DOI QR코드

DOI QR Code

Dietary composition of two coexisting bat species, Myotis ikonnikovi and Plecotus ognevi, in the Mt. Jumbong forests, South Korea

  • Sungbae Joo (Ecological Observatory Team, National Institute of Ecology) ;
  • Injung An (Ecological Technology Research Team, National Institute of Ecology) ;
  • Sun-Sook Kim (Ecological Technology Research Team, National Institute of Ecology)
  • Received : 2023.08.25
  • Accepted : 2023.10.02
  • Published : 2023.12.31

Abstract

Background: Many insectivorous bats have flexible diets, and the difference in prey item consumption among species is one of the key mechanisms that allows for the avoidance of interspecies competition and promotes coexistence within a microhabitat. In Korea, of the 24 bat species that are known to be distributed, eight insectivorous bats use forest areas as both roosting and foraging sites. Here, we aimed to understand the resource partitioning and coexistence strategies between two bat species, Myotis ikonnikovi and Plecotus ognevi, cohabiting the Mt. Jumbong forests, by comparing the differences in dietary consumption based on habitat utilization. Results: Upon examining their dietary composition using the DNA meta-barcoding approach, we identified 403 prey items (amplicon sequence variants). A greater prey diversity including Lepidoptera, Diptera, Coleoptera, and Ephemeroptera, was detected from M. ikonnikovi, whereas most prey items identified from P. ognevi belonged to Lepidoptera. The diversity index of prey items was higher for M. ikonnikovi (H': 5.67, D: 0.995) than that for P. ognevi (H': 4.31, D: 0.985). Pianka's index value was 0.207, indicating little overlap in the dietary composition of these bat species. Our results suggest that M. ikonnikovi has a wider diet composition than P. ognevi. Conclusions: Based on the dietary analysis results, our results suggests the possibility of differences in foraging site preferences or microhabitat utilization between two bat species cohabiting the Mt. Jumbong. In addition, these differences may represent one of the important mechanism in reducing interspecific competition and enabling coexistence between the two bat species. We expected that our results will be valuable for understanding resource partitioning and the coexistence of bats inhabiting the Korean forests.

Keywords

Acknowledgement

This research was funded by research projects of the National Institute of Ecology, Republic of Korea, grant numbers NIE-2017-02 and NIE-2023-38.

References

  1. Anderson ME, Racey PA. Feeding behaviour of captive brown longeared bats, Plecotus auritus. Anim Behav. 1991;42(3):489-93. https://doi.org/10.1016/S0003-3472(05)80048-X.
  2. Andreas M, Reiter A, Benda P. Dietary composition, resource partitioning and trophic niche overlap in three forest foliage-gleaning bats in Central Europe. Acta Chiropt. 2012;14(2):335-45. https://doi.org/10.3161/150811012X661657.
  3. Andriollo T, Michaux JR, Ruedi M. Food for everyone: differential feeding habits of cryptic bat species inferred from DNA metabarcoding. Mol Ecol. 2021;30(18):4584-600. https://doi.org/10.1111/mec.16073.
  4. Arrizabalaga-Escudero A, Clare EL, Salsamendi E, Alberdi A, Garin I, Aihartza J, et al. Assessing niche partitioning of co-occurring sibling bat species by DNA metabarcoding. Mol Ecol. 2018;27(5):1273-83. https://doi.org/10.1111/mec.14508.
  5. Bazzaz FA, Catovsky S. Resource partitioning. In: Levin SA, editor. Encyclopedia of biodiversity. San Diego: Academic Press; 2001. p. 173-84.
  6. Bininda-Emonds ORP, Russell AP. Flight style in bats as predicted from wing morphometry: the effects of specimen preservation. J Zool. 1994;234(2):275-87. https://doi.org/10.1111/j.1469-7998.1994.tb06075.x.
  7. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852-7. Erratum in: Nat Biotechnol. 2019;37(9):1091. https://doi.org/10.1038/s41587-019-0209-9.
  8. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581-3. https://doi.org/10.1038/nmeth.3869.
  9. Catozzi C, Cusco A, Lecchi C, Talenti A, Martucciello A, Cappelli G, et al. Short communication: intra- and inter-individual milk microbiota variability in healthy and infected water buffalo udder quarters. J Dairy Sci. 2019;102(8):7476-82. https://doi.org/10.3168/jds.2019-16352.
  10. Cho KY. A study on the distribution of delicate insects to climate change by altitude in Mt.Jeombong [MSc Thesis]. Wonju: Sang Ji University; 2013.
  11. Chung CU, Han SH, Cha JY, Kim SC, Kim JJ, Jeong JC, et al. The diet composition of the serotine bat, Eptesicus serotinus revealed by faecal analysis. Korean J Environ Ecol. 2015;29(3):368-73. https://doi.org/10.13047/KJEE.2015.29.3.368.
  12. Chung CU, Han SH, Lee CI. Use of bridges as roosting site by bats(Chiroptera). Korean J Environ Ecol. 2009;23(3):294-301.
  13. Chung CU, Han SH, Lee CI. Home-range analysis of pipistrelle bat (Pipistrellus abramus) in non-reproductive season by using radiotracking. Korean J Environ Ecol. 2010;24(4):487-92.
  14. Clare EL, Symondson WO, Broders H, Fabianek F, Fraser EE, MacKenzie A, et al. The diet of Myotis lucifugus across Canada: assessing foraging quality and diet variability. Mol Ecol. 2014;23(15):3618-32. https://doi.org/10.1111/mec.12542.
  15. Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, et al. Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data? Mol Ecol. 2019;28(2):391-406. https://doi.org/10.1111/mec.14734.
  16. Denzinger A, Schnitzler HU. Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Front Physiol. 2013;4:164. https://doi.org/10.3389/fphys.2013.00164.
  17. Entwistle AC, Racey PA, Speakman JR. Habitat exploitation by a gleaning bat, Plecotus auritus. Philos Trans Biol Sci. 1996;351(1342):921-31. https://doi.org/10.1098/rstb.1996.0085
  18. Fenton MB. Science and the conservation of bats. J Mammal. 1997;78(1):1-14. https://doi.org/10.2307/1382633.
  19. Fenton MB. Echolocation, insect hearing, and feeding ecology of insectivorous bats. In: Kunz TH, editor. Ecology of bats. Boston: Springer; 1982. p. 261-85.
  20. Finke DL, Snyder WE. Niche partitioning increases resource exploitation by diverse communities. Science. 2008;321(5895):1488-90. https://doi.org/10.1126/science.1160854.
  21. Fukui D, Hill DA, Kim SS, Han SH. Echolocation call structure of fourteen bat species in Korea. Anim Syst Evol Diversity. 2015;31(3):160-75. https://doi.org/10.5635/ASED.2015.31.3.160.
  22. Global Biodiversity Information Facility (GBIF). Myotis ikonnikovi Ognev, 1912. 2022a. https://www.gbif.org/species/2432431. Accessed 7 Sep 2022.
  23. Global Biodiversity Information Facility (GBIF). Phyllonorycter trifasciella (Haworth, 1828). 2022b. https://www.gbif.org/species/205787717. Accessed 7 Sep 2022.
  24. Gomez-Llano M, Germain RM, Kyogoku D, McPeek MA, Siepielski AM. When ecology fails: how reproductive interactions promote species coexistence. Trends Ecol Evol. 2021;36(7):610-22. https://doi.org/10.1016/j.tree.2021.03.003.
  25. Han SH, Kim SS, Fukui D, Oh DS, Jun JM. Biodiversity and phylogenetic research of bats in forest (II). Incheon: National Institute of Biological Resources; 2012.
  26. Heim O, Puisto AIE, Saaksjarvi I, Fukui D, Vesterinen EJ. Dietary analysis reveals differences in the prey use of two sympatric bat species. Ecol Evol. 2021;11(24):18651-61. https://doi.org/10.1002/ece3.8472.
  27. IUCN Red List of Threatened Species in 2018. Siberian long-eared bat. 2018. https://www.iucnredlist.org/species/136598/21996784. Accessed 15 Jul 2022.
  28. IUCN Red List of Threatened Species 2019. Ikonnikov's Bat. 2019. https://www.iucnredlist.org/species/14168/22057122. Accessed 31 Aug 2022.
  29. Kim SS, Fukui D, Ha SH, Hur WH, Oh DS. Habitat characteristics of Myotis ikonnikovi. Korean J Ecol Environ. 2014;47(1):41-52. https://doi.org/10.11614/KSL.2014.47.1.041.
  30. Kim SS, Choi YS, Kim L. The relationship between thermal preference and hibernation strategies in endangered Plecotus ognevi. Korean J Ecol Environ. 2018;51(4):345-53. https://doi.org/10.11614/KSL.2018.51.4.345.
  31. Kruskop SV, Borisenko AV, Ivanova NV, Lim BK, Eger JL. Genetic diversity of northeastern Palaearctic bats as revealed by DNA barcodes. Acta Chiropt. 2012;14(1):1-14. https://doi.org/10.3161/150811012X654222.
  32. MacArthur RH. Geographical ecology: patterns in the distribution of species. Princeton: Princeton University Press; 1984.
  33. Magoga G, Forni G, Brunetti M, Meral A, Spada A, De Biase A, et al. Curation of a reference database of COI sequences for insect identification through DNA metabarcoding: COins. Database (Oxford). 2022;2022:baac055. https://doi.org/10.1093/database/baac055.
  34. Matthews AK, Neiswenter SA, Ammerman LK. Trophic ecology of the free-tailed bats Nyctinomops femorosaccus and Tadarida brasiliensis (Chiroptera: Molossidae) in big bend national park, Texas. Southwest Nat. 2010;55(3):340-46. https://doi.org/10.1894/JKF-08.1
  35. National Institute of Biological Resources (NIBR). Stenoloba fontinalis Ronkay and Kononenko, 1998. 2023. https://species.nibr.go.kr/home/mainHome.do?cont_link=009&subMenu=009002&contCd=009002&ktsn=120000035337. Accessed 25 Sep 2023.
  36. Norberg UM, Rayner JMV. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc Lond B Biol Sci. 1987;316(1179):335-427 https://doi.org/10.1098/rstb.1987.0030.
  37. Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. Community ecology package. 2022. https://CRAN.R-project.org/package=vegan. Accessed 15 Jul 2022.
  38. Salinas-Ramos VB, Herrera Montalvo LG, Leon-Regagnon V, Arrizabalaga-Escudero A, Clare EL. Dietary overlap and seasonality in three species of mormoopid bats from a tropical dry forest. Mol Ecol. 2015;24(20):5296-307. https://doi.org/10.1111/mec.13386.
  39. Schnitzler HU, Moss CF, Denzinger A. From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol. 2003;18(8):386-94. https://doi.org/10.1016/S0169-5347(03)00185-X.
  40. Schoener TW. Resource partitioning in ecological communities. Science. 1974;185(4145):27-39. https://doi.org/10.1126/science.185.4145.27.
  41. Spitzenberger F, Strelkov PP, Winkler H, Haring E. A preliminary revision of the genus Plecotus (Chiroptera, Vespertilionidae) based on genetic and morphological results. Zool Scr. 2006;35(3):187-230. https://doi.org/10.1111/j.1463-6409.2006.00224.x.
  42. Starik N, Gottert T, Zeller U. Spatial behavior and habitat use of two sympatric bat species. Animals (Basel). 2021;11(12):3460. https://doi.org/10.3390/ani11123460.
  43. Whitaker JO Jr. Prey selection in a temperate zone insectivorous bat community. J Mammal. 2004;85(3):460-9. https://doi.org/10.1644/1383943.
  44. Yoon KB, Lim SJ, Park YC. Analysis on habitat characteristics of the Korean bats (Chiroptera) using geographic information system (GIS). J For Environ Sci. 2016;32(4):377-83. https://doi.org/10.7747/JFES.2016.32.4.377.
  45. Zeale MR, Butlin RK, Barker GL, Lees DC, Jones G. Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Mol Ecol Resour. 2011;11(2):236-44. https://doi.org/10.1111/j.1755-0998.2010.02920.x.
  46. Zhang J. Species association analysis. 2016. https://cran.r-project.org/web/packages/spaa/index.html. Accessed 15 Jul 2022.