From the bottom up – attributes of small vesper bats’ activity sites in an upland ecosystem in Chiapas, México

Authors

Keywords:

Forest loss, hierarchical partitioning, landscape level, local level, Myotis spp., small natural features, targeted conservation

Abstract

We studied bats in a natural protected area and the influence zone in Chiapas, México. Focusing on small vesper bats (Vespertilionidae: Myotinae) in water sinkholes, flooded surfaces, and forested locations (sampling sites), our objectives were to: 1) differentiate the sampling sites based on abiotic and biotic variables, 2) compare the relative activity between the contrasting sampling sites, and 3) determine the relative importance of surrounding land covers amounts on the relative activity. We expected the following: 1) that sampling sites would be differentiable based on an interaction of environmental conditions and nocturnal flying insects’ biomass, 2) to find a significantly higher relative activity associated with water bodies as a reflection of potential drinking and feeding supplies, and 3) that forest cover would have a significant association in a positive direction with the relative activity as a reflection of roosting and commuting opportunities. We obtained weather data with a portable station, collected flying nocturnal insects with a passive trap, and recorded bats with ultrasonic detectors. We also used satellite imagery to calculate land covers amounts around the sampling sites. We performed a multivariate analysis to compare sampling sites, and elaborated correlation models of relative activity against surrounding land covers amounts. The only significant variable for differentiating sampling sites was wind speed; in water sinkholes, with lower mean value compared to flooded surfaces and forested locations, along with a comparatively higher percentage of dipterans in the samples. The mean relative activity of bats was significantly higher in water sinkholes, with maximum values reaching 95 %, which we can relate to environmental conditions and resources available. We found associations in a positive direction with forest cover, secondary forest and water surface, and negative with agricultural land and human development. Finally, we argue that some of the water sinkholes meet the criteria of small natural features supported by the unusual activity of the studied bats, and that targeted conservation actions will complement other strategies implemented in the area.

References

AGUIAR, L. M. S., AND Y. ANTONINI. 2008. Diet of two sympatric insectivores bats (Chiroptera: Vespertilionidae) in the Cerrado of Central Brazil. Revista Brasileira de Zoologia 25:28-31.

ARROYO-RODRÍGUEZ, V., ET AL. 2016. Landscape composition is more important than landscape configuration for phyllostomid bat assemblages in a fragmented biodiversity hotspot. Biological Conservation 198:84-92.

BADER, E., ET AL. 2015. Mobility explains the response of aerial insectivorous bats to anthropogenic habitat change in the Neotropics. Biological Conservation 186:97-106.

BARQUEZ, R., AND M. DIAZ. 2016. Myotis keaysi. In: IUCN 2022. The IUCN Red List of Threatened Species. Version 2022-1. www.iucnredlist.org. Accessed on 7 December 2022.

BRADLEY, E.S., ET AL. 1993. Estimation of insect biomass by length and width. The American Midland Naturalist 129:234-240.

CHEVAN, A., AND M. SUTHERLAND. 1991. Hierarchical partitioning. The American Statistician 45:90-96.

COLEMAN, L.S., ET AL. 2014. Comparison of radio-telemetric home-range analysis and acoustic detection for little brown bat habitat evaluation. Northeastern Naturalist 21:431-445.

EASTMAN, J.R. 2012. IDRISI selva tutorial: manual version 17. Clark Labs. Clark University. Massachusetts, U.S.A.

ESTRADA-VILLEGAS, S., B. J. MCGILL, AND E. K. V. KALKO. 2012. Determinants of species evenness in a Neotropical bat ensemble. Oikos 121:927-941.

FAHRIG, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics 34:487-515.

FALCÃO, F., ET AL. 2021. Landscape structure shapes activity levels and composition of aerial insectivorous bats at different spatial scales. Biodiversity and Conservation 30:2545-2564.

FENTON, M. B., AND W. BOGDANOWICZ. 2002. Relationships between external morphology and foraging behaviour: bats in the genus Myotis. Canadian Journal of Zoology 80:1004-1013.

FINDLEY, J. S. 1993. Bats. A Community Perspective. Cambridge University Press. Cambridge, Great Britain.

FISCHER, J., AND D. B. LINDENMAYER. 2007. Landscape modification and habitat fragmentation: a synthesis. Global Ecology and Biogeography 16:265-280.

FREY-EHRENBOLD, A., ET AL. 2013. Landscape connectivity, habitat structure and activity of bat guilds in farmland-dominated matrices. Journal of Applied Ecology 50:252-261.

FROIDEVAUX, J. S. P., ET AL. 2021. Bat responses to changes in forest composition and prey abundance depend on landscape matrix and stand structure. Scientific Reports 11:10586.

FUENTES-MONTEMAYOR E, ET AL. 2013. Fragmented forests in agricultural landscapes: The influence of forest character and landscape context on bats and their insect prey. Agriculture, Ecosystems & Environment 172:6-15.

FUENTES-MONTEMAYOR, E., ET AL. 2017. Species mobility and landscape context determine the importance of local and landscape-level attributes. Ecological Applications 27:1541-1554.

GAMBOA ALURRALDE, S., AND M. M. DÍAZ. 2019. Feeding habits of four species of Myotis (Mammalia, Chiroptera) from Argentina. Mammal Research 64:511-518.

GILLIES, M. T., AND T. J. WILKES. 1981. Field experiments with a wind tunnel on the flight speed of some West African mosquitoes (Diptera: Culicidae). Bulletin of Entomological Research 71:65-70.

GONSALVES, L., ET AL. 2013. Mosquito consumption by insectivorous bats: Does size matters? PLoS ONE 8:e77183.

GONZÁLEZ, E. M., AND M. N. RAMÍREZ. 2013. Comunidades vegetales terrestres. Pp. 21-42 in La Biodiversidad en Chiapas: Estudio de Estado. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Gobierno del Estado de Chiapas, Chiapas, México.

HEIM, O., ET AL. 2015. The importance of landscape elements for bat activity and species richness in agricultural areas. PLoS ONE 10:e0134443.

HUNTER, JR., M. L. 2017. Conserving small natural features with large ecological roles: An introduction and definition. Biological Conservation 211:1-2.

HUNTER, JR., M. L., ET AL. 2017. Conserving small natural features with large ecological roles: A synthetic overview. Biological Conservation 211:88-95.

INGALA, M. R., ET AL. 2021. Molecular diet analysis of neotropical bats based on fecal DNA metabarcoding. Ecology and Evolution 11:7474-7491.

JUNG, K., AND E. K. V. KALKO. 2011. Adaptability and vulnerability of high flying Neotropical aerial insectivorous bats to urbanization. Diversity and Distributions 17:262-274.

JONES, G., AND J. RYDELL. 2003. Attack and defense: Interactions between echolocating bats and their insect prey. Pp. 301-345, in Bat Ecology (Kunz, T. H., and M. B. Fenton, eds.). The University of Chicago Press. Chicago, U.S.A.

LACKI, M. J., J. P. HAYES, AND A. KURTA (eds.). 2007. Bats in Forests: Conservation and Management. The Johns Hopkins University Press. Baltimore, U.S.A.

LAURINDO, R. S., ET AL. 2020. Feeding habits define habitat use by bats in an agricultural landscape of the Atlantic Forest. Revista Mexicana de Biodiversidad 91:e913223.

LÓPEZ-GONZÁLEZ, C., ET AL. 2016. Activity of insectivorous bats is related to water availability in a highly modified Mexican temperate forest. Acta Chiropterologica 18:409-421.

LU, D., AND Q. WENG. 2007. A survey of image classification methods and techniques for improving classification performance. International Journal of Remote Sensing 28:823-870.

MAC NALLY, R. 2000. Regression and model-building in conservation biology, biogeography and ecology: the distinction between – and reconcilitation of – ‘predictive’ and ‘explanatory’ models. Biodiversity and Conservation 9:655-671.

MAC NALLY, R. 2002. Multiple regression and inference in ecology and conservation biology: further comments on identifying important predictor variables. Biodiversity and Conservation 1:1397-1401.

MACSWINEY G., M. C., F. M. CLARKE, AND P. A. RACEY. 2009. Insectivorous bats activity at cenotes in the Yucatan Peninsula, México. Acta Chiropterologica 11:139-147.

MARTINO, A. M. G., D. BORGES, AND J. M. NASSAR. 2019. Activity records of the endangered Paraguaná moustached bat, Pteronotus paraguanensis, in the main vegetation types of the Paraguaná Peninsula, Venezuela. Acta Chiropterologica 21:165-174.

MENDES, E. S., ET AL. 2017. Bat richness and activity in heterogeneous landscapes: guild-specific and scale-dependent? Landscape Ecology 32:295-311.

MILLER, B. W. 2001. A method for determining relative activity of free flying bats using a new activity index for acoustic monitoring. Acta Chiropterologica 3:93-105.

MILLER, B., ET AL. 2016. Rhogeessa tumida. In: IUCN 2022. The IUCN Red List of Threatened Species. Version 2022-1. www.iucnredlist.org. Accessed on 7 December 2022.

NORBERG, U. M., AND J. M. V. RAYNER. 1987. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society B: Biological Sciences 316:335-427.

NOVELLA-FERNANDEZ, R., ET AL. 2022. The role of forest structure and composition in driving the distribution of bats in Mediterranean regions. Scientific Reports 12:3224.

O’FARRELL, M. J., AND B. W. MILLER. 1999. Use of vocal signatures for the inventory of free-flying Neotropical bats. Biotropica 31:507-516.

OLEA, P. P., P. MATEO-TOMÁS P, AND Á. DE FRUTOS. 2010. Estimating and modelling bias of the hierarchichal partitioning public-domain software: implications in environmental management and conservation. Plos One 5:e11698.

OROZCO-LUGO, C. L., ET AL. 2013. Descripción de los pulsos de ecolocalización de once especies de murciélagos insectívoros aéreos de una selva baja caducifolia en Morelos, México. Therya 4:33-46.

OWEN, S. F., ET AL. 2003. Home-range size and habitat used by the northern Myotis (Myotis septentrionalis). The American Midland Naturalist 150:352-359.

PARREIRA PEIXOTO, F., P. H. PEREIRA BRAGA, AND P. MENDES. 2018. A synthesis of ecological and evolutionary determinants of bat diversity across spatial scales. BMC Ecology 18:18.

PETTERSSON, L. 2002. The properties of sound and bat detectors. Pp. 9-12 in Bat Echolocation Research: Tools Techniques and Analysis (Brigham, R. M., et al., eds.). Bat Conservation International. Texas, U.S.A.

POPESCU, V. D., AND P. GIBBS. 2010. Landscape ecology and GIS methods. Pp. 339-360, in Amphibian Ecology and Conservation: A Handbook of Techniques (Kenneth Jr., C., ed.). Oxford University Press. New York, U.S.A.

PUIG-MONTSERRAT, X., ET AL. 2020. Bats actively prey on mosquitoes and other deleterious insects in rice paddies: Potential impact on human health and agriculture. Pest Management Science 76:3759-3769.

PUT, J. E., L. FAHRIG, AND G. W. MITCHELL. 2019. Bats respond negatively to increases in the amount and homogenization of agricultural land cover. Landscape Ecology 34:1889-1903.

QUEIROZ DE OLIVEIRA, L., ET AL. 2015. Activity of the insectivorous bat Pteronotus parnellii relative to insect resources and vegetation structure. Journal of Mammalogy 96:1036-1044.

RAUCHENSTEIN, K., ET AL. 2022. LiDAR metrics predict suitable forest foraging areas of endangered mouse-eared bats (Myotis myotis). Forest Ecology and Management 515:120210.

R CORE TEAM. 2019. R: A language and environment for statistical computing. Foundation for Statistical Computing. http://R-project.org. Accessed 19 December 2019.

RADFORD, J. Q., AND A. F. BENNETT. 2007. The relative importance of landscape properties for forest birds in agricultural environments. Journal of Applied Ecology 44:737-747.

RODRÍGUEZ-SAN PEDRO, A., AND J. A. SIMONETTI. 2015. The relative influence of forest loss and fragmentation on insectivorous bats: does the type of matrix matter? Landscape Ecology 30:1561-1572.

RUSSO, D., ET AL. 2015. The buzz of drinking on the wing in echolocating bats. Ethology 122:226-235.

RUTLEDGE, C. R. 2008. Mosquitoes (Diptera: Culicidae). Pp. 2476-2483, in Encyclopedia of Entomology (Capinera, J. L., ed.). Springer. Dordrecht, Netherlands.

RYDELL, J., ET AL. 2017. Testing the performances of automated identification of bat echolocation calls: A request for prudence. Ecological Indicators 78:416-420.

SCHNITZLER, H.-U., AND E. K. V. KALKO. 2001. Echolocation by Insect-Eating Bats. Bioscience 51:557-569.

SALINAS-RAMOS, V. B., ET AL. 2015. Dietary overlap and seasonality in three species of mormoopid bats from a tropical dry forest. Molecular Ecology 24:5296-5307.

SEGURA-TRUJILLO, C. A., M. R. WILLIG, AND S. T. ÁLVAREZ-CASTAÑEDA. 2018. Correspondence between ecomorphotype and use of arthropod resources by bats of the genus Myotis. Journal of Mammalogy 99:659-667.

SEIBOLD, S., ET AL. 2013. Ponds in acidic mountains are more important providing drinking water than insect prey. Journal of Zoology 290:302-308.

SOLARI, S. 2019. Myotis nigricans. In: IUCN 2022. The IUCN Red List of Threatened Species. Version 2022-1. www.iucnredlist.org. Accessed on 7 December 2022.

VERBYLA, D. L. 1995. Satellite remote sensing of natural resources. CRC Press. Boca Raton, U.S.A.

WALSH, C., AND R. MAC NALLY. 2022. Package ‘hier.part’, version 1.0-6. https://cran.r-project.org/web/packages/hier.part/hier.part.pdf. Accessed 21 October 2022.

WHITAKER, J. O. 2004. Prey selection in a temperate zone insectivorous bat community. Journal of Mammalogy 85:460-469.

WICKRAMASINGHE, L. P., ET AL. 2004. Abundance and species richness of nocturnal insects on organic and conventional farms: effects of agricultural intensification on bat foraging. Conservation Biology 18:1283-1292.

WILLIAMS-GUILLÉN, K., AND I. PERFECTO. 2011. Ensemble composition and activity levels of insectivorous bats in response to management intensification in coffee agroforestry systems. Plos One 6:e16502.

ZAMORA-GUTIÉRREZ, V., ET AL. 2016. Acoustic identification of Mexican bats based on taxonomic and ecological constraints on call design. Methods in Ecology and Evolution 7:1082-1091.

Published

2023-02-14

Issue

Section

Articles