Harmonia axyridis
(harlequin ladybird)

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.

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).

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).

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).

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).

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.

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.

Environmental

• Biological control

General

• Laboratory use
• Research model

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.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

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.

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.

03/04/2015 Updated by:

Helen Roy, Centre for Ecology & Hydrology, UK

21/10/2008 Updated by:

Marc Kenis, CABI Europe - Switzerland