Skip to main content
SpringerLink
Log in

Potential for exploitative competition, not intraguild predation, between invasive harlequin ladybirds and flowerbugs in urban parks

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

In aphidophagous insect communities invaded by the harlequin ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), intraguild predation (IGP) is widely implicated in the displacement of native predators, however, indirect trophic interactions are rarely assessed. Using molecular gut-content analysis, we investigated the relative frequencies of IGP by H. axyridis on the predatory flowerbug Anthocoris nemoralis Fabricius (Heteroptera: Anthocoridae) and prey overlap for a shared prey, the lime aphid Eucallipterus tiliae L. (Hemiptera: Aphididae), in Tilia × europaea crowns in urban parks. The frequency of IGP by H. axyridis was low: 2.7 % of larvae and 3.4 % of adults tested positive for A. nemoralis DNA. The presence of lime aphid DNA in predators was higher: 56.5 and 47.9 % of H. axyridis larvae and adults, respectively, contained E. tiliae DNA, whereas 60.8 % of adult A. nemoralis tested positive for aphid DNA. Incorporating insect densities revealed that the density of H. axyridis larvae had a strong negative effect on the likelihood of detecting aphid DNA in A. nemoralis. Prey overlap for E. tiliae was widespread in space (2–13 m height in tree crowns) and time (May–October 2011) which suggests that interspecific exploitative competition, mediated by predator life-stage, more so than IGP, is an important indirect trophic interaction between co-occurring H. axyridis and A. nemoralis. Whether exploitative competition equates to displacement of A. nemoralis populations requires further investigation. Our results emphasize the need to incorporate indirect interactions in studies of insect communities following invasion, not least because they potentially affect more species than direct interactions alone.

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

Similar content being viewed by others

References

  • Adriaens T, Branquart E, Maes D (2003) The multicoloured Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), a threat for native aphid predators in Belgium? Belg J Zool 133:195–196

    Google Scholar 

  • Adriaens T, San M, Maes D (2008) Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. Biocontrol 53:69–88

    Article  Google Scholar 

  • Aebi A, Brown PM, De Clercq P, Hautier L, Howe A, Ingels B, Ravn HP, Sloggett JJ, Zindel R, Thomas A (2011) Detecting arthropod intraguild predation in the field. Biocontrol 56:429–440

    Article  Google Scholar 

  • Alford DV (2002) Pests of ornamental trees, shrubs and flowers. Manson Publishing Ltd., London

    Google Scholar 

  • Alhmedi A, Haubruge E, Francis F (2010) Intraguild interactions implicating invasive species: Harmonia axyridis as a model species. Biotechnol Agron Soc Environ 14:187–201

    Google Scholar 

  • Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biol Invasions 6:463–471

    Article  Google Scholar 

  • Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122

    Article  Google Scholar 

  • Anderson NH (1962) Bionomics of six species of Anthocoris (Heteroptera: Anthocoridae) in England. Trans R Entomol Soc Lond 114:67–95

  • Armstrong RA, Mcgehee R (1980) Competitive-exclusion. Am Nat 115:151–170

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-6

  • Brown JS, Kotler BP, Mitchell WA (1994) Foraging theory, patch use, and the structure of a Negev Desert granivore community. Ecology 75:2286–2300

    Article  Google Scholar 

  • Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN (2008) Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. Biocontrol 53:55–67

    Article  Google Scholar 

  • Brown PMJ, Frost R, Doberski J, Sparks T, Harrington R, Roy HE (2011a) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol Entomol 36:231–240

    Article  Google Scholar 

  • Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Handley LJL (2011b) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56:623–641

    Article  Google Scholar 

  • Brown PMJ, Ingels B, Wheatley A, Rhule EL, de Clercq P, van Leeuwen T, Thomas A (2015) Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples. Entomol Sci 18:130–133

    Article  Google Scholar 

  • Chapin JB, Brou VA (1991) Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proc Entomol Soc Wash 93:630–635

    Google Scholar 

  • Chen Y, Giles KL, Payton ME, Greenstone MH (2000) Identifying key cereal aphid predators by molecular gut analysis. Mol Ecol 9:1887–1898

    Article  CAS  PubMed  Google Scholar 

  • Crowder DW, Snyder WE (2010) Eating their way to the top? Mechanisms underlying the success of invasive insect generalist predators. Biol Invasions 12:2857–2876

    Article  Google Scholar 

  • Dixon AFG (1971a) Role of aphids in wood formation. 2. Effect of lime aphid, Eucallipterus tiliae L. (Aphididae), on growth of lime, Tilia x vulgaris Hayne. J Appl Ecol 8:393

    Article  Google Scholar 

  • Dixon AFG (1971b) Role of intra-specific mechanisms and predation in regulating numbers of lime aphid, Eucallipterus tiliae L. Oecologia 8:179

    Article  Google Scholar 

  • Dixon AFG (1998) Aphid ecology: an optimization approach. Chapman & Hall, London

    Google Scholar 

  • Dixon AFG, Russel RJ (1972) Effectiveness of Anthocoris nemorum and A. Confusus (Hemiptera: Anthocoridae) as predators of sycamore aphid, Drepanosiphum platanoides. 2. Searching behavior and incidence of predation in field. Entomol Exp Appl 15:35

    Article  Google Scholar 

  • Evans EW, Soares AO, Yasuda H (2011) Invasions by ladybugs, ladybirds, and other predatory beetles. Biocontrol 56:597–611

    Article  Google Scholar 

  • Foltan P, Sheppard S, Konvicka M, Symondson WOC (2005) The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR. Mol Ecol 14:4147–4158

    Article  CAS  PubMed  Google Scholar 

  • Foottit RG, Maw HEL, Von Dohlen CD, Hebert PDN (2008) Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Mol Ecol Resour 8:1189–1201

    Article  CAS  PubMed  Google Scholar 

  • Gagnon AE, Brodeur J (2014) Impact of plant architecture and extraguild prey density on intraguild predation in an agroecosystem. Entomol Exp Appl 152:165–173

    Article  Google Scholar 

  • Gagnon AE, Doyon J, Heimpel GE, Brodeur J (2011a) Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species. Mol Ecol Resour 11:1022–1032

    Article  CAS  PubMed  Google Scholar 

  • Gagnon AE, Heimpel GE, Brodeur J (2011b) The ubiquity of intraguild predation among predatory arthropods. Plos One 6(11):e28061

  • Greenstone MH, Payton ME, Weber DC, Simmons AM (2014) The detectability half-life in arthropod predator–prey research: what it is, why we need it, how to measure it, and how to use it. Mol Ecol 23:3799–3813

    Article  PubMed  Google Scholar 

  • Harmon JP, Stephens E, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. J Insect Conserv 11:85–94

    Article  Google Scholar 

  • Hautier L, Martin GS, Callier P, de Biseau JC, Gregoire JC (2011) Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol Invasions 13:1805–1814

    Article  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, de Waard JR (2003) Biological Identifications through DNA Barcodes. Proceedings: Biological Sciences: 270(1512):313–321

  • Hironori Y, Katsuhiro S (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163

    Article  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  PubMed  Google Scholar 

  • Hoogendoorn M, Heimpel GE (2004) Competitive interactions between an exotic and a native ladybeetle: a field cage study. Entomol Exp Appl 111:19–28

    Article  Google Scholar 

  • Hosseini R, Schmidt O, Keller MA (2008) Factors affecting detectability of prey DNA in the gut contents of invertebrate predators: a polymerase chain reaction-based method. Entomol Exp Appl 126:194–202

    Article  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • Howe AG, Ransijn J, Ravn HP (2015) A sublethal effect on native Anthocoris nemoralis through competitive interactions with Harmonia axyridis. Ecol Entomol. 40:639–649

    Article  Google Scholar 

  • Hoy MA (1994) Insect molecular genetics: an introduction to principals and applications. Academic Press, San Diego

    Google Scholar 

  • Hutchinson GE (1959) Homage to Santa-Rosalia or why are there so many kinds of animals. Am Nat 93:145–159

    Article  Google Scholar 

  • Jackson CH (2011) Multi-state models for panel data: the msm package for R. J Stat Softw 38(8):1–29

    Article  Google Scholar 

  • Janssen A, Sabelis MW, Magalhaes S, Montserrat M, Van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:2713–2719

    Article  PubMed  Google Scholar 

  • Kasper ML, Reeson AF, Cooper SJB, Perry KD, Austin AD (2004) Assessment of prey overlap between a native (Polistes humilis) and an introduced (Vespula germanica) social wasp using morphology and phylogenetic analyses of 16S rDNA. Mol Ecol 13:2037–2048

    Article  CAS  PubMed  Google Scholar 

  • Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Pere C, Cock M, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45

    Article  Google Scholar 

  • Kenis M, Adriaens T, Brown P, Katsanis A Van, Vlaenderen J, Eschen R, Golaz L, Zindel R San, Martin y Gomez G, Babendreier D, Ware R (2010) Impact of Harmonia axyridis on European ladybirds: which species are most at risk? IOBC/WPRS Bull 58:57–59

    Google Scholar 

  • King RA, Read DS, Traugott M, Symondson WOC (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol Ecol 17:947–963

    Article  CAS  PubMed  Google Scholar 

  • Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:32

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. Biocontrol 53:23–35

    Article  Google Scholar 

  • Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  CAS  PubMed  Google Scholar 

  • Labrie G, Lucas E, Coderre D (2006) Can developmental and behavioral characteristics of the multicolored Asian lady beetle Harmonia axyridis explain its invasive success? Biol Invasions 8:743–754

    Article  Google Scholar 

  • Lattin JD (1999) Bionomics of the Anthocoridae. Annu Rev Entomol 44:207–231

    Article  CAS  PubMed  Google Scholar 

  • Lawton JH, Hassell MP (1984) Interspecific competition in insects. In: Huffaker CB, Rabb RL (eds) Ecological entomology. Wiley, New York, pp 451–495

    Google Scholar 

  • Losey JE, Denno RF (1998) Positive predator–predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79:2143–2152

    Google Scholar 

  • Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–363

    Article  Google Scholar 

  • Lucas E, Coderre D, Brodeur J (2000) Selection of molting and pupation sites by Coleomegilla maculata (Coleoptera: Coccinellidae): avoidance of intraguild predation. Environ Entomol 29:454–459

    Article  Google Scholar 

  • Lucas E, Labrie G, Lazarovits G (2007) The multicolour Asian ladybird beetle: beneficial or nuisance organism? In: Vincent C, Goettel MS, Lazarovits G (eds) Biological control: a global perspective. CABI Publishing, Wallingford, pp 38–52

    Chapter  Google Scholar 

  • MacArthur R, Levins R (1967) Limiting similarity convergence and divergence of coexisting species. Am Nat 101:377

    Article  Google Scholar 

  • Meyling NV, Enkegaard A, Brødsgaard H (2003) Two Anthocoris bugs as predators of glasshouse aphids—voracity and prey preference. Entomol Exp Appl 108:59–70

    Article  Google Scholar 

  • Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ Entomol 31:827–835

    Article  Google Scholar 

  • Miura T, Nishimura S (1980) The larval period and predacious activity of an aphidophagous coccinellid, Harmonia axyridis PALLAS. Bull Fac Agric Shimane Univ 14:144–148

    Google Scholar 

  • Mizell RF (2007) Impact of Harmonia axyridis (Coleoptera: Coccinellidae) on native arthropod predators in pecan and crape myrtle. Fla Entomol 90:524–536

    Article  Google Scholar 

  • Nedved O, Fois X, Ungerova D, Kalushkov P (2013) Alien vs. predator—the native lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive ladybird Harmonia axyridis. Bull Insectol 66(1):73–78

    Google Scholar 

  • Noia M, Borges I, Soares AO (2008) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of intra and extraguild prey densities. Biol Control 46:140–146

    Article  Google Scholar 

  • Obrycki JJ, Giles KL, Ormord AM (1998) Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia 117:279–285

    Article  Google Scholar 

  • Osawa N (2000) Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Popul Ecol 42:115–127

    Article  Google Scholar 

  • Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. Biocontrol 53:147–168

    Article  Google Scholar 

  • Péricart J (1996) Family Anthocoridae Fieber. 1836—flower bugs, minute pirate bugs. In: Aukema B, Rieger C (eds) Catalogue of the Heteroptera. Ponsen and Looijen, Wageningen, pp 108–140

    Google Scholar 

  • Persson L, Eklov P (1995) Prey refuges affecting interactions between piscivorous perch and juvenile perch and roach. Ecology 76:70–81

    Article  Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846

    Article  Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation—potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing

  • Raak-van Den Berg CL, De Lange HJ, Van Lenteren JC (2012) Intraguild predation behaviour of ladybirds in semi-field experiments explains invasion success of Harmonia axyridis. Plos One 7(7):e40681

  • Ratnasingham S, Hebert PDN (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 7:355–364

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465

    Article  CAS  PubMed  Google Scholar 

  • Rondoni G, Athey KJ, Harwood JD, Conti E, Ricci R, Obrycki JJ (2014) Development and application of molecular gut-content analysis to detect aphid and coccinellid predation by Harmonia axyridis (Coleoptera: Coccinellidae) in Italy. Insect Sci 00:1–12. doi:10.1111/1744-7917.12165

    Google Scholar 

  • Roy HE, Handley LJL (2012) Networking: a community approach to invaders and their parasites. Funct Ecol 26:1238–1248

    Article  Google Scholar 

  • Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, San Martin G, Brown PMJ, Hautier L, Poland R, Roy DB, Comont R, Eschen R, Frost R, Zindel R, Van Vlaenderen J, Nedved O, Ravn HP, Gregoire JC, de Biseau JC, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725

    Article  Google Scholar 

  • Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator–prey food-webs. Funct Ecol 19:751–762

    Article  Google Scholar 

  • Sigsgaard L (2010) Habitat and prey preferences of the two predatory bugs Anthocoris nemorum (L.) and A. nemoralis (Fabricius) (Anthocoridae: Hemiptera-Heteroptera). Biol Control 53:46–54

    Article  Google Scholar 

  • Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122

  • Southwood TRE, Leston D (1959) Land and water bugs of the British Isles (CD-ROM version). Pisces Conservation Limited, Lymington

    Google Scholar 

  • Thomas AP, Trotman J, Wheatley A, Aebi A, Zindel R, Brown PMJ (2013) Predation of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): detection in Britain by PCR-based gut analysis. Insect Conserv Divers 6:20–27

    Article  Google Scholar 

  • Tilman D (1982) Resource competition and structure. Princeton University Press, Princeton

    Google Scholar 

  • Tomov R, Trencheva K, Trenchev G, Kenis M (2009) The multicolored invasive Asian ladybird Harmonia axyridis (PALLAS, 1773) (Coleoptera: Coccinellidae) new to the fauna of Bulgaria. Acta Zool Bulg 61:307–311

    Google Scholar 

  • Tylianakis JM (2008) Understanding the web of life: the birds, the bees, and sex with aliens. PLoS Biol 6:224–228

    Article  CAS  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40(15):e115

  • Vandereycken A, Durieux D, Joie É, Haubruge É, Verheggen FJ (2012) Habitat diversity of the multicolored Asian ladybeetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in agricultural and arboreal ecosystems: a review. Biotechnol Agron Soc Environ 16(4):553–563

    Google Scholar 

  • Ware R, Yguel B, Majerus M (2009) Effects of competition, cannibalism and intra-guild predation on larval development of the European coccinellid Adalia bipunctata and the invasive species Harmonia axyridis. Ecol Entomol 34:12–19

    Article  Google Scholar 

  • White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455

    Article  Google Scholar 

  • Wickham H (2009) Ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Yasuda H, Evans EW, Kajita Y, Urakawa K, Takizawa T (2004) Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141:722–731

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Lars Skipper (www.miridae.dk) for verifying the identity of mirids and EWH BioProduction ApS for provision of A. nemoralis; Gitte Jensen (DK), Renate Zindel and Mario Waldburger (Agroscope ART, CH) for technical assistance; and Peter Brown (UK) and Brecht Ingels (BEL) for collection of specificity samples. We also thank three anonymous reviewers for their insightful comments. HPR was financed by Villum Fonden, AGH was supported by a PhD grant from University of Copenhagen.

Author information

Authors and Affiliations

  1. Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, 1958, Frederiksberg C, Denmark

    Andy G. Howe & Hans Peter Ravn

  2. Section of Biostatistics, Department of Public Health, University of Copenhagen, Øster Farimagsgade 5, 1014, Copenhagen K, Denmark

    Christian Bressen Pipper

  3. Laboratoire de Biologie du Sol, Institut de biologie, Université de Neuchâtel, Emile-Argand 11, 2000, Neuchâtel, Switzerland

    Alexandre Aebi

Authors
  1. Andy G. Howe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hans Peter Ravn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Bressen Pipper
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandre Aebi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andy G. Howe.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Howe, A.G., Ravn, H.P., Pipper, C.B. et al. Potential for exploitative competition, not intraguild predation, between invasive harlequin ladybirds and flowerbugs in urban parks. Biol Invasions 18, 517–532 (2016). https://doi.org/10.1007/s10530-015-1024-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-1024-y

Keywords

Search

Navigation