Abstract
In recent years Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) has become a very popular insect among biological control practitioners and scientists, not only for its potential to be an efficient biological control agent but also because it is considered invasive. Individuals of this species were deliberately introduced into several countries for biological control of different arthropods pests. However the predator itself became an invasive species, affecting the dynamics and composition of several guilds through direct or indirect interactions with established species, including intraguild predation. In this paper we discuss the reasons why the species has a high invasiveness and what are the limits to invasion by this species. It is not clear if the invasiveness of the beetle is linked to its biological, ecological and behavioural abilities, or to other factors such as invasibility and interactions between the invaders, the noninvaders, and the habitat, which may in part explain the reasons of its success and help us to answer the question “what will stop the invader?” We also discuss the reason for the absence of the predator in the Azores islands. Despite the intentional introduction of H. axyridis in the Azores and the high number of individuals released, there are no records of this species in the wild, despite recent extensive sampling effort. In this paper we discuss the reasons for the apparent failure or the delay in establishment of the predator. One factor which may hamper the establishment of H. axyridis in some of the Azores islands is the absence of winter environmental conditions, mainly the temperature which is seldom lower than 12°C, essential for the induction of diapause. The lack of success in the establishment could be also related to functional diversity saturation, that is species saturation and competitive exclusion of H. axyridis by other previously established species may be operating.
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References
Adriaens T, Branquart E, Maes D (2003) The multicolored Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), a threat for native aphid predators in Belgium? Belg J Zool 133:195–196
Adriaens T, San Martin y Gomez G, Maes D (2007) Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl (this issue). doi:10.1007/s10526-007-9137-6
Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biol Invasions 6:463–471
Andermatt M (1996) Marienkäferlarven als blattlaus-bekämpfungsmittel? Andermatt Biocontrol 3:10–11
Azevedo EB (2005) “Projecto CLIMAAT—Clima e Meteorologia dos Arquipélagos Atlânticos”—Interreg IIIB, MAC 2.3/A3—Açores, Madeira e Canárias. http://www.climaat.angra.uac.pt. Accessed 19 Sept 2007
Balduf WV (1926) The bionomics of Dinocampus coccinellae Schrank. Ann Entomol Soc Am 19:465–489
Bazzochi GG, Lanzoni G, Accinelli G, Burgio G (2004) Overwintering, phenology and fecundity of Harmonia axyridis in comparison with native coccinellid species in Italy. BioControl 49:245–260
Bell G (2005) The co-distribution of species in relation to the neutral theory of community ecology. Ecology 86:757–770
Borges I, Soares AO, Hemptinne J-L (2006b) Abundance and spatial distributions of aphids and scales select for different life histories in their ladybird beetle predators. J Appl Entomol 130:461–464
Borges PAV, Cunha R, Gabriel R, Martins AF, Silva L, Vieira V, Dinis F, Lourenço P, Pinto N (2005) Description of the terrestrial Azorean biodiversity. In: Borges PAV, Cunha R, Gabriel R, Martins AMF, Silva L, Vieira V (eds) A list of the terrestrial fauna (Mollusca and Arthropoda) and flora (Bryophyta, Pteridophyta and Spermatophyta) from the Azores. Direcção Regional de Ambiente and Universidade dos Açores, Horta, Angra do Heroísmo and Ponta Delgada
Borges PAV, Lobo JM, Azevedo EB, Gaspar C, Melo C, Nunes VL (2006a) Invasibility and species richness of island endemic arthropods: a general model of endemic vs. exotic species. J Biogeogr 33:169–187
Borges PAV, Ugland KI, Dinis FO, Gaspar C (in press a) Insect and spider rarity in an oceanic island (Terceira, Azores): true rare and pseudo-rare species. In: Fattorini S (ed) Insect ecology and conservation. Research Signpost
Borges PAV, Amorim IR, Cunha R, Gabriel R, Martins AF, Silva L, Costa A, Vieira V. (in press b) Azores—biology. In: Gillespie R, Clagu D (eds) Encyclopedia of Islands. University of California Press, California
Brakefield PM, Willmer PG (1985) The basis of thermal-melanism in the ladybird Adalia bipunctata: differences in reflectance and thermal properties between the morphs. Heredity 54:9–14
Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg 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 (2007) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl (this issue). doi:10.1007/s10526-007-9132-y
Burgio G, Lanzoni A, Accinelli G, Maini S (2007) Estimation of mortality by entomophages on exotic Harmonia axyridis versus native Adalia bipunctata in semi-field conditions in northern Italy. BioControl (this issue). doi:10.1007/s10526-007-9133-x
Carrillo AM (2006) El sarantontón asiático Harmonia axyridis (Pallas, 1773) presente en Canárias (Coleoptera: Coccinellidae). Vieraea 34:71–72
Coderre D, Lucas E, Gagne I (1995) The occurrence of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) in Canada. Can Entomol 127:609–611
Cottrell TE (2004) Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae. Biol Control 31:362–371
Cottrell TE, Shapiro-Ilan DI (2003) Susceptibility of a native and an exotic lady beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. J Invertebr Pathol 84:137–144
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
Crawley JC (1989) Chance and timing in biological invasions. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmánek M, Williamson M (eds) Biological invasion: a global perspective. Scope 37. Wiley, Chichester
De Almeida LM, da Silva VB (2002) Primeiro registro de Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae): um coccinelideo originario da região Paleartica. Revta Bras Zool 19:941–944
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
De Jong PW, Gussekloo SWS, Bakefield PM (1996) Differences in thermal balance, body temperature and activity between non-melanic and melanic two-spot ladybird beetles (Adalia bipunctata) under controlled conditions. J Exp Biol 199:2655–2666
Dixon AFG (2000) Insect predator–prey dynamics: ladybird beetles & biological control. Cambridge University Press, Cambridge
Dobzhansky ThG (1933) Geographical variations in lady-beetles. Am Nat 709:97–126
Ehler LE (1998) Invasion biology and biological control. Biol Control 13:127–133
Elliott N, Kieckhefer R, Kauffman W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105:537–544
Ellis DR, Prokrym DR, Adams RG (1999) Exotic lady beetle survey in northeastern United States: Hippodamia variegata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). Entomol News 110:73–84
Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647
Félix S, Soares AO (2004) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of body weight. Eur J Entomol 101:237–242
Firlej A, Boivin G, Lucas É, Coderre D (2005) First report of Harmonia axyridis Pallas being attacked by Dinocampus coccinellae Schrank in Canada. Biol Invasions 7:553–556
Fye RE (1981) Rearing and release of coccinellids for potential control of pear Psylla. Agric Res Serv (Western Region) 20:1–9
Garcia V (1986) Approaches to integrated control of some citrus pests in the Azores and Algarve (Portugal). In: Cavalloro R, Di Martino E (eds) Integrated pest control in citrus groves. Proc. CEC Experts Meeting, Acireale
Gillespie RG, Roderick GK (2002) Arthropods on Islands: colonization, speciation, and conservation. Annu Rev Entomol 47:595–632
Gordon RD (1985) The Coccinellidae (Coleoptera) of America north of Mexico. J N Y Entomol Soc 93:1–912
Gratton C, Welter SC (1999) Does “enemy-free space” exist? Experimental host shifts of an herbivorous fly. Ecology 80:773–785
Hagley EAC (1999) Predatory insects in fruit orchards in Southern Ontario. Publication 208 Agriculture and Agri-Food Canada and Ontario Ministry of Agriculture, Food and Rural Affairs, 32 pp
Halpern SL, Underwood N (2006) Approaches for testing herbivore effects on plant population dynamics. J Appl Ecol 43:922–929
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
Hodek I (1973) Biology of Coccinellidae. Dr. W. Junk NV Publishers, The Hague, Prague
Hodek I, Honěk A (1996) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, 464 pp
Holt RD, Brakefield M, Gomulkiewicz R (2005) Theories of niche conservation and evolution-could exotic species be potential pest? In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions—insights into ecology, evolution and biogeography. Sinauer Associates, Inc. Publishers, Massachusetts
Hoogendoorn M, Heimpel GE (2002) Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biol Control 25:224–230
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton monographs in population biology. Princeton University Press, Princeton
Hubbell SP (2005) Neutral theory in community ecology and the hypothesis of functional equivalence. Funct Ecol 19:166–172
Hubbell SP (2006) Neutral theory and the evolution of ecological equivalence. Ecology 87:1387–1398
Huelsman MF, Jasinski J, Young C, Kovach J (2001) The multicolored Asian lady beetle (Harmonia axyridis) as a nuisance pest in households throughout Ohio. http://ipm.osu.edu/lady/icup.htm. Accessed 5 Sept 2007
Iablokoff-Khnzorian SM (1982) Les Coccinelles; Coléoptères-Coccinellidae. Société Nouvelle des Éditions Boubée, Paris, 568 pp
Iperti G, Bertrand E (2001) Hibernation of Harmonia axyridis (Coleoptera: Coccinellidae) in South-Eastern France. Acta Soc Zool Bohem 65:207–210
Kalaskar A, Evans EW (2001) Larval responses of aphidophagous lady beetles (Coleoptera: Coccinellidae) to weevil larvae versus aphid as prey. Ann Entomol Soc Am 94:76–81
Katsoyannos P, Kontodimas DC, Stathas GJ, Tsartsalis CT (1997) Establishment of Harmonia axyridis on citrus and some data on its phenology in Greece. Phytoparasitica 25:183–191
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. TREE 17:164–170
Kidd KA, Nalepa CA (1995) Distribution of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in North Carolina and Virginia. Proc Entomol Soc Wash 97:729–731
Koch RL (2003) The multicoloured Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control and non-target impacts. J Insect Sci 3:1–16
Koch RL, Hutchison WD, Venette RC, Heimpel GE (2003) Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biol Control 28:265–270
Koch RL, Venette RC, Hutchison WD (2005) Influence of alternate prey on predation of monarch butterfly (Lepidoptera: Nymphalidae) larvae by the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Environ Entomol 34:410–416
Komai T (1956) Genetics of ladybeetles. Adv Genet 8:155–189
Komai T, Hosino Y (1951) Contributions to the evolutionary genetics of the lady-beetle, Harmonia. II. Microgeographic variations. Genetics 36:382–390
Kovach J (2004) Impact of multicolored Asian lady beetles as a pest of fruit and people. Am Entomol 50:159–161
Labrie G, Coderre D, Lucas E (2007) Overwintering strategy of the multicolored Asian ladybeetle (Coleoptera: Coccinellidae): a cold-free space as a factor of invasive success. Ann Entomol Soc Am (in press)
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
LaMana ML, Miller JC (1996) Field observations on Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in Oregon. Biol Control 6:232–237
Lanzoni A, Accinelli G, Bazzocchi GG, Burgio G (2004) Biological traits and life table of the exotic Harmonia axyridis compared with Hippodamia variegata and Adalia bipunctata (Col. Coccinellidae). J Appl Entomol 128:298–306
Lee CE (2002) Evolutionary genetics of invasive species. TREE 17:386–391
Liebhold AM, Work TT, Mccullough DG, Cavey JF (2006) Airline baggage as a pathway for alien insect species invading the United States. Am Entomol 52:48–54
Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–326
Lombaert E, Malausa T, Devred R, Estoup A (2007) Phenotypic variation in invasive and biocontrol populations of the harlequin ladybird, Harmonia axyridis. BioControl (this issue). doi:10.1007/s10526-007-9131-z
Lucas E, Coderre D, Vincent C (1997) Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae. Entomol Exp Appl 85:151–159
Lucas E, Gagné I, Coderre D (2002) Impact of the arrival of Harmonia axyridis on adults of Coccinella septempunctata and Coleomegilla maculata (Coleoptera: Coccinellidae). Eur J Entomol 99:457–463
Lucas E, Labrie G, Vincent C, Kovach J (2007a) The multicolored Asian ladybeetle, Harmonia axyridis—beneficial or nuisance organism? In: Vincent C, Goettel M, Lazarovitz G (eds) Biological control: a global perspective. CABI Publishing, UK
Lucas E, Vincent C, Labrie G, Chouinard G, Fournier F, Pelletier F, Bostanian NJ, Coderre D, Mignault M-P, Lafontaine P (2007b) The multicolored Asian ladybeetle Harmonia axyridis in Quebec agroecosystems ten year after its arrival. Eur J Entomol 104:737–743
Lundgren JG, Razzak AA, Wiedenmann RN (2004) Population responses and food consumption by predators Coleomegilla maculata and Harmonia axyridis (Coleoptera: Coccinellidae) during anthesis in an Illinois cornfield. Environ Entomol 33:958–963
Maeta Y (1969) Biological studies on the natural enemies of some Coccinellid beetles. I. On Perilitus coccinellae (Schrank). Kontyu 37:147–166
Majerus M, Strawson V, Roy H (2006) The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol Entomol 31:207–215
Marco DA, Páez SA, Cannas SA (2002) Species invasiveness in biological invasions: a modelling approach. Biol Invasions 4:193–205
McClure MS (1986) Role of predators in regulation of endemic populations of Matsucoccus matsumurae (Kuwana) (Homoptera: Margarodidae) in Japan. Environ Entomol 15:976–983
McClure MS (1987) Potential of the Asian predator, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), to control Matsucoccus resinosae Bean and Godwin (Homoptera: Margarodidae) in the United States. Environ Entomol 16:224–230
Michaud JP (2001) Numerical response of Olla v-nigrum (Coleoptera: Coccinellidae) to infestations of Asian citrus psyllid, (Hemiptera: Psyllidae) in Florida. Fla Entomol 84:608–612
Michaud JP (2002) Biological control of Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae) in Florida: a preliminary report. Entomol News 113:216–222
Michaud JP (2004) Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biol Control 29:260–269
Michaud JP, Olsen LE (2004) Suitability of Asian citrus psyllid, Diaphorina citri, as prey for ladybeetles. BioControl 49:417–431
Mignault M-P, Roy M, Brodeur J (2006) Soybean aphid predators in Québec and the suitability of Aphis glycines as prey for three Coccinellidae. BioControl 51:89–106
Mooney HA, Drake JA (1989) Biological invasions: a SCOPE program overview. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmánek M, Williamson M (eds) Biological invasion: a global perspective. Scope 37. Wiley, Chichester
Musser FR, Shelton AM (2003a) Predation of Ostrinia nubilalis (Lepidoptera: Crambidae) eggs in sweet corn by generalist predators and the impact of alternative foods. Environ Entomol 32:1131–1138
Musser FR, Shelton AM (2003b) Factors altering the temporal and within-plant distribution of coccinellids in corn and their impact on potential intraguild predation. Environ Entomol 32:575–583
Musser FR, Nyrop JP, Shelton AM (2004) Survey of predators and sampling method comparison in sweet corn. J Econ Entomol 97:136–144
Nalepa CA, Kidd KA, Ahlstrom KR (1996) Biology of Harmonia axyridis (Coleoptera, Coccinellidae) in winter aggregations. Ann Entomol Soc Am 89:681–685
Nault BA, Kennedy 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
O’Dowd DJ, Green PT, Lake PS (2003) Invasional “meltdown” on an oceanic island. Ecol Lett 6:812–817
Ongagna P, Giuge L, Iperti G, Ferran A (1993) Cycle de développement d’Harmonia axyridis (Col. Coccinellidae) dans son aire d’introduction : le sud-est de la France. Entomophaga 38:125–128
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
Osawa N, Nishida T (1992) Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): the role of non-random mating. Heredity 69:297–307
Park Y-L, Obrycki JJ (2004) Spatio-temporal distribution of corn leaf Aphids (Homoptera: Aphididae) and ladybeetles (Coleoptera: Coccinellidae) in Iowa cornfields. Biol Control 31:210–217
Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2007) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl (this issue). doi:10.1007/s10526-007-9125-x
Petren K, Case TJ (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77:118–132
Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic cost of nonindigenous species in the United States. Bioscience 50:53–65
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288
Poutsma J, Loomans AJM, Aukema B, Heijerman T (2007) Predicting the potential geographical distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX model. BioControl (this issue). doi:10.1007/s10526-007-9140-y
Rabitsch W, Schuh R (2006) First record of the multicoloured Asian ladybird Harmonia axyridis (Pallas, 1773) in Austria. Beiträge Zur Entomofaunistik 7:161–164
Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN (2007) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Cocinella septempunctata and Adalia bipunctata. BioControl (this issue). doi:10.1007/s10526-007-9122-0
Saini ED (2004) Presencia de Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) en la provincia de Buenos Aires. Aspectos Biologicos y Morfologicos Ria 33:151–160
Sakurai H, Kawai T, Takeda S (1992) Physiological changes related to diapause of the lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae). Appl Entomol Zool 4:479–487
Schanderl H (1987) Détermination des conditions optimales d’élevage de la coccinelle Harmonia axyridis Pallas (Col., Coccinellidae), et possibilité d’une production continue à l’aide d’une proie de substitution, les œufs d’Ephestia kuehniella Zeller (Lep., Pyralidae). Dissertation, Université de Droit, d’Economie et des Sciences, d’Aix-Marseille III
Schanderl H, Almeida JM (1992) Introdução de Harmonia axyridis Pallas (Col., Coccinellidae) na ilha de S. Maria. Açoreana 7:401–406
Schanderl H, Ferran A, Larroque MM (1985) Les besoins trophiques et thermiques des larves de la coccinelle Harmonia axyridis Pallas. Agronomie 5:417–421
Schanderl H, Ferran A, Coderre D, Ventura A, Soares AO, Almeida JMP, Taveira J (1991) Capacidade de dispersão de Harmonia axyridis Pallas (Col., Coccinellidae) após uma largada inundativa para controlo de afídeos do Milho Rhopalosiphum padi L. e Sitobion avenae F. (Hom., Aphididae). Relatórios e Comunicações do Departamento de Biologia 20:59–64
Schneider N, Loomans AJM (2006) Sur la présence au Luxembourg de la coccinelle arlequin Harmonia axyridis (Pallas, 1773) (Insecta, Coleoptera, Coccinellidae). Bulletin de la Société des Naturalistes Luxembourgeois 106:71–74
Shapiro-Ilan DI, Cottrell TE (2005) Susceptibility of lady beetles (Coleoptera: Coccinellidae) to entomopathogenic nematodes. J Invertebr Pathol 89:150–156
Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, Oxford
Sidlyarevich VI, Voronin KE (1973) Trials on using Leis axyridis under glass. Zashchita Rastenii 6:24
SIFA (Servicio de información fitosanitaria de Almería) (2004) Organismos de control biológico
Silva L, Smith CW (2006) A quantitative approach to the study of non-indigenous plants: an example from the Azores archipelago. Biodivers Conserv 15:1661–1679
Simberloff D (1996) Risks of species introduced for biological control. Biol Conserv 78:185–192
Simberloff D (1989) Which insect introductions succeed and which fail? In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmánek M, Williamson M (eds) Biological invasion: a global perspective. Scope 37. Wiley, Chichester
Simberloff D (2004) Community ecology: is it time to move on? Am Nat 163:787–799
Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974
Snyder WE, Clevenger GM (2004) Negative dietary effects of Colorado potato beetle eggs for the larvae of native and introduced ladybird beetles. Biol Control 31:353–361
Snyder WE, Clevenger GM, Eigenbrode SD (2004) Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140:559–565
Soares AO, Serpa A (2007) Interference competition between ladybird beetle adults (Coleoptera: Coccinellidae): effects on the growth and reproductive capacity. Popul Ecol 49:37–43
Soares AO, Coderre D, Schanderl H (2001) Influence of phenotype on fitness parameters of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Eur J Entomol 98:287–293
Soares AO, Coderre D, Schanderl H (2003a) Effect of temperature and intraspecific allometry on predation by two phenotypes of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Environ Entomol 32:939–944
Soares AO, Elias RB, Resendes R, Figueiredo H (2003b) Contribution to the knowledge of the Coccinellidae (Coleoptera) fauna from the Azores islands. Arquipélago Life Mar Sci 20A:47–53
Soares AO, Coderre D, Schanderl H (2004) Dietary self-selection behaviour by the adults of the aphidophagous ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae). J Anim Ecol 73:478–486
Soares AO, Coderre D, Schanderl H (2005) Influence of prey quality on the fitness of two phenotypes of the adults of Harmonia axyridis. Entomol Exp Appl 114:227–232
Stals R, Prinsloo G (2007) Discovery of an alien invasive, predatory insect in South Africa. The multicoloured Asian ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). S Afr J Sci 103:123–126
Stastny M, Schaffner URS, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37
Stathas GJ, Eliopoulos PA, Kontodimas DC, Giannopapas J (2001) Parameters of reproductive activity in females of Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 98:547–549
Staverloekk A, Saethre MG, Haagvar E (2007) A review of the biology of the invasive harlequin ladybird Harmonia axyridis (Pallas, 1773) (Coleoptera, Coccinellidae). Nor J Entomol (in press)
Stewart LA, Dixon AFG (1989) Why big species of ladybird beetles are not melanic? Funct Ecol 3:165–177
Stuart RJ, Michaud JP, Olsen LE, McCoy CW (2002) Lady beetles as potential predators of the root weevil Diaprepes abbreviatus (Coleoptera: Curculionidae) in Florida citrus. Fla Entomol 85:409–416
Tan CC (1946) Mosaic dominance in the inheritance of color patterns in the lady-bird beetle, Harmonia axyridis. Genetics 31:195–210
Tan CC (1949) Seasonal variations of color patterns in Harmonia axyridis. Proceedings of the 8th international congress genetics, pp 669–670
Tedders WL, Schaefer PW (1994) Release and establishment of Harmonia axyridis (Coleoptera, Coccinellidae) in the southeastern United-States. Entomol News 105:228–243
Watanabe M (2002) Cold tolerance and myo-inositol accumulation in overwintering adults of a lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 99:5–9
Vermeij GJ (1996) An agenda for invasion biology. Biol Conserv 78:3–9
Vermeij GJ (2005) Invasion as expectation-A historical fact of life. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions—insights into ecology, evolution and biogeography. Sinauer Associates, Inc. Publishers, Massachusetts
Vitousek PM, Di Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as a global environment change. Am Sci 84:468–487
Vitousek PM, Di Antonio CM, Lloyd L Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16
Ware RL, Majerus MEN (2007) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl (this issue). doi:10.1007/s10526-007-9135-8
Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography-ecology, evolution and conservation. Oxford University Press, Oxford
Williamson M (1981) Island populations. Oxford University Press, Oxford
Williamson M (1996) Biological invasions. Chapman & Hall, London
Wise IL, Turnock WJ, Roughley RE (2001) New records of Coccinellid species for the province of Manitoba. Proc Entomol Soc Man 57:5–10
With KA, Pavuk DM, Worchuck JL, Oates RK, Fisher JL (2002) Threshold effects of landscape structure on biological control in agroecosystems. Ecol Appl 12:52–65
Yasuda H, Ohnuma N (1999) Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomol Exp Appl 93:63–67
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
Acknowledgements
The authors would like to thank Peter Brown for his helpful comments on Table 1 and for sending original references about geographical distribution of H. axyridis in Europe. Thanks are also due to Ivo Hodek and Luis Silva, for their helpful comments on the following topics, overwintering of ladybird beetles and vegetation cover on the Azores, respectively.
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Soares, A.O., Borges, I., Borges, P.A.V. et al. Harmonia axyridis: What will stop the invader?. BioControl 53, 127–145 (2008). https://doi.org/10.1007/s10526-007-9141-x
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DOI: https://doi.org/10.1007/s10526-007-9141-x