Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-15T04:06:58.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Drivers potentially influencing host–bat fly interactions in anthropogenic neotropical landscapes at different spatial scales

Published online by Cambridge University Press:  21 May 2018

Jacqueline Hernández-Martínez ,
Juan B. Morales-Malacara ,
Mariana Yolotl Alvarez-Añorve ,
Sergio Amador-Hernández ,
Ken Oyama  and
Luis Daniel Avila-Cabadilla Open the ORCID record for Luis Daniel Avila-Cabadilla [Opens in a new window]
Jacqueline Hernández-Martínez
Affiliation:
Escuela Nacional de Estudios Superiores, Unidad Morelia, Universidad Nacional Autónoma de México (UNAM), Antigua Carretera a Pátzcuaro no. 8701 Col. ExHacienda de San José de La Huerta, C.P. 58190 Morelia Michoacán, México
Juan B. Morales-Malacara
Affiliation:
Unidad Multidisciplinaria de Docencia e Investigación-Juriquilla, Facultad de Ciencias, Universidad Nacional Autónoma de México, C.P. 76230, Juriquilla, Querétaro, México
Mariana Yolotl Alvarez-Añorve
Affiliation:
Escuela Nacional de Estudios Superiores, Unidad Morelia, Universidad Nacional Autónoma de México (UNAM), Antigua Carretera a Pátzcuaro no. 8701 Col. ExHacienda de San José de La Huerta, C.P. 58190 Morelia Michoacán, México
Sergio Amador-Hernández
Affiliation:
Escuela Nacional de Estudios Superiores, Unidad Morelia, Universidad Nacional Autónoma de México (UNAM), Antigua Carretera a Pátzcuaro no. 8701 Col. ExHacienda de San José de La Huerta, C.P. 58190 Morelia Michoacán, México
Ken Oyama
Affiliation:
Escuela Nacional de Estudios Superiores, Unidad Morelia, Universidad Nacional Autónoma de México (UNAM), Antigua Carretera a Pátzcuaro no. 8701 Col. ExHacienda de San José de La Huerta, C.P. 58190 Morelia Michoacán, México
Luis Daniel Avila-Cabadilla
Affiliation:
Escuela Nacional de Estudios Superiores, Unidad Morelia, Universidad Nacional Autónoma de México (UNAM), Antigua Carretera a Pátzcuaro no. 8701 Col. ExHacienda de San José de La Huerta, C.P. 58190 Morelia Michoacán, México
Get access Rights & Permissions [Opens in a new window]

Abstract

The anthropogenic modification of natural landscapes, and the consequent changes in the environmental conditions and resources availability at multiple spatial scales can affect complex species interactions involving key-stone species such as bat–parasite interactions. In this study, we aimed to identify the drivers potentially influencing host–bat fly interactions at different spatial scales (at the host, vegetation stand and landscape level), in a tropical anthropogenic landscape. For this purpose, we mist-netted phyllostomid and moormopid bats and collected the bat flies (streblids) parasitizing them in 10 sites representing secondary and old growth forest. In general, the variation in fly communities largely mirrored the variation in bat communities as a result of the high level of specialization characterizing host–bat fly interaction networks. Nevertheless, we observed that: (1) bats roosting dynamics can shape bat–streblid interactions, modulating parasite prevalence and the intensity of infestation; (2) a degraded matrix could favor crowding and consequently the exchange of ectoparasites among bat species, lessening the level of specialization of the interaction networks and promoting novel interactions; and (3) bat–fly interaction can also be shaped by the dilution effect, as a decrease in bat diversity could be associated with a potential increase in the dissemination and prevalence of streblids.

Keywords

Anthropogenic landscapesbatshost–bat fly interactionsinteraction networksneotropicsstreblidstropical dry forest
Type
Research Article
Information
Parasitology , Volume 146 , Issue 1 , January 2019 , pp. 74 - 88
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Both authors have contributed equally to this work.

References

Abundes-Gallegos, J et al. (2018) Detection of Dengue virus in Bat flies (Diptera: Streblidae) of common vampire bats Desmodus rotundus, in Progreso, Hidalgo, Mexico. Vector-Borne and Zoonotic Diseases 18, 70–73.Google Scholar
Alvarez-Añorve, MY et al. (2012) Functional regeneration and spectral reflectance of trees during succession in a highly diverse tropical dry forest ecosystem. American Journal of Botany 99, 816–826.Google Scholar
Avila-Cabadilla, LD et al. (2009) Composition, structure and diversity of phyllostomid bat assemblages in different successional stages of a tropical dry forest. Forest Ecology and Management 258, 986–996.Google Scholar
Avila-Cabadilla, LD et al. (2012) Local and landscape factor determining ocurrence of Phyllostomid bats in tropical secondary forests. PLoS ONE 7(4), e35228.Google Scholar
Avila-Cabadilla, LD et al. (2014) Phyllostomid bat ocurrence in successional stages of neotropical dry forests. PLoS ONE 9(1), e84572.Google Scholar
Bai, Y et al. (2012) Prevalence and diversity of Bartonella spp. in bats in Peru. The American Journal of Tropical Medicine and Hygiene 87, 518–523.Google Scholar
Blüthgen, N and Klein, AM (2011) Functional complementarity and specialisation: the role of biodiversity in plant-pollinator interactions. Basic and Applied Ecology 12, 282–291.Google Scholar
Blüthgen, N, Menzel, F and Blüthgen, N (2006) Measuring specialization in species interaction networks. BMC Ecology 6, 9.Google Scholar
Bobrowiec, PED and Gribel, R (2010) Effects of different secondary vegetation types on bat community composition in Central Amazonia, Brasil. Animal Conservation 13, 204–216.Google Scholar
Burnham, KP and Anderson, DR (2002). Model Selection and Multimodel Inference: A Practical Information–Theoretical Approach, 2nd Edn. New York, USA: Springer-Verlag.Google Scholar
Ceballos, G (2014) Mammals of Mexico, 1st Edn. Johns Hopkins, USA: Johns Hopkins University Press.Google Scholar
Ceballos, G and Miranda, A (2000). Guía de campo de los mamíferos de la costa de Jalisco. México, 1st Edn. México: Fundación ecológica de Chamela-Cuixmala, A.C, UNAM. Instituto de Biología.Google Scholar
Cisneros, LM, Fagan, ME and Willig, MR (2016) Environmental and spatial drivers of taxonomic, functional, and phylogenetic characteristics of bat communities in human-modified landscapes. Peer Journal 4, e2551.Google Scholar
Civitello, DJ et al. (2015) Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences 112, 8667–8671.Google Scholar
Colín-Martínez, H, Morales-Malacara, JB and García-Estrada, C (2018) Epizoic fauna survey on Phyllostomid bats (Chiroptera: Phyllostomidae) in a Shaded Coffee Plantation in Southeastern Chiapas, Mexico. Journal of Medical Entomology 51, 172–182.Google Scholar
Colwell, RK and Coddington, JA (1994) Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B Biological Sciences 345, 101–118.Google Scholar
Cottontail, VM, Wellinghausen, N and Kalko, EKV (2009) Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensis (Phyllostomidae) in a tropical lowland forest in Panama. Parasitology 136, 1133–1145.Google Scholar
Cuxim-Koyoc, A et al. (2015) Streblidae (Diptera: Hippoboscoidea) from Yucatan and updated species list for Mexico. Journal of Medical Entomology 52, 947–961.Google Scholar
Cuxim-Koyoc, A et al. (2016) Nuevos registros de Streblidae (Diptera: Hippoboscoidea) para México. Revista Colombiana de Entomología 42, 192–196.Google Scholar
Dáttilo, W, Guimaraes, PR Jr. and Izzo, TJ (2013). Spatial structure of ant-plant mutualistic networks. Oikos 122, 1643–1648.Google Scholar
De la Peña-Cuellar, E et al. (2015) Structure and diversity of phyllostomid bat assemblages on riparian corridors in a human-dominated tropical landscape. Ecology and Evolution 5, 903–913.Google Scholar
Dick, CW and Patterson, BD (2006) Bat flies: Obligate ectoparasites of bats. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo: Springer, pp. 179–194.Google Scholar
Dirzo, R et al. (2011) Seasonally Dry Forests: Ecology and Conservation, 1st Edn. Washington, USA: Island Press.Google Scholar
Eigenbrod, F, Hecnar, S and Fahrig, L (2011) Sub-optimal study design has major impacts on landscape-scale inference. Biological Conservation 144, 298–305.Google Scholar
Fenton, MB and Kunz, TH (1977) Movements and behavior. In Baker, RJ, Jones, JK Jr. and Carter, DC (eds), Biology of Bats of the New World Family Phyllostomatidae Part 2. Lubbock, Texas, USA: Special Publications, The Museum Texas Tech University, pp. 351–364.Google Scholar
Fenton, MB et al. (2000) Roosts used by Sturnira lilium (Chiroptera: Phyllostomidae) in Belize. Biotropica 3, 729–733.Google Scholar
Fonseca, P et al. (2016) Parasite-host interactions of bat flies (Diptera: Hippoboscoidea) in Brazilian tropical dry forest. Parasitology Research 115, 367–377.Google Scholar
Fraga-Ramírez, Y et al. (2017) Multiscale analysis of factors influencing herpetofaunal assemblages in early successional stages of a tropical dry forest in western Mexico. Biological Conservation 209, 196–210.Google Scholar
Gorresen, PM and Willig, MR (2004) Landscape responses of bats to habitat fragmentation in Atlantic forest of Paraguay. Journal of Mammalogy 85, 688–697.Google Scholar
Green, A (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82, 1473–1483.Google Scholar
Guerrero, R (1995) Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. III. Los grupos: dugesii, dunni y phyllostominae del género Trichobius Gervais, 1844. Acta Biológica Venezuelica 15, 1–27.Google Scholar
Guerrero, R and Morales-Malacara, JB (1996) Streblidae (Diptera: Calyptratae) parásitos de murciélagos (Mammalia: Chiroptera) cavernícolas del centro y sur de México, con descripción de una especie nueva del género Trichobius. Anales del Instituto de Biología. Serie Zoología 67, 357–373.Google Scholar
Jaeger, JA (2000) Landscape división, splitting index, and effective mesh size: new measures of landscape fragmentation. Landscape Ecology 15, 115–130.Google Scholar
Jones, G et al. (2009) Carpe noctem: the importance of bats as bioindicators. Endanger Species Research 8, 93–115.Google Scholar
Judson, SD, Frank, HK and Hadly, EA (2015) Bartonellae are revalent and diverse in Costa Rican bats and bat flies. Zoonoses and Public Health 62, 609–617.Google Scholar
Jung, M (2016) Lecos –A python plugin for automated landscape ecology analysis. Ecological Informatics 31, 18–21.Google Scholar
Kindt, R and Coe, R (2005) Tree Diversity Analysis. A Manual and Software for Common Statistical Methods for Ecological and Biodiversity Studies. Nairobi, Kenya: World Agroforestry Centre (ICRAF).Google Scholar
Klingbeil, BT and Willig, MR (2009) Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian rainforest. Journal of Applied Ecology 46, 203–213.Google Scholar
Kunz, TH et al. (2011) Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223, 1, 1–38.Google Scholar
Lemke, TO (1984) Foraging ecology of the long-nosed bat, Glossophaga soricina, with respect to resource availability. Ecology 65, 538–548.Google Scholar
Leulmi, H et al. (2016) Detection of Bartonella tamiae, Coxiella burnetii and rickettsiae in arthropods and tissues from wild and domestic animals in northeasterns Algeria. Parasites & Vectors 9, 27.Google Scholar
Lobova, TA, Geiselman, CK and Mori, SA (2009) Seed dispersal by bats in the neotropics. New York Botanical Garden 101, 1–47.Google Scholar
Lott, EJ (2002) Lista anotada de las plantas vasculares de Chamela–Cuixmala. In Noguera, FA, Vega, JH, García, AN and Quesada, (eds), Historia Natural de Chamela. México: Instituto de Biología UNAM, pp. 99–136.Google Scholar
Luna, P, (2017) The risk of use small matrices to measure specialization in host–parasite interaction networks: a comment to Rivera-García, et al. (2016). Parasitology 144, 1102–1106.Google Scholar
Magurran, AE and McGill, BJ (2011) Biological Diversity: Frontiers in Measurement and Assessment. New York, USA: Oxford University Press.Google Scholar
Marshall, AG (1982) Ecology of insects ectoparasitic on bats. In Kunz, TH (ed.), Ecology of Bats. USA: Plenum Press, Springer, pp. 369–401.Google Scholar
Marques, JT, Ramos-Pereira, MJ, Marques, TA, Santos, CD, Santana, J, Beja, P and Palmeirim, J (2013) Optimizing sampling design to deal with mist-net avoidance in Amazonian birds and bats. PLoS ONE 8, e74505. doi: 10.1371/journal.pone.0074505.Google Scholar
McCauley, DJ et al. (2015) Effects of land use on plague (Yersinia pestis) activity in rodents in Tanzania. American Journal of Tropical Medicine and Hygiene 92, 776–783.Google Scholar
McCune, B and Grace, JB (2002) Analysis of Ecological Communities. Gleneden Beach, Oregon, USA: MJM Software Desing.Google Scholar
McGarigal, K (2002) Landscape pattern metrics. In El-Shaa-rawi, AH and Piegorsch, WW (eds), Encyclopedia of Environmetrics, Vol. 2. Chichester: Wiley, pp. 1135–1142.Google Scholar
Medellín, RA, Arita, HT and Sanchez, O (2007) Identificación de los murciélagos de México, 2nd Edn. México: Instituto de Ecología, UNAM. d.f.Google Scholar
Morrison, DW (1978) Influence of hábitat on the foraging distances of the fruit bat, Artibeus jamaicensis. Journal of Mammalogy 59, 622–624.Google Scholar
Muscarella, R and Fleming, TH (2007) The role of frugivorous bats in tropical forest succession. Biological Reviews 82, 573–590.Google Scholar
Neter, J, Wasserman, W and Kutner, MH (1990) Applied Linear Statistical Models, 3rd Edn. Chicago, USA: Irwin.Google Scholar
Oksanen, J (2015) Multivariate Analysis of Ecological Communities in R: Vegan Tutorial. Finland: University of Oulu.Google Scholar
Ortega, J and Castro-Arellano, I (2001) Artibeus jamaicensis. Mammalian species. American Society of Mammalogists 662, 1–9.Google Scholar
Ortiz-Ramírez, D et al. (2006) Roost selection by three frugivorous bats Chiroptera: Phyllostomidae in the Lacandon Forest, Chiapas, Mexico. Revista Mexicana de Biodiversidad 77, 261–270.Google Scholar
Ostfeld, RS and Keesing, F (2012) Effect of host diversity on infectious disease. Annual Review of Ecology, Evolution, and Systematics 43, 157–182.Google Scholar
Ostfeld, RS, Keesing, F and Eviner, VT (2008) Infectious Disease Ecology: Effect of Ecosystems on Diseases and of Diseases on Ecosystems. New Jersey, USA: Princeton University Press.Google Scholar
Patterson, BD, Dick, CW and Dittmar, K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23, 177–189.Google Scholar
Peig, J and Green, A (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 1883–1891.Google Scholar
Peterson, BV and Hurka, K (1974) Ten new species of bat flies of the genus Trichobius (Diptera: Streblidae). The Canadian entomologist 106, 1049–1066.Google Scholar
Pilosof, S et al. (2012) Effect of anthropogenic disturbance and climate on patterns of bat fly parasitism. PLoS ONE 7, e41487.Google Scholar
Pinheiro, J et al. (2016) _nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1–128. http://CRAN.R-project.org/package=nlme.Google Scholar
Portillo-Quintero, CA and Sánchez-Azofeifa, GA (2010) Extent and conservation of tropical dry forests in the Americas. Biological Conservation 143, 144–155.Google Scholar
Presley, SJ (2011) Interspecific aggregation of ectoparasites on bats: importance of host as habitats supersedes interspecific interactions. Oikos 120, 832–841.Google Scholar
QGIS Geographic Information System. QGIS Development Team (2015) Open Source Geospatial Foundation Project. [accessed 2016 March 27]. Available from: http://qgis.osgeo.org.Google Scholar
R Development Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.Google Scholar
Reeder, D and Wilson, D (2005). Mammal Species of the World, 1st Edn. Baltimore, USA: Johns Hopkins: University Press.Google Scholar
Sanchez-Azofeifa, GA et al. (2005) Research priorities for neotropical dry forests. Biotropica 37, 477–485.Google Scholar
Sánchez-Azofeifa, GA et al. (2013). Human and Biophysical Dimensions of Tropical Dry Forest in the Americas. Boca Raton, USA: Taylor and Francis Group.Google Scholar
Schmidt, KA and Ostfeld, RS (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619.Google Scholar
Sikes, RS, Gannon, WH and The Animal Care and Use Committee of The American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92, 235–253.Google Scholar
Smith, EP and van Belle, G (1984) Nonparametric estimation of species richness. Biometrics 40, 119–129.Google Scholar
Suzán, G et al. (2012) Habitat fragmentation and infectious disease ecology. In Aguirre, AA, Ostfeld, RS and Daszak, P (eds), New Directions in Conservation Medicine: Applied Cases of Ecological Health. Oxford University Press, New York, pp. 135–150.Google Scholar
Velazco, PM and Patterson, BD (2013) Diversification of the Yellow-shouldered bats, genus Sturnira (Chiroptera, Phyllostomidae), in the New World tropics. Molecular Phylogenetics and Evolution 68, 683–698.Google Scholar
Wenzel, RL (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin. Biological Series 20(4), 1–177.Google Scholar
Wenzel, RL, Tipton, VJ and Kiewlicz, A (1966) The Streblid Batflies of Panama (Diptera Calypterae: Streblidae). Chicago, USA: Field Museum of Natural History.Google Scholar
Whitaker, JO and Morales-Malacara, JB (2005) Ectoparasites and other associates (Ectodytes) of Mammals of Mexico. In Sánchez-Cordero, V and Medellín, R (eds), Contribuciones mastozoológicas en homenaje a Bernardo Villa. México: Instituto de Biología, UNAM; Instituto de Ecología, UNAM; CONABIO. d.f., pp. 535–666.Google Scholar
Young, HS et al. (2015) Drivers of intensity and prevalence of flea parasitism on small mammals in East African savannah ecosystems. Journal of Parasitology 101, 327–335.Google Scholar
Zarazúa-Carbajal, M et al. (2017) Importance of riparian habitat for frugivorous bats in a tropical dry forest in western Mexico. Journal of Tropical Ecology 33, 74–82.Google Scholar
Supplementary material: File

Hernández-Martínez et al. supplementary material

Table S1

Download Hernández-Martínez et al. supplementary material(File)
File 101.8 KB
Supplementary material: File

Hernández-Martínez et al. supplementary material

Table S2

Download Hernández-Martínez et al. supplementary material(File)
File 121.4 KB