Abstract
Cattle ranching is one of the main production activities in the Neotropics that has unavoidably led to cattle exposure to the common vampire bat (Desmodus rotundus) and rabies virus. Although many studies have assessed this issue, the influence of environmental characteristics associated with land use and social and production constraints have received little attention. We used satellite imagery classification to identify a gradient of landscape disturbance and analyzed the effects of cattle management and landscape structure on common vampire bat abundance and feeding prevalence. Evidence of the common vampire bat feeding on cattle was common in the study area: 87.5% of the ranchers interviewed claimed to have experienced this problem. The abundance and feeding prevalence of the common vampire bat was lower in landscapes dominated by open fields, scarce forest cover, and agricultural land. Bat abundance was positively associated with the presence of streams in the proximity of grazing areas, whereas cave’s presence was associated with higher feeding prevalence. We suggest that cattle grazing should avoid the proximity of streams, caves, and forests as much as possible, as these conditions increase the exposure of cattle to the common vampire bat and the potential for feeding, which can increase the likelihood of rabies virus transmission.
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10 August 2021
A Correction to this paper has been published: https://doi.org/10.1007/s13364-021-00588-1
References
Acha PN, Málaga A (1988) Economic losses due to Desmodus rotundus. In: Greenhall AM, Schmidt U (eds) Natural History of Vampire Bats. CRC Press, Boca Raton, pp 207–214
Aguirre LF (2007) Historia natural, distribución y conservación de los murciélagos de Bolivia. Centro de Ecología y Difusión Simón I, Patiño, Santa Cruz de la Sierra
Anderson A, Shwiff S, Gebhardt K, Ramírez A, Shwiff S, Kohler D, Lecuona L (2014a) Economic evaluation of vampire bat (Desmodus rotundus) rabies prevention in Mexico. Trans Emerg Dis 61(2):140–146. https://doi.org/10.1111/tbed.12007
Anderson A, Shwiff S, Shwiff S (2014b) Economic impact of the potential spread of vampire bats into south Texas. USDA National Wildlife Research Center - Staff Publications. U.S. Department of Agriculture: Animal and Plant Health Inspection Service (APHIS), pp. 305–309.
Ávila-Cabadilla L, Sánchez-Azofeifa G, Stoner K, Álvarez-Añorve M, Quesada M, Portillo-Quintero C (2012) Local and landscape factors determining occurrence of phyllostomid bats in tropical secondary forests. PLoS ONE 7:e35228. https://doi.org/10.1371/journal.pone.0035228
Ávila-Flores R, Bolaina-Badal A, Gallegos-Ruiz A, Sánchez-Gómez W (2019) Use of linear features by the common vampire bat (Desmodus rotundus) in a tropical cattle-ranching landscape. Therya 10:229–234
Ávila-Gómez E, Moreno C, García-Morales R, Zuria I, Sánchez-Rojas G, Briones-Salas M (2015) Deforestation thresholds for phyllostomid bat populations in tropical landscapes in the Huasteca region, Mexico. Trop Conserv Sci 8:646–661. https://doi.org/10.1177/194008291500800305
Bárcenas-Reyes I, Loza-Rubio E, Zendejas-Martínez H, Luna-Soria H, Cantó-Alarcón G, Milián-Suazo F (2015) Comportamiento epidemiológico de la rabia paralitica bovina en la región central de México, 2001–2013. Rev Panam Salud Publ 38: 396–402. https://www.scielosp.org/scielo.php?script=sci_arttext&pid=S1020-49892015001000007&lang=pt. Accessed 19 May 2019
Barton K (2016) MuMIn: Multi-model Inference. R Package Version 1(15):6
Benítez R (1997) Epidemiología de la Rabia Paralítica Bovina en México. VII Reunión Anual del Consejo Nacional de Salud Animal.
Brown DE (1994) Vampiro: The Vampire Bat in Fact and Fantasy. High-Lonesome Books, Silver City
Burnham K, Anderson D (1998) Model selection and inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New York, Inc, U.S.A
Chambers C, Cushman S, Medina-Fitoria A, Martínez-Fonseca J, Chávez-Velásquez M (2016) Influences of scale on bat habitat relationships in a forested landscape in Nicaragua. Landsc Ecol 31:1299–1318. https://doi.org/10.1007/s10980-016-0343-4
Covaleda S, Aguilar S, Ranero A, Marín I, Paz F (2014) Diagnóstico sobre determinantes de deforestación en Chiapas. Agencia de los Estados Unidos Para el Desarrollo Internacional (USAID), Alianza México para la Reducción de Emisiones por Deforestación y Degradación (MREDD+). The Nature Conservancy (TNC), México, D.F.
De Andrade F, Gomes M, Uieda W, Begot A, Ramos O, Fernandes M (2016) Geographical analysis for detecting high-risk areas for bovine/human rabies transmitted by the common hematophagous bat in the Amazon region. Brazil PLoS ONE 11:e0157332. https://doi.org/10.1371/journal.pone.0157332
Delpietro H, Marchevsky N, Simonetti E (1992) Relative population densities and predation of the common vampire bat (Desmodus rotundus) in natural and cattle-raising areas in north-east Argentina. Prev Vet Med 14:13–20. https://doi.org/10.1016/0167-5877(92)90080-Y
DiGiano M, Ellis E, Keys E (2013) Changing landscapes for forest commons: linking land tenure with forest cover change following Mexico’s 1992 Agrarian Counter-Reforms. Hum Ecol 41:707–723. https://doi.org/10.1007/s10745-013-9581-0
Dufumier M (1990) Importancia de tipología de unidades de producción agrícolas en el análisis de diagnóstico de realidades agrarias. In: Berdegué J, Dufumier M, Escobar G (eds) Tipificación de Sistemas de Producción Agrícola. Red Internacional de Metodología de Investigación de Sistemas de Producción (Rimisp), Centro Latinoamericano para el Desarrollo Rural, Santiago de Chile, pp 63–81
Ellis EA, Romero-Montero A, Hernández-Gómez IU (2015) Evaluación y Mapeo de los Determinantes de Deforestación en la Península Yucatán. USAID, TNC, Alianza MREDD+, Mexico, D.F.
Ellis EA, Hernández-Gómez IU, Romero-Montero JA (2017) Los procesos y causas del cambio en la cobertura forestal de la Península Yucatán, México. Ecosist 26:101–111. https://doi.org/10.7818/ECOS.2017.26-1.16
Espinosa J, Góngora S, García A, Cervantes F, Moctezuma G, Mancilla M, Rangel J, Cuevas V, Dávalos J, Villegas A, Velázquez L (2015) Aspectos socioeconómicos de la ganadería bovina tropical. In: González E, Dávalos J (eds) Estado del Arte sobre Investigación e Innovación Tecnológica en Ganadería Bovina Tropical. Red de Investigación e Innovación Tecnológica para la Ganadería Bovina Tropical (REDGATRO)/Consejo Nacional de Ciencia y Tecnología (CONACyT), Mexico, pp 230–250
Flores-Crespo R (1978) La Rabia, los Murciélagos y el Control de los Hematófagos. Instituto Nacional de Investigaciones Pecuarias/Secretaría de Agricultura y Recursos Hidráulicos (SARH), Mexico, D.F.
Flores-Crespo R (2003) Técnicas. Substancias y Estrategias para el Control de Murciélagos Vampiros, Organización Panamericana de la Salud, México, D.F.
Flores-Crespo R, Said F, Burns R, Mitchell G (1974) Observaciones sobre el comportamiento del vampiro común Desmodus rotundus al alimentarse en condiciones naturales. Tec Pecu Mex 27:39–45
Fox J (2016) Applied Regression Analysis and Generalized Linear Models, 3rd edn. McMaster University, Sage
García G, Méndez L, Aguilar W, Orellana R (2010) Contexto físico: ambientes terrestres. In: Durán R, Méndez M (eds) Biodiversidad y Desarrollo Humano en Yucatán. CICY, PPD-FMAM, CONABIO, SEDUMA, Mérida, pp 17–20
García-García J, Santos-Moreno A (2014) Efectos de la estructura del paisaje y de la vegetación en la diversidad de murciélagos filostómidos (Chiroptera: Phyllostomidae) de Oaxaca. México Revista de Biología Tropical 62(1):217–239
Geist HJ, Lambin EF (2001) What Drives Tropial Deforestation? A meta-analysis of proximate and underlying causes of deforestation based on subnational case study evidence. LUCC Report Series; 4. LUCC International Project Office, University of Louvain, Louvain-la-Neuve.
Gomes MN, Vieira-Monteiro AM, Filho V, Gonçalves CA (2007) Áreas propícias para o ataque de morcegos hematófagos Desmodus rotundus em bovinos na região de São João da Boa Vista, estado de São Paulo. Pesquisa Vet Brasil 27:307–313. https://doi.org/10.1590/S0100-736X2007000700009
Gomes MN, Vieira-Monteiro AM, Lewis N, Gonçalves CA, Filho V (2010) Landscape risk factors for attacks of vampire bats on cattle in Sao Paulo, Brazil. Prev Vet Med 93:139–146. https://doi.org/10.1016/j.prevetmed.2009.10.006
Gonçalves F, Fisher E, Dirzo R (2017) Forest conversion to cattle ranching differentially affects taxonomic and functional groups of Neotropical bats. Biol Conserv 210:343–348. https://doi.org/10.1016/j.biocon.2017.04.021
Gonzalez R, Mitchell GC (1976) Vampire bat control programs in Latin America. In: Proceedings of the 7th Vertebrate Pest Conference. Vertebr Pest Conf Proc Paper 22: 254–257.
Gotelli NJ, Ellison AM (2004) A Primer of Ecological Statistics, 2nd edn. Sinauer Associates Inc., Sunderland
Greenhall A (1971) Lucha contra los murciélagos vampiros. Estudio y proyecto de programa para América Latina. B Ofic Sanit Panam 71:231–246
Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol Electron 4: 1–9. http://palaeoelectronica.org/2001_1/past/issue1_01.htm. Accessed 17 June 2018
Hardy MA (1993) Regression with Dummy Variables. Sage university papers series. Quantitative applications in the social sciences; No. 07–093 Sage Publications, Newbury Park.
Hidalgo M (2005) La rabia: una zoonosis mortal. Rev. Digit, CENIAP Hoy, No, p 7
IBM Corp - International Business Machines Corporation (2016) IBM SPSS Statistics for Windows. Version 24.0. IBM Corp Armonk.
Instituto Nacional de Estadística y Geografía - INEGI (2013) Uso de Suelo y Vegetación escala 1:250 000 Serie IV.
Joermann G (1984) Recognition of spatial parameters by echolocation in the vampire bat, Desmodus rotundus. J Comp Physiol 155:67–74. https://doi.org/10.1007/BF00610932
Kraker-Castañeda C, Echeverría J, Chicas J, García P (2010) Impacto del murciélago vampiro en áreas ganaderas y poblaciones humanas aledañas en el departamento de Izabal. Guatemala, CECON-USAC-SENACYT
Kaplan M (1996) Safety precautions in handling rabies virus, in: Laboratory techniques in rabies (Meslin F, Kaplan M, Koprowski H, eds). Fourth edition. World Health Organization. Geneva.
Legendre P, Fortin M, Borcard D (2015) Should the Mantel test be used in spatial analysis? Met Ecol & Evol 6:1239–1247. https://doi.org/10.1111/2041-210X.12425
Leos-Rodríguez J, Serrano-Páez A, Salas-González J, Ramírez-Moreno P, Sagarnaga-Villegas M (2008) Caracterización de ganaderos y unidades de producción pecuaria beneficiarios del programa de estímulos a la productividad ganadera (PROGAN) en México. Agric Soc Desarro 5: 213–230. http://www.redalyc.org/articulo.oa?id=360533080005. Accessed 10 Aug 2019
Lindhe-Norberg UM, Brooke AP, Trewhella WJ (2000) Soaring and non-soaring bats of the family pteropodidae (flying foxes, Pteropus spp.): wing morphology and flight performance. J Exp Biol 203:651–664
Lord R (1988) Control of vampire bats. In: Greenhall AM, Schmidt U (eds) Natural History of Vampire Bats. CRC Press, Boca Raton, pp 215–226
Manly BFJ (1986) Multivariate Statistical Methods: A Primer. Chapman and Hall, New York
Manly BFJ (1986) Randomization and regression methods for testing for associations with geographical, environmental and biological distances between populations. Res Popul Ecol 28:201–218. https://doi.org/10.1007/BF02515450
Mas J, Díaz-Gallegos J, Pérez A (2003) Evaluación de la confiabilidad temática de mapas o de imágenes clasificadas: una revisión. Investigaciones Geográficas, Boletín del Instituto de Geografía, UNAM 51:53–72
Matteucci S (1998) La cuestión del patrón y la escala en la ecología del paisaje y de la región. In: Matteucci S, Buzai G (eds) Sistemas Ambientales Complejos: Herramientas de Análisis Espacial. EUDEBA, Buenos Aires, pp 219–248
Maxwell MJ, Freire de Carvalho MH, Hoet AE, Vigilato MAN, Pompei JC, Cosivi O, del Rio VJ (2017) Building the road to a regional zoonoses strategy: A survey of zoonoses programmes in the Americas. PLoS ONE 12(3):1–19. https://doi.org/10.1371/journal.pone.0174175
McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. Version 4.2.1. University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html. Accessed 7 Jan 2018
McIntyre S, Hobbs R (1999) A framework for conceptualizing human effects on landscapes and its relevance to management and research models. Conserv Biol 13: 1282–1292. https://www.jstor.org/stable/2641952. Accessed 3 May 2018
Mendes P, With KA, Signorelli L, De Marco P (2017) The relative importance of local versus landscape variables on site occupancy in bats of the Brazilian Cerrado. Landsc Ecol 32:745–762. https://doi.org/10.1007/s10980-016-0483-6
Mialhe P (2013) Characterization of Desmodus rotundus (E. Geoffroy, 1810) (Chiroptera, Phyllostomidae) shelters in the Municipality of São Pedro – SP. Braz J Biol 73(3):521–526
Moya MI, Pacheco LF, Aguirre LF (2015) Relación de los ataques de Desmodus rotundus con el manejo del ganado caprino y algunas características del hábitat en la Prepuna de Bolivia. Mastozool Neotrop 22: 73–84. https://www.redalyc.org/articulo.oa?id=457/45739766008. Accessed 10 May 2019
Orlando S, Panchana V, Calderón J, Muñoz O, Campos D, Torres-Lasso P, Arcos F, Quentin E (2019) Risk factors associated with attacks of hematophagous bats (Desmodus rotundus) on cattle in Ecuador. Vector-Borne and Zoo Dis 19(6):407–413. https://doi.org/10.1089/vbz.2017.2247
QGIS Development Team (2017) QGIS Geographic Information Systems. Version 2.18. Open Source Geospatial Foundation Project, Beaverton.
Ramírez R, González A, Nevárez A, Rodríguez L (2011) Informe de tres casos de rabia paralítica y babesiosis bovina en el municipio de Aldama, Tamaulipas. Vet Mx 42: 331–338. http://www.redalyc.org/articulo.oa?id=42321608007. Accessed 13 June 2019
Ripperberg S, Tschapka M, Kalko E, Rodríguez-Herrera B, Mayer F (2014) Resisting habitat fragmentation: high connectivity among populations of the frugivorous bat Carollia castanea in an agricultural landscape. Agric Ecosyst & Environ 185:9–15. https://doi.org/10.1016/j.agee.2013.12.006
Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria - SENASICA (2019). http://senasica.gob.mx (accessed 15 March 2019).
Siegel S, Castellan J (1995) Estadística no paramétrica. Editorial Trillas, México, D.F.
Silva J, Moreira E, Haddad J, Sampaio I, Modena C, Tubaldini M (2001) Uso da terra como determinante da distribuição da raiva bovina em Minas Gerais, Brasil. Arq Bras Med Vet Zoo 53:273–283. https://doi.org/10.1590/S0102-09352001000300002
Stoner-Duncan B, Streicker D, Tedeschi C (2014) Vampire bats and rabies: toward an ecological solution to a public health problem. PLoS Negl Trop Dis 8(6):e2867. https://doi.org/10.1371/journal.pntd.0002867
Straube F, Bianconi G (2002) Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiropt Neotrop 8:50–152
Streicker D, Allgeier J (2016) Foraging choices of vampire bats in diverse landscapes: potential implications for land-use change and disease transmission. J App Ecol 53:1280–1288. https://doi.org/10.1111/1365-2664.12690
Streicker D, Recuenco S, Valderrama W, Gómez J, Vargas I, Pacheco V, Condori R, Montgomery J, Rupprecht C, Rohani P, Altizer S (2012) Ecological and anthropogenic drivers of rabies exposure in vampire bats: implications for transmission and control. The Royal Society B 279:3384–3392. https://doi.org/10.1098/rspb.2012.0538
Tadei VA, Gonçalves C, Pedro W, Tadei W, Kotait I, Arieta C (1991) Distribuição do morcego vampiro Desmodus rotundus no Estado de São Paulo e a raiva dos animais domésticos. Impresso Especial CATI, Campinas, Coordenadoria de Assistência Técnica Integral
Thornton P, Van de Steeg J, Notenbaert A, Herrero M (2009) The impacts of climate change on livestock and livestock systems in developing countries: a review of what we know and what we need to know. Agric Syst 101(3):113–127. https://doi.org/10.1016/j.agsy.2009.05.002
Turner DC (1975) The Vampire Bat: A Field Study in Behavior and Ecology. John Hopkins University Press, Baltimore
Trajano E (1996) Movements of cave bats in southeastern Brazil, with emphasis on the population ecology of the common vampire bat, Desmodus rotundus. Biotropica 28: 121–129. https://www.jstor.org/stable/2388777. Accessed 14 Oct 2017
Turner M, Gardner RH (2015) Landscape Ecology in Theory and Practice: Pattern and Process. Pattern and Process, second ed. Springer-Verlag, New York.
Uieda W (1996) Biologia e dinâmica populacional de morcegos hematófagos, in: Anais do II Curso de Atualização em raiva dos herbívoros, Curitiba, 63–87.
World Health Organization - WHO (2005) WHO Expert Consultation on Rabies: First Report. WHO Technical Report Series No. 931. Pp. 1–88. Geneva, Switzerland.
Acknowledgments
We thank the ranch owners who graciously granted access to their properties and supplied information: Reynaldo Morales, Pedro López, Rusbel Mendoza, Hugo López, Darinel Camposeco, Antonio Vera, David Fernández, Odilio Carbajal, and Rodolfo Hernández. We also thank Viridiana Llaven, Gerardo Vera, Iván Orantes, and Eylin Sio Fan Siu for their assistance during fieldwork. The editor and three anonymous reviewers made substantial contributions to improve the manuscript. Elida Leiva and María Elena Sánchez-Salazar edited the English manuscript.
Funding
This work was partially funded by the Rufford Foundation (project grant No. 23513–1). Idea Wild supplied equipment for the fieldwork (project grant ID. MENDMEXI0617). V.H. Mendoza-Sáenz was supported by a Ph.D. scholarship (No. 307774) from the Consejo Nacional de Ciencia y Tecnología (CONACyT) of Mexico.
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Mendoza-Sáenz, V.H., Navarrete-Gutiérrez, D.A., Jiménez-Ferrer, G. et al. Abundance of the common vampire bat and feeding prevalence on cattle along a gradient of landscape disturbance in southeastern Mexico. Mamm Res 66, 481–495 (2021). https://doi.org/10.1007/s13364-021-00572-9
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DOI: https://doi.org/10.1007/s13364-021-00572-9