Abstract
Rice fields may represent an important habitat for biodiversity conservation. Unfortunately, rice farming intensification reduced the value of rice crops as a surrogate habitat for many species. Currently, major threats for wildlife in rice fields derive from cultivation techniques in dry soils. In this paper, we aim to describe the effect of water management techniques in rice paddies on the flight and feeding activity of bats. We investigated the habitat use of 14 bat taxa in the rice paddies of northwest Italy and tested for a difference in the number of echolocation calls recorded in flooded vs non-flooded and organic vs conventional rice paddies. We observed no significant differences among flooded and non-flooded fields in conventional farms, whereas in organic farms bat activity was strongly affected by water management techniques with a large decrease in passes and feeding buzzes when rice paddies were dry. A dry seeding-based rice cultivation may nullify the positive effects of environmentally friendly management practices that are often able to restore suitable foraging sites for bats. In addition, the negative effects of dry rice paddies appeared to be more pronounced shortly after bats emerged from hibernation, when energy demand for body mass growth and offspring gestation is higher. The recent spread of dry seeding may therefore threaten the suitability of rice fields as a foraging habitat for bats. As already observed for other taxonomic groups, changes in water management strategies may compromise bat conservation in rice paddies, requiring the adoption of alternative rice cultivation practices.
Similar content being viewed by others
References
Altringham JD (2011) Bats: from evolution to conservation. Oxford University Press, Oxford
Appel G, López-Baucells A, Magnusson WE, Bobrowiec PED (2016) Aerial insectivorous bat activity in relation to moonlight intensity. Mamm Biol-Zeitschrift für Säugetierkd. 85:37–46. https://doi.org/10.1016/j.mambio.2016.11.005
Azam C, Kerbiriou C, Vernet A, Julien JF, Bas Y, Plichard L, Maratra J, Le Viol I (2015) Is part-night lighting an effective measure to limit the impacts of artificial lighting on bats? Glob Chang Biol 21:4333–4341. https://doi.org/10.1111/gcb.13036
Balsari P, Bocchi S, Tano F (1989) First test results of rice sowing on dry soil by pneumatic fertilizer spreader. In: Dodd V, Grace PM (ed) Proceedings of the Eleventh international congress on agricultural engineering. Dublin, Ireland, pp 1673–1679
Bambaradeniya CNB, Edirisinghe JP, De Silva DN, Gunatilleke CVS, Ranawana KB, Wijekoon S (2004) Biodiversity associated with an irrigated rice agro-ecosystem in Sri Lanka. Biodivers Conserv 13(9):1715–1753. https://doi.org/10.1023/B:BIOC.0000029331.92656.de
Barataud M (2015) Acoustic Ecology of European Bats. Species Identification, study of Their Habitats and Foraging Behaviour. Biotope Édition, Mèze, Muséum National d’Histoire Naturelle, Paris
Bogliani G (2008) Habitat risicolo e fauna. In: Ferrero A (ed) Il riso. Bayer Crop Science, Bologna, pp 236–253
Brooks SPB, Gelman AG (1998) General methods for monitoring convergence of iterative simulations. J Comput Graph Stat 7:434–455. https://doi.org/10.2307/1390675
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Cardarelli E, Bogliani G (2014) Effects of grass management intensity on ground beetle assemblages in rice field banks. Agric Ecosyst Environ 195:120–126. https://doi.org/10.1016/j.agee.2014.05.004
Czech HE, Parsons KC (2002) Agricultural wetlands and waterbirds: a review. Waterbirds 25:56–65
De Oliveira LQ, Marciente R, Magnusson WE, Bobrowiec PED (2015) Activity of the insectivorous bat Pteronotus parnellii relative to insect resources and vegetation structure. J Mammal 96:1036–1044. https://doi.org/10.1093/jmammal/gyv108
Duré MI, Kehr AI, Schaefer EF, Marangoni F (2008) Diversity of amphibians in rice fields from Northeastern Argentina. Interciencia 33(7):523–527
Ente Nazionale Risi (2016) http://www.enterisi.it/servizi/seriestoriche/superfici_fase01.aspx. Accessed 24 Jan 2017
Erickson JL, West SD (2002) The influence of regional climate and nightly weather conditions on activity patterns of insectivorous bats. Acta Chiropter 4(1):17–24
Erkert HG (1982) Ecological aspects of bat activity rhythms. In: Kunz TH (ed) Ecology of Bats. Plenum Publishing Corporation, New York, pp 201–242
Farooq M, Siddique KH, Rehman H, Aziz T, Lee DJ, Wahid A (2011) Rice direct seeding: experiences, challenges and opportunities. Soil Tillage Res 111(2):87–98. https://doi.org/10.1016/j.still.2010.10.008
Fasola M, Cardarelli E (2015) Long-term changes in the food resources of a guild of breeding Ardeinae (Aves) in Italy. Ital J Zool 82(2):238–250. https://doi.org/10.1080/11250003.2014.966256
Fasola M, Ruíz X (1996) The value of rice fields as substitutes for natural wetlands for waterbirds in the Mediterranean region. Colon Waterbirds 19:22–128
Fasola M, Cardarelli E, Pellitteri-Rosa D, Ranghetti L (2014) The recent decline of heron populations in Italy and the changes in rice cultivation practice. In: 25th International ornithological congress, Ornithological Science, Supplement, The Ornithological Society of Japan, Campos do Jordão, SP, Brazil, vol. 13
Ferrari IA, de Marchi P, Menozzi F, Minzoni F, Piccoli F (1984) Heleoplankton seasonal succession in an experimental ricefield in Northern Italy. Internationale Vereinigung fur Theoretische und An gewandte Limnologie 22:1711–1716
Flaquer C, Torre I, Ruiz-Jarillo R (2006) The value of bat-boxes in the conservation of Pipistrellus pygmaeus in wetland rice paddies. Biol Conserv 128(2):223–230
Flaquer C, Puig-Montserrat X, Goiti U, Vidal F, Curcó A, Russo D (2009) Habitat selection in Nathusius’ pipistrelle (Pipistrellus nathusii): the importance of wetlands. Acta Chiropter 11(1):149–155. https://doi.org/10.3161/150811009X465767
Fujioka M, Lane SJ (1997) The impact of changing irrigation practices in rice fields on frog populations of the Kanto Plain, central Japan. Ecol Res 12(1):101–108. https://doi.org/10.1007/BF02523615
Giuliano D, Bogliani G (2019) Odonata in rice agroecosystems: testing good practices for their conservation. Agric Ecosyst Environ 275:65–72. https://doi.org/10.1016/j.agee.2019.01.009
Giuliano D, Cardarelli E, Bogliani G (2018) Grass management intensity affects butterfly and orthopteran diversity on rice field banks. Agric Ecosyst Environ 267:147–155. https://doi.org/10.1016/j.agee.2018.08.019
Griffin DR, Webster FA, Michael CR (1960) The echolocation of flying insects by bats. Anim Behav 8:141–154
Heim O, Schröder A, Eccard J, Jung K, Voigt CC (2016) Seasonal activity patterns of European bats above intensively used farmland. Agric Ecosyst Environ 233:130–139. https://doi.org/10.1016/j.agee.2016.09.002
Hutson AM, Mickleburgh SP, Racey PA(2001) Global status survey and conservation action plan: microchiropteran bats. World Conservation Union, Gland, Switzerland, and Cambridge, United Kingdom
Kadoya T, Suda SI, Washitani I (2009) Dragonfly crisis in Japan: a likely consequence of recent agricultural habitat degradation. Biol Conserv 142(9):1899–1905. https://doi.org/10.1016/j.biocon.2009.02.033
Katayama N, Baba YG, Kusumoto Y, Tanaka K (2015) A review of post-war changes in rice farming and biodiversity in Japan. Agric Syst 132:73–84. https://doi.org/10.1016/j.agsy.2014.09.001
Kemp J, López-Baucells A, Rocha R, Wangensteen OS, Andriatafika Z, Nair A, Cabeza M (2019) Bats as potential suppressors of multiple agricultural pests: a case study from Madagascar. Agric Ecosyst Environ 269:88–96
Kery M, Schaub M (2012) Bayesian population analysis using WinBUGS: a hierarchical perspective. Academic Prress, Waltham
Kidera N, Kadoya T, Yamano H, Takamura N, Ogano D, Wakabayashi T, Takezawa M, Hasegawa M (2018) Hydrological effects of paddy improvement and abandonment on amphibian populations; long-term trends of the Japanese brown frog, Rana japonica. Biol Conserv 219:96–104. https://doi.org/10.1016/j.biocon.2018.01.007
Korine C, Adams R, Russo D, Fisher-Phelps M, Jacobs D (2016) Bats and water: anthropogenic alterations threaten global bat populations. In: Kingston T, Voigt CC (eds) Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer, Berlin, pp 215–241
Lawler SP (2001) Rice fields as temporary wetlands: a review. Israel J Zool 47:513–528
Lesiński G, Durka A, Rembiałkowska E (2013) Flight activity of serotine Eptesicus serotinus on organic and conventional farms in central Poland. Zool Ecol 23:93–96. https://doi.org/10.1080/21658005.2013.805500
Luo Y, Fu H, Traore S (2014) Biodiversity conservation in rice paddies in China: toward ecological sustainability. Sustainability 6(9):6107–6124. https://doi.org/10.3390/su6096107
Lupi D, Rocco A, Rossaro B (2013) Benthic macroinvertebrates in Italian rice fields. J Limnol 72(1):184–200. https://doi.org/10.4081/jlimnol.2013.e15
Mesléard F, Garnero S, Beck N, Rosecchi É (2005) Uselessness and indirect negative effects of an insecticide on rice field invertebrates. C R Biol 328(10–11):955–962. https://doi.org/10.1016/j.crvi.2005.09.003
Michaelsen TC (2016) Spatial and temporal distribution of bats (Chiroptera) in bright summer nights. Anim Biol J 66(1):65–80
Middleton N, Froud A, French K (2014) Social calls of the bats of Britain and Ireland. Pelagic Publishing Ltd, Pelagic
Müller J, Mehr M, Bässler C, Fenton MB, Hothorn T, Pretzsch H, Klemmt HJ, Brandl R (2012) Aggregative response in bats: prey abundance versus habitat. Oecologia 169:673–684. https://doi.org/10.1007/s00442-011-2247-y
Natuhara Y (2013) Ecosystem services by paddy fields as substitutes of natural wetlands in Japan. Ecol Eng 56:97–106. https://doi.org/10.1016/j.ecoleng.2012.04.026
Pfalzer G, Kusch J (2003) Structure and variability of bat social calls: implications for specificity and individual recognition. J Zool 261:21–33. https://doi.org/10.1017/S0952836903003935
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York
Puig-Montserrat X, Torre I, Lopez-Baucells A, Guerrieri E, Monti MM, Ràfols-Garcia R, Ferrer X, Gisbert D, Flaquer C (2015) Pest control service provided by bats in Mediterranean rice paddies: linking agroecosystems structure to ecological functions. Mamm Biol 80:237–245. https://doi.org/10.1016/j.mambio.2015.03.008
Ranghetti L, Cardarelli E, Boschetti M, Busetto L, Fasola M (2018) Assessment of water management changes in the Italian Rice Paddies from 2000 to 2016 using satellite data: a contribution to agro-ecological studies. Remote Sens 10(3):416
Riservato E, Fabbri R, Festi A, Grieco C, Hardersen S, Landi F, Utzeri C, Rondinini C, Battistoni A, Teofili C (2014) Lista Rossa IUCN delle libellule Italiane. Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Roma
Roemer C, Disca T, Coulon A, Bas Y (2017) Bat flight height monitored from wind masts predicts mortality risk at wind farms. Biol Conserv 215:116–122
Rossi O, Moroni A, Baroni P, Caravello P (1974) Annual evolution of the zooplankton diversity in twelve italian rice fields. Boll Zool 41:3–10
Rughetti M, Toffoli R (2014) Sex-specific seasonal change in body mass in two species of vespertilionid bats. Acta Chiropterol 16(1):149–155
Russo D, Jones G (1999) The social calls of Kuhl’s pipistrelles Pipistrellus kuhlii (Kuhl, 1819): structure and variation (Chiroptera: Vespertilionidae). J Zool 249:476–481. https://doi.org/10.1111/j.1469-7998.1999.tb01219.x
Russo D, Jones G (2002) Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy by analysis of time-expanded recordings of echolocation calls. J Zool 258:91–103. https://doi.org/10.1017/S0952836902001231
Russo D, Jones G (2003) Use of foraging habitats by bats in a Mediterranean area determined by acoustic surveys: conservation implications. Ecography (Cop.) 26:197–209. https://doi.org/10.1034/j.1600-0587.2003.03422.x
Russo D, Voigt CC (2016) The use of automated identification of bat echolocation calls in acoustic monitoring: a cautionary note for a sound analysis. Ecol Indic 66:598–602. https://doi.org/10.1016/j.ecolind.2016.02.036
Rydell J, Nyman S, Eklöf J, Jones G, Russo D (2017) Testing the performances of automated identification of bat echolocation calls: a request for prudence. Ecol Indic 78:416–420. https://doi.org/10.1016/j.ecolind.2017.03.023
Salvarina I (2016) Bats and aquatic habitats: a review of habitat use and anthropogenic impacts. Mamm Rev 46:131–143. https://doi.org/10.1111/mam.12059
SINAB (2015) BIO in Cifre 2015. Ministero delle politiche agricole, alimentari e forestali. http://www.sinab.it/sites/default/files/share/Bio%20in%20Cifre%202015.pdf. Accessed 29 June 2019
Stenert C, de Mello ÍCMF, Pires MM, Knauth DS, Katayama N, Maltchik L (2018) Responses of macroinvertebrate communities to pesticide application in irrigated rice fields. Environ Monit Assess 190:74. https://doi.org/10.1007/s10661-017-6425-1
Subrero E, Sforzini S, Viarengo A, Cucco M (2018) Exposure to anti-mosquito insecticides utilized in rice fields affects survival of two non-target species, Ischnura elegans and Daphnia magna. Paddy Water Environ, 17(1):1–11. https://doi.org/10.1007/s10333-018-0678-3
R Core Team (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 23 June 2019
Toffoli R (2016) The importance of linear landscape elements for bats in a Farmland area: the influence of height on activity. J Landsc Ecol 9:49–62. https://doi.org/10.1515/jlecol-2016-0004
Toffoli R, Rughetti M (2017) Bat activity in rice paddies: organic and conventional farms compared to unmanaged habitat. Agric Ecosyst Environ 249(123):129. https://doi.org/10.1016/j.agee.2017.08.022
Walsh A, Harris S (1996) Foraging habitat preferences of vespertilionid bats in Britain. J Appl Ecol 33:519–529
Washitani I (2007) Restoration of biologically-diverse floodplain wetlands including paddy fields. Glob J Environ Res 11:135–140
Wickramasinghe LP, Harris S, Jones G, Vaughan Jennings N (2003) Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. J Appl Ecol 40:984–993
Wickramasinghe LP, Harris S, Jones G, Vaughan Jennings N (2004) Abundance and species richness of nocturnal insects on organic and conventional farms: effects of agricultural intensification on bat foraging. Conserv Biol 18:1283–1292
Acknowledgements
The research was partially funded by ISPRA (Istituto Superiore per la Protezione e la Ricerca Ambientale, Italy) in the framework of the project “Testing measures for the sustainable use of pesticides according to guidelines provided in PAN” (National Action Plan for the sustainable use of pesticides-The Ministry of the Environment and Protection of Land and Sea of Italy). We thank D. Giuliano for insightful remarks on previous draft of this paper and two anonymous reviewers for their comments on this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Toffoli, R., Rughetti, M. Effect of water management on bat activity in rice paddies. Paddy Water Environ 18, 687–695 (2020). https://doi.org/10.1007/s10333-020-00811-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10333-020-00811-w