Zdenka Martinkova

The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is native to Asia but has been intentionally introduced to many countries as a biological control agent of pest insects. In numerous countries, however, it has been introduced unintentionally. The dramatic spread of H. axyridis within many countries has been met with considerable trepidation. It is a generalist top predator, able to thrive in many habitats and across wide climatic conditions. It poses a threat to biodiversity, particularly aphidophagous insects, through competition and predation, and in many countries adverse effects have been reported on other species, particularly coccinellids. However, the patterns are not consistent around the world and seem to be affected by many factors including landscape and climate. Research on H. axyridis has provided detailed insights into invasion biology from broad patterns and processes to approaches in surveillance and monitoring. An impressive number of studies on this alien species have provided mechanistic evidence alongside models explaining large-scale patterns and processes. The involvement of citizens in monitoring this species in a number of countries around the world is inspiring and has provided data on scales that would be otherwise unachievable. Harmonia axyridis has successfully been used as a model invasive alien species and has been the inspiration for global collaborations at various scales. There is considerable scope to expand the research and associated collaborations, particularly to increase the breadth of parallel studies conducted in the native and invaded regions. Indeed a qualitative comparison of biological traits across the native and invaded range suggests that there are differences which ultimately could influence the population dynamics of this invader. Here we provide an overview of the invasion history and ecology of H. axyridis globally with consideration of future research perspectives. We reflect broadly on the contributions of such research to our understanding of invasion biology while also informing policy and people.

Seasonal variation in seed predation by adult carabid beetles

In many agro‐ecosystems of the temperate region, granivorous ground beetles (Coleoptera: Carabidae) are the most important invertebrate predators of seeds after dispersal. The consumption of a particular species of seed differs among carabid species, but seasonal variation in consumption has not yet been studied. Seasonal differences in the quantity of seed consumed by the carabids Harpalus affinis (Schrank) and Harpalus distinguendus (Duftschmid) were studied in a cafeteria experiment. Adults were collected on five dates between April and November and provided with seeds of 28 species of dicotyledonous herbaceous plants. Proportions eaten of the seeds offered (preferences) were nearly identical in both carabid species. Overall seed consumption increased from early spring until late June, then gradually decreased towards autumn. Despite this variation, the preferences on particular dates were essentially similar. Seasonal variation in carabid physiology and feeding experience thus influenced overall seed consumption, but not their preferences for particular seed species.

Body size, reproductive allocation, and maximum reproductive rate of two species of aphidophagous Coccinellidae exploiting the same resource

To test the predictions of allometric analyses of laboratory data on aphidophagous ladybirds, a study was carried out on a small [Propylea quatuordecimpunctata (L.); dry female body mass 3.7 mg] and large species (Coccinella septempunctata L.; 15.4 mg) (both Coleoptera: Coccinellidae) of predatory ladybird, which regularly exploit cereal aphids. In 2003–2006, females of C. septempunctata and in 2006 P. quatuordecimpunctata were collected at 2‐ to 5‐day intervals during the 30‐day period around the peak in cereal aphid abundance, and the number of eggs they laid in the following 24 h in the laboratory was recorded. In addition to the number of eggs laid, clutch mass, live weight, and scutum width of ovipositing females and the sizes of the clutches laid in the field were recorded. As predicted, the reproductive allocation in both species was similar. The weight of the eggs of C. septempunctata (0.20 mg) and P. quatuordecimpunctata (0.18 mg) differed little, and the proportion of body mass allocated to daily reproduction (ca. 12%) was identical in both species. In addition, the maximum number of eggs laid per day in the field by the large species was, as predicted, greater than by the small species. Interestingly, the size of the egg clutches laid by C. septempunctata in the field was similar to the daily oviposition of field‐collected adults recorded in the laboratory, whereas for P. quatuordecimpunctata it was significantly smaller. The role of morphology and physiology of ladybirds in structuring aphidophagous ladybird guilds is discussed.

Long-term trends in the composition of aphidophagous coccinellid communities in Central Europe

Coccinellids (Coleoptera: Coccinellidae) provide important ecosystem services as biocontrol agents in contributing to the regulation of key agricultural pests. It is generally accepted that biodiversity of native coccinellid communities has been declining during recent decades. Here, we present the results of a long‐term study of coccinellid communities and report an attempt to determine whether recent changes in land use have affected their composition. Coccinellids were sampled in cereal crops, on wild herbaceous plants and deciduous trees during two periods (1976–1983 and 2002–2010). There are similar species‐rich communities of coccinellids on trees and wild herbaceous plants (average numbers of species 3.18 and 3.06, respectively) and a poorer community on cereals (2.63). Only a few species, associated with particular types of vegetation, differed in their absolute abundance in the first and second period. There was no obvious cause of this variation in abundance. Diversity of coccinellid communities was higher in the second than in the first period (Shannon‐Wiener index 1.32 and 1.14 respectively), although the number of individuals was lower (average catch per sampling session 10.0 and 18.6 individuals respectively). Over the 35 years of this study, the compositions of the communities remained essentially similar with the numbers of particular species more closely correlated in the two periods on cereals (R2 = 0.97) than on herbaceous plants (R2 = 0.74) and trees (R2 = 0.67).

Seed age and storage conditions influence germination of barnyardgrass (Echinochloa crus-galli)

Abstract Germination was investigated in 1-yr and 8-yr-old seed lots of barnyardgrass. Each seed lot was divided into a portion stored dry at 25 C (afterripening) and a portion buried in the field (stratification) in central Europe (latitude 50°N, longitude 14°E). The afterripened seed lost dormancy within 2 yr after dispersal, whereas buried seed passed through annual dormancy/nondormancy cycles. The seed was germinated at five constant temperatures between 17 and 35 C with an 18/6-h light/dark photoperiod. Germination was affected by both seed age and storage conditions. Germination percentage and rate in 8-yr-old afterripened and each of the stratified seed lots varied with temperature. Optimum temperatures for germination were between 27 and 31 C, and the range of adequate temperatures increased with seed age. A common base temperature for germination was 11.7 C. In 1-yr-old afterripened material, the proportion of germinating seed (< 5%) and germination rate were similar at all temperatures. Barnyard...

Long-term changes in communities of native coccinellids: population fluctuations and the effect of competition from an invasive non-native species

We assessed the changes in abundance and community composition of native species of coccinellids (Coleoptera: Coccinellidae) on deciduous trees that occurred between 1970s and 2010s, in the Czech Republic. As the composition of adult communities varies with host plant and season, coccinellids were sampled in May–June from Acer, Betula and Tilia trees using a standardised sweeping method. This was done before (1976–1986) and after (2011–2014) the arrival of Harmonia axyridis in 2006, with interim samples from a period immediately before it arrived in the Czech Republic (2002–2006). Twenty‐one native species were identified in the total sample of 2674 adults. The abundance of Adalia bipunctata, Coccinella quinquepunctata and Propylea quatuordecimpunctata decreased over the whole period sampled. Declines in abundance of these species were already evident prior to the arrival of H. axyridis. Recent declines in Adalia decempunctata and Calvia quatuordecimguttata followed the arrival H. axyridis. Their abundance was increasing prior to the arrival of H. axyridis, but decreased following its invasion and the latter species might have affected their decline. The abundance of only one species, Calvia decemguttata, increased. Although the abundance of many species decreased and the frequency of some species varied, the diversity of native coccinellid populations (Shannon index) was similar over the 40 years of this study. The changes in species composition can in part be attributed to H. axyridis, the role of other factors (e.g. climate change, habitat degradation) in the long‐term fluctuations in abundance of coccinellids should be considered in future assessments.

Contrast adaptation to time constraints on development of two pre-dispersal predators of dandelion (Taraxacum officinale) seed

Pre-dispersal seed predators of quickly maturing inflorescences of Asteraceae are constrained by shortage of development time. At seed dispersal, they should pupate or, if still immature, relocate into another inflorescence. To investigate how dominant coleopteran predators of dandelion seed, Glocianus punctiger (Curculionidae) and Olibrus bicolor (Phalacridae), cope with time limitation we combined observation (development and temperature of dandelion capitulum, thermal constants of predator development, age structure of larval populations at seed dispersal) and analogy (“rate isomorphy” in predator development, comparing “model” coleopteran species with similar temperature requirements). Development of a dandelion capitulum takes 21 days. The time available to G. punctiger (140–190 day degrees, development threshold 6.3°C) is sufficient to complete development and pupate after seed dispersal. By contrast, only 30–50 day degrees are available to O. bicolor (threshold 13.5°C) and this is not enough to complete development and consequently immature larvae should move to other capitula to continue feeding until pupation. These contrast strategies which are determined by this thermal adaptation, are accompanied by differences in larval morphology. The “cold adapted” G. punctiger has an apodous larva not capable of migrating between capitula while the “warm adapted” O. bicolor has a mobile campodeiform larva capable of migration.

Geographic variation in seed dormancy among populations of Echinochloa crus-galli

In 1991–1993, we investigated the incidence of seed dormancy in 25 local populations of barnyard grass, Echinochloa crus-galli (L.) P.Beauv., in the western Czech Republic. The percentage of germination after 4 months afterripening of dry seeds at 25°C varied between 0.0 and 83.6%. Although there were significant annual differences in the percentage of germination at some localities, typical proportions of dormant seeds persisted over 3 years at field sites where the seed bank was not disturbed. One-way ANOVA (using data from 14 cultivated or abandoned fields) revealed that 73.0% of variance in seed dormancy incidence could be attributed to the effect of locality (P<0.001). Incidence of dormancy was not correlated with mother plant stature (dry above-ground biomass, number of tillers, maximal stem height) nor seed mass. There was a significant correlation (r2=0.403, P<0.005) between dormancy incidence at natural localities in 1991 and in F1 offspring sown at experimental grounds at Praha-Ruzyně in 1992. The results indicate that heredity is important in maintaining local variation in seed dormancy, probably favoured by the self-pollinating reproduction of barnyard grass.

Spatial and temporal changes in the abundance and compostion of ladybird (Coleoptera: Coccinellidae) communities

Because of their services to agriculture most ladybirds (Coleoptera: Coccinellidae) are intensively studied predators of mainly phytophagous pests. The study of the long-term variation in the composition of their communities was stimulated by recent dramatic changes in the abundance of some species. We review and evaluate possible effects of the main causes cited in the literature. Agricultural and habitat changes (particularly urbanization) affect coccinellid abundance, both negatively and positively. In the temperate zone dominant species occur most frequently associated with abundant prey populations on crops, weeds and planted stands of trees resulting from human activity. Invasive non-native species of coccinellids may endanger native species through intraguild predation or competition for resources, but their supposed serious negative effects on native species can differ considerably. Climatic change may influence coccinellid species in several ways, including indirect effects through lower trophic levels and desynchronisation of the phenologies of host plants, prey and coccinellid populations. In the near future we do not expect climate warming to have important effects on ladybird diversity globally, but local changes in the composition of coccinellid communities and abundance of particular species could occur.

The invasion history, distribution and colour pattern forms of the harlequin ladybird beetle Harmonia axyridis (Pall.) (Coleoptera, Coccinellidae) in Slovakia, Central Europe

Abstract The harlequin ladybird beetle Harmonia axyridis (Coleoptera, Coccinellidae) has invaded and established in Slovakia. Following unintentional introduction in 2008, the spread of the alien coccinellid was very fast. By the end of 2009, it was recorded across the whole country, and by the end of 2012 it was widely distributed and common in various habitats, particularly gardens, orchards and urban areas, where it was most frequent on trees. The rate of eastward spread was approximately 200 km year-1, similar to the overall rate of spread in Europe. Between 2008 and 2012, the coccinellid was recorded in a total of 153 localities, in altitudes ranging from 98 to 1,250 m. Most records of this species were made in lowlands, hilly areas and valleys separating mountain ridges. However, it was only rarely documented in areas above 700 m a.s.l. The non-melanic colour form (f. succinea) was dominant along a longitudinal transect including eight urban areas across Slovakia, with the frequency of melanic forms (f. spectabilis and f. conspicua together) between 6.3 and 19.2% and a median equal to 10.5%. The invasion history and distribution of H. axyridis in Slovakia are discussed with regard to the time sequence of records, rate of spread, altitudinal distribution, anthropogenic dispersal, effective recording, proportion of melanic forms and other relevant aspects associated with the spread of this successful invader.