Abstract
The diet of Rhinolophus euryale was studied in southeastern Slovakia by an analysis of faeces collected from netted bats. Prey availability was studied using light traps, counting flying insects on the transect, and sweeping the vegetation. The diet composition was dominated by Lepidoptera, especially in July and September, which corresponds with most diet analyses reporting the species as a Lepidopteran specialist. Nonflying arthropods were almost absent from the diet, suggesting that the species obtains most of its food mainly by aerial hawking. The spring diet showed unusually high volumes of Diptera; this differed significantly from the evidence from its core distribution area in the Mediterranean. This suggests a higher flexibility of the trophic niche in the marginal parts of the species range. Our results suggest sex differences in diet. Possible conservation measures for these marginal populations should consider the protection of diverse mosaic landscapes, including urbanised patches. Such areas with long, warm interfaces of open and bushy and/or forest habitats have high moth flying activity, and riparian patches provide dipteran prey in spring when moths are scarce. The prediction of the prosperity of the studied northernmost populations of R. euryale during the ongoing climate change is ambiguous since various conceivable scenarios could work: (i) good prosperity of the population thanks to a warmer climate, higher production and higher flying activity of prey, or (ii) a worse situation due to unevenly distributed precipitation and higher evaporation, which may negatively affect wet habitats providing the important spring diet of tipulid dipterans.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmim M, Moali A (2013) The diet of four species of horseshoe bat (Chiroptera: Rhinolophidae) in a mountainous region of Algeria: evidence for gleaning. Hystrix 24:174–176. https://doi.org/10.4404/hystrix-24.2-8728
Aizpurua O, Budinski I, Georgiakakis P et al (2017) Agriculture shapes the trophic niche of a bat preying on multiple pest arthropods across Europe: evidence from DNA metabarcoding. Mol Ecol 27:815–825. https://doi.org/10.1111/mec.14474
Aldasoro M, Garin I, Vallejo N et al (2019) Gaining ecological insight on dietary allocation among horseshoe bats through molecular primer combination. PLoS One 14:e0220081. https://doi.org/10.1371/journal.pone.0220081
Andreas M, Reiter A, Benda P (2012) Prey selection and seasonal diet changes in the western barbastelle bat (Barbastella barbastellus). Acta Chiropt 14:81–92. https://doi.org/10.3161/150811012X654295
Andreas M, Reiter A, Benda P (2012) Dietary composition, resource partitioning and trophic niche overlap in three forest foliage-gleaning bats in Central Europe. Acta Chiropt 14:335–345. https://doi.org/10.3161/150811012X661657
Andreas M, Reiter A, Cepáková E, Uhrin M (2013) Body size as an important factor determining trophic niche partitioning in three syntopic rhinolophid bat species. Biologia 68:170–175. https://doi.org/10.2478/s11756-012-0139-1
Andriollo T, Gillet F, Michaux JR, Ruedi M (2019) The menu varies with metabarcoding practices: a case study with the bat Plecotus auritus. PLoS ONE 14:e0219135. https://doi.org/10.1371/journal.pone.0219135
Andriollo T, Michaux JR, Ruedi M (2021) Food for everyone: differential feeding habits of cryptic bat species inferred from DNA metabarcoding. Mol Ecol 30:4584–4600. https://doi.org/10.1111/mec.16073
Arrizabalaga-Escudero A, Garin I, García-Mudarra JL et al (2015) Trophic requirements beyond foraging habitats: the importance of prey source habitats in bat conservation. Biol Conserv 191:512–519. https://doi.org/10.1016/j.biocon.2015.07.043
Arrizabalaga-Escudero A, Clare EL, Salsamendi E et al (2018) Assessing niche partitioning of co-occurring sibling bat species by DNA metabarcoding. Mol Ecol 27:1273–1283. https://doi.org/10.1111/mec.14508
Bauerová Z (1982) Contribution to the trophic ecology of the grey long-eared bat, Plecotus austriacus. Folia Zool 31:113–122
Baroja U, Garin I, Vallejo N et al (2022) Molecular assays to reliably detect and quantify predation on a forest pest in bats faeces. Sci Rep 12:2243. https://doi.org/10.1038/s41598-022-06195-7
Bella P (2000) Slovensko. Sprístupnené jaskyne [Slovakia. The caves open to the public]. DTP štúdio Grafon, Liptovský Mikuláš, p 64
Benda P, Andreas M, Kock D et al (2006) Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 4. Bat fauna of Syria: distribution, systematics, ecology. Acta Soc Zool Bohem 70:1–329
Benda P, Lučan R, Obuch J et al (2010) Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 8. Bats of Jordan: fauna, ecology, echolocation, ectoparasites. Acta Soc Zool Bohem 74:185–353
Berthinussen A, Richardson OC, Altringham JD (2014) Bat conservation: global evidence for the effects of interventions. Pelagic Publishing, Exeter
Blaker H (2000) Confidence curves and improved exact confidence intervals for discrete distributions. Can J Stat 28:783–798. https://doi.org/10.2307/3315916
Boldogh S (2007) Kereknyergű patkósdenevér Rhinolophus euryale Blasius, 1853. [Mediterranean Horseshoe bat Rhinolophus euryale Blasius, 1853] In: Bihari Z, Csorba G, Heltai M (eds) Magyarországi emlőseinek atlasza. [The atlas of mammals of Hungary] Kossuth Kiadó, Budapest, pp 70–71
Borkin KM, Parsons S (2011) Sex-specific roost selection by bats in clearfell harvested plantation forest: improved knowledge advises management. Acta Chiropt 13:373–383. https://doi.org/10.3161/150811011X624848
Bowler DE, Heldbjerg H, Fox AD et al (2019) Long-term declines of European insectivorous bird populations and potential causes. Conserv Biol 33:1120–1130. https://doi.org/10.1111/cobi.13307
Cryan PM, Bogan MA, Altenbach JS (2000) Effect of elevation on distribution of female bats in the Black Hills, South Dakota. J Mammal 81:719–725. https://doi.org/10.1644/1545-1542(2000)081%3c0719:EOEODO%3e2.3.CO;2
Denno RF, Dingle H (1981) Insect life history patterns: habitat and geographic variation. Springer-Verlag, New York
Dietz C, Helversen O, Nill D (2009) Bats of Britain. Europe & Northwest Africa. A & C Black Publishers Ltd., London
Dietz M, Kalko EKV (2006) Seasonal changes in daily torpor patterns of free-ranging female and male Daubenton’s bats (Myotis daubentonii). J Comp Physiol B 176:223–231. https://doi.org/10.1007/s00360-005-0043-x
Elbrecht V, Leese F (2017) Validation and development of COI metabarcoding primers for freshwater macroinvertebrate bioassessment. Front Environ Sci 5:11. https://doi.org/10.3389/fenvs.2017.00011
Ferrari S, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Stat 31:799–815. https://doi.org/10.1080/0266476042000214501
Frey-Ehrenbold A, Bontadina F, Arlettaz R, Obrist MK (2013) Landscape connectivity, habitat structure and activity of bat guilds in farmland-dominated matrices. J Appl Ecol 50:252–261. https://doi.org/10.1111/1365-2664.12034
Frick WF, Baerwald EF, Pollock JF et al (2017) Fatalities at wind turbines may threaten population viability of a migratory bat. Biol Conserv 209:172–177. https://doi.org/10.1016/j.biocon.2017.02.023
Garin I, Goiti U (2020) Mediterranean horseshoe bat Rhinolophus euryale Blasius, 1853. In: Hackländer K, Zachos FE (eds) Handbook of the mammals of Europe. Springer International Publishing, Cham, pp 1–25
Goiti U, Aihartza JR, Almenar D et al (2006) Seasonal foraging by Rhinolophus euryale (Rhinolophidae) in an Atlantic rural landscape in northern Iberian Peninsula. Acta Chiropt 8:141–155. https://doi.org/10.3161/150811006777070776
Goiti U, Aihartza JR, Garin I (2004) Diet and prey selection in the Mediterranean horseshoe bat Rhinolophus euryale (Chiroptera, Rhinolophidae) during the pre-breeding season. Mammalia 68:397–402. https://doi.org/10.1515/mamm.2004.039
Goiti U, Aihartza JR, Garin I, Zabala J (2003) Influence of habitat on the foraging behaviour of the Mediterranean horseshoe bat, Rhinolophus euryale. Acta Chiropt 5:75–84. https://doi.org/10.3161/001.005.0106
Goiti U, Garin I, Almenar D et al (2008) Foraging by Mediterranean horsheshoe bat (Rhinolophus euryale) in relation to prey distribution and edge habitat. J Mammal 89:493–502. https://doi.org/10.1644/07-MAMM-A-054R2.1
Heath J (1965) A genuinely portable MV light trap. Entomol’s Rec J Var 77:236–238
Horáček I, Zima J (1979) Zur Frage der Synanthropie bei Hufeisennasen in der Tschechoslowakei. Nyctalus (NF) 1:139–141
Jones G (1990) Prey selection by the greater Horseshoe Bat (Rhinolophus ferrumequinum): optimal foraging by echolocation? J Anim Ecol 59:587–602
Juste J, Alcaldé J (2016) Rhinolophus euryale. The IUCN Red List of Threatened Species 2016: e.T19516A21971185. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T19516A21971185.en. Accessed 21 Dec 2022
Koselj K (2002) Diet and ecology of Mediterranean horseshoe bat (Rhinolophus euryale Blasius, 1853; Mammalia: Chiroptera) in south-eastern Slovenia. Graduation thesis. University of Ljubljana, Ljubljana, p 135
Kunz TH (1988) Methods of assessing the availability of prey to insectivorous bats. In: Kunz TH (ed) Ecological and behavioural methods for the study of bats. Smithsonian Institution Press, Washington, pp 191–210
Lapin M, Faško P, Melo M, Šťastný P, Tomlain J (2002) Klimatické oblasti (Climatic regions). In: Miklos L, Hrnčiarová T (eds) Atlas krajiny Slovenskej republiky (Landscape atlas of the Slovak Republic). MŽP SR, Bratislava, SAŽP Banská Bystrica, p 95
Mata VA, Amorim F, Corley MFV et al (2016) Female dietary bias towards large migratory moths in the European free-tailed bat (Tadarida teniotis). Biol Lett 12:20150988. https://doi.org/10.1098/rsbl.2015.0988
McAney CM, Shiel CB, Sullivan C, Fairley JS (1991) The analysis of bat droppings. The Mammal Society, London
McGeachie WJ (1989) The effects of moonlight illuminance, temperature and wind speed on light-trap catches of moths. Bull Entomol Res 79:185–192. https://doi.org/10.1017/S0007485300018162
Merritt RW, Lawson DL (1981) Adult emergence patterns and species distribution and abundance of Tipulidae in three woodland floodplains. Environ Entomol 10:915–921
Miková E, Varcholová K, Boldogh S, Uhrin M (2013) Winter diet analysis in Rhinolophus euryale (Chiroptera). Cent Eur J Biol 8:848–853. https://doi.org/10.2478/s11535-013-0199-9
Obrtel R, Holišová V (1974) Trophic niches of Apodemus flavicollis and Clethrionomys glareolus in a lowland forest. Acta Sc Nat Brno 8:1–37
O’Shea TJ, Cryan PM, Hayman DTS et al (2016) Multiple mortality events in bats: a global review: multiple mortality events in bats. Mammal Rev 46:175–190. https://doi.org/10.1111/mam.12064
Pavey CR (2020) Comparative echolocation and foraging ecology of horseshoe bats (Rhinolophidae) and Old World leaf-nosed bats (Hipposideridae). Aust J Zool 68:382–392. https://doi.org/10.1071/ZO20047
Pironon S, Papuga G, Villellas J et al (2017) Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biol Rev 92:1877–1909. https://doi.org/10.1111/brv.12313
R Core Team (2020) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Razgour O, Clare EL, Zeale MRK et al (2011) High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species. Ecol Evol 1:556–570
Rebelo H, Tarroso P, Jones G (2010) Predicted impact of climate change on European bats in relation to their biogeographic patterns. Glob Change Biol 16:561–576. https://doi.org/10.1111/j.1365-2486.2009.02021.x
Robinson RA, Sutherland WJ (2002) Post-war changes in arable farming and biodiversity in Great Britain. J Appl Ecol 39:157–176. https://doi.org/10.1046/j.1365-2664.2002.00695.x
Russo D, Ancillotto L (2015) Sensitivity of bats to urbanization: a review. Mamm Biol 80:205–212. https://doi.org/10.1016/j.mambio.2014.10.003
Salsamendi E, Garin I, Arostegui I et al (2012) What mechanism of niche segregation allows the coexistence of sympatric sibling rhinolophid bats? Front Zool 9:30. https://doi.org/10.1186/1742-9994-9-30
Scherer R (2018) PropCIs: various confidence interval methods for proportions. R package version 0.3–0. Version 0.3–0.URL https://CRAN.R-project.org/package=PropCIs. Accessed 20 Dec 2021
Seamark ECJ, Bogdanowicz W (2002) Feeding ecology of the common slit-faced bat (Nycteris thebaica) in KwaZulu-Natal, South Africa. Acta Chiropt 4:49–54. https://doi.org/10.3161/001.004.0106
Service MW (1973) Spatial and temporal distribution of aerial populations of woodland Tipulids (Diptera). J Anim Ecol 42:295–303
Shiel CB, McAney CM, Sullivan C, Fairley JS (1997) Identification of arthropod fragments in bat droppings. The Mammal Society, London
Siemers BM, Ivanova T (2004) Ground gleaning in horseshoe bats: comparative evidence from Rhinolophus blasii, R. euryale and R. mehelyi. Behav Ecol Sociobiol 56:464–471. https://doi.org/10.1007/s00265-004-0807-4
Simmons BI, Balmford A, Bladon AJ et al (2019) Worldwide insect declines: an important message, but interpret with caution. Ecol Evol 9:3678–3680. https://doi.org/10.1002/ece3.5153
Smithson M, Verkuilen J (2006) A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol Methods 11:54–71. https://doi.org/10.1037/1082-989X.11.1.54
Svitavská-Svobodová H, Andreas M, Krištůfek V et al (2015) The thousand-year history of the Slovak Karst inferred from pollen in bat guano inside the Domica Cave (Slovakia). Folia Geobot 50:49–61. https://doi.org/10.1007/s12224-015-9205-0
Thomas CD, Jones TH, Hartley SE (2019) “Insectageddon”: a call for more robust data and rigorous analyses. Glob Chang Biol 25:1891–1892. https://doi.org/10.1111/gcb.14608
Uhrin M, Boldogh S, Bücs S et al (2012) Revision of the occurrence of Rhinolophus euryale in the Carpathian region, Central Europe. Vespertilio 16:289–328
Uhrin M, Gahurová V, Andreas M et al (2021) Spatial activity and habitat use of a marginal population of the endangered Mediterranean horseshoe bat (Rhinolophus euryale). Mamm Res 66:499–508. https://doi.org/10.1007/s13364-021-00568-5
Vaughan N (1997) The diets of British bats (Chiroptera). Mammal Rev 27:77–94
Vogel G (2017) Where have all the insects gone? Science 356:576–579. https://doi.org/10.1126/science.356.6338.576
Whitaker JO Jr, Karatas A (2009) Food and feeding habits of some bats from Turkey. Acta Chiropter 11:393–403. https://doi.org/10.3161/150811009X485611
Whitaker JO Jr, McCracken GF, Siemers BM (2009) Food habits analysis of insectivorous bats. In: Kunz TH, Parsons S (eds) Ecological and behavioural methods for the study of bats. Johns Hopkins University Press, Baltimore, pp 567–592
Williams CB (1939) An analysis of four years captures of insects in a light trap. Part I. General survey; sex proportion; phenology and time of flight. Trans R Ent Soc Lond 89:79–132
Wray AK, Peery MZ, Jusino MA et al (2021) Predator preferences shape the diets of arthropodivorous bats more than quantitative local prey abundance. Mol Ecol 30:855–873. https://doi.org/10.1111/mec.15769
Yela JL, Holyoak M (1997) Effects of moonlight and meteorological factors on light and bait trap catches of noctuid moths (Lepidoptera: Noctuidae). Environ Entomol 26:1283–1290. https://doi.org/10.1093/ee/26.6.1283
Zar JH (2007) Biostatistical analysis, 4th edn. Prentice-Hall Inc., New Jersey
Žiak D, Urban P (2001) Red (Ecosozological) List of mammals (mammalia) of Slovakia. In: Baláž D, Marhold K, Urban P (eds) Red list of plants and animals of Slovakia. Ochr. Prír. 20 (Suppl.) ŠOP SR, Banská Bystrica, pp 154–156
Acknowledgements
This study was conducted under licence from the Ministry of Environment of the Slovak Republic (2598/03-5.1). Thanks for field support to the Abbey of Order of Canons Regular of Prémontré in Jasov, ing. J. Menda (Slovak Caves Administration), V. Gahurová and L. Žďárská (Charles University, Prague), D. Lőbbová (Slovak Bat Conservation Society, Vrchslatina), M. Ševčík (Constantine the Philosopher University, Nitra), M. Dobrý (P. J. Šafárik University, Košice), P. Bačkor (Otonycteris, Prostredná Môlča).
Funding
This study was financially supported by the Scientific Grant Agency VEGA (#1/0298/19), by the Ministry of Culture of the Czech Republic (# DKRVO 2019–2023/6.IX.c, 00023252), and the Ministry of Education of the Czech Republic (# CZ.02.1.01/0.0/0.0/16_019/0000803 financed by OP RDE).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by: Zuzanna Hałat
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Appendix
Appendix
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Andreas, M., Naďo, L., Bendová, B. et al. Trophic niche and diet composition of the northernmost population of the Mediterranean horseshoe bat (Rhinolophus euryale) with conservation implications. Mamm Res 68, 189–202 (2023). https://doi.org/10.1007/s13364-023-00674-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13364-023-00674-6