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Helminth Diversity in Synanthropic Rodents from an Urban Ecosystem

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Abstract

Richness and diversity of parasites depend on a set of interrelated factors related to the characteristics of the host, the environment and the parasites itself. In the City of Buenos Aires, rodent communities vary according to landscape structure. The goal of this paper was to study the variations of helminth richness and diversity among invasive rodent species in different landscape units of the City of Buenos Aires. 73% of the rodents were parasitized with at least one of the 10 identified helminth species. Each rodent species presented its own characteristics in terms of richness, diversity and helminth composition, keeping these characteristics still occupying more than one landscape unit. The infracommunities with greater diversity corresponded to R. norvegicus due to its high values of parasitic richness, proportion of infected hosts and parasite prevalence. Instead, R. rattus and M. musculus infracommunities had lower diversity since a high percentage of them presented a unique helminth species. Within the city, the inhabitants of shantytowns would be the most exposed to zoonotic diseases transmitted by rodents due to high abundance of rodents harboring a high parasite load, including species like Hymenolepis nana and H. diminuta, recognized worldwide from a zoonotic aspect.

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References

  • Arneberg P (2002) Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25: 88-94

    Article  Google Scholar 

  • Battersby SA, Parsons R, Webster JP (2002) Urban rat infestations and the risk to public health. Journal of Environmental Health Research 1: 57-65

    Google Scholar 

  • Bordes F, Blasdell K, Morand S (2015) Transmission ecology of rodent-borne diseases: New frontiers. Integrative Zoology 10: 424-435

    Article  PubMed  Google Scholar 

  • Bordes F, Morand S (2009) Parasite diversity: an overlooked metric of parasite pressures? Oikos 118: 801-806

    Article  Google Scholar 

  • Bordes F, Morand S (2008) Helminth species diversity of mammals: parasite species richness is a host species attribute. Parasitology 135: 1701-1705

    Article  CAS  PubMed  Google Scholar 

  • Bordes F, Morand S, Kelt DA, Van Vuren DH (2009) Home range and parasite diversity in mammals. The American Naturalist 173: 467-474

    Article  PubMed  Google Scholar 

  • Bursey CR, Goldberg SR, Parmelee JR (2001) Gastrointestinal helminths of 51 species of anurans from Reserva Cuzco Amazónico, Peru. Comparative Parasitology 68: 21-35

    Google Scholar 

  • Bush AO, Holmes JC (1986) Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64: 132-141

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Calegaro-Marques C, Amato SB (2014) Urbanization breaks up host-parasite interactions: a case study on parasite community ecology of Rufous-bellied Thrushes (Turdus rufiventris) along a rural-urban gradient. PloSOne 9: e103144

    Article  PubMed  PubMed Central  Google Scholar 

  • Caut S, Casanovas JG, Virgos E, Lozano J, Witmer GW, Courchamp F (2007) Rats dying for mice: modelling the competitor release effect. Austral Ecology 32: 858-868

    Article  Google Scholar 

  • Cavia R, Cueto GR, Suárez OV (2009) Changes in rodent communities according to the landscape structure in an urban ecosystem. Landscape and Urban Planning 90: 11-19

    Article  Google Scholar 

  • Cavia R, Muschetto E, Cueto GR, Suárez OV (2015) Commensal Rodents in the City of Buenos Aires: A Temporal, Spatial, and Environmental Analysis at the Whole City Level. EcoHealth 12: 468-479

    Article  PubMed  Google Scholar 

  • Chaisiri K, Siribat P, Ribas A, Morand S (2015) Potentially zoonotic helminthiases of murid rodents from the Indo-Chinese peninsula: impact of habitat and the risk of human infection. Vector-Borne and Zoonotic Diseases 15: 73-85

    Article  PubMed  PubMed Central  Google Scholar 

  • Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 5: 3-21

    Article  Google Scholar 

  • Cueto GR, Cavia R, Bellomo C, Padula PJ, Suárez OV (2008) Prevalence of hantavirus infection in wild Rattus norvegicus and R. rattus populations of Buenos Aires City, Argentina. Tropical Medicine and International Health 13: 46-51

    Article  PubMed  Google Scholar 

  • Deplazes P, Hegglin D, Gloor S, Romig T (2004) Wilderness in the city: the urbanization of Echinococcus multilocularisTrends in Parasitology 20: 77-84

    Article  PubMed  Google Scholar 

  • Dunn AM, Hatcher MJ (2015) Parasites and biological invasions: parallels, interactions, and control. Trends in Parasitology 31: 189-199

    Article  PubMed  Google Scholar 

  • Easterbrook JD, Kaplan JB, Vanasco NB, Reeves WK, Purcell RH, Kosoy MY, Glass GE, Watson J, Klein SL (2007) A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiology and Infection 135: 1192-1199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández MS, Cavia R, Cueto GR, Suárez OV (2007) Implementation and evaluation of an integrated program for rodent control in a Shantytown of Buenos Aires City, Argentina. EcoHealth 4: 271-277

    Article  Google Scholar 

  • Gómez Villafañe IE, Robles MR, Busch M (2008) Helminth communities and host-parasite relationships in argentine brown rat (Rattus norvegicus). Helminthologia 45: 126-129

    Article  Google Scholar 

  • Hancke D, Navone GT, Suárez OV (2011) Endoparasite community of Rattus norvegicus captured in an urban area of Argentina. Helminthologia 48:167-173

    Article  Google Scholar 

  • Hancke D, Suárez OV (2014) Environmental health education in schools as strategy for rodent control: an experience in a shantytown of Buenos Aires, Argentina. EcoHealth 11: 133-140

    Article  PubMed  Google Scholar 

  • Hancke D, Suárez OV (2016) Infection levels of the cestode Hymenolepis diminuta in rat populations from Buenos Aires, Argentina. Journal of Helminthology 90: 199-205

    Article  CAS  PubMed  Google Scholar 

  • Himsworth CG, Parsons KL, Jardine C, Patrick DM (2013) Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector-Borne and Zoonotic Diseases 13: 349-359

    Article  PubMed  Google Scholar 

  • Himsworth CG, Jardine CM, Parsons KL, Feng AYT, Patrick DM (2014) The characteristics of wild rat (Rattus spp.) populations from an inner-City neighborhood with a focus on factors critical to the understanding of rat-associated zoonoses. PLoSOne 9: e91654

    Article  PubMed  PubMed Central  Google Scholar 

  • Kataranovski DS, Vukićević-Radić OD, Kataranovski MV, Radović DL, Mirkov II (2008) Helminth fauna of Mus musculus Linnaeus, 1758 from the suburban area of Belgrade, Serbia. Archives of Biological Sciences 60: 609-617

    Article  Google Scholar 

  • Kataranovski M, Mirkov I, Belij S, Popov A, Petrovic Z, Gaci Z, Kataranovski D (2011) Intestinal helminths infection of rats (Ratus norvegicus) in the Belgrade area (Serbia): the effect of sex, age and habitat. Parasite (Paris, France) 18: 189-196

    Article  CAS  Google Scholar 

  • Kosoy M, Khlyap L, Cosson JF, Morand S (2015) Aboriginal and invasive rats of genus Rattus as hosts of infectious agents. Vector-Borne and Zoonotic Diseases 15: 3-12

    Article  PubMed  Google Scholar 

  • Mackenstedt U, Jenkins D, Romig T (2015) The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. International Journal for Parasitology: Parasites and Wildlife 4: 71-79

    PubMed  PubMed Central  Google Scholar 

  • Magurran AE (2013) Measuring Biological Diversity. John Wiley & Sons

  • Mahan CG, O’Connell TJ (2005) Small mammal use of suburban and urban parks in central Pennsylvania. Northeastern Naturalist 12: 307-314

    Article  Google Scholar 

  • Marsh RE (1994) Roof rats. In: Prevention and Control of Wildlife Damage, Hyngstrom SE, Timm RM, Larson GE (editors), California, pp B125–B132

  • Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35: 221-270

    Article  PubMed  Google Scholar 

  • Milazzo C, Ribas A, Casanova JC, Cagnin M, Geraci F, Di Bella C (2010) Helminths of the brown rat (Rattus norvegicus) (Berkenhout, 1769) in the city of Palermo, Italy. Helminthologia 47: 238-240

    Article  Google Scholar 

  • Morand S, Bordes F, Chen HW, Claude J, Cosson JF, Galan M, Czirják G, Greenwood AD, Latinne A, Michaux J, Ribas A (2015) Global parasite and Rattus rodent invasions: the consequences for rodent-borne diseases. Integrative Zoology 10: 409-423

    Article  PubMed  Google Scholar 

  • Neiderud CJ (2015) How urbanization affects the epidemiology of emerging infectious diseases. Infection Ecology and Epidemiology 5: 27060

    Article  PubMed  Google Scholar 

  • Nguyen-Viet H, Zinsstag J, Schertenleib R, Zürbrugg C, Obrist B, Montangero A, Surkinkul N, Koné D, Morel A, Cissé G, Koottatep T, Bonfoh B, Tanner M (2009) Improving environmental sanitation, health, and well-being: a conceptual framework for integral interventions. EcoHealth 6:180–191

    Article  PubMed  Google Scholar 

  • Palmeirim M, Bordes F, Chaisiri K, Siribat P, Ribas, A, Morand S (2014) Helminth parasite species richness in rodents from Southeast Asia: role of host species and habitat. Parasitology Research 113: 3713-3726

    Article  PubMed  Google Scholar 

  • Poulin R (1993) The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23: 937-944

    Article  CAS  PubMed  Google Scholar 

  • Pullan RL, Brooker SJ (2012) The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasites and Vectors 5: 81

    Article  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/. Last access June 2015

  • Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86: 228-232

    Article  PubMed  Google Scholar 

  • United Nations (2012) Department of Economic and Social Affairs, Population Division. World Urbanization Prospects: The 2011 Revision. CD-ROM Edition—Data in digital form (POP/DB/WUP/Rev.2011)

  • Vadell MV, Cavia R, Suárez OV (2010) Abundance, age structure and reproductive patterns of Rattus norvegicus and Mus musculus in two areas of the city of Buenos Aires. International Journal of Pest Management 56: 327-336

    Article  Google Scholar 

  • Walther BA, Morand S (1998) Comparative performance of species richness estimation methods. Parasitology 116: 395-405

    Article  PubMed  Google Scholar 

  • Weaver HJ, Hawdon JM, Hoberg EP (2010) Soil-transmitted helminthiases: implications of climate change and human behavior. Trends in Parasitology 26: 574-581

    Article  PubMed  Google Scholar 

  • Wells K, O’Hara RB, Morand S, Lessard JP, Ribas A (2015) The importance of parasite geography and spillover effects for global patterns of host–parasite associations in two invasive species. Diversity and Distributions 21: 477-486

    Article  Google Scholar 

  • Wells K, Smales LR, Kalko EK, Pfeiffer M (2007) Impact of rain-forest logging on helminth assemblages in small mammals (Muridae, Tupaiidae) from Borneo. Journal of Tropical Ecology 23: 35-43

    Article  Google Scholar 

  • Zain SNM, Behnke JM, Lewis JW (2012) Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia. Parasites and Vectors 5: 1-23

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, New York, 574 p

    Book  Google Scholar 

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Acknowledgements

We want to be especially grateful to the team of Laboratorio de Ecología de Poblaciones for their assistance during the field sampling and to Dr. Graciela Navone and Dr. Rosario Robles from CEPAVE (La Plata) for their help during parasitological identification. Financial support was provided by CONICET (Argentina) and the University of Buenos Aires.

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Correspondence to Diego Hancke.

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Hancke, D., Suárez, O.V. Helminth Diversity in Synanthropic Rodents from an Urban Ecosystem. EcoHealth 14, 603–613 (2017). https://doi.org/10.1007/s10393-017-1239-8

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  • DOI: https://doi.org/10.1007/s10393-017-1239-8

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