Life history of the harlequin ladybird, <Emphasis Type="Italic">Harmonia axyridis</Emphasis>: a global meta-analysis

The harlequin ladybird, Harmonia axyridis, is an important natural enemy of aphids throughout the world, but is now also considered an invasive alien species. We performed a meta-analysis of published life history data to address the question whether invading populations in Europe and North America have life history parameters that differ from native populations in Asia, explaining the beetle’s invasion success in new territories. In this meta-analysis, we accounted for important covariables that are often reported in published studies such as temperature, food source (aphids or eggs of Ephestia kuehniella), strain (laboratory or field populations) and photoperiod. Temperature was a key factor having consistent large effects on development rate, survival and reproductive characteristics of H. axyridis. Food source, strain, and photoperiod had effects on some, but not all characteristics, and their overall effect across characteristics was minor. Individuals of invasive populations had a shorter pre-oviposition period and higher fecundity at low temperatures than those of native populations, and a greater longevity across all temperatures. No differences in survival were found between native and invasive populations, while differences in development rate were not consistent, with opposing results obtained according to the way development rate was measured in trials reported in the literature. Results of this meta-analysis support the hypothesis that the life history of the beetle has changed during its invasion into North America and Europe. Invasive populations had a shorter pre-oviposition period and higher fecundity at low temperatures, as well as a greater longevity across all temperatures than native populations. These differences may partially explain the invasive success of H. axyridis.     

Paternity following multiple mating in ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

We investigated factors which may determine realised paternity following multiple mating in a promiscuous ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), namely the mating order and ability of males of different morphs to fertilize females. In experiments using males of two colour morphs, we found that the first male had a reproductive advantage over the second male (sperm precedence P2 = 0.38). Males of the melanic morph spectabilis had a reproductive advantage over males of the semi-melanic morph axyridis (P2 = 0.35). Analysis of paternity using microsatellites applied to young larvae, which avoids possible differential mortality of progeny, confirmed the precedence of the first male and higher paternity rate of colour morphs that are more frequent in the wild. Hatchability of eggs increased from 65% after the first mating to 85% after the second mating delayed by five days. Average duration of mating was 157 min and did not differ between the first and second mating and between the colour morphs of males.     

The aggregation behavior of <Emphasis Type="Italic">Harmonia axyridis</Emphasis> in its native range in Northeast China

Harmonia axyridis has become notorious as an urban pest in many of the regions where it has been introduced, despite its numerous contributions to the biological control of insects injurious to agriculture and horticulture. Aggregative behavior prior to overwintering leads to invasions of human habitations as beetles seek refuge from freezing temperatures. Here we describe the aggregation behavior of native H. axyridis populations of northeast China that breed in agricultural fields (mostly corn and rice) and shrub/forest habitats and then migrate through rural villages in autumn. More than 140,000 beetles were collected during direct observations in 16 villages in five townships in Jilin Province. Beetles aggregated on dwellings shortly after agricultural harvests, favoring white walls with southern exposures, the largest aggregations occurring in villages in mountainous townships at higher elevations. The sex ratio was consistently female-biased and succinic phenotypes were more than twice as abundant as melanic phenotypes in all locations. A special trap compared the relative attractiveness of different surface colors (white > yellow = black > green > red = natural wood) and potential baits (corn pollen = honey > caramel = cocoa > milk = blank control). All aggregations disappeared abruptly just prior to the first frost, whereupon beetles were discovered sheltering in montane caves with southern aspects at higher elevations. Villagers reported substantial expenditures on pesticides in efforts to eliminate beetles from their homes every autumn. Invasion of human habitations appears to be an intrinsic tendency of native H. axyridis populations in China, which is the result of behavioral adaptations for cold-avoidance.     

Intraguild predation on the aphid parasitoid <Emphasis Type="Italic">Aphelinus asychis</Emphasis> by the ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

We investigated intraguild predation (IGP) on an aphid parasitoid, Aphelinus asychis Walker (Hymenoptera: Aphelinidae), by the multicolored Asian ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), and used the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) as the prey/host in the laboratory. The ladybirds reared on artificial diet and on aphids consumed more aphids than mummies, while those reared on parasitized aphids consumed similar numbers of aphids and mummies. The ladybirds chose more mummies in treatments when mummies were more abundant, and more aphids when numbers of aphids and mummies were equal, or when aphids were more abundant. However, at all density treatments, rejection rates of mummies (36%) were much greater than of aphids (2%). H. axyridis prey on more aphids than A. asychis mummies, which enhances biological control by the two species. However, prior feeding experience affected subsequent choice, increasing the competition between natural enemies which would reduce their combined effectiveness for biological control.     

Spotlight on the positive effects of the ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis> on agriculture

In the midst of considerable negativity surrounding the ladybird Harmonia axyridis (Pallas), this paper sheds some light on the positive effects that this predator has had on agriculture. Using resources available at the USDA, National Agricultural Library (DigiTop literature database, Navigator platform), I searched the abstracts of published literature on H. axyridis using the search term “Harmonia axyridis” or “Leis axyridis.” After deleting duplicate records, there were 1193 total records on this ladybird in the database dating from 1961–2015. Of this total, 90 records (7.54 %) highlighted positive effects of H. axyridis on agriculture in terms of its spectacular voracity, predation capacity, and effectiveness in suppressing plant pests, primarily aphids and scales, in forests, orchards, crop fields, gardens, greenhouses, and in laboratory bioassays. More concerted research is necessary to develop methodologies to exploit the positive behaviors of H. axyridis, while managing its negative ones.     

The chemical ecology of <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

We review the chemical ecology of the ladybird beetle Harmonia axyridis from the perspective of its invasiveness and the deleterious effects it exerts in the regions it has colonised. We outline the nature and quantification of its chemical defence, and discuss the protection this provides against natural enemies, particularly intraguild predators. We consider the role of infochemicals in location of prey, intraspecific communication and intraguild interactions. We also discuss the role of prey allelochemicals in relation to H. axyridis extreme dietary generalism. Harmonia axyridis poses a number of practical problems for human health and well-being, including “ladybug taint” wine contamination and problems resulting from large aggregations overwintering in buildings. We consider chemical insights into these issues and, in particular, how attractants and repellents might help manage H. axyridis populations through a push–pull strategy. We conclude by discussing future perspectives for research.     

Living with the enemy: parasites and pathogens of the ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

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

Heritable bacterial endosymbionts in native and invasive populations of <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

Harmonia axyridis Pallas (1773) (Coleoptera: Coccinellidae) is the well-studied system of invasive insect species. Native and invasive parts of the area of H. axyridis are isolated geographically. We studied the species composition and the distribution of bacterial symbionts Spiroplasma and Rickettsia in seven localities of the native area and six localities of the invasive area of H. axyridis. Rickettsia was detected in H. axyridis populations for the first time. We found that the proportion of beetles infected with Rickettsia in native and invasive populations of H. axyridis is about 0.03. Spiroplasma was found only in native populations of H. axyridis. The proportion of infected individuals with Spiroplasma in native populations of H. axyridis is about 0.08. All studied native populations of H. axyridis are infected with Spiroplasma, while all invasive populations are not. We discuss the possible influence of Spiroplasma and Rickettsia in the formation of invasive populations of H. axyridis.     

Life cycle of <Emphasis Type="Italic">Harmonia axyridis</Emphasis> in central Europe

The development and reproduction, and maximum number of generations across seasons were ascertained for populations of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Central Europe. Number of generations was calculated using the thermal characteristics of development and summation of daily average air temperatures, in 2007–2016. This species can produce 2–3 generations per year. However, there is insufficient time for it to achieve its full reproductive potential. Delayed emigration from hibernacula (late April) shortened the period of seasonal activity by 1–6%. Breeding occurred from May to mid September. Oviposition continued into late summer, which left insufficient time for the late-hatching immatures to complete their development before the onset of winter. A high mobility, opportunistic use of prey patches and weak tendency to enter dormancy provide the potential for population increase by extending the period of development of immatures at the risk of failure if the cold period comes early.     

Species assemblages of ladybirds including the harlequin ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis>: a comparison at large spatial scale in urban habitats

We evaluated the status of native ladybird assemblages in the presence of the non-native ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in three European countries. To achieve this, we assessed the abundance of ladybirds from common host plants in urban areas of Great Britain, Czech Republic and Slovak Republic in 2014. We determined (i) the effects of season, host plant, location, abundance of H. axyridis and aphids on the ladybird species assemblage, (ii) the relationship between ladybird abundance and aphid density, (iii) the relationship between diversity of native ladybird species and the abundance of H. axyridis. There was a non-linear relationship between abundance of ladybirds and abundance of aphids but we found the abundance of other ladybird species was not correlated with H. axyridis. We highlight the value of large-spatial scale studies for revealing patterns in community assemblages and ultimately informing understanding of ecosystem resilience.     

Parasites of <Emphasis Type="Italic">Harmonia axyridis</Emphasis>: current research and perspectives

Harmonia axyridis (Coleoptera: Coccinellidae) has been introduced widely for biological control of agricultural pests. Harmonia axyridis has established in four continents outside of its native range in Asia and it is considered an invasive alien species (IAS). Despite a large body of work on invasion ecology, establishment mechanisms of IAS and their interactions with natural enemies remain open questions. Parasites, defined as multicellular organisms that do not directly kill the host, could potentially play an important role in regulating host populations. This study presents a review of the parasites of H. axyridis, discussing their distributions and effects on host populations across the host’s native and invasive range. These parasites are: Hesperomyces virescens Thaxt. fungi, Coccipolipus hippodamiae (McDaniel and Morrill) mites, and Parasitylenchus bifurcatus Poinar and Steenberg nematodes.     

First report of <Emphasis Type="Italic">Harmonia axyridis</Emphasis> Pallas being attacked by <Emphasis Type="Italic">Dinocampus coccinellae</Emphasis> Schrank in Canada

Field parasitism of two lady beetles, a recently introduced species, Harmonia axyridis Pallas, and an indigenous species, Coleomegilla maculata lengi Timberlake, by Dinocampus coccinellae Schrank (Hymenoptera: Braconidae) was investigated in southwestern Québec. Adult coccinellids were sampled from June to September 2001 in alfalfa and corn fields. Parasitism rates were recorded by dissection and rearing of coccinellids in controlled condition. The average proportions of coccinellids with a parasitoid larva were 4.6%for H. axyridis and 32%for C. maculata but 0%of the H. axyridis and 5.9%of theC. maculatawere successfully parasitized. In July, more C. maculata than H. axyridiswere found to be parasitized and among all individuals dissected, C. maculata were more frequently found superparasitized than H. axyridis. Our results suggest that D. coccinellae is not well adapted to H. axyridis in Quebec. This is the first mention of H. axyridis being attacked by D. coccinellae in Canada.     

Reduced population size can induce quick evolution of inbreeding depression in the invasive ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

Understanding biological invasion is currently one of the main scientific challenges for ecologists. The introduction process is crucial for the success of an invasion, especially when it involves a demographic bottleneck. A small introduced population is expected to face a higher risk of extinction before the first stage of invasion is complete if inbreeding depression, caused by the expression of deleterious alleles, is important. Changes in mating regimes or in population size can induce the evolution of deleterious allele frequencies, either by selection or by drift, possibly resulting in the purging or the fixation of such alleles within the population. The harlequin ladybird Harmonia axyridis became invasive on several continents following a scenario including at least one event of demographic bottleneck. Although native populations suffered from severe inbreeding depression, it was greatly reduced in invasive ones suggesting that deleterious alleles were purged during the invasion process. In this study, we performed an experiment designed to manipulate the effective population size of H. axyridis across successive generations to mimic contrasting introduction events. We used the measurement of two fitness-related phenotypic traits in order to test (1) if inbreeding depression can evolve at the time-scale of an invasion; and (2) if the changes in inbreeding depression following a bottleneck in laboratory conditions are compatible with the purging of deleterious alleles observed in this species. We found that two generations of very low population size are enough to induce a substantial change in inbreeding depression. Although the genetic changes mostly consisted in fixation of deleterious alleles, purging did also occur, sometimes simultaneously with fixation.     

Alkaloids provide evidence of intraguild predation on native coccinellids by <Emphasis Type="Italic">Harmonia axyridis</Emphasis> in the field

Over a period of less than 5 years, Belgium was thoroughly invaded by the multicolored Asian coccinellid, Harmonia axyridis. At the same time, a decline of some native coccinellid species was observed in tree habitats. One hypothesis about the cause of this decline was that it might have been due to intraguild predation (IGP) by H. axyridis. In natural conditions, IGP between coccinellids can be tracked by using defensive compounds. Exogenous alkaloids in H. axyridis were therefore examined by gas chromatography-mass spectrometry (GC–MS), using individuals sampled from lime trees that were also occupied by other species of coccinellids. Harmonia axyridis was the dominant species at all life stages, in terms of both numbers of sites occupied and local abundance. The GC–MS analysis of H. axyridis larvae revealed traces of exogenous alkaloids from 19 of the 20 sites and, in nine of those 19 sites, more than 30% of the larvae analyzed contained exogenous alkaloids. Three alkaloids were detected: adaline from Adalia spp., calvine from Calvia spp. and propyleine from Propylea quatuordecimpunctata. Predation by H. axyridis on two different coccinellid species was also detected in the same larva, reinforcing the status of H. axyridis as a top predator. A generalized linear model indicated that IGP frequency was positively influenced by two variables: the abundance of extraguild and intraguild prey; and the interaction between these two variables. Our results therefore support the hypothesis that IGP by H. axyridis on native coccinellids in tree habitats has led to the decline of several of these species.     

Importance of early arrival of adult <Emphasis Type="Italic">Harmonia axyridis</Emphasis> for control of <Emphasis Type="Italic">Aphis spiraecola</Emphasis> on apple

The biological control of aphid populations may only be possible when natural enemies arrive soon after aphid colonization. This study was done to identify how quickly adult Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) need to arrive at newly established spirea aphid [Aphis spiraecola Patch (Homoptera: Aphididae)] colonies on apple (Malus domestica Borkh.) to provide population control. A total of 100 newly established spirea aphid colonies were caged in an experimental apple orchard in West Virginia, USA. A single adult H. axyridis was added to each of ten caged colonies at day 0, 5, 10, 15 and 20 days after caging. An additional ten caged colonies were opened for exposure to natural levels of predation at each of the treatment intervals as a control. The single H. axyridis eliminated the aphid colonies significantly more quickly than natural predation for up to ten days after colony establishment. The probability of an aphid colony producing alates was significantly lower in the presence of a single H. axyridis adult than when exposed to natural predation for the first ten days. Adult H. axyridis beetles are capable of completely controlling individual spirea aphid colonies on apple only if they are abundant enough to find colonies within one week of colony establishment.     

Effect of size,extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis> and the hoverfly <Emphasis Type="Italic">Episyrphus balteatus</Emphasis>

Intraguild predation (IGP) is a widespread interaction between predatory arthropods, and is influenced by several factors. The harlequin ladybird, Harmonia axyridis (Coleoptera: Coccinellidae), has frequently been reported as an intraguild predator of other Coccinellidae, but little is known about its interactions with other aphidophagous predators, including syrphids. This study investigated the incidence of IGP between H. axyridis and Episyrphus balteatus (Diptera: Syrphidae), the most abundant hoverfly species in Europe and a commercially available aphid biocontrol agent. The influence of size, presence of extraguild prey and habitat complexity were investigated through laboratory experiments in Petri dishes and on potted broad bean plants. In both types of arenas, IGP between H. axyridis and E. balteatus was found to be asymmetric, with the coccinellid in the majority of cases being the intraguild predator. There was a significant effect of size on the frequency of IGP. The efficiency of H. axyridis as an intraguild predator increased with the developmental stage. Early instars of E. balteatus were the most vulnerable to IGP. Pupae of either species were not attacked. In the presence of extraguild prey, the frequency of IGP was substantially reduced. However, IGP still occurred, mainly in combinations of older larvae of H. axyridis with first or second instars of E. balteatus. The size of the arena affected the incidence of IGP in combinations with second instars of E. balteatus, but not in combinations with third instars. Field research is needed to elucidate the ecological relevance of IGP among these predators.     

Ecology of <Emphasis Type=Italic>Harmonia axyridis</Emphasis> in natural habitats within its native range

Originally distributed in northeast Asia, Harmonia axyridis (Coleoptera: Coccinellidae) is now found throughout much of the temperate zone. In its native area, H. axyridis maintains stable populations in heterogeneous and temporary habitats because of its great ability to find prey and reproduce, coupled with density-dependent and self-regulatory population regulation. A negative correlation of H. axyridis on the biodiversity of the aphidophagous community has been observed in its native range. The decrease in biodiversity may be mainly caused by the wider range of habitats available to H. axyridis than to the coexisting species. From a theoretical perspective, density-dependent regulation of H. axyridis populations, e.g., cannibalism, may be more important in maintaining the H. axyridis-dominated system, probably than is intraguild predation. Habitat heterogeneity may also be important to the coexistence of H. axyridis and other predators in both native and invaded areas.     

<Emphasis Type="Italic">Ty</Emphasis>1<Emphasis Type="Italic">/copia</Emphasis>- and <Emphasis Type="Italic">Ty</Emphasis>3<Emphasis Type="Italic">/gypsy</Emphasis>-like DNA sequences in <Emphasis Type="Italic">Helianthus </Emphasis>species

Two repeated DNA sequences isolated from a partial genomic DNA library of Helianthus annuus, p HaS13 and p HaS211, were shown to represent portions of the int gene of a Ty3 /gypsy retroelement and of the RNase-Hgene of a Ty1 /copia retroelement, respectively. Southern blotting patterns obtained by hybridizing the two probes to BglII- or DraI-digested genomic DNA from different Helianthus species showed p HaS13 and p HaS211 were parts of dispersed repeats at least 8 and 7 kb in length, respectively, that were conserved in all species studied. Comparable hybridization patterns were obtained in all species with p HaS13. By contrast, the patterns obtained by hybridizing p HaS211 clearly differentiated annual species from perennials. The frequencies of p HaS13- and p HaS211-related sequences in different species were 4.3x10(4)-1.3x10(5) copies and 9.9x10(2)-8.1x10(3) copies per picogram of DNA, respectively. The frequency of p HaS13-related sequences varied widely within annual species, while no significant difference was observed among perennial species. Conversely, the frequency variation of p HaS211-related sequences was as large within annual species as within perennials. Sequences of both families were found to be dispersed along the length of all chromosomes in all species studied. However, Ty3 /gypsy-like sequences were localized preferentially at the centromeric regions, whereas Ty1/ copia-like sequences were less represented or absent around the centromeres and plentiful at the chromosome ends. These findings suggest that the two sequence families played a role in Helianthusgenome evolution and species divergence, evolved independently in the same genomic backgrounds and in annual or perennial species, and acquired different possible functions in the host genomes.     

Population variation of elytral ridge occurrence in ladybirds <Emphasis Type="Italic">Harmonia axyridis</Emphasis> Pallas

Intra- and interpopulation variation of occurrence of elytral ridge (neutral morphological character with the known genetic determination) in some populations of Harmonia axyridis from the Russian part of the species area was studied for the first time. Comparative analysis of the frequencies of the recessive allele r of a corresponding gene and the frequencies of recessive homozygotes in 32 samples from 16 localities has shown the lack of temporal and microgeographic variations of this trait. The character of its geographic variation con-firms the hypothesis advanced earlier on the basis of analysis of elytral pattern variation about the existence of two subspecies of H. axyridis and suggests the existence of a zone of secondary hybridization between them in the central part of the area.     

New combinations and typifications in <Emphasis Type="Italic">Bistorta</Emphasis>, <Emphasis Type="Italic">Persicaria</Emphasis>, <Emphasis Type="Italic">Polygonum,</Emphasis> and <Emphasis Type="Italic">Rumex</Emphasis> (Polygonaceae)

New combinations are proposed in anticipation of the Polygonaceae treatment in the forthcoming volume of Intermountain Flora: Polygonum kelloggii var. esotericum, P. kelloggii var. watsonii , Rumex densiflorus var. pycnanthus , R. salicifolius var. utahensis, and R. occidentalis var. tomentellus. Typifications are proposed to facilitate ongoing studies in Polygonaceae and to maintain current usage.