Skip to main content
SpringerLink
Log in

The role of exotic ladybeetles in the decline of native ladybeetle populations: evidence from long-term monitoring

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

Abstract

Ladybeetles (Coleoptera: Coccinellidae) are ubiquitous predators which play an important role in suppressing pest insects. In North America, the coccinellid community is increasingly dominated by exotic species, and the abundance of some native species has declined dramatically since the 1980s. Several hypotheses have been proposed to describe the mechanism of invasion coupled with native species declines, e.g. vacant niche exploitation, intraguild predation, competitive exploitation and habitat compression. We analyze a 24-year dataset of coccinellid community structure in southwestern Michigan to elucidate the most likely mechanism(s) of native coccinellid decline and implications for their conservation. Correlation analyses indicated that impact of exotic species on native coccinellids varies with their degree of interaction. Although several native species were observed to be in numerical decline, only Adalia bipunctata and Coleomegilla maculata had declines that were statistically significant. The magnitude of decline in these two species varied with the degree of dietary overlap with invaders, thus their decline is most likely driven by competitive exploitation. Habitat use patterns by some native species (A. bipunctata and Coccinella trifasciata) changed during years when the exotic Harmonia axyridis reached high numbers, lending support to the habitat compression hypothesis, where native species survive in ancestral (i.e. natural or semi-natural) habitats when invaders dominate cultivated habitats. Coccinellid communities occurring in semi-natural forested habitats were unique in both composition and variability from those occurring in cultivated habitats. Such semi-natural habitats can act as refuges for native coccinellids and may play a role in maintaining the functional resilience of coccinellid communities.

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
Fig. 4

Similar content being viewed by others

References

  • Acorn J (2007) Invasion of the seven-spotted certainty snatchers. Am Entomol 53:191–192

    Google Scholar 

  • Adriaens T, Martin San, y Gomez GSM, Maes D (2008) Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. In: Roy HE, Wajnberg E (eds) From biological control to invasion: the ladybird Harmonia axyridis as a model species. Springer, Dordrecht, pp 69–88

    Chapter  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 

  • Anderies JM, Ryan P, Walker BH (2006) Loss of resilience, crisis, and institutional change: lessons from an intensive agricultural system in southeastern Australia. Ecosystems 9:865–878

    Article  Google Scholar 

  • Bahlai CA, Sears MK (2009) Population dynamics of Harmonia axyridis and Aphis glycines in Niagara Peninsula soybean fields and vineyards. J Entomol Soc Ont 140:27–39

    Google Scholar 

  • Bahlai CA, Colunga-Garcia M, Gage SH et al (2013) Long term functional dynamics of an aphidophagous coccinellid community are unchanged in response to repeated invasion. PLoS One 8:e83407

    Article  PubMed Central  PubMed  Google Scholar 

  • Brown MW (2003) Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis. Biocontrol 48:141–153

    Article  Google Scholar 

  • Clarke K, Gorley R (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Colunga-Garcia M, Gage SH (1998) Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environ Entomol 27:1574–1580

    Article  Google Scholar 

  • Costamagna AC, Landis DA (2006) Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol Appl 16:1619–1628

    Article  PubMed  Google Scholar 

  • Costamagna AC, Landis DA (2007) Quantifying predation on soybean aphid through direct field observations. Biol Control 42:16–24

    Article  Google Scholar 

  • Cottrell TE (2005) Predation and cannibalism of lady beetle eggs by adult lady beetles. Biol Control 34:159–164

    Article  Google Scholar 

  • Dysart RJ (1988) The European lady beetle Propylea quatuordecimpunctata: new locality records for North America (Coleoptera: Coccinellidae). J N Y Entomol Soc 96:119–121

    Google Scholar 

  • Elliott N, Kieckhefer R, Kauffman W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105:537–544

    Article  Google Scholar 

  • Evans EW (2000) Morphology of invasion: body size patterns associated with establishment of Coccinella septempunctata (Coleoptera: Coccinellidae) in western North America. Eur J Entomol 97:469–474

    Article  Google Scholar 

  • Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Finlayson CJ, Landry KM, Alyokhin AV (2008) Abundance of native and non-native lady beetles (Coleoptera: Coccinellidae) in different habitats in Maine. Ann Entomol Soc Am 101:1078–1087

    Article  Google Scholar 

  • Foley JA, Coe MT, Scheffer M et al (2003) Regime shifts in the Sahara and Sahel: interactions between ecological and climatic systems in northern Africa. Ecosystems 6:524–532

    Article  Google Scholar 

  • Fox TB, Landis DA, Cardoso FF et al (2004) Predators suppress Aphis glycines Matsumura population growth in soybean. Environ Entomol 33:608–618

    Article  Google Scholar 

  • Gagnon A-E, Heimpel GE, Brodeur J (2011) The ubiquity of intraguild predation among predatory arthropods. PLoS One 6:e28061

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gardiner MM, O’Neal ME, Landis DA (2011) Intraguild predation and native lady beetle decline. PLoS One 6:e23576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gardiner MM, Allee LL, Brown PMJ et al (2012) Lessons from lady beetles: accuracy of monitoring data from US and UK citizen-science programs. Front Ecol Environ. doi:10.1890/110185

  • Gordon RD (1985) The Coccinellidae (Coleoptera) of America North of Mexico. J N Y Entomol Soc 93:i-912

  • Gordon RD (1987) The first North American records of Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). J N Y Entomol Soc 95:307–309

    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 

  • Harrell Jr FE, Dupont C (2013) Package ‘Hmisc’ for R v. 3.12-2

  • Hautier L, San Martin G, Callier P et al (2011) Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol Invasions 13:1805–1814

    Article  Google Scholar 

  • Heimpel G, Frelich L, Landis D et al (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:2913–2931

    Article  Google Scholar 

  • Hesler LS, Kieckhefer RW (2008) Status of exotic and previously common native coccinellids (Coleoptera) in South Dakota landscapes. J Kans Entomol Soc 81:29–49

    Article  Google Scholar 

  • Hodek I, Honek A (1996) Ecology of Coccinellidae. Kluwer Academic, Dordrecht

    Book  Google Scholar 

  • Hodek I, Michaud JP (2008) Why is Coccinella septempunctata so successful? (A point-of-view). Eur J Entomol 105:1–12

    Article  Google Scholar 

  • Kajita Y, Evans E (2010) Alfalfa fields promote high reproductive rate of an invasive predatory lady beetle. Biol Invasions 12:2293–2302

    Article  Google Scholar 

  • Kajita Y, Obrycki J, Sloggett J et al (2010) Intraspecific alkaloid variation in ladybird eggs and its effects on con- and hetero-specific intraguild predators. Oecologia 163:313–322

    Article  PubMed  Google Scholar 

  • Kenis M, Auger-Rozenberg M-A, Roques A et al (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45

    Article  Google Scholar 

  • Knapp AK, Smith MD, Hobbie SE et al (2012) Past, present, and future roles of long-term experiments in the LTER Network. Bioscience 62:377–389

    Article  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 3:1–16

    Article  Google Scholar 

  • Krassoi FR, Brown KR, Bishop MJ et al (2008) Condition-specific competition allows coexistence of competitively superior exotic oysters with native oysters. J Anim Ecol 77:5–15

    Article  PubMed  Google Scholar 

  • Labrie G, Lucas É, 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 

  • LaMana ML, Miller JC (1996) Field observations on Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in Oregon. Biol Control 6:232–237

    Article  Google Scholar 

  • Maredia K, Gage S, Landis D et al (1992a) Ecological observations on predatory Coccinellidae (Coleoptera) in southwestern Michigan. Gt Lakes Entomol 25:265–270

    Google Scholar 

  • Maredia KM, Gage SH, Landis DA et al (1992b) Habitat use patterns by the seven-spotted lady beetle (Coleoptera: Coccinellidae) in a diverse agricultural landscape. Biol Control 2:159–165

    Article  Google Scholar 

  • Marshall SA (2006) Insects- their natural history and diversity: with a photographic guide to insects of Eastern North America. Firefly Books, Richmond Hill

    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 

  • Musser FR, Nyrop JP, Shelton AM (2004) Survey of predators and sampling method comparison in sweet corn. J Econ Entomol 97:136–144

    Article  PubMed  Google Scholar 

  • Ostrom PH, Colunga-Garcia M, Gage SH (1996) Establishing pathways of energy flow for insect predators using stable isotope ratios: field and laboratory evidence. Oecologia 109:108–113

    Article  Google Scholar 

  • 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:e40681

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ragsdale DW, Landis DA, Brodeur J et al (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing 2.15.3. R Foundation for Statistical Computing

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

    Article  CAS  PubMed  Google Scholar 

  • Rhainds M, Yoo HJS, Kindlmann P et al (2010) Two-year oscillation cycle in abundance of soybean aphid in Indiana. Agric For Entomol 12:251–257

    Google Scholar 

  • Rosenheim JA, Kaya HK, Ehler LE et al (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335

    Article  Google Scholar 

  • Roy H, Brown P, Frost R et al (2011) Ladybirds (Coccinellidae) of Britain and Ireland. Natural Environment Research Council (NERC), Swindon

  • Smith BC (1960) A technique for rearing coccinellid beetles on dry foods, and influence of various pollens on the development of Coleomegilla maculata lengi Timb. (Coleoptera: Coccinellidae). Can J Zool 38:1047–1049

    Article  Google Scholar 

  • Smith CA, Gardiner MM (2013) Oviposition habitat influences egg predation of native and exotic coccinellids by generalist predators. Biol Control 67:235–245

  • Snyder WE (2009) Coccinellids in diverse communities: which niche fits? Biol Control 51:323–335

    Article  Google Scholar 

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

  • Takizawa T, Snyder WE (2012) Alien vs. predator: could biotic resistance by native generalist predators slow lady beetle invasions? Biol Control 63:79–86

    Article  Google Scholar 

  • Turnock WJ, Wise IL, Matheson FO (2003) Abundance of some native coccinellines (Coleoptera: Coccinellidae) before and after the appearance of Coccinella septempunctata. Can Entomol 135:391–404

    Article  Google Scholar 

  • van de Koppel J, Rietkerk M, Weissing FJ (1997) Catastrophic vegetation shifts and soil degradation in terrestrial grazing systems. Trends Ecol Evol 12:352–356

    Article  PubMed  Google Scholar 

  • Wheeler AG, Hoebeke ER (2008) Rise and fall of an immigrant lady beetle: is Coccinella undecimpunctata L. (Coleoptera: Coccinellidae) still present in North America? Proc Entomol Soc Wash 110:817–823

    Article  Google Scholar 

  • Woltz JM, Landis DA (2013) Coccinellid immigration to infested host patches influences suppression of Aphis glycines in soybean. Biol Control 64:330–337

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Aaron Fox, Rufus Isaacs, Helen Roy and William Snyder for helpful comments offered on an earlier draft of this manuscript, as well as the input of two anonymous reviewers. We acknowledge the numerous field assistants for weekly field data collection and data preservation. We also thank the Kellogg Biological Station Long-Term Ecological Research Management Team for their assistance with trapping logistics, and Sven Bohm for database management. Funding for this work was provided by the National Science Foundation Long Term Ecological Research program Grant #1027253 and Michigan State University AgBioResearch.

Author information

Authors and Affiliations

  1. Department of Entomology, Center for Integrated Plant Systems Lab, Room 204, Michigan State University, 578 Wilson Rd., East Lansing, MI, 48824, USA

    Christine A. Bahlai & Douglas A. Landis

  2. Center for Global Change and Earth Observations, Room 205, Michigan State University, 1405 South Harrison Road, East Lansing, MI, 48823, USA

    Manuel Colunga-Garcia

  3. Department of Entomology, Michigan State University, 101 Manly Miles Building, 1405 South Harrison Road, Lansing, MI, 48824, USA

    Stuart H. Gage

Authors
  1. Christine A. Bahlai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel Colunga-Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stuart H. Gage
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Douglas A. Landis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine A. Bahlai.

Appendix

Appendix

Spearman rank correlation analysis results for abundance of 13 species of coccinellid partitioned by habitat type (Tables 2, 3, 4).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bahlai, C.A., Colunga-Garcia, M., Gage, S.H. et al. The role of exotic ladybeetles in the decline of native ladybeetle populations: evidence from long-term monitoring. Biol Invasions 17, 1005–1024 (2015). https://doi.org/10.1007/s10530-014-0772-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-014-0772-4

Keywords

Search

Navigation