Skip to main content
SpringerLink
Log in

The influence of aphids (Myzus persicae) and pink lady beetle larvae (Coleomegilla maculata) on host plant preference of imported cabbageworm (Pieris rapae)

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Oviposition decisions by herbivorous insects hinge on multiple factors, with some of the most important being enemy-free space and competition for resources. It is important to understand whether and how herbivores and predators can influence the maternal egg-laying preference when they are alone and in combination with host plants. Here, we evaluate whether the presence of aphids (a competitor) or a lady beetle larvae (a predator) influence host plant selection by an ovipositing butterfly. Canola (Brassica napus L.) was the highest quality of three putative Brassicaceae host plants for aphids Myzus persicae (Sulzer) (Hemiptera: Aphididae), while the butterfly Pieris rapae (L.) (Lepidoptera: Pieridae) showed similar survival on all. Canola was used to determine that the presence of a competitor herbivore (aphids) had no effect on butterfly oviposition behavior. However, predators significantly influenced the number of eggs laid on the plants, especially on those plants that had both aphids and a lady beetle larva present in combination. We expect that adult female P. rapae did not lay their eggs on the treatment that involved both herbivorous competition and predation risk, due to the combined risk factors along with the volatile chemicals and aphid alarm pheromones emitted on those plants that contained both the aphids and lady beetle larva.

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

Similar content being viewed by others

References

  • Andaloro JT, Rose KB, Shelton AM, Hoy CW, Becker RF (1983) Cabbage growth stages. New York’s Food Life Sci Bull. 101. http://fls.cals.cornell.edu/OCRPDF/101a.pdf

  • Ashby JW, Pottinger RP (2012) Natural regulation of Pieris rapae Linnaeaus (Lepidoptera: Pieridae) in Canterbury, New Zealand. N Z J Agric Res 17(2):229–239. doi:10.1080/00288233.1974.10421002

    Article  Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:814–844. doi:10.1146/annurev.ento.47.091201.145300

    Article  Google Scholar 

  • Baker JR (1982) Insect and related pests of flowers and foliage plants. The North Carolina Agricultural Extension Service, Pp 75

    Google Scholar 

  • Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892. doi:10.2307/1941237

    Article  Google Scholar 

  • Carlson DG, Daxenbichler ME, Tookey HL (1987) Glucosinolates in turnip tops and roots: cultivars grown for greens and/or roots. J Am Soc Hortic Sci 112:179–183

    CAS  Google Scholar 

  • Cippollini D (2002) Variation in the expression of chemical defenses in Alliaria petiolate (Brassicaceae) in the field and common garden. Am J Bot 89(9):1422–1430. doi:10.3732/ajb.89.9.1422

    Article  Google Scholar 

  • Ciska E, Martyniak-Przybyszekska B, Kozlowska H (2000) Content of glucosinolates in cruciferous vegetables grown at the same site for two years under different climatic conditions. J Agric Food Chem 48:2862–2867. doi:10.1021/jf981373a

    Article  CAS  PubMed  Google Scholar 

  • Craig TP, Itami JK, Price PW (1989) A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70:1691–1699

    Article  Google Scholar 

  • Dempster JP (1967) The control of Pieris rapae with DDT. I. The natural mortality of the young stages of Pieris. J Appl Ecol 4(2):485–500

    Article  Google Scholar 

  • De-Silva DL, Vasquez AS, Mallet J (2011) Selection for enemy-free space: eggs placed away from the host plant increase survival of a neotropical ithomiine butterfly. Ecol Entomol 36:667–672. doi:10.1111/j.1365-2311.2011.01310.x

    Article  Google Scholar 

  • Desneux N, Ramirez-Romero R (2009) Plant characteristics mediated by growing conditions can impact parasitoid’s ability to attack host aphids in winter canola. J Pest Sci 82:335–342. doi:10.1007/s10340-009-0258-9

    Article  Google Scholar 

  • Dicke M (2000) Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective. Biol Syst Ecol 28:601–617. doi:10.1016/S0305-1978(99)00106-4

    Article  CAS  Google Scholar 

  • Dixon AFG (1998) Aphid Ecology. Chapman & Hall, London

    Google Scholar 

  • Evans EW (2009) Lady beetles as predators of insects other than Hemiptera. Biol Control 51:255–267. doi:10.1016/j.biocontrol.2009.05.011

    Article  Google Scholar 

  • Goncalves-Souza T, Omena PM, Souza JC, Romero GQ (2008) Trait-mediated effects on flowers: artificial spiders deceive pollinators and decrease plant fitness. Ecology 89(9):2407–2413

    Article  PubMed  Google Scholar 

  • Harcourt DG (1963) Biology of cabbage caterpillars in eastern Ontario. Proc Entomol Soc Ontario. 93:61–75

    Google Scholar 

  • Heisswolf A, Obermaier E, Poethke HJ (2005) Selection of large host plants for oviposition in a monophagous leaf beetle: Nutritional quality or enemy-free space? Ecol Entomol 30:299–306. doi:10.1111/j.0307-6946.2005.00706.x

    Article  Google Scholar 

  • Herbert SL, Jia L, Goggin FL (2007) Quantitative differences in aphid virulence and foliar symptom development on tomato plants carrying the Mi resistance gene. Environ Entomol 36:458–467. doi:10.1093/ee/36.2.458

    Article  Google Scholar 

  • Hopkins RJ, van Loon JJA (2001) The effect of host acceptability on oviposition accumulation by the small white butterfly, Pieris rapae. Physiol Entomol 26:149–157. doi:10.1046/j.1365-3032.2001.00228.x

    Article  Google Scholar 

  • Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Ann Rev Entomol 54:57–83. doi:10.1146/annurev.ento.54.110807.090623

    Article  CAS  Google Scholar 

  • Ives PM (1978) How discriminating are cabbage butterflies? Aust J Ecol 3:261–276

    Article  Google Scholar 

  • Jaenike J (1978) On optimal oviposition behaviour in phytophagous insects. Theor Popul Biol 14:350–356

    Article  CAS  PubMed  Google Scholar 

  • Johnson WT, Lyon HH (1988) Insects that feed on trees and shrubs, 2nd edn. Cornell University Press, New York, p 556

    Google Scholar 

  • Kushad MMAF, Brown AC, Kurilich JA, Juvik B, Klein MA, Wallig EH Jeffery (1999) Variation of glucosinolates in vegetables subspecies of Brassica oleracea. J Food Agric Chem 47:1541–1548. doi:10.1021/jf980985s

    Article  CAS  Google Scholar 

  • Layman ML, Lundgren JG (2015) Mutualistic and antagonistic trophic interactions in canola: the role of aphids in shaping pest and predator populations. Biol Control 91:62–70

    Article  Google Scholar 

  • Lundgren JG, Heimpel GE, Bomgren SA (2002) Comparisons of Trachogramma brassicae (Hymenoptera: Trichogrammatidae) augmentation with organic and synthetic pesticides for control of cruciferous Lepidoptera. Enviorn Entomol 31(6):1231–1239. doi:10.1603/0046-225X-31.6.1231

    Article  CAS  Google Scholar 

  • Lundgren JG, Moser SE, Hellmich RL, Seagraves MP (2011) Effects of diet on herbivory by a predacious lady beetle. Biocontrol Sci Technol 21(1):71–74. doi:10.1080/09583157.2010.524917

    Article  Google Scholar 

  • Ma WC, Schoonhoven LM (1973) Tarsal contract chemosensory hairs of the large white butterfly, Pieris rapae, and their possible role in oviposition behaviour. Entomol Exp Appl 16:343–357

    Article  Google Scholar 

  • Miller JR, Strickler KL (1984) Finding and accepting host plants. Chemical ecology of insects. Chapman and Hall, London, pp 127–157

    Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. TREE 13(10):403–407. doi:10.1016/S0169-5347(98)01472-4

    CAS  PubMed  Google Scholar 

  • Ngu VQ, Zevenbergen M, Bruinsma M, van Loom J (2008) How do plant defense compounds influence the oviposition behavior of small cabbage white butterfly Pieris rapae (Linnaeus)? J Sci Devel. April:75–82

  • Nishida R (1995) Oviposition stimulants of swallowtail butterflies. Their Ecology and Evolutionary Biology. Scientific Publishers, Gainesville, pp 17–26

    Google Scholar 

  • Palaniswamy P, Lamb RJ (1993) Wound-induced antixenotic resistance to flea beetles Phyllotreta cruciferae Goeze (Coleoptera: Chyrsomleidae) in crucifers. Can Entomol 125:903–912

    Article  Google Scholar 

  • Pickett JA, Wadhams LJ, Woodcock CM, Hardie J (1992) The chemical ecology of aphids. Ann Rev Entomol 37:67–90. doi:10.1146/annurev.en.37.010192.000435

    Article  CAS  Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AW (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • Pumarinno L, Alomar O, Lundgren JG (2012) Effects of floral and extrafloral resource diversity on the fitness of an omnivorous bug, Orius insidiosus. Entomol Exp App 145:181–190. doi:10.1111/eea.12002

    Article  Google Scholar 

  • Qureshi JA, Michaud JP (2005) Interactions among three species of cereal aphids simultaneously infesting wheat. J Insect Sci 5:8. doi:10.1093/jis/5.1.13

    Article  Google Scholar 

  • Raven PH, Johnson GB, Manson K, Losos J, Singer S (2013) Biology, 10th edn. New York, McGraw-Hill

    Google Scholar 

  • Renwick JAA, Chew FS (1994) Oviposition behavior in Lepidoptera. Ann Rev Entomol 39:377–400. doi:10.1146/annurev.en.39.010194.002113

    Article  Google Scholar 

  • Renwick JAA, Radke CD, Sachdev-Gupta K, Stadler E (1992) Leaf surface chemicals stimulating oviposition by Pieris rapae (Lepidoptera: Pieridae) on cabbage. Chemoecology 3:33–38. doi:10.1007/BF01261454

    Article  CAS  Google Scholar 

  • Richards OW (1940) The biology of the small white butterfly (Pieris rapae), with special reference to the factors controlling its abundance. J Anim Ecol 9(2):243–288

    Article  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primary of trait-mediated indirect interactions. Ecol Lett 7:153–163. doi:10.1111/j.1461-0248.2003.00560.x

    Article  Google Scholar 

  • Seagraves MP (2009) Lady beetle oviposition behavior in response to the trophic environment. Biol Control 51:313–322. doi:10.1016/j.biocontrol.2009.05.015

    Article  Google Scholar 

  • Seagraves MP, Yeargan KV (2006) Selection and evaluation of a companion plant to indirectly augment densities of Coleomegilla maculata (Coleoptera: Coccinellidae) in sweet corn. Environ Entomol 35(5):1334–1341. doi:10.1093/ee/35.5.1334

    Article  Google Scholar 

  • Sendoya SF, Freitas AVL, Oliveira PS (2009) Egg-laying butterflies distinguish predaceous ants by sight. Am Nat 174(1):134–140

    Article  PubMed  Google Scholar 

  • Siemens DH, Mitchell-Olds T (1996) Glucosinolates and herbivory specialists (Coleoptera: Chrysomelidae, Lepidoptera: Plutellidae): consequences of concentration and induced resistance. Environ Entomol 25:1334–1353. doi:10.1093/ee/25.6.1344

    Article  Google Scholar 

  • Stein SJ, Price PW (1995) Relative effects or plant resistance and natural enemies by plant developmental age on sawfly (Hymenoptera: Tenthredinidae) preference and performance. Environ Entomol 24(4):909–916. doi:10.1093/ee/24.4.909

    Article  Google Scholar 

  • Thompson JN (1988) Coevolution and alternative hypothesizes on insect/plant interactions. Ecology 69:893–895

    Article  Google Scholar 

  • Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89. doi:10.1146/annurev.en.36.010191.000433

    Article  Google Scholar 

  • Traw MB, Dawson TE (2002) Reduced performance of two specialist herbivores (Lepidoptera: Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environ Entomol 34(4):712–722. doi:10.1603/0046-225X-31.4.714

    Google Scholar 

  • Van Dam NM, Raaijmakers CE, Van Der Putten WH (2005) Root herbivory reduces growth and survival rate of the shoot feeding specialist Pieris rapae on Brassica nigra. Entomol Exp Appl 115(1):161–170. doi:10.1111/j.1570-7458.2005.00241.x

    Article  Google Scholar 

  • van Emden HF, Eastop VF, Hughs RD, Way MJ (1969) The ecology of Myzus persicae. Ann Rev Entomol 14:192–270. doi:10.1146/annurev.en.14.010169.001213

    Google Scholar 

  • van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent completion, quantitative food webs, and the structure of phytophagous insect communities. Ann Rev Entomol 51:187–208

    Article  Google Scholar 

  • VanEtten CH, Daxenbichler ME, Williams PH, Kwolek F (1976) Glucosinolates and derived products in cruciferous vegetables. Analysis of the edible part from twenty-two varieties of cabbage. J Agric Food Chem 24:452–455. doi:10.1021/jf60205a049

    Article  CAS  PubMed  Google Scholar 

  • Visser JH (1986) Host odor perception in phytophagous insects. Annu Rev Entomol 31:121–144. doi:10.1146/annurev.en.31.010186.001005

    Article  Google Scholar 

  • Wiklund C (1975) The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon. Oecologia 18:185–197. doi:10.1007/BF00345421

    Article  Google Scholar 

  • Wiklund C (1984) Egg-laying patterns in butterflies in relation to their phenology and the visual apparentcy and abundance of their host plants. Oecologia 63:23–29. doi:10.1007/BF00379780

    Article  Google Scholar 

  • Wiklund C, Friberg M (2008) Enemy-free space and habitat-specific host specialization in a butterfly. Oecologia 157:287–294. doi:10.1007/s00442-008-1077-z

    Article  PubMed  Google Scholar 

  • Wool D (2004) Galling aphids: specialization, biological complexity, and variation. Ann Rev Entomol 49:175–192. doi:10.1146/annurev.ento.49.061802.123236

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Greta Schen, Laurène Freydier, Cally Strobel, and Nicole Berg for their technical assistance in carrying out this project. Claire Bestul, Nathan Koens, Meagan Abraham, Nicole Schultz, and Mark Longfellow assisted with catching the butterflies used throughout this experiment. We thank Dr. Emilie Snell-Rood (University of Minnesota), Dr. Nate Morehouse (University of Pittsburgh), and Dr. Joel Kingsolver (The University of North Carolina) for their guidance and helpful tips in rearing P. rapae. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture.

Author information

Authors and Affiliations

  1. Biology Microbiology Department, South Dakota State University, Brookings, SD, 57007, USA

    Marissa L. Layman

  2. North Central Agricultural Research Laboratory, USDA-ARS, 2923 Medary Avenue, Brookings, SD, 57006, USA

    Jonathan G. Lundgren

Authors
  1. Marissa L. Layman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan G. Lundgren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan G. Lundgren.

Additional information

Communicated by Robert Glinwood.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Layman, M.L., Lundgren, J.G. The influence of aphids (Myzus persicae) and pink lady beetle larvae (Coleomegilla maculata) on host plant preference of imported cabbageworm (Pieris rapae). Arthropod-Plant Interactions 9, 507–514 (2015). https://doi.org/10.1007/s11829-015-9392-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-015-9392-x

Keywords

Search

Navigation