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.     

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.     

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.     

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.     

Aggregation of polyphagous predators in response to multiple prey: ladybirds (Coleoptera: Coccinellidae) foraging in alfalfa

The spatial distribution of polyphagous predators may often reflect the integration of aggregative responses to local densities of multiple species of prey, and as such may have consequences for the indirect linkages among the prey sharing these predators. In a factorial field experiment in which we manipulated local prey densities within a field of alfalfa in Utah (USA), we tested whether aphidophagous ladybirds would aggregate not only in response to their primary aphid prey, but also in response to an abundant alternative prey, the alfalfa weevil (Hypera postica [Gyllenhal]). Native North American ladybirds (primarily Hippodamia convergens Guerin and H. quinquesignata quinquesignata [Kirby]) responded only to spatial variation in aphid density. In contrast, the introduced ladybird, Coccinella septempunctata L., aggregated also at local concentrations of the weevil late in the experiment when weevil density was high and aphid density was relatively low throughout all experimental plots. The results support the hypothesis that C. septempunctata is more responsive than are native ladybirds to the availability of alternative prey in alfalfa, which may account in part for the displacement of native ladybirds from alfalfa by the introduced species as aphid numbers have declined. The differing responses of the native and introduced ladybirds to spatial patterns of the alternative prey underscore the importance of extending the study of predator aggregation to understand better how polyphagous predators distribute themselves in response to spatial patterns of multiple species of potential prey.     

Response of passerine birds and chicks to larvae and pupae of ladybirds

1. Few, if any, experimental tests have demonstrated the anti‐predator protection of the developmental stages of ladybirds (Coleoptera: Coccinellidae) against vertebrates, despite the fact that both the visual appearance of ladybirds and the content of defensive compounds fulfil the definition of an aposematic prey. 2. In this study, avian predators of three species were confronted with fourth‐instar larvae and pupae of the harlequin ladybird (Harmonia axyridis) – a large, conspicuous, and toxic ladybird species. 3. The selected predators differed in their individual experience and attitude to ladybirds. Wild‐caught great tits (Parus major) strongly avoided attacking ladybirds in general, whereas wild‐caught tree sparrows (Passer montanus) were willing to include ladybirds in their diet. Domestic chicks (Gallus gallus domesticus) have never been confronted with ladybirds but usually show avoidance of aposematic signals. In this study, great tits and domestic chicks avoided both developmental stages, but in the case of chicks the avoidance had to be learned over the course of repeated encounters. Sparrow avoidance was significantly lower, with more than one‐third of the prey being attacked and eaten. 4. The protection of both developmental stages of ladybirds is similar to adults, despite substantially different visual appearance.     

Habitat and introduced predators influence the occupancy of small threatened macropods in subtropical Australia

Australia has had the highest rate of mammal extinctions in the past two centuries when compared to other continents. Frequently cited threats include habitat loss and fragmentation, changed fire regimes and the impact of introduced predators, namely the red fox (Vulpes vulpes) and the feral cat (Felis catus). Recent studies suggest that Australia's top predator, the dingo (Canis dingo), may have a suppressive effect on fox populations but not on cat populations. The landscape of fear hypothesis proposes that habitat used by prey species comprises high to low risk patches for foraging as determined by the presence and ubiquity of predators within the ecosystem. This results in a landscape of risky versus safe areas for prey species. We investigated the influence of habitat and its interaction with predatory mammals on the occupancy of medium‐sized mammals with a focus on threatened macropodid marsupials (the long‐nosed potoroo [Potorous tridactylous] and red‐legged pademelon [Thylogale stigmatica]). We assumed that differential use of habitats would reflect trade‐offs between food and safety. We predicted that medium‐sized mammals would prefer habitats for foraging that reduce the risk of predation but that predators would have a positive relationship with medium‐sized mammals. We variously used data from 298 camera trap sites across nine conservation reserves in subtropical Australia. Both dingoes and feral cats were broadly distributed, whilst the red fox was rare. Long‐nosed potoroos had a strong positive association with dense ground cover, consistent with using habitat complexity to escape predation. Red‐legged pademelons showed a preference for open ground cover, consistent with a reliance on rapid bounding to escape predation. Dingoes preferred areas of open ground cover whereas feral cats showed no specific habitat preference. Dingoes were positively associated with long‐nosed potoroos whilst feral cats were positively associated with red‐legged pademelons. Our study highlights the importance of habitat structure to these threatened mammals and also the need for more detailed study of their interactions with their predators.     

Avoidance responses of an aphidophagous ladybird, Adalia bipunctata, to aphid-tending ants

Abstract.  1. Insect predators often aggregrate to patches of high prey density and use prey chemicals as cues for oviposition. If prey have mutualistic guardians such as ants, however, then these patches may be less suitable for predators.
2. Ants often tend aphids and defend them against predators such as ladybirds. Here, we show that ants can reduce ladybird performance by destroying eggs and physically attacking larvae and adults.
3. Unless ladybirds are able to defend against ant attacks they are likely to have adaptations to avoid ants. We show that Adalia bipunctata ladybirds not only move away from patches with Lasius niger ants, but also avoid laying eggs in these patches. Furthermore, ladybirds not only respond to ant presence, but also detect ant semiochemicals and alter oviposition strategy accordingly.
4. Ant semiochemicals may signal the extent of ant territories allowing aphid predators to effectively navigate a mosaic landscape of sub-optimal patches in search of less well-defended prey. Such avoidance probably benefits both ants and ladybirds, and the semiochemicals could be regarded as a means of cooperative communication between enemies.
5. Overall, ladybirds respond to a wide range of positive and negative oviposition cues that may trade-off with each other and internal motivation to determine the overall oviposition strategy.     

Dietary preference of cheetahs (Acinonyx jubatus) in south‐eastern Kenya

The conversion of natural ecosystems due to anthropogenic activities has led to the destruction of natural habitats and to the deterioration of habitat quality. Top predators particularly respond sensitively to changes in habitat structures, including the availability of prey. The cheetah Acinonyx jubatus prefers small‐medium‐sized, wild ungulate prey due to the cheetah''s morphological adaptations. However, the majority of the species’ population is found beyond protected areas, where habitat structures, species abundances, and community composition are highly influenced by human activities. Only few studies have analyzed the diet preference of cheetahs in relation to prey availability and abundance for rangelands beyond protected areas in Eastern Africa. The study aimed to determine cheetah prey preference in the rangelands of south‐eastern Kenya based on scat analyses. We compared dietary preference of cheetah with prey availability. For this purpose, we conducted standardized game counts. We analyzed 27 cheetah scat samples collected across the same study area where we also conducted game counts. We found that Grant''s gazelle Gazella granti contributed the highest portion of cheetah''s diet, although Thomson''s gazelle Gazella thomsonii was the most abundant medium‐sized ungulate prey in the study areas. We also recorded two primate species, yellow baboon Papio cynocephalus and vervet monkey Chlorocebus pygerythrus, as well as the rock hyrax Procavia capensis in the cheetah diet. These species have never been documented as cheetah prey before. Furthermore, our results document livestock as potential prey for cheetahs. These observations underline that cheetah use diverse prey in rangelands outside protected areas, and that the abundance of specific prey does not influence cheetah prey preference.     

Role of surface chemicals in egg cannibalism and intraguild predation by neonates of two aphidophagous ladybirds, Propylea dissecta and Coccinella transversalis

Abstract:  The role of surface chemicals in egg cannibalism and intraguild predation by neonates of two aphidophagous ladybirds, Propylea dissecta and Coccinella transversalis were examined. Neonates of both species prefer to eat non-sibling conspecific eggs than heterospecific eggs, with higher preference in P. dissecta . Surface chemicals appear to play a major role for the preference of conspecific eggs, as the ladybird behaviour was reversed when these chemicals were interchanged. The surface chemicals present on the eggs possibly act as feeding stimulants to conspecific neonates but not for heterospecific neonates. Egg clustering enhances the effect of surface chemical and stimulate non-sibling egg cannibalism and appears to reduce intraguild predation. Egg clustering is advantageous to ladybirds, as it can stimulate non-sibling cannibalism by neonates. It appears that aggregation of chemicals present on the conspecific egg surface possibly attracts the hungry conspecific neonate, providing the first meal for its survival, while protecting against heterospecific predators. Neonates of both ladybirds were reluctant to eat heterospecific eggs.     

Biogeographic variation in behavioral and morphological responses to predation risk

The expression of prey antipredator defenses is often related to ambient consumer pressure, and prey express greater defenses under intense consumer pressure. Predation is generally greater at lower latitudes, and antipredator defenses often display a biogeographic pattern. Predation pressure may also vary significantly between habitats within latitudes, making biogeographic patterns difficult to distinguish. Furthermore, invasive predators may also influence the expression of prey defenses in ecological time. The purpose of this study was to determine how these factors influence the strength of antipredator responses. To assess patterns in prey antipredator defenses based upon geographic range (north vs. south), habitat type (wave-protected vs. wave-exposed shores), and invasive predators, we examined how native rock (Cancer irroratus) and invasive green (Carcinus maenas) crab predators influence the behavioral and morphological defenses of dogwhelk (Nucella lapillus) prey from habitats that differ in wave exposure across an ~230 km range within the Gulf of Maine. The expression of behavioral and morphological antipredatory responses varied according to wave exposure, geographic location, and predator species. Dogwhelks from areas with an established history with green crabs exhibited the largest behavioral and morphological antipredator responses to green crabs. Dogwhelk behavioral responses to rock crabs did not vary between habitats or geographic regions, although morphological responses were greater further south where predation pressure was greatest. These findings suggest that dogwhelk responses to invasive and native predators vary according to geographic location and habitat, and are strongly affected by ambient predation pressure due to the invasion history of an exotic predator.     

Antipredator response of pea aphids <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis> (Hemiptera: Aphididae): effects of predation risks from an alternative patch on a current patch

To escape from predators, herbivorous prey could leave their current patch and relocate to an alternative patch. However, when other predators are present on the new patch, prey are again exposed to predation risk. Thus, patch leaving might be affected by the other predators. We studied patch leaving of pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in response to ladybird larvae Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on broad bean Vicia faba L. shoots that were offered as patches for aphids. We tested whether shoot leaving was affected by the presence of predators on alternative shoots under laboratory conditions. Odors from alternative shoots were evaluated as possible cues used by aphids to assess predation risk on the shoots. We exposed aphids to odors from alternative shoots with conspecifics plus either adult or larval ladybirds or larval green lacewings Mallada desjardinsi Navas (Neuroptera: Chrysopidae). Shoot leaving was reduced only when adult ladybirds were present on the alternative shoots compared with controls (i.e., no predators on the alternative shoots). Odors of both adult ladybirds and of conspecifics being attacked by ladybird larvae were required for reduced leaving. Hence, predation risks on current and alternative patches might affect the antipredator responses of aphids.     

Consumption,developmental and reproductive attributes of two con-generic ladybird predators under variable prey supply

Availability of aphid prey in habitat is often heterogeneous in space and time and its deprivation causes severe effects on life attributes of ladybird predators. Sometimes ladybirds locate high prey biomass while on certain occasions prey biomass may be either medium/low or altogether absent. Present study has been designed in view of three prey biomass conditions in nature, viz. low, medium and high, selecting Coccinella septempunctata and Coccinella transversalis as experimental ladybirds. Results revealed that consumption, developmental and reproductive attributes of both ladybirds changed in response to prey availability. On high prey biomass larvae had higher consumption and growth rates, developed faster and had low mortality, while emerging adults were large in size, had high consumption rates and utilized prey biomass maximally on production of eggs, self maintenance and survival. In contrast low prey biomass reduced chances of larval survival and emerging adults were small in size, had poor prey consumption rates, low fecundity, egg fertility and short life span. Females exhibited triangular fecundity and egg fertility functions and plateau shaped prey consumption rate function with age, indicating towards their highest reproductive performance during middle age on three prey biomasses; being highest on high prey biomass. On three prey biomasses, females had higher body biomass conversion efficiency during pre- and post-oviposition periods and higher egg biomass conversion efficiency during oviposition period; being highest on high prey biomass. Thus middle aged ladybirds reared on high prey biomass may suppress pest populations better than those reared on low/medium prey biomass.     

Habitat preferences and diet in the predatory Coccinellidae (Coleoptera): an evolutionary perspective

Coccinellids (ladybird beetles) exhibit considerable diversity in habitat and dietary preference and specificity. This is evident even when comparing species within some coccinellid genera. Resource limitation and competition are suggested as of greatest importance in the evolution of coccinellid habitat preferences. Dietary and habitat specialization has probably occurred in some lineages within broader preferences possessed by generalist ancestors, to avoid the costs associated with migration between habitats and prey switching. Feeding in atypical habitats, on alternative food, when optimal prey are scarce, is likely to have been of great importance in facilitating evolutionary shifts to novel diets and habitats. The broad host ranges of many coccinellid parasitoids and observed interspecific differences in parasitoid prevalence resulting from physiological differences between coccinellid species argue that enemy free space has been of limited importance in habitat and prey shifts in this group. Rapid change may occur in coccinellid foraging patterns, perhaps due to conditioning, and coccinellids may swiftly adapt to new habitats through selection acting on the expression pre-existing traits. Diet, as a determinant of coccinellid migration and gene flow, is likely to affect probable modes of speciation in different coccinellid groups. Parapatric speciation and possibly sympatric speciation are suggested as of possible importance in the genesis of new coccinellid species through prey and habitat shifts.     

Partitioning mechanisms of Predator Interference in different Habitats

Prey are often consumed by multiple predator species. Predation rates on shared prey species measured in isolation often do not combine additively due to interference or facilitation among the predator species. Furthermore, the strength of predator interactions and resulting prey mortality may change with habitat type. We experimentally examined predation on amphipods in rock and algal habitats by two species of intertidal crabs, Hemigrapsus sanguineus (top predators) and Carcinus maenas (intermediate predators). Algae provided a safer habitat for amphipods when they were exposed to only a single predator species. When both predator species were present, mortality of amphipods was less than additive in both habitats. However, amphipod mortality was reduced more in rock than algal habitat because intermediate predators were less protected in rock habitat and were increasingly targeted by omnivorous top predators. We found that prey mortality in general was reduced by (1) altered foraging behavior of intermediate predators in the presence of top predators, (2) top predators switching to foraging on intermediate predators rather than shared prey, and (3) density reduction of intermediate predators. The relative importance of these three mechanisms was the same in both habitats; however, the magnitude of each was greater in rock habitat. Our study demonstrates that the strength of specific mechanisms of interference between top and intermediate predators can be quantified but cautions that these results may be habitat specific. An erratum to this article can be found at     

Prey habitat selection under shared predation: tradeoffs between risk and competition?

An individual's choice of habitat should optimize amongst conflicting demands in a way that maximizes its fitness. Habitat selection by one species will often be influenced by presence and abundance of competitors that interact directly and indirectly with each other (such as through shared predators). The optimal habitat choice will thus depend on competition for resources by other species that can also modify predation risk. It may be possible to disentangle these two effects with careful analysis of density‐dependent habitat selection by a focal prey species. We tested this conjecture by calculating habitat isodars (graphs of density assuming ideal habitat selection) of chital deer living in two adjoining dry‐forest habitats in Gir National Park and Sanctuary, western India. The habitats differed only in presence (Sanctuary) and absence (National Park) of domestic prey (cattle and buffalo). Both species are preyed on by Asiatic lions. The habitat isodar revealed at low densities, that chital live in small groups and prefer habitat co‐occupied by livestock that reduce food resources, but also reduce predation risk. At higher densities, chital form larger groups and switch their preference toward risky habitat without livestock. The switch in chital habitat use is consistent with theories predicting that prey species should trade off safety in favor of food as population density increases.     

Exotic ladybirds for biological control of herbivorous insects – a review

Since the late 19th century, exotic ladybirds (Coleoptera: Coccinellidae) have been used extensively for suppressing herbivorous insects of economic importance. In recent decades, the introduction of non‐native biological control (BC) agents has been greatly limited due to the awareness of the potential non‐target effects of introductions. Nonetheless, recent episodes of biological invasions of economically important pests have raised the need to carefully consider whether the expected benefits of pest control go beyond the possible environmental risks of introduction. To better understand the factors that contributed to successful BC programs, here we review the literature behind classical and augmentative BC using exotic ladybirds. Additionally, by means of case studies, we discuss the BC efficacy of selected exotic species, e.g., Coccinella septempunctata L., Harmonia axyridis (Pallas), and Hippodamia variegata (Goeze), and their position within the communities of predators in the introduced areas of USA, Canada, and Chile. In Europe, much of the research on exotic ladybirds has been conducted on the undesired impact of H. axyridis. Therefore, we summarize the risk assessment data for this species and review the field research investigating the ecological impact on European aphidophagous predators. According to the BIOCAT database of classical BC programs, 212 ladybird species belonging to 68 genera have been released in about 130 years of BC activity, with 14.6% of introductions having resulted in partial, substantial, or complete control of the target pest. However, because post‐release evaluation of establishment and BC success has not always been conducted, this rate could underestimate the successful cases. Among other factors, ladybird establishment and pest suppression mostly depend on (1) intrinsic factors, i.e., high voracity, synchronized predator‐prey life cycle, and high dispersal ability, and (2) extrinsic factors, i.e., adaptability to the new environment and landscape composition. This review contributes to improved understanding of ladybirds as exotic BC agents.     

Habitat preferences of an endangered insect species,Cepero’s ground-hopper (<Emphasis Type="Italic">Tetrix ceperoi</Emphasis>)

Preventing the global decline in biodiversity is a major task for conservation biologists. Although habitat loss has been identified as a key factor driving extinction processes, our knowledge on the habitat requirements of many endangered species, particularly invertebrates, is still sparse. We present a feasible method to study the microhabitat preferences of insect species. In Central Europe, the endangered Cepero’s ground-hopper, Tetrix ceperoi, is believed to have its only remaining natural habitats in dune slacks of the Wadden Sea Islands. Our results suggest that this species performs an active habitat choice of damp, bare patches with high temperatures. While ponds and fens in dune slacks provide large areas of damp bare ground and algal mats, grasslands, degraded dune slacks and the transitional zone between salt marsh and dunes are less suited as habitats. The major threat for T. ceperoi is found in the succession of its pioneer habitats due to the reduced natural dynamics. In industrialized countries, pioneer habitats and species are threatened substantially by coastal protection and floodplain regulation. This is only compensated in part by anthropogenic creation of secondary habitats, such as different kinds of pits or coal heaps. Nevertheless, there is a strong need for restoration of dynamic habitats by floodplain revitalization and dune slack restoration.     

Abundance of macrofauna in dense seagrass is due to habitat preference,not predation

Summary Two main hypotheses compete to explain why prey abundance decreases when seagrass density is reduced. One proposes that predators are more successful amongst seagrass of lower density; the other invokes habitat choice by prey. We reduced the density of seagrass in the presence, and in the absence, of predators in a field experiment to discriminate between these hypotheses. When seagrass was manipulated abundances of all six prey species decreased simultaneously both in the presence and in the absence of predators. We conclude that correlations of prey abundance and shoot density within a seagrass bed are proximately due to habitat preference of dense seagrass by prey. We report another experiment which supports this conclusion and shows that habitat preference is exercised at the earliest opportunity. However, the habitat preferences may have been selected by predation pressure.     

Territory quality, survival and reproductive success in southern emu-wrens Stipiturus malachurus

Multi-factor analyses of territory quality in relation to fitness components of adults are rare, especially in non-migratory species. I studied the influence of multiple attributes of territory quality (habitat type and the abundance of food and predators) on the reproductive success and survival of a threatened Australian passerine, the southern emu-wren Stipiturus malachurus . The abundance of frequently-selected prey types (lepidoptera, diptera, hemiptera and larvae) varied significantly across territories according to habitat type. Reproductive success (number of offspring fledged) was highest in territories containing a greater proportion of tall shrubland, which had the highest insect abundance of any habitat. Closed heathland and sedge/rushland also had high food abundance compared to other habitat types, but higher fledging success occurred only within closed heathland, possibly because predator density was lower in this habitat type. High snake density was associated with reduced adult survival during the breeding season and a lower probability of nest success. In sedge/rushland, any benefits of prey abundance may therefore be offset by a high density of predators. Emu-wren age and size were unrelated to breeding output of pairs, suggesting that ecological factors may swamp effects of individual quality on emu-wren fitness components. Preservation of tall shrubland and closed heathland habitats appear to be of key conservation priority for emu-wrens.