Eur. J. Entomol. 109 (3): 353-362, 2012 | DOI: 10.14411/eje.2012.046

Laboratory studies on intraguild predation and cannibalism among coccinellid larvae (Coleoptera: Coccinellidae)

Gabriele RONDONI, Andrea ONOFRI, Carlo RICCI*
Department of Agricultural and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121 Perugia, Italy; e-mail: gabrielerondoni@libero.it
* GR and CR contributed to all the phases of the work and AO contributed to the statistical analysis.

Intraguild predation (IGP) and cannibalism occur in the field and could affect the dominance structure of guilds of coccinellid species. The exotic biological control agent Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is now well established in most areas of Northern and Central Italy, but it is unclear what effect this species could have on native dominant and non-dominant coccinellids with which it co-occurs. In order to predict the trophic interactions in coccinellid guilds and the likely effect of H. axyridis, the incidence of IGP and cannibalism among the following six species were evaluated under laboratory conditions: H. axyridis, three native dominant species, Adalia bipunctata (L.), Oenopia conglobata (L.) and Coccinella septempunctata L. and two native non-dominant species, Platynaspis luteorubra (Goeze) and Scymnus apetzi (Mulsant). Unfed and fed fourth instar larvae of the above species were paired in an experimental arena and the incidence of predation recorded over a period of 24 h. In absence of aphids, the survival probabilities (SP) of A. bipunctata and O. conglobata were lowest when paired with either C. septempunctata or H. axyridis (< 0.20 SP after 24 h). The SP of C. septempunctata was similar if paired with either a conspecific larva or H. axyridis (< 0.34 SP after 24 h) and that of H. axyridis was reduced similarly if paired with either a conspecific larva or C. septempunctata (> 0.71 SP after 24 h). The SP of P. luteorubra was lower when paired with A. bipunctata and C. septempunctata (< 0.07 SP after 24 h) than with other species and that of S. apetzi was greatly reduced when paired with all the dominant and exotic species (< 0.27 SP after 24h). In presence of aphids no predatory events occurred in most combinations. H. axyridis acted as a strong predator of native dominant and non-dominant coccinellids when the aphids are scarce. We did not find any evidence, however, that the incidence of IGP among exotic and native species is higher than either IGP or cannibalism in native species. The likelihood of IGP occurring in the field is discussed.

Keywords: Coccinellidae, Harmonia axyridis, intraguild predation, biological control, invasive species, Italy, interval-censored survival analysis

Received: July 7, 2011; Accepted: January 20, 2012; Published: July 2, 2012

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References

  1. ADRIAENS T., SAN MARTIN G., HAUTIER L., BRANQUART E. & MAES D. 2010: Toward a Noah's Ark for native ladybirds in Belgium? IOBC/WPRS Bull. 58: 1-3
  2. AGARWALA B.K. & DIXON A.F.G. 1992: Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol. Entomol. 17: 303-309 Go to original source...
  3. AGARWALA B.K. & YASUDA H. 2001: Larval interactions in aphidophagous predators: effectiveness of wax cover as defence shield of Scymnus larvae against predation from syrphids. Entomol. Exp. Appl. 100: 101-107 Go to original source...
  4. ALYOKHIN A. & SEWELL G. 2004: Changes in a lady beetle community following the establishment of three alien species. Biol. Invas. 6: 463-471 Go to original source...
  5. AMEIXA O.M.C.C., HONEK A., MARTINKOVA Z. & KINDLMANN P. 2010: Position of Harmonia axyridis in aphidophagous guilds in the Czech Republic. IOBC/WPRS Bull. 58: 7-14
  6. BARBAGALLO S. & RICCI C. 2006: A faunistic survey on aphids of Marche and Umbria territory in middle-eastern Italy. Boll. Zool. Agr. Bachicolt. 38: 39-101 [in Italian, English abstr.]
  7. BAZZOCCHI G.G., LANZONI A., ACCINELLI G. & BURGIO G. 2004: Overwintering, phenology and fecundity of Harmonia axyridis in comparison with native coccinellid species in Italy. BioControl 49: 245-260 Go to original source...
  8. BLUM M.S. & SANNASI A. 1974: Reflex bleeding in the lampyrid Photinus pyralis: defensive function. J. Insect Physiol. 20: 451-460 Go to original source...
  9. BROWN M.W. 2004: Role of aphid predator guild in controlling spirea aphid populations on apple in West Virginia, USA. Biol. Contr. 29: 189-198 Go to original source...
  10. BROWN M.W. & MILLER S.S. 1998: Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomol. News 109: 143-151
  11. BROWN P.M.J., FROST R., DOBERSKI J., SPARKS T., HARRINGTON R. & ROY H.E. 2011: Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol. Entomol. 36: 231-240 Go to original source...
  12. BURGIO G., SANTI F. & MAINI S. 2002: On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biol. Contr. 24: 110-116 Go to original source...
  13. BURGIO G., SANTI F., LANZONI A., MASETTI A., DE LUIGI V., MELANDRI M., REGGIANI A., RICCI C., LOOMANS A.J.M. & MAINI S. 2008: Harmonia axyridis recordings in northern Italy. Bull. Insectol. 61: 361-364
  14. CABRAL S., SOARES A.O., MOURA R. & GARCIA P. 2006: Suitability of Aphis fabae, Myzus persicae (Homoptera: Aphididae) and Aleyrodes proletella (Homoptera: Aleyrodidae) as prey for Coccinella undecimpunctata (Coleoptera: Coccinellidae). Biol. Contr. 39: 434-440 Go to original source...
  15. CAESAR A.J. 2003: Synergistic interaction of soilborne plant pathogens and root-attacking insects in classical biological control of an exotic rangeland weed. Biol. Contr. 28: 144-153 Go to original source...
  16. CAESAR A.J., CAESAR T. & MAATHUIS M.H. 2010: Pathogenicity, characterization and comparative virulence of Rhizoctonia spp. from insect-galled roots of Lepidium draba in Europe. Biol. Contr. 52: 140-144 Go to original source...
  17. CLARK T.G., BRADBURN M.J., LOVE S.B. & ALTMAN D.G. 2003: Survival analysis Part I: Basic concepts and first analysis. Br. J. Cancer 89: 232-238. Go to original source...
  18. COTTRELL T.E. & YEARGAN K.V. 1998: Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J. Kansas Entomol. Soc. 71: 159-163
  19. CROCI F., BRACALINI M., RONDONI G. & RICCI C. 2010: Chorology of invasive ladybird Harmonia axyridis (Pallas) in Italy considering the first records from Tuscany. Proceedings of the International Symposium "Ecology of Aphidophaga 11", Perugia, Italy, 19-24 September 2010. p. 121
  20. 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 Go to original source...
  21. DENNO R.F. & FINKE D.L. 2006: Multiple predator interactions and food-web connectance: Implications for biological control. In Brodeur J. & Boivin G. (eds): Trophic and Guild Interactions in Biological Control. Springer, Dordrecht, pp. 45-70
  22. DIXON A.F.G. 2000: Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge University Press, Cambridge, 257 pp
  23. DUKES J.S. & MOONEY H.A. 1999: Does global change increase the success of biological invaders? Trends Ecol. Evol. 14: 135-139 Go to original source...
  24. ELLIOTT N., KIECKHEFER R. & KAUFFMAN W. 1996: Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105: 537-544 Go to original source...
  25. ENGLUND G. 1997: Importance of spatial scale and prey movements in predator caging experiments. Ecology 78: 2316-2325 Go to original source...
  26. ERLER F. 2004: Natural enemies of the pear psylla Cacopsylla pyri in treated vs untreated pear orchards in Antalya, Turkey. Phytoparasitica 32: 295-304 Go to original source...
  27. ERNSTING G. & VAN DER WERF D.C. 1988: Hunger, partial consumption of prey and prey size preference in a carabid beetle. Ecol. Entomol. 13: 155-164 Go to original source...
  28. EVANS E.W. 2004: Habitat displacement of North American ladybirds by an introduced species. Ecology 85: 637-647 Go to original source...
  29. EVANS E.W. & GUNTHER D.I. 2005: The link between food and reproduction in aphidophagous predators: a case study with Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 102: 423-430 Go to original source...
  30. EVANS E.W., COMONT R.F. & RABITSCH W. 2011a: Alien arthropod predators and parasitoids: interactions with the environment. BioControl 56: 395-407 Go to original source...
  31. EVANS E.W., SOARES A.O. & YASUDA H. 2011b: Invasions by ladybugs, ladybirds, and other predatory beetles. BioControl 56: 597-611 Go to original source...
  32. FAY M.P. & SHAW P.A. 2010: Exact and asymptotic weighted logrank tests for interval censored data: The interval R Package. J. Statist. Softw. 36: 1-34 Go to original source...
  33. FORRESTER G.E. & STEELE M.A. 2004: Predators, prey refuges, and the spatial scaling of density-dependent prey mortality. Ecology 85: 1332-1342 Go to original source...
  34. GARDINER M.M, LANDIS D.A., GRATTON C., SCHMIDT N., O'NEAL M., MUELLER E., CHACON J., HEIMPEL G.E. & DIFONZO C.D. 2009: Landscape composition influences patterns of native and exotic lady beetle abundance. Divers. Distrib. 15: 554-564 Go to original source...
  35. GOMEZ G., CALLE M.L., OLLER R. & LANGOHR K. 2009: Tutorial on methods for interval-censored data and their implementation in R. Statist. Model. 9: 259-297 Go to original source...
  36. HAMPTON S.E. 2004: Habitat overlap of enemies: temporal patterns and the role of spatial complexity. Oecologia 138: 475-484 Go to original source...
  37. HARWOOD J.D. & OBRYCKI J.J. 2005: Quantifying aphid predation rates of generalist predators in the field. Eur. J. Entomol. 102: 335-350 Go to original source...
  38. HAUTIER L., GREGOIRE J.C., DE SCHAUWERS J., SAN MARTIN G., CALLIER P., JANSEN J.P. & DE BISEAU J.C. 2008: Intraguild predation by Harmonia axyridis on coccinellids revealed by exogenous alkaloid sequestration. Chemoecology 18: 191-196 Go to original source...
  39. HAUTIER L., SAN MARTIN G., CALLIER P., DE BISEAU J.C. & GREGOIRE J.C. 2011: Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol. Invas. 13: 1805-1814 Go to original source...
  40. HESLER L.S. & KIECKHEFER R.W. 2008: Status of exotic and previously common native coccinellids (Coleoptera) in South Dakota landscapes. J. Kansas Entomol. Soc. 81: 29-49 Go to original source...
  41. HINDAYANA D., MEYHOFER R., SCHOLZ D. & POEHLING H.M. 2001: Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol. Contr. 20: 236-246 Go to original source...
  42. 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 Go to original source...
  43. HODEK I. & HONEK A. 1996: Ecology of Coccinellidae. Kluwer Academic Publishers Dordrecht, 480 pp
  44. HODEK I. & MICHAUD J.P. 2008: Why is Coccinella septempunctata so successful? (A point-of-view). Eur. J. Entomol. 105: 1-12 Go to original source...
  45. HOLM S. 1979: A simple sequentially rejective multiple test procedure. Scand. J. Statist. 6: 65-70
  46. HONEK A. 1985: Habitat preferences of aphidophagous coccinellids (Coleoptera). Entomophaga 30: 253-264 Go to original source...
  47. INGELS B. & DE CLERCQ P. 2011: Effect of size, extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. BioControl 56: 871-882 Go to original source...
  48. IPERTI G. 1999: Biodiversity of predaceous coccinellidae in relation to bioindication and economic importance. Agric. Ecosyst. Environ. 74: 323-342 Go to original source...
  49. JANSEN J.P. & HAUTIER L. 2008: Ladybird population dynamics in potato: comparison of native species with an invasive species, Harmonia axyridis. BioControl 53: 223-233 Go to original source...
  50. KAJITA Y. & EVANS E.W. 2010: Alfalfa fields promote high reproductive rate of an invasive predatory lady beetle. Biol. Invas. 12: 2293-2302 Go to original source...
  51. KAJITA Y., TAKANO F., YASUDA H. & AGARWALA B.K. 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 Go to original source...
  52. KAJITA Y., TAKANO F., YASUDA H. & EVANS E.W. 2006: Interactions between introduced and native predatory ladybirds (Coleoptera, Coccinellidae): factors influencing the success of species introductions. Ecol. Entomol. 31: 58-67 Go to original source...
  53. 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
  54. KHAN I., DIN S., KHALIL S.K. & RAFI M.A. 2007: Survey of predatory Coccinellids (Coleoptera: Coccinellidae) in the Chitral District, Pakistan. J. Insect Sci. 7: 1-6 Go to original source...
  55. KOCH R.L. 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 Go to original source...
  56. 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. Invas. 8: 743-754 Go to original source...
  57. LEE J.H. & KANG T.J. 2004: Functional response of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to Aphis gossypii Glover (Homoptera: Aphididae) in the laboratory. Biol. Contr. 31: 306-310 Go to original source...
  58. LOGAN B., WANG H. & ZHANG M. 2005: Pairwise multiple comparison adjustment in survival analysis. Statist. Medic. 24: 2509 Go to original source...
  59. LOSEY J.E. & DENNO R.F. 1998: Positive predator-predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79: 2143-2152
  60. LUCAS E. 2005: Intraguild predation among aphidophagous predators. Eur. J. Entomol. 102: 351-363 Go to original source...
  61. LUCAS E., CODERRE D. & BRODEUR J. 1998: Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79: 1084-1092 Go to original source...
  62. MAJERUS M.E.N. 1994: Ladybirds. New Naturalist Series, Harper Collins, London, 368 pp
  63. MAJERUS M.E.N. & KEARNS P. 1989: Ladybirds. Richmond Publishing, Slough, 103 pp
  64. MAJERUS M.E.N., STRAWSON V. & ROY H.E. 2006: The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol. Entomol. 31: 207-215 Go to original source...
  65. MAJERUS M.E.N., SLOGGETT J.J., GODEAU J.F. & HEMPTINNE J.L. 2007: Interactions between ants and aphidophagous and coccidophagous ladybirds. Popul. Ecol. 49: 15-27 Go to original source...
  66. MEYHOFER R. 2001: Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras. Entomol. Exp. Appl. 100: 77-87 Go to original source...
  67. MEYHOFER R. & HINDAYANA D. 2000: Effects of intraguild predation on aphid parasitoid survival. Entomol. Exp. Appl. 97: 115-122 Go to original source...
  68. MICHAUD J.P. 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 Go to original source...
  69. MILLS N. 2006: Interspecific competition among natural enemies and single versus multiple introductions in biological control. In Brodeur J. & Boivin G. (eds): Trophic and Guild Interactions in Biological Control. Springer, Dordrecht, pp. 191-220
  70. MONTSERRAT M., JANSSEN A., MAGALHAES S. & SABELIS M.W. 2006: To be an intra guild predator or a cannibal: is prey quality decisive? Ecol. Entomol. 31: 430-436 Go to original source...
  71. MOONEY H.A. & CLELAND E.E. 2001: The evolutionary impact of invasive species. Proc. Nat. Acad. Sci. 98: 5446-5451 Go to original source...
  72. MOSER S.E. & OBRYCKI J.J. 2009: Competition and intraguild predation among three species of coccinellids (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 102: 419-425 Go to original source...
  73. NAULT B.A. & KENNEDY G.G. 2003: Establishment of multicolored Asian lady beetle in Eastern North Carolina: Seasonal abundance and crop exploitation within an agricultural landscape. BioControl 48: 363-378 Go to original source...
  74. OBRYCKI J.J. & KRING T.J. 1998: Predaceous Coccinellidae in biological control. Annu. Rev. Entomol. 43: 295-321 Go to original source...
  75. OBRYCKI J.J., GILES K.L. & ORMORD A.M. 1998: Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia 117: 279-285 Go to original source...
  76. OBRYCKI J.J., ELLIOTT N.C. & GILES K.L. 2000: Coccinellid introductions: potential for and evaluation of non-target effects. In Follett P.A. & Duan J.J. (eds): Nontarget Effects of Biological Control. Kluwer Academic, Boston, pp. 127-145
  77. PASTOROK R.A. 1980: The effects of predator hunger and food abundance on prey selection by Chaoborus larvae. Limnol. Oceanogr. 25: 910-921 Go to original source...
  78. PELL J.K., BAVERSTOCK J., ROY H.E., WARE R.L. & MAJERUS M.E.N. 2008: Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53: 147-168 Go to original source...
  79. PHOOFOLO M.W. & OBRYCKI J.J. 1998: Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol. Exp. Appl. 89: 47-55 Go to original source...
  80. PROVOST C., LUCAS E., CODERRE D. & CHOUINARD G. 2006: Prey selection by the lady beetle Harmonia axyridis: The influence of prey mobility and prey species. J. Insect Behav. 19: 265-277 Go to original source...
  81. R DEVELOPMENT CORE TEAM 2010: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna
  82. RICCI C. 1979: The piercing-sucking mouth part of the Platynaspis luteorubra Goeze (Col., Coccinellidae). Boll. Lab. Entomol. Agr. Filippo Silvestri 36: 179-198 [in Italian, English abstr.]
  83. ROSENHEIM J.A., KAYA H.K., EHLER L.E., MAROIS J.J. & JAFFEE B.A. 1995: Intraguild predation among biological-control agents: theory and evidence. Biol. Contr. 5: 303-335 Go to original source...
  84. ROY H. & WAJNBERG E. 2008: From biological control to invasion: the ladybird Harmonia axyridis as a model species. BioControl 53: 1-4 Go to original source...
  85. ROY H.E., BROWN P. & MAJERUS M.E.N. 2006: Harmonia axyridis: a successful biocontrol agent or an invasive threat? In Eilenberg J. & Hokkanen H.M.T. (eds): An Ecological and Societal Approach to Biological Control. Kluwer Academic Publishers, Dordrecht, pp. 295-309
  86. ROY H.E., DE CLERCQ P., LAWSON HANDLEY L.J., POLAND R.L., SLOGGETT J.J. & WAJNBERG E. 2011: Alien arthropod predators and parasitoids: an ecological approach. BioControl 56: 375-382 Go to original source...
  87. SATO S., YASUDA H. & EVANS E.W. 2005: Dropping behaviour of larvae of aphidophagous ladybirds and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas. Ecol. Entomol. 30: 220-224 Go to original source...
  88. SATO S., KUSHIBUCHI K. & YASUDA H. 2009: Effect of reflex bleeding of a predatory ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), as a means of avoiding intraguild predation and its cost. Appl. Entomol. Zool. 44: 203-206 Go to original source...
  89. SCHELLHORN N. & ANDOW D. 1999: Cannibalism and interspecific predation: role of oviposition behavior. Ecol. Appl. 9: 418-428
  90. SCHOENER T.W. 1971: Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2: 369-404 Go to original source...
  91. SLOGGETT J.J. & DAVIS A.J. 2010: Eating chemically defended prey: alkaloid metabolism in an invasive ladybird predator of other ladybirds (Coleoptera: Coccinellidae). J. Exp. Biol. 213: 237-241 Go to original source...
  92. SNYDER W.E. & EVANS E.W. 2006: Ecological effects of invasive arthropod generalist predators. Annu. Rev. Ecol. Evol. Syst. 37: 95-122 Go to original source...
  93. SNYDER W.E., CLEVENGER G.M. & EIGENBRODE S.D. 2004: Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140: 559-565 Go to original source...
  94. SOARES A.O., CODERRE D. & SCHANDERL H. 2004: Dietary selfselection behaviour by the adults of the aphidophagous ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae). J. Anim. Ecol. 73: 478-486. Go to original source...
  95. STATHAS G.J., ELIOPOULOS P.A., KONTODIMAS D.C. & GIANNOPAPAS J. 2001: Parameters of reproductive activity in females of Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 98: 547-549 Go to original source...
  96. STRAUB C.S. & SNYDER W.E. 2008: Increasing enemy biodiversity strengthens herbivore suppression on two plant species. Ecology 89: 1605-1615 Go to original source...
  97. VOLKL W. 1995: Behavioral and morphological adaptations of the coccinellid, Platynaspis luteorubra for exploiting antattended resources (Coleoptera: Coccinellidae). J. Insect Behav. 8: 653-670 Go to original source...
  98. VOLKL W. & VOHLAND K. 1996: Wax covers in larvae of two Scymnus species: Do they enhance coccinellid larval survival? Oecologia 107: 498-503 Go to original source...
  99. WALLNER W. 1996: Invasive pests ('biological pollutants') and US forests: whose problem, who pays? EPPO Bull. 26: 167-180 Go to original source...
  100. WALTHER G.R., ROQUES A., HULME P.E., SYKES M.T., PYSEK P., KUHN I., ZOBEL M., BACHER S., BOTTA-DUKAT Z., BUGMANN H., CZUCZ B., DAUBER J., HICKLER T., JAROSIK V., KENIS M., KLOTZ S., MINCHIN D., MOORA M., NENTWIG W., OTT J., PANOV V.E., REINEKING B., ROBINET C., SEMENCHENKO V., SOLARZ W., THUILLER W., VILA M., VOHLAND K. & SETTELE J. 2009: Alien species in a warmer world: risks and opportunities. Trends Ecol. Evol. 24: 686-693 Go to original source...
  101. WALZER A. & SCHAUSBERGER P. 2011: Threat-sensitive antiintraguild predation behaviour: maternal strategies to reduce offspring predation risk in mites. Anim. Behav. 81: 177-184 Go to original source...
  102. WARE R.L. & MAJERUS M.E.N. 2008: Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53: 169-188 Go to original source...
  103. 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 Go to original source...
  104. YASUDA H. & OHNUMA N. 1999: Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomol. Exp. Appl. 93: 63-67 Go to original source...
  105. YASUDA H., EVANS E.W., KAJITA Y., URAKAWA K. & TAKIZAWA T. 2004: Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141: 722-731 Go to original source...
  106. 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: 373-384 Go to original source...