António O. Soares

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.

Harmonia axyridis: What will stop the invader?

In recent years Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) has become a very popular insect among biological control practitioners and scientists, not only for its potential to be an efficient biological control agent but also because it is considered invasive. Individuals of this species were deliberately introduced into several countries for biological control of different arthropods pests. However the predator itself became an invasive species, affecting the dynamics and composition of several guilds through direct or indirect interactions with established species, including intraguild predation. In this paper we discuss the reasons why the species has a high invasiveness and what are the limits to invasion by this species. It is not clear if the invasiveness of the beetle is linked to its biological, ecological and behavioural abilities, or to other factors such as invasibility and interactions between the invaders, the noninvaders, and the habitat, which may in part explain the reasons of its success and help us to answer the question “what will stop the invader?” We also discuss the reason for the absence of the predator in the Azores islands. Despite the intentional introduction of H. axyridis in the Azores and the high number of individuals released, there are no records of this species in the wild, despite recent extensive sampling effort. In this paper we discuss the reasons for the apparent failure or the delay in establishment of the predator. One factor which may hamper the establishment of H. axyridis in some of the Azores islands is the absence of winter environmental conditions, mainly the temperature which is seldom lower than 12°C, essential for the induction of diapause. The lack of success in the establishment could be also related to functional diversity saturation, that is species saturation and competitive exclusion of H. axyridis by other previously established species may be operating.

Effect of Temperature and Intraspecific Allometry on Predation by Two Phenotypes of Harmonia axyridis Pallas (Coleoptera: Coccinellidae)

Abstract Harmonia axyridis Pallas is a highly polymorphic coccinellid with a wide geographic distribution. Genetic polymorphism seems to be the strategy adopted for facing different habitats at different times. Many modifications, such as body shape, body size, and elytral patterns, may be adaptive through imparting increased tolerance to adverse conditions. Previous studies evaluating differences in the light-colored aulica and dark colored nigra phenotypes found differences in biological performances at 20°C. However, whether the predatory activity of the different phenotypes changes under different temperatures remains unknown. Relative consumption rate and predation activity of fourth instars and adults of aulica and nigra phenotypes were compared at 10, 15, 20, 25, and 30°C. Our results showed that temperature is a limiting factor to larval and adult relative consumption rate. The thermal optimum of nigra adults was 3.7°C lower than that of aulica. Both larvae and adults of nigra were more stenothermic than aulica. Close to the upper limit of tolerance (30°C), predation activity of nigra adults was more affected than aulica. In larvae body size and shape could explain the differences observed, because aulica is significantly bigger than nigra and thus aulica presumably can better control heat exchange.

Invasions by ladybugs, ladybirds, and other predatory beetles.

Species of predatory Coleoptera have become abundant in new geographic regions recently, raising concerns for invaded ecosystems. We address this topic by focusing on invasive alien ladybird beetles (Coccinellidae; known also as ladybugs). Humans appear directly or indirectly responsible for all or most ladybird invasions. Factors hypothesized to have promoted ladybird invasions include genetic diversity (e.g., for polymorphism), phenotypic plasticity, adaptation and genetic shift, generalized diet and habitat preferences, flexible life history and reproduction, large body size, and release from enemies. Factors such as climate, habitat and prey availability, and biotic resistance may sometimes prevent or slow ladybird invasions. Indigenous species (e.g., herbivores) may suffer from invasions, and biological control programs may be affected. Species of indigenous ladybirds throughout the world are reported to have declined in abundance following ladybird invasions, with increased competition and/or intraguild predation most often hypothesized or inferred. Similar recent studies especially of ground beetles (Carabidae) also make clear the potential of invasive alien predatory Coleoptera to disrupt invaded natural and agricultural ecosystems.

Influence of prey quality on the fitness of two phenotypes of Harmonia axyridis adults

The performance of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) adults of the aulica and nigra phenotypes fed on Aphis fabae Scopoli and Myzus persicae (Sulzer) was compared by measuring their voracity, daily biomass consumption, daily weight gain, efficiency of food utilisation, and reproductive capacity. Our results demonstrated differences in the suitability of A. fabae and M. persicae for the two phenotypes of the predator. This suggests that either differences occur in the nutritive requirements of the predators, or in the nutritive value of the two prey species. Both A. fabae and M. persicae supported the growth and oviposition of the aulica and nigra phenotypes. Although nigra females consumed fewer M. persicae, they achieved the same daily weight gain as aulica females. The predator phenotypes consumed the same amount of A. fabae, but the daily weight gain of aulica females was higher than that of nigra. The two predator phenotypes had the same feeding efficiency when consuming M. persicae or A. fabae. The reproductive capacity of nigra females was higher, when this phenotype consumed A. fabae rather than M. persicae.

Interference competition between ladybird beetle adults (Coleoptera: Coccinellidae): effects on growth and reproductive capacity

Cage experiments were used to determine the minimum number of Aphis fabae Scopoli that females of the Azorean native ladybird beetle Coccinella undecimpunctata L. require per day to achieve maximum fecundity and to assess the effects of interference competition from conspecific and heterospecific [Harmonia axyridis (Pallas)] adult ladybirds on its growth and reproduction. The number of A. fabae at which females of C. undecimpunctata ate most aphids, achieved maximum reproduction and maintained their body weight, was 200. The presence of H. axyridis adults, unlike the presence of C. undecimpunctata, significantly affected the reproductive numerical response of C. undecimpunctata even though the resource was not in short supply. The results suggest that interference competition with heterospecifics may adversely affect the reproductive capacity of C. undecimpunctata. Based on previous results and those reported here, we suggest that the introduction of H. axyridis could endanger the population abundance and/or result in the competitive displacement of C. undecimpunctata from the Azorean ecosystem.

Effects of pirimicarb, buprofezin and pymetrozine on survival, development and reproduction of Coccinella undecimpunctata (Coleoptera: Coccinellidae)

Abstract The effects of pirimicarb (a neurotoxin), buprofezin (an insect growth regulator) and pymetrozine (an antifeedant) on Coccinella undecimpunctata were assessed by studying the survival and development of all immature stages and the survival and reproductive performance of adults. Insecticides were sprayed at doses recommended by the manufacturers for the control of aphids and/or whiteflies. None of the three insecticides had a significant effect on the survival of C. undecimpunctata eggs. When sprayed on larvae, buprofezin significantly reduced survival to adulthood to <33%, compared to >45% for the control and other insecticide treatments. Rates of adult survival, fecundity, and fertility, and the percentage of egg hatch, were not significantly different between control and insecticide treatments. Thus, larval stages were more susceptible to insecticides than were adults. In general, pirimicarb and pymetrozine had no adverse effects on immature or adult stages of C. undecimpunctata, and hence are suitable for IPM of sucking pests.

Prey availability in time and space is a driving force in life history evolution of predatory insects.

Environmental constraints can be determinant key factors conditioning predator life history evolution. Prey seems to have conditioned life history evolution in their ladybird predator, with the predators of aphids apparently presenting faster development, greater fecundity and shorter longevity than species preying on coccids. However a rigorous comparison has never been done. We hypothesize that aphids and coccids differ by their developmental rate, abundance, and distribution in the field, which act as ecological constraints promoting life history evolution in ladybird predators. Field data reveal that aphids are ephemeral resources available in the form of large colonies randomly distributed in the habitat whereas coccids form smaller colonies that tend to be aggregated in space and available for longer periods. A comparison in laboratory conditions of two predatory species belonging to the tribe Scymnini (Coleoptera: Coccinellidae) show that the aphidophagous species lives at a faster pace than the coccidophagous: it develops faster, matures earlier, is more fecund, has a shorter reproductive life-span and allocate proportionally more fat in its gonads relative to soma. This indicates that the life histories of aphidophagous and coccidophagous ladybird predators appear to have evolved in response to particular patterns of prey availability in time and space. Under the light of these results, the existence of a slow-fast continuum in ladybirds is briefly addressed.

Abundance and spatial distribution of aphids and scales select for different life histories in their ladybird beetle predators

Abstract:  Life history parameters tend to differ between aphidophagous and coccidophagous ladybird beetles. It seems that the nature of prey, in particular the abundance, number and size of the colonies and their spatial distribution, may have been selected for the evolution of the life histories in these two groups of coccinellids, leading the aphidophagous ladybird beetles to develop at a fast pace and the coccidophagous beetles at a slower pace. To study the abundance, number and size of the colonies and the spatial distribution of aphid and coccid species, 100 sampling plots regularly spaced along four parallel transects were surveyed in the summer of 2004. At each sampling plot, species abundance, and the number and size of colonies of aphid and coccid species were recorded. Iwaos patchiness regression was used to assess the spatial distribution of aphids and coccids. From this study, it was found that coccids are much rarer than aphids but formed more colonies. Whereas aphids display a stonger tendency to crowding, aphid colonies are randomly distributed in space while coccid groups are aggregated. So, it seems that the abundance and spatial distribution of prey distribution may be factors selecting for the evolution of different life histories among aphidophagous and coccidophagous ladybird beetles.

Voracity of Coccinella undecimpunctata: effects of insecticides when foraging in a prey/plant system

Coccinella undecimpunctata L. is a euryphagous predator established in Azores that offers interesting potential as a control agent in the context of integrated pest management (IPM). However, to further develop IPM against aphids, it is important to evaluate the effects that insecticides might have on voracity. Thus, we proposed to evaluate the effects of pirimicarb and pymetrozine on the voracity of 4th instar larvae and adults of C. undecimpunctata, under distinct scenarios of exposure to chemicals within a prey/plant system. Voracity of C. undecimpunctata was not significantly affected by pirimicarb or pymetrozine when treatments were directly sprayed on the predator; however, when insecticides were sprayed on the prey/plant system, the predator’s voracity was significantly increased. Results suggest that C. undecimpunctata does not detect the insecticide on the aphids and indicate that the increase in voracity may be due to a decrease in the mobility of insecticide-treated aphids, since their capture should be easier than highly mobile non-treated prey. The consequences of such increase in the voracity for IPM programs are discussed.