Descubriendo la biodiversidad de parásitos en los Trópicos: Un marco de referencia basado en modelos de nicho ecológico de múltiples especies hospedadoras

Diego Santiago, Octavio Rafael Rojas-Soto


The current threats to biodiversity imposed by human activities highlights the need to focus efforts not only in conserving what we already know, but also in the discovery of new species, particularly of poorly known but ecologically important groups such as parasites and underground fauna. Focusing on parasites, we must consider that their hosts represent their entire habitat, that most host species are infected by more than one parasite species, and that many studies have shown that some host traits (e.g., host body size, geographic range) and host diversity in general are positively correlated with parasite diversity. Thus, host diversity can be a surrogate for parasite diversity, where we would always expect higher parasite species richness than host species richness. Here, we propose a framework using multi-host-species ecological niche models – i.e., stacked species distribution models – or alternatively, the use of host joint species distribution models to guide parasite biodiversity discovery studies. We suggest then to focusing biodiversity surveys on areas with high host species richness and endemicity, which will help making use of limited economic resources because it will concentrate field surveys in
areas with a higher likelihood of parasite discovery (e.g., host diversity hotspots that provide larger habitat heterogeneity for parasites).

Palabras clave

biotic interactions, ecological niche, host communities, parasite assemblages, vector-borne diseases

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Barve N, Barve V, Jiménez-Valverde A, Lira-Noriega A, Maher SP, Peterson AT, Soberón J & Villalobos F. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222: 1810–1819.

Bordes F, Morand S, Krasnov BR & Poulin R. 2010. Para site diversity and latitudinal gradients in terrestrial mammals. In: Morand S & Krasnov B (Eds.) The biogeography of host-parasite interactions, Oxford University Press, New York, USA, pp. 89–98.

Brooks DR. 1985. Historical ecology: a new approach to studying the evolution of ecological associations. Annals of the Missouri Botanical Garden 72: 660–680.

Brooks DR, McLennan DA & McLennan DA. 1991. Phylogeny, ecology, and behavior: a research program in comparative biology. University of Chicago press, Chicago, USA.

Bush AO, Lafferty KD, Lotz JM & Shostak AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of parasitology 83: 575–583.

Carlson CJ, Burgio KR, Dougherty ER, Phillips AJ, Bueno VM, Clements CF, Castaldo G, Dallas TA, Cizauskas CA, Cumming GS et al. 2017. Parasite biodiversity faces extinction and redistribution in a changing climate. Science Advances 3: e1602422.

Carlson CJ, Dallas TA, Alexander LW, Phelan AL & Phillips AJ. 2020a. What would it take to describe the global diversity of parasites? Proceedings of the Royal Society B 287: 20201841.

Carlson CJ, Hopkins S, Bell KC, Doña J, Godfrey SS, Kwak ML, Lafferty KD, Moir ML, Speer KA, Strona G et al. 2020b. A global parasite conservation plan. Biological Conservation 250: 108596.

Cheviron Z, Hackett SJ & Capparella AP. 2005. Complex evolutionary history of a Neotropical lowland forest bird (Lepidothrix coronata) and its implications for historical hypotheses of the origin of Neotropical avian diversity. Molecular Phylogenetics and Evolution 36: 338–357.

Clark NJ. 2018. Phylogenetic uniqueness, not latitude, explains the diversity of avian blood parasite communities worldwide. Global Ecology and Biogeography 27: 744–755.

Clark NJ & Clegg SM. 2017. Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity. Molecular Ecology 26: 3074–3086.

Clark NJ, Clegg SM & Lima MR. 2014. A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology 44: 329–338.

Currie DJ, Mittelbach GG, Cornell HV, Field R, Guégan JF, Hawkins BA, Kaufman DM, Kerr JT, Oberdorff T, O’Brien E et al. 2004. Predictions and tests of climatebased hypotheses of broad-scale variation in taxonomic richness. Ecology letters 7: 1121–1134.

Dunn RR, Harris NC, Colwell RK, Koh LP & Sodhi NS. 2009. The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society B: Biological Sciences 276: 3037–3045.

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. Journal of Animal Ecology 89: 423–435.

Fecchio A, Pinheiro R, Felix G, Faria I, Pinho J, Lacorte G, Braga E, Farias I, Aleixo A, Tkach V et al. 2018. Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds. Ecography 41: 505–515.

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. Ecology letters 22: 547–557.

Gómez A & Nichols E. 2013. Neglected wildlife: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife 2: 222–227.

Gutiérrez JS, Rakhimberdiev E, Piersma T & Thieltges DW. 2017. Migration and parasitism: habitat use, not migration distance, influences helminth species richness in Charadriiform birds. Journal of Biogeography 44: 1137–1147.

Hatcher MJ & Dunn AM. 2011. Parasites in ecological communities: from interactions to ecosystems. Cambridge University Press, Cambridge, UK.

Hawkins BA, Diniz-Filho JAF, Jaramillo CA & Soeller SA. 2006. Post-Eocene climate change, niche conservatism, and the latitudinal diversity gradient of New World birds. Journal of Biogeography 33: 770–780.

Hawkins BA, Diniz-Filho JAF, Jaramillo CA & Soeller SA. 2007. Climate, niche conservatism, and the global bird diversity gradient. The American Naturalist 170: S16–S27.

Hawkins BA, Field R, Cornell HV, Currie DJ, Guégan JF, Kaufman DM, Kerr JT, Mittelbach GG, Oberdorff T, O’Brien EM et al. 2003a. Energy, water, and broad-scale geographic patterns of species richness. Ecology 84: 3105–3117.

Hawkins BA, Porter EE & Felizola Diniz-Filho JA. 2003b. Productivity and history as predictors of the latitudinal diversity gradient of terrestrial birds. Ecology 84: 1608–1623.

Hechinger RF & Lafferty KD. 2005. Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B: Biological Sciences 272: 1059–1066.

Hoberg EP, Brooks DR, Siegel-Causey D et al. 1997. Hostparasite co-speciation: history, principles, and prospects. In: Clayton D & Moore J (Eds.) Host–Parasite Evolution: General Principles and Avian Models, Oxford University Press, Oxford, UK, pp. 212–235.

Ilgūnas M, Chagas CRF, Bukauskaitė D, Bernotienė R, Iezhova T & Valkiūnas G. 2019. The life-cycle of the avian haemosporidian parasite Haemoproteus majoris, with emphasis on the exoerythrocytic and sporogonic development. Parasites & Vectors 12: 1–15.

Ishtiaq F & Renner SC. 2020. Bird migration and vector-borne parasite transmission. In: Santiago-Alarcon D & Marzal A (Eds.) Avian malaria and related parasites in the tropics: Ecology, Evolution and Systematics, Springer International Publishing, Cham, Switzerland, pp. 513–526.

Jetz W, Thomas GH, Joy JB, Hartmann K & Mooers AO. 2012. The global diversity of birds in space and time. Nature 491: 444–448.

Johnson PT, Wood CL, Joseph MB, Preston DL, Haas SE & Springer YP. 2016. Habitat heterogeneity drives the hostdiversity-

begets-parasite-diversity relationship: evidence from experimental and field studies. Ecology Letters 19: 752–761.

Kattan GH & Franco P. 2004. Bird diversity along elevational gradients in the Andes of Colombia: area and mass effects. Global Ecology and Biogeography 13: 451–458.

Krasnov BR, Shenbrot GS, van der Mescht L, Warburton EM & Khokhlova IS. 2019. Phylogenetic and compositional diversity are governed by different rules: a study of fleas parasitic on small mammals in four biogeographic realms. Ecography 42: 1000–1011.

Kwak ML, Heath AC & Cardoso P. 2020. Methods for the assessment and conservation of threatened animal parasites. Biological Conservation 248: 108696.

Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PT, Kuris AM, Marcogliese DJ et al. 2008. Parasites in food webs: the ultimate missing links. Ecology Letters 11: 533–546.

Leung TL & Koprivnikar J. 2016. Nematode parasite diversity in birds: the role of host ecology, life history and migration. Journal of Animal Ecology 85: 1471–1480.

Lobo JM, Jiménez-Valverde A & Hortal J. 2010. The uncertain nature of absences and their importance in species distribution

modelling. Ecography 33: 103–114.

Lovette I & Fitzpatrick J. 2011. Handbook of bird biology. Wiley-Blackwell. Chichester, West Sussex, UK.

Marcogliese DJ. 2005. Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35: 705–716.

Maxwell SL, Fuller RA, Brooks TM & Watson JE. 2016. Biodiversity: The ravages of guns, nets and bulldozers. Nature News 536: 143.

McQuaid C & Britton N. 2013. Host–parasite nestedness: a result of co-evolving trait-values. Ecological Complexity 13: 53–59.

Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA et al. 2007. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters 10: 315–331.

Ovaskainen O & Abrego N. 2020. Joint species distribution modelling: with applications in R. Cambridge University Press, Cambridge, UK.

Owens HL, Campbell LP, Dornak LL, Saupe EE, Barve N, Soberón J, Ingenloff K, Lira-Noriega A, Hensz CM, Myers CE et al. 2013. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecological Modelling 263: 10–18.

Pacheco MA & Escalante AA. 2020. Cophylogenetic Patterns and Speciation in Avian Haemosporidians. In: Santiago-Alarcon D & Marzal A (Eds.) Avian malaria and related parasites in the tropics: Ecology, Evolution and Systematics, Springer International Publishing, Cham, Switzerland, pp. 401–427.

Pappalardo P, Morales-Castilla I, Park AW, Huang S, Schmidt JP & Stephens PR. 2020. Comparing methods for mapping global parasite diversity. Global Ecology and Biogeography 29: 182–193.

Peterson AT, Soberón J, Pearson RG, Anderson RP, Martínez-Meyer E, Nakamura M & Araújo MB. 2011. Ecological niches and geographic distributions (MPB-49). Princeton University Press, New Jersey, USA.

Poulin R. 2011. The many roads to parasitism: a tale of convergence. Advances in Parasitology 74: 1–40.

Poulin R. 2014. Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology 44: 581–589.

Poulin R, Guilhaumon F, Randhawa HS, Luque JL & Mouillot D. 2011. Identifying hotspots of parasite diversity from species–area relationships: host phylogeny versus host ecology. Oikos 120: 740–747.

Poulsen BO & Krabbe N. 1997. The diversity of cloud forest birds on the eastern and western slopes of the Ecuadorian Andes:

a latitudinal and comparative analysis with implications for conservation. Ecography 20: 475–482.

Prieto-Torres DA, Rojas-Soto O & Lira-Noriega A. 2020. Ecological Niche Modeling and Other Tools for the Study of Avian Malaria Distribution in the Neotropics: A Short Literature Review. In: Santiago-Alarcon D & Marzal A (Eds.) Avian malaria and related parasites in the tropics: Ecology, Evolution and Systematics, Springer International Publishing, Cham, Switzerland, pp. 251–280.

Prieto-Torres DA, Rojas-Soto OR, Bonaccorso E, Santiago-Alarcon D & Navarro-Sigüenza AG. 2019a. Distributional patterns of Neotropical seasonally dry forest birds: a biogeographical regionalization. Cladistics 35: 446–460.

Prieto-Torres DA, Rojas-Soto OR, Santiago-Alarcon D, Bonaccorso E & Navarro-SigüEnza AG. 2019b. Diversity, endemism, species turnover and relationships among avifauna of neotropical seasonally dry forests. Ardeola 66: 257–277.

Proctor H & Owens I. 2000. Mites and birds: diversity, parasitism and coevolution. Trends in Ecology & Evolution 15: 358–364.

Rahbek C. 1995. The elevational gradient of species richness: a uniform pattern? Ecography 18: 200–205.

Rahbek C. 1997. The relationship among area, elevation, and regional species richness in neotropical birds. The American Naturalist 149: 875–902.

Rahbek C & Graves G. 2001. Multiscale assessment of patterns of avian species richness. Proceedings of the National Academy of Sciences of the USA 98: 4534–4539.

Ricklefs RE. 2004. A comprehensive framework for global patterns in biodiversity. Ecology Letters 7: 1–15.

Rohde K. 1992. Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65: 514–527.

Roth RR. 1976. Spatial heterogeneity and bird species diversity. Ecology 57: 773–782.

Santiago-Alarcon D & Marzal A. 2020. Avian Malaria and Related Parasites in the Tropics: Ecology, Evolution and Systematics.

Springer International Publishing, Cham, Switzerland.

Santiago-Alarcon D, Rodríguez-Ferraro A, Parker PG & Ricklefs RE. 2014. Different meal, same flavor: cospeciation and host switching of haemosporidian parasites in some nonpasserine birds. Parasites & Vectors 7: 1–9.

Scordato ES & Kardish MR. 2014. Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. Journal of Animal Ecology 83: 1387–1397.

Stephens PR, Altizer S, Smith KF, Alonso Aguirre A, Brown JH, Budischak SA, Byers JE, Dallas TA, Jonathan Davies T, Drake JM et al. 2016. The macroecology of infectious diseases: A new perspective on global-scale drivers of pathogen

distributions and impacts. Ecology letters 19: 1159–1171.

Strona G. 2015. Past, present and future of host–parasite coextinctions. International Journal for Parasitology: Parasites and Wildlife 4: 431–441.

Terborgh J. 1971. Distribution on environmental gradients: theory and a preliminary interpretation of distributional patterns in the avifauna of the Cordillera Vilcabamba, Peru. Ecology 52: 23–40.

Terborgh J. 1985. The role of ecotones in the distribution of Andean birds. Ecology 66: 1237–1246.

Terborgh J & Weske JS. 1975. The role of competition in the distribution of Andean birds. Ecology 56: 562–576.

Vuilleumier F. 1970. Insular biogeography in continental regions. I. The northern Andes of South America. The American Naturalist

: 373–388.

Wood CL, Summerside M & Johnson PT. 2020. How host diversity and abundance affect parasite infections: Results from a whole-ecosystem manipulation of bird activity. Biological Conservation 248: 108683.

Wright DH. 1993. Energy supply and patterns of species richness on local and regional scales. In: Ricklefs R & Santiago-Alarcon D (Eds.) Species diversity in ecological communities: historical and geographical perspectives, University of Chicago Press, Chicago, USA, pp. 66–74.

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