Advertisement

Mammalian Biology

, Volume 95, Issue 1, pp 93–101 | Cite as

Influence of vegetation and abiotic factors on habitat use by insectivorous bats in subtropical mountain forests

  • Marcial Alejandro Rojo Cruz
  • Susana Zuloaga-Aguilar
  • Ramón Cuevas-Guzmán
  • María Cristina MacSwiney González
  • Luis Ignacio Iñiguez-DávalosEmail author
Original investigation
First Online:

Abstract

Forest structure and abiotic factors influence the habitat use of many mammals. For insectivorous bats, characteristics such as plant density, canopy cover, temperature, relative humidity and other seasonal changes over the course of the year can be important as regulators of food resource accessibility, and consequently of their nutritional health. The aim of this study was to determine the influence of the structure in two different forest types and of two abiotic factors, temperature and relative humidity, on habitat use by insectivorous bats in forests that present relatively small seasonal phenological changes. Sampling was conducted with ultrasonic detectors and the resulting recordings were used to analyse bat calls for identification of species and determination of bat activity. We found significant differences among the relative activities of the study species in both vegetation types. There was a tendency towards a greater increase in activity throughout the year in forests with either greater canopy cover or higher plant density. We found a positive correlation between temperature and activity in most of the recorded species, and a negative correlation between relative humidity and this activity. Our results show that relative humidity seems to be more influential than temperature on the activity patterns of insectivorous bats. Attenuation and its consequences could be more important to habitat use than heat loss in temperate subtropical forests (both cloud forest and pine forest).

Keywords

Insectivorous bats Relative activity Relative humidity Seasonality Temperature Vegetation structure 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aldridge, H.D.J.N., Rautenbach, L., 1987. Morphology, echolocation and resource partitioning in insectivorous bats. J. Anim. Ecol. 56 (3), 763–778.Google Scholar
  2. Almeida, M.H., Ditchfield, A.D., Tokumaru, R.S., 2014. Habitat characteristics and insectivorous bat activity. Chiropt. Neotrop. 20 (2), 1264–1270.Google Scholar
  3. Ayala-Berdón, J., Solís-Cárdenas, V., 2017. New record and site characterization of a hibernating colony ofMyotis velifer in a mountain ecosystem of central Mexico. Therya 8 (2), 171–174.Google Scholar
  4. Barros, M.A.S., Pessoa, D.M.A., Rui, A.M., 2014. Habitat use and seasonal activity of insectivorous bats (Mammalia: Chiroptera) in the grasslands of southern Brazil. Zoologia 31 (2), 153–161.Google Scholar
  5. Braun de Torrez, E.C., Ober, H.K., McCleery, R.A., 2017. Critically imperiled forest fragment supports bat diversity and activity within a subtropical grassland. J. Mammal. 20 (10), 1–10.Google Scholar
  6. Brunner, E., Domhof, S., Langer, F., 2002. Nonparametric Analysis of Longitudinal Data in Factorial Experiments. J. Wiley and Sons, New York, NY.Google Scholar
  7. Canals, M., Iriarte-Diaz, J., Olivares, R., Novoa, F.F., 2001. Comparación de la morfología alar deTadarida brasiliensis (Chiroptera: Molossidae) y Myotis chiloensis(Chiroptera: Vespertilionidae), representantes de dos diferentes tipos de vuelo. Rev. Chil. Hist. Nat. 74, 699–704.Google Scholar
  8. Ciechanowski, M., Zieliñska, T.A., Dunajskin, R., 2010. Seasonal activity patterns of seven vespertilionid bat species in Polish lowlands. Acta Theriol. 55 (4), 301–314.Google Scholar
  9. CONANP, 2000. Programa De Manejo Reserva De La Biosfera Sierra De Manantlán, México. Comisión Nacional de Áreas Naturales Protegidas, México D.F., México.Google Scholar
  10. Cryan, P.M., Bogan, M.A., Altebach, J.S., 2000. Effect of elevation on distribution of female bats in black hills, South Dakota. J. Mammal. 81 (3), 719–725.Google Scholar
  11. Cuevas-Guzmán, R., Jardel-Peláez, E.J., 2004. Flora Y Vegetación De La Estación Científica Las Joyas. Universidad de Guadalajara, Autlán de Navarro, Jalisco, México.Google Scholar
  12. Erickson, J.L., West, S.D., 2002. The influence of regional climate and nightly weather conditions on activity patterns of insectivorous bats. Acta Chiropt. 4 (1), 17–24.Google Scholar
  13. Estrada-Villegas, S., McGill, B.J., Kalko, E.K.V., 2012. Climate, habitat, and species interactions at different scales determine the structure of a neotropical bat community. Ecology 93 (5), 1183–1193.PubMedGoogle Scholar
  14. Fenton, M.B., 1970. A technique for monitoring bat activity with results obtained from different environments in southern Ontario. Can. J. Zool. 48, 847–851.Google Scholar
  15. Fleming, T.H., Eby, P., 2003. Ecology of bat migration. In: Kunz, T.H., Fenton, M.B. (Eds.), Bat Ecology. The University of Chicago Press, Chicago, Illinois, pp. 156–208.Google Scholar
  16. Fukui, D., Murakami, M., Nakano, S., Aoi, T., 2006. Effect of emergent aquatic insects on bat foraging in a riparian forest. J. Anim. Ecol. 75, 1252–1258.PubMedGoogle Scholar
  17. Gonsalves, L.B., Law, B., Webb, C., Monammy, V., 2013. Foraging ranges of insectivorous bats shift relative to changes in mosquito abundance. PLoS One 8 (5), e64081, http://dx.doi.org/10.1371/journal.pone.006408.PubMedPubMedCentralGoogle Scholar
  18. Griffin, D.R., 1971. The importance of atmospheric attenuation forthe echolocation of bats (Chiroptera). Animal Behav. 19, 55–61.Google Scholar
  19. Guillén, A., Juste, B.J., Ibanez, C., 2000. Variation in the frequency of the echolocation calls of Hipposideros ruber in the Gulf of Guinea: an exploration of the adaptive meaning of the constant frequency value in rhinolophoid CF bats. J. Evol. Bio. 13, 70–80.Google Scholar
  20. Hamilton, I.M., Barclay, R.M.R., 1994. Patterns of daily torpor and day-roost selection by male and female big brown bats (Eptesicus fuscus). Can. J. Zool. 72, 744–749.Google Scholar
  21. Iniguez-Dávalos, L.I., 1993. Patrones ecológicos de la comunidad de murciélagos de la Sierra de Manantlán. In: Medellin, R., Ceballos, G. (Eds.), Avances En El Estudio De Los Mamíferos De Mexico. Asociacion Mexicana de Mastozoologia A.C. México DF, México, pp. 355–370.Google Scholar
  22. Iniguez-Dávalos, L.I., Jalisco, Mexico. Ph.D. Dissertation 2005. Hábitos alimentarios de murciélagos frugivoros en el bosque mesófilo de montan˜a de la Sierra de Manantlán. Universidad Nacional Autónoma de México. México DF, México.Google Scholar
  23. Jardel-Peláez, E.J., 1992. Estrategia para la conservación de la Reserva de la Biosfera Sierra de Manantlán. Universidad de Guadalajara, Guadalajara, Jalisco, México.Google Scholar
  24. Jardel-Peláez, E.J., 2015. Guía para lacaracterizacióny clasificaciónde hábitats forestales. Comisión Nacional Forestal (CONAFOR), México.Google Scholar
  25. Jung, K., Kaiser, S., Böm, S., Nieschulze, J., Kalko, E.K.V., 2012. Moving in three dimensions: effects of structural complexity on occurrence and activity of insectivorous bats in managed forest stands. J. Appl. Ecol. 49, 523–531.Google Scholar
  26. Kapfner, G., Aron, S., 2007. Temporal variation in flight activity, foraging activity and social interactions by bats around a suburban pond. Lutra 50 (1), 9–18.Google Scholar
  27. Kraker-Castañeda, C., Santos-Moreno, A., Garcia, J.L, 2013. Riqueza de especies y actividad relativa de murciélagos insectívoros aéreos en una selva tropical y pastizales en Oaxaca, México. Mastozool. Neotrop. 20 (2), 255–267.Google Scholar
  28. Kusch, J., Weber, C., Idelberger, S., 2004. Foraging habitat preferences of bats in relation to food supply and spatial vegetation structures in a western European low mountain. Folia Zool. Brno 53, 113–128.Google Scholar
  29. Lawrence, B.D., Simmons, J.A., 1982. Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. J. Acoust. Soc. Am. 71 (3), 585–590.PubMedGoogle Scholar
  30. Lewis, S., 1993. Effect of climatic variation on reproduction by pallid bats (Antrozous pallidus). Can. J. Zool. 71, 1429–1433.Google Scholar
  31. Loeb, S.C., OKeffe, J.M., 2006. Habitat use by forest bats in South Carolina in relation to local, stand and landscape characteristics. J. Wildl. Manage. 70 (5), 1210–1218.Google Scholar
  32. Lucz, T.M.J., Barclay, R.M.R., 2016. Influence of forest composition and age on habitat use by bats in southwestern British Columbia. Can. J. Zool. 94, 145–153.Google Scholar
  33. Marques, J.T., Ramos-Pereira, M.J., Palmeirim, J.M., 2016. Patterns inthe use of rainforest vertical space by Neotropical aerial insectivorous bats: all the action is up inthe canopy. Ecography 39, 476–486.Google Scholar
  34. Martins, M.A., De Carvalho, W.D., Dias, D., Franc¸a, D., De Oliveira, M.B., Peracchi, A.L., 2015. Bat species richness (Mammalia, Chiroptera) along an elevational gradient inthe Atlantic forest of southeastern Brazil. Acta Chirop. 17 (2), 401–409.Google Scholar
  35. McCune, B., Mefford, M.J., 2011. PC-ORD. Multivariate Analysis of Ecological Data. Version 6.0. MjM Software, Gleneden Beach, Oregon, U.S.A.Google Scholar
  36. McGuire, L.P., Boyle, W.A., 2013. Altitudinal migration in bats: evidence, patterns, and drivers. Biol. Rev. 88, 767–786.PubMedGoogle Scholar
  37. Miller, B.W., 2001. A method for determining relative activity of free flying bats using a new activity index for acoustic monitoring. Acta Chirop. 3, 93–105.Google Scholar
  38. Norberg, U.M., Rayner, J.M., 1987. Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Biol. Sci. 316, 335–427.Google Scholar
  39. O’Donell, C.F.J., 2000. Influence of season, habitat, temperature, and invertebrate availability on nocturnal activity of the New Zealand long-tailed bat (Chalinolobus tuberculatus). N.Z.J. Zool. 27 (3), 207–221.Google Scholar
  40. O’Donell, C.F.J., Christie, J.E., Simpson, W., 2006. Habitat use and nocturnal activity of lesser short-tailed bats (Mystacina tuberculata) in comparison with long-tailed bats (Chalinolobus tuberculatus) in temperate rainforest. N.Z. J. Zool. 33 (2), 113–124.Google Scholar
  41. Ober, H.K., Hayes, J.P., 2008. Prey selection by bats in forests of western Oregon. J. Mammal. 89, 1191–1200.Google Scholar
  42. Orozco-Lugo, L., Guillén-Servent, A., Valenzuela, D., Arita, H.T., 2013. Descripción de los pulsos de ecolocalización de once especies de murciélagos insectívoros aéreos de una selva baja caducifolia en Morelos, México. Therya 4 (1), 33–46.Google Scholar
  43. Orozco-Lugo, L., Guillén-Servent, A., Valenzuela, D., Arita, H.T., Bonigo, N.A., 2017. Variación espacio-temporal en la actividad relativa de murciélagos insectívoros aéreos en la Reserva de la Biosfera Sierra de Huautla, Morelos, México. Áreas Nat. Protegidas Scr. 3 (1), 35–57.Google Scholar
  44. Patriquin, K.J., Hogberg, L.K., Chruszcz, B.J., Barclay, R.M.R., 2003. The influence of habitat structure on the ability to detect ultrasound using bat detectors. Wildl. Soc. Bull. 31 (2), 475–481.Google Scholar
  45. Petit, T.W., Wilkins, K.T., 2012. Canopy and edge activity of bats in a quaking aspen (Populus tremuloides) forest. Can. J. Zool. 90, 798–807.Google Scholar
  46. Pohlert, T., 2014. The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR). R Package. http://CRAN.R-project.org/package=PMCMR.Google Scholar
  47. R Core Team, 2017. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/.Google Scholar
  48. Raimondo, S., Strazanac, J.S., Butler, L., 2004. Comparison of sampling techniques used in studying Lepidoptera population dynamics. Environ. Entomol. 33, 418–425.Google Scholar
  49. Ramírez-Pulido, J., González-Ruiz, N., Gardner, A.L., Arroyo-Cabrales, J., 2014. List of Recent Land Mammals of Mexico. Special Publications, vol. 63. Museum of Texas Tech University, pp. 1–69.Google Scholar
  50. Ruggiero, A., 2001. Interacciones entre la biogeografía ecológica y la macroecología: aportes para comprender los patrones espaciales en la diversidad biológica. In: Llorente-Bousquets, J., Morrone, J.J. (Eds.), Introducción a La Biogeografía En Latinoámerica: Teorías, Conceptos, Métodos Y Aplicaciones. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO). México DF, México, pp. 81–95.Google Scholar
  51. Russ, J.M., Briffa, M., Montgomery, W.I., 2003. Seasonal patterns in activity and habitat use by bats (Pipistrellus spp. and Nyctalus leisleri) in Northern Ireland, determined using a driven transect. J. Zool. 259, 289–299.Google Scholar
  52. Russell, A.L., Medellín, R.A., McCracken, G.F., 2005. Genetic variation and migration in the Mexican free tailed bat (Tadarida brasiliensis). Mol. Ecol. 14, 2207–2222.PubMedGoogle Scholar
  53. Russo, D., Cistrone, L., Jones, G., 2007. Emergence time in forest bats: the influence of canopy closure. Acta Oecol. Montrouge (Montrouge) 31, 119–126.Google Scholar
  54. Schnitzler, H.U., Kalko, E.K.V., 2001. Echolocation by insect-eating bats. BioScience 51 (7), 557–569.Google Scholar
  55. Snell-Rood, E.C., 2012. The effect of climate on acoustic signals: does atmospheric sound absorption matter for bird song and bat echolocation? J. Acoust. Soc. Am. 131, 1650–1658.PubMedGoogle Scholar
  56. Speakman, J.R., Racey, P.A., 1987. The energetics of pregnancy and lactation in the brown long-eared bat, Plecotus aurituss. In: Fenton, M.B., Racey, P.A., Rayner, J.M.V. (Eds.), Recent Advances in the Study of Bats. Cambridge University Press, Cambridge, UK, pp. 367–393.Google Scholar
  57. Stones, R.C., Wiebers, J.E., 1965. A review of temperature regulation in bats (Chiroptera). Am. Midl. Nat. 74, 155–167.Google Scholar
  58. Velica-Zúñiga, G., 2013. Vegetación y patrones geoecológicos de la Reserva de la Biosfera Sierra de Manantlán. Master in Science (Natural Resources Management) dissertation. Autlán de Navarro, Jalisco, México.Google Scholar
  59. Waters, D.A., Rydell, J., Jones, G., 1995. Echolocation calls design and limits on preys size: a case study using the aerial-hawking bat Nyctalus lesileri. Behav. Ecol. Sociobiol. (Print) 37, 321–328.Google Scholar
  60. Wickramasinghe, L.P., Harris, S., Jones, G., Vaughan, N., 2003. Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. J. Appl. Ecol. 40, 984–993.Google Scholar
  61. Wilcox, E.V., Giuliano, W.M., Watine, L.N., Mills, D.J., Andreu, M.G., 2017. Forest structure and composition affect bats in a tropical evergreen broadleaf forest. Forest 8, 317–331.Google Scholar
  62. Wilkinson, G.S., Fleming, T.H., 1996. Migration and evolution of lesser long-nosed bats Leptonycteris curasoae, inferred from mitochondrial DNA. Mol. Ecol. 5, 329–339.PubMedGoogle Scholar
  63. Wolbert, S.J., Zellner, A.S., Whidden, H.P., 2014. Bat activity, insect biomass, and temperature along an elevational gradient. Northeast. Nat. (Steuben) 21 (1), 72–85.Google Scholar
  64. Wolda, H., 1988. Insects seasonality: Why? Ann. Rev. Ecol. Syst. 19, 1–18.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2019

Authors and Affiliations

  • Marcial Alejandro Rojo Cruz
    • 1
  • Susana Zuloaga-Aguilar
    • 2
  • Ramón Cuevas-Guzmán
    • 2
  • María Cristina MacSwiney González
    • 3
  • Luis Ignacio Iñiguez-Dávalos
    • 2
    Email author
  1. 1.Doctorado en Biosistemática, Ecología y Manejo de Recursos Naturales y AgrícolasUniversidad de GuadalajaraAutlánMexico
  2. 2.Departamento de Ecología y Recursos Naturales - IMECBIOUniversidad de GuadalajaraAutlánMexico
  3. 3.Centro de Investigaciones TropicalesUniversidad VeracruzanaXalapa, VeracruzMexico

Personalised recommendations

Cite article

Buy options