BioControl

, Volume 56, Issue 4, pp 663–679 | Cite as

Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis

  • Helen E. Roy
  • Emma Rhule
  • Susanne Harding
  • Lori-Jayne Lawson Handley
  • Remy L. Poland
  • Eric W. Riddick
  • Tove Steenberg
Article

Abstract

Harmonia axyridis is an invasive alien predator in many countries across the world. The rapid establishment and spread of this species is of concern because of the threat it poses to biodiversity as a generalist predator. Understanding the mechanisms that contribute to the success of this species as an invader is not only intriguing but also critical to our understanding of the processes governing such invasions. The enemy release hypothesis (ERH) could explain the rapid population growth of many invasive alien species. However, empirical evidence in support of the ERH is lacking. An alternative hypothesis that could explain rapid population growth is evolution of increased competitive ability (EICA). Here we provide an overview of the parasites and pathogens of coccinellids with a particular focus on H. axyridis as a host. We examine the differential susceptibility of host species and highlight the resilience of H. axyridis in comparison to other coccinellids. We recognise the paucity and limitations of available information and suggest that studies, within a life-table framework, comparing life history traits of H. axyridis in both the native and introduced ranges are necessary. We predict that H. axyridis could benefit from both enemy release and EICA within the introduced range but require further empirical evidence.

Keywords

Harmonia axyridis Natural enemies Enemy release hypothesis EICA Parasites Pathogens 

Notes

Acknowledgments

HER is funded through the Centre for Ecology & Hydrology (Natural Environmental Research Council (NERC). HER is also funded by the Joint Nature Conservation Committee (JNCC) and receives funding from the Department for Environment, Food and Rural Affairs (Defra) for work on the GB Non-Native Species Information Portal. ER is funded by Microsoft Research. Mention of a commercial or proprietary product does not constitute an endorsement of the product by any of the universities or by the United States Department of Agriculture.

References

  1. Abdel-Moniem ASH, Gesraha MA (2001) Evaluation of certain entomopathogenic nematodes against the melon ladybird, Epilachna chrysomelina F. (Coleoptera: Coccinellidae). Arch Phytopathol Plant Prot 34:327–336CrossRefGoogle Scholar
  2. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30CrossRefGoogle Scholar
  3. Berkvens N, Moens J, Berkvens D, Samih MA, Tirry L, De Clercq P (2010) Dinocampus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe. Biol Control 53:92–99CrossRefGoogle Scholar
  4. Bjørnson S (2008) Natural enemies of the convergent lady beetle, Hippodamia convergens Guerin-Meneville: their inadvertent importation and potential significance for augmentative biological control. Biol Control 44:305–311CrossRefGoogle Scholar
  5. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive non-indigenous plants—a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  6. Bonte D, Hovestadt T, Pethke HJ (2008) Male-killing endosymbionts: influence of environmental conditions on persistence of host metapopulation. BMC Evol Biol 8:243PubMedPubMedCentralCrossRefGoogle Scholar
  7. Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hagg T, Kenis M, Klausnitzer BEM, Kovar I, Loomans AJM, Majerus MEN, Nedved O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov IA, Roy DB (2008a) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53:5–21CrossRefGoogle Scholar
  8. Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN (2008b) Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl 53:55–67CrossRefGoogle Scholar
  9. Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Lawson Handley L-J (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl. doi: 10.1007/s10526-011-9379-1
  10. Brownlie JC, Johnson KN (2009) Symbiont-mediated protection in insect hosts. Trends Microbiol 17:348–354PubMedCrossRefGoogle Scholar
  11. Burgio G, Lanzoni A, Accinelli G, Maini S (2008) Estimation of mortality by entomophages on exotic Harmonia axyridis versus native Adalia bipunctata in semi-field conditions in northern Italy. BioControl 53:277–287CrossRefGoogle Scholar
  12. Cerretti P, Tschorsnig H-P (2010) Annotated host catalogue for the Tachinidae (Diptera) of Italy. Stuttgart Beitr Naturk Ser A Neue Ser 3:305–340Google Scholar
  13. Ceryngier P, Hodek I (1996) Enemies of Coccinellidae. In: Hodek I, Honěk A (eds) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, pp 319–350CrossRefGoogle Scholar
  14. Ceryngier P, Roy HE, Ware RL (2011) Natural enemies of ladybird beetles. In: Hodek I, Honěk A, van Emden H (eds) Ecology of the Coccinellidae. Kluwer, Boston (in press)Google Scholar
  15. Clopton RE (2009) Phylogenetic relationships, evolution, and systematic revision of the septate gregarines (Apicomplexa: Eugregarinorida: Septatorina). Comp Parasitol 76:167–190CrossRefGoogle Scholar
  16. Clopton RE, Gold RE (1996) Host specificity of Gregarina blattarum von Siebold, 1839 (Apicomplexa: Eugregarinida) among five species of domiciliary cockroaches. J Invertebr Path 67:219–223CrossRefGoogle Scholar
  17. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  18. Cottrell TE (2004) Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae. Biol Control 31:362–371CrossRefGoogle Scholar
  19. Cottrell TE, Shapiro-Ilan DI (2003) Susceptibility of a native and an exotic lady beetle (Coleoptera, Coccinellidae) to Beauveria bassiana. J Invertebr Path 84:137–144CrossRefGoogle Scholar
  20. Cottrell TE, Shapiro-Ilan DI (2008) Susceptibility of endemic and exotic North American ladybirds (Coleoptera: Coccinellidae) to endemic fungal entomopathogens. Eur J Entomol 105:455–460CrossRefGoogle Scholar
  21. Delucchi V (1953) Aphidecta obliterata L. (Coleoptera, Coccinellidae) als Räuber von Dreyfusia (Adelges) piceae Ratz. Pflanzenschutz Berichte 11:73–83Google Scholar
  22. Disney RHL (1994) Scuttle flies: the Phoridae. Chapman & Hall, LondonCrossRefGoogle Scholar
  23. Disney RHL (1997) A new species of Phoridae (Diptera) that parasitises a wide-spread Asian ladybird beetle (Coleoptera: Coccinellidae). Entomol 116:163–168Google Scholar
  24. Disney RHL, Beuk PLT (1997) European Phalacrotophora (Diptera: Phoridae). Entomol Gaz 48:185–192Google Scholar
  25. Disney RHL, Chazeau J (1990) The recognition and biology of Phalacratophora quadrimaculata (Diptera: Phoridae) parasitising Olla v-nigrum (Coleoptera: Coccinellidae) used in attempts to control the Leucaena psyllid. Ann Parasitol Hum Comp 65:98–100CrossRefGoogle Scholar
  26. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstadter J, Hurst GDD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27PubMedPubMedCentralCrossRefGoogle Scholar
  27. Elnagdy S, Majerus MEN, Lawson Handley LJ (2011) The value of an egg: resource reallocation in ladybirds (Coleoptera: Coccinellidae) infected with male-killing bacteria. J Evol Biol (in press)Google Scholar
  28. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  29. Engelstadter J, Hurst GDD (2007) The impact of male-killing bacteria on host evolutionary processes. Genetics 175:245–254PubMedPubMedCentralCrossRefGoogle Scholar
  30. Filatova IT (1974) The parasites of Coccinellidae (Coleoptera) in West Siberia. In: Kolomyjetz NG (ed) The fauna and ecology of insects in Siberia. Nauka, Novasobirsk, pp 173–185Google Scholar
  31. Firlej A, Boivin G, Lucas E, Coderre D (2005) First report of Harmonia axyridis Pallas being attacked by Dinocampus coccinellae Schrank in Canada. Biol Invasions 7:553–556CrossRefGoogle Scholar
  32. Firlej A, Lucas E, Coderre D, Boivin G (2007) Teratocytes growth pattern reflects host suitability in a host-parasitoid assemblage. Physiol Entomol 32:181–187CrossRefGoogle Scholar
  33. Garces S, Williams R (2004) First record of Hesperomyces virescens Thaxter (Laboulbeniales: Ascomycetes) on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). J Kansas Entomol Soc 77:156–158CrossRefGoogle Scholar
  34. Glavendekic M, Roques A, Mihajlovic L (2011) An ALARM case study: the rapid colonization of an introduced tree, black locust by an invasive north-American midge and its parasitoids. In: Settele J, Penev LD, Georgiev TA, Grabaum R, Grobelnik V, Hammen V, Klotz S, Kotarac MIK (eds) Atlas of biodiversity risk. Pensoft, Sofia, pp 22–23Google Scholar
  35. Hajiqanbar H, Husband RW, Karnali K, Saboori A, Karnali H (2007) Ovacarus longisetosus n. sp (Acari: Podapolipidae) from Amara (Paracelia) saxicola zimm. (Coleoptera: carabidae) and new records of Coccipolipus, Dorsipes, Eutarsopolipus and Tarsopolipus from Iran. Int J Acarol 33:241–244CrossRefGoogle Scholar
  36. Harding S, Poinar GO, Dimitrova DV, Steenberg T (2011) Parasitylenchus sp. (Tylenchomorpha: Allantonematidae) parasitizing field populations of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Eur J Entomol 108:487–488CrossRefGoogle Scholar
  37. Heimpel GE, Lundgren JG (2000) Sex ratios of commercially reared biological control agents. Biol Control 19:77–93CrossRefGoogle Scholar
  38. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 281:215–220PubMedPubMedCentralCrossRefGoogle Scholar
  39. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256PubMedCrossRefGoogle Scholar
  40. Hoogendoorn M, Heimpel GE (2002) Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biol Control 25:224–230CrossRefGoogle Scholar
  41. Hurst GDD, Hurst LD, Majerus MEN (1992a) Evolutionary genetics—selfish genes moves sideways. Nature 356:659–660PubMedCrossRefGoogle Scholar
  42. Hurst GDD, Majerus MEN, Walker LE (1992b) Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera, Coccinellidae). Heredity 69:84–91CrossRefGoogle Scholar
  43. Hurst GDD, Purvis EL, Sloggett JJ, Majerus MEN (1994) The effect of infection with male-killing Rickettsia on the demography of Adalia bipunctata L. (2-spot ladybird). Heredity 73:309–316CrossRefGoogle Scholar
  44. Hurst GDD, McMeechan FK, Majerus MEN (1998) Phoridae (Diptera) parasitizing Coccinella septempunctata (Coleoptera: Coccinellidae) select older prepupal hosts. Eur J Entomol 95:179–181Google Scholar
  45. Hurst GDD, Jiggins FM, von der Schulenburg JHG, Bertrand D, West SA, Goriacheva II, Zakharov IA, Werren JH, Stouthamer R, Majerus MEN (1999) Male-killing Wolbachia in two species of insect. Proc R Soc Lond B 266:735–740CrossRefGoogle Scholar
  46. Husband RW (1984) Dilopolipus, Panesthipolipus, Peripolipus and Stenopolipus, new genera of Podapolipidae (Acarina) from the Indo-Australian Region. Int J Acarol 10:251–269CrossRefGoogle Scholar
  47. Iperti G (1964) Les parasites des coccinelles aphidiphages dans les Alpes-Maritimes et les Basses-Alpes. Entomophaga, pp 153–180Google Scholar
  48. Kamburov SS, Nadel DJ, Kenneth R (1967) Observations on Hesperomyces virescens Thaxter (Laboulbeniales), a fungus associated with premature mortality of Chilocorus bipustulatus L. in Israel. Israel J Agric Res Rehovot 17:131–134Google Scholar
  49. Katsoyannos P, Aliniazee MT (1998) First record of Strongygaster triangulifera (Loew) (Diptera: Tachinidae) as a parasitoid of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in western North America. Can Entomol 130:905–906CrossRefGoogle Scholar
  50. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  51. Kenis M, Roy HE, Zindel R, Majerus MEN (2008) Current and potential management strategies against Harmonia axyridis. BioControl 53:235–252CrossRefGoogle Scholar
  52. Knell RJ, Webberley KM (2004) Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour. Biol Rev 79:557–581PubMedCrossRefGoogle Scholar
  53. Koyama S, Majerus MEN (2008) Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain. BioControl 53:253–264CrossRefGoogle Scholar
  54. Kuznetsov VN (1997) Lady beetles of the Russian Far East. vol Memoir no 1. Center for Systematic Entomology, The Sandhill Crane Press, Inc, Gainsville, Florida, 248 pGoogle Scholar
  55. Laudého Y, Ormiéres R, Iperti G (1969) Les entomophages de Parlatoria blanchardi Targ dans les palmeraies de l’Adar Mauritanien. II. Etude d’un parasite de Coccinellidae Gregarina katherina Watson. Ann Zool Ecol Anim 1:395–406Google Scholar
  56. Lee SC, Corradi N, Byrnes EJ, Torres-Martinez S, Dietrich FS, Keeling PJ, Heitman J (2008) Microsporidia evolved from ancestral sexual fungi. Curr Biol 18:1675–1679PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lipa J, Pruszyński S, Bartkowski J (1975) The parasites and survival of the lady bird beetles (Coccinellidae) during winter. Acta Parasitol Pol 23:453–461Google Scholar
  58. Liu CL (1950) Contribution to the knowledge of Chinese Coccinellidae X. Occurrence of Perilitus coccinellidae (Schrank), a parasite of adult Coccinelidae in North China (Hymenoptera, Braconidae). Entomol News 61:207–208Google Scholar
  59. Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS One 5(3):e9743. doi: 10.1371/journal.pone.0009743
  60. Majerus MEN (2006) The impact of male-killing bacteria on the evolution of aphidophagous coccinellids. Eur J Entomol 103:1–7CrossRefGoogle Scholar
  61. Majerus MEN, Hurst GDD (1997) Ladybirds as a model system for the study of male-killing symbionts. Entomophaga 42:13–20CrossRefGoogle Scholar
  62. Majerus TMO, Majerus MEN, Knowles B, Wheeler J, Bertrand D, Kuznetzov VN, Ueno H, Hurst GDD (1998) Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae). Heredity 81:683–691CrossRefGoogle Scholar
  63. Majerus TMO, von der Schulenburg JHG, Majerus MEN, Hurst GDD (1999) Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol Biol 8:551–555PubMedCrossRefGoogle Scholar
  64. Majerus MEN, Hinrich J, Schulenburg GVD, Zakharov IA (2000) Multiple causes of male-killing in a single sample of the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae) from Moscow. Heredity 84:605–609PubMedCrossRefGoogle Scholar
  65. Matsuka M, Hashi H, Okada I (1975) Abnormal sex-ratio found in the lady beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Appl Entomol Zool 10:84–89Google Scholar
  66. McDaniel B, Morrill W (1969) New species of Tetrapolipus from Hippodamia convergens from South Dakota (Acarina: Podopolipidae). Ann Entomol Soc Am 62:1456–1458CrossRefGoogle Scholar
  67. Mills NJ (1981) The mortality and fat content of Adalia bipunctata during hibernation. Entomol Exp Appl 30:265–268CrossRefGoogle Scholar
  68. Nakamura K, Ueno H, Miura K (2005) Prevalence of inherited male-killing microorganisms in Japanese population of ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). Ann Entomol Soc Am 98:96–99CrossRefGoogle Scholar
  69. Nalepa CA, Kidd KA (2002) Parasitism of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) by Strongygaster triangulifer (Diptera: Tachinidae) in North Carolina. J Entomol Sci 37:124–127Google Scholar
  70. Nalepa CA, Weir A (2007) Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): role of mating status and aggregation behavior. J Invertebr Pathol 94:196–203PubMedCrossRefGoogle Scholar
  71. Narsi RY, Narayan RP (1984) First report of Parasitylenchus coccinellae Iperti & Waerebeke (1968) from India in two new hosts Menochilus sexmaculatus (F.) and Illeis indica Timberlake. Riv Parassit 45:133–137Google Scholar
  72. Obrycki JJ, Tauber MJ, Tauber CA (1985) Perilitus coccinellae (Hymenoptera: Braconidae): parasitisation and development in relation to host-stage attacked. Ann Entomol Soc Am 78:852–854CrossRefGoogle Scholar
  73. Ormond EL, Thomas APM, Pugh PJA, Pell JK, Roy HE (2010) A fungal pathogen in time and space: the population dynamics of Beauveria bassiana in a conifer forest. FEMS Microbiol Ecol 74:146–154PubMedCrossRefGoogle Scholar
  74. Ormond EL, Thomas APM, Pell JK, Freeman SN, Roy HE (2011) Avoidance of a generalist entomopathogenic fungus by the ladybird, Coccinella septempunctata. FEMS Microbiol Ecol. doi: 10.1111/j.1574-6941.2011.01100.x
  75. Osawa N (1992) A life table of the ladybird beetle Harmonia axyridis Pallas (Coleoptera, Coccinellidae) in relation to the aphid abundance. Jpn J Entomol 60:575–579Google Scholar
  76. Park H-C, Park YC, Hong OK, Cho SY (1996) Parasitoids of the aphidophagous ladybeetles, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Chuncheon areas, Korea. Korean J Entomol 26:143–147Google Scholar
  77. Randerson JP, Smith NGC, Hurst LD (2000) The evolutionary dynamics of male-killers and their hosts. Heredity 84:152–160PubMedCrossRefGoogle Scholar
  78. Reeves WK (2004) First report of Strongygaster triangulifera (Diptera: Tachinidae) as a parasitoid of a cantharid beetle, Chauliognathus pennsylvanicus (Coleoptera: Cantharidae). Can Entomol 136:661–662CrossRefGoogle Scholar
  79. Rhamhalinghan M (1986) Pathologies caused by Coccinellimermis Rubtzov (Nematoda: Mermithidae) in Coccinella septempunctata L, (Coleoptera, Coccinellidae). Proc Indian Natl Sci Acad 52:228–321Google Scholar
  80. Rhule EL, Majerus MEN, Jiggins FM, Ware RL (2010) Potential role of the sexually transmitted mite Coccipolipus hippodamiae in controlling populations of the invasive ladybird Harmonia axyridis. Biol Control 53:243–247CrossRefGoogle Scholar
  81. Riddick EW (2006) Influence of host gender on infection rate, density and distribution of the parasitic fungus, Hesperomyces virescens, on the multicolored Asian lady beetle, Harmonia axyridis. J Insect Sci 6:1–15PubMedCrossRefGoogle Scholar
  82. Riddick EW (2010) Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bull Insectol 63:13–20Google Scholar
  83. Riddick EW, Cottrell TE (2010) Is the prevalence and intensity of the ectoparasitic fungus Hesperomyces virescens related to the abundance of entomophagous coccinellids? Bull Insectol 63:71–78Google Scholar
  84. Riddick EW, Schaefer PW (2005) Occurrence, density, and distribution of parasitic fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on multicolored Asian lady beetle (Coleoptera: Coccinellidae). Ann Entomol Soc Am 98:615–624CrossRefGoogle Scholar
  85. Riddick EW, Cottrell TE, Kidd KA (2009) Natural enemies of the Coccinellidae: parasites, pathogens, and parasitoids. Biol Control 51:306–312CrossRefGoogle Scholar
  86. Roy HE, Cottrell TE (2008) Forgotten natural enemies: interactions between coccinellids and insect-parasitic fungi. Eur J Entomol 105:391–398CrossRefGoogle Scholar
  87. Roy HE, Rudge H, Goldrick L, Hawkins D (2007) Eat or be eaten: prevalence and impact of egg cannibalism on two-spot ladybirds, Adalia bipunctata. Entomol Exp Appl 125:33–38CrossRefGoogle Scholar
  88. Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN (2008) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl 53:265–276CrossRefGoogle Scholar
  89. Roy HE, Lawson Handley L-J, Schonrogge K, Poland RL, Purse BV (2011) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl. doi: 10.1007/s10526-011-9349-7
  90. Saito T, Bjørnson S (2006) Horizontal transmission of a microsporidium from the convergent lady beetle, Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae), to three coccinellid species of Nova Scotia. Biol Control 39:427–433CrossRefGoogle Scholar
  91. Semyanov VP (1978) An unusual pattern of parasitism in the braconid Dinocampus coccinellae Schrank (Hymenoptera, Braconidae). Entomol Obozr 57:513–514Google Scholar
  92. Shapiro-Ilan DI, Cottrell TE (2005) Susceptibility of lady beetles (Coleoptera: Coccinellidae) to entomopathogenic nematodes. J Invertebr Pathol 89:150–156PubMedCrossRefGoogle Scholar
  93. Shoemaker DD, Ross KG, Keller L, Vargo EL, Werren JH (2000) Wolbachia infections in native and introduced populations of fire ants (Solenopsis spp.). Insect Mol Biol 9:661–673PubMedCrossRefGoogle Scholar
  94. Sloggett JJ, Magro A, Verheggen FJ, Hemptinne JL, Hutchison WD, Riddick EW (2011) The chemical ecology of Harmonia axyridis. BioControl. doi: 10.1007/s10526-011-9376-4
  95. Song P, Wang Q-Y, Wu H-X, Lu X-J, Wang Y (2008) Identification of the cry gene in Bacillus thuringiensis strain WZ-9 and its toxicity against Henosepilachna vigintioctomaculata. Chin J Agric Biotech 5:245–250CrossRefGoogle Scholar
  96. Steenberg T, Harding S (2009a) The harlequin ladybird (Harmonia axyridis L.) in Denmark: spread and phenology during the initial phase of invasion. Entomol Medd 77:27–39Google Scholar
  97. Steenberg T, Harding S (2009b) Entomopathogenic fungi recorded from the harlequin ladybird, Harmonia axyridis. J Invertebr Pathol 102:88–89PubMedCrossRefGoogle Scholar
  98. Steenberg T, Harding S (2010a) The harlequin ladybird (Harmonia axyridis) in Denmark: spread, phenology, colour forms and natural enemies in the early phase of establishment. IOBC/WPRS Bull 58:143–147Google Scholar
  99. Steenberg T, Harding S (2010b) Entomopathogenic fungi found in field populations of the harlequin ladybird, Harmonia axyridis. IOBC/WPRS Bull 58:137–141Google Scholar
  100. Telschow A, Engelstadter J, Yamamura N, Hammerstein P, Hurst GDD (2006) Asymmetric gene flow and constraints on adaptation caused by sex ratio distorters. J Evol Biol 19:869–878PubMedCrossRefGoogle Scholar
  101. Thaxter R (1931) Contribution towards a monograph of the Laboulbeniaceae. Mem Am Acad Arts Sci 16:1–35Google Scholar
  102. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630PubMedCrossRefGoogle Scholar
  103. Tschorsnig H-P, Herting B (1994) The tachinids (Diptera: Tachinidae) of central Europe: identification keys for the species and data on distribution and ecology. Stuttgart Beitr Naturk Ser A (Biol) 506:1–170Google Scholar
  104. Ware R, Michie L-J, Otani T, Rhule E, Hall R (2010) Adaptation of native parasitoids to a novel host: the invasive coccinellid Harmonia axyridis. IOBC/WPRS Bull 58:175–182Google Scholar
  105. Webberley KM, Hurst GDD, Buzcko J, Majerus MEN (2002) Lack of parasite mediated sexual selection in an insect-STD system. Anim Behav 63:131–141CrossRefGoogle Scholar
  106. Webberley KM, Hurst GDD, Husband RW, von der Schulenburg JHG, Sloggett JJ, Isham V, Buzcko J, Majerus MEN (2004) Host reproduction and a sexually transmitted disease: causes and consequences of Coccipolipus hippodamiae distribution on coccinellid beetles. J Anim Ecol 73:1195–1200CrossRefGoogle Scholar
  107. Webberley KM, Tinsley MC, Sloggett JJ, Majerus MEN, Hurst GDD (2006) Spatial variation in the incidence of a sexually transmitted parasite of the ladybird beetle Adalia bipunctata (Coleoptera: Coccinellidae). Eur J Entomol 103:793–797CrossRefGoogle Scholar
  108. Weinert LA, Tinsley MC, Temperley M, Jiggins FM (2007) Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. Biol Lett 3:678–681PubMedPubMedCentralCrossRefGoogle Scholar
  109. Weir A, Beakes GM (1996) Correlative light- and scanning electron microscope studies on the developmental morphology of Hesperomyces virescens. Mycol 88:677–693CrossRefGoogle Scholar
  110. Welch VL, Sloggett JJ, Webberley KM, Hurst GDD (2001) Short-range clinal variation in the prevalence of a sexually transmitted fungus associated with urbanisation. Ecol Entomol 26:547–550CrossRefGoogle Scholar
  111. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751PubMedCrossRefGoogle Scholar
  112. Zindel R, Gottleib Y, Aebi A (2011). Arthropod symbioses: a neglected parameter in pest- and disease-control programmes. J Appl Ecol. doi: 10.1111/j.1365-2664.2011.01984.x

Copyright information

© International Organization for Biological Control (IOBC) 2011

Authors and Affiliations

  • Helen E. Roy
    • 1
  • Emma Rhule
    • 2
  • Susanne Harding
    • 3
  • Lori-Jayne Lawson Handley
    • 4
  • Remy L. Poland
    • 5
  • Eric W. Riddick
    • 6
  • Tove Steenberg
    • 7
  1. 1.Centre for Ecology & HydrologyCrowmarsh GiffordUK
  2. 2.Department of GeneticsUniversity of CambridgeCambridgeUK
  3. 3.Department of Agriculture and EcologyUniversity of CopenhagenFrederiksberg CDenmark
  4. 4.Evolutionary Biology Group, Department of Biological SciencesThe University of HullKingston-Upon-HullUK
  5. 5.Clifton CollegeBristolUK
  6. 6.National Biological Control LaboratoryUSDA-Agricultural Research ServiceStonevilleUSA
  7. 7.Department of AgroecologyUniversity of AarhusSlagelseDenmark

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