The ecological niche of Echinococcus multilocularis in North America: understanding biotic and abiotic determinants of parasite distribution with new records in New Mexico and Maryland, United States

Autores/as

  • Sebastian Botero-Cañola University of Nebraska - Lincoln
  • Altangerel T. Dursahinhan
  • Sara E. Racz
  • Parker V. Lowe
  • John E. Ubelaker
  • Scott L. Gardner

Palabras clave:

Carnivora, disease geography, Echinococcosis, Echinococcus multilocularis, ecological niche model, maxent, Nearctic, parasite, Rodentia, multivariate statistics.

Resumen

Understanding the factors shaping the niche of parasites and its expression over geographical space and through time continues to be a modern scientific challenge with the results of research in this area directly influencing both theoretical and applied biology. This is especially important for proactive management of zoonotic parasites such as Echinococcus multilocularis, the etiologic agent of alveolar echinococcosis. Echinococcus multilocularis has a Holarctic distribution; with its geographic range and prevalence increasing recently in areas of the western Palearctic, while its distribution dynamics are poorly understood in the Nearctic. In this paper, we use an ecological niche modeling (ENM) approach to: i) estimate the current spatial distribution of suitable conditions for the parasite in the Nearctic. ii) Evaluate the abiotic and biotic factors influencing the species distribution. iii) Assess the potential impact of climatic change on the distribution of this species in the Nearctic. Additionally, we report two new occurrence records of this parasite that significantly expands its known geographic range. We reviewed the occurrence records of E. multilocularis for the Nearctic. This was complemented by two new records of the species from Maryland and New Mexico identified using morphology and multivariate morphometrics of the rostellar hooks. From these data we created two ENMs using the software Maxent. The first ENM included climatic variables, while the second included the same abiotic data plus biotic information consisting of four host community-related data sets. We evaluated model performance and variable importance to explore the relation of these variables to the parasite niche. Finally, we projected the resulting niche model onto future climate change scenarios. We found that an important portion of the Nearctic has suitable conditions for E. multilocularis with adequate habitat in the West and East of the continent where the parasite has not been detected. We also found that the proposed biotic variables improve the model performance and provide unique information, while the most critical abiotic variable was related to the amount of solar radiation. Finally, under the future emission scenarios explored, the distribution of suitable habitat for the parasite is predicted to increase by 56 % to 76 %. We obtained a robust model that provides detail on the distribution of suitable areas for E. multilocularis, including areas that have not been explored for the presence of the parasite. The host community variables included in this study seem a promising way to include biotic data for ecological parasite niche modeling.

Biografía del autor/a

Sebastian Botero-Cañola, University of Nebraska - Lincoln

School of Biological Sciences.Estudiante de doctorado

Citas

Aiello-Lammens, M. E., R. A. Boria, A. Radosavljevic, B. Vilela, and R. P. Anderson. 2015. spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38:541–545.

Almasieh, K., M. Kaboli, and P. Beier. 2016. Identifying habitat cores and corridors for the Iranian black bear in Iran. Ursus 27:18–30.

Anderson, R. P. 2017. When and how should biotic interactions be considered in models of species niches and distributions? Journal of Biogeography 44:8–17.

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

Brooks, D. R., and D. A. Mclennan. 1993. Parascript: Parasites and the language of evolution. Smithsonian Institution Press, Washington D.C.

Brooks, D. R., and W. A. Boeger. 2019. Climate change and emerging infectious diseases: Evolutionary complexity in action. Current Opinions in Systems Biology 13:75-81.

Brooks, D. R., E. P. Hoberg, W. A. Boeger, S. L. Gardner, K. E. Galbreath, D. Herczeg, H. H. Mejía-Madrid, S. E. Rácz, and A. T. Dursahinhan. 2014. Finding them before they find us: Informatics, parasites, and environments in accelerating climate change. Comparative Parasitology 81:155–164.

Brooks, D. R., and E. P. Hoberg. 2007. How will global climate change affect parasite – host assemblages? Trends in Parasitology 23:27–30.

Brownstein, J. S., T. R. Holford, and D. Fish. 2005. Effect of Climate Change on Lyme Disease Risk in North America. EcoHealth 2:38–46.

Budke, C. M., A. Casulli, P. Kern, and D. A. Vuitton. 2017. Cystic and alveolar echinococcosis: Successes and continuing challenges. PLOS Neglected Tropical Diseases 11:e0005477.

Campbell, L. P., C. Luther, D. Moo-Llanes, J. M. Ramsey, R. Danis-Lozano, and A. T. Peterson. 2015. Climate change influences on global distributions of dengue and chikungunya virus vectors. Philosophical Transactions of the Royal Society: Biological Sciences 370:20140135–20140135.

Chapman, A. D., and J. Wieczorek (eds.). 2006. Guide to Best Practices for Georeferencing. Copenhagen: Global Biodiversity Information Facility.

Chetan, N., K. K. Praveen, and G. K. Vasudeva. 2014. Delineating ecological boundaries of hanuman langur species complex in peninsular India using MaxEnt modeling approach. PLoS ONE 9:1–11.

Civitello, D. J., J. Cohen, H. Fatima, N. T. Halstead, J. Liriano, T. A. Mcmahon, C. N. Ortega, E. L. Sauer, T. Sehgal, S. Young, and J. R. Rohr. 2015. Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proceedings of the National Academy of Sciences 112:8667–8671.

Da Silva, A. M. 2010. Human echinococcosis: A neglected disease. Gastroenterology Research and Practice 2010:583297.

Davidson, R. K., A. Lavikainen, S. Konyaev, J. Schurer, A. L. Miller, A. Oksanen, K. Skírnisson, and E. Jenkins. 2016. Echinococcus across the north: Current knowledge, future challenges. Food and Waterborne Parasitology 4:39–53.

Elith, J., C. H. Graham, R. P. Anderson, M. Dudík, S. Ferrier, A. Guisan, R. J. Hijmans, F. Huettmann, J. R. Leathwick, A. Lehmann, J. Li, L. G. Lohmann, B. A. Loiselle, G. Manion, C. Moritz, M. Nakamura, Y. Nakazawa, J. M. M. Overton, A. T. Peterson, S. J. Phillips, K. Richardson, R. Scachetti-Pereira, R. E. Schapire, J. Soberón, S. Williams, M. S. Wisz, and N. E. Zimmermann. 2006. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151.

Elith, J., S. J. Phillips, T. Hastie, M. Dudík, Y. E. Chee, and C. J. Yates. 2011. A statistical explanation of MaxEnt for ecologists. Diversity and Distributions 17:43–57.

Escobar, L. E., and M. E. Craft. 2016. Advances and limitations of disease biogeography using ecological niche modeling. Frontiers in Microbiology 7:1–21.

Estrada-Peña, A., R. S. Ostfeld, A. T. Peterson, R. Poulin, and J. De La Fuente. 2014. Effects of environmental change on zoonotic disease risk: an ecological primer. Trends in Parasitology 30:205–14.

Fick, S. E., and Hijmans, R. J. 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37:4302–4315.

Filz, K. J., and T. Schmitt. 2015. Niche overlap and host specificity in parasitic Maculinea butterflies (Lepidoptera: Lycaenidae) as a measure for potential extinction risks under climate change. Organisms Diversity and Evolution 15:555–565.

Fourcade, Y., J. O. Engler, D. Rödder, and J. Secondi. 2014. Mapping species distributions with MAXENT using a geographically biased sample of presence data: A performance assessment of methods for correcting sampling bias. PLoS ONE 9:1–13.

Gardner, S. L., A. T. Dursahinhan, G. R. Rácz, N. Batsaikhan, and S. Ganzorig. 2013. Sylvatic species of Echinococcus from rodent intermediate hosts in Asia and South America. Occasional Papers, Museum of Texas Tech University 318:1–13.

Gardner, S. L., and G. D. Schmidt. 1988. Cestodes of the genus Hymenolepis Weinland, 1858 sensu stricto from pocket gophers Geomys and Thomomys spp. [Rodentia: Geomyidae] in Colorado and Oregon, with a discriminant analysis of four species of Hymenolepis. Canadian Journal of Zoology 66: 896-903.

Gesy, K. M., J. M. Schurer, A. Massolo, S. Liccioli, B. T. Elkin, R. Alisauskas, and E. J. Jenkins. 2014. Unexpected diversity of the cestode Echinococcus multilocularis in wildlife in Canada. International Journal for Parasitology: Parasites and Wildlife 3:81–87.

Giannini, T. C., D. S. Chapman, A. M. Saraiva, I. Alves-Dos-Santos, and J. C. Biesmeijer. 2013. Improving species distribution models using biotic interactions: a case study of parasites, pollinators and plants. Ecography 36:649–656.

Harrison, D. J. 1992. Dispersal Characteristics of Juvenile Coyotes in Maine. The Journal of Wildlife Management 56:128–138.

Haverkost, T. R., S. L. Gardner, and A. T. Peterson. 2010. Predicting the distribution of a parasite using the ecological niche model, GARP Predicción de la distribución de un parásito usando el modelo de nicho ecológico, GARP. Revista Mexicana de Biodiversidad 81:895–902.

Hill, N. J., A. J. Tobin, A. E. Reside, J. G. Pepperell, and T. C. L. Bridge. 2016. Dynamic habitat suitability modelling reveals rapid poleward distribution shift in a mobile apex predator. Global Change Biology 22:1086–1096.

Iucn. 2016. The IUCN Red List of Threatened Species. Version 2016-1.

Kern, P., A. M. Da Silva, O. Akhan, B. Müllhaupt, K. A. Vizcaychipi, C. Budke, and D. A. Vuitton. 2017. The echinococcoses: diagnosis, clinical management and burden of disease. Advances in parasitology 96:259-369.

Kramer-Schadt, S., J. Niedballa, J. D. Pilgrim, B. Schröder, J. Lindenborn, V. Reinfelder, M. Stillfried, I. Heckmann, A. K. Scharf, D. M. Augeri, S. M. Cheyne, A. J. Hearn, J. Ross, D. W. Macdonald, J. Mathai, J. Eaton, A. J. Marshall, G. Semiadi, R. Rustam, H. Bernard, R. Alfred, H. Samejima, J. W. Duckworth, C. Breitenmoser-Wuersten, J. L. Belant, H. Hofer, and A. Wilting. 2013. The importance of correcting for sampling bias in MaxEnt species distribution models. Diversity and Distributions 19:1366–1379.

Kriticos, D. J., V. Jarošik, and N. Ota. 2014. Extending the suite of bioclim variables: a proposed registry system and case study using principal components analysis. Methods in Ecology and Evolution 5:956–960.

Kuhn, T., S. Cunze, J. Kochmann, and S. Klimpel. 2016. Environmental variables and definitive host distribution: a habitat suitability modelling for endohelminth parasites in the marine realm. Scientific Reports 6:30246.

Lass, A., B. Szostakowska, P. Myjak, and K. Korzeniewski. 2015. The first detection of Echinococcus multilocularis DNA in environmental fruit, vegetable, and mushroom samples using nested PCR. Parasitology Research 114:4023–4029.

Leiby, P. D., and D. C. Kritsky. 1972. Echinococcus multilocularis: a possible domestic life cycle in central North America and its public health implications. Journal of Parasitology 58:1213–1215.

Leiby, P. D., and O. W. Olsen. 1964. The cestode Echinococcus multilocularis in foxes in North Dakota. Science 145:1066.

Manter, H. W. 1966. Parasites of fishes as biological indicators of recent and ancient conditions. Pp. 59-71 in Host-Parasite Relationships. (McCauley, J. E. Ed.). Oregon State University Press, Corvallis, Oregon, USA.

Massolo, A., S. Liccioli, C. Budke, and C. Klein. 2014. Echinococcus multilocularis in North America: the great unknown. Parasite 21:73.

Muscarella, R., P. J. Galante, M. Soley-Guardia, R. A. Boria, J. M. Kass, M. Uriarte, and R. P. Anderson. 2014. ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution 5:1198–1205.

Nakao, M., N. Xiao, M. Okamoto, T. Yanagida, Y. Sako, and A. Ito. 2009. Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitology International 58:384–389.

Norris, D. 2014. Model thresholds are more important than presence location type: Understanding the distribution of lowland tapir (Tapirus terrestris) in a continuous Atlantic forest of southeast Brazil. Tropical Conservation Science 7:529–547.

Nylin, S., S. Agosta, S. Bensch, W. A. Boeger, M. P. Braga, D. R. Brooks, M. L. Forister, P. A. Hambäck, E. P. Hoberg, T. Nyman, A. Schäpers, A. L. Stigall, C. W. Wheat, M. Österling, and N. Janz. 2018. Embracing Colonizations: A New Paradigm for Species Association Dynamics. Trends in Ecology and Evolution 33:4–14.

Ostfeld, R. S., and J. L. Brunner. 2015. Climate change and Ixodes tick-borne diseases of humans. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences 370:20140051.

Pandey, R., and M. Papeş. 2018. Changes in future potential distributions of apex predator and mesopredator mammals in North America. Regional Environmental Change 18:1223–1233.

Peterson, A. T., M. PapeÅŸ, and J. Soberón. 2008. Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecological Modelling 213:63–72.

Peterson, A. T., and J. Soberón. 2012. Species distribution modeling and ecological niche modeling: getting the concepts right. Natureza and Conservação, 10:102–107.

Phillips, S. J., R. P. Anderson, and R. E. Schapire. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190:231–259.

Phillips, S. J., and M. Dudík. 2008. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175.

Phillips, S. J., M. Dudík, and R. E. Schapire. 2017. [Internet] Maxent software for modeling species niches and distributions (Version 3.4.1). http://biodiversityinformatics.amnh.org/open_source/maxent/> (June 11, 2018).

Pickles, R. S. A., D. Thornton, R. Feldman, A. Marques, and D. L. Murray. 2013. Predicting shifts in parasite distribution with climate change: A multitrophic level approach. Global Change Biology 19:2645–2654.

Radosavljevic, A., and R. P. Anderson. 2014. Making better Maxent models of species distributions: Complexity, overfitting and evaluation. Journal of Biogeography 41:629–643.

Raes, N., M. C. Roos, J. W. F. Slik, E. E. Van Loon, and H. Ter Steege. 2009. Botanical richness and endemicity patterns of Borneo derived from species distribution models. Ecography 32:180–192.

Raghavan, R. K., D. G. Goodin, G. A. Hanzlicek, G. Zolnerwich, M. W. Dryden, G. A. Anderson, and R. R. Ganta. 2016. Maximum Entropy-Based Ecological Niche Model and Bio-Climatic Determinants of Lone Star Tick (Amblyomma americanum) Niche. Vector-Borne and Zoonotic Diseases X:vbz.2015.1837.

Rausch, R. L., and S. H. Richards. 1971. Observations on parasite-host relationships of Echinococcus multilocularis Leuckart, 1863, in North Dakota. Canadian Journal of Zoology 49:1317–1330.

Rausch, R. L., and E. L. Schiller. 1954. Studies on the helminth fauna of Alaska. XXIV. Echinococcus sibiricensis n. sp., from St. Lawrence Island. Journal of Parasitol 40:659–662.

Romig, T., D. Thoma, and A. K. Weible. 2006. Echinococcus multilocularis--a zoonosis of anthropogenic environments? Journal of Helminthology 80:207–212.

Sage, K. M., T. L. Johnson, M. B. Teglas, N. C. Nieto, and T. G. Schwan. 2017. Ecological niche modeling and distribution of Ornithodoros hermsi associated with tick-borne relapsing fever in western North America. PLoS Neglected Tropical Diseases 11.

Samy, A. M., L. P. Campbell, and A. Townsend-Peterson. 2014. Leishmaniasis transmission: Distribution and coarse-resolution ecology of two vectors and two parasites in Egypt. Revista da Sociedade Brasileira de Medicina Tropical 47:57–62.

Schurer, J. M., K. M. Gesy, B. T. Elkin, and E. J. Jenkins. 2014. Echinococcus multilocularis and Echinococcus canadensis in wolves from western Canada. Parasitology 141:159–163.

Schweiger, A., R. W. Ammann, D. Candinas, P. Clavien, J. Eckert, B. Gottstein, N. Halkic, B. Muellhaupt, B. M. Prinz, J. Reichen, P. E. Tarr, P. E. Torgerson, and P. Deplazes. 2007. Human alveolar echinococcosis after fox population increase, Switzerland. Emerging Infectious Diseases 13:878–882.

Searcy, C. A., and H. B. Shaffer. 2016. Do ecological niche models accurately identify climatic determinants of species ranges? American Naturalist 187:423–435.

Sehgal, R. N. M., W. Buermann, R. J. Harrigan, C. Bonneaud, C. Loiseau, A. Chser, I. Sepil, G. Valkiûnas, T. Iezhova, S. Saatchi, and T. B. Smith. 2011. Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird. Proceedings of the Royal Society B: Biological Sciences 278:1025–1033.

Soberon, J. 2007. Grinnellian and Eltonian niches and grographic distribution of species. Ecology Letters 10:1115–1123.

Staubach, C., L. Hoffmann, V. J. Schmid, M. Ziller, K. Tackmann, and F. J. Conraths. 2011. Bayesian space-time analysis of Echinococcus multilocularis-infections in foxes. Veterinary Parasitology 179:77–83.

Stensgaard, A. S., J. Utzinger, P. Vounatsou, E. Hürlimann, N. Schur, C. F. Saarnak, C. Simoonga, P. Mubita, N. B. Kabatereine, L. A. Tchuem Tchuenté, C. Rahbek, and T. K. Kristensen. 2013. Large-scale determinants of intestinal schistosomiasis and intermediate host snail distribution across Africa: Does climate matter? Acta Tropica 128:378–390.

Takumi, K., A. De Vries, M. L. Chu, J. Mulder, P. Teunis, and J. Van Der Giessen. 2008. Evidence for an increasing presence of Echinococcus multilocularis in foxes in the Netherlands. International Journal for Parasitology 38:571–578.

Torgerson, P. R. 2013. The emergence of echinococcosis in central Asia. Parasitology 140:1667–1673.

Torgerson, P. R., K. Keller, M. Magnotta, and N. Ragland. 2010. The global burden of alveolar echinococcosis. PLoS Neglected Tropical Diseases 4.

Trewhella, W. J., S. Harris, F. E. and Mcallister. 1988. Dispersal distance, home-range size and population density in the Red Fox (Vulpes vulpes): A Quantitative Analysis. The Journal of Applied Ecology 25:423–434.

Tufts, D. M., N. Batsaikhan, A. T. Dursahinhan, and S. L. Gardner. 2016. Identification of Taenia metacestodes from Mongolian mammals using multivariate morphometrics of the rostellar hooks. Erforschung Biologischer Ressourcen Der Mongolei (Halle/Saale) 13:361-375.

Veit, P., B. Bilger, V. Schad, J. Schäfer, W. Frank, and R. Lucius. 1995. Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110:79–86.

Warren, D. L., Wright, A. N., Seifert, S. N., and H. B Shaffer. 2014. Incorporating model complexity and spatial sampling bias into ecological niche models of climate change risks faced by 90 California vertebrate species of concern. Diversity and distributions 20:334–343.

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2019-04-11

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