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1 December 2013 Is the Multicolored Asian Ladybeetle, Harmonia axyridis, the Most Abundant Natural Enemy to Aphids in Agroecosystems?
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Abstract

The multicolored Asian ladybeetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), was introduced into Western Europe in the late 1990s. Since the late 2000s, this species has been commonly considered one of the most abundant aphid predators in most Western European countries. In spite of the large amount of research on H. axyridis, information concerning its relative abundance in agroecosystems is lacking. This study aims to evaluate the abundance of H. axyridis within the aphidophage community in four crops situated in southern Belgium: wheat, Triticum aestivum L. (Poales: Poaceae), corn, Zea mays, potato, Solanum tuberosum (Solanales: Solanaceae), and broad bean Vicia faba (Fabales: Fabaceae). In order to assess the species diversity, the collected data were analyzed by considering (1) the species richness and (2) the evenness according to the Shannon diversity index. Eleven aphidophages were observed in every inventoried agroecosystem, including five abundant species: three coccinellids, the seven-spotted ladybug, Coccinella septempunctata L. (Coleoptera: Coccinellidae), the 14-spotted Ladybird, Propylea quatuordecimpunctata, and H. axyridis; one hoverfly, the marmalade hoverfly, Episyrphus balteatus De Geer (Diptera: Syrphidae); and one lacewing, the common green lacewing, Chrysoperla carnea Stephens sensu lato (= s.l.) (Neuroptera: Chrysopidae). Harmonia axyridis has been observed to thrive, breed, and reproduce on the four studied crops. Harmonia axyridis is the most abundant predator of aphids in corn followed by C. septempunctata, which is the main aphid predator observed in the three other inventoried crops. In wheat and potato fields, H. axyridis occurs in low numbers compared to other aphidophage. These observations suggest that H. axyridis could be considered an invasive species of agrosystems, and that potato and wheat may intermittently act as refuges for other aphidophages vulnerable to intraguild predation by this invader. Harmonia axyridis is not the most abundant aphid predator in the main Belgian crops.

Introduction

The multicolored Asian ladybeetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), was introduced from Asia into Western Europe and other parts of the world to control aphid and coccid populations (Adriaens et al. 2008; Brown et al. 2008). In Belgium, H. axyridis was used as a biological control agent beginning in 1997 and was first observed in the wild in 2001. Since then H. axyridis populations have increased and gradually expanded into Belgium (Adriaens et al. 2008).

This species presents all the characteristics shared by an efficient aphid predator: large body size, high voracity, high predation efficiency (Labrie et al. 2006), high colonization aptitude (With et al. 2002), rapid development, high fecundity, and low susceptibility to pathogens or natural enemies (Marco et al. 2002). Harmonia axyridis has become ubiquitous in many parts of the world, including America, Europe, and Africa (Lombaert et al. 2010; Brown et al. 2011b), and has been reported in many different habitats, such as agroecosystems, gardens, and arboreal habitats (Majerus et al. 2006).

Due to its large body and efficient physical and chemical defenses, H. axyridis has become an intraguild predator (Sato and Dixon 2004; Ware and Majerus 2008). Intraguild predation has been observed among other ladybeetle species (Pell et al. 2008; Ware and Majerus 2008); other aphid natural enemies, including syrphids, chrysopids, and parasitoids (Phoofolo and Obrycki 1998; Wells et al. 2010; Ingels and De Clercq 2011); and aphid pathogenic fungus (Roy et al. 2008). This intraguild predation behavior is thought to have led to a decrease in native species (Brown and Miller 1998; Harmon et al. 2007; Ware et al. 2009; Brown et al. 2011a; Roy et al. 2012). In Belgian urban areas, Adriaens et al. (2010) found a significant decline in native species, including the two-spot ladybird, Adalia bipunctata L. (Coleoptera: Coccinellidae), and the 10 spotted ladybird, Adalia decempunctata L., on pine, lime, and maple trees following the arrival of H. axyridis. The decline of native species can possibly be explained by the decline in number of their principal prey, resulting in reduced survivorship in local habitats and altered dynamics of habitat use and dispersal (Evans 2004).

According to previous reports, the most dominant aphidophage in Belgian agroecosystems appear to be two coccinellids, the seven-spotted ladybug, Coccinella septempunctata L. (Coleoptera: Coccinellidae), and H. axyridis; one hoverfly, the marmalade hoverfly, Episyrphus balteatus De Geer (Diptera: Syrphidae); and one braconid, the parasitic wasp Aphidius ervi Haliday (Hymenoptera: Braconidae) (Derume et al. 2007; Adriaens et al. 2008; Alhmedi et al. 2009). In arboreal habitats, four coccinellids were reported as abundant species: A. bipunctata.,the 14-spotted ladybird, Propylea quatuordecimpunctata L. (Coleoptera: Coccinellidae), the 22-spot ladybird Psyllobora vigintiduopunctata (L.), and H. axyridis (Adriaens et al. 2008). In 2001, the same results were observed by Francis (2001), with the exception of H. axyridis.

Our study was conducted eight years after the first observation of H. axyridis in the wild in Belgium (Adriaens et al. 2003). Following aphidophagous decline highlighted by several studies, the current study was conducted in order to assess the relative abundance of H. axyridis through the quantification of the abundance of this exotic species and other aphidophages in four important Belgian crops (wheat, Triticum aestivum L. (Poales: Poaceae), corn, Zea mays, potato, Solanum tuberosum (Solanales: Solanaceae), and broad bean Vicia faba (Fabales: Fabaceae)) using a three-year inventory.

Materials and Methods

Study site

Aphidophagous insect populations were sampled from 2009 to 2011 in Hesbaye, an intensive agricultural production area in Wallonia, the southern region of Belgium (individual sites given in Table 1). Four crops were chosen for their agronomic importance: wheat, corn, potato, and broad bean Vicia faba. The sampling period ran from mid-May to late September. Every week, nine fields of each crop were sampled.

Sampling methods

The sampling methods used to assess the numbers of aphidophagous predators and aphids consisted of whole-plant visual inspections, using 1 m2 quadrats distributed randomly throughout the whole field. In order to avoid the influence of surrounding crops, a 20 m buffer zone around the edge of each field was not sampled. Visual sampling was conducted, as it provides an easy and accurate method for the estimation of larval and adult densities of coccinellids in agroecosystems (Michels and Behle 1992). Forty-eight quadrats were examined in each crop every week. Quadrats were located along transect lines across each field and spaced 20 m apart. All leaves and stems within the quadrat were examined, and all aphidophagous stages were recorded. Aphid species were also quantified on all leaves and stems. Larvae and pupae were brought to the laboratory to develop under laboratory conditions (24 ± 1° C, 75 ± 5% RH) for identification at the species level. All aphid predators were identified, with the exception of members of the common green lacewing, Chrysoperla carnea Stephens (Neuroptera: Chrysopidae) species complex, which were pooled together. This group comprises three cryptic species, C. kolthoffi Navas, C. lucasina Lacroix, and C. carnea Stephens, which can only be differentiated using molecular techniques (Bozsik et al. 2003; Lourenco et al. 2006).

Statistical analysis

In order to assess the species diversity, the collected data were analyzed by considering (1) species richness and (2) evenness according to the Shannon diversity index (H) (Magurran 1988), which considers both the number of species and the distribution of individuals among species. H is minimal if all individuals belong to only one species or if all species are represented by one individual; H is maximal if all individuals are evenly distributed. Evenness (J) varies from 0, if only one species dominates, to 1, if all species show similar abundance. Evenness (J) and the Shannon diversity index (H) were calculated as follows:

e01_01.gif

Because mean densities per m2 were low, these values are presented per 100 m2 The mean abundance per species was analyzed with an analysis of variance (ANOVA: general linear models) with crops (q = 4) and years (n = 3) used as factors (α = 0.05). Within crops, densities of species were compared using the least square difference (LSD; α = 0.05). To account for the variations of predator abundances, the abundance per species was analyzed using an analysis of covariance (ANCOVA: general linear models) with crops (q = 4) and years (n = 3) used as factors (α = 0.05) and aphid densities used as the covariable. Prior to analyses, a log10(x + 1) was used to transform the data distribution (counting) due to its asymmetry (Dagnelie 2011). Although statistical analyses were performed on transformed data, untransformed data are presented in Tables 4 and 5. Statistical analyses were performed using Minitab® release 1.5 ( www.minitab.com).

Results

Diversity of aphidophages

During the three years (2009–2011), 11 aphidophagous taxa were observed on the four different cultures: the hoverfly E. balteatus, the coccinellids C. septempunctata, C. quinquepunctata L. (Coleoptera: Coccinellidae), C. undecimpunctata (L.), H. axyridis, P. quatuordecimpunctata, A. bipunctata, A. decempunctata, the cream-spot ladybird, Calvia quatuordecimguttata (L.), Hippodamia variegata Goeze; and the C. carnea species group (Table 2).

From 2009 to 2011, species richness increased in broad bean, corn, and wheat, reaching 6, 8, and 7 species respectively (Table 3). Species richness did not evolve in potato crops, remaining at five species during the entire period. Overall, five aphidophages were continually observed during the three-year period in each crop and represented 95% of all the aphidophage observed in 2009 and 99% in both 2010 and 2011: E. balteatus, C. carnea s.l., C. septempunctata, P. quatuordecimpunctata, and H. axyridis.

The evenness value was low in wheat with J = 0.35, 0.25, and 0.38 in 2009, 2010, and 2011, respectively, with the numerical dominance of two species: C. septempunctata and E. balteatus (Tables 3, 4, and 5). In broad bean and potato, evenness varied from year to year. In broad bean, C. septempunctata was the most abundant in 2010 (J = 0.45) and 2011 (J = 0.59). In potato, C. carnea s.l. and C. septempunctata numerically dominated the aphidophagous guild in all three years (J = 0.65, 0.79, 0.74) (Table 3). In corn, the evenness during the three years decreased from 0.82 (2009) to 0.61 (2010).

Relative abundance of aphidophage in four crops

The relative abundance of both adult and larval stages of the five aphidophage within each crop showed significant differences (Tables 4 and 5), with the exception of potato in 2010, in which densities of larvae populations of different predators were not significantly different (F4.3570 = 1.4; p = 0.25) (Table 5).

Corn

The most abundant adult species in 2009 and 2010 was C. carnea s.l. and C. septempunctata (2009: F4,1065 = 10.7, p < 0.001 ; 2010: F4,3425 = 14.3, p < 0.001) (p < 0.05; LSD) (Table 4). In 2011, H. axyridis and C. septempunctata densities were both significantly higher than those of other species (p < 0.05; LSD) (F4,4055 = 24.2, p < 0.001) (Table 4). H. axyridis larvae densities were significantly higher in 2009 and 2011 (2009: F4,1065 = 5.4, p < 0.001 ; 2010: F4,3425 = 25.5, p < 0.001 ; 2011: F4,4055 = 57.0, p < 0.001) than those observed for the other species (Table 5).

Wheat

Adult populations of H. axyridis remained lower than other species during the three-year sampling (2009: F 4,1765 = 5.4, p < 0.001 ; 2010: F4,2925 = 24.1, p < 0.001; 2011: F4,2625 = 38.0, p < 0.001) (p < 0.05; LSD) and did not exceed 1.1 ± 0.6 adults per 100 m2 (Table 4). Episyrphus balteatus was the most frequently encountered adult species in 2009, whereas in 2010 and 2011 C. septempunctata was the most abundant species (p < 0.05; LSD) (Table 4). Larvae of E. balteatus were the most abundant (p < 0.05; LSD) of the aphidophage during the three years (2009: F4,1765 =11.7, p < 0.001 ; 2010: F4,2925 = 91.1, p < 0.001; 2011: F 4,2625 = 213.6, p < 0.001) (Table 5).

Potato

Trends for H. axyridis were the same in potato as in wheat: H. axyridis was not the most abundant species, and its density did not exceed 2.5 ± 0.7 adults per 100 m2 (Table 4). Two species were more abundant than others: C. carnea s.l. in 2009 and 2011 (2009: F 4,500 = 7.7, p < 0.001 ; 2011: F4,3250 = 10.8, p < 0.001), and C. septempunctata in 2010 (F4,3570 = 12.8, p < 0.001) and 2011 (p > 0.05; LSD). In 2009, larvae of C. carnea s.l., P. quatuordecimpunctata, and H. axyridis were the most abundant species but densities remained low (Table 5). In 2010, larvae densities of the five above-mentioned species were not significantly different from each other (F4,3570 = 1.4, p = 0.25) (Table 5). In 2011, only C. carnea s.l. numerically dominated the aphidophages community (F4,3250 = 5.5, p < 0.001) (p > 0.05; LSD) (Table 5).

Broad bean

In 2009, H. axyridis and C. septempunctata adults were the only adult species observed in broad bean (F 4,160 = 0.7, p > 0.05). Coccinella septempunctata was the most abundant species in 2010 (F4,2415 = 22.1, p < 0.001), while in 2011 both C. septempunctata and C. carnea s.l. were profusely observed (F4,280 = 37.5, p < 0.001) (p < 0.05; LSD) (Table 4). In 2009, three species were present at the larval stage: P. quatuordecimpunctata, C. carnea s.l., and E. balteatus (F4,160 = 1.0 ,p = 0.43) (p < 0.05; LSD). In 2010 (F4,2415 = 8.35, p < 0.001) and 2011 (F4,2480 = 21.2, p < 0.001), all species were observed, and C. septempunctata was the most abundant (Table 5).

Effect of aphid densities and sampling year on relative abundance of aphidophage

Abundances of H. axyridis in wheat and potatoes were not analyzed, due to very low numbers of individuals observed during the three-year inventory. Over the three-year sampling, adult populations of H. axyridis in corn significantly increased (F 2,1709 = 14.5, p < 0.001) (Table 6) from 7.8 ± 2.0 in 2009 to 19.9 ± 1.8 individuals per 100 m2 in 2011 (Table 4). Larval populations in the same crop also increased statistically (F 2,1709 = 39.9, p < 0.001) (Table 6), rising from 11.9 ± 4.2 to 70.8 ± 6.6 larvae per 100 m2 (Table 5). In broad bean, relative abundance of H. axyridis was not significantly different among the three years, neither at the adult (Table 6) nor larval (Table 7) stages.

Coccinella septempunctata larvae declined in broad bean (F2,1011 = 4.7, p = 0.009), wheat (F 2,1463 = 14.4, p < 0.001), and corn (F 2,1709 = 31.9, p < 0.001) (Table 7); densities decreased by 10 and 29.6 times in corn and broad bean respectively. In wehat, no larvae were observed in 2011, while 13.4 ± 3.9 larvae per 100 m2 were observed in 2009.

The abundances of three other aphidophage showed variable changes (Tables 6 and 7).

Aphid populations and correlation with aphidophage densities

In 2009, 2010, and 2011, seven, nine, and 10 species of aphids were identified, respectively: the pea aphid, Acyrthosiphon pisum Scopoli (Hemiptera: Aphididae); the cowpea aphid, Aphis craccivora Koch; the black bean aphid, Aphis fabae Scopoli; Aphis frangulae Walker; the buckthorn aphid, Aphis nasturtii Kaltenbach; the potato aphid, Macrosiphon euphorbiae Thomas; the vetch aphid, Megoura viciae Buckton; the rose grain aphid, Metopolophium dirhodum Walker; the green peach aphid, Mizns persicae Sulzer; Rhopalosiphum sp.; and Sitobion sp. (Table 8). The mean number of observed aphids increased in corn (F2,2589 = 39., p < 0.001) and potato (F2,1410 = 17.11, p < 0.001) from 2009 to 2011. Aphid densities also statistically varied in broad bean (F2,974 = 8.7, p < 0.001) and wheat (F2,1392 = 102.7, p < 0.001) from 2009 to 2011, but without any general evolution (Table 8).

The ANCOVA analyses showed a linear relationship between aphid and predator populations in 55% of adult populations (Table 6) and 35% of larvae populations (Table 7) (p aphids < 0.05, ANCOVA). In these cases, aphid densities influenced the predator abundance. Results (p years) comparison between ANOVA and ANCOVA showed that the influence of aphid populations on predator abundance variations between years was not statistically significant.; pyears of the two statistic analyses showed the same results.

Discussion

Since the invasive coccinellid H. axyridis spread over Europe (Brown et al. 2008), imposing negative impacts on native aphidophage and affecting composition of several guilds (Soares et al. 2008; Roy et al. 2012), studies have evaluated the population spread of this coccinellid. The current study's sampling of aphid predators in Belgian agroecosystems from 2009 to 2011 showed that H. axyridis lives and reproduces more efficiently in corn and broad bean than in wheat and potato. In corn, the evenness during the three years decreased when H. axyridis population increased strongly and was higher than the population of other species.

During the three-year sampling, 11 aphidophage were observed in these agroecosystems, but five of them predominated: E. balteatus, C. septempunctata, P. quatuordecimpunctata, H. axyridis, and C. carnea s.l. Five dominant species in agroecosystems is a common observation (Hodek and Honěk 1996). Observations on predator densities highlight that H. axyridis was not the numerically dominant species in every crop: in wheat and potato, C. septempunctata was more abundant than H. axyridis. In many European agricultural crops, both C. septempunctata and P. quatuordecimpunctata were dominant prior to the arrival of H. axyridis (Honěk 1979; Bode 1980; Chambers et al. 1982), and it appears that these two species have maintained their dominance in spite of being prone to intraguild predation by H. axyridis in the field (Hautier et al. 2008).

In our study, larvae of E. balteatus were the most abundant observed predators in wheat, which has already been reported by Tenhumberg and Poehling (1995) prior to the arrival of H. axyridis. Episyrphus balteatus has also been previously reported as one of the most abundant aphidophage in vegetable crops, such as broad beans (Colignon et al. 2001; Colignon et al. 2002). This could be explained by abiotic conditions (high density cereal crop, with high humidity and low temperature) that are more favorable to the larvae of E. balteatus (Honěk 1983).

The fact that H. axyridis is not the most abundant aphidophage in agrosystems is probably due to its generalist behavior and arboreal habitat selection (Hodek 1973; Chapin and Brou 1991; LaMana and Miller 1996; Brown and Miller 1998; Labrie 2007). However, it has been reported that H. axyridis can also thrive in agrosystems such as wheat, corn, and potato (LaMana and Miller 1996; Buntin and Bouton 1997; Colunga-Garcia and Gage 1998; Michaud 2002; Brown 2003; Nault and Kennedy 2003; Snyder et al. 2004; Jansen and Hautier 2008), as well as in herbaceous habitats (LaMana and Miller 1996; Koch et al. 2006; Alhmedi et al. 2007).

There were evident changes in the abundance of aphidophages in crops through the years, but this study does not propose to identify a global evolution (increase or decline) in any of the species that were observed in this study. The causes of such fluctuations are diverse and may include factors such as the diversity and abundance of aphid species (Wright and Laing 1980; Honěk 1982; Thalji 2006). The results of the ANCOVA showed that there was a linear relationship between prey and predator populations, but additional biotic and abiotic factors contribute to the annual variability of predator abundance. Climate could be one such factor, due to its influence on natural enemies, overwintering mortality, and aphid populations (Hodek and Honěk 1996; Szentkirályi 2001; Rotheray and Gilbert 2011). Several other factors could also explain the variation between crops: insolation, humidity (Honěk 1985), quantity and quality of host plants (Alhmedi et al. 2009), and adjacent habitats (Colignon et al. 2001; Alhmedi et al. 2009).

A particularly interesting finding is that although H. axyridis breeding occurred in all four inventoried crops to some extent, adults of this species are not ubiquitous; few immature individuals were recovered from potato and wheat. Assuming that declines in native species are caused by H. axyridis (Roy et al. 2012), this suggests that certain crops, such as wheat and potato, could act as refuges from H. axyridis at certain times, while native species, such as E. balteatus and C. septempunctata, are able to breed with a lower risk of intraguild predation or other forms of competition from the invaders. Such habitats could become even more important as native species adapt to the invader by evolving to avoid habitats where H. axyridis occurs in high numbers, as has been seen in co-occurring aphidophages in their native habitats (Sloggett 2012).

In conclusion, our study indicates that H. axyridis was not the most frequently observed aphidophage in the four most important Belgian agronomical crops. In future studies, longer samplings would be preferable in order to eventually identify quantitative changes in the native fauna suggested from other studies. Agroecosystems may even constitute an ecological reservoir for certain native aphidophage.

Table 1.

Sites surveyed for aphidophage from 2009 to 2011 in Belgium.

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Table 2.

Aphidophage diversity in four crops (broad bean, wheat, corn, and potato) from 2009 to 2011.

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Table 3.

Species richness and diversity index (H= Shannon-Weiner diversity index, where absolute diversity = 1.00; J = evenness or relative diversity (H/Hmax), where absolute evenness = 1.00).

t03_01.gif

Table 4.

Abundance (means and SE) of aphidophage (adults) per 100 m2 in four agroeco system s from 2009 to 2011. Means within a crop followed by the same letter were not significantly different for the same field (p > 0.05; LSD test).

t04_01.gif

Table 5.

Abundance (means and SE) of aphidophage (larvae) per 100 m2 in four agroecosystems from 2009 to 2011. Means within a crop followed by the same letter were not significantly different for the same field (p > 0.05; LSD test).

t05_01.gif

Table 6.

ANOVA and ANCOVA summary of the effects of aphid abundance and year sampling (2009, 2010, 2011) on the abundane of five predators at the adult stage in four crops (corn, wheat, potato, and broad bean).

t06_01.gif

Table 7.

ANOVA and ANCOVA summary of the effects of aphid abundance and year sampling (2009, 2010, 2011) on the abundance of five predators at the larval stage in four crops (corn, wheat, potato, and broad bean).

t07_01.gif

Table 8.

Mean numbers and SE of aphids/100 m2 observed in four fields (wheat, broad bean, corn, and potato) from 2009 to 2011.

t08_01.gif

Acknowledgements

We thank V. Sibret and A.M. Buset for their technical assistance, Dr Y. Brostaux for his advice on statistical analysis, and P. Leroy and C. De Clerck for their helpful comments on previous versions of the manuscript. The authors are grateful to Professor B. Bodson and F. Vancutsem of the Unité de Phytotechnie des Régions Tempérées (ULg, GxABT) for the availability of fields. This research was funded by the Service Public de Wallonie (SPW - DGO3, project n°D311197). Delphine Durieux was financially supported by a Ph.D. grant from the Fonds pour la formation à la Recherche dans l'Industrie et l'Agriculture (FRIA), Belgium.

References

  1. T Adriaens , E Branquart , D. Maes 2003. The Multicoloured Asian Ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), a threat for native aphid predators in Belgium? Belgian Journal of Zoology 133(2): 195–196. Google Scholar

  2. T Adriaens , GMY Gomez , D. Maes 2008. Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl 53(1): 69–88. Google Scholar

  3. T Adriaens , G San Martin , L Hautier , E Branquart , D. Maes 2010. Toward a Noah's Ark for native ladybirds in Belgium. IOBC/wprs Bulletin 58: 1–3. Google Scholar

  4. A Alhmedi , E Haubruge , B Bodson , F. Francis 2007. Aphidophagous guilds on nettle (Urtica dioica) strips close to fields of green pea, rape and wheat. Insect Science 14: 419– 424. Google Scholar

  5. A Alhmedi , E Haubruge , F. Francis 2009. Effect of stinging nettle habitats on aphidophagous predators and parasitoids in wheat and green pea fields with special attention to the invader Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Entomological Science 12(4): 349–358. Google Scholar

  6. E. Bode 1980. Aphids in winter wheat: abundance and limiting factors from 1976 to 1979. Bulletin SROP 3(4): 49–57. Google Scholar

  7. A Bozsik , J Mignon , C. Gaspar 2003. The Chrysoperla carnea complex in Belgium (Neuroptera: Chrysopidae). Notes fauniques de Gembloux (50): 9–14. Google Scholar

  8. MW. Brown 2003. Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis. BioControl 48(2): 141–153. Google Scholar

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

  10. PMJ Brown , T Adriaens , H Bathon , J Cuppen , A Goldarazena , T Hagg , M Kenis , BEM Klausnitzer , I Kovar , AJM Loomans , MEN Majerus , O Nedved , J Pedersen , W Rabitsch , HE Roy , V Ternois , IA Zakharov , DB. Roy 2008. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53(1):5–21. Google Scholar

  11. PMJ Brown , R Frost , J Doberski , T Sparks , R Harrington , HE. Roy 2011a. Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecological Entomology 36(2): 231–240. Google Scholar

  12. PMJ Brown , CE Thomas , E Lombaert , DL Jeffries , A Estoup , L-JL. Handley 2011b. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl 56(4): 623–641. Google Scholar

  13. GD Buntin , JH. Bouton 1997. Aphid (Homoptera: Aphididae) management in alfalfa by spring grazing with cattle. Journal of Entomological Science 32(3): 332–341. Google Scholar

  14. RJ Chambers , KD Sunderland , DL Stacey , IJ. Wyatt 1982. A survey of cereal aphids and their natural enemies in winter-wheat in 1980. Annals of Applied Biology 101(1): 175–178. Google Scholar

  15. JB Chapin , VA. Brou 1991. Harmonia axyridis (Pallas), the 3rd species of the genus to be found in the United-States (Coleopera, Coccineliidae). Proceedings of the Entomological Society of Washington 93(3): 630–635. Google Scholar

  16. P Colignon , C Gaspar , F. Francis 2002. Effets de l'environnement proche sur la biodiversité entomologique en carottes de plein champ. Annales de la 2ème Conférence Internationale sur les moyens alternatifs de lutte contre les organismes nuisibles aux végétaux : 252–257. Google Scholar

  17. P Colignon , P Hastir , C Gaspar , F. Francis 2001. Effets de l'environnement proche sur la biodiversité entomologique en cultures maraichères de plein champ. Parasitica 56: 59–70. Google Scholar

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

  19. P. Dagnelie 2011. Les transformations de variables. In: Statistique théorique et appliquée. Tome 2. Inférence statistique à une et à deux dimensions. pp. 103–124. De Boeck. Google Scholar

  20. M Derume , P Hauteclair , C. Bauffe 2007. Inventaire et comparaison de la faune des coccinelles (Coleoptera: Coccinellidae) des terrils des bassins miniers wallons liégeois et hennuyer (Belgique). Natura Mosana 60(2): 33–56. Google Scholar

  21. EW. Evans 2004. Habitat displacement of North American ladybirds by an introduced species. Ecology 85(3): 637–647. Google Scholar

  22. F. Francis 2001. Etude de la diversité et des plantes hôtes des Coccinellidae de Belgique. Notes fauniques de Gembloux 44: 3–11. Google Scholar

  23. JP Harmon , E Stephens , J. Losey 2007. The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. Journal of Insect Conservation 11(1): 85–94. Google Scholar

  24. L Hautier , JC Gregoire , J de Schauwers , GS Martin , P Callier , JP Jansen , JC. de Biseau 2008. Intraguild predation by Harmonia axyridis on coccinellids revealed by exogenous alkaloid sequestration. Chemoecology 18(3): 191–196. Google Scholar

  25. I. Hodek 1973. Biology of Coccinellidae. Dr. W. Junk. Google Scholar

  26. I Hodek , A. Honěk 1996. Ecology of Coccinellidae. Kluwer Academic Publishers. Google Scholar

  27. A. Honěk 1979. Plant -density and occurrence of Coccinella septempunctata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in cereals. Acta Entomologica Bohemoslovaca 76(5): 308–312. Google Scholar

  28. A. Honěk 1982. Factors which determine the composition of field communities of adult aphidophagous coccinellidae (Coleoptera) Journal of Applied Entomology 94(2): 157– 168. Google Scholar

  29. A. Honěk 1983. Factors affecting the distribution of larvae of aphid predators (Col., Coccinellidae and Dipt., Syrphidae) in cereal stands. Journal of Applied Entomology 95(4): 336–345. Google Scholar

  30. A. Honěk 1985. Habitat preferences of aphidophagous coccinellids (Coleoptera). Entomophaga 30(3): 253–264. Google Scholar

  31. B Ingels , P. De Clercq 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. Google Scholar

  32. J Jansen , L. Hautier 2008. Ladybird population dynamics in potato: comparison of native species with an invasive species, Harmonia axyridis. Biological Control to Invasion 53: 223–233. Google Scholar

  33. RL Koch , RC Venette , WD. Hutchison 2006. Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western Hemisphere: implications for South America. Neotropical Entomology 35(4): 421–434. Google Scholar

  34. G. Labrie 2007. Les mécanismes d'invasion de la coccinelle asiatique Harmonia axyridis Pallas au Québec. Biologie : 272. Google Scholar

  35. G Labrie , E Lucas , D. Coderre 2006. Can developmental and behavioral characteristics of the multicolored Asian lady beetle Harmonia axyridis explain its invasive success? Biological Invasions 8(4): 743–754. Google Scholar

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

  37. E Lombaert , T Guillemaud , JM Cornuet , T Malausa , B Facon , A. Estoup 2010. Bridgehead Effect in the Worldwide Invasion of the Biocontrol Harlequin Ladybird. PLOS ONE 5(3). Google Scholar

  38. P Lourenco , C Brito , T Backeljau , D Thierry , MA. Ventura 2006. Molecular systematics of the Chrysoperla carnea group (Neuroptera: Chrysopidae) in Europe. Journal of Zoological Systematics and Evolutionary Research 44(2): 180–184. Google Scholar

  39. AE. Magurran 1988. Ecological diversity and its measurement. Croom Helm. Google Scholar

  40. M Majerus , V Strawson , H. Roy 2006. The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecological Entomology 31(3): 207– 215. Google Scholar

  41. DE Marco , SA Paez , SA. Cannas 2002. Species invasiveness in biological invasions: a modelling approach. Biological Invasions 4: 193–205. Google Scholar

  42. JP. Michaud 2002. Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environmental Entomology 31(5): 827–835. Google Scholar

  43. GJ Michels , RW. Behle 1992. Evaluation of sampling methods for lady beetles (Coleoptera: Coccinellidae) in grain-sorghum. Journal of Economic Entomology 85(6): 2251–2257. Google Scholar

  44. BA Nault , GG. Kennedy 2003. Establishment of multicolored Asian lady beetle in Eastern North Carolina: seasonal abundance and crop exploitation within an agricultural landscape. BioControl 48(4): 363–378. Google Scholar

  45. JK Pell , J Baverstock , HE Roy , RL Ware , MEN. Majerus 2008. Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53(1): 147–168. Google Scholar

  46. MW Phoofolo , JJ. Obrycki 1998. Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomologia Experimentalis Et Applicata 89(1): 47–55. Google Scholar

  47. G Rotheray , FS. Gilbert 2011. The Natural History of Hoverflies. Forrest Text. Google Scholar

  48. HE Roy , T Adriaens , NJB Isaac , M Kenis , T Onkelinx , GS Martin , PMJ Brown , L Hautier , R Poland , DB Roy , R Comont , R Eschen , R Frost , R Zindel , J Van Vlaenderen , O Nedvěd , HP Ravn , J-C Grégoire , J-C de Biseau , D. Maes 2012. Invasive alien predator causes rapid declines of native European ladybirds. Diversity and Distributions 18(7): 717–725. Google Scholar

  49. HE Roy , J Baverstock , RL Ware , SJ Clark , MEN Majerus , KE Baverstock , JK. Pell 2008. Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecological Entomology 33(2): 175–182. Google Scholar

  50. S Sato , AFG. Dixon 2004. Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds: consequences for invasive species. Agricultural and Forest Entomology 6(1): 21– 24. Google Scholar

  51. JJ. Sloggett 2012. Harmonia axyridis invasions: Deducing evolutionary causes and consequences. Entomological Science 15: 261–273. Google Scholar

  52. WE Snyder , GM Clevenger , SD. Eigenbrode 2004. Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140(4): 559–565. Google Scholar

  53. AO Soares , I Borges , PAV Borges , G Labrie , E. Lucas 2008. Harmonia axyridis: What will stop the invader? BioControl 53(1): 127–145. Google Scholar

  54. F. Szentkirályi 2001. Ecology and habitat relationships. In: PK McEwen , TR New , AE Whittington , Editors. Lacewings in the Crop Environment , pp. 82–115. University Press. Google Scholar

  55. B Tenhumberg , HM. Poehling 1995. Syrphids as natural enemies of cereal aphids in Germany: aspects of their biology and efficacy in different years and regions. Agriculture, Ecosystems and Environment 52(1): 39–43. Google Scholar

  56. R. Thalji 2006. Composition of coccinellid communities in sugar beet fields in Vojvodina. Zbornik Matice Srpske za Prirodne Nauke 2006(110): 267–273. Google Scholar

  57. R Ware , B Yguel , M. Majerus 2009. Effects of competition, cannibalism and intra-guild predation on larval development of the European coccinellid Adalia bipunctata and the invasive species Harmonia axyridis. Ecological Entomology 34(1): 12–19. Google Scholar

  58. RL Ware , MEN. Majerus 2008. Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53(1): 169– 188. Google Scholar

  59. PM Wells , J Baverstock , MEN Majerus , FM Jiggins , H Roy , JK. Pell 2010. Intraguild predation of non-coccinellid aphid natural enemies by Harmonia axyridis: prey range and factors influencing intraguild predation. IOBC/wprs Bulletin 58: 185–192. Google Scholar

  60. KA With , DM Pavuk , JL Worchuck , RK Oates , JL. Fisher 2002. Threshold effects of landscape structure on biological control in agroecosystems. Ecological Applications 12(1): 52–65. Google Scholar

  61. EJ Wright , JE. Laing 1980. Numerical response of coccinellids to aphids in corn in Southern Ontario. Canadian Entomologist 112(10): 977–988. Google Scholar

Copyright: This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed.
Axel Vandereycken, Delphine Durieux, Emilie Joie, John J. Sloggett, Eric Haubruge, and François J. Verheggen "Is the Multicolored Asian Ladybeetle, Harmonia axyridis, the Most Abundant Natural Enemy to Aphids in Agroecosystems?," Journal of Insect Science 13(158), (1 December 2013). https://doi.org/10.1673/031.013.15801
Received: 11 June 2012; Accepted: 1 April 2013; Published: 1 December 2013
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