DOI QR코드

DOI QR Code

Identification of orb-web spider species and their food source through environmental DNA analysis

  • Keonhee Kim (Human and Eco Care Center, Konkuk University) ;
  • Seung Tae Kim (Life and Environment Research Institute, Konkuk University)
  • Received : 2024.03.12
  • Accepted : 2024.06.06
  • Published : 2024.09.30

Abstract

Spiders play a vital role in agricultural ecosystems by capturing and preying on small insects, thereby controlling the pests around crops. However, without directly collecting the specimen, it is challenging to accurately determine the species of the spider that formed the web and its diet. Spiders dissolve their prey with digestive fluids while consuming; thus, leaving very little residue in their digestive system. This study aimed to identify the spider that formed the web and the prey caught in the web using environmental DNA (eDNA) present in the spider web. For this purpose, eDNA using the mitochondrial cytochrome C oxidase subunit I (COI) gene was extracted from five adjacent spider webs collected from residences near agricultural environments. Based on the genes extracted from spider webs, it was confirmed that the most commonly found gene in all five spider webs was COI of Parasteatoda tepidariorum, and no other spider genes were detected. Among the five spider webs, prey was found in only one web, and in that web, genes of arthropods other than spiders were detected. The genes of the prey found in the spider web were identified to be those of Orthocladius tamarutilus, Tanytarsus tamagotoi, and Yemma exilis. Thus, without directly collecting arthropod specimens from the spider web, it was possible to identify the spider and its prey. This provides crucial information that can help in clearly understanding the predatory activities of spiders in agricultural ecosystems in the future.

Keywords

Acknowledgement

This work was carried out with the support of "Cooperative Research Program for Agriculture Science & Technology Development (Project No. RS-2020-RD009339)" Rural Development Administration, Republic of Korea.

References

  1. Astrin JJ, Huber BA, Misof B, Klutsch CFC. Molecular taxonomy in pholcid spiders (Pholcidae, Araneae): evaluation of species identification methods using CO1 and 16S rRNA. Zool Scr. 2006;35(5):441-57. https://doi.org/10.1111/j.1463-6409.2006.00239.x.
  2. Bairoliya S, Koh Zhi Xiang J, Cao B. Extracellular DNA in environmental samples: occurrence, extraction, quantification, and impact on microbial biodiversity assessment. Appl Environ Microbiol. 2022;88(3):e0184521. https://doi.org/10.1128/AEM.01845-21.
  3. Barrett RD, Hebert PD. Identifying spiders through DNA barcodes. Can J Zool. 2005;83(3):481-91. https://doi.org/10.1139/z05-024.
  4. Benamu M. The importance of spider diversity in agroecosystems and the effect of pesticides. Glob J Ecol. 2020;5(1):60-1. https://doi.org/10.17352/gje.000022.
  5. Blackledge TA. Prey capture in orb weaving spiders: are we using the best metric? J Arachnol. 2011;39(2):205-10.
  6. Blagoev GA, Nikolova NI, Sobel CN, Hebert PD, Adamowicz SJ. Spiders (Araneae) of Churchill, Manitoba: DNA barcodes and morphology reveal high species diversity and new Canadian records. BMC Ecol. 2013;13(1):44. https://doi.org/10.1186/1472-6785-13-44.
  7. Blasco-Arostegui J, Calatayud-Mascarell A. All you can eat: autochthonous vertebrate and invertebrate predation by the alien spider Parasteatoda tepidariorum (C.L. Koch, 1841) (Araneae: Theridiidae) in two anthropogenic habitats of Italy. Graellsia. 2023;79(1):e193. https://doi.org/10.3989/graellsia.2023.v79.350.
  8. Bradley RA. Common spiders of North America. Berkeley: University of California Press; 2012.
  9. Corse E, Tougard C, Archambaud-Suard G, Agnese JF, Messu Mandeng FD, Bilong Bilong CF, et al. One-locus-several-primers: a strategy to improve the taxonomic and haplotypic coverage in diet metabarcoding studies. Ecol Evol. 2019;9(8):4603-20. https://doi.org/10.1002/ece3.5063.
  10. Craig CL, Freeman CR. Effects of predator visibility on prey encounter: a case study on aerial web weaving spiders. Behav Ecol Sociobiol. 1991;29:249-54. https://doi.org/10.1007/BF00163981.
  11. Eberhard WG, Barrantes G, Weng JL. Tie them up tight: wrapping by Philoponella vicina spiders breaks, compresses and sometimes kills their prey. Naturwissenschaften. 2006;93(5):251-4. https://doi.org/10.1007/s00114-006-0094-1.
  12. Edwards GB. The common house spider, Parasteatoda tepidariorum (C. L. Koch) (Arachnida: Araneae: Theridiidae). EDIS 2004;8. https://doi.org/10.32473/edis-in394-2001.
  13. Elbrecht V, Leese F. Validation and development of COI metabarcoding primers for freshwater macroinvertebrate bioassessment. Front Environ Sci. 2017;5:11. https://doi.org/10.3389/fenvs.2017.00011.
  14. Elbrecht V, Vamos EE, Steinke D, Leese F. Estimating intraspecific genetic diversity from community DNA metabarcoding data. PeerJ. 2018;6:e4644. https://doi.org/10.7717/peerj.4644.
  15. Gogoi J, Ningthoujam K. Arthropod biodiversity in agricultural, horticultural and silvicultural ecosystems with special reference to spiders (Araneae) in mid-hills of Meghalaya, India. J Agri Horti Res. 2023;6(2):244-62.
  16. Goyal K, MeLampy F, Osborn R, Turrill M. Prey size preference of the American house spider Parasteatoda tepidariorum. Ann Arbor: Biological Station, University of Michigan (UMBS); 2017.
  17. Graf N, Battes KP, Cimpean M, Entling MH, Frisch K, Link M, et al. Relationship between agricultural pesticides and the diet of riparian spiders in the field. Environ Sci Eur. 2020;32:1. https://doi.org/10.1186/s12302-019-0282-1.
  18. Gregoric M, Kutnjak D, Bacnik K, Gostincar C, Pecman A, Ravnikar M, et al. Spider webs as eDNA samplers: biodiversity assessment across the tree of life. Mol Ecol Resour. 2022;22(7):2534-45. https://doi.org/10.1111/1755-0998.13629.
  19. Harrison JB, Sunday JM, Rogers SM. Predicting the fate of eDNA in the environment and implications for studying biodiversity. Proc Biol Sci. 2019;286(1915):20191409. https://doi.org/10.1098/rspb.2019.1409.
  20. Im MS, Kim ST. Field guide of Korean spiders. Seoul: Konkuk University Press; 2000. 
  21. Kohno K, Hirose Y. The stilt bug Yemma exilis (Heteroptera: Berytidae) as a predator of Aphis gossypii (Homoptera: Aphididae) and Thrips palmi (Thysanoptera: Thripidae) on eggplant. Appl Entomol Zool. 1997;32(2):406-9. https://doi.org/10.1303/aez.32.406.
  22. Kong SH. Checklist of organisms in Korean; 9. Seoul: Nature and Ecology; 2013.
  23. Korenko S, Niedobova J, Kolarova M, Hamouzova K, Kysilkova K, Michalko R. The effect of eight common herbicides on the predatory activity of the agrobiont spider Pardosa agrestis. BioControl. 2016;61:507-17. https://doi.org/10.1007/s10526-016-9729-0.
  24. Ludwig L, Barbour MA, Guevara J, Aviles L, Gonzalez AL. Caught in the web: Spider web architecture affects prey specialization and spider-prey stoichiometric relationships. Ecol Evol. 2018;8(13):6449-62. https://doi.org/10.1002/ece3.4028.
  25. Maloney D, Drummond FA, Alford R. TB190: spider predation in agroecosystems: can spiders effectively control pest populations. Orono: Maine Agricultural and Forest Experiment Station; 2003.
  26. Manicom C, Schwarzkopf L, Alford RA, Schoener TW. Self-made shelters protect spiders from predation. Proc Natl Acad Sci U S A. 2008;105(39):14903-7. https://doi.org/10.1073/pnas.0807107105.
  27. Marc P, Canard A, Ysnel F. Spiders (Araneae) useful for pest limitation and bioindication. Agric Ecosyst Environ. 1999;74(1-3):229-73. https://doi.org/10.1016/S0167-8809(99)00038-9.
  28. Menalled FD, Smith RG, Dauer JT, Fox TB. Impact of agricultural management on carabid communities and weed seed predation. Agric Ecosyst Environ. 2007;118(1-4):49-54. https://doi.org/10.1016/j.agee.2006.04.011.
  29. Milne LJ, Milne M. The Audubon Society field guide to North American insects and spiders. New York: Distributed by Random House; 1980.
  30. Minamoto T, Miya M, Sado T, Seino S, Doi H, Kondoh M, et al. An illustrated manual for environmental DNA research: water sampling guidelines and experimental protocols. Environ DNA. 2021;3(1):8-13. https://doi.org/10.1002/edn3.121.
  31. Murakami Y. Factors determining the prey size of the orb-web spider, Argiope amoena (L. Koch) (Argiopidae). Oecologia. 1983;57(1-2):72-7. https://doi.org/10.1007/BF00379564.
  32. Murali A, Bhargava A, Wright ES. IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences. Microbiome. 2018;6(1):140. https://doi.org/10.1186/s40168-018-0521-5.
  33. Nentwig W, Ansorg J, Bolzern A, Frick H, Ganske AS, Hanggi A, et al. How spiders eat: feeding through the straw. In: Nentwig W, Ansorg J, Bolzern A, Frick H, Ganske AS, Hanggi A, et al, editors. All you need to know about spiders. Cham: Springer; 2022. p. 101-8.
  34. Newton JP, Nevill P, Bateman PW, Campbell MA, Allentoft ME. Spider webs capture environmental DNA from terrestrial vertebrates. iScience. 2024;27(2):108904. https://doi.org/10.1016/j.isci.2024.108904.
  35. National Institute of Biological Resources (NIBR). Biodiversity of Korea peninsula, National Institute of Biological Resources (NIBR). Incheon: Ministry of Environment; 2016. https://species.nibr.go.kr/index.do.
  36. Nyffeler M. Prey selection of spiders in the field. J Arachnol. 1999;27(1):317-24.
  37. Oda H, Akiyama-Oda Y. The common house spider Parasteatoda tepidariorum. Evodevo. 2020;11:6. https://doi.org/10.1186/s13227-020-00152-z.
  38. Park HH, Lee JH. Arthropod trophic relationships in a temperate rice ecosystem: a stable isotope analysis with δ13C and δ15N. Environ Entomol. 2006;35(3):684-93. https://doi.org/10.1603/0046-225X-35.3.684.
  39. Sarma S, Pujari D, Rahman Z. Role of spiders in regulating insect pests in the agricultural ecosystem - an overview. J Int Acad Res Multidiscip. 2013;1(5):100-17.
  40. Scherr SJ, McNeely JA. Biodiversity conservation and agricultural sustainability: towards a new paradigm of 'ecoagriculture' landscapes. Philos Trans R Soc Lond B Biol Sci. 2008;363(1491):477-94. https://doi.org/10.1098/rstb.2007.2165.
  41. Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S, Khovanskaya R, et al. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford). 2020;2020:baaa062. https://doi.org/10.1093/database/baaa062.
  42. Stecher G, Tamura K, Kumar S. Molecular evolutionary genetics analysis (MEGA) for macOS. Mol Biol Evol. 2020;37(4):1237-9. https://doi.org/10.1093/molbev/msz312.
  43. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10(3):512-26. https://doi.org/10.1093/oxfordjournals.molbev.a040023.
  44. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38(7):3022-7. https://doi.org/10.1093/molbev/msab120.
  45. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44(14):6614-24. https://doi.org/10.1093/nar/gkw569.
  46. Thomsen PF, Willerslev E. Environmental DNA - an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv. 2015;183:4-18. https://doi.org/10.1016/j.biocon.2014.11.019.
  47. Valentin RE, Kyle KE, Allen MC, Welbourne DJ, Lockwood JL. The state, transport, and fate of aboveground terrestrial arthropod eDNA. Environ DNA. 2021;3(6):1081-92. https://doi.org/10.1002/edn3.229.
  48. Wilgers DJ. Investigating community food WEBS: the ecological importance of spiders. 2016. https://www.sciencefriday.com/educational-resources/investigating-community-food-webs-ecological-importance-spiders/. Accessed 1 Feb 2024.
  49. Wright ES. Using DECIPHER v2.0 to analyze big biological sequence data in R. R J. 2016;8(1):352-9.
  50. Xu CC, Yen IJ, Bowman D, Turner CR. Spider web DNA: a new spin on noninvasive genetics of predator and prey. PLoS One. 2015;10(11):e0142503. https://doi.org/10.1371/journal.pone.0142503.