3D acoustic tracking; chiroptera; competition; facilitation; foraging flight behavior; interindividual interactions; Ecology, Evolution, Behavior and Systematics; Animal Science and Zoology
Abstract :
[en] Foraging is a key function in the animal kingdom. Foraging in groups drives food patch discovery through social information transfer that maximizes an individual's foraging success through either cooperation or competition in response to congener presence. Understanding how congener presence affects the foraging strategy is especially challenging as it requires close monitoring of animal movements, foraging success, and competitive interactions. The consequences of congener presence on the foraging flight strategy of bats, a highly social taxon with strong behavioral plasticity in response to resource ephemerality, remain little tested. Through a 3D acoustic tracking of individual echolocation calls, we assessed to which extent foraging flight strategy of bats varied in response to conspecific and heterospecific presence. We found that flight speed, the main lever for adjusting energy balance during foraging (ie slowing down to capture prey and speeding up to find new prey patches), is no longer used in the presence of intra-guild heterospecifics. Also, the overall foraging level increased regardless of co-occurring species, through a facilitation and/or a higher prey availability. The study shows that bats integrate species identity in making decisions about their foraging flight strategy, with a stronger tolerance toward conspecifics with which social relations are most important, eg because they share the same roost. This might have important implications in understanding the consequences of interactions, especially in relation to anthropogenic pressures that rearrange bat communities and their prey in time and space, which could exacerbate natural competition.
Disciplines :
Zoology
Author, co-author :
Delmotte, Montaine; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne Université, Paris, France ; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Station de Biologie Marine, Concarneau, France ; INRAE, UR1115, Plantes et Systèmes de Culture Horticoles, Domaine Saint-Paul - Site Agroparc, Avignon, France
Baudouin, Alice; Ligue Pour la Protection des Oiseaux Auvergne-Rhône-Alpes, Chabeuil, France
Pessato, Anaïs; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne Université, Paris, France ; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Station de Biologie Marine, Concarneau, France
Ravache, Andréas; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne Université, Paris, France ; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Station de Biologie Marine, Concarneau, France
Thibault, Martin; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne Université, Paris, France ; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Station de Biologie Marine, Concarneau, France ; UMR ENTROPIE (UR-IRD-IFREMER-CNRS-UNC), Labex-CORAIL, France
Verniest, Fabien; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne Université, Paris, France ; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Station de Biologie Marine, Concarneau, France
BARRE, Kevin ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Engineering (DoE) ; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne Université, Paris, France ; Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum National d'Histoire Naturelle, Station de Biologie Marine, Concarneau, France
External co-authors :
yes
Language :
English
Title :
Foraging flight strategy varies with species identity of co-occurring individuals in bats
Office Français de la Biodiversité Compagnie Nationale du Rhône Agence de la Transition Écologique Muséum National d’Histoire Naturelle Actions Thématiques du Muséum Ligue pour la Protection des Oiseaux
Funding text :
This work was supported by the Office Francais de la Biodiversite (OFB), the Compagnie Nationale du Rhone (CNR), and the Agence de la Transition Ecologique (ADEME). The equipment was funded by the Museum National d'Histoire Naturelle (MNHN) through the Actions Thematiques du Museum (ATM) and the Ligue pour la Protection des Oiseaux (LPO) Auvergne-Rhone-Alpes.This work was supported by the Office Fran\u00E7ais de la Biodiversit\u00E9 (OFB), the Compagnie Nationale du Rh\u00F4ne (CNR), and the Agence de la Transition \u00C9cologique (ADEME). The equipment was funded by the Mus\u00E9um National d\u2019Histoire Naturelle (MNHN) through the Actions Th\u00E9matiques du Mus\u00E9um (ATM) and the Ligue pour la Protection des Oiseaux (LPO) Auvergne\u2013Rh\u00F4ne\u2013Alpes.
Allen JA et al. 2024. Evidence of sociality and group foraging in Antarctic minke whales (Balaenoptera bonaerensis). Behav Ecol Sociobiol. 78: 61. 10.1007/s00265-024-03481-4.
Amarasekare P. 2002. Interference competition and species coexistence. Proc Biol Sci. 269: 2541-2550. 10.1098/rspb.2002.2181.
Amichai E, Blumrosen G, Yovel Y. 2015. Calling louder and longer: how bats use biosonar under severe acoustic interference from other bats. Proc Biol Sci. 282: 20152064. 10.1098/rspb.2015.2064.
Barré K. 2025. Data from: foraging flight strategy varies with species identity of co-occurring individuals in bats [data set]. Dryad. 10.5061/dryad.6q573n6b0.
Barré K et al. 2021a. Bats seek refuge in cluttered environment when exposed to white and red lights at night. Mov Ecol. 9: 3. 10.1186/s40462-020-00238-2.
Barré K et al. 2021b. Artificial light may change flight patterns of bats near bridges along urban waterways. Anim Conserv. 24: 259-267. 10.1111/acv.12635.
Barré K, Baudouin A, Froidevaux JSP, Chartendrault V, Kerbiriou C. 2024. Insectivorous bats alter their flight and feeding behaviour at ground-mounted solar farms. J Appl Ecol. 61: 328-339. 10.1111/1365-2664.14555.
Bas Y, Bas D, Julien J-F. 2017. Tadarida: a toolbox for animal detection on acoustic recordings. J Open Res Softw. 5: 6. 10.5334/jors.154.
Bas Y, Kerbiriou C, Julien JF, Roemer C. 2023. Maps predicted activity. Team-Chiro. [accessed 2024 Aug 01]. https://croemer3.wixsite.com/teamchiro/maps-predicted-activity?lang=fr.
Beauchamp G, Fernández-Juricic E. 2005. The group-size paradox: effects of learning and patch departure rules. Behav Ecol. 16: 352-357. 10.1093/beheco/arh169.
Bell G. 2010. Fluctuating selection: the perpetual renewal of adaptation in variable environments. Philos Trans R Soc B Biol Sci. 365: 87-97. 10.1098/rstb.2009.0150.
Britton ARC, Jones G. 1999. Echolocation behaviour and prey-capture success in foraging bats: laboratory and field experiments on Myotis daubentonii. J Exp Biol. 202: 1793-1801. 10.1242/jeb.202.13.1793.
Buckley NJ. 1997. Experimental tests of the information-center hypothesis with black vultures (Coragypsatratus) and turkey vultures (Cathartesaura). Behav Ecol Sociobiol. 41: 267-279. 10.1007/s002650050388.
Caraco T, Giraldea LA. 1991. Social foraging: producing and scrounging in a stochastic environment. J Theor Biol. 153: 559-583. 10.1016/S0022-5193(05)80156-0.
Charnov EL. 1976. Optimal foraging, the marginal value theorem. Theor Popul Biol. 9: 129-136. 10.1016/0040-5809(76)90040-X.
Chaverri G, Ancillotto L, Russo D. 2018. Social communication in bats. Biol Rev Camb Philos Soc. 93: 1938-1954. 10.1111/brv.12427.
Chiu C, Reddy PV, Xian W, Krishnaprasad PS, Moss CF. 2010. Effects of competitive prey capture on flight behavior and sonar beam pattern in paired big brown bats, Eptesicus fuscus. J Exp Biol. 213: 3348-3356. 10.1242/jeb.044818.
Clark CW, Mangel M. 1986. The evolutionary advantages of group foraging. Theor Popul Biol. 30: 45-75. 10.1016/0040-5809(86)90024-9.
Connell JH. 1983. On the prevalence and relative importance of interspecific competition: evidence from field experiments. Am Nat. 122: 661-696. 10.1086/284165.
Corcoran AJ. 2022. Sing or jam? Density-dependent food competition strategies in Mexican free-tailed bats (Tadarida brasiliensis). Front Ecol Evol. 10: 877579. 10.3389/fevo.2022.877579.
Cvikel N et al. 2015. Bats aggregate to improve prey search but might be impaired when their density becomes too high. Curr Biol. 25: 206-211. 10.1016/j.cub.2014.11.010.
Dall SRX, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW. 2005. Information and its use by animals in evolutionary ecology. Trends Ecol Evol. 20: 187-193. 10.1016/j.tree.2005.01.010.
Danchin É, Giraldeau L-A, Valone TJ, Wagner RH. 2004. Public information: from nosy neighbors to cultural evolution. Science. 305: 487-491. 10.1126/science.1098254.
Dechmann DKN et al. 2009. Experimental evidence for group hunting via eavesdropping in echolocating bats. Proc Biol Sci. 276: 2721-2728. 10.1098/rspb.2009.0473.
Denzinger A, Schnitzler H. 2013. Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Front Physiol. 4: 164. 10.3389/fphys.2013.00164.
Deygout C, Gault A, Duriez O, Sarrazin F, Bessa-Gomes C. 2010. Impact of food predictability on social facilitation by foraging scavengers. Behav Ecol. 21: 1131-1139. 10.1093/beheco/arq120.
Egert-Berg K et al. 2018. Resource ephemerality drives social foraging in bats. Curr Biol. 28: 3667-3673.e5. 10.1016/j.cub.2018.09.064.
Fenton MB. 2003. Eavesdropping on the echolocation and social calls of bats. Mamm Rev. 33: 193-204. 10.1046/j.1365-2907.2003.00019.x.
Flemming SP, Smith PC, Seymour NR, Bancroft RP. 1992. Ospreys use local enhancement and flock foraging to locate prey. Auk. 109: 649-654. 10.1093/auk/109.3.649.
Fraser EE, Silvis A, Brigham RM, Czenze ZJ. 2020. Bat echolocation research: a handbook for planning and conducting acoustic studies. 2nd ed. Bat Conservation International.
Gager Y. 2019. Information transfer about food as a reason for sociality in bats. Mamm Rev. 49: 113-120. 10.1111/mam.12146.
Gillam EH. 2007. Eavesdropping by bats on the feeding buzzes of conspecifics. Can J Zool. 85: 795-801. 10.1139/Z07-060.
Giraldeau L-A, Caraco T. 2000. Social foraging theory. Princeton University Press.
Griffin DR. 1958. Listening in the dark: the acoustic orientation of bats and men. Yale University Press.
Griffin DR, Webster FA, Michael CR. 1960. The echolocation of flying insects by bats. Anim Behav. 8: 141-154. 10.1016/0003-3472(60)90022-1.
Grodzinski U, Spiegel O, Korine C, Holderied MW. 2009. Context-dependent flight speed: evidence for energetically optimal flight speed in the bat Pipistrellus kuhlii? J Anim Ecol. 78: 540-548. 10.1111/j.1365-2656.2009.01526.x.
Hartig F. 2022. DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6.1. [accessed 2024 Aug 01]. https://github.com/florianhartig/dharma.
Hillen J, Kiefer A, Veith M. 2009. Foraging site fidelity shapes the spatial organisation of a population of female western barbastelle bats. Biol Conserv. 142: 817-823. 10.1016/j.biocon.2008.12.017.
Holderied M, Jones G. 2009. Flight dynamics. In: Kunz TH, Parsons S, editors. Ecological and behavioral methods for the study of bats. Johns Hopkins University Press. p. 459-475.
Ing RK et al. 2016. Echolocation calls and flight behaviour of the elusive pied butterfly bat (Glauconycteris superba), and new data on its morphology and ecology. Acta Chiropt. 18: 477-488. 10.3161/15081109ACC2016.18.2.014.
Jägerbrand AK, Spoelstra K. 2023. Effects of anthropogenic light on species and ecosystems. Science. 380: 1125-1130. 10.1126/science.adg3173.
Jiang G et al. 2015. Intra- and interspecific interactions and environmental factors determine spatial-temporal species assemblages of rodents in arid grasslands. Landsc Ecol. 30: 1643-1655. 10.1007/s10980-014-0039-6.
Jones G, Rayner JMV. 1988. Flight performance, foraging tactics and echolocation in free-living Daubenton's bats Myotis daubentoni (Chiroptera: Vespertilionidae). J Zool. 215: 113-132. 10.1111/j.1469-7998.1988.tb04888.x.
Jones G, Siemers BM. 2011. The communicative potential of bat echolocation pulses. J Comp Physiol A. 197: 447-457. 10.1007/s00359-010-0565-x.
Kelt DA et al. 2019. Advances in population ecology and species interactions in mammals. J Mammal. 100: 965-1007. 10.1093/jmammal/gyz017.
Koblitz JC. 2018. Arrayvolution: using microphone arrays to study bats in the field. Can J Zool. 96: 933-938. 10.1139/cjz-2017-0187.
Krivoruchko K et al. 2024. A social foraging trade-off in echolocating bats reveals that they benefit from some conspecifics but are impaired when many are around. Proc Natl Acad Sci U S A. 121: e2321724121. 10.1073/pnas.2321724121.
Lenth R., Singmann H., Love J., Buerkner P., & Herve M. (2018). Package "Emmeans". R package version 4.0-3. [accessed 2024 Aug 01]. http://cran.r-project.org/package=emmeans.
Lewanzik D, Sundaramurthy AK, Goerlitz HR. 2019. Insectivorous bats integrate social information about species identity, conspecific activity and prey abundance to estimate cost-benefit ratio of interactions. J Anim Ecol. 88: 1462-1473. 10.1111/1365-2656.12989.
Mariton L, Le Viol I, Bas Y, Kerbiriou C. 2023. Characterising diel activity patterns to design conservation measures: case study of European bat species. Biol Conserv. 277: 109852. 10.1016/j.biocon.2022.109852.
McGuire LP, Boyles JG. 2024. Chapter 10 - energetics of foraging bats. In: Russo D, Fenton B, editors. A natural history of bat foraging. Academic Press. p. 173-198.
Mizuguchi Y, Fujioka E, Heim O, Fukui D, Hiryu S. 2022. Discriminating predation attempt outcomes during natural foraging using the post-buzz pause in the Japanese large-footed bat, Myotis macrodactylus. J Exp Biol. 225: jeb243402. 10.1242/jeb.243402.
Monier SA. 2024. Social interactions and information use by foraging seabirds. Biol Rev Camb Philos Soc. 99: 1717-1735. 10.1111/brv.13089.
O'Brien WJ, Browman HI, Evans BI. 1990. Search strategies of foraging animals. Am Sci. 78: 152-160.
Racey PA, Swift SM. 1985. Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. I. Foraging behaviour. J Anim Ecol. 54: 205-215. 10.2307/4631.
R Core Team. 2024. R: a language and environment for statistical computing. R Foundation for Statistical Computing. [accessed 2024 Aug 01]. https://www.R-project.org/.
Ridley AR, Wiley EM, Thompson AM. 2013. The ecological benefits of interceptive eavesdropping. Funct Ecol. 28: 197-205. 10.1111/1365-2435.12153.
Roemer C et al. 2021. An automatic classifier of bat sonotypes around the world. Methods Ecol Evol. 12: 2432-2444. 10.1111/2041-210X.13721.
Ryer CH, Olla BL. 1995. Influences of food distribution on fish foraging behaviour. Anim Behav. 49: 411-418. 10.1006/anbe.1995.0054.
Salinas-Ramos VB, Ancillotto L, Bosso L, Sánchez-Cordero V, Russo D. 2020. Interspecific competition in bats: state of knowledge and research challenges. Mamm Rev. 50: 68-81. 10.1111/mam.12180.
Schnitzler H-U, Moss CF, Denzinger A. 2003. From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol. 18: 386-394. 10.1016/S0169-5347(03)00185-X.
Silk JB. 2007. The adaptive value of sociality in mammalian groups. Philos Trans R Soc B Biol Sci. 362: 539-559. 10.1098/rstb.2006.1994.
Smith JE, Holekamp KE. 2023. Hunting success in the spotted hyena: morphological adaptations and behavioral strategies. In: Srinivasan M, Würsig B, editors. Social strategies of carnivorous mammalian predators: hunting and surviving as families. Springer. p. 139-175.
Snijders L, Kurvers RH, Krause S, Ramnarine IW, Krause J. 2018. Individual-and population-level drivers of consistent foraging success across environments. Nat Ecol Evol. 2: 1610-1618. 10.1038/s41559-018-0658-4.
Stidsholt L et al. 2023. Echolocating bats prefer a high risk-high gain foraging strategy to increase prey profitability. eLife. 12: e84190. 10.7554/eLife.84190.
Stilz W-P, Schnitzler H-U. 2012. Estimation of the acoustic range of bat echolocation for extended targets. J Acoust Soc Am. 132: 1765-1775. 10.1121/1.4733537.
Stone E et al. 2015. Managing conflict between bats and humans: the response of soprano pipistrelles (Pipistrellus pygmaeus) to exclusion from roosts in houses. PLoS One. 10: e0131825. 10.1371/journal.pone.0131825.
Troxell SA, Holderied MW, Pētersons G, Voigt CC. 2019. Nathusius' bats optimize long-distance migration by flying at maximum range speed. J Exp Biol. 222: jeb176396. 10.1242/jeb.176396.
Vaughan N. 1997. The diets of British bats (Chiroptera). Mamm Rev. 27: 77-94. 10.1111/j.1365-2907.1997.tb00373.x.