Diversity and abundance of coccinellids (Coleoptera: Coccinellidae) on trees in parks and tree rows of Belgrade

Harmonia axyridis is an invasive coccinellid species that was first recorded in Serbia in 2008. In order to establish whether after its arrival it became the dominant coccinellid species, we investigated the diversity and abundance of coccinelids on trees in parks and tree rows of Belgrade during 2015 and 2016. Thirteen coccinellid species were recorded in these investigations. Frequently occurring among them were Adalia bipunctata, A. decempunctata, Coccinella septempunctata, Exochomus quadripustulatus, Harmonia axyridis, H. quadripunctata, Oenopia conglobata, and Popylea quatuordecimpunctata. All of them had different dynamics of appearance during the vegetation. As a result of this, the values of their dominance in the coccinellid community constantly changed. However, only in the cases of H. axyridis, O. conglobata, and C. septempunctata were those values high enough for us to be able to say that they were dominant in terms of abundance during a certain period. Although the amounts of summer precipitation in Serbia were very different during 2015 and 2016, the trends of changes in the diversity of coccinellids throughout the growing season in these two years were similar.     

Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples

Intraguild predation (IGP) is a potential mechanism of negative effects on native species populations by invasive non‐native species such as Harmonia axyridis. Molecular techniques (polymerase chain reaction) were used to probe for the presence of various insect (coccinellid, syrphid and chrysopid) prey DNA in the guts of 177 H. axyridis larvae field‐collected in England, France, Germany, Slovakia and the Czech Republic in 2010. Three of the four target prey species were detected in the guts of H. axyridis at the following rates: Adalia decempunctata 9.6%, Adalia bipunctata 2.8% and Episyrphus balteatus 2.8%. IGP on Chrysoperla carnea was not detected. IGP detection of at least one target species was made in England, France, Slovakia and the Czech Republic, but not in Germany. These results strengthen the evidence that H. axyridis is a very generalist predator. Results are discussed in the context of their ecological significance.     

Biodiversity Loss following the Introduction of Exotic Competitors: Does Intraguild Predation Explain the Decline of Native Lady Beetles?

Exotic species are widely accepted as a leading cause of biodiversity decline. Lady beetles (Coccinellidae) provide an important model to study how competitor introductions impact native communities since several native coccinellids have experienced declines that coincide with the establishment and spread of exotic coccinellids. This study tested the central hypothesis that intraguild predation by exotic species has caused these declines. Using sentinel egg experiments, we quantified the extent of predation on previously-common (Hippodamia convergens) and common (Coleomegilla maculata) native coccinellid eggs versus exotic coccinellid (Harmonia axyridis) eggs in three habitats: semi-natural grassland, alfalfa, and soybean. Following the experiments quantifying egg predation, we used video surveillance to determine the composition of the predator community attacking the eggs. The extent of predation varied across habitats, and egg species. Native coccinellids often sustained greater egg predation than H. axyridis. We found no evidence that exotic coccinellids consumed coccinellid eggs in the field. Harvestmen and slugs were responsible for the greatest proportion of attacks. This research challenges the widely-accepted hypothesis that intraguild predation by exotic competitors explains the loss of native coccinellids. Although exotic coccinellids may not be a direct competitor, reduced egg predation could indirectly confer a competitive advantage to these species. A lower proportion of H. axyridis eggs removed by predators may have aided its expansion and population increase and could indirectly affect native species via exploitative or apparent competition. These results do not support the intraguild predation hypothesis for native coccinellid decline, but do bring to light the existence of complex interactions between coccinellids and the guild of generalist predators in coccinellid foraging habitats.     

Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain

1. Harmonia axyridis was first recorded in Britain in 2004. Two subsequent earlier records were received from 2003. 2. The UK Ladybird Survey, a citizen science initiative involving online recording, was launched in 2005 to encourage people across Britain to track the spread of H. axyridis. Tens of thousands of people have provided records of H. axyridis and other species of ladybirds, creating an invaluable dataset for large‐scale and long‐term research. Declines in the distribution of seven (of eight assessed) native species of ladybird have been demonstrated, and correlated with the arrival of H. axyridis, using the records collated through the UK Ladybird Survey. 3. Experimental research and field surveys have also contributed to our understanding of the ecology of H. axyridis and particularly the process of invasion. Harmonia axyridis arrived in Britain through dispersal and introduction events from regions in which it was deliberately released as a biological control agent. The rapid spread of this species has been attributed to its high natural dispersal capability by means of both flight and anthropogenic transport. A number of factors have contributed to the successful establishment and indeed dominance of this polymorphic species within aphidophagous guilds, including high reproductive capacity, intra‐guild predation, eurytopic nature, high resistance to natural enemies within the invaded range, and potentially phenotypic plasticity. 4. The global invasion by H. axyridis and subsequent research on this species has contributed to the general understanding of biological invasions.     

Invasion of the coccinellid community associated with a tropical annual agroecosystem

1. Detailed understanding of the mechanisms enabling or limiting the impacts of invasive generalist predators is needed. Harmonia axyridis is an invasive generalist coccinellid predator that may have destabilised coccinellid communities worldwide and is an excellent candidate for investigating invasion dynamics.
2. We evaluated four hypotheses: (1) Nine years after being detected in Central Brazil, Ha. axyridis has dominated the coccinellid community. This is facilitated by (2) its broader aphid prey range than the other aphidophagous coccinellids, (3) its superiority as an asymmetrical intraguild predator, and (4) the invasibility of the present coccinellid community.
3. We sampled the invertebrate communities associated with six organic vegetable farms in Brazil during 2017 and 2018, conducted a feeding trial to measure prey niche breadth and overlap, and estimated intra- and interspecific interaction strengths corresponding to first-order Lotka-Volterra parameters to evaluate the strength of intraguild predation and create a community matrix.
4. We found (1) Ha. axyridis comprised ≤8.3% of the coccinellid community. (2) Hi. convergens had the broadest prey niche and dominated the prey niche of Ha. axyridis. (3) We could not determine from the population data if Ha. axyridis was the dominant intraguild predator because its density was too low and constant. (4) The community matrix indicated that the present-day coccinellid community was stable.
5. We conclude Ha. axyridis has not become invasive in Central Brazil, in part because it does not have the broadest prey niche breadth and the present coccinellid community is stable to the present perturbation of Ha. axyridis.

     

Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid

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. Although not known to have been deliberately introduced to Great Britain, it was first recorded there in 2004, in south-east England. Harmonia axyridis arrived in Great Britain by various means, primarily from mainland Europe, but also from Canada. Extensive national and local media coverage, and a dedicated website (), facilitated public involvement in recording H. axyridis in Great Britain; in excess of 4,000 verified records of the species were received between 2004 and 2006. Through detailed mapping, the objective of our study was to quantify and analyse the spread of H. axyridis in its early stages of invasion in Great Britain. Our data shows that between 2004 and 2006, the species spread north through Great Britain at the rate of 58 km year^-1 and west at the rate of 144.5 km year^-1. In England H. axyridis spread north to Yorkshire and west to Cornwall by the end of 2006, and also reached Wales. Recorded occurrence (of one or more H. axyridis individuals at larval, pupal and/or adult stage) in 10 km squares in Great Britain was: 2004—51; 2005—149; 2006—447. Records of juvenile H. axyridis extend through most of the recorded British range of the species, and we present evidence of bi-voltinism in the population in 2006.     

Entomopathogenic fungi recorded from the harlequin ladybird, Harmonia axyridis

Entomopathogenic fungi were recorded from field samples of the harlequin ladybird Harmonia axyridis, an invasive coccinellid that has recently arrived in Denmark. Larvae, pupae and adults were found to be infected by Isaria farinosa, Beauveria bassiana and species of Lecanicillium. This is the first record of entomopathogenic fungi infecting larvae and pupae. Winter mortality due to fungal infection reached 17.9% in adults collected at one location. The larval stage was most susceptible to fungal infection, as confirmed through bioassay with I. farinosa.     

<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.     

The Harlequin ladybird continues to invade southeastern Europe

The ladybird Harmonia axyridis (Pallas) is considered one of the most serious invasive species around the globe. It has spread all over North America and Western Europe, while data from southeastern Europe, especially in the Mediterranean region, are scarce. In this study we present the first confirmed data of the spread of H. axyridis throughout Croatia. Specimens were sampled and identified during the period 2008–2010. The species was recorded at 18 localities in all three colour forms in various habitat types. Light trapping was found to be a satisfactory method for collecting H. axyridis. Since there is no evidence to suggest the deliberate introduction of H. axyridis in Croatia, it can be assumed that it has spread southwards from Central and Eastern Europe, and that it will probably continue to spread. Further investigations should focus on monitoring and detailed mapping of H. axyridis in Croatia and neighbouring countries, especially in the Mediterranean region, to determine whether stable populations are present.     

Ecological correlates of local extinction and colonisation in the British ladybird beetles (Coleoptera: Coccinellidae)

Five main drivers of population declines have been identified: climate change, habitat degradation, invasive alien species (IAS), overexploitation and pollution. Each of these drivers interacts with the others, and also with the intrinsic traits of individual species, to determine species’ distribution and range dynamics. We explored the relative importance of life-history and resource-use traits, climate, habitat, and the IAS Harmonia axyridis in driving local extinction and colonisation dynamics across 25 ladybird species (Coleoptera: Coccinellidae).Species were classified as continually present, continually absent, extinct, or colonising in each of 4,642 1-km² grid squares. The spatial distribution of local extinction and colonisation events (in the grid squares) across all species’ ranges were related to ecological traits, overlap with H. axyridis, climate, and habitat factors within generalised linear models (GLMs). GLMs were also used to relate species’ traits, range characteristics, and niche overlap with H. axyridis to extinction and colonisation rates summarised at the species level. Bayesian model averaging was used to account for model uncertainty, and produce reduced sets of models which were well-supported by data. Species with a high degree of niche overlap with H. axyridis suffered higher extinction rates in both analyses, while at the spatial scale extinctions were more likely and colonisations less likely in areas with a high proportion of urban land cover. In the spatial analysis, polymorphic species with large range sizes were more likely to colonise and less likely to go extinct, and sunny grid squares were more likely to be colonised. Large, multivoltine species and rainy grid squares were less likely to colonise or be colonised. In conclusion for ladybirds, extinction and colonisation dynamics are influenced by several factors. The only factor that both increased the local extinction likelihood and reduced colonisation likelihood was urban land cover, while ecological overlap with H. axyridis greatly increased extinction rates. Continued spread of H. axyridis is likely to adversely affect native species and urban areas may be particularly vulnerable.     

Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain

The establishment, spread and increase of the invasive coccinellid Harmonia axyridis Pallas in North America and Britain have coincided with declines in native ladybirds. In Britain, this pattern was predicted soon after H. axyridis was first recorded. However, predictions of the impact that H. axyridis may have on the parasites, parasitoids and pathogens of native coccinellids have been less certain, largely because of uncertainty over whether H. axyridis would become an alternate host for such agents. Dinocampus coccinellae (Schrank) is a braconid parasitoid of ladybirds of the sub-family Coccinellinae. In Japan, this wasp uses both Coccinella septempunctata brucki Mulsant and H. axyridis as hosts, but successfully parasitizes a higher proportion of the former species. Data are here presented that indicate the same is true in Britain, but to a greater extent. This study investigates the interactions of D. coccinellae with C. septempunctata L. and H. axyridis from Japan and Britain. We show that coccinellid activity affects encounter rates with the wasp, with H. axyridis being more active than C. septempunctata in the tests. Escalation rates from investigation to ovipositional attack were higher for C. septempunctata than H. axyridis for both Japanese and British wasps. Wasp emergence was higher, relative to ovipositional attack, from C. septempunctata than from H. axyridis. Wasps did not discriminate between Japanese and British ladybirds of the same species. British wasp eclosion rates were higher from Japanese than from British H. axyridis. We consider both the effect D. coccinellae may have on H. axyridis population demography, and the effect H. axyridis may have on D. coccinellae in Europe.     

Geographic variation of color polymorphism in two sibling ladybird species,Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae)

Geographical variation of elytra color pattern in two sibling ladybird species, Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae), was examined. The two species are distributed sympatrically in central Japan; however, only H. yedoensis and H. axyridis occur in the Ryukyu Islands (southern Japan) and Hokkaido island (northern Japan), respectively. The frequency of elytra color patterns was significantly different between the two species in all sympatric locations and our results were inconsistent with the classical theory on Müllerian mimicry. The most dominant pattern of H. axyridis was the least dominant of H. yedoensis in all sympatric populations. Furthermore, the frequency of the non‐melanic form (red ground color with or without black spots) increased towards the south in H. yedoensis. This tendency was in contrast to the known geographical cline in H. axyridis in which the melanic form (black ground color with red spots) was gradually displaced with the non‐melanic form northwards in the Japanese archipelago. We discuss possible selective factors including predator avoidance, thermal adaptation and reproductive character displacement, all of which might contribute to the maintenance of the color polymorphism in the two Harmonia species.     

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.     

Potential spatial interaction of the invasive species Harmonia axyridis (Pallas) with native and endemic coccinellids

Biological invasions represent a serious menace to local species assemblages, mainly due to interspecific relationships such as competition and predation. One important invasive species worldwide is Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), which has invaded many regions of the world, threatening the native and endemic coccinellid assemblages due to negative interspecific interactions. These interactions have been widely studied at a local scale, but have been less studied at regional scales. Our aim was to estimate and analyse the potential spatial interaction associated with the co‐occurrence of H. axyridis with native and endemic species in Chile, considering bioclimatic and land cover variables. First, we created species distribution models (SDM) for H. axyridis, native and endemic coccinellids and six representative coccinellid species using maximum entropy technique. Then, we overlapped each SDM with land cover types to estimate the bioclimatic suitability within each land cover type. Finally, we identified the co‐occurrences of organisms according to the SDM and the land cover types, estimating in what land covers H. axyridis and the other coccinellids are more likely to co‐occur. Our results show that the suitable area for H. axyridis occurs from 30° to 42°S in Chile, while for native and endemic species this area is greater. The six selected species are mainly concentrated in central Chile, but differ in their potential suitable areas; Adalia angulifera Mulsant and Scymnus bicolor (Germain) have the largest range, and Mimoscymnus macula (Germain) has the most restricted one. The highest level of potential spatial interactions with H. axyridis occurs in central Chile, specifically in croplands and scrublands, and the lowest in primary native forest for all the species. Our results provide a spatially explicit baseline for coccinellid conservation and management of this invasive species.     

Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis

Abstract Individuals can adapt to heterogeneity in their environment through either local adaptation or phenotypic plasticity. Colour forms of the ladybird Harmonia axyridis are a classic example of local adaptation, in which the frequency of melanic forms varies greatly between populations. In some populations, there are also large seasonal changes in allele frequency, with melanism being costly in summer and beneficial in winter. We report that the non‐melanic morph of H. axyridis dramatically increases its degree of melanization at cold temperatures. Furthermore, there is genetic variation in reaction norms, with different families responding to temperature in different ways. Variation at different spatial and temporal scales appears to have selected for either genetic or phenotypically plastic adaptations, which may be important in thermoregulation. As melanism is known to have a large effect on fitness in H. axyridis, this plasticity of melanization may have hastened its spread as an invasive species.     

Genetic estimations for body size characters,development period and development rate in a coccinelid beetle,Harmonia axyridis

Heritabilities and genetic correlations for body size characters and development period in a coccinellid beetle,Harmonia axyridis were estimated by a sib-analysis experiment. Positive genetic correlations were detected between size characters and development rate. If this is upheld in the field, genetic variation would be eliminated, as the loci affecting the characters are supposed to be fixed. However, the results indicated moderate heritabilities for all characters. Possible explanations for the results are discussed.     

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.     

Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis

The effects of the invasion ofan exotic predator, Harmonia axyridis(Pallas) (Coleoptera: Coccinellidae), wereinvestigated using three experiments on theecology of aphid predators on apple. Oneexperiment, 1992, was collected prior to theH. axyridis invasion, and two others,1996 to 1997 and 1999 to 2000, were collectedafter the invasion. Except for one year, 1999,H. axyridis was the dominant coccinellid,replacing the formerly dominant Coccinellaseptempunctata L. (Coleoptera: Coccinellidae),another exotic species. The dominance of H. axyridis was greater among larvae thanamong adults. There was no apparent effect ofthe H. axyridis invasion on abundance ofthe predator, Aphidoletes aphidimyza(Rondani) (Diptera: Cecidomyiidae) and apossible positive effect on the abundance ofchrysopids (Neuroptera: Chrysopidae). Principal component analysis indicated thatalthough individual species were affected, theoverall effect of H. axyridis invasion onthe predator guild as a whole was negligible. The data indicate that the interaction betweenthe two exotic species, H. axyridis andC. septempunctata, may be allowing nativecoccinellids to become more abundant on applethan when C. septempunctata was thedominant coccinellid.     

Incipient colonisation of Lutzomyia longipalpis in the city of Resistencia,province of Chaco,Argentina (2010-2012)

Lutzomyia longipalpis was recorded for the first time in Argentina in 2004, in the province of Formosa. In the following years, the vector spread to the south and west in the country and was recorded in the province of Chaco in 2010. From November 2010-May 2012, captures of Phlebotominae were made in the city of Resistencia and its surroundings, to monitor the spread and possible colonisation of Lu. longipalpis in the province of Chaco. In this monitoring, Lu. longipalpis was absent in urban sampling sites and its presence was restricted to Barrio de los Pescadores. This suggests that the incipient colonisation observed in 2010 was not followed by continuous installation of vector populations and expansion of their spatial distribution as in other urban centres of Argentina.     

Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae

Predation upon lady beetle (Coleoptera: Coccinellidae) eggs in the field is most often instances of egg cannibalism by larvae or adults while the majority of the remaining predation events upon coccinellid eggs is done by other species of Coccinellidae. Thus the recent introduction and establishment of Harmonia axyridis in the US could negatively affect native species of Coccinellidae via egg predation. However, little is known regarding the suitability of interspecific coccinellid eggs as a food source for larval development. In this study, it was found that native first or third instar Coleomegilla maculata and Olla v-nigrum larvae were incapable of surviving to the adult stage when provided solely exotic H. axyridis eggs. In stark contrast, H. axyridis larvae survived equally well when cannibalizing eggs or eating eggs of either native species. When C. maculata and O. v-nigrum were grouped as ‘native’ and compared with the exotic H. axyridis, more native eggs were attacked than exotic eggs and a higher percentage of eggs was attacked by H. axyridis larvae. Native and exotic larvae attacked a similar percentage of native eggs but native larvae attacked significantly fewer exotic eggs than did exotic larvae. These data suggest that H. axyridis may prey upon the eggs of these native species, when encountered in the field, compared with the likelihood of the native species preying upon H. axyridis eggs. Therefore, eggs of the native species C. maculata and O. v-nigrum will continue to be subjected to cannibalism and also to possible predation by other native species and the exotic H. axyridis.