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Asymmetric larval interactions between introduced and indigenous ladybirds in North America

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Abstract

Understanding the mechanisms that result in the success of introduced species will contribute to predicting future invasions and managing invaded systems. We examined interactions between larvae of two predatory ladybird species recently introduced to North America, Coccinella septempunctata (CS) and Harmonia axyridis (HA), and two indigenous ladybirds, Coccinella transversoguttata (CT) and Hippodamia convergens (HC). By pairing young and old larvae in the laboratory at low and high levels of aphid availability, we assessed the degree of asymmetry in intraguild predation (IGP), the strength of competitive effects on growth and development of larvae escaping predation, and the nature of attack and escape behavior among the species. Interactions were generally asymmetric, with larvae of introduced species acting most frequently as intraguild predators and larvae of indigenous species serving most frequently as intraguild prey (the two Coccinella spp., however, preyed on each other at similar rates). Because they were especially aggressive and because other larvae were least successful in escaping their attacks, larvae of HA had stronger negative effects on larvae of the two indigenous species than did larvae of CS. Such negative effects, expressed most strongly when aphid availability was low, were especially adverse for the smaller of the two indigenous species, HC. In general, older larvae interacted with each other more strongly than young larvae did, and older larvae had especially strong negative effects on young larvae when interactions occurred between age classes. Our results suggest that HA more than CS may represent a threat to indigenous ladybirds as an intraguild predator, and that IGP in turn may play a stronger role for HA than for C. septempunctata in promoting the successful invasion of North America.

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References

  • Agarwala BK, Dixon AFG (1992) Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol Entomol 17:303–309

    Google Scholar 

  • Angalet GW, Tropp JM, Eggert AN (1979) Coccinella septempunctata in the United States: recolonizations and notes on its ecology. Environ Entomol 8:896–901

    Google Scholar 

  • Balfour RA, Buddle CM, Rypstra AL, Walker SE, Marshall SD (2003) Ontogenetic shifts in competitive interactions and intra-guild predation between two wolf spider species. Ecol Entomol 28:25–30

    Article  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 

  • Brown MW, Miller SS (1998) Coccinellidae in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis (Coleoptera: Coccinellidae). Entomol News 109:136–142

    Google Scholar 

  • Burgio G, Santi F, Maini S (2002) On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biol Control 24:110–116

    Article  Google Scholar 

  • Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239

    Google Scholar 

  • Cisneros JJ, Rosenheim JA (1997) Ontogenetic change of prey preference in the generalist predator Zelus renardii and its influence on predator–predator interactions. Ecol Entomol 22:399–407

    Google Scholar 

  • Coderre D, Provencher L, Tourneur J-C (1987) Oviposition and niche partitioning in aphidophagous insects on maize. Can Entomol 119:195–203

    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

    Google Scholar 

  • Cottrell TE, Yeargan KV (1998) Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J Kans Entomol Soc 71:159–163

    Google Scholar 

  • De Clercq P, Peeters I, Vergauwe G, Thas O (2003) Interaction between Podisus maculiventris and Harmonia axyridis, two predators used in augmentative biological control in greenhouse crops. BioControl 48:39–55

    Article  Google Scholar 

  • Dixon AFG (2000) Insect predator-prey dynamics. Cambridge University Press, Cambridge, pp 257

    Google Scholar 

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

    Google Scholar 

  • Evans EW (1991) Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids. Oecologia 87:401–408

    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

    Google Scholar 

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

    Google Scholar 

  • Evans EW, Richards DR (1997) Managing the dispersal of ladybird beetles (Col.: Coccinellidae): use of artificial honeydew to manipulate spatial distributions. Entomophaga 42:93–102

    Google Scholar 

  • Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–652

    Google Scholar 

  • Gagné WC, Martin JL (1968) The insect ecology of Red Pine plantations in central Ontario. V. The Coccinellidae (Coleoptera). Can Entomol 113:835–846

    Google Scholar 

  • Gordon RD (1985) The Coccinellidae (Coleoptera) of America north of Mexico. J NY Entomol Soc 93:1–912

    Google Scholar 

  • Gordon RD, Vandenberg N (1991) Field guide to recently introduced species of Coccinellidae (Coleoptera) in North America, with a revised key to North American genera of Coccinellini. Proc Entomol Soc Wash 93:845–864

    Google Scholar 

  • Hill AH, Lodge DM (1994) Diel changes in resource demand: competition and predation in species replacement among crayfishes. Ecology 75:2118–2126

    Google Scholar 

  • Hindayana D, Meyhofer R, Scholz D, Poehling H-M (2001) Intraguild predation among the hoverfly Episyrphus balteatus (Diptera: Syrphidae) and other aphidophagous predators. Biol Control 20:236–246

    Article  Google Scholar 

  • Hodek I, Honek A (1988) Sampling, rearing and handling of aphid predators. In: Minks AK, Harrewijn P (eds) Aphids, their Biology, Natural Enemies and Control, vol 2B. Elsevier, Amsterdam, pp 311–321

  • Hodek I, Honek A (1996) Ecology of Coccinellidae. Entomologica series 54. Kluwer, Dordrecht. pp 464

  • Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251

    Google Scholar 

  • Kajita Y, Takano F, Yasuda H, Agarwala BK (2000) Effects of indigenous ladybird species (Coleoptera: Coccinellidae) on the survival of an exotic species in relation to prey abundance. Appl Entomol Zool 35:473–479

    Article  Google Scholar 

  • Kalaskar A, Evans EW (2001) Larval responses of aphidophagous lady beetles (Coleoptera: Coccinellidae) to weevil larvae versus aphids as prey. Ann Entomol Soc Am 94:76–81

    Google Scholar 

  • Kiesecker JM, Blaustein AR, Miller CL (2001) Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82:1964–1970

    Google Scholar 

  • Kupferberg SJ (1997) Bullfrog (Rana catesbeiana) invasion of a California river: the role of larval competition. Ecology 78:1736–1751

    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 

  • Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092

    Google Scholar 

  • Lucas E, Gagné I, Coderre D (2002) Impact of the arrival of Harmonia axyridis on adults of Coccinella septempunctata and Coleomegilla maculate (Coleoptera: Coccinellidae). Eur J Entomol 99:457–463

    Google Scholar 

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

    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

    Google Scholar 

  • Musser FR, Shelton AM (2003) Factors altering the temporal and within-plant distribution of coccinellids in corn and their impact on potential intra-guild predation. Environ Entomol 32:575–583

    Google Scholar 

  • Nault BA and Kennedy GG (2003) Establishment of multicolored Asian lady beetle in Eastern North Carolina: seasonal abundance and crop exploitation within an agricultural landscape. BioControl 48:363–378

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Obrycki JJ, Giles KL, Ormord AM (1998b) Experimental assessment of interactions between larval Coleomegilla muculata and Coccinella septempunctata (Coleoptera: Coccinellidae) in field cages. Environ Entomol 27:1280–1288

    Google Scholar 

  • Okuyama T (2002) The role of antipredator behavior in an experimental community of jumping spiders with intraguild predation. Popul Ecol 44:121–125

    Article  Google Scholar 

  • Phoofolo MW, Obrycki JJ (1998) Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol Exp Appl 89:47–55

    Google Scholar 

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

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  • Rosenheim JA, Limburg DD, Colfer RG (1999) Impact of generalist predators on a biological control agent, Chrysoperla carnea: direct observations. Ecol Appl 9:409–417

    Google Scholar 

  • Roy K, Jablonski D, Valentine JW (2002) Body size and invasion success in marine bivalves. Ecol Lett 5:163–167

    Article  Google Scholar 

  • Sato S, Dixon AFG (2004) Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds: consequences for invasive species. Agric For Entomol 6:21–24

    Article  Google Scholar 

  • Sato S, Dixon AFG, Yasuda H (2003) Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol Entomol 28:628–633

    Article  Google Scholar 

  • Schaefer PW, Dysart RJ, Specht HB (1987) North American distribution of Coccinella septempunctata (Coleoptera: Coccinellidae) and its mass appearance in coastal Delaware. Environ Entomol 16:368–373

    Google Scholar 

  • Schellhorn NA, Andow DA (1999) Cannibalism and interspecific predation: role of oviposition behavior. Ecol Appl 9:418–428

    Google Scholar 

  • Schmitz OJ, Suttle KB (2001) Effects of top predator species on direct and indirect interactions in a food web. Ecology 82:2072–2081

    Google Scholar 

  • Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355

    Article  Google Scholar 

  • Snyder WE, Clevenger GM, Eigenbrode SD (2004) Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia (in press)

  • Staines CL Jr, Rothschild MJ, Trumble RB (1990) A survey of the Coccinellidae (Coleoptera) associated with nursery stock in Maryland. Proc Entomol Soc Wash 92:310–313

    Google Scholar 

  • Takahashi K (1989) Intra- and interspecific predations of lady beetles in spring alfalfa fields (in Japanese with English abstract). Jpn J Entomol 57:199–203

    Google Scholar 

  • Tedders WL, Schaefer PW (1994) Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the southeastern United States. Entomol News 105:228–243

    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

    Google Scholar 

  • Wheeler AG, Hoebeke ER (1995) Coccinella novemnotata in northeastern North America: historical occurrence and current status (Coleoptera: Coccinellidae). Proc Entomol Soc Wash 97:701–716

    Google Scholar 

  • Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Anim Ecol 71:1063–1074

    Article  Google Scholar 

  • Yasuda H, Kimura T (2001) Interspecific interactions in a tri-trophic arthropod system: effects of a spider on the survival of larvae of three predatory ladybirds in relation to aphids. Entomol Exp Appl 98:17–25

    Google Scholar 

  • Yasuda H, Ohnuma N (1999) Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomol Exp Appl 93:63–67

    Google Scholar 

  • Yasuda H, Shinya K (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163

    Google Scholar 

  • Yasuda H, Kikuchi T, Kindlmann P, Sato S (2001) Relationships between attack and escape rates, cannibalism, and intraguild predation in larvae of two predatory ladybirds. J Insect Behav 14:373–383

    Article  Google Scholar 

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Acknowledgements

We thank T. Toler, M. Benson, S. Higbee, J. Hunt, M. Johnson, and K. Labrum for assistance. We also thank two anonymous reviewers for commenting on the manuscript, and W. E. Snyder for providing us with a preprint that we incorporated in the revision. This work was supported by a grant-in-aid from the Japan Society for the Promotion of Science (no. 15380039), the US–Japan Cooperative Science Program (NSF INT-0089374), the USDA (99-35302-8104, NRI), and the Utah Agricultural Experiment Station.

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Correspondence to Hironori Yasuda.

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Yasuda, H., Evans, E.W., Kajita, Y. et al. Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141, 722–731 (2004). https://doi.org/10.1007/s00442-004-1680-6

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