Harmonia axyridis
(harlequin ladybird)

Pictures

Picture	Title	Caption	Copyright
Title Adult Caption Harmonia axyridis (harlequin ladybird); adult. The beetles are 5-8mm long and 4-6.5mm wide. The body is moderately convex, shortened, oval and approximately 4/5 wide as long. Copyright ©Scott Bauer/USDA-ARS	Adult	Harmonia axyridis (harlequin ladybird); adult. The beetles are 5-8mm long and 4-6.5mm wide. The body is moderately convex, shortened, oval and approximately 4/5 wide as long.	©Scott Bauer/USDA-ARS
Title Adult Caption Harmonia axyridis (harlequin ladybird); typical adult of f. succinea. Copyright ©Mike Majerus/UK Ladybird Survey	Adult	Harmonia axyridis (harlequin ladybird); typical adult of f. succinea.	©Mike Majerus/UK Ladybird Survey
Title Adult (f. axyridis) Caption Harmonia axyridis (harlequin ladybird); orange and red forms may be patterned with anything from 0 to 21 black spots (f. succinea complex), or may display a grid-like black pattern (f. axyridis). Copyright ©Remy Ware/UK Ladybird Survey	Adult (f. axyridis)	Harmonia axyridis (harlequin ladybird); orange and red forms may be patterned with anything from 0 to 21 black spots (f. succinea complex), or may display a grid-like black pattern (f. axyridis).	©Remy Ware/UK Ladybird Survey
Title Adult (f. spectabilis) Caption Harmonia axyridis (harlequin ladybird); black or melanic forms usually have two (f. conspicua) or four (f. spectabilis) large orange or red spots. Copyright ©Mike Majerus/UK Ladybird Survey	Adult (f. spectabilis)	Harmonia axyridis (harlequin ladybird); black or melanic forms usually have two (f. conspicua) or four (f. spectabilis) large orange or red spots.	©Mike Majerus/UK Ladybird Survey
Title Adult (f. conspicua) Caption Harmonia axyridis (harlequin ladybird); black or melanic forms usually have two (f. conspicua) or four (f. spectabilis) large orange or red spots. Copyright ©Mike Majerus/UK Ladybird Survey	Adult (f. conspicua)	Harmonia axyridis (harlequin ladybird); black or melanic forms usually have two (f. conspicua) or four (f. spectabilis) large orange or red spots.	©Mike Majerus/UK Ladybird Survey
Title Adult (f. succinea) Caption Harmonia axyridis (harlequin ladybird); adults are highly polymorphic for both colour and pattern. The ground colour may be orange, red or black. Orange and red forms may be patterned with anything from 0 to 21 black spots (f. succinea complex). Copyright ©Mike Majerus/UK Ladybird Survey	Adult (f. succinea)	Harmonia axyridis (harlequin ladybird); adults are highly polymorphic for both colour and pattern. The ground colour may be orange, red or black. Orange and red forms may be patterned with anything from 0 to 21 black spots (f. succinea complex).	©Mike Majerus/UK Ladybird Survey
Title Similar species Caption Hippodamia convergens (convergent ladybird); adult for comparison with H. axyridis. Copyright ©Russ Ottens/University of Georgia/Bugwood.org - CC BY 3.0 US	Similar species	Hippodamia convergens (convergent ladybird); adult for comparison with H. axyridis.	©Russ Ottens/University of Georgia/Bugwood.org - CC BY 3.0 US
Title Similar species Caption Coccinella septempunctata (seven-spot ladybird); adult, for comparison with H. axyridis. Ahlen, Germany. April 2011. Copyright ©Quartl/via wikipedia - CC BY-SA 3.0	Similar species	Coccinella septempunctata (seven-spot ladybird); adult, for comparison with H. axyridis. Ahlen, Germany. April 2011.	©Quartl/via wikipedia - CC BY-SA 3.0
Title Copulation Caption Harmonia axyridis (harlequin ladybird); adults of f. succinea, mating. Copyright ©Mike Majerus/UK Ladybird Survey	Copulation	Harmonia axyridis (harlequin ladybird); adults of f. succinea, mating.	©Mike Majerus/UK Ladybird Survey
Title Ova Caption Harmonia axyridis (harlequin ladybird); eggs are oval and ca.1.2 mm long. They are pale yellow when first laid, but progressively turn a darker yellow. Copyright ©Mike Majerus/UK Ladybird Survey	Ova	Harmonia axyridis (harlequin ladybird); eggs are oval and ca.1.2 mm long. They are pale yellow when first laid, but progressively turn a darker yellow.	©Mike Majerus/UK Ladybird Survey
Title Larva Caption Harmonia axyridis (harlequin ladybird); larva feeding on an aphid. Copyright ©Mike Majerus/UK Ladybird Survey	Larva	Harmonia axyridis (harlequin ladybird); larva feeding on an aphid.	©Mike Majerus/UK Ladybird Survey
Title Ecdysis Caption Harmonia axyridis (harlequin ladybird); larval ecdysis. Copyright ©Mike Majerus/UK Ladybird Survey	Ecdysis	Harmonia axyridis (harlequin ladybird); larval ecdysis.	©Mike Majerus/UK Ladybird Survey
Title Pupa Caption Harmonia axyridis (harlequin ladybird); pupae of H. axyridis are exposed and the exuvium of the fourth instar remains attached posteriorly to the pupa at the point of substrate attachment. Copyright ©Mike Majerus/UK Ladybird Survey	Pupa	Harmonia axyridis (harlequin ladybird); pupae of H. axyridis are exposed and the exuvium of the fourth instar remains attached posteriorly to the pupa at the point of substrate attachment.	©Mike Majerus/UK Ladybird Survey
Title Natural enemy Caption Harmonia axyridis (harlequin ladybird); adult, attacked by Hesperomyces virescens, a Laboulbeniales parasitic fungi. Copyright ©Gilles San Martin, Namur, Belgium/via flickr - CC BY-SA 2.0	Natural enemy	Harmonia axyridis (harlequin ladybird); adult, attacked by Hesperomyces virescens, a Laboulbeniales parasitic fungi.	©Gilles San Martin, Namur, Belgium/via flickr - CC BY-SA 2.0
Title Natural enemy Caption Harmonia axyridis (harlequin ladybird); adult, attacked by Hesperomyces virescens, a Laboulbeniales parasitic fungi. Copyright ©Gilles San Martin, Namur, Belgium/via flickr - CC BY-SA 2.0	Natural enemy	Harmonia axyridis (harlequin ladybird); adult, attacked by Hesperomyces virescens, a Laboulbeniales parasitic fungi.	©Gilles San Martin, Namur, Belgium/via flickr - CC BY-SA 2.0
Title Inter-species predation Caption Harmonia axyridis (harlequin ladybird); two larvae feeding on a Coccinella septempunctata (7-spot ladybird) larva. Copyright ©Mike Majerus/UK Ladybird Survey	Inter-species predation	Harmonia axyridis (harlequin ladybird); two larvae feeding on a Coccinella septempunctata (7-spot ladybird) larva.	©Mike Majerus/UK Ladybird Survey

Identity

Preferred Scientific Name

• Harmonia axyridis Pallas

Preferred Common Name

• harlequin ladybird

Other Scientific Names

• Anatis circe Mulsant
• Coccinella 19-sinata Faldermann
• Coccinella axyridis Pallas
• Coccinella conspicua Faldermann
• Coccinella succinea Hop
• Cocinella bisex-notata Herbst
• Harmonia spectabilis Faldermann
• Leis axyridis Pallas
• Ptychanatis axyridis Pallas
• Ptychanatis yedoensis Takizawa

International Common Names

• English: multicoloured Asian ladybird; multicoloured ladybird
• Portuguese: mariquita asiática

Local Common Names

• Belgium: veelkeurig aziatisch lieveheersbeestje
• France: coccinelle asiatique multicolore
• Germany: Asiatische Marienkäfer
• Netherlands: veelkeurig aziatisch lieveheersbeestje
• Poland: biedronka azjatycka; harlekin
• Spain: mariquita asiática
• USA: Asian lady beetle; Halloween beetle; Japanese ladybeetle; multicolored Asian lady beetle; multivariate ladybeetle; pumpkin beetle; southern ladybeetle

EPPO code

• HARNAX (Harmonia axyridis)

Summary of Invasiveness

H. axyridis, a species of Asian origin, has been used as a biological control agent against aphids worldwide. The first releases were made in North America in 1916, but it was not until 1988 that the first individuals were found in the wild. Since then, it has rapidly invaded most of North America and Europe, and it is now spreading in other regions such as South America and South Africa. In most invaded regions, numbers have increased exponentially and H. axyridis has quickly become the most abundant ladybird in a wide range of habitats. The invasion of H. axyridis causes concern for the populations of native ladybirds and other aphidophagous insects, which it may displace through intraguild predation and competition for resources. It is also regarded as a grape [Vitis vinifera] and wine pest, and as a human nuisance because it aggregates in buildings when seeking overwintering sites in the autumn.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Coleoptera
•                         Family: Coccinellidae
•                             Genus: Harmonia
•                                 Species: Harmonia axyridis

Notes on Taxonomy and Nomenclature

H. axyridis is a member of the Coccinellidae family within the Coleoptera. There are approximately 5200 species of Coccinellidae described worldwide. In 1990, Fürsch proposed a system based on that originally constructed by Chazeau et al. (1989), which includes six subfamilies within the Coccinellidae. Hodek and Honek (1996) proposed seven subfamilies: Coccidulinae, Scymninae, Chilocorinae, Ortaliinae, Coccinellinae, Epilachninae and Sticholotidinae. H. axyridis is within the subfamily Coccinellinae. The tribes of this subfamily share a large number of truly synapomorphic characters (shared traits derived from a common ancestor).

Coccinellids are small to medium sized beetles (1-10 mm long) and are usually round or oval. The pronotum is broader than it is long and extends forward at the margins. The head retracts under the pronotum and the antennae are short and clubbed. The legs are also short and retract under the body. The tarsi have four segments, but the third is very small and often hidden inside the deeply lobed second segment (Majerus and Kearns, 1989). The common names 'ladybird', 'ladybug' and 'ladybeetle' refer to members of the Coccinellidae that have brightly coloured elytra and are conspicuous. H. axyridis is designated as a ladybird within the Coccinellidae. Some species of coccinellid are highly conserved in colour form whereas others are highly polymorphic. H. axyridis is highly variable and over 100 colour forms have been identified worldwide. The distribution of colour forms varies geographically and some forms also vary seasonally. For example, the dark forms (form spectabilis and f. conspicua) are common in Asia (native range), but rare in the USA where the orange colour forms (f. succinea complex) dominate (Hodek and Honek, 1996). In the UK, H. axyridis f. succinea is the dominant colour form (Majerus and Roy, 2006).

H. axyridis has many common names worldwide such as harlequin ladybird, multicoloured Asian ladybird, multicoloured ladybird, etc.; however, many countries do not have a species specific common name for H. axyridis, but do have a general name for ladybirds, for example, marihøne (Norway) and mariehøne (Denmark).

Description

Adults

The adults are 5-8 mm long and 4-6.5 mm wide. The body is convex (moderately), shortened oval and approximately 4/5 wide as long (Kuznetsov, 1997). The head can be black, yellow or black with yellow markings. The pronotum is creamish-yellow with black markings. These black markings can be in the form of four black spots, two curved lines, a black M-shaped mark or a solid black trapezoid (Chapin and Brou, 1991). Elytra range from yellow-orange to red with 0 to 21 black spots (Majerus and Roy, 2006) or may be black with red spots. A transverse plica is often situated above the apex of the elytra.

Adult H. axyridis are highly polymorphic for both colour and pattern (Majerus and Roy, 2006). The ground colour may be orange, red or black. Orange and red forms may be patterned with anything from 0 to 21 black spots (f. succinea complex), or may display a grid-like black pattern (f. axyridis). Black or melanic forms usually have two (f. conspicua) or four (f. spectabilis) large orange or red spots. Other forms with bars or stripes, or large patches of pale colour on a black ground colour (f. aulica) also occur in the native range of H. axyridis. The colour polymorphism of H. axyridis is hereditary and associated with multiple alleles (Hodek and Honek, 1996). However, the larval diet and temperatures to which pupae are exposed also influence colour and pattern (Sakai et al., 1974; Grill and Moore, 1998). It is interesting to note that the dark forms (such as f. spectabilis and f. conspicua) are common in parts of Asia (native range), but rare in the USA where the succinea complex of forms occurs (Hodek and Honek, 1996). In the UK, H. axyridis f. succinea is the dominant colour form (Majerus et al., 2005). More recently, studies have highlighted the effects of temperature during pupation on the spot size of H. axyridis f. succinea; eclosion at cool temperatures results in larger spot size than at warmer temperatures (Michie et al., 2011).

Eggs

The eggs are approximately 1.2 mm long and are oval shaped. The eggs are pale-yellow when first laid, but progressively turn a darker yellow. Twenty-four hours prior to hatching the eggs turn grey-black.

Larvae

The first-instar larvae are approximately 2 mm long and reach 7.5-10.5 mm by the fourth (final) instar. The larvae are covered with scoli (branched setae). These scoli are three pronged on the dorsal surface of the abdomen and two pronged on the dorsal-lateral surface. The first-instar larvae are usually darker (black) than later instars. El-Sebaey and El-Gantiry (1999) noted a red spot located medially on the sixth abdominal segment of the first instar. The second instars have a similar appearance to the first instars although the first and sometimes first and second abdominal segments have an orange colouration in the dorsal-lateral regions. The orange colouration is more pronounced in the third instar and covers the dorsal and dorsal-lateral areas of the first abdominal segment and the dorsal lateral regions of the second to fifth segments. The fourth instar is very similar in colouration to the third, but the scoli of the dorsal regions of the fourth and fifth abdominal segments are also orange (Sasaji, 1977).

Pupae

The pupae are exposed and the exuvium of the fourth instar remains attached posteriorly to the pupa at the point of substrate attachment.

Distribution

H. axyridis is native to central and eastern Asia, with a range extending from the Altai Mountains to the Pacific Coast and Japan (west to east) and from central Siberia to southern China (north to south) (Dobzhansky, 1933; Chapin, 1965; Sasaji, 1971; Koch, 2003). It is known to have been introduced (both intentionally and unintentionally) to Europe, North America, South America, the Middle East and South Africa (Stals and Prinsloo, 2007; Brown et al., 2008a). Dead beetles have also been recently intercepted in Australia (Smith and Fisher, 2008). Information on the global distribution of H. axyridis is far from comprehensive; however, there is a high probability that it occurs widely, mainly through intentional introductions coupled with natural dispersal.

With reference to the distribution table, please note that all the dates refer to first observations or establishment in the wild, not the date of first intentional release. For some countries (Spain, Sweden, Norway, Alberta and Hungary), only a few specimens have been found and establishment is not yet certain, but probable.

Brown et al. (2008a) also mention that there were releases of H. axyridis in Portugal, Canary islands, Ukraine and Belarus (and in Hawaii, according to Poutsma et al. (2008)), but evidence of establishment is lacking (M Kenis, CABI, personal communication, 2008).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

H. axyridis has a long history of introductions as a biological control agent of coccids and aphids around the world. The first release in North America was in 1916 and since this time it has been repeatedly released in the USA as a classical biological control agent (Gordon, 1985). H. axyridis was favoured for the biological control of aphids because of its size, diverse dietary range, efficiency as a predator and wide niche colonization ability. These very traits now contribute to the invasive nature of this beetle. However, initial introductions of H. axyridis to USA agroecosystems failed to establish until 1988, when populations were found in Louisiana (Chapin and Brou, 1991). There is uncertainty surrounding the origin of these populations and whether they resulted from intentionally released beetles or accidental introductions (Day et al., 1994; Tedders and Schaefer, 1994). H. axyridis has now spread across most of the USA and into Canada. Indeed it has become the most common aphidophagous coccinellid in many regions of the USA (Tedders and Schaefer, 1994; Dreistadt et al., 1995; Smith et al., 1996; Colunga-Garcia and Gage, 1998; Hesler et al., 2001). H. axyridis can now be found in all USA states except for Montana, Wyoming and parts of the south-western USA; it is also established in South America (de Almeida and da Silva, 2002) and South Africa (Stals and Prinsloo, 2007).

H. axyridis has been intentionally released as a biological control agent in at least 12 European countries since 1982. Brown et al. (2008a) have documented the introduction history and spread of H. axyridis in Europe. The first feral populations were found in Germany in 1999 and in Belgium in 2001. Since then numbers have increased exponentially. It is now established in at least 15 countries, from Denmark in the north to Italy in the south, and from Great Britain in the west to Czech Republic and Hungary in the east. Based on climate matching models, Poutsma et al. (2008) predict that H. axyridis may establish in most of Europe as well as in many temperate and subtropical regions worldwide.

Please note that only the intentional introductions have been included in the Introductions table. Clearly the beetle has often been introduced unintentionally because it became established in countries where no releases were made (e.g. UK, South Africa, Brazil and many European countries), but the precise pathways are not known. It is also often unclear whether it has entered countries by itself or has been transported by humans (e.g. in the UK) (M Kenis, CABI, personal communication, 2008).

Introductions

Risk of Introduction

H. axyridis pupae have been found on imported cut flowers and fruit (Majerus et al., 2005b). Therefore imports of this kind represent a risk in terms of movement of H. axyridis.

With reference to the Pathway tables, there is a chance that the adults can hide in containers because they occupy such places in the autumn for overwintering (M Kenis, CABI, personal communication, 2008).

Habitat

H. axyridis is reported to be primarily a polyphagous arboreal species that inhabits orchards, forest stands and old-field vegetation (Hodek, 1973; McClure, 1986; Chapin and Brou, 1991; Tedders and Schaefer, 1994; Coderre et al., 1995; LaMana and Miller, 1996; Brown and Miller, 1998); however, it has the ability to exploit resources in a wide range of habitats including agricultural ecosystems, riparian zones, urban areas and wetlands (NBII, 2005; Adriaens et al., 2008; Roy and Brown, 2015). Comprehensive studies on the establishment of H. axyridis in south-western Michigan, USA, where the landscape is one of agricultural fields interspersed with deciduous and coniferous plantations (Burbank et al., 1992; Colunga-Garcia and Gage, 1998) have demonstrated that H. axyridis thrives and breeds in agricultural habitats, such as forage crops (LaMana and Miller, 1996; Buntin and Bouton, 1997), maize (Zea mays), soyabean (Glycine max) and wheat (Triticum aestivum) (Colunga-Garcia and Gage, 1998) and conifer woodland (McClure, 1986). Indeed within 4 years of its arrival in Michigan, H. axyridis had become a dominant coccinellid, found in all the habitats monitored (Colunga-Garcia and Gage, 1998). Further evidence to support the eurytopic nature of H. axyridis comes from its extensive native Asian range and its recent successful dispersal across North America and throughout Europe (Brown et al., 2008a). This ability to exploit a diverse range of habitats suggests that H. axyridis has the potential to spread and invade a wide range of ecosystems.

With reference to the Habitat list, please note that in cultivated areas, this beetle is at the same time beneficial (in biocontrol) and harmful for indigenous ladybird species. The situation in the invaded regions has been indicated in the Habitat list. In its native region, it is found in the same habitat, but the status is natural and productive/non-natural (M Kenis, CABI, personal communication, 2008).

Habitat List

Hosts/Species Affected

H. axyridis has recently been designated pest status of fruit production and processing (Koch, 2003). As insect prey become scarce in the autumn, adult H. axyridis begin to aggregate and feed on fruits such as apples (Malus domestica), pears (Pyrus communis) and grapes (Vitis vinifera). This is problematic to orchard crops and vineyards in particular. Not only do H. axyridis cause blemishing to the fruit, but they are hard to remove from clusters of grapes and so get crushed during harvest and crop processing. The toxic alkaloids contained within H. axyridis taint the vintage (Ejbich, 2003).

The potential threat that H. axyridis poses to wildlife is more worrying than its impacts on crops. H. axyridis is a polyphagous predator and as such has been used widely as a biological control agent of pest aphids and scale insects. However, a wide range of literature sources (Hironori and Katsuhiro, 1997; Cottrell and Yeargan, 1998; Phoofolo and Obrycki, 1998; Dixon, 2000; Lynch et al., 2001; Koch et al., 2003; Pell et al., 2008; Ware and Majerus, 2008; Ware et al., 2008) document that H. axyridis consume non-pest insects including: immature stages of many species of coccinellids (Adalia bipunctata, Adalia decempunctata, Calvia quatuordecimguttata, Coleomigilla maculata, Coccinella quinquepunctata, Coccinella septempunctata, Coccinella septempunctata brucki, Cyclomeda sanguinea, Eocaria muiri, Harmonia quadripunctata, Hippodamia variegata, Propylea japonica and Propylea quatuordecimpunctata); one nymphalid (Danaus plexippus) and one Chrysopidae (Chrysoperla carnea). It is widely accepted that this list is far from exhaustive because of the highly polyphagous nature of H. axyridis. H. axyridis is a voracious predator and as such has the capacity to directly outcompete other aphid and coccid predators, in addition to acting as an intra-guild predator, thus posing a serious risk to native biodiversity.

H. axyridis can also directly impact on humans through its aggregation behaviour. In the late autumn, H. axyridis migrate to overwintering sites and form spectacular aggregations. Buildings are a preferred overwintering location of H. axyridis in urban localities and the swarms of H. axyridis in homes may cause a human nuisance. Furthermore H. axyridis has been reported to bite humans and some people have developed an allergic rhinoconjunctivitis (Yarbrough et al., 1999; Magnan et al., 2002).

Host Plants and Other Plants Affected

Growth Stages

List of Symptoms/Signs

Biology and Ecology

Genetics

The chromosome number of H. axyridis is not yet confirmed. Most species of Coccinellidae have a chromosome number of 10 (2n = 20). The closely related species, Harmonia quadripunctata, has a chromosome number of 7 (2n =14). It is expected that the chromosome number of H. axyridis will be within this range. H. axyridis c value = 0.34 (Gregory et al., 2003).

The elytra and pronotum colour and pattern of H. axyridis adults are highly polymorphic. This variation has been shown to have a genetic basis, controlled by a multi-allelic gene, with melanic forms generally being genetically dominant to non-melanic forms (Hosino, 1933, 1936; Tan and Li, 1934; Komai, 1956; Sasaji, 1971). There is variation globally in the colour patterns found and frequency of forms. For example, only f. conspicua, f. spectabilis, and forms of the succinea complex have been recorded in the UK: f. axyridis, which is the predominant form over large parts of central Russia, and the rarer Asian forms have not been found (Majerus and Roy, 2006).

The main colour pattern morphs are clearly under genetic control; however, environmental factors also influence the elytral pattern variation. Pupal exposure to low temperatures leads to slow imaginal development, resulting in forms of the succinea complex having more and larger spots, which are frequently fused, one into another (Tan and Li, 1934; Tan and Li, 1946). This increase in the deposition of melanic pigments is likely to be adaptive through thermal melanism. In comparison to less melanised individuals, these adults will remain active at lower temperatures and have a longer opportunity to forage to store resources in their fat body for the winter. From a survey of pupae collected in London, UK, during autumn (October and November, 2004) it was apparent that the majority were very heavily spotted, and subsequent breeding experiments using these beetles showed that their large, fused spots were not inherited, indicating an environmental cause (Majerus and Roy, 2006). Further research indicated an effect of temperature during pupation on spot size (Michie et al., 2011). The natural genetic variation in H. axyridis provides considerable scope for adaptive changes in the developmental rate and size of this species (Grill et al., 1997).

Physiology and Phenology

H. axyridis is considered bivoltine in much of Asia (Sakurai et al., 1992; Osawa, 2000), North America (LaMana and Miller, 1996; Koch and Hutchison, 2003) and Europe (Ongagna et al., 1993). Although in favourable conditions it can be multivoltine and up to four or five generations per year have been observed (Wang, 1986; Katsoyannos et al., 1997). Many British coccinellids, such as Coccinella septempunctata, Anatis ocellata and Exochomus quadripustulatus, require a dormancy period before becoming reproductively mature (Majerus and Kearns, 1989) and so are univoltine. H. axyridis does not have such a requirement, although in very hot dry summers it undergoes summer dormancy. Therefore, in temperate regions H. axyridis can breed continuously throughout the summer. Indeed in England it is not uncommon to see thelarvae of H. axyridis feeding and subsequently pupating throughout November. This indicates the late activity of H. axyridis; all native British aphidophagous coccinellids disperse to overwintering sites from September to October. This prolonged breeding confirms the continual breeding of the species if food is available and temperatures are not too low. Although these larvae eclose when aphid populations have declined to very low levels, their wide dietary range (including intra-guild predation) is likely to increase the survival of these late-season larvae. Combinations of a range of other foods (coccids, adelgids, psyllids, honeydew and the eggs, larvae and pupae of many insects including conspecifics) are sufficient to ensure some successful development (Tedders and Schaefer, 1994; Hodek, 1996; Koch, 2003).

H. axyridis exhibits pupal and adult colour pattern plasticity and this factor may further contribute to the successful development of individuals produced late-season. The pupal colour of H. axyridis ranges from almost completely orange to almost completely black, depending on temperature; the lower the temperature experienced by a final-instar larva, the darker the pupa that is produced. This is adaptive because darker colours absorb more heat allowing faster adult development and earlier eclosion in cool conditions (Hodek, 1958; Majerus, 1994; Michie et al., 2011).

Reproductive Biology

H. axyridis undergo a holometabolous (complete metamorphosis) life cycle consisting of egg, four larval instars, pre-pupa, pupa and adult. An adult H. axyridis produces 20-50 eggs per day. This equates to 1000-4000 in her life. The development of the immature stages is dependent on a variety of factors including temperature and diet. In temperate regions, the egg stage will take 4-5 days, the larval stage takes approximately 3 weeks and the pupal stage takes 1 week. The adults will typically live for a year. The adult ladybirds are reproductively active for approximately 3 months, but some species of coccinellid, such as Coccinella septempunctata (seven-spot ladybird), require a period of winter dormancy (diapause) before they become reproductively mature. However, adult H. axyridis can reproduce without a dormancy period and so they typically have two generations a year in much of Asia, North America and Europe (Koch, 2003). In regions with an extended warm season they may have up to five generations (Wang, 1986).

Environmental Requirements

The wide latitudinal and longitudinal range of H. axyridis in Asia (native range) shows that it can develop and breed in both warm and cool climes. This is further supported by the establishment and spread of H. axyridis in the USA, from sub-tropical Florida in the south to cold temperate regions of Canada in the north. Lamana and Miller (1998) demonstrated that H. axyridis is well-adapted to winter temperatures below freezing and to summer temperatures of 30°C. Such temperatures are similar to the range that H. axyridis will experience in temperate regions and so it is unlikely that climatic factors will prevent the spread of H. axyridis.

H. axyridis has been shown to reproduce successfully in a wide range of climates, whereas many species of coccinellid are more habitat and niche-specific. Therefore, if the predicted changes in global climate are realised, the climatic adaptability of H. axyridis may give it a competitive advantage over some of the more niche-specific ladybirds and other aphidophagous predators that are less climatically adaptable.

Climate

Latitude/Altitude Ranges

Air Temperature

Rainfall

Rainfall Regime

Natural enemies

Notes on Natural Enemies

H. axyridis contains toxic alkaloids and secretes these in reflex blood when attacked. H. axyridis are brightly coloured (aposematic) to warn potential natural enemies of the toxins they contain. Despite this, a number of predators, parasitoids and pathogens attack these ladybirds. These are reviewed by Kenis et al. (2008). However, H. axyridis generally has a low susceptibility to natural enemies within the invaded range (Roy et al., 2008; Berkvens et al., 2010; Roy et al., 2011a; Roy et al., 2011b; Comont et al., 2014).

Several predators, including a few species of birds, true bugs and some other ladybirds, will feed on H. axyridis. However, many vertebrate predators avoid these beetles.

Only two polyphagous parasitoids were reared from H. axyridis in its introduction range and these are not considered as important mortality factors. The tachinid fly, Strongygaster triangulifera was found in adult beetles in North Carolina, USA and the braconid wasp, Dinocampus coccinellae was reared from adults in North America and Europe. The survival of D. coccinellae in H. axyridis appears much lower than in other ladybirds.  Information on parasitism in the native range of the ladybird is scarce. D. coccinellae and a tachinid fly, Medina luctuosa are recorded from adults, and two phorid flies, Phalacrotophora philaxyridis and Phalacrotophora fasciata have been reared from pupae.

H. axyridis are susceptible to the soil-borne fungal pathogen, Beauveria bassiana. Although the transmission of this fungus to ladybirds is poorly understood, it is thought to infect ladybirds overwintering in leaf litter with close contact to the soil, and so is unlikely to affect H. axyridis significantly because these ladybirds favour elevated positions for overwintering. Another fungal entomopathogen, Hesperomyces virescens, was found on H. axyridis in North America, infecting 22-38% of the adult beetles at the beginning of the winter and 62% by the end of winter (Nalepa and Weir, 2007). This fungus has subsequently been found on H. axyridis adults in London (UK) However, the impact of the fungus is unclear. It does not appear to affect survival, but heavy infections may impede flight, foraging and mating.

A male-killing bacterium has been isolated from H. axyridis in Asia. This vertically transmitted Spiroplasma kills males early in embryogenesis and so results in female biased sex ratios. Neonate female siblings consume the inviable male eggs and, thus, are less likely to starve than first-instar larvae produced by females who do not carry the male-killer (Majerus et al., 1998). There is no evidence to suggest that H. axyridis in the USA have biased sex ratios and therefore it is unlikely that they possess the male-killing bacterium. It is not yet known whether H. axyridis in other parts of the world harbour male-killers.

H. axyridis is cannibalistic; indeed cannibalism is thought to be important in the regulation of H. axyridis populations. The rate of cannibalism increases as aphid density declines and certainly provides nutritional benefits. Interestingly, H. axyridis recognize their kin and are less likely to cannibalise a sibling than a non-related individual (Michaud, 2003). If normal prey becomes scarce, larval mortality can be very high, with in excess of 95% of larvae failing to survive to adulthood, and in such circumstances cannibalism can be essential for survival.

Means of Movement and Dispersal

Natural Dispersal

H. axyridis is a highly dispersive coccinellid species. It flies readily between host plants during breeding periods, seeking high-density aphid populations. In both Asia and America it migrates over long distances to and from dormancy sites (I. Zakharov, [address available from CABI], personal communication, 2008). Flights to winter dormancy sites may start as early as late August in Siberia; however, most take place from late September through to late November (Liu and Qin, 1989; Sakurai et al., 1993). H. axyridis adults spend the adverse winter months in a state of dormancy in large aggregations, often on prominent, light-coloured objects such as rocky outcrops of mountains or light-coloured buildings (Tanagishi, 1976; Obata, 1986). As the environmental conditions become favourable for activity in the spring, these ladybirds undertake another dispersal flight to seek food and suitable host plants on which to breed (LaMana and Miller, 1996). H. axyridis are able to travel 18 km in a “typical” high-altitude flight, but up to 120 km if flying at higher altitudes, indicating a high capacity for long-distance dispersal (Jeffries et al., 2013). Such dispersal may result in a considerable increase in their distribution.

The distribution and abundance of H. axyridis in the USA provides an indication of the rapid colonisation ability of this beetle. Just 2 years after H. axyridis had initially established in Georgia, its spread was documented throughout the entire state and into the neighbouring states of Florida and South Carolina (Tedders and Schaefer, 1994). Such rapid dispersal, coupled with the polyphagous nature of H. axyridis and low habitat or host plant specificity, will aid the spread of this beetle.

Accidental Introduction

H. axyridis has not been intentionally introduced into the UK or South Africa. Therefore, the arrival of this species to these two countries is likely to be through unintentional introduction (Majerus et al., 2005b; Stals and Prinsloo, 2007) and dispersal from neighbouring countries.

Intentional Introduction

H. axyridis has a long history of introductions as a biological control agent of coccids and aphids around the world. The first release in North America was in 1916 and since this time it has been repeatedly released in the USA as a classical biological control agent (Gordon, 1985). H. axyridis was favoured for the biological control of aphids because of its size, diverse dietary range, efficiency as a predator and wide niche colonisation ability. These very traits now contribute to the invasive nature of this beetle. However, initial introductions of H. axyridis to USA agroecosystems failed to establish until 1988, when populations were found in Louisiana (Chapin and Brou, 1991). There is uncertainty surrounding the origin of these populations and whether they resulted from intentionally released beetles or accidental introduction (Day et al., 1994; Tedders and Schaefer, 1994). The species has now spread across most of the USA and into Canada. Indeed it has become the most common aphidophagous coccinellid in many regions of the USA (Tedders and Schaefer, 1994; Dreistadt et al., 1995; Smith et al., 1996; Colunga-Garcia and Gage, 1998; Hesler et al., 2001). H. axyridis can now be found in all USA states except for Montana, Wyoming and parts of south-western USA; it was also intentionally introduced in Argentina in the late 1990s and became subsequently established in Argentina and Brazil (de Almeida and da Silva, 2002; Koch et al., 2006).

H. axyridis has been intentionally released as a biological control agent in at least 12 European countries since 1982. Brown et al. (2008a) have documented the introduction history and spread of H. axyridis in Europe. The first feral populations were found in Germany in 1999 and in Belgium in 2001. Since then numbers have increased exponentially. It is now established in at least 15 countries, from Denmark in the north to Italy in the south, and from Great Britain in the west to Czech Republic and Hungary in the east. Based on climate matching models, Poutsma et al. (2008) predict that H. axyridis may establish in most of Europe as well as in many temperate and subtropical regions worldwide.

Pathway Causes

Pathway Vectors

Plant Trade

Wood Packaging

Impact Summary

Environmental Impact

Impact on Biodiversity

Monitoring and research in the USA is demonstrating that H. axyridis is adversely affecting other aphidophages. Brown and Miller (1998) found that the abundance of native coccinellids in apple (Malus domestica) orchards in West Virginia decreased over a 13-year period following the establishment of both Coccinella septempunctata (an introduced species in the USA) and H. axyridis. A 9-year study in agricultural landscapes in Michigan showed that populations of Brachiacantha ursina, Cycloneda munda and Chilocorus stigma had all declined following the establishment of H. axyridis (Colunga-Garcia and Gage, 1998). Similarly a 5-year study in citrus groves indicated that an increase in H. axyridis was correlated to a decline in Cycloneda sanguinea (Michaud, 2002c) whereas Alyokhin and Sewell (2004) observed a decline in populations of Coccinella tranversoguttata and Hippodamia tredecimpunctata in potato fields in Maine after the arrival of H. axyridis. At a larger scale, Harmon et al. (2007) highlighted the dramatic decline of Adalia bipunctata in North America after the arrival of H. axyridis and C. septempunctata. It is proposed that H. axyridis is likely to have a negative effect on other aphidophages in three ways: resource competition, intraguild predation and intra-specific competition.

H. axyridis is a voracious aphid predator; the adults consume up to 65 aphids per day (Hukusima and Kamei, 1970; Luo, 1987; Hu et al., 1989; Lucas et al., 1997). The adults are typically active for 30 to 120 days (He et al., 1994; El-Sebaey and El-Gantiry, 1999; Soares et al., 2001) and so can consume in excess of 5000 aphids, or equivalent of other insect prey, during their lives. Michaud (2002c) demonstrated that H. axyridis was more voracious, fertile and fecund than C. sanguinea and consequently directly out-competed C. sanguinea. The voracity, wide dietary range, dispersability and potential to continuously breed gives H. axyridis the potential to significantly reduce the prey species of many less competitive aphidophages. So traits that are considered favourable in terms of potential for controlling pest insects in crop and horticultural systems will, in other habitats, contribute to a reduction in biodiversity and concomitant declines in native beneficial predators and parasitoids of aphids and coccids. For example, both adult and larval H. axyridis feed on parasitized aphids that have not yet mummified (Nakata, 1995) and so will impact directly on parasitoids. The presence of H. axyridis larvae within an aphid colony may reduce the rate that parasitoids oviposit (Takizawa et al., 2000) and so reduce their numbers.

It is apparent that H. axyridis is one of the top predators within the guilds of aphidophages and coccidophages and it will survive on a varied diet with the potential to engage in intra-guild predation, including other species of ladybird (Yasuda and Ohnuma, 1999; Ware and Majerus, 2008; Ware et al., 2008). In Japan, it has been reported that H. axyridis repeatedly arrived in lucerne (Medicago sativa) fields a short time after a number of other ladybirds, allowing H. axyridis to feed on the prepupae and pupae of other coccinellids (Takahashi, 1989). Indeed, reports of H. axyridis larvae and adults feeding on the immature stages of other aphidophagous insects are common (Koch, 2003). In contrast, there are few reports of other coccinellids persistently attacking H. axyridis, indeed most evidence suggests that the immature stages of this ladybird are resistant to reciprocal attacks (Ware and Majerus, 2008). Assessment of the competitive interactions between H. axyridis and C. septempunctata indicated that H. axyridis dominated and Yasuda et al. (2001) attributed the success of the former to its higher attack rates and greater escape ability. Majerus (1994) reports that in predatory interactions between coccinellid larvae it is generally the larger that eats the smaller, as long as both are mobile, therefore the large size of H. axyridis compared to many coccinellids may also contribute to its competitive advantage.

Mesocosm studies have included interactions between coccinellids and non-coccinellid aphidophages such as neuropterans (Wells et al., 2010; Wells, 2011) and syrphids (Ingels and De Clercq, 2011). However, extrapolating findings from laboratory studies to the field is challenging and many questions remain with respect to the ecological relevance of intraguild predation. Roy et al. (2012) explored large-scale and long-term datasets from the UK and Belgium to demonstrate declines in native coccinellids in response to the arrival of H. axyridis.

The defensive chemistry of H. axyridis appears to be central to the resistance of H. axyridis to attack by other aphidophages. Various studies have shown the unidirectional nature of intraguild interactions between H. axyridis and other immature stages of coccinellid and attributed this to unpalatability of H. axyridis (Agarwala et al., 1998; Agarwala and Dixon, 1992; Hemptinne et al., 2000; Alam et al., 2002; Ware and Majerus, 2008). Although generally levels of intraguild predation are inversely correlated to aphid or coccid density (Hironori and Katsuhiro, 1997; Burgio et al., 2002), neonate H. axyridis larvae frequently attack and consume the eggs of other coccinellid species when they encounter them, even when aphids are plentiful (MEN Majerus, personal communication, 2008). Intraguild predation is considered to be an important force in structuring aphidophagous ladybird guilds (Yasuda and Shinya, 1997; Yasuda and Ohnuma, 1999; Kajita et al., 2000), and therefore H. axyridis has the potential to dramatically disrupt native guilds globally. The evidence from North America supports the contention that H. axyridis is an aggressive coccinellid with a tendency for intraguild predation that could seriously affect the abundance of native coccinellids and dramatically reduce their available niches in the predator complex (Elliott et al., 1996).

Threatened Species

Social Impact

Wine Industry

H. axyridis impacts on the wine industry because of its tendency to aggregate in clusters of grapes (Vitis vinifera) prior to harvest. H. axyridis are difficult to separate from the grapes and so are processed with the grapes to make wine. The alkaloids contained within these beetles adversely affect the taste and bouquet of the vintage (Pickering et al., 2005).

Recently concerns have been raised that both H. axyridis and C. septempunctata cause such problems to the wine industry in North America (Botezatu et al., 2013).Both H. axyridis and C. septempunctata contribute alkyl methoxypyrazines, and particularly isopropyl methoxypyrazine, to wine at concentrations that are considered to have a negative impact on wine quality (Botezatu et al., 2013). There are indications that sulphur dioxide (in the form of potassium metabisulphite) a commonly used antimicrobial and antioxidant in wine production, repels H. axyridis from grape vines (Glemser et al., 2012).

Orchards

H. axyridis has been designated as a pest of orchard crops (apples, Malus domestica and pears, Pyrus communis) because, as aphids become scarce in the late summer and autumn, H. axyridis feed on soft fruit causing blemishing and an associated reduction in market value (Koch, 2003).

Domestic Nuisance

The large aggregations of H. axyridis formed during the autumn and winter in buildings are regarded as a nuisance because of the  propensity to swarm, and associated implications. Some people have reported allergic reactions to H. axyridis (Goetz, 2008) and others have complained of experiencing bites (Koch, 2003). Reflex blood from H. axyridis may stain soft furnishings. There have been recent reports from Austria that H. axyridis is causing problems within hospital operating theatres through the winter months.

Risk and Impact Factors

• Proved invasive outside its native range
• Has a broad native range
• Abundant in its native range
• Highly adaptable to different environments
• Is a habitat generalist
• Capable of securing and ingesting a wide range of food
• Highly mobile locally
• Benefits from human association (i.e. it is a human commensal)
• Long lived
• Fast growing
• Has high reproductive potential
• Has high genetic variability

• Negatively impacts human health
• Negatively impacts livelihoods
• Reduced native biodiversity
• Threat to/ loss of native species

• Causes allergic responses
• Competition - monopolizing resources
• Predation

• Highly likely to be transported internationally accidentally
• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field
• Difficult/costly to control

Uses

H. axyridis has been used as a classical biological control agent of aphids and coccids in North America and Europe. It has many attributes that contribute to its economic viability as a biological control agent. Perhaps most notable is its polyphagous nature. H. axyridis preys on a wide variety of tree-dwelling homopteran insects, such as aphids, psyllids, coccids, adelgids and other insects (Tedders and Schaefer, 1994; Hodek, 1996; Koch, 2003). In North America, H. axyridis is documented as offering effective control of target pests, such as aphids in pecans (Carya illinoinensis) (Tedders and Schaefers, 1994), Aphis spiraecola in apple (Malus domestica) orchards (Brown and Miller, 1998) and several citrus pests (Michaud, 1999, 2000, 2001a,b, 2002a; Stuart et al., 2002). In Asia and North America, H. axyridis contributes to the control of aphids on sweetcorn (Zea mays subsp. mays) (Musser and Shelton, 2003), lucerne (Medicago sativa) (Buntin and Bouton, 1997; Colunga-Garcia and Gage, 1998), cotton (Gossypium spp.) (Wells et al., 2001), tobacco (Nicotiana spp.) (Wells and McPherson, 1999), winter wheat (Triticum aestivum) (Colunga-Garcia and Gage, 1998) and soyabean (Glycine max) (Koch, 2003). The spread and increase of H. axyridis may therefore prove to be beneficial to crop systems through a reduction in aphid numbers below economically damaging levels and thus an associated reduction in the use of chemical pesticides (Koch and Galvan, 2008).

H. axyridis has not only been used as a classical biological control agent, but also in augmentative strategies in which control is achieved through inundative or inoculative releases of natural enemies (Seo and Youn, 2000). In China, releases have successfully suppressed target pests, such as Chaetosiphon fragaefolii on strawberry (Fragaria x ananassa) (Sun et al., 1996) and coccids in pine forests (Wang, 1986).

The role of H. axyridis in integrated pest management schemes has also been assessed through laboratory and field studies (Koch, 2003). General insecticides were found to be lethal to H. axyridis even at low doses. However, synthetic pyrethroids and some relatively new pesticides, such as spinosad, indoxacarb and pyriproxyfen, showed minimal toxic effects or were less toxic to H. axyridis than to aphids (Cho et al., 1997; Michaud 2002b; Michaud, 2003; Musser and Shelton, 2003). Biorational pesticides, such as the fungus Beauvaria bassiana and soap, were also shown to be less toxic than conventional pesticides (Smith and Krischik, 2000). Investigations considering the interaction between H. axyridis and insect resistant transgenic crops have shown negligible effects on H. axyridis (Wold et al., 2001; Ferry et al., 2003; Musser and Shelton, 2003). Fungicides have little effect on H. axyridis (Michaud, 2001b; Wells et al., 2001; Michaud and Grant, 2003). H. axyridis seems compatible with many of the strategies employed in integrated pest management schemes (Koch, 2003).

Uses List

Environmental

• Biological control

General

• Laboratory use
• Research model

Similarities to Other Species/Conditions

H. axyridis could be confused with a number of other polymorphic species from the Coccinellidae such as the two-spot ladybird, Adalia bipunctata, or ten-spot ladybird, Adalia decimpunctata. However, H. axyridis is a much larger beetle (Majerus et al., 2005a). Hippodamia convergens could also be mistaken for H. axyridis (NBII, 2005). The larvae of H. axyridis are similar to larvae of some other members of the genus, such as Harmonia quadripunctata.

Prevention and Control

Current and potential management strategies against H. axyridis have been reviewed by Kenis et al. (2008).

Cultural Control

Ensuring that fruit and cut flower imports are free from H. axyridis will reduce movement. In addition, several recommendations on cultivation practices in vineyards have been suggested to lower the impact of the ladybird in regions where H. axyridis causes recurrent problems to fruits (Kenis et al., 2008). Key components of an integrated pest management strategy against H. axyridis in vineyards include proper surveys for beetle densities before harvest and the determination of a threshold density, to assist in management decisions. Galvan et al. (2007) have described various sampling plans and assessed their usefulness. Kovach (2004) and Pickering et al. (2007) evaluated the threshold density for wine contamination to be about 0.9 and 1.3-1.5 beetle per kg of grapes (Vitis vinifera), respectively, but the latter authors recommend a more conservative limit of 0.2 to 0.4 beetles per kg of grapes above which interventions in the field or in the winery should be considered. Including berry injuries in the sampling procedures may also be useful because ladybirds are primarily found on damaged fruits (Galvan et al., 2007). Such damage is caused by a variety of mechanisms including by splitting, feeding by birds or other insects, disease (rot) etc. (Galvan et al., 2007). Growers could reduce berry injury by using irrigation to avoid long periods of drought and by avoiding injuring to berries when pruning or spraying. Selecting varieties with higher resistance or tolerance to splitting may also be envisaged, as a potential long-term measure, when vineyards are replanted through the normal process of renewing stock.

Harvesting methods may have an impact on the density of beetles in harvested grapes. The beetles may be more likely to leave the grapes during day harvesting rather than during night harvesting. Hand-harvesting may be more favourable than mechanical harvesting because aggregations of beetles in grape clusters can be monitored during harvesting and infested grapes can be discarded. The beetles can be removed by shaking clusters, by hand or by using shaking tables, and by floating clusters in water or vacuum clusters (Kenis et al., 2008).

Mechanical Control

The invasion of H. axyridis into households can be limited by preventing the beetles from entering the building. Koch and Hutchison (2003) recommend sealing holes or covering them with fine mesh to limit the movement of H. axyridis into buildings. In addition, H. axyridis adults and late-instar larvae are large and relatively easily identified, therefore they can be removed from unwanted locations manually, for example, using a vacuum cleaner with a mesh covering (such as a stocking) placed over the distal end of the hose to prevent the ladybirds from moving into the vacuum drum. Where large aggregations occur in buildings, care should be taken to avoid disturbance resulting in excessive reflex bleeding, which can cause damage (staining) to soft furnishings. In addition, light traps can be used to attract H. axyridis although the efficiency of these is not yet quantified. New trapping methods for use in buildings and open fields could be developed, based on aggregative semiochemicals, but our current understanding of pheromonal and kairomonal communication by ladybirds and, specifically, H. axyridis, is still limited.

Chemical Control

For persistent aggregations in buildings Koch and Hutchison (2003) suggested exteriorly applying an insecticide such as a synthetic pyrethroid. The applications can be targeted to entry points such as windows, doors, eaves and foundations. Repellents could also be employed such as camphor and menthol (Koch, 2003). Other species of ladybird (such as Adalia bipunctata), which also use buildings for overwintering, may be adversely affected by such control measures. Insecticide use inside buildings is usually not advised.

Chemical control of H. axyridis in field situations such as orchards and vineyards is feasible, but less applicable because of the impact of insecticides on other aphidophages and beneficial insects. One of the limiting factors of using insecticides is that many of them, e.g. most pyrethroids, have a pre-harvest interval of several weeks whereas, to be efficient, treatments should be applied within a week before harvest (Galvan et al., 2006). Insecticide treatments against H. axyridis in vineyards should not be carried out preventively, but should rather follow decision protocols based on rigorous sampling plans and well-defined action thresholds.

Biological Control

H. axyridis has a range of natural enemies, but few of them show potential as biological control agents (Kenis et al., 2008). In the regions of introduction, observations suggest that natural enemies are of little importance in the population dynamics of the ladybird. Only the sudden adaptation of a natural enemy of native ladybirds or the importation of a natural enemy from the area of origin of H. axyridis may ultimately lower population densities (Kenis et al., 2008). However, H. axyridis is a difficult target for classical biological control, firstly because the invasion of H. axyridis is, in itself, most probably the result of bad biological control practices and, secondly, because specific biological control agents may be difficult to find in the area of origin.

Gaps in Knowledge/Research Needs

Research is needed in at least two fields. Firstly, the impact of H. axyridis on native biodiversity needs to be better assessed in long term studies, and the mechanisms underlying this impact should be better understood. It will be particularly important to consider the implications of intraguild predation by H. axyridis on ecological resilience and function. Recent research from America found no evidence that H. axyridis consumed coccinellid eggs in the field but suggested that exploitative and apparent competition might explain declines of native species in the presence of H. axyridis (Smith and Gardiner, 2013). There is an urgent need for detailed field studies to quantitatively document the interactions between H. axyridis and other species within the aphidophagous community. Ecological network analysis provides opportunities for exploration of such complex interactions (Roy and Handley, 2012). Secondly, sustainable control methods need to be developed both for controlling H. axyridis in buildings and vineyards and for lowering the general level of populations to limit the impact on native biodiversity. This includes a better knowledge of the role of natural enemies in the population dynamics of the beetle in the region of origin and the region of introduction.

References

Adriaens T, Martin y Gomez GS, Maes D, 2008. Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl, 53(1):69-88. http://www.springerlink.com/link.asp?id=102853

Agarwala BK, Bhattacharya S, Bardhanroy P, 1998. Who eats whose eggs? Intra- versus inter-specific interactions in starving ladybird beetles predaceous on aphids. Ethology, Ecology & Evolution, 10(4):361-368

Agarwala BK, Dixon AFG, 1992. Laboratory study of cannibalism and interspecific predation in ladybirds. Ecological Entomology, 17(4):303-309

Alam N, Choi IS, Song KS, Hong J, Lee CO, Jung JH, 2002. A new alkaloid from two coccinellid beetles Harmonia axyridis and Aiolocaria haexapilota. Bulletin of the Korean Chemical Society, 23:497-499

Almeida LM de, Silva VB da, 2002. First record of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae): a lady beetle native to the Palaearctic region. Revista Brasileira de Zoologia, 19(3):941-944

Alyokhin A, Sewell G, 2004. Changes in a lady beetle community following the establishment of three alien species. Biological Invasions, 6:463-471

Arruda Filho GPde, Berti Filho E, Pereira RA, 2009. Occurrence of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) in the state of São Paulo, Brazil. (Ocorrência de Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) no Estado de São Paulo.) Revista de Agricultura (Piracicaba), 84(2):145-148. http://www.fealq.org.br/revista_agricultura.asp

Barševskis A, 2009. Multicoloured Asian lady beetle (Harmonia axyridis (Pallas, 1773)) (Coleoptera: Coccinellidae) for the first time in the fauna of Latvia. Baltic Journal of Coleopterology, 9(2):135-138. http://bjc.sggw.waw.pl

Ben Halima Kamel, M., Mdellel, L., Zouari, S., Adouani, R., 2018. Occurrence of Harmonia axyridis in Tunisia. Bulletin OEPP/EPPO Bulletin, 48(2), 307-308. https://onlinelibrary.wiley.com/journal/13652338 doi: 10.1111/epp.12473

Berkvens N, Moens J, Berkvens D, Samih MA, Tirry L, Clercq Pde, 2010. Dinocampus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe. Biological Control, 53(1):92-99. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6WBP-4XNW45N-1&_user=10&_coverDate=04%2F30%2F2010&_rdoc=14&_fmt=high&_orig=browse&_srch=doc-info(%23toc%236716%232010%23999469998%231723116%23FLA%23display%23Volume)&_cdi=6716&_sort=d&_docanchor=&_ct=20&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=96247e0f8b544d9d2d6007d86df04d6e

Botezatu AI, Kotseridis Y, Inglis D, Pickering GJ, 2013. Occurrence and contribution of alkyl methoxypyrazines in wine tainted by Harmonia axyridis and Coccinella septempunctata. Journal of the Science of Food and Agriculture, 93(4):803-810. http://onlinelibrary.wiley.com/journal/10.1002/(ISSN)1097-0010

Brown MW, Miller SS, 1998. Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomological News, 109(2):143-151

Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg T, Kenis M, Klausnitzer BEM, Kovárbreve~ I, Loomans AJM, Majerus MEN, Nedved O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov IA, Roy DB, 2008. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl, 53(1):5-21. http://www.springerlink.com/link.asp?id=102853

Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN, 2008. Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl, 53(1):55-67. http://www.springerlink.com/link.asp?id=102853

Buntin GD, Bouton JH, 1997. Aphid (Homoptera: Aphididae) management in alfalfa by spring grazing with cattle. Journal of Entomological Science, 32(3):332-342

Burbank DH, Pregitzer KS, Gross KL, 1992. Vegetation of the WK Kellogg Biological Station. Michigan, USA: Michigan State University/Agricultural Experiment Station

Burgio G, Santi F, Maini S, 2002. On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biological Control, 24(2):110-116

CABI/EPPO, 2007. Harmonia axyridis. [Distribution map]. Distribution Maps of Plant Pests, No.June. Wallingford, UK: CABI, Map 689

Carton B, Smagghe G, Tirry L, 2003. Toxicity of two ecdysone agonists, halofenozide and methoxyfenozide, against the multicoloured Asian lady beetle Harmonia axyridis (Col., Coccinellidae). Journal of Applied Entomology, 127(4):240-242; 14 ref

Chapin JB, Brou VA, 1991. Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proceedings of the Entomological Society of Washington, 93(3):630-635

Chazeau J, Fürsch H, Sasaji H, 1989. Taxonomy of Coccinellids. Coccinella (Passau), 1:6-8

Cho JR, Hong KJ, Yoo JK, Bang JR, Lee JO, 1997. Comparative toxicity of selected insecticides to Aphis citricola, Myzus malisuctus (Homoptera: Aphididae), and the predator Harmonia axyridis (Coleoptera: Coccinellidae). Journal of Economic Entomology, 90(1):11-14

Coderre D, Lucas T, GagnT I, 1995. The occurrence of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Canada. Canadian Entomologist, 127(4):609-611

Colunga-Garcia M, Gage SH, 1998. Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environmental Entomology, 27(6):1574-1580

Comont RF, Purse BV, Phillips W, Kunin WE, Hanson M, Lewis OT, Harrington R, Shortall CR, Rondoni G, Roy HE, 2014. Escape from parasitism by the invasive alien ladybird, Harmonia axyridis. Insect Conservation and Diversity, 7(4):334-342. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1752-4598

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). Journal of the Kansas Entomological Society, 71(2):159-163

Day WH, Prokrym DR, Ellis DR, Chianese RJ, 1994. The known distribution of the predator Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in the United States, and thoughts on the origin of this species and five other exotic lady beetles in eastern North America. Entomological News, 105(4):244-256

Dixon AFG, 2000. Insect predator-prey dynamics: ladybird beetles and biological control. Insect predator-prey dynamics: ladybird beetles and biological control., ix + 257 pp.; 33 pp

Dobzhansky T, 1933. Geographical variation in ladybeetles. The American Naturalist, 67:97-126

Dreistadt SH, Hagen KS, Bezark LG, 1995. Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), first western United States record for this Asiatic lady beetle. Pan-Pacific Entomologist, 71(2):135-136

Ejbich K, 2003. Producers in Ontario and northern US bugged by bad odors in wine. Wine Spectator, 15 May, 16

Elliott N, Kieckhefer R, Kauffman W, 1996. Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia, 105(4):537-544

El-Sebaey IIA, El-Gantiry AM, 1999. Biological aspects and description of different stages of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Bulletin of Faculty of Agriculture, University of Cairo, 50(1):87-97; 13 ref

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Fan YH, Yang SY, 1983. Occurrence of Leis axyridis (Pallas) (Col.: Coccinellidae). Natural Enemies of Insects (Kunchong Tiandi), 5(2):94-96

Ferry N, Raemaekers RJM, Majerus MEN, Jouanin L, Port G, Gatehouse JA, Gatehouse AMR, 2003. Impact of oilseed rape expressing the insecticidal cysteine protease inhibitor oryzacystatin on the beneficial predator Harmonia axyridis (multicoloured Asian ladybeetle). Molecular Ecology, 12(2):493-504

Foley IA, Ivie MA, Denke PM, 2009. The first state record for the multicolored Asian lady beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), from Montana. Coleopterists Bulletin, 63(3):351-352. http://www.bioone.org/perlserv/?request=get-current-issue

Fürsch H, 1990. Taxonomy of Coccinellids, corrected version. Coccinella (Passau), 2:4-6

Galvan TL, Burkness EC, Hutchison WD, 2006. Efficacy of selected insecticides for management of the multicolored Asian lady beetle on wine grapes near harvest. Plant Health Progress, October:1-5. http://www.plantmanagementnetwork.org/sub/php/research/2006/lady/

Galvan TL, Burkness EC, Hutchison WD, 2007. Enumerative and binomial sequential sampling plans for the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in wine grapes. Journal of Economic Entomology, 100:1000-1010

Garcés S, Williams R, 2004. First record of Hesperomyces virescens Thaxter (Laboulbeniales: Ascomycetes) on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Journal of the Kansas Entomological Society, 77(2):156-158

Glemser EJ, Dowling L, Inglis D, Pickering GJ, McFadden-Smith W, Sears MK, Hallett RH, 2012. A novel method for controlling multicolored Asian lady beetle (Coleoptera: Coccinellidae) in vineyards. Environmental Entomology, 41(5):1169-1176. http://esa.publisher.ingentaconnect.com/content/esa/envent/2012/00000041/00000005/art00017

Goetz DW, 2008. Harmonia axyridis ladybug invasion and allergy. Allergy and Asthma Proceedings, 29(2):123-129. http://www.ingentaconnect.com/content/ocean/aap/2008/00000029/00000002/art00005

Gordon RD, 1985. The Coccinellidae (Coleoptera) of America north of Mexico. Journal of the New York Entomological Society, 93(1):912 pp

Greathead DJ, Greathead AH, 1992. Biological control of insect pests by insect parasitoids and predators: the BIOCAT database. Biocontrol News and Information, 13(4):61N-68N

Gregory TR, Nedved O, Adamowicz SJ, 2003. C-value estimates for 31 specis of ladybird beetles (Coleoptera: Coccinellidae). Heriditas, 139:121-127

Grez A, Zaviezo T, González G, Rothmann S, 2010. Harmonia axyridis in Chile: a new threat. Ciencia e Investigación Agraria, 37(3):145-149. http://rcia.uc.cl/English/pdf/37-3/13_GREZ_37-3.pdf

Grill CP, Moore AJ, 1998. Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle. Oecologia, 114(2):274-282

Grill CP, Moore AJ, Brodie EDIII, 1997. The genetics of phenotypic plasticity in a colonizing population of the ladybird beetle, Harmonia axyridis. Heredity, 78(3):261-269

Guo JianYing, Zhou HongXu, Wan FangHao, Han ZhaoJun, 2007. Community structure of arthropods in transgenic cotton fields and their seasonal dynamics. Acta Agriculturae Boreali-Sinica, 22(6):183-189

Harmon JP, Stephens E, Losey J, 2007. The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. Journal of Insect Conservation, 11(1):85-94. http://www.springerlink.com/link.asp?id=100177

He JL, MaEP, Shen YC, Chen WL, Sun XQ, 1994. Observations of the biological characteristics of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Journal of Shanghai Agricultural College, 12(2):119-124

Hemptinne JL, Gaudin M, Dixon AFG, Lognay G, 2000. Social feeding in ladybird beetles: adaptive significance and mechanism. Chemoecology, 10(3):149-152

Hesler LS, Kieckhefer RW, Beck DA, 2001. First record of Harmonia axyridis (Coleoptera: Coccinellidae) in South Dakota and notes on its activity there and in Minnesota. Entomological News, 112(4):264-270

Hicks B, Majka CG, Moores SP, 2010. Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) found in Newfoundland. Coleopterists Bulletin, 64(1):50. http://www.bioone.org/perlserv/?request=get-current-issue

Hironori Y, Katsuhiro S, 1997. Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga, 42(1/2):153-163; 34 ref

Hodek I, 1958. Influence of temperature, relative humidity and photoperiodicity on the speed of development of Coccinella septempunctata L. Casopis Ceskoslovenske Spolecnosti Entomologicke, 55:121-141

Hodek I, 1973. Life history and biological properties. In: Biology of Coccinellidae. The Hague, Holland: Dr W Junk N V Publishers, 70-76

Hodek I, 1996. Food Relationships. In: Hodek I, Honek A, eds. Ecology of Coccinellidae. Dortrecht, Netherlands: Kluwer Academic Publishers, 143-238

Hodek I, Honek A, 1996. Ecology of Coccinellidae. Dortrecht, Netherlands: Kluwer Academic Publishers

Hoebeke ER, Wheeler AGJr, 1996. Adventive lady beetles (Coleoptera: Coccinellidae) in the Canadian maritime provinces, with new eastern U.S. records of Harmonia quadripunctata. Entomological News, 107(5):281-290

Hosino Y, 1933. On variation in the pattern of Harmonia axyridis. Zoolical Magazine, 45:255-67

Hosino Y, 1936. Genetical study of the lady-bird beetle, Harmonia axyridis Pallas Rep. II. Japanese Journal of Genetics, 12:307-20

Hu YS, Wang ZM, Ning CL, Pi ZQ, Gao GQ, 1989. The functional response of Harmonia (Leis) axyridis to their prey of Cinara sp. Natural Enemies of Insects, 11(4):164-168

Hukusima S, Kamei M, 1970. Effects of various species of aphids as food on development, fecundity and longevity of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Research Bulletin of the Faculty of Agriculture, Gifu University, 29:53-66

Hukusima S, Ohwaki T, 1972. Further notes on feeding biology of Harmonia axyridis Pallas (Coleoptera : Coccinellidae). Research Bulletin of the Faculty of Agriculture, Gifu University, No. 33:75-82

Ingels B, Clercq Pde, 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(6):871-882. http://www.springerlink.com/link.asp?id=102853

Insectarium de Montreal, 2006. http://www2.ville.montreal.qc.ca/insectarium/toile/nouveau/preview.php?section=fiches&page=4

Jeffries DL, Chapman J, Roy HE, Humphries S, Harrington R, Brown PMJ, Handley LJL, 2013. Characteristics and drivers of high-altitude ladybird flight: insights from vertical-looking entomological radar. PLoS ONE, 8(12):e82278. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0082278

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. Applied Entomology and Zoology, 35(4):473-479

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(3):183-191

Kenis M, Roy HE, Zindel R, Majerus MEN, 2008. Current and potential management strategies against Harmonia axyridis. BioControl, 53(1):235-252. http://www.springerlink.com/link.asp?id=102853

Knodel JJ, Hoebeke ER, 1996. Multicolored Asian Lady Beetle, Harmonia axyridis (Pallas) Coleoptera:Coccinellidae. Cornell Cooperative Extension - Insect Diagnostic Laboratory fact sheets, http://www.entomology.cornell.edu/Extension/DiagnosticLab/IDLFS

Koch RL, 2003. The multicoloured Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control and non-target impacts. Journal of Insect Science, 3:32

Koch RL, Galvan TL, 2008. Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl, 53(1):23-35. http://www.springerlink.com/link.asp?id=102853

Koch RL, Hutchison WD, 2003. Multicoloured Asian Lady beetle. http://www.vegedge.umn.edu/vegpest/Harmonia/Harmonia.htm

Koch RL, Hutchison WD, 2003. Phenology and blacklight trapping of the multicolored Asian Lady Beetle (Coleoptera:Coccinellidae) in a Minnesota Agricultural Landscape. Journal of Entomological Science, 38(3):477-480

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). Biological Control, 28:265-270

Koch RL, Venette RC, Hutchison WD, 2006. Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western Hemisphere: implications for South America. Neotropical Entomology, 35(4):421-434. http://www.scielo.br/ne

Kohiyama K, 2006. Insect Gallery. http://kohiyama.wem.sfc.keio.ac.jp/eng/insect_e/adventure/011.html

Komai T, 1956. Genetics of Ladybeetles. Advances in Genetics, 8:155-88

Kovach J, 2004. Impact of the multicolored Asian lady beetle as a pest of fruit and people. American Entomologist, 50:165-167

Kuznetsov VN, 1997. Lady beetles of Russian Far East. Gainesville, FL, USA: Memoir Seis Editor, CSE

Labanowski G, Soika G, 2010. Beneficial organisms associated with ornamental pests. (Organizmy pozyteczne zwiazane ze szkodnikami roslin ozdobnych.) Progress in Plant Protection, 50(4):2003-2007. http://www.progress.plantprotection.pl/pliki/2010/PPP_50_4_70_Labanowski_G_R.pdf

LaMana ML, Miller JC, 1996. Field observations on Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in Oregon. Biological Control, 6(2):232-237

Lamana ML, Miller JC, 1998. Temperature-dependent development in an Oregon population of Harmonia axyridis (Coleoptera: Coccinellidae). Environmental Entomology, 27(4):1001-1005

Liu H, Qin L, 1989. The population fluctuations of some dominant species of ladybird beetles in Eastern Hebei Province. Chinese Journal of Biological Control, 5:92

Liu Jian, Ma FengMing, Zhao KuiJun, 2009. Predominant natural enemy insects in soybean field in northeast China. Chinese Bulletin of Entomology, 46(4):592-596. http://www.ilib.cn/P-kczs.html

Lucas é, Coderre D, Vincent C, 1997. Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae. Entomologia Experimentalis et Applicata, 85(2):151-159; 49 ref

Luo HH, 1987. Functional response of Harmonia axyridis to the density of Rhopalosiphum prunifolip. Natural Enemies of Insects, 9(2):84-87

Lynch LD, Hokkanen HMT, Babendreier D, Bigler F, Burgio G, Gao ZH, Kuske S, Loomans A, Menzler-Hokkanen I, Thomas MB, Tommasini G, Waage JK, Lenteren JCvan, Zeng QQ, 2001. Insect biological control and non-target effects: a European perspective. Evaluating indirect ecological effects of biological control. Key papers from the symposium "Indirect ecological effects in biological control", Montpellier, France, 17-20 October 1999, 99-125; 26 ref

Magnan EM, Sanchez H, Luskin AT, Bush RK, 2002. Multicolored Asian lady beetle (Harmonia axyridis) sensitivity. Journal of Allergy and Clinical Immunology, 109:205

Majerus M, Kearns P, 1989. Ladybirds. Naturalists' Handbooks Slough, UK; Richmond Publishing Co. Ltd., No. 10:103 pp

Majerus MEN, 1994. Ladybirds. London, UK; HarperCollins Academic, 367 pp

Majerus MEN, 2004. Harmonia axyridis in Britain:update (8th November 2004) http://www.gen.cam.ac.uk/Research/Majerus/Harmoniaupdate0811.doc

Majerus MEN, Brown P, Rowland F, Roy HE, 2005. Harlequin Ladybird Survey. http://www.harlequin-survey.org/

Majerus MEN, Roy HE, 2006. Colour pattern variation in the founding population of the harlequin ladybird, Harmonia axyridis, in Britain. Entomologist’s Record and Journal of Variation, in press

Majerus MEN, Roy HE, Mabbott P, 2006. The arrival of the harlequin ladybird, Harmonia axyridis, in Britain. Entomologists' Monthly Magazine, in press

Majerus MEN, Strawson V, Roy HE, 2005. The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Antenna, 29, 196-208

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(6):683-691; 26 ref

Markó V, Pozsgai G, 2009. Spread of Harlequin Ladybird (Harmonia axyridis Pallas, 1773) (Coleoptera, Coccinellidae) in Hungary, and the first records from Romania and Ukraine. (A harlekinkatica (Harmonia axyridis Pallas, 1773) (Coleoptera, Coccinellidae) elterjedése Magyarországon és megjelenése Romániában, Ukrajnában.) Növényvédelem, 45(9):481-490

McClure MS, 1986. Role of predators in regulation of endemic populations of Matsucoccus matsumurae (Homoptera: Margarodidae) in Japan. Environmental Entomology, 15(4):976-983

Menchetti M, Mori E, Ceccolini F, Paggetti E, Pizzocaro L, Cianferoni F, 2016. New occurrences of the alien invasive species Harmonia axyridis (Pallas, 1773) in Southern Italy (Coleoptera: Coccinellidae). Onychium, No.12:137-139

Merkl O, 2008. First record of the harlequin ladybird (Harmonia axyridis Pallas) in Hungary (Coleoptera: Coccinellidae). (A harlekinkatica (Harmonia axyridis Pallas) Magyarországon (Coleoptera: Coccinellidae).) Növényvédelem, 44(5):239-242

Michaud JP, 1999. Sources of mortality in colonies of brown citrus aphid, Toxoptera citricida. BioControl, 44(3):347-367

Michaud JP, 2000. Development and reproduction of ladybeetles (Coleoptera: Coccinellidae) on the citrus aphids Aphis spiraecola Patch and Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae). Biological Control, 18(3):287-297

Michaud JP, 2001. Numerical response of Olla v-nigrum (Coleoptera: Coccinellidae) to infestations of Asian citrus psyllid, (Hemiptera: Psyllidae) in Florida. Florida Entomologist, 84(4):608-612

Michaud JP, 2001. Responses of two ladybeetles to eight fungicides used in Florida citrus: implications for biological control. Journal of Insect Science (Tucson), 1(6):1-7; [available online: insectscience.org/1.6]

Michaud JP, 2002. Biological control of Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae) in Florida: a preliminary report. Entomological News, 113(3):216-222

Michaud JP, 2002. Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera:Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environmental Entomology, 31:827-835

Michaud JP, 2002. Relative toxicity of six insecticides to Cycloneda sanguinea and Harmonia axyridis (Coleoptera: Coccinellidae). Journal of Entomological Science, 37(1):83-93

Michaud JP, 2003. Toxicity of fruit fly baits to beneficial insects in citrus. Journal of Insect Science, 3:1-9

Michaud JP, Grant AK, 2003. Sub-lethal effects of a copper sulfate fungicide on development and reproduction in three coccinellid species. Journal of Insect Science, 3:1-6

Michie LJ, Masson A, Ware RL, Jiggins FM, 2011. Seasonal phenotypic plasticity: wild ladybirds are darker at cold temperatures. Evolutionary Ecology, 25(6):1259-1268. http://springerlink.metapress.com/link.asp?id=100160

Murchie AK, Moore JP, Moore GA, Roy HE, 2008. The Harlequin Ladybird (Harmonia axyridis (Pallas)) (Coleoptera: Coccinellidae), found in Ireland. Irish Naturalists' Journal, 29(1):25-26. http://www.habitas.org.uk/inj/

Musser FR, Shelton AM, 2003. Bt sweet corn and selective insecticides: impacts on pests and predators. Journal of Economic Entomology, 96(1):71-80

Nakata T, 1995. Population fluctuations of aphids and their natural enemies on potato in Hokkaido, Japan. Applied Entomology and Zoology, 30(1):129-138

Nalepa CA, Kidd KA, Hopkins DI, 2000. The multicolored Asian lady beetle (Coleoptera: Coccinellidae): orientation to aggregation sites. Journal of Entomological Science, 35(2):150-157

Nalepa CA, Weir A, 2007. Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): role of mating status and aggregation behavior. Journal of Invertebrate Pathology, 94(3):196-203. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6WJV-4MMP659-1&_user=10&_coverDate=03%2F31%2F2007&_rdoc=7&_fmt=summary&_orig=browse&_srch=doc-info(%23toc%236888%232007%23999059996%23644313%23FLA%23display%23Volume)&_cdi=6888&_sort=d&_docanchor=&view=c&_ct=13&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=44953fd4c98c5038e715df904516db26

NBII, 2005. Global Invasive Species Database: Harmonia axyridis. National Biological Information Infrastructure, http://www.issg.org/database/species/ecology.asp?si=668&fr=1&sts=

Nedved O, Háva J, 2016. New record of the invasive ladybeetle Harmonia axyridis in Afrotropical Region: Tanzania, Zanzibar. African Entomology, 24(1):247-249. http://www.bioone.org/loi/afen

Obata S, 1986. Determination of hibernation site in the ladybird beetle, Harmonia axyridis Pallas (Coleoptera, Coccinellidae). Kontyu, 54(2):218-223

Obata S, Johki Y, Hidaka T, 1986. Location of hibernation sites in the ladybird beetle, Harmonia axyridis In: Ecology of Aphidophaga. Dordrecht, Netherlands: Dr. W. Junk

Ongagna P, Giuge L, Iperti G, Ferran A, 1993. Life cycle of Harmonia axyridis (Col. Coccinellidae) in its area of introduction: south-eastern France. Entomophaga, 38(1):125-128

Osawa N, 2000. Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Population Ecology, 42(2):115-127

Parrella G, Varricchio ML, Giorgini M, 2015. Harmonia axyridis recorded in Campania, Southern Italy. (Harmonia axyridis segnalata in Campania.) Protezione delle Colture, No.3:26-27

Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN, 2008. Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl, 53(1):147-168. http://www.springerlink.com/link.asp?id=102853

Phoofolo MW, Obrycki JJ, 1998. Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomologia Experimentalis et Applicata, 89(1):47-55; 34 ref

Pickering GJ, Ker K, Soleas GJ, 2007. Determination of the critical stages of processing and tolerance limits for Harmonia axyridis for 'ladybug taint' in wine. Vitis, 46(2):85-90. //vitis-vea.zadi.de

Pickering GJ, Lin Yong, Reynolds A, Soleas G, Riesen R, Brindle I, 2005. The influence of Harmonia axyridis on wine composition and aging. Journal of Food Science, 70(2):S128-S135

Poinar GO Jr, Steenberg T, 2012. Parasitylenchus bifurcatus n. sp. (Tylenchida: Allantonematidae) parasitizing Harmonia axyridis (Coleoptera: Coccinellidae). Parasites and Vectors, 5(218):(1 October 2012). http://www.parasitesandvectors.com/content/pdf/1756-3305-5-218.pdf

Poutsma J, Loomans AJM, Aukema B, Heijerman T, 2008. Predicting the potential geographic distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX model. BioControl, 53:103-125

Przewoz´ny M, Barozek T, Bunalski M, 2007. Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) new species of ladybird beetle for Polish fauna. Polskie Pismo Entomologiczne, 76(3):177-182

Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, San Martin G, Brown PMJ, Hautier L, Poland R, Roy DB, Comont R, Eschen R, Frost R, Zindel R, Vlaenderen Jvan, Nedved O, Ravn HP, Grégoire J, Biseau JCde, Maes D, 2012. Invasive alien predator causes rapid declines of native European ladybirds. Diversity and Distributions, 18(7):717-725. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1472-4642

Roy HE, Brown P, Majerus MEN, 2006. Harmonia axyridis:A successful biocontrol agent or an invasive threat? In: Eilenberg J, Hokkanen H, eds. An Ecological and Societal Approach to Biological Control. Netherlands: Kluwer Academic Publishers

Roy HE, Brown PMJ, 2015. Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain. Ecological Entomology, 40(4):336-348. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2311

Roy HE, Cottrell TE, 2008. Forgotten natural enemies: interactions between coccinellids and insect-parasitic fungi. European Journal of Entomology [Proceedings of the International Symposium "Ecology of Aphidophaga 10", held in September 2007 in Athens, Greece.], 105(3):391-398. http://www.eje.cz/scripts/content.php

Roy HE, Handley LJL, 2012. Networking: a community approach to invaders and their parasites. Functional Ecology, 26(6):1238-1248. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2435

Roy HE, Handley LJL, Schönrogge K, Poland RL, Purse BV, 2011. Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl, 56(4):451-468. http://www.springerlink.com/link.asp?id=102853

Roy HE, Rhule E, Harding S, Handley LJL, Poland RL, Riddick EW, Steenberg T, 2011. Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. BioControl, 56(4):663-679. http://www.springerlink.com/link.asp?id=102853

Sakai T, Uehara Y, Matsuka M, 1974. The effect of temperature and other factors on the expression of elytral pattern in lady beetle, Harmonia axyridis Pallas. Bulletin of the Faculty of Agriculture, Tamagawa University, 14:33-39

Sakurai H, Kawai T, Takeda S, 1992. Physiological changes related to diapause of the lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae). Applied Entomology and Zoology, 27(4):479-487

Sakurai H, Kumada Y, Takeda S, 1993. Seasonal prevalence and hibernating diapause behaviour in the lady beetle, Harmonia axyridis. Research Bulletin of the Faculty of Agriculture, Gifu University, No. 58:51-55

Sasaji H, 1971. Fauna Japonica, Coccinellidae (Insecta:Coleoptera). Tokyo, Japan: Academic Press

Sasaji H, 1977. Larval characters of Asian Species of the Genus Harmonia Mulsant. Memoir of the Faculty of Education, Fukui University, Series II, Natural Science, 27:1-17

Savoiskaya GI, 1970. The Far-Eastern ladybird against the apple aphid. Zashchita Rastenii, 15(6):12-13

Seo M-J, Youn Y-N, 2000. The Asian ladybird, Harmonia axyridis, as biological control agents: I. Predacious behavior and feeding ability. Korean Journal of Applied Entomology, 39(2):59-71

Shi S-S, 1995. Occurrence of Harmonia axyridis var. axyridis in Jilin province. Journal of Jilin Agricultural University, 17(1):106-108

Smith B, Fisher D, 2008. Biosecurity risk - Asian lady beetle. Wine Industry Newsletter., 3

Smith CA, Gardiner MM, 2013. Biodiversity loss following the introduction of exotic competitors: does intraguild predation explain the decline of native lady beetles? PLoS ONE, 8(12):e84448. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0084448

Smith MW, Arnold DC, Eikenbary RD, Rice NR, Shiferaw A, Cheary BS, Carroll BL, 1996. Influence of ground cover on beneficial arthropods in pecan. Biological Control, 6(2):164-176; 52 ref

Smith SF, Krischik VA, 2000. Effects of biorational pesticides on four coccinellid species (Coleoptera: Coccinellidae) having potential as biological control agents in interiorscapes. Journal of Economic Entomology, 93(3):732-736

Soares AO, Coderre D, Schanderl H, 2001. Fitness of two phenotypes of Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology, 98(3):287-293

Solano Y, Arcaya E, 2014. First record of Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) in Venezuela. (Primer registro de Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) en Venezuela.) Entomotropica, 29(1):57-61. http://www.entomotropica.org/index.php/entomotropica

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). South African Journal of Science, 103(3/4):123-126. http://www.sajs.co.za

Stuart RJ, Michaud JP, Olsen L, McCoy CW, 2002. Lady beetles as potential predators of the root weevil Diaprepes abbreviatus (Coleoptera: Curculionidae) in Florida citrus. Florida Entomologist, 85(3):409-416

Sun XingQuan, Qiu HongLiu, Zhu KeLong, Gu BaoLong, Zhang XiuLong, Lu ZhiXing, Liu XiaoPing, 2002. Determination of supercooling temperature of Harmonia axyridis (Pallas) and its control over vegetable aphids in plastic covering. Journal of Shanghai Jiaotong University - Agricultural Science, 20(4):346-347

Sun XQ, Chen WL, Chen ZB, He JL, Ye WJ, 1996. A preliminary study on the artificial diet of an aphidophagous coccinellid, Harmonia axyridis (Palas), and its use to control strawberry aphids under plastic covering. Journal of Shanghai Agricultural College, 14:133-137

Takahashi K, 1989. Intra- and inter-specific predation of lady beetles in spring alfalfa fields. Japanese Journal of Entomology, 57(1):199-203

Takizawa T, Yasuda H, Agarwala BK, 2000. Effect of three species of predatory ladybirds on oviposition of aphid parasitoids. Entomological Science, 3(3):465-469

Tan C-C, Li J-C, 1934. Inheritance of the elytral color patterns in the lady-bird beetle, Harmonia axyridis Pallas. American Naturalist, 68:252-65

Tan C-C, Li J-C, 1946. Mosaic dominance in the inheritance of color patterns in the lady beetle, Harmonia axyridis. Genetics, 31:195-210

Tanagishi K, 1976. Hibernation of the lady beetle, Harmonia axyridis. Insectarium, 13:294-298

Tedders WL, Schaefer PW, 1994. Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the southeastern United States. Entomological News, 105(4):228-243

Thalji R, Stojanovic D, 2008. First sighting of the invasive ladybird Harmonia axyridis Pallas (Coleoptera, Coccinellidae) in Serbia. (Prvi nalaz invazivne bubamare Harmonia axyridis Pallas (Coleoptera, Coccinellidae) u Srbiji.) Biljni Lekar (Plant Doctor), 36(6):389-393

Wang LY, 1982. Control of Matsucoccus massonianp Young et Hu (Hom.: Margarodidae) by Leis axyridis (Pallas). Natural Enemies of Insects, 4(4):37-39

Wang LY, 1986. Mass rearing and utilization in biological control of the lady beetle Leis axyridis (Palla) [Harmonia axyridis]. Acta Entomologica Sinica, 29(1):104

Wang Su, Michaud JP, Zhang RunZhi, Zhang Fan, Liu ShuAng, 2009. Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. Ecological Entomology, 34(4):483-494. http://www.blackwell-synergy.com/loi/een

Ware RL, Evans N, Malpas L, Michie LJ, O'Farrell K, Majerus MEN, 2008. Intraguild predation by the invasive ladybird Harmonia axyridis: 1. British and Japanese coccinellid eggs. Neobiota, 7:263-275

Ware RL, Majerus MEN, 2008. Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl, 53(1):169-188. http://www.springerlink.com/link.asp?id=102853

Wells ML, McPherson RM, 1999. Population dynamics of three coccinellids in flue-cured tobacco and functional response of Hippodamia convergens (Coleoptera: Coccinellidae) feeding on tobacco aphids (Homoptera: Aphididae). Environmental Entomology, 28(4):768-773; 25 ref

Wells ML, McPherson RM, Ruberson JR, Herzog GA, 2001. Coccinellids in cotton:population response to pesticide application and feeding response to cotton aphids (Homoptera:Aphididae). Environmental Entomology, 30:785-793

Wells PM, 2011. Intraguild predation by Harmonia axyridis: effects on native enemies and aphid suppression. PhD Thesis. Cambridge, UK: University of Cambridge

Wells PM, Baverstock J, Majerus MEN, Jiggins FM, Roy HE, Pell JK, 2010. Intraguild predation of non-coccinellid aphid natural enemies by Harmonia axyridis: prey range and factors influencing intraguild predation. IOBC/wprs Bulletin (Working Group "Benefits and Risks of exotic biological Control Agents"), 58:185-196

Wisconsin Department of Natural Resources, 2005. Invasive Species. http://www.dnr.state.wi.us/invasives/

Wise IL, Turnock WJ, Roughley RE, 2001. New records of coccinellid species for the Province of Manitoba. Proceedings of the Entomological Society of Manitoba, 57:5-10; 13 ref

Wold SJ, Burkness EC, Hutchison WD, Venette RC, 2001. In-field monitoring of beneficial insect populations in transgenic corn expressing a Bacillus thuringiensis toxin. Journal of Entomological Science, 36(2):177-187

Wu QL, 1986. Investigation on the fluctuations of dominant natural enemy populations in different cotton habitats and integrated application with biological agents to control cotton pests. Natural Enemies of Insects, 8(1):29-34

Xie Y-P, Xue J-L, Tang X-Y, Zhao S-L, 2004. The Bunge Prickly-Ash tree damaged by a mealybug, Phenacoccus azaleae attracting the ladybug, Harmonia axyridis. Scientia Silvae Sinicae, 40(5):116-122

Yang M-J, Zhang Y, Tao M, 2009. Study on the population dynamics of pests and natural enemies of capsicum in Qiubei. Journal of Yunnan Agricultural University, 24(1):150-153

Yarbrough JA, Armstrong JL, Blumberg MZ, Phillips AE, McGahee E, Dolen WK, 1999. Allergic rhinoconjunctivitis caused by Harmonia axyridis (Asian lady beetle, Japanese lady beetle, or lady bug). Journal of Allergy and Clinical Immunology, 104:705

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. Journal of Insect Behavior, 14(3):373-384; 32 ref

Yasuda H, Ohnuma N, 1999. Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomologia Experimentalis et Applicata, 93(1):63-67; 32 ref

Yasuda H, Shinya Y, 1997. Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga, 42:153-163

Zawadneak MAC, Schuber JM, Poltronieiri AS, Cardoso NA, 2008. Occurrence of coccinelid predators in nectarine orchards in the municipality of Araucária, Paraná. (Ocorrência de coccinelídeos predadores em pomares de nectarina no município de Araucária, Paraná.) Scientia Agraria, 9(4):555-557. http://ojs.c3sl.ufpr.br/ojs2/index.php/agraria

Links to Websites

Contributors

03/04/2015 Updated by:

Helen Roy, Centre for Ecology & Hydrology, UK

21/10/2008 Updated by:

Marc Kenis, CABI Europe - Switzerland

Distribution Maps