Skip to main content

Advertisement

SpringerLink
Log in

Buckwheat strip crops increase parasitism of Apolygus lucorum in cotton

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Cropping system diversification, including the in-field establishment of strip crops can improve the effectiveness of natural enemies and enhance biological control of pestiferous herbivores. In China, habitat management such as the in-field establishment of alfalfa strips is used for pest control in cotton. However, their effect on other economically important pests, such as the mirid bug Apolygus lucorum (Meyer-Dür), has not been evaluated. In this study, we first assessed parasitism of A. lucorum within plots of 13 different host plant species. Next, we established strips of one suitable plant species within a commercial cotton field and evaluated its effect on A. lucorum parasitism level. The results showed that two A. lucorum parasitoids, i.e., Peristenus spretus Chen et van Achterberg and Peristenus relictus Ruthe, responded differently to host plant species. In 2014, the parasitism levels of P. spretus were highest on buckwheat Fagopyrum esculentum Moench, while parasitism levels of P. relictus were generally low and did not differ between the various plants. Furthermore, A. lucorum attained low population levels on buckwheat. In 2016, A. lucorum parasitism levels in buckwheat plots were higher than in cotton. When (2 m wide) buckwheat strips were established in cotton fields, P. spretus parasitism of A. lucorum on cotton plants increased 2.4-fold in 2016 and 8.5-fold in 2017 compared to cotton monocrops. In conclusion, the establishment of buckwheat strips in commercial cotton fields enhances A. lucorum parasitism. By deploying these habitat management tactics, parasitoid-mediated biological control may complement existing management schemes for the polyphagous mirid bug in China and abroad.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Agusti N, Bourguet D, Spataro T, Delos M, Eychenne N, Folcher L, Arditi R (2005) Detection, identification and geographical distribution of European corn borer larval parasitoids using molecular markers. Mol Ecol 14:3267–3274

    Article  CAS  PubMed  Google Scholar 

  • Araj S, Wratten S, Lister A, Buckley HL (2006) Floral nectar affects longevity of the aphid parasitoid Aphidius ervi and its hyperparasitoid Dendrocerus aphidum. N Z Plant Prot 59:178–183

    Google Scholar 

  • Ashfaq M, Braun L, Hegedus D, Erlandson ME (2004) Estimating parasitisim levels in Lygus spp. (Hemiptera: Miridae) field populations using standard and molecular techniques. Biocontrol Sci Technol 14:731–735

    Article  Google Scholar 

  • Bach CE, Tabashnik BE (1990) Effects of nonhost plant neighbors on population densities and parasitism rates of the diamondback moth (Lepidoptera: Plutellidae). Environ Entomol 19:987–994

    Article  Google Scholar 

  • Baggen LR, Gurr GM (1998) The Influence of food on Copidosoma koehleri (Hymenoptera: Encyrtidae), and the use of flowering plants as a habitat management tool to enhance biological control of potato moth, Phthorimaea operculella (Lepidoptera: Gelechiidae). Biol Control 11:9–17

    Article  Google Scholar 

  • Baggen LR, Gurr GM, Meats A (1999) Flowers in tritrophic systems: mechanisms allowing selective exploitation by insect natural enemies for conservation biological control. Entomol Exp Appl 91:156–161

    Article  Google Scholar 

  • Berndt LA, Wratten SD, Hassan PG (2002) Effects of buckwheat flowers on leafroller (Lepidoptera: Tortricidae) parasitoids in a New Zealand vineyard. Agric For Entomol 4:39–45

    Article  Google Scholar 

  • Cappuccino N, Houle MJ, Stein J (1999) The influence of understory nectar resources on parasitism of the spruce budworm Choristoneura fumiferana in the field. Agric Forest Entomol 1:33–36

    Article  Google Scholar 

  • Carignan S, Stewart RK, Godin C, Boivin G (2007) Parasitism activity of Peristenus spp. (Hymenoptera: Braconidae) on Lygus lineolaris (Hemiptera: Miridae) nymphs prior to the establishment of P. digoneutis in southwestern Quebec. Biocontrol Sci Technol 17:623–633

    Article  Google Scholar 

  • Clough Y, Kruess A, Tscharntke T (2007) Local and landscape factors in differently managed arable fields affect the insect herbivore community of a non-crop plant species. J Appl Ecol 44:22–28

    Article  Google Scholar 

  • Day WH (1994) Estimating mortality caused by parasites and diseases of insects: comparisons of the dissection and rearing methods. Environ Entomol 23:543–550

    Article  Google Scholar 

  • Day WH (1996) Evaluation of biological control of the tarnished plant bug (Hemiptera: Miridae) in alfalfa by the introduced parasite Peristenus digoneutis (Hymenoptera: Braconidae). Environ Entomol 25:512–518

    Article  Google Scholar 

  • Day WH, Hedlund RC, Saunders LB, Coutinot D (1990) Establishment of Peristenus digoneutis (Hymenoptera: Braconidae), a parasite of the tarnished plant bug (Hemiptera: Miridae), in the United States. Environ Entomol 19:1528–1533

    Article  Google Scholar 

  • Delaquis E, de Haan S, Wyckhuys KAG (2018) On-farm diversity offsets environmental pressures in tropical agro-ecosystems: a synthetic review for cassava-based systems. Agric Ecosyst Environ 251:226–235

    Article  Google Scholar 

  • Folmer O, Black MB, Hoeh W, Lutz RC, 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  PubMed  Google Scholar 

  • Foti MC, Peri E, Wajnberg E, Colazza S, Rostas M (2019) Contrasting olfactory responses of two egg parasitoids to buckwheat floral scent is reflected in field parasitism rates. J Pest Sci 92:747–756

    Article  Google Scholar 

  • Gariepy TD, Kuhlmann U, Gillott C, Erlandson M (2007) Parasitoids, predators and PCR: the use of diagnostic molecular markers in biological control of arthropods. J Appl Entomol 131:225–240

    Article  CAS  Google Scholar 

  • Greenstone MH (2006) Molecular methods for assessing insect parasitism. Bull Entomol Res 96:1–13

    Article  CAS  PubMed  Google Scholar 

  • Gurr GM, Wratten SD (2000) Biological control: measures of success. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Gurr GM, Wratten SD, Luna JM (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl Ecol 4:107–116

    Article  Google Scholar 

  • Haye T, Kuhlmann U, Goulet H, Mason PG (2006) Controlling Lygus plant bugs (Heteroptera: Miridae) with European Peristenus relictus (Hymenoptera: Braconidae) in Canada—risky or not? Bull Entomol Res 96:187–196

    Article  CAS  PubMed  Google Scholar 

  • Heimpel GE, Jervis MA (2005) Does floral nectar improve biological control by parasitoids? In: Wackers FL, van Rijin PCJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 267–304

    Chapter  Google Scholar 

  • Isbell F, Adle PR, Eisenhauer N, Fornara D, Kimmel K, Kremen C, Letourneau DK, Liebman M, Polley HW, Quijas S, Scherer-Lorenzen M (2010) Benefits of increasing plant diversity in sustainable agroecosystems. J Ecol 105:871–879

    Article  Google Scholar 

  • Jiang YY, Lu YH, Zeng J (2015) Forecast and management of mirid bugs in multiple agroecosystems of China. China Agricultural Science Press, Beijing

    Google Scholar 

  • Khan ZR, Ampong-Nyarko K, Chiliswa P, Hassanali A, Kimani S, Lwande W, Overholt WA, Picketta JA, Smart LE (1997) Intercropping increases parasitism of pests. Nature 388:631–632

    Article  CAS  Google Scholar 

  • Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    Article  CAS  PubMed  Google Scholar 

  • Lee JC, Heimpel GE (2003) Nectar availability and parasitoid sugar feeding. In: van Driesche RG (ed) Proceedings of the 1st international symposium on biological control of arthropods, pp. 220--225, USDA Forest Service, Honolulu, USA

  • Lee JC, Heimpel GE (2005) Impact of flowering buckwheat on Lepidopteran cabbage pests and their parasitoids at two spatial scales. Biol Control 34:290–301

    Article  Google Scholar 

  • Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, Escobar S, Galindo V, Gutiérrez C, López SD, Mejía JL, Rangel AMA, Rangel JH, Rivera L, Saavedra CA, Torres AM, Trujilo AR (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21

    Article  PubMed  Google Scholar 

  • Lu YH (2008) Studies on ecological adaptability of the mirids. PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing, China

  • Lu YH, Wu KM (2011) Mirid bugs in China: pest status and management strategies. Outlooks Pest Manag 22:248–252

    Article  Google Scholar 

  • Lu YH, Wu KM, Jiang YY, Xia B, Li P, Feng HQ, Wyckhuys KAG, Guo YY (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328:1151–1154

    Article  CAS  PubMed  Google Scholar 

  • Luo SP (2013) Study on nymphal parasitoids of mirid bugs. Post-doctoral report. Chinese Academy of Agricultural Sciences, Beijing

    Google Scholar 

  • Luo SP, Li HM, Lu YH, Zhang F, Haye T, Kuhlmann U, Wu KM (2014a) Functional response and mutual interference of Peristenus spretus (Hymenoptera: Braconidae), a parasitoid of Apolygus lucorum (Heteroptera: Miridae). Biocontrol Sci Technol 24(3):247–256

    Article  Google Scholar 

  • Luo SP, Naranjo SE, Wu KM (2014b) Biological control of cotton pests in China. Biol Control 68:6–14

    Article  Google Scholar 

  • Luo SP, Zhang F, Wu KM (2015) Effect of temperature on the reproductive biology of Peristenus spretus (Hymenoptera: Braconidae), a biological control agent of the plant bug Apolygus lucorum (Hemiptera: Miridae). Biocontrol Sci Technol 25:1410–1425

    Article  Google Scholar 

  • Luo SP, Zhang F, Wu KM (2017) Interspecific competition between Peristenus spretus and Peristenus relictus (Hymenoptera: Braconidae), larval parasitoids of Apolygus lucorum (Hemiptera: Miridae). Biol Control 117:115–122

    Article  Google Scholar 

  • Pan HS, Lu YH, Wyckhuys KAG, Wu KM (2013) Preference of a polyphagous mirid bug, Apolygus lucorum (Meyer-Dür) for flowering host plants. PLoS ONE 8(7):e68980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan HS, Liu B, Lu YH (2019) Host-plant switching promotes the population growth of Apolygus lucorum: implications for laboratory rearing. Bull Entomol Res 109(3):1–7

    Article  Google Scholar 

  • Pickett CH, Rodriguez R, Brown J, Coutinot D, Hoelmer KA, Kuhlmann U, Goulet H, Schwartz MD, Goodell P (2007) Establishment of Peristenus digoneutis and P. relictus (Hymenoptera: Braconidae) in California for the control of Lygus spp. (Heteroptera: Miridae). Biocontrol Sci Technol 17:261–272

    Article  Google Scholar 

  • Stephens MJ, France CM, Wratten SD, Frampton C (1998) Enhancing biological control of leafrollers (Lepidoptera: Tortricidae) by sowing buckwheat (Fagopyrum esculentum) in an orchard. Biocontrol Sci Technol 8:547–558

    Article  Google Scholar 

  • Tilmon KJ, Danforth BN, Day WH, Hoffmann MP (2000) Determining parasitoid species composition in a host population: a molecular approach. Ann Entomol Soc Am 93:640–647

    Article  CAS  Google Scholar 

  • Tittonell P (2014) Ecological intensification of agriculture-sustainable by nature. Curr Opin Env Sustain 8:53–61

    Article  Google Scholar 

  • Traugott M, Bell JR, Broad GR, Powell W, Veen FJFV, Vollhardt IMG, Symondson WOC (2008) Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community. Mol Ecol 17:3928–3938

    Article  CAS  PubMed  Google Scholar 

  • Wäckers FL, van Rijn P (2012) Pick and mix: selecting flowering plants to meet the requirements of target biological control insects. Wiley, Hoboken

    Google Scholar 

  • Wäckers FL, Romeis J, van Rijn P (2007) Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annu Rev Entomol 52:301–323

    Article  PubMed  CAS  Google Scholar 

  • Winkler K, Wäckers FL, Kaufman LV, Larraz V, van Lenteren JL (2009) Nectar exploitation by herbivores and their parasitoids is a function of flower species and relative humidity. Biol Control 50:299–306

    Article  Google Scholar 

  • Wyckhuys KAG, Lu YH, Morales H, Vazquez LL, Legaspi JC, Eliopoulos PA, Hernandez LM (2013) Current status and potential of conservation biological control for agriculture in the developing world. Biol Control 65:152–167

    Article  Google Scholar 

  • Xie HC, Chen JL, Cheng DF, Zhou HB, Sun JR, Yong L, Francis F (2012) Impact of wheat-mung bean intercropping on English grain aphid (Hemiptera: Aphididae) populations and its natural enemy. J Econ Entomol 105:854–859

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

This work was supported by the National Key Research and Development Program of China (2017YFD0201003-22), China Agriculture Research System (CARS-15-19), National Natural Science Funds of China (31621064) and the funding from MoA-CABI Joint Laboratory for Bio-safety.

Author information

Authors and Affiliations

  1. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

    Jinhua Li, Bing Liu, Shuping Luo, Kris A. G. Wyckhuys & Yanhui Lu

  2. College of Agronomy, Jilin Agricultural University, Changchun, China

    Jinhua Li & Haibin Yuan

  3. Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences, Urumqi, China

    Hongsheng Pan

Authors
  1. Jinhua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hongsheng Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuping Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kris A. G. Wyckhuys
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Haibin Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yanhui Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yanhui Lu.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Stefano Colazza

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 403 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, J., Liu, B., Pan, H. et al. Buckwheat strip crops increase parasitism of Apolygus lucorum in cotton. BioControl 64, 645–654 (2019). https://doi.org/10.1007/s10526-019-09961-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-019-09961-1

Keywords

Search

Navigation