Native Ladybird Research Articles

Invasive Harlequin Ladybird Carries Biological Weapons Against Native Competitors

Invasive species that proliferate after colonizing new habitats have a negative environmental and economic impact. The reason why some species become successful invaders, whereas others, even closely related species, remain noninvasive is often unclear. The harlequin ladybird Harmonia axyridis, introduced for biological pest control, has become an invader that is outcompeting indigenous ladybird species in many countries. Here, we show that Harmonia carries abundant spores of obligate parasitic microsporidia closely related to Nosema thompsoni. These microsporidia, while not harming the carrier Harmonia, are lethal pathogens for the native ladybird Coccinella septempunctata. We propose that intraguild predation, representing a major selective force among competing ladybird species, causes the infection and ultimate death of native ladybirds when they feed on microsporidia-contaminated Harmonia eggs or larvae.

Refuge for native lady beetles (Coccinellidae) in perennial grassland habitats

The proportion of native individuals in North American lady bee- tle communities has declined precipitously over the past 30 years, particularly in annual cropping systems. At the same time, the number and abundance of exotic coccinellid species have been on the rise as beetles are introduced both inadvertently and intentionally for the purposes of biological control. 2. Perennial grasslands have been proposed as refuge habitats that promote native lady beetles, either by resisting the invasion of exotics or by providing a consistent source of shelter and resources. 3. Our objective is to compare the conservation value for native lady beetles of different perennial grassland habitats that vary in their degree of habitat modification and disturbance. 4. The abundance, species richness, and species composition of native and exotic lady beetles were compared across remnant native tallgrass prairies, native tallgrass prairies actively restored from cultivation and exotic tall fescue grasslands grown as forage crops. 5. Native species dominated the lady beetle community in all perennial grass- land habitats, with more than 95% of captured individuals being native in ori- gin. Exotic lady beetle species were equally rare across all habitat types. 6. The grassland habitat considered the most disturbed, agriculturally grown exotic tall fescue, had the highest abundance and species richness of native lady beetles and a unique composition of species as compared to prairie habitats. Lady beetle communities in remnant and restored tallgrass prairies were indistinguishable, indicating that prairie restoration successfully re-established coccinellid communities. 7. Promoting perennial grasslands, both natural and agricultural, within disturbed landscapes has the potential to enhance native lady beetle populations.

Occurrence of the exotic predatory ladybird Platynaspidius maculosus (Coleoptera: Coccinellidae) in citrus groves in Shizuoka City, Central Japan: seasonal prevalence of adults captured on sticky traps

Platynaspidius maculosus (Weise, 1910) (Coleoptera: Coccinellidae) is a ladybird beetle that preys on aphids and is distributed in China, Taiwan, and Vietnam. Recently, P. maculosus has invaded the southern parts of Japan; it was recorded on Okinawa Island in 1998, in Kagoshima Prefecture in 2006, and in Fukuoka Prefecture in 2010. In citrus groves in Shizuoka City, Central Japan in 2009–2012, the exotic ladybird was monitored by use of yellow sticky traps set inside citrus tree canopies. Adults of P. maculosus were captured in three out of the eight groves in 2010. This capture might be the first record of the ladybird from Honshu Island. Adults were trapped in three consecutive years, 2010–2012, in two groves; this suggests the possibility that the ladybird has become established in Shizuoka City. Adults were almost continuously caught on the traps from late April through October, being more abundant in early autumn (early September to early October), late spring (late April to mid-June), and mid-summer (early July to early August). During these periods, citrus shoots are growing and aphids are abundant. This finding suggests that the exotic ladybird might prey on citrus-infesting aphids, thereby reproducing in citrus groves. Based on the results obtained, potential impacts of the exotic ladybird on native aphidophagous ladybirds are also discussed.

Expansion of the antimicrobial peptide repertoire in the invasive ladybirdHarmonia axyridis

The harlequin ladybird beetle Harmonia axyridis has emerged as a model species in invasion biology because of its strong resistance against pathogens and remarkable capacity to outcompete native ladybirds. The invasive success of the species may reflect its well-adapted immune system, a hypothesis we tested by analysing the transcriptome and characterizing the immune gene repertoire of untreated beetles and those challenged with bacteria and fungi. We found that most H. axyridis immunity-related genes were similar in diversity to their counterparts in the reference beetle Tribolium castaneum, but there was an unprecedented expansion among genes encoding antimicrobial peptides and proteins (AMPs). We identified more than 50 putative AMPs belonging to seven different gene families, and many of the corresponding genes were shown by quantitative real-time RT–PCR to be induced in the immune-stimulated beetles. AMPs with the highest induction ratio in the challenged beetles were shown to demonstrate broad and potent activity against Gram-negative bacteria and entomopathogenic fungi. The invasive success of H. axyridis can therefore be attributed at least in part to the greater efficiency of its immune system, particularly the expansion of AMP gene families and their induction in response to pathogens.

Releases of a natural flightless strain of the ladybird beetle Adalia bipunctata reduce aphid-born honeydew beneath urban lime trees

Aphids can cause major environmental problems in urban areas. One important problem is the annual outbreaks of lime aphid, Eucallipterus tiliae (L.) (Hemiptera: Aphididae), which spoil the surroundings of lime trees by depositing honeydew. To date no environmentally friendly method has been demonstrated to yield effective control of lime aphids. Attempts are made in some cities to control lime aphids by releasing larvae of the native two-spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae). However, it is known that adult ladybird beetles disperse soon after release, and there is little indication they provide control of the aphids. Here, we demonstrate experimentally that releases of a flightless strain of A. bipunctata, obtained from natural variation in wing length, can reduce the impact of honeydew from lime aphid outbreaks on two species of lime in an urban environment. Both larvae and adult beetles were released, and we discuss the contribution of the flightless adults to the decline in honeydew.

Alien vs. predator: Could biotic resistance by native generalist predators slow lady beetle invasions?

Interactions with native species often influence whether exotic species will become invasive. The lady beetles Coccinella septempunctata and Harmonia axyridis are broadly successful invaders, but they have failed to fully establish in some parts of western North America. One possibility is that the locally-abundant, generalist predatory bugs Nabis alternatus and Geocoris bullatus resist invasion by acting as intraguild predators. We investigated the relative likelihoods of (1) the invasive lady beetles falling prey to the native generalist bugs compared to two native lady beetles, Hippodamia convergens and Coccinella transversoguttata, and (2) the relative likelihood of these exotic vs. native lady beetles committing reciprocal intraguild predation and consuming the two native predatory bugs. A series of predation trials demonstrated that C. septempunctata exhibited similar susceptibility to predation by Nabis and Geocoris, and a similar likelihood to commit reciprocal intraguild predation on the two bugs, relative to its native congener C. transversoguttata. In contrast, among all species tested, the exotic species H. axyridis was the least susceptible to intraguild predation by the bugs and was the most likely to consume Nabis and Geocoris. Altogether, these results suggest that native predatory bugs would have similar effects on the native and exotic Coccinella species, conferring no particular harm or advantage to C. septempunctata during its invasion. However, H. axyridis enjoyed advantages over the native bugs by being a rare victim but common perpetrator of intraguild predation; all else being equal, this would tend to favor replacement of native species by H. axyridis.

Invasive alien predator causes rapid declines of native European ladybirds

AbstractAim Invasive alien species (IAS) are recognized as major drivers of biodiversity loss, but few causal relationships between IAS and species declines have been documented. In this study, we compare the distribution (Belgium and Britain) and abundance (Belgium, Britain and Switzerland) of formerly common and widespread native ladybirds before and after the arrival of Harmonia axyridis, a globally rapidly expanding IAS.Location EuropeMethods We used generalized linear mixed‐effects models (GLMMs) to assess the distribution trends of eight conspicuous and historically widespread and common species of ladybird within Belgium and Britain before and after the arrival of H. axyridis. The distribution data were collated largely through public participatory surveys but verified by a recognized expert. We also used GLMMs to model trends in the abundance of ladybirds using data collated through systematic surveys of deciduous trees in Belgium, Britain and Switzerland.Results Five (Belgium) and seven (Britain) of eight species studied show substantial declines attributable to the arrival of H. axyridis. Indeed, the two‐spot ladybird, Adalia bipunctata, declined by 30% (Belgium) and 44% (Britain) over 5 years after the arrival of H. axyridis. Trends in ladybird abundance revealed similar patterns of declines across three countries.Main conclusion Together, these analyses show H. axyridis to be displacing native ladybirds with high niche overlap, probably through predation and competition. This finding provides strong evidence of a causal link between the arrival of an IAS and decline in native biodiversity. Rapid biotic homogenization at the continental scale could impact on the resilience of ecosystems and severely diminish the services they deliver.

Dominance of the multicoloured Asian lady beetle Harmonia axyridis in an undisturbed wild meadow ecosystem

Fifteen years after its arrival in Quebec (Canada), the multicoloured Asian lady beetle Harmonia axyridis (Pallas 1773) (Coleoptera: Coccinellidae) has become one of the dominant coccinellid species in agricultural, forested and urban areas. Several studies conducted in North American agricultural ecosystems show that the arrival of H. axyridis and other exotic coccinellid species was followed by decreases in the populations of native coccinellid species. In this study, the abundances of H. axyridis and other native and exotic species were determined in an undisturbed wild meadow located in a protected area. In 2009 and 2010, mainly Solidago canadensis L. (Asteraceae) and Asclepias syriaca L. (Asclepiadaceae) infested with aphids were surveyed. A total of 1522 individuals, belonging to seven different species, were recorded. In 2009, on all the plants monitored, H. axyridis was clearly the dominant species (69% of the coccinellid assemblage). In addition, this exotic species constituted 84% of the coccinellid assemblage, including Propylea quatuordecimpunctata (L.) and Coccinella septempunctata (L). It is likely the dominance of the eurytopic Asian lady beetle in agricultural, forested, urban and undisturbed open ecosystems, poses a threat to native lady beetles. These results also provide evidence that undisturbed wild meadow ecosystems will not constitute a natural refuge from Harmonia axyridis for native species of lady beetles.

Biotic interactions betweenEriopis connexaandHippodamia variegata, a native and an exotic coccinellid species associated with alfalfa fields in Chile

AbstractHuman‐assisted introductions, including those in the context of biological control, are considered to be one of the most important factors of global environmental change. However, the mechanisms underlying environmental changes, such as a decrease in the relative abundance of native species, are poorly understood. Since the introduction of the ladybird beetle,Hippodamia variegata(Goeze) (Coleoptera: Coccinellidae), in Chile in the 1970s for biological control of aphids, a reduction in the relative abundance of the native ladybird beetleEriopis connexa(Germar) has been noticed. To explore the role of cannibalism, intraguild predation (IGP) or competition as possible mechanisms that might increase dominance ofH. variegataoverE. connexa, several laboratory experiments were carried out. The native and the exotic species were very similar in their voracity and biotic interactions. AlthoughH. variegatawas able to maintain constant reproductive performance,E. connexareproduction decreased at lower densities of aphids,Acyrthosiphon pisum(Harris) (Hemiptera: Aphididae). The impacts of cannibalism, IGP, and competition exerted by these species were very symmetrical in both larvae and adults. We conclude that these biotic factors may not fully explain the increase in relative abundance ofH. variegata.The higher sensitivity ofE. connexato prey patch size, along with other factors such as chemical‐mediated negative interspecific interactions may be operating in alfalfa fields, changing the composition of associated coccinellid assemblages.

Winter survival of Harmonia axyridis in The Netherlands

Since the establishment of Harmonia axyridis in Europe, populations of native ladybirds have decreased. Overwintering survival is one of the aspects of the biology of H. axyridis that may contribute to its firm establishment in and invasion of a new area. In this study winter survival of five wild H. axyridis populations was assessed under natural and semi-natural conditions, with a focus on the potential influence of location and orientation on winter survival. Overwintering survival of H. axyridis in the Netherlands is high: 70.8–88.2%. When overwintering at one central site, populations sampled at five locations showed statistically significant different mortality rates. Furthermore, winter survival of H. axyridis at the sample sites was higher when beetles were hibernating at the southwestern sides of buildings, where most aggregations of ladybirds were found. Survival was higher at sheltered sites compared to exposed sites. Harmonia axyridis has a comparable or higher overwintering survival than most common native ladybird species. A high overwintering survival results in a large post-hibernation population in spring, leading to a rapid population build-up. Thus, the high winter survival probably contributes to the success of the exotic H. axyridis.

Harmonine, a defence compound from the harlequin ladybird, inhibits mycobacterial growth and demonstrates multi-stage antimalarial activity

The harlequin ladybird beetle Harmonia axyridis has been introduced in many countries as a biological control agent, but has become an invasive species threatening the biodiversity of native ladybirds. Its invasive success has been attributed to its vigorous resistance against diverse pathogens. This study demonstrates that harmonine ((17R,9Z)-1,17-diaminooctadec-9-ene), which is present in H. axyridis haemolymph, displays broad-spectrum antimicrobial activity that includes human pathogens. Antibacterial activity is most pronounced against fast-growing mycobacteria and Mycobacterium tuberculosis, and the growth of both chloroquine-sensitive and -resistant Plasmodium falciparum strains is inhibited. Harmonine displays gametocytocidal activity, and inhibits the exflagellation of microgametocytes and zygote formation. In an Anopheles stephensi mosquito feeding model, harmonine displays transmission-blocking activity.

Intraguild Predation and Native Lady Beetle Decline

Coccinellid communities across North America have experienced significant changes in recent decades, with declines in several native species reported. One potential mechanism for these declines is interference competition via intraguild predation; specifically, increased predation of native coccinellid eggs and larvae following the introduction of exotic coccinellids. Our previous studies have shown that agricultural fields in Michigan support a higher diversity and abundance of exotic coccinellids than similar fields in Iowa, and that the landscape surrounding agricultural fields across the north central U.S. influences the abundance and activity of coccinellid species. The goal of this study was to quantify the amount of egg predation experienced by a native coccinellid within Michigan and Iowa soybean fields and explore the influence of local and large-scale landscape structure. Using the native lady beetle Coleomegilla maculata as a model, we found that sentinel egg masses were subject to intense predation within both Michigan and Iowa soybean fields, with 60.7% of egg masses attacked and 43.0% of available eggs consumed within 48 h. In Michigan, the exotic coccinellids Coccinella septempunctata and Harmonia axyridis were the most abundant predators found in soybean fields whereas in Iowa, native species including C. maculata, Hippodamia parenthesis and the soft-winged flower beetle Collops nigriceps dominated the predator community. Predator abundance was greater in soybean fields within diverse landscapes, yet variation in predator numbers did not influence the intensity of egg predation observed. In contrast, the strongest predictor of native coccinellid egg predation was the composition of edge habitats bordering specific fields. Field sites surrounded by semi-natural habitats including forests, restored prairies, old fields, and pasturelands experienced greater egg predation than fields surrounded by other croplands. This study shows that intraguild predation by both native and exotic predators may contribute to native coccinellid decline, and that landscape structure interacts with local predator communities to shape the specific outcomes of predator-predator interactions.

Mode of overwintering of invasive Harmonia axyridis in the Netherlands

After establishment of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Europe, population densities of native ladybird species have decreased. The post-hibernation onset of female reproduction, a key characteristic influencing population dynamics and competition with related species, was studied. Hibernating individuals were collected and transferred to outdoor cages to continue overwintering. Every two weeks a sample of individuals was transferred to long-day, warm conditions. Intensity of dormancy was studied by determining the pre-oviposition period and ovarian development. Pre-oviposition periods were short throughout our observations, indicating that Harmonia axyridis was not in diapause but in a quiescent state. H. axyridis becomes active rapidly when temperature rises in spring but is not active earlier in the year than native species. Neither the mode of overwintering, nor the onset of spring activity can explain the invasion success of H. axyridis.

Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England

1. Harmonia axyridis (Coleoptera: Coccinellidae) is an invasive non-native ladybird in Europe, where it was introduced as a biological control agent of aphids and coccids. 2. This study assesses changes to ladybird species assemblages, in arboreal habitats, over a 3-year period encompassing the invasion phase of H. axyridis in eastern England. The effects of H. axyridis and other factors (weather and prey availability) on native ladybirds are assessed. 3. Harmonia axyridis increased from 0.1% to 40% of total ladybirds sampled, whilst native aphidophagous species declined from 84% to 41% of total ladybirds. The actual number of native aphidophagous ladybirds per survey decreased from a mean of 19.7 in year 1, to 10.2 in year 3. 4. Three ladybird species in particular experienced declines: Adalia bipunctata, Coccinella septempunctata, and Propylea quattuordecimpunctata. Harmonia axyridis was the most abundant species by the end of the study. 5. The decline in native aphidophagous ladybirds could be attributed to competition for prey and intraguild predation of eggs, larvae, and pupae by H. axyridis. Physiological and behavioural traits of H. axyridis are likely to confer an advantage over native ladybird species.

Predation of ladybird beetles by the orb-web spider Araneus diadematus

Ladybirds face a diversity of potential predators from which their main protection is powerful alkaloid-based chemical defence. In the laboratory, adults of the European orb-web spider Araneus diadematus Clerck readily consumed the native European ladybird Coccinella septempunctata L. and non-melanics and melanics of the exotic Harmonia axyridis (Pallas). The spider was little deterred by their defensive chemistry and apparently suffered no ill effects after eating ladybirds. This is particularly notable for H. axyridis, which possesses a novel alkaloid not known from European ladybirds and to which European predators are not expected to be adapted. Examination of inhabited A. diadematus webs and experimental determination of for how long captured ladybirds remained in webs indicated that ≤2% of spiders consume a ladybird each day. Ladybirds and A. diadematus are probably complementary rather than antagonistic in controlling crop pests, with ladybirds being at greatest risk from A. diadematus predation in autumn, during migration to overwintering sites.

Alfalfa fields promote high reproductive rate of an invasive predatory lady beetle

Invasive insect species often may attain high fecundity in agricultural habitats, thereby contributing to their establishment in new geographic regions and their displacement of similar native species. Such may be true for predatory lady beetles (Coleoptera: Coccinellidae) that have been introduced to North America in recent decades, raising concerns of adverse impact on native lady beetles. In northern Utah, Coccinella septempunctata L. first appeared in 1991, and is now predominant among lady beetles especially in alfalfa fields. We assessed the suitability of alfalfa fields as breeding habitat for females of C. septempunctata and the native, similarly sized Coccinella transversoguttata richardsoni Brown. The timing and amount of egg production differed significantly between C. septempunctata and C. transversoguttata as populations of aphids increased through spring and early summer. Reproduction by both species conformed to the egg window hypothesis, with populations of the predators producing most eggs before aphid numbers peaked. But consistently among fields and years, females of C. septempunctata produced more eggs, and did so earlier in the spring, than C. transversoguttata females even at low prey density. Furthermore, C. septempunctata females were more successful than females of C. transversoguttata in approaching their maximum body weights and reproductive output as measured in the laboratory under ideal conditions. The strong reproductive success of C. septempunctata may contribute to its displacement of C. transversoguttata in irrigated alfalfa in the generally arid Intermountain West of North America and to its establishment as an abundant species in this region of North America.

Hidden costs to an invasive intraguild predator from chemically defended native prey

Studies of invasive species tend to concentrate on the reasons for their success, rather than on the potential costs that they face. Invasive predators are potentially vulnerable to chemical defences of native prey that they have not previously encountered, and evolved to tolerate, within their natural range. While novel chemical defences have been cited as a factor facilitating invasion by exotic prey, the potential costs of chemical novelty to invasive predators have been ignored or remained hidden. We here consider one such example. Although a dominant intraguild predator in interactions with native ladybird beetles, the invasive ladybird Harmonia axyridis finds the defensive alkaloids of certain native ladybirds either distasteful or toxic, although laboratory and field evidence suggests it readily attacks these prey; these natives appear to possess novel alkaloids not previously encountered by H. axyridis. This effect has hitherto remained hidden, due to the methodological approaches used in earlier studies.

Reproductive Responses of Invasive and Native Predatory Lady Beetles (Coleoptera: Coccinellidae) to Varying Prey Availability

As adults, many predatory insects must adjust to a constantly changing prey environment while balancing between survival and reproduction. Two laboratory experiments were conducted to compare reproductive responses of females of two species of lady beetles, invasive Coccinella septempunctata L. and native C. transversoguttata richardsoni (Brown), in Utah alfalfa fields to varying availability of prey. When both lady beetles were placed immediately on experimental diets after being collected from the field (first experiment) and when they were provided excess prey for 14 d before being placed on experimental diets (second experiment), C. septempunctata produced more but individually smaller eggs than C. transversoguttata. Overall, however, in both experiments, C. septempunctata and C. transversoguttata responded similarly when they consumed pea aphids in varying amounts, by laying fewer and less viable eggs when fewer prey were consumed. In particular, the experiments provided no evidence that C. septempunctata converts pea aphids into eggs at a relatively higher rate than C. transversoguttata under limited prey availability. However, C. septempunctata had greater ability than C. transversoguttata to maintain body weight, even as they were producing eggs at low rates. This suggests that low aphid availability is less stressful for C. septempunctata, perhaps because it has more physiological ability than C. transversoguttata to assimilate pea aphid nutrients at low aphid availability. Such ability might contribute to the numerical dominance of the introduced C. septempunctata in alfalfa fields, which have supported low numbers of aphids in recent years.

Abundance of Native and Non-Native Lady Beetles (Coleoptera: Coccinellidae) in Different Habitats in Maine

Abstract Several studies suggest the possibility that non-native lady beetles may have replaced native lady beetles in some agricultural habitats. There is relatively little information, however, about lady beetle species composition outside of agricultural habitats. Evans (2004) suggested that native species have retreated to nonagricultural habitats in response to the arrival of non-native lady beetles (habitat compression hypothesis). To test this hypothesis, a survey of lady beetles was conducted in 2004 and 2005 in different habitats in Maine. From May to October, lady beetles were sampled in a variety of agricultural and nonagricultural habitats. In total, 3,487 and 2,903 lady beetles were collected in 2004 and 2005, respectively. Non-native lady beetles were found in a variety of habitats, including the habitats that would have likely served as a refuge for native species if the habitat compression hypothesis applied to the surveyed areas. Native species were found in a higher proportion in agricultural habitats compared with nonagricultural habitats and in very low numbers in all of the habitats surveyed. Hippodamia tredecimpunctata tibialis (Say) and Coccinella transversoguttata Brown, the two native species that were once dominant here, made up only 1.09 and 0.07% of the total lady beetles collected, respectively. In this survey, we failed to detect evidence that native lady beetles have retreated to nonagricultural habitats in response to the arrival of non-native lady beetles.

Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium

Harmonia axyridis Pallas (Coleoptera: Coccinellidae) is native to Asia, and was widely introduced as a biocontrol agent of aphids and coccids in Europe and North America. In Europe, H. axyridis is considered to be an invasive alien species because of its potential to disrupt native ladybird communities. Since 1999, the Belgian Ladybird Working Group mapped all Belgian Coccinellidae and recorded data on substratum plants and habitat. The first feral H. axyridis population in Belgium was recorded in 2001, but the expansion rate is decreasing because it now colonised the whole country. Recorded occupancy in Belgium showed an average rate of increase of 189% between 2002 and 2006. In Belgium, H. axyridis occurred in a wide range of habitats, including those of high conservation value. However, habitat and land cover analysis showed that H. axyridis is more frequently found in urbanised landscapes than in semi-natural landscapes. A niche overlap analysis based on plant use data showed that the potential to affect native species is higher for generalist, deciduous and coniferous tree ladybird species than for heathland and wetland specialist species. Phenology data showed that H. axyridis is able to reproduce later in the year than native species. Based on recorded distribution, ecology and phenology, we discuss the potential of H. axyridis to disrupt native ladybird assemblages in Belgium.