Éric Lucas

INTRAGUILD PREDATION AMONG APHID PREDATORS: CHARACTERIZATION AND INFLUENCE OF EXTRAGUILD PREY DENSITY

Intraguild predation (IGP), a common interaction in invertebrates and vertebrates, affects the abundance and distribution of many species. Several parameters influence the magnitude and direction of IGP: feeding specificity, size, mobility, and aggressiveness of the protagonists, as well as extraguild prey density. Under laboratory conditions, we studied IGP among three species of aphid predators, Aphidoletes aphidimyza (Diptera: Cecidomyiidae), Chrysoperla rufilabris (Neuroptera: Chrysopidae), and Coleomegilla maculata lengi (Coleoptera: Coccinellidae), which commonly attack the potato aphid (extraguild prey) Macrosiphum euphorbiae (Homoptera: Aphididae). We characterized the levels and symmetry of IGP among the various stages of the predators in the absence of extraguild prey. The aphid specialist A. aphidimyza was more vulnerable to IGP than C. rufilabris and C. maculata, two generalist predators. The C. maculata/C. rufilabris interaction was symmetric (mutual IGP), whereas the C. maculata/A. aphidimyza and C. rufilabris/A. aphidimyza interactions were asymmetric, in favor of the coccinellid and the lacewing, respectively. Sessile and low mobility stages of all species were extremely vulnerable to IGP. Generally, the larger sized individual won confrontations. For similar sizes, lacewing larvae were superior to coccinellid larvae. We also tested whether IGP decreases when extraguild prey are introduced into the system. Data from five predator combinations revealed three types of responses: (1) an exponential decrease in IGP (lacewing instar I vs. coccinellid instar I); (2) a constant IGP (lacewing instar III vs. coccinellid instar I); (3) a constant IGP at low densities decreasing at high densities (lacewing instar III vs. gall midge old larva). Four theoretical scenarios are derived from these responses. Each is discussed according to the ecological attributes of the protagonists. This study shows that IGP is influenced by factors inherent to the predators and external factors such as extraguild prey density. The results are discussed further in the context of aphid biological control.

Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae

Voracity and feeding preferences of adult Coccinella septempunctata L. and Harmonia axyridis Pallas (Coleoptera: Coccinellidae, tribe Coccinellini) were evaluated in the laboratory on a common prey, the spirea aphid, Aphis citricola van der Goot (Homoptera: Aphididae), and on the twospotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae), a prey previously unrecorded for these two predators. The experiments were carried out in the laboratory on apple saplings (Malus domestica Borkhausen). Adult males and females of H. axyridis consumed significantly more mites than adults of C. septempunctata. For H. axyridis, males consumed 41.3 spider mites in 24 h and females 48.4, whereas for C. septempunctata males consumed 14.1 prey and females 15.2. The consumption of spirea aphids by the males was similar for the two species. Consumption by the females was significantly greater for H. axyridis (46.5) than for C. septempunctata (22.2). The two coccinellids showed a significant preference for A. citricola in the presence of T. urticae. This preference was more pronounced for C. septempunctata. The total number of prey consumed and the percentage of exploited biomass decreased significantly for C. septempunctata and stayed relatively constant for H. axyridis as the number of mites increased in the prey ratio. Our results suggest that T. urticae is only an alternative prey for both predators, and that H. axyridis should be more efficient than C. septempunctata in a prey assemblage with aphids and mites.

Can Developmental and Behavioral Characteristics of the Multicolored Asian Lady Beetle Harmonia Axyridis Explain its Invasive Success

Major impacts of biological invasions are widely recognized and underscore the need to understand the relation between life-history traits of invasive species and the invasion process. Growth of juveniles and adult survival of invasive species are key factors in invasion process. Life-history traits that increase juvenile fitness including increased rates of development and behavioral characteristics that facilitate competitive success such as increased predator efficiency and foraging ability may explain invasiveness of a species. Invasion of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in North America provides an opportunity to investigate life-history traits of juveniles of an invasive species. Here, we evaluate both developmental and behavioral traits that may explain the success of H. axyridis by comparing it to an ecologically similar indigenous species Coleomegilla maculata lengi Timberlake (Coleoptera: Coccinellidae). Three points may contribute to the invasiveness of H. axyridis. First, development of H. axyridis was faster during the 2nd larval instar than C. maculata, a characteristic that may reduce vulnerability at young instars. Second, H. axyridis reached the 4th instar more rapidly than C. maculata. The 4th instar of H. axyridis was also characterized by higher predation efficiency with increased voracity, lethal contact and search efficiency of pea aphids Acyrthosiphon pisum. Finally, surprisingly, a 5th larval instar occured in 33% of the individuals of H. axyridis and was characterized by the same developmental time, but with increased voracity and weight gain compared to 4th larval instars, suggesting an increased fitness of these individuals. These developmental characteristics coupled with increased predation efficiency and behavioral characteristics enhanced the juvenile growth and predatory abilities of this species and may contribute to the invasive ability of H. axyridis.

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.

Instar-specific defense ofColeomegilla maculata lengi (Col.: Coccinellidae): Influence on attack success of the intraguild predatorChrysoperla rufilabris (Neur.: Chrysopidae)

We conducted a laboratory study of the behavioural interactions between larval stages of the lady beetleColeomegilla maculata lengi Timberlake and an intraguild predator, the lacewingChrysoperla rufilabris Burmeister. Ladybird susceptibility to predation by third instarC. rufilabris is age-specific and influenced by larval defensive strategies. First and second instars ofC. maculata were captured more consistently by chrysopid larvae than third and fourth instars. Young coccinellids generally exhibit escape reactions (dropping, fleeing, retreating) but, do not survive after being caught by lacewings. In addition to escape reactions, older larvae may actively defend themselves by wriggling or biting, even after being pierced. The proportion of physical interactions that resulted in coccinellid death was significantly lower for older instars (<2%) than for first (35%) and second (19%) instars. Capture efficiency byC. rufilabris was related to the coccinellid-chrysopid size ratio. Dropping off the leaves, the most common defensive behaviour displayed by coccinellid larvae, contributed to reduce overall mortality of first instars to a level similar to the one observed for older stages. However, lacewings were able to prevent coccinellid dropping by impaling and holding their prey in the air, or by falling with the ladybirds to the ground where they continued their attack.RésuméLe comportement des différents stades larvaires de la coccinelleColeomegilla maculata lengi Timberlake a été étudié en laboratoire lors de confrontations avec un prédateur intraguilde soit le chrysopeChrysoperla rufilabris Burmeister. La susceptibilité des larves de coccinelle décroit avec l’âge et dépend des stratégies défensives utilisées par la larve. Les larves de stades I et II étaient capturées significativement plus souvent par le chrysope que les larves de stades III et IV. A l’approche d’un chrysope, les jeunes stades démontraient généralement une réaction d’évitement (chute, fuite ou retraite) et ne survivaient pas après avoir été capturés. Les larves plus âgées utilisent, outre les comportements d’évitement, une stratégie défensive plus aggressive en se contorsionnant ou en mordant le chrysope. La proportion de contacts causant la mort de la coccinelle s’avérait moindre pour les stades âgés (<2 %), que pour les premiers (35 %) et seconds stades larvaires (19 %). L’efficacité de capture deC. rufilabris était reliée au ratio de taille coccinelle/chrysope. La chute, lorsqu’elle était possible, constituait la principale défense employée par tous les stades. Elle permettait au premier stade larvaire de diminuer sa mortalité à un niveau comparable aux stades plus avancés. Néanmoins, à plusieurs occasions, le chrysope est parvenu à contourner cette défense en maintenant la coccinelle dans les airs, ou en se laissant tomber avec elle, pour poursuivre l’attaque au sol.

Prey Selection by the Lady Beetle Harmonia axyridis : The Influence of Prey Mobility and Prey Species

The influence of prey mobility and species on prey selection by the coccinellid Harmonia axyridis Pallas was determined under laboratory conditions for two prey species, Hyaliodes vitripennis (Say) and Tetranychus urticae Koch. Prey selection was influenced by prey mobility. In the presence of active prey, the coccinellid selected T. urticae while in presence of immobilized prey, H. vitripennis was preferred. Harmonia axyridis searching time was longer in the presence of active H. vitripennis than in the presence of active T. urticae. Moreover, the coccinellid capture rate was lower for active H. vitripennis caused by effective defensive mechanisms. Prey suitability was affected by prey mobility and species. Immobilized H. vitripennis were the most profitable prey, i.e. induced a shorter developmental time and no mortality. However, active H. vitripennis were not a suitable food source for H. axyridis. Our results suggested that three factors are involved in prey selection by H. axyridis: (i) prey mobility; (ii) prey defensive mechanisms; and (iii) prey species.

A fox in sheep's clothing : furtive predators benefit from the communal defense of their prey

Many animals live in temporary or permanent groups, either as gregarious or social species, to reduce predation risk. The solitary midge, Aphidoletes aphidimyza, preys specifically on aphids and spends its entire larval development within a prey colony where it is susceptible to intraguild predation. We hypothesized that midge larvae profit from a dilution effect produced by aphids which enhances their chances of survival. We examined the defensive behaviors of aphids in response to foraging midges, and investigated the effect of aphid density on the predation risk of A. aphidimyza by the lacewing Chrysoperla rufilabris. We found that a foraging midge displays furtive hunting behavior which triggers little defensive reaction by aphids, and does not stimulate significant disturbance of the gregarious prey. Within the aphid colony the midge benefits from a dilution effect which reduces the incidence of predation by lacewing larvae. However, the effectiveness of such a mechanism is determined by the level of disturbance caused by foraging intraguild predators. Large lacewing larvae tend to dislodge aphids from their feeding sites, thereby eliminating the dilution effect. We conclude that prey not only provide food to midge larvae, but also protection against natural enemies.

Selection of Molting and Pupation Sites by Coleomegilla maculata (Coleoptera: Coccinellidae): Avoidance of Intraguild Predation

Abstract Molting and pupating insects are especially vulnerable to natural enemies and one possible component of their defensive strategy is the selection of suitable microhabitats. We hypothesized that larvae of the lady beetle Coleomegilla maculata lengi Timberlake select molting and pupation sites that effectively reduce their susceptibility to intraguild predation. We characterized microsites on potato plants and evaluated their associated risk of predation by the lacewing Chrysoperla rufilabris Burmeister (Neuroptera: Chrysopidae), a common intraguild predator. The majority of molts (>60%) occurred on potato plants in sites similar to those used by mobile coccinellid larvae. In contrast, 90% of the larvae left the plant to pupate. Second, third, and fourth instars selected artificial shelters for both molting and pupation when these were available. Vulnerability of pupae and newly molted larvae to lacewing larvae depended on plant microsite, with leaves supporting an aphid colony as the most risky sites. Molting and pupating microhabitat selection by coccinellid larvae appears to be a trade-off between the advantages of remaining close to the aphid resource, and the costs of being exposed to intraguild predators.

Biological and mechanical control of Sitophilus oryzae (Coleoptera: Curculionidae) in rice

The combination of mechanical and biological methods was evaluated in the laboratory to assess their impact on the rice weevil Sitophilus oryzae in rice. Mechanical methods comprising the conventional polishing process applied either before or after infestation, resulting in reduced nutritional quality plus the added effect of mechanical impact in the presence of the pest, biological methods including parasitism by the pteromalids Anisopteromalus calandrae and Lariophagus distinguendus, and combined methods (combinations of mechanical and subsequent biological treatments), were tested in the laboratory. All treatments significantly reduced the number of weevil progeny and individual weevil weight. Of the two parasitoids, L. distinguendus had the greater effect, reducing weevil populations by 98% in unpolished rice. In the combined treatments, parasitism increased the effect of mechanical methods. However, mechanical methods had a detrimental impact on parasitoid survival, especially in A. calandrae. Furthermore, in the presence of mechanical treatments, the sex ratio of A. calandrae was unbalanced in favour of males indicating the high vulnerability of females. The impact of both parasitoid species on weevils was attributed to successful parasitism as well as to aborted parasitism and host-feeding.

Teratocytes growth pattern reflects host suitability in a host–parasitoid assemblage

Abstract In some parasitoid species, the serosa membrane breaks apart at hatching and produces teratocyte cells that assume various functions (immunossupression, secretion and nutrition) mediating host–parasitoid relationships. Teratocyte growth pattern may thus reflect the host suitability for a parasitoid. The teratocyte growth pattern (increase in size and number of teratocytes as a function of time) is studied and used as an indirect measure of fitness to compare the development of the endoparasitoid Dinocampus coccinellae in a marginal host, the coccinellid Harmonia axyridis, and in a suitable host, Coleomegilla maculata. Indirect measures of fitness recorded in both host species confirm that C. maculata is a suitable host for D. coccinellae contrary to the marginal host H. axyridis. According to regression analysis, teratocyte numbers decrease linearly whereas teratocyte size increases linearly with time in the suitable host C. maculata (larvae or adults). In the marginal host, parasitism occurs only in the larval stage where a delay in the parasitoid larval development is observed. Increase in teratocyte size is also highly variable. The teratocyte growth pattern of the parasitoid in the marginal host does not follow the linear model found in the suitable host. Teratocyte growth pattern may be a useful criterion to evaluate host‐suitability and host range of parasitoids.