The food web in a subterranean ecosystem is driven by intraguild predation
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33654189
PubMed Central
PMC7925651
DOI
10.1038/s41598-021-84521-1
PII: 10.1038/s41598-021-84521-1
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Trophic interactions of cave arthropods have been understudied. We used molecular methods (NGS) to decipher the food web in the subterranean ecosystem of the Ardovská Cave (Western Carpathians, Slovakia). We collected five arthropod predators of the species Parasitus loricatus (gamasid mites), Eukoenenia spelaea (palpigrades), Quedius mesomelinus (beetles), and Porrhomma profundum and Centromerus cavernarum (both spiders) and prey belonging to several orders. Various arthropod orders were exploited as prey, and trophic interactions differed among the predators. Linear models were used to compare absolute and relative prey body sizes among the predators. Quedius exploited relatively small prey, while Eukoenenia and Parasitus fed on relatively large prey. Exploitation of eggs or cadavers is discussed. In contrast to previous studies, Eukoenenia was found to be carnivorous. A high proportion of intraguild predation was found in all predators. Intraspecific consumption (most likely cannibalism) was detected only in mites and beetles. Using Pianka's index, the highest trophic niche overlaps were found between Porrhomma and Parasitus and between Centromerus and Eukoenenia, while the lowest niche overlap was found between Parasitus and Quedius. Contrary to what we expected, the high availability of Diptera and Isopoda as a potential prey in the studied system was not corroborated. Our work demonstrates that intraguild diet plays an important role in predators occupying subterranean ecosystems.
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Mulec J. Phototrophs in caves. In: Moldovan OT, Kováč Ľ, Halse S, editors. Cave Ecology. Cham: Springer; 2018. pp. 91–106.
Culver DC, Pipan T. The Biology of Caves and Other Subterranean Habitats. New York: Oxford University Press Inc.; 2009.
Engel AS. Chemoautotrophy. In: White WB, Culver DC, editors. Encyclopedia of caves. 2. Amsterdam: Elsevier; 2012. pp. 125–134.
Kinkle BK, Kane TC. Chemolithotrophic microorganisms and their potential role in subsurface environments. In: Wilkens H, Culver DC, Humphreys WF, editors. Ecosystems of the World 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000. pp. 309–319.
Sarbu SM. Movile cave: A chemoautotrophically based groundwater ecosystem. In: Wilkens H, Culver DC, Humphreys WF, editors. Ecosystems of the World 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2001. pp. 319–343.
Simon KS, Pipan T, Culver DC. A conceptual model of the flow and distribution of organic carbon in caves. J. Cave Karst Stud. 2007;69:279–284.
Camassa MM. Food resources. In: Gunn J, editor. Encyclopaedia of Caves and Karst Science. London: Fitzroy Dearborn; 2004. pp. 755–760.
Poulson TL, Lavoie KH. (The trophic basis of subsurface ecosystems. In: Wilkens H, Culver DC, Humphreys WF, editors. Ecosystems of the World 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000. pp. 323–334.
Gibert J, Deharveng L. Subterranean ecosystems: A truncated functional biodiversity. Bioscience. 2002;52(6):473–481. doi: 10.1641/0006-3568(2002)052[0473:SEATFB]2.0. DOI
Chen B, Wise DH. Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web. Ecology. 1999;80(3):761–772. doi: 10.2307/177015. DOI
Venarsky MP, Huntsman BM. Food webs in caves. In: Moldovan OT, Kováč Ľ, Halse S, editors. Cave Ecology. Cham: Springer; 2018. pp. 309–331.
Gnaspini P. Guano communities. In: White WB, Culver DC, editors. Encyclopedia of caves. 2. Amsterdam: Elsevier; 2012. pp. 357–364.
Ipsen A. The Segeberger Höhle—A phylogenetically young cave ecosystem in northern Germany. In: Wilkens H, Culver DC, Humphreys WF, editors. Ecosystems of the World 30. Subterranean Ecosystems. Amsterdam: Elsevier; 2000. pp. 569–579.
Stone FD, Howarth FG, Hoch H, Asche M. Root communities in lava tubes. In: White WB, Culver DC, editors. Encyclopedia of Caves. 2. Amsterdam: Elsevier; 2012. pp. 658–664.
Mammola S, Piano E, Isaia M. Step back! Niche dynamics in cave-dwelling predators. Acta Oecol. 2016;75:35–42. doi: 10.1016/j.actao.2016.06.011. DOI
Mammola S, Isaia M. Cave communities and species interactions. In: Moldovan OT, Kováč Ľ, Halse S, editors. Cave Ecology. Cham: Springer; 2018. pp. 255–269.
Scheu S, Setälä H. Multitrophic interactions in decomposer food webs. In: Tscharntke T, Hawkins BA, editors. Multitrophic Interactions in Terrestrial Systems. Cambridge University Press: Cambridge; 2001. pp. 223–264.
Wood PJ. Subterranean ecology. In: Gunn J, editor. Encyclopaedia of Caves and Karst Science. London: Fitzroy Dearborn; 2004. pp. 1514–1519.
Pekár S, García LF, Viera C. Trophic niche and trophic adaptations of prey specialised spiders of the Neotropics: A guide. In: Viera C, Gonzaga MO, editors. Behavioural Ecology of Neotropical Spiders. Cham: Springer; 2017. pp. 247–274.
Pohlman JW, Iliffe TM, Cifuentes LA. A stable isotope study of organic cycling and the ecology of an anchialine cave ecosystem. Mar. Ecol. Prog. Ser. 1997;155:17–27. doi: 10.3354/meps155017. DOI
Pohlman JW, Cifuentes LA, Iliffe TM. Food web dynamics and biogeochemistry of anchialine caves: A stable isotope approach. In: Wilkens H, Culver DC, Humphreys WF, editors. Ecosystems of the World 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000. pp. 345–357.
Sarbu SM, Galdenzi S, Menichetti M, Gentile G. Geology and biology of the Frasassi caves in Central Italy: An ecological multi-disciplinary study of a hypogenic underground karst system. In: Wilkens H, Culver DC, Humphreys WF, editors. Ecosystems of the World 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000. pp. 359–378.
Eitzinger B, Micic A, Körner M, Traugott M, Scheu S. Unveiling soil food web links: New PCR assays for detection of prey DNA in the gut of soil arthropod predators. Soil Biol. Biochem. 2013;57:943–945. doi: 10.1016/j.soilbio.2012.09.001. DOI
Juen A, Traugott M. Revealing species-specific trophic links in soil food webs: Molecular identification of scarab predators. Mol. Ecol. 2007;16:1545–1557. doi: 10.1111/j.1365-294X.2007.03238.x. PubMed DOI
King RA, Read DS, Traugott M, Symondson WOC. Molecular analysis of predation: A review of best practice for DNA-based approaches. Mol. Ecol. 2008;17:947–963. doi: 10.1111/j.1365-294X.2007.03613.x. PubMed DOI
Symondson WOC. Molecular identification of prey in predator diets. Mol. Ecol. 2002;11(4):627–641. doi: 10.1046/j.1365-294x.2002.01471.x. PubMed DOI
Traugott M, Kamenova S, Ruess L, Seeber J, Plantegenest M. Empirically characterising trophic networks: What emerging DNA-based methods, stable isotope and fatty acid analyses can offer. Adv. Ecol. Res. 2013;49:177–224. doi: 10.1016/B978-0-12-420002-9.00003-2. DOI
Kováč Ľ, et al. Terrestrial arthropods of the Domica Cave system and the Ardovská Cave (Slovak Karst): Principal microhabitats and diversity. In: Tajovský K, Schlaghamerský J, Pižl V, et al., editors. Contributions to Soil Zoology in Central Europe I. České Budějovice: ISB AS CR; 2005. pp. 61–70.
Kováč, Ľ. et al.The cave biota of Slovakia. Speleologia Slovaca 5. (Liptovský Mikuláš, State Nature Conservancy SR, Slovak Caves Administration, 2014). 10.13140/2.1.3473.0569
Kováč Ľ, Parimuchová A, Miklisová D. Distributional patterns of cave Collembola (Hexapoda) in association with habitat conditions, geography and subterranean refugia in the Western Carpathians. Biol. J. Linn. Soc. Lond. 2016;119(3):571–592. doi: 10.1111/bij.12555. DOI
Smrž J, Kováč Ľ, Mikeš J, Lukešová A. Microwhip scorpions (Palpigradi) feed on heterotrophic Cyanobacteria in Slovak caves: A curiosity among Arachnida. PLoS ONE. 2013;8(10):e75989. doi: 10.1371/journal.pone.0075989. PubMed DOI PMC
Pekár S, Coddington JA, Blackledge T. Evolution of stenophagy in spiders (Araneae): Evidence based on the comparative analysis of spider diets. Evolution. 2012;66(3):776–806. doi: 10.1111/j.1558-5646.2011.01471.x. PubMed DOI
Alderweireldt M. Prey selection and prey capture strategies of linyphiid spiders in highinput agricultural fields. Bull. Br. Arachnol. Soc. 1994;9:300–308.
Lukić, M., Collembola in caves. Croatian Biospeleological Society, DVD, 10.25 min (2012).
Roewer CF. Palpigradi. In: Bronns HG, editor. Klassen und Ordnungen des Tierreichs 5: Arthropoda IV: Arachnoidea. Leipzig: Akademische Verlagsgesellschaft MBH; 1932. pp. 640–707.
van der Hammen L. Comparative studies in Chelicerata II. Epimerata (Palpigradi and Actinotrichida) Zool. Verh. 1982;196:3–70.
Wheeler WM. A singular arachnid Koenenia mirabilis (Grassi) occurring in Texas. Am. Nat. 1900;34:837–850. doi: 10.1086/277805. DOI
Harwood JD, Phillips SW, Sunderland KD, Symondson WOC. Secondary predation: quantification of food chain errors in an aphid–spider–carabid system using monoclonal antibodies. Mol. Ecol. 2001;10(8):2049–2057. doi: 10.1046/j.0962-1083.2001.01349.x. PubMed DOI
Szafranek P, Lewandowski M, Kozak M. Prey preference and life tables of the predatory mite Parasitus bituberosus (Acari: Parasitidae) when offered various prey combinations. Exp. Appl. Acarol. 2013;61(1):53–67. doi: 10.1007/s10493-013-9701-y. PubMed DOI PMC
Al-Amidi AHK, Downes MJ. Parasitus bituberosus (Acari: Parasitidae), a possible agent for biological control of Heteropeza pygmaea (Diptera: Cecidomyiidae) in mushroom compost. Exp. Appl. Acarol. 1990;8(1–2):13–25. doi: 10.1007/BF01193378. DOI
Adams BJ, Nguyen KB. Nematode parasites of insects. In: Capinera JL, editor. Encyclopedia of Entomology. Cham: Springer; 2008. pp. 2577–2584.
Cokendolpher JC. Pathogens and parasites of opiliones (arthropoda: arachnida) J. Arachnol. 1993;21(2):120–146.
Kruse PD, Toft S, Sunderland KD. Temperature and prey capture: Opposite relationships in two predator taxa. Ecol. Entomol. 2008;33(2):305–312. doi: 10.1111/j.1365-2311.2007.00978.x. DOI
Krooss S, Schaefer M. How predacious are predators? A study on Ocypus similis, a rove beetle of cereal fields. Ann. Appl. Biol. 1998;133(1):1–16. doi: 10.1111/j.1744-7348.1998.tb05797.x. DOI
Waldbauer GP, Friedman S. Self-selection of optimal diets by insects. Annu. Rev. Entomol. 1991;36(1):43–63. doi: 10.1146/annurev.en.36.010191.000355. DOI
Mayntz D, Toft S. Nutrient composition of the prey’s diet affects growth and survivorship of a generalist predator. Oecologia. 2001;127:207–213. doi: 10.1007/s004420000591. PubMed DOI
Finke DL, Denno RF. Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology. 2002;83:643–652. doi: 10.2307/3071870. DOI
Staudacher K, et al. Habitat heterogeneity induces rapid changes in the feeding behaviour of generalist arthropod predators. Funct. Ecol. 2018;32(3):809–819. doi: 10.1111/1365-2435.13028. PubMed DOI PMC
Finke DL, Denno RF. Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecol. Lett. 2005;8:1299–1306. doi: 10.1111/j.1461-0248.2005.00832.x. DOI
Schausberger P, Croft BA. Nutritional benefits of intraguild predation and cannibalism among generalist and specialist phytoseiid mites. Ecol. Entomol. 2000;25(4):473–480. doi: 10.1046/j.1365-2311.2000.00284.x. DOI
Schausberger P. Cannibalism among phytoseiid mites: a review. Exp. Appl. Acarol. 2003;29(3/4):173–191. doi: 10.1023/a:1025839206394. PubMed DOI
Elgar MA, Crespi BJ. Cannibalism: Ecology and Evolution Among Diverse Taxa. Oxford: Oxford University Press; 1992.
Polis GA. The evolution and dynamics of intraspecific predation. Annu. Rev. Ecol. Syst. 1981;12(1):225–251. doi: 10.1146/annurev.es.12.110181.001301. DOI
Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ. Nitrogen in insects: Implications for trophic complexity and species diversification. Am. Nat. 2002;160(6):784–802. doi: 10.1086/343879. PubMed DOI
Fagan WF, Denno RF. Stoichiometry of actual vs. potential predator–prey interactions: Insights into nitrogen limitation for arthropod predators. Ecol. Lett. 2004;7(9):876–883. doi: 10.1111/j.1461-0248.2004.00641.x. DOI
Denno RF, Fagan WF. Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology. 2003;84(10):2522–2531. doi: 10.1890/02-0370. PubMed DOI
Snyder WE, Joseph SB, Preziosi RF, Moore AJ. Nutritional benefits of cannibalism for the lady beetle Harmonia axyridis (Coleoptera: Coccinellidae) when prey quality is poor. Environ. Entomol. 2000;29(6):1173–1179. doi: 10.1603/0046-225x-29.6.1173. DOI
Nováková A, et al. Feeding sources of invertebrates in the Ardovská Cave and Domica Cave systems: preliminary results. In: Tajovský K, Schlaghamerský J, Pižl V, et al., editors. Contributions to Soil Zoology in Central Europe I. České Budějovice: ISB AS CR; 2005. pp. 107–112.
Crossley D, Blair JM. A high efficiency, “low-technology” Tullgren-type extractor for soil microarthropods. Agric. Ecosyst. Environ. 1991;34:187–192. doi: 10.1016/0167-8809(91)90104-6. DOI
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 1994;3(5):294–299. PubMed
de Groot AG, Laros I, Geisen S. Molecular identification of soil eukaryotes and focused approaches targeting protist and faunal groups using high-throughput meta-barcoding methods in molecular biology. Methods Mol. Biol. 2016;1399:125–140. doi: 10.1007/978-1-4939-3369-3_7. PubMed DOI
Aronesty E. Comparison of sequencing utility programs. Open Bioinform. J. 2013;7(1):1–8. doi: 10.2174/1875036201307010001. DOI
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–12. doi: 10.14806/ej.17.1.200. DOI
Mahé F, Rognes T, Quince C, de Vargas C, Dunthorn M. Swarm: robust and fast clustering method for amplicon-based studies. PeerJ. 2014;2:e593. doi: 10.7717/peerj.593. PubMed DOI PMC
Belshaw R, Lopez-Vaamonde C, Degerli N, Quicke DLJ. Paraphyletic taxa and taxonomic chaining: Evaluation the classification of braconine wasps (Hymenoptera: Braconidae) using 28S D2–3 rDNA sequences and morphological characters. Biol. J. Linn. Soc. Lond. 2001;73(4):411–424. doi: 10.1111/j.1095-8312.2001.tb01370.x. DOI
Hurlbert SH. The measurement of niche overlap and some relatives. Ecology. 1978;59(1):67–77. doi: 10.2307/1936632. DOI
Novakowski GC, Hahn NS, Fugi R. Diet seasonality and food overlap of the fish assemblage in a pantanal pond. Neotrop. Ichthyol. 2008;6(4):567–576. doi: 10.1590/S1679-62252008000400004. DOI
Pianka ER. The structure of lizard communities. Annu. Rev. Ecol. Syst. 1973;4(1):53–74. doi: 10.1146/annurev.es.04.110173.000413. DOI
Pekár S, Brabec M. Modern Analysis of Biological Data. Generalized Linear Models in R. Brno: MUNI Press; 2016.
R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, Vienna). https://www.R-project.org/ (2017).
Breheny P, Burchett W. Visualization of regression models using visreg. R J. 2017;9:56–71. doi: 10.32614/RJ-2017-046. DOI
Kučera B. Krasová morfologie a vývoj Ardovské jeskyně v Jihoslovenském krasu. Československý Kras. 1964;16:41–56.