Skip to main content

Advertisement

Log in

Abundance of the common vampire bat and feeding prevalence on cattle along a gradient of landscape disturbance in southeastern Mexico

  • Original Paper
  • Published:
Mammal Research Aims and scope Submit manuscript

A Correction to this article was published on 01 July 2021

This article has been updated

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Change history

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Burnham K, Anderson D (1998) Model selection and inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New York, Inc, U.S.A

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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.

    Google Scholar 

  • 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

    Google Scholar 

  • Fox J (2016) Applied Regression Analysis and Generalized Linear Models, 3rd edn. McMaster University, Sage

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Greenhall A (1971) Lucha contra los murciélagos vampiros. Estudio y proyecto de programa para América Latina. B Ofic Sanit Panam 71:231–246

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Manly BFJ (1986) Multivariate Statistical Methods: A Primer. Chapman and Hall, New York

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Turner DC (1975) The Vampire Bat: A Field Study in Behavior and Ecology. John Hopkins University Press, Baltimore

    Google Scholar 

  • 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.

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Víctor Hugo Mendoza-Sáenz.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Communicated by Shannon Currie.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: The labels on Figures 2, 5 and 6 were missing and these has been updated above.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 26 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-021-00572-9

Keywords

Navigation