Long term changes in the communities of native ladybirds in Northern Italy: impact of the invasive species <Emphasis Type="Italic">Harmonia axyridis</Emphasis> (Pallas)

Since the mid-2000s, the exotic coccinellid species Harmonia axyridis (Pallas) has established itself in Northern Italy, raising serious concerns about possible repercussions on native ladybirds. In this study we compared the ladybird assemblages in 2015–2016 with those sampled in 1995–1996, before the arrival of H. axyridis. Surveys were carried out in the same sites and with the same methods for both periods. Aphidophagous ladybirds were sampled in hedgerows and herbaceous habitats at field margins by mechanical knockdown and sweeping net, respectively. The changes in the structure of ladybird communities after the arrival of H. axyridis were significantly different between arboreal and herbaceous habitats. Harmonia axyridis is currently the dominant species in shrubs and trees, and all the native ladybird species taken together account for only approximately one third of the total individuals sampled in 2015–2016. On the other hand, the relative abundance of the exotic species in herbaceous habitats was low, and it has had a negligible relevance on the structure of ladybird communities on grasslands. Among native species, Adalia bipunctata (L.), whose ecological niche largely overlaps with that of H. axyridis, suffered the largest decline between 1995–1996 and 2015–2016. The co-occurrence of H. axyridis invasion and the regression of A. bipunctata suggest a direct impact of the exotic species, because no other major modifications occurred in the studied areas between sampling periods.     

New data on the changes in the abundance and distribution of several species of beetles (Coleoptera) in European Russia and the Caucasus

Changes in the abundance and distribution of selected species of beetles in European Russia and in the Caucasus are reported. Most of these species have been recorded from the Northwestern Caucasus in the last 10–15 years. The abundance and distribution during the last two years have changed most sharply in the introduced species, the Harlequin lady beetle Harmonia axyridis and two East Asian bruchids, Megabruchidius dorsalis and M. tonkineus. In 2016, the latter has been found in Georgia for the first time, and Harmonia axyridis was found in St. Petersburg. Abundance of the weevil Alcidodes karelinii with the range situated mostly east of the Caucasus and Volga River remains in Northwestern Caucasus at about the previous level. The flea-weevil species, a leaf miner on Ulmus pumila, misidentified previously as Orchestes mutabilis, is described in this paper as Orchestes steppensis sp. n. based on the material from Russia, Kazakhstan, Mongolia and Northern China; no its further distribution westward in 2015–2016 has been found. This species, rapidly widening its range in North America in the recent decade, is misidentified there as Orchestes alni. A key for differentiation of Orchestes alni, O. mutabilis and O. steppensis sp. n. is provided with photographs of adults of all three species. Magdalis armigera has increased abundance in Northwestern Caucasus in 2016 and was for the first time found in Northwestern Russia (Pskov Province) in 2015. Regular faunistic surveys during several decades provide a possibility of recording considerable changes in the abundance of some common species of Coleoptera, often associated with changes in their distribution.     

<Emphasis Type="Italic">Harmonia axyridis</Emphasis> failed to establish in the Azores: the role of species richness,intraguild interactions and resource availability

To understand the role of native ladybird biodiversity in habitat susceptibility on the establishment and spread of Harmonia axyridis Pallas (Coleoptera: Coccinellidae), we characterized and compared European communities where they had established and where they had not established. The local communities of ladybirds were characterized in terms of biodiversity, the average difference in body mass between H. axyridis and other coccinellid species and the rarefied total body mass of all individuals (as a surrogate for aphid abundance and availability). The lack of success of H. axyridis in the Azores, as well as its low success in Southern Europe, can be explained by a combination of resource availability and intraguild competition. We suggest the success of this invasive alien species to establish in a habitat depends first on resource availability and second when most direct competitors for limited resources are absent or are uncommon.     

Chemical defences of native European coccinellid eggs against intraguild predation by the invasive Asian coccinellid, <Emphasis Type="Italic">Harmonia axyridis</Emphasis> (Pallas)

Harmonia axyridis (Pallas) is a coccinellid of Asian origin that has recently invaded substantial parts of Europe and is suspected to affect native coccinellid populations through intraguild predation and competition for food. Previous work has shown that two species from the Calvia genus appeared to be well protected against H. axyridis predation. To deepen our understanding on chemical protection of Calvia spp. and the predation risk by H. axyridis, we tested for susceptibility and palatability of Calvia spp. and H. axyridis eggs against predation by H. axyridis neonate larvae. Results show that eggs of C. quatuordecimguttata were mostly not eaten by H. axyridis, while eggs of the congeneric C. decemguttata were found to be largely unprotected against predation by the invasive coccinellid. We also observed that H. axyridis first instars successfully cannibalized on conspecific eggs. Removing the surface chemicals from C. quatuordecimguttata eggs resulted in significantly reduced protection from being preyed upon by H. axyridis, while applying these extracts onto C. decemguttata and H. axyridis eggs resulted in increased protection against H. axyridis larvae. The importance of surface chemicals in the interactions between H. axyridis and native coccinellids was confirmed by GC–MS analysis, showing a high diversity of hydrocarbons located on the surface of C. quatuordecimguttata eggs, i.e. more than twice as many when compared to C. decemguttata. Survival of H. axyridis larvae feeding on eggs of C. quatuordecimguttata, C. decemguttata or conspecific eggs, from which surface chemicals were removed by washing them with hexane, was not different from survival on unwashed eggs.     

Determining the effects of life stage,shared prey density and host plant on intraguild predation of a native lacewing (<Emphasis Type="Italic">Chrysoperla carnea</Emphasis>) by an invasive coccinellid (<Emphasis Type="Italic">Harmonia axyridis</Emphasis>)

Negative impacts of non-native Harmonia axyridis (Pallas) on members of the native aphid enemy guild have been widely hypothesised but mainly only assessed with other coccinellid species, and mostly in small experimental arenas. Here we investigated the interactions between H. axyridis and Chrysoperla carnea Stephens larvae. In small-scale (Petri dish) arenas 2nd-instar C. carnea were at risk of predation from larval (2nd and 4th-instar) and adult (male and female) H. axyridis while 3rd-instar C. carnea were only at minimal risk from 4th-instar and adult female H. axyridis. Plant species, aphid species and aphid density did not affect intraguild predation of 2nd-instar C. carnea by 4th-instar and adult H. axyridis in mesocosm experiments. Chrysoperla carnea consumed similar numbers of Megoura viciae Buckton, Aphis fabae Scop. and Acyrthosiphon pisum Harris aphids while H. axyridis consumed fewer M. viciae than the other two species. The greatest suppression of A. pisum was achieved in treatments with both C. carnea and H. axyridis. Life stage and the sex of H. axyridis as well as the life stage of C. carnea are important variables affecting intraguild predation and these attributes should be considered when assessing the potential threat of other potentially invasive alien predators.     

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.     

Reaping benefits from an invasive species: role of <Emphasis Type="Italic">Harmonia axyridis</Emphasis> in natural biological control of <Emphasis Type="Italic">Aphis glycines</Emphasis> in North America

Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is an invasive species present in numerous agroecosystems in North America. Despite adverse impacts as a threat to native biodiversity, a nuisance household invader and a pest in fruit production, H. axyridis also plays a beneficial role as a major component of assemblages of generalist predators in several agricultural crops. Here, we review the role of H. axyridis as a natural enemy of Aphis glycines Matsumura (Hemiptera: Aphididae), an invasive pest of soybean, Glycine max (L.) Merrill (Fabales: Fabaceae), in North America. Harmonia axyridis is often the most abundant predator species attacking A. glycines in soybean agroecosystems. This predator has the potential to both prevent and suppress A. glycines outbreaks. Further studies are needed to fully understand and utilize the potential of H. axyridis as a natural enemy in the management of A. glycines and other agricultural pests in agroecosystems worldwide.     

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.     

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.     

Functional convergence and phenotypic divergence in two specialist species of pine-associated ladybirds

Traditionally, convergent evolution has been considered to produce phenotypic similarity in independently evolved species. By contrast, recent studies have detected morphological divergence between species even in similar selective environments when different morphological traits combine to produce a specific functional output. However, it is still unclear whether a complex combination of non-morphological phenotypic traits, such as behavioural and life-history traits, can produce a similar performance in different species. In this study, I examined prey capture performance and related phenotypes in two sympatric ladybird species, Sospita oblongoguttata and Harmonia yedoensis, which specialize on the giant pine aphid, which is known to be elusive for ladybird hatchlings. In particular, I focused on egg size and proportion of trophic eggs in the clutch, since the amount of maternal investment per offspring can contribute to prey capture performance of ladybird hatchlings. Predation success of hatchlings against the giant pine aphid was higher in both S. oblongoguttata and H. yedoensis than in Harmonia axyridis, a generalist ladybird species that feeds on various kinds of aphid species in nature. Sospita oblongoguttata females, however, produced relatively larger eggs and in most clutches provided no trophic eggs, whereas H. yedoensis females produced smaller eggs and provided more trophic eggs per clutch. Moreover, hatchling morphology in H. yedoensis more closely resembled that of its congener, H. axyridis, than that of the more distantly related S. oblongoguttata, although like H. yedoensis, S. oblongoguttata predates on the elusive pine aphid. These results in two pine-associated specialist ladybirds indicate that divergent phenotypes can nonetheless have similar prey capture performance. In conclusion, this work demonstrates that the general ultimate function can be achieved by various mechanisms through convergence that operates at different level of life.     

Predators and parasitoids of the harlequin ladybird, <Emphasis Type="Italic">Harmonia axyridis</Emphasis>, in its native range and invaded areas

The harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) has rapidly spread in several continents over the past 30 years and is considered an invasive alien species. The success of H. axyridis as an invader is often attributed to weak control by natural enemies. In this paper, we provide an overview of current knowledge on predators and parasitoids of H. axyridis. The common feature of predators and parasitoids is that they directly kill exploited organisms. Currently available data show that H. axyridis, displaying a variety of chemical, mechanical, and microbiological anti-predator defenses, is usually avoided by predators. However, some birds and invertebrates can eat this ladybird without harmful consequences. The primary defenses of H. axyridis against parasitoids include immune response and physiological and nutritional unsuitability for parasitoid development. These defenses are probably relatively efficient against most ladybird parasitoids, but not against flies of the genus Phalacrotophora. The latter are idiobiont parasitoids and hence can evade the host’s immune response. Indeed, rates of parasitism of H. axyridis by Phalacrotophora in the Palaearctic region (both in the native range in Asia and in Europe) are relatively high. While strong evidence for enemy release on the invasive populations of H. axyridis is lacking, several cases of parasitoid acquisition have been recorded in Europe, North America, and South America. We conclude that enemy release cannot be excluded as a possible mechanism contributing to the spread and increase of H. axyridis in the early stages of invasion, but adaptation of parasitoids may lead to novel associations which might offset previous effects of enemy release. However, further work is required to elucidate the population-level effects of such interactions.     

The contribution of a beneficial insectary plant <Emphasis Type="Italic">Scaevola aemula</Emphasis> to survival and long-term establishment of flightless <Emphasis Type="Italic">Harmonia axyridis</Emphasis> in greenhouses

The fairy fan flower, Scaevola aemula R. Br., is a primary candidate insectary plant for maintaining populations of generalist predators. We conducted release experiments in greenhouses of cultivated eggplants to evaluate the effects of intercropping S. aemula on the establishment of flightless Harmonia axyridis Pallas. Compared with a monoculture of eggplant, all release experiments showed that flightless H. axyridis remained in greater numbers in plots with S. aemula planted alongside eggplant. In the release experiment of flightless H. axyridis larvae, the incidence of aphids in the plot with transplanted S. aemula was suppressed compared with that in the release plot without transplanted S. aemula. In a laboratory experiment, the longevity of flightless H. axyridis adults on blossom stems of S. aemula was greater than when open flowers and buds were removed, suggesting that the insects fed on floral resources such as the pollen of S. aemula. Our findings showed that the floral resources of S. aemula can enhance aphid suppression by improving the establishment of flightless H. axyridis.     

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.     

Potential for exploitative competition,not intraguild predation,between invasive harlequin ladybirds and flowerbugs in urban parks

In aphidophagous insect communities invaded by the harlequin ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), intraguild predation (IGP) is widely implicated in the displacement of native predators, however, indirect trophic interactions are rarely assessed. Using molecular gut-content analysis, we investigated the relative frequencies of IGP by H. axyridis on the predatory flowerbug Anthocoris nemoralis Fabricius (Heteroptera: Anthocoridae) and prey overlap for a shared prey, the lime aphid Eucallipterus tiliae L. (Hemiptera: Aphididae), in Tilia × europaea crowns in urban parks. The frequency of IGP by H. axyridis was low: 2.7 % of larvae and 3.4 % of adults tested positive for A. nemoralis DNA. The presence of lime aphid DNA in predators was higher: 56.5 and 47.9 % of H. axyridis larvae and adults, respectively, contained E. tiliae DNA, whereas 60.8 % of adult A. nemoralis tested positive for aphid DNA. Incorporating insect densities revealed that the density of H. axyridis larvae had a strong negative effect on the likelihood of detecting aphid DNA in A. nemoralis. Prey overlap for E. tiliae was widespread in space (2–13 m height in tree crowns) and time (May–October 2011) which suggests that interspecific exploitative competition, mediated by predator life-stage, more so than IGP, is an important indirect trophic interaction between co-occurring H. axyridis and A. nemoralis. Whether exploitative competition equates to displacement of A. nemoralis populations requires further investigation. Our results emphasize the need to incorporate indirect interactions in studies of insect communities following invasion, not least because they potentially affect more species than direct interactions alone.     

Intraguild predation between the invasive ladybird Harmonia axyridis and non-target European coccinellid species

The coccinellid Harmonia axyridis (Pallas) has been used for augmentative and classical biological control in many environments. More recently it has invaded large parts of Europe and negative effects for native populations of aphidophagous coccinellids are beginning to emerge. Here we investigate intraguild predation (IGP) between H. axyridis and eleven native non-target European coccinellids, including less common species which have not been studied so far within this context of non-target effects. When first-instars of H. axyridis were paired with the native species, only Anatis ocellata (Linnaeus) and Calvia quatuordecimguttata (L.) were significantly superior to the former whereas H. axyridis was superior in three cases, i.e. against Aphidecta obliterata (L.), Coccinella septempunctata L. and Hippodamia variegata (Goeze). Non-significant results were obtained for all other pairings. Similar tests with the fourth larval instar revealed stronger IGP rates and H. axyridis was found to be superior in the interactions with Adalia bipunctata (L.), Adalia decempunctata (L.), A. obliterata, Calvia decemguttata (L.), C. quatuordecimguttata, C. septempunctata, H. variegata, Oenopia conglobata (L.) and Propylea quatuordecimpunctata (L.) whereas non-significant results were obtained for interactions with two other native species. Another experiment revealed that H. axyridis was able to prey more successfully upon egg of most native coccinellid species than vice versa. However, C. quatuordecimguttata eggs seem to be more protected against predation than those of the other species. Survival of first-instar H. axyridis was higher on conspecific eggs compared to eggs of any other species tested. Our results suggest that H. axyridis may become a threat to a wide range of native aphidophagous coccinellids sharing similar ecological niches except species showing high potential for chemical or physical protection.     

Assessing the ecological risk posed by a recently established invasive alien predator: <Emphasis Type="Italic">Harmonia axyridis</Emphasis> as a case study

Invasive alien predators are a serious threat to biodiversity worldwide. However, there is no generic method for assessing which local species are most at risk following the invasion of a new predator. The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is an alien in Europe and many other parts of the world where it affects other species of ladybirds through competition for food and intra-guild predation (IGP). Here, we describe a method developed to assess which European ladybird species are most at risk following the invasion of H. axyridis. The three components of the risk assessment are: the likelihood that the assessed native species encounters H. axyridis in the field, the hazard of competition for food, and the IGP hazard. Thirty native European ladybird species were assessed through data obtained from field observations, laboratory experiments and literature reviews. The species that are considered most at risk are found on deciduous trees, have immature stages which are highly vulnerable to IGP by H. axyridis, and are primarily aphidophagous. These species should be the focus of specific studies and possibly conservation actions. The risk assessment method proposed here could be applied to other alien predators which are considered a threat to native species through competition and predation.     

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.     

The influence of density-dependent factors on larval development in native and invasive populations of <Emphasis Type="Italic">Harmonia axyridis</Emphasis> (Pall.) (Coleoptera,Coccinellidae)

Effects of the number of larvae per Petri dish (1, 5, and 10) on the preimaginal development of individuals of the native (Irkutsk, southern Siberia) and invasive (Sochi, the Northern Caucasus) populations of the multicolored Asian ladybird Harmonia axyridis were investigated in the laboratory. The experiments were conducted under short (12 h) and long (18 h) day conditions; the larvae were fed on the green peach aphid Myzus persicae or on the eggs of the grain moth Sitotroga cerealella. An increase in the number of larvae developed in one Petri dish resulted in a significant decrease in the rate of development in individuals from both populations which fed on aphids. Survival decreased with an increase in the number of larvae developed in one Petri dish fed on both prey species, but only in larvae from the invasive population of H. axyridis. The weight of emerging adults decreased with the number of larvae per dish in individuals from both study populations, but only when fed on aphids. These data suggest that the influence of density-dependent factors on the development of H. axyridis depends significantly on larval prey species. In addition, larvae from the invasive population have somewhat more aggressive interactions with competitors, this possibly having been one of the prerequisites for invasion.     

The Influence of Diet and Population Density on Maturation of Females from Native and Invasive Populations of the Multicolored Asian Ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis> (Pallas) (Coleoptera,Coccinellidae)

Population density can influence insect reproduction both directly and indirectly causing quantitative and qualitative changes in the feeding regime. We investigated the impact of diet and population density on reproductive maturation of females from native (Irkutsk) and invasive (Sochi) populations of the multicolored Asian ladybird Harmonia axyridis. During the study the beetles fed either on the green peach aphid, Myzus persicae, or on less suitable factitious food (eggs of the grain moth Sitotroga cerealella). Population density was determined by the number of females and males placed in a standard Petri dish. The experiments showed that feeding on the grain moth eggs (other conditions being equal) delayed maturation and increased the tendency to enter reproductive diapause in females from the native but not from the invasive population of H. axyridis. In addition, the preoviposition period increased with the number of females but decreased with the number of males in a dish, although these effects were observed only in individuals from the invasive population and their strength depended on the food of the beetles. Earlier we have demonstrated that the impact of the density-dependent factors on the larvae of the invasive population of H. axyridis was stronger than that on the larvae of the native population because the larvae of the invasive population have somewhat more aggressive interactions with competitors. In the present study, similar differences were revealed between females of these populations.     

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.