Skip to main content
Log in

Molecular quantification of spider preying on springtails in winter-spring fallow waterlogged paddy fields

  • Original Research Paper
  • Published:
Applied Entomology and Zoology Aims and scope Submit manuscript

A Correction to this article was published on 30 January 2021

This article has been updated

Abstract

Fallow waterlogged paddy field (FWPF) is a subtropical type of winter-spring fallow rice fields. Arthropod predation is crucial for their survival during the long-duration FWPF seasons. No research has been conducted in the trophic link of arthropod predators and their prey in FWPFs. Here, we used a quantitative real-time PCR approach, both in lab and field, to detect the trophic link. DNA-based identification confirmed the results of a morphological classification in two dominant species of springtail, Homidia socia Denis and H. tiantaiensis Chen and Lin (Collembola: Entomobryidae). The fastest degradation in H. socia DNA copy numbers in spider Pirata subpiraticus (Bösenberg and Strand) (Araneida: Lycosidae) guts occurred within 8 h under lab conditions. Quantitative comparisons of preying on H. socia by H. socia DNA copy numbers indicated that Oedothorax insecticeps (Bösenberg and Strand), Erigonidium graminicolum (Sundevall) (Araneida: Linyphiidae) and P. subpiraticus were more active springtail predators than others under field conditions. There were significant differences in the DNA copy numbers of springtails in gut of P. subpiraticus among different overwintering periods that was significantly positive related to the springtail densities. This study highlights springtail importance at species level as the prey of spiders in FWPFs and illustrates the utility of our approach to quantify their trophic linkages among different spider species or postharvest seasons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig.1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Change history

References

  • Agustí N, Shayler SP, Harwood JD, Vaughan IP, Sunderland KD, Symondson WOC (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Mol Ecol 12:3467–3475

    Article  Google Scholar 

  • Bai YY, Yan RH, Ye GY, Huang FN, Cheng JA (2010) Effects of transgenic rice expressing Bacillus thuringiensis Cry1Ab protein on ground-dwelling collembolan community in postharvest seasons. Environ Entomol 39:243–251

    Article  CAS  Google Scholar 

  • Bai YY, Yan RH, Ye GY, Huang FN, Wangila DS, Wang JJ, Cheng JA (2012) Field response of aboveground non-target arthropod community to transgenic Bt-Cry1Ab rice plant residues in postharvest seasons. Transgenic Res 21:1023–1032

    Article  CAS  Google Scholar 

  • Chapman EG, Schmidt JM, Welch KD, Harwood JD (2013) Molecular evidence for dietary selectivity and pest suppression potential in an epigeal spider community in winter wheat. Biol Control 65:72–86

    Article  CAS  Google Scholar 

  • Eitzinger B, Unger EM, Traugott M (2014) Effects of prey quality and predator body size on prey DNA detection success in a centipede predator. Mol Ecol 23:3767–3776

    Article  CAS  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  Google Scholar 

  • Furul S, Miyanoshita A, Imamura T, Minegishi Y, Kokutani R (2019) Qualitative real-time PCR identification of the khapra beetle, Trogoderma granarium (Coleoptera: Dermestidae). Appl Entomol Zool 54:101–107

    Article  Google Scholar 

  • Gomez-Polo P, Alomar O, Castañé C, Lundgren JG, Piñol J, Agustí N (2015) Molecular assessment of predation by hoverflies (Diptera: Syrphidae) in Mediterranean lettuce crops. Pest Manag Sci 71:1219–1227

    Article  CAS  Google Scholar 

  • Gomez-Polo P, Alomar O, Castañé C, Agustí N (2016) Molecular tracking of arthropod predator-prey interactions in Mediterranean lettuce crops. Food Webs 9:18–24

    Article  Google Scholar 

  • Harper GL, Sheppard SK, Harwood JD, Read DS, Glen DM, Bruford MW, Symondson WOC (2006) Evaluation of temperature gradient gel electrophoresis for the analysis of prey DNA within the guts of invertebrate predators. Bull Entomol Res 96:295–304

    Article  CAS  Google Scholar 

  • Hoogendoorn M, Heimpel GE (2001) PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. Mol Ecol 10:2059–2067

    Article  CAS  Google Scholar 

  • Kuusk AK, Agustí N (2008) Group-specific primers for DNA-based detection of springtails (Hexapoda: Collembola) within predator gut contents. Mol Ecol Resour 8:678–681

    Article  CAS  Google Scholar 

  • Kuusk AK, Cassel-Lundhagen A, Kvarnheden A, Ekbom B (2008) Tracking aphid predation by lycosid spiders in spring-sown cereals using PCR-based gut-content analysis. Basic Appl Ecol 9:718–725

    Article  CAS  Google Scholar 

  • Mateos E (2008) Definition of Lepidocyrtus lusitanicus Gama, 1964 species-complex (Collembola, Entomobryidae), with description of new species and colour forms from the Iberian Peninsula. Zootaxa 1917:38–54

    Article  Google Scholar 

  • Pang BP, Cheng JA, Wang QF (1998) On the functional response and preference of two paddyfield spiders to a springtail. J Plant Protect 25(3):193–196 (In Chinese with English abstract)

    Google Scholar 

  • Pang S, Wang C, Wang GH, Wang XQ, Zhu ZR, Bai YY (2017) Analysis of predation of the spiders on collembolans using the gene of 18S rDNA in fallow waterlogged paddy fields in Chongqing. J Plant Protect 44:1011–1016 (In Chinese with English abstract)

  • Park HH, Lee JH (2006) Arthropod trophic relationships in a temperate rice ecosystem: a stable isotope analysis with δ13C and δ15N. Environ Entomol 35:684–693

    Article  CAS  Google Scholar 

  • Pekar S (2002) Differential effects of formaldehyde concentration and detergent on the catching efficiency of surface active arthropods by pitfall traps. Pedobiologia 46:539–547

    Article  CAS  Google Scholar 

  • Roubinet E, Birkhofer K, Malsher G, Staudacher K, Ekbom B, Traugott M, Jonsson M (2017) Diet of generalist predators reflects effects of cropping period and farming system on extra- and intraguild prey. Ecol Appl 27:1167–1177

    Article  Google Scholar 

  • Schoenly KG, Cohen JE, Heong KL, Litsinger JA, Barrion AT, Arida GS (2010) Fallowing did not disrupt invertebrate fauna in Philippine low-pesticide irrigated rice fields. J Appl Ecol 47:593–602

    Article  Google Scholar 

  • Shi SD, Pan ZX, Zhang F (2010) A new species and a new record of genus Homidia Börner, 1906 from east China (Collembola: Entomobryidae). Zootaxa 2351:29–38

    Article  Google Scholar 

  • Wang GH, Wang XQ, Qiao F, Zhu ZR, Cheng JA (2013) Development and preliminary application of a triplex real-time polymerase chain reaction assay for evaluating predation on three planthoppers in a rice ecosystem. Mol Ecol Resour 13:811–819

    Article  CAS  Google Scholar 

  • Wang Y, Chen J, Xiao DH, Ma FG, Hua HX (2016) Assessing the efficacy of different sampling methods for arthropods in rice field. J Environ Entomol 38(6):1090–1098 (In Chinese with English abstract)

  • Wang XQ, Wang GH, Zhu ZR, Tang QY, Hu Y, Qiao F, Heong KL, Cheng JA (2017) Spider (Araneae) predations on white-backed planthopper Sogatella furcifera in subtropical rice ecosystems, China. Pest Manag Sci 73:1277–1286

    Article  CAS  Google Scholar 

  • Weber DC, Lundgren JG (2009) Detection of predation using qPCR: effect of prey quantity, elapsed time, chaser diet, and sample preservation on detectable quantity of prey DNA. J Insect Sci 9:41

    Article  Google Scholar 

  • Wei CF, Gao M, Huang Q, Che FC, Yang JH, Xie DT, Cai ZC, Xu H (2000) Effects of tillage-cropping systems on methane emissions from year-round flooded paddy field in southwest China. Acta Pedolog Sin 37:157–165 (In Chinese with English abstract)

    CAS  Google Scholar 

  • Yang TB, Liu J, Yuan LY, Zhang Y, Li DQ, Agnarsson I, Chen J (2017) Molecular identification of spiders preying on Empoasca vitis in a tea plantation. Sci Rep 7:7784

    Article  Google Scholar 

  • Yang TB, Liu J, Chen J (2020) Compared with conventional PCR assay, qPCR assay greatly improves the detection efficiency of predation. Ecol Evol 10:7713–7722

    Article  Google Scholar 

  • You MS, Hou YM, Liu YF, Yang G, Li ZS, Cai HJ (2004) Non-crop habitat manipulation and integrated pest management in agroecosystems. Acta Entomol Sin 47:260–268 (In Chinese with English abstract)

    Google Scholar 

  • Yuan X, Zhao WC, Cheng JA, Zhu ZR (2014) Monoclonal antibody: a powerful tool for quantitatively evaluating predatory function. Chin J Appl Entomol 51:292–298 (In Chinese with English abstract)

    CAS  Google Scholar 

  • Zhang GF, Lü ZC, Wan FH, Lövel GL (2007) Real-time PCR quantification of Bemisia tabaci (Homoptera: Aleyrodidae) B-biotype remains in predator guts. Mol Ecol Notes 7:947–954

    Article  CAS  Google Scholar 

  • Zhang J, Zheng X, Jian H, Qin XW, Yuan FH, Zhang RJ (2013) Arthropod biodiversity and community structures of organic rice ecosystems in Guangdong province, China. Florida Entomol 96:1–9

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by National Natural Science Foundation of China (31772161). We thank Dr. David Stanley (the USDA/Agricultural Research Service Biological Control of Insects Research Laboratory, USA) for revising and reviewing the early draft of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yaoyu Bai.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised due to some errors were found in the 3rd paragraph of results section and corrected in this version.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (docx 92 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, J., Pang, S., Wang, X. et al. Molecular quantification of spider preying on springtails in winter-spring fallow waterlogged paddy fields. Appl Entomol Zool 56, 165–172 (2021). https://doi.org/10.1007/s13355-020-00712-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-020-00712-8

Keywords

Navigation