGoogle ScholarPubMed
Hernández-Lara, C, González-García, F and Santiago-Alarcon, D (2017) Spatial and seasonal variation of avian malaria infections in five different land use types within a Neotropical montane forest matrix. Landscape and Urban Planning 157, 151160.CrossRefGoogle Scholar
Hijmans, RJ, Cameron, SE, Parra, JL, Jones, PG and Jarvis, A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 19651978.CrossRefGoogle Scholar
Huijben, S, Schaftenaar, W, Wijsman, A, Paaijmans, K and Takken, W (2007) Avian malaria in Europe: an emerging infectious disease? In Takken, W and Knols, BGJ (eds), Emerging Pests and Vector-Borne Diseases in Europe. Wageningen: Wageningen Academic Publishers, pp. 5974. https://doi.org/10.3920/978-90-8686-626-7.Google Scholar
Ilgūnas, M, Bukauskaitė, D, Palinauskas, V, Iezhova, TA, Dinhopl, N, Nedorost, N, Weissenbacher-Lang, C, Weissenböck, H and Valkiūnas, G (2016) Mortality and pathology in birds due to Plasmodium (Giovannolaia) homocircumflexum infection, with emphasis on the exoerythrocytic development of avian malaria parasites. Malaria Journal 15, 111. https://doi.org/10.1186/s12936-016-1310-xCrossRefGoogle ScholarPubMed
Illera, JC, López, G, García-Padilla, L and Moreno, Á (2017) Factors governing the prevalence and richness of avian haemosporidian communities within and between temperate mountains. PLoS ONE 12, e0184587.CrossRefGoogle ScholarPubMed
INEGI (2008) Características edafológicas, fisiográficas, climáticas e hidrográficas de México. Instituto Nacional de Estadística y Geografía.Google Scholar
IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC. Geneva, Switzerland. 151pp.Google Scholar
Jiménez-García, D, Li, X, Lira-Noriega, A and Peterson, AT (2021) Upward shifts in elevational limits of forest and grassland for Mexican volcanoes over three decades. Biotropica 53, 798807.CrossRefGoogle Scholar
Kamiya, T, O'Dwyer, K, Nakagawa, S and Poulin, R (2013) What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Reviews 89, 123134.CrossRefGoogle ScholarPubMed
Khasnis, AA and Nettleman, MD (2005) Global warming and infectious disease. Archives of Medical Research 36, 689696.CrossRefGoogle ScholarPubMed
Krama, T, Rantala, MJ, Krams, R, Krams, IA, Cırule, D and Moore, FR (2015) Intensity of haemosporidian infection of parids positively correlates with proximity to water bodies, but negatively with host survival. Journal of Ornithology 156, 10751084.CrossRefGoogle Scholar
Kurane, I (2010) The effect of global warming on infectious diseases. Public Health and Research Perspectives 1, 49.10.1016/j.phrp.2010.12.004CrossRefGoogle ScholarPubMed
Liao, W, Atkinson, CT, LaPointe, DA and Samuel, MD (2017) Mitigating future avian malaria threats to Hawaiian forest birds from climate change. PLoS ONE 12, e0168880.CrossRefGoogle ScholarPubMed
Lindsay, SW and Martens, WJM (1998) Malaria in the African highlands: past, present, and future. Bulletin of the World Health Organization 76, 3345.Google Scholar
Liverman, DM and O'Brien, KL (1991) Global warming and climate change in Mexico. Global Environmental Change 1, 351364.CrossRefGoogle Scholar
Lobo, JM, Jiménez-Valverde, A and Real, R (2007) AUC: a misleading measure of the performance of predictive distribution models. Global Ecology and Biogeography 17, 145151.CrossRefGoogle Scholar
Loiseau, C, Harrigan, RJ, Bichet, C, Julliard, R, Garnier, S, Lendvai, AZ, Chastel, O and Sorci, G (2013) Predictions of avian Plasmodium expansion under climate change. Scientific Reports 3, 16. https://doi.org/10.1038/srep01126.CrossRefGoogle ScholarPubMed
Lotta, IA, Pacheco, MA, Escalante, AA, González, AD, Mantilla, JS, Moncada, LI, Adler, PH and Matta, NE (2016) Leucocytozoon diversity and possible vectors in the neotropical highlands of Colombia. Protist 167, 185204.CrossRefGoogle ScholarPubMed
Mandrekar, JN (2010) Receiver operating characteristic curve in diagnostic test assessment. Journal of Thoracic Oncology 5, 13151316.10.1097/JTO.0b013e3181ec173dCrossRefGoogle ScholarPubMed
Marcogliese, DJ (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Revue scientifique et technique (International Office of Epizootics) 27, 467484.Google ScholarPubMed
Martens, P, Kovats, RS, Nijhof, S, de Vries, P, Livermore, LTJ, Bradley, DJ, Cox, J and McMichael, AJ (1999) Climate change and future populations at risk of malaria. Global Environmental Change 9, S89S107.CrossRefGoogle Scholar
Massad, E, Becerra-Coutinho, FA, Fernandez-Lopez, L and Rodrigues da Silva, D (2011) Modeling the impact of global warming on vector-borne infections. Physics of Life Reviews 8, 169199.Google ScholarPubMed
McClure, KM (2017) Disease ecology of avian malaria in native and introduced birds in lowland Hawaii (Unpublished doctoral dissertation). University of California, Santa Cruz, CA, p. 140.Google Scholar
Møller, AP (2010) Host-parasite interactions and vectors in the barn swallow in relation to climate change. Global Change Biology 16, 11581170.CrossRefGoogle Scholar
Morand, S and Krasnov, BR (2010) The Biogeography of Host–Parasite Interactions. Oxford: Oxford Univ. Press, p. 288.Google Scholar
Odum, EP and Barrett, GW (2004) Fundamentals of Ecology, 5th Edn. Philadelphia: W.B. Saunders Company, pp. 624.Google Scholar
Ojogba, OM, Emmanuel, NN, Ikenna, OK and Okokon, I (2012) Will climate change affect parasite-host relationship? Jos Journal of Medicine 6, 2731.Google Scholar
Osorio-Olvera, L, Lira-Noriega, A, Soberón, J, Peterson, AT, Falconi, M, Contreras-Díaz, RG, Martínez-Meyer, E, Barve, V and Barve, N (2020) ntbox: an R package with graphical user interface for modeling and evaluating multidimensional ecological niches. Methods in Ecology and Evolution 11, 11991206.CrossRefGoogle Scholar
Paaijmans, KP and Thomas, MB (2013) Relevant temperatures in mosquito and malaria biology. In Takken, W and Koenraadt, CJM (eds). Ecology of Parasite-Vector Interactions. Ecology and Control of Vector-Borne Diseases, vol. 3. Wageningen, The Netherlands: Wageningen Academic Publishers, pp. 103121. http://dx.doi.org/10.3920/978-90-8686-744-8.CrossRefGoogle Scholar
Pacheco, MA, Cepeda, AS, Bernotiene, R, Lotta, IA, Matta, NE, Valkiūnas, G and Escalante, AA (2018) Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. International Journal for Parasitology 48, 657670.CrossRefGoogle ScholarPubMed
Patz, JA and Reisen, WK (2001) Immunology, climate change and vector-borne diseases. TRENDS in Immunology 22, 171172.CrossRefGoogle ScholarPubMed
Peterson, AT, Ortega-Huerta, MA, Bartley, J, Sánchez-Cordero, V, Soberón, J, Buddemeier, RH and Stockwell, DRB (2002) Future projections for Mexican faunas under global climate change scenarios. Nature 416, 626629.10.1038/416626aCrossRefGoogle ScholarPubMed
Peterson, AT, Papeş, M and Soberón, J (2008) Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Elsevier Ecological Modelling 213, 6372.CrossRefGoogle Scholar
Phillips, SJ, Anderson, RP and Schapire, RE (2006) Maximum entropy modeling of species geographic distributions. Elsevier Ecological Modelling 190, 231259.CrossRefGoogle Scholar
Ponce-Reyes, R, Reynoso-Rosales, VH, Watson, JEM, Jeremy VanDerWal, J, Fuller, RA, Pressey, RL and Possingham, HP (2012) Vulnerability of cloud forest reserves in Mexico to climate change. Nature Climate Change 2, 448452.CrossRefGoogle Scholar
Ponce-Reyes, R, Plumptre, AJ, Segan, D, Ayebare, S, Fuller, RA, Possingham, HP and Watson, JEM (2017) Forecasting ecosystem responses to climate change across Africa's Albertine Rift. Biological Conservation 209, 464472.CrossRefGoogle Scholar
Prieto-Torres, DA, Rojas-Soto, O and Lira-Noriega, A (2020) Chapter 7: ecological niche modeling and other tools for the study of avian malaria distribution in the Neotropics: a short literature review. In Santiago-Alarcon, D and Marzal, A (eds), Avian Malaria and Related Parasites in the Tropics. Cham, Switzerland: Springer Nature, pp. 251280. https://doi.org/10.1007/978-3-030-51633-8.CrossRefGoogle Scholar
Ramey, AM, Reed, JA, Schmutz, JA, Fondell, TF, Meixell, BW, Hupp, JW, Ward, DH, Terenzi, J and Ely, CR (2014) Prevalence, transmission, and genetic diversity of blood parasites infecting tundra-nesting geese in Alaska. Canadian Journal of Zoology 92, 699706.CrossRefGoogle Scholar
R Core-Team (2013). R: a language and environment for statistical computing [Software]. R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Reinoso-Pérez, MT, Canales-Delgadillo, JC, Chapa-Vargas, L and Riego-Ruiz, L (2016) Haemosporidian parasite prevalence, parasitemia, and diversity in three resident bird species at a shrubland dominated landscape of the Mexican highland plateau. Parasites & Vectors 9, 112.CrossRefGoogle Scholar
Riahi, K, Grübler, A and Nakicenovic, N (2007) Scenarios of long-term socio-economic and environmental development under climate stabilization. Technological Forecasting & Social Change 74, 887935.CrossRefGoogle Scholar
Riahi, K, Rao, S, Krey, V, Cho, C, Chirkov, V, Fischer, G, Kindermann, G, Nakicenovic, N and Rafaj, P (2011) RCP 8.5 – a scenario of comparatively high greenhouse gas emissions. Climatic Change 109, 3357.CrossRefGoogle Scholar
Robles-Fernández, ÁL, Santiago-Alarcon, D and Lira-Noriega, A (2021) American mammals susceptibility to dengue according to geographical, environmental, and phylogenetic distances. Frontiers in Veterinary Science 8. https://doi.org/10.3389/fvets.2021.604560.CrossRefGoogle ScholarPubMed
Rodríguez-Hernández, K, Álvarez-Mendizábal, P, Chapa-Vargas, L, Escobar, F, González-García, F and Santiago-Alarcon, D (2021) Haemosporidian prevalence, parasitemia and aggregation in relation to avian assemblage life history traits at different elevations. International Journal for Parasitology 51, 365378.CrossRefGoogle Scholar
Rooyen, JV, Lalubin, F, Glaizot, O and Christe, P (2013) Altitudinal variation in haemosporidian parasite distribution in great tit populations. Parasites & Vectors 6, 1–10. https://doi.org/10.1186/1756-3305-6-139.CrossRefGoogle ScholarPubMed
Ryan, BF, Ryan, TA Jr and Joiner, BL (2013) Minitab 17.1.0 Statistical Software [Software]. State College, PA: Minitab, Inc. https://www.minitab.com.Google Scholar
Rzedowski, J (1965) Vegetación del estado de San Luis Potosí. San Luis Potosí: Universidad Autónoma de San Luis Potosí, pp. 291. http://books.google.com/books?id=8kcQAQAAMAAJ.Google Scholar
Samuel, MD, Hobbelen, PHF, DeCastro, F, Ahumada, JA, LaPointe, D, Atkinson, CT, Woodworth, BL, Hart, PJ and Daffy, DC (2011) The dynamics, transmission, and population impacts of avian malaria in native Hawaiian birds: a modeling approach. Ecological Applications 21, 29602973.CrossRefGoogle Scholar
Santiago-Alarcon, D and Carbó-Ramírez, P (2015) Parásitos sanguíneos de malaria y géneros relacionados (orden: Haemosporida) en aves de México: recomendaciones metodológicas para campo y laboratorio. Ornitología Neotropical 26, 5977.Google Scholar
Santiago-Alarcon, D, Palinauskas, V and Schaefer, HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928964.CrossRefGoogle ScholarPubMed
Schröder, W and Schmidt, G (2008) Mapping the potential temperature-dependent tertian malaria transmission within the ecoregions of Lower Saxony (Germany). International Journal of Medical Microbiology 298, 3849.CrossRefGoogle Scholar
Sehgal, RNM, Buermann, W, Harrigan, RJ, Bonneaud, C, Loiseau, C, Chasar, A, Sepil, I, Valkiūnas, G, Iezhova, TA, Saatchi, S and Smith, TB (2011) Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird. Proceedings of the Royal Society 278, 10251033.Google Scholar
SEMARNAT-INECC (2016) Mexico's Climate Change Mid-Century Strategy, 1st Edn Ministry of Environment and Natural Resources (SEMARNAT) and National Institute of Ecology and Climate Change (INECC), México City México, p. 106.Google Scholar
SEMARNAT (2016) Informe de la Situación del Medio Ambiente en México. Compendio de Estadísticas Ambientales. Indicadores Clave y de Desempeño Ambiental, Edición 2015. México: Secretaría de Medio Ambiente y Recursos Naturales, p. 498. In process.Google Scholar
Smith, SJ and Wigley, TML (2006) Multi-gas forcing stabilization with Minicam. The Energy Journal 27, 373391. https://www.jstor.org/stable/23297091.Google Scholar
Smith, MM, Van Hemert, C and Merizon, R (2016) Haemosporidian parasite infections in grouse and ptarmigan: prevalence and genetic diversity of blood parasites in resident Alaskan birds. International Journal for Parasitology: Parasites and Wildlife 5, 229239.Google ScholarPubMed
Sprygin, AV, Fiodorova, OA, Babin, YY, Elatkin, NP, Mathieu, B, England, ME and Kononov, AV (2014) Culicoides biting midges (Diptera, Ceratopogonidae) in various climatic zones of Russia and adjacent lands. Journal of Vector Ecology 39, 306315.CrossRefGoogle ScholarPubMed
Stresman, GH (2010) Beyond temperature and precipitation: ecological risk factors that modify malaria transmission. Acta Tropica 116, 167172.CrossRefGoogle ScholarPubMed
Thomson, AM, Calvin, KV, Smith, SJ, Kyle, GP, Volke, A, Patel, P, Delgado-Arias, S, Bond-Lamberty, B, Wise, MA, Clarke, LE and Edmonds, JA (2010) RCP4.5: a pathway for stabilization of radiative forcing by 2100. Climatic Change 109, 7794.CrossRefGoogle Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia, 1st Edn. Boca Raton, Florida: CRC Press, p. 946.Google Scholar
Wanji, S, Tayong, DB, Ebai, R, Opoku, V, Kien, CA, Ndongmo, WPC, Njouendou, AJ, Ghani, RN, Ritter, M, Debrah, YA, Layland, LE, Enyong, PA and Hoerauf, A (2019) Update on the biology and ecology of Culicoides species in the South-West region of Cameroon with implications on the transmission of Mansonella perstans. Parasites & Vectors 12, 112. https://doi.org/10.1186/s13071-019-3432-9.CrossRefGoogle ScholarPubMed
Wayne, GP (2013) The beginner's guide to representative concentration pathways.Google Scholar
Whitford, WG and Duval, BD (2019) Chapter 12 – desertification. In Whitford, WG and Duval, BD (eds), Ecology of Desert Systems. London: Academic Press, pp. 371395. https://doi.org/10.1016/B978-0-12-815055-9.00012-6.Google Scholar
Wise, MA, Calvin, K, Thomson, A, Clarke, LE, Bond-Lamberty, B, Sands, R, Smith, SJ, Janetos, A and Edmonds, JA (2009) Implications of limiting CO2 concentrations for land use and energy. Science 324, 11831186.CrossRefGoogle Scholar
Zamora-Vilchis, I, Williams, SE and 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, 1–8. https://doi.org/10.1371/journal.pone.0039208.CrossRefGoogle Scholar