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.     

Contrasting population growth parameters of the aphidophagous Scymnus nubilus and the coccidophagous Nephus reunioni

Compared to coccidophagous ladybirds, aphidophagous ladybirds develop and live faster. They also produce more eggs at a faster rate. As we wanted to know how these traits influence population dynamics, we have determined the population growth parameters for the aphidophagous Scymnus nubilus Mulsant (Coleoptera: Coccinellidae) and the coccidophagous Nephus reunioni Fürsch (Coleoptera: Coccinellidae) fed Rhopalosiphum padi (L.) (Hemiptera: Aphidoidea) and Planococccus citri (Risso) (Hemiptera: Coccoidea) respectively under controlled laboratory conditions. Net reproductive rate, intrinsic rate of natural increase, and finite rate of increase were all significantly higher, and generation time and doubling time were both significantly shorter in S. nubilus compared to N. reunioni. The reproductive output of the aphidophagous species rapidly reaches a peak and then sharply declines while it is regularly distributed throughout adult life in the coccidophagous predator. A significant difference in late survival was found, with S. nubilus exhibiting higher survival. Adaptation to the consumption of aphids and coccids occurred in several species during the co-evolutionary history of ladybird beetles and their prey. Thus, comparing other species would be valuable to confirm the differences reported here.     

Body size and resource partitioning in ladybirds

Aphidophagous insects all exploit aphids as food, but there appears to be no association between the size of the aphidophagous predator and that of the species or the age structure of the aphid colonies they exploit. Aphid colonies generally increase, peak and decline in abundance, and are exploited by a sequence of predators, which is consistent from year to year. The objective of this study was to determine the rules underlying this temporal pattern. For example, in the field, aphid colonies are often first attacked by a small and then a larger species of ladybird. Theory based on the geometry and physiology of ladybirds predicts that the quantity of food required for oviposition and the area searched per unit time should scale with body weight, with exponents of 1 and 0.66, respectively. An analysis of empirical data supports these predictions. Thus, in relative terms a 35 mg ladybird requires 1.5 times more aphids per unit area for oviposition than a 10 mg ladybird. That is, the temporal pattern in oviposition is possibly mainly determined by geometrical and physiological constraints associated with body size, with small species of ladybird able to lay eggs at lower aphid population densities than large species. Cannibalism is thought to be the mechanism by which these predators are able to coexist.     

Does the satiation hypothesis account for the differences in efficacy of coccidophagous and aphidophagous ladybird beetles in biological control? A test with Adalia bipunctata and Cryptolaemus montrouzieri

Mills (1982) formulated the satiationhypothesis in order to explain why ladybirdsare generally more effective in the biologicalcontrol of coccids than of aphids:aphidophagous ladybirds are supposedly lessefficient because they become more rapidlysatiated than coccidophagous ladybirds. If thisis true, the former should spend less timeeating than the latter. This hypothesis istested in this study using the coccidophagousCryptolaemus montrouzieri Mulsant(Coleoptera: Coccinellidae) and theaphidophagous Adalia bipunctata (L.) (Coleoptera: Coccinellidae). Contrary to Mills'(1982) prediction the coccidophagous ladybirddid not feed continuously and even spent lesstime feeding than the aphidophagous ladybird.Furthermore, the gut capacity of C. montrouzieri is smaller than that of A. bipunctata.     

Interactions between ants and aphidophagous and coccidophagous ladybirds

Aphidophagous and coccidophagous coccinellids come into conflict with homopteran-tending ants for access to food. Antagonistic interactions between coccinellids and ants may be competitive or non-competitive. Competitive interactions occur when coccinellids attack aphids or coccids that are being tended by ants for honeydew. Non-competitive interactions include all interactions away from ant-tended homopteran colonies. We here review observations and studies of such interactions. We note that most competitive interactions occur at times when untended aphids/coccids are scarce. We describe the chemical and physical defences that coccinellids use against ant aggression and consider whether these have evolved as general anti-predator deterrents or specifically in response to ants. Myrmecophilous coccinellids are then considered, with particular focus on the two most studied species, Coccinella magnifica and Platynaspis luteorubra. We note that the myrmecophily of the two species has the same adaptive rationale—to enable the ladybirds to prey on ant-tended aphids at times of aphid scarcity—but that it is based on different traits to facilitate life with ants. Finally, we consider the role of ants in the evolution of habitat specialisation in some coccinellids.     

Aphid and ladybird beetle abundance depend on the interaction of spatial effects and genotypic diversity

Intraspecific variation and genotypic diversity of host-plants can affect the structure of associated arthropod communities and the dynamics of populations. Similarly, neighboring plants can also affect interactions between host-plants and their associated arthropods. However, most studies on the effects of host-plant genotypes have largely ignored the potential effects of neighboring host-plants on arthropod communities. In this study, we used a common garden experiment to ask how spatial effects of neighboring patches, along with genotype identity and genotypic diversity in tall goldenrod (Solidago altissima), affect the abundances of a common goldenrod herbivore (Uroleucon nigrotuberculatum) and their dominant predator (Harmonia axyridis, a ladybird beetle). Aphid abundance varied 80-fold among genotypes, while ladybird beetle abundance was not affected by genotype identity. Additionally, there were strong effects of neighboring plots: aphid abundance in a focal plot was positively correlated to aphid abundance in nearby plots, suggesting strong spatial patterning in the abundance of aphids. Neither aphid nor ladybird beetle abundance was affected by genotypic diversity. However, focal plot genotypic diversity mediated the strength of the neighborhood effect (i.e., strong effects for genotype polyculture focal plots and weak effects for genotype monoculture focal plots). Our results show that aphids were directly influenced by host-plant genotype identity while ladybird beetles responded mainly to prey abundance, and suggest that genotypic diversity can influence the effects of spatial processes on the plant-herbivore interactions.     

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.     

Weak responses to dietary enrichment in a specialized aphid predator

Some ladybeetles are specialist predators of aphids, coccids or other prey, although they often eat a variety of species from their focal prey taxon. In addition, the diet is often supplemented with alternative prey. How larvae of the aphidophagous Coccinella septempunctata L. utilize a non‐aphid alternative prey (fruit‐fly larvae Drosophila melonogaster Meigen) is compared with adequate (i.e. high‐quality) aphid prey provided alone (monotypic diet) or in mixed diets. The alternative prey are presented either nutrient‐enriched (i.e. raised on dog food supplemented medium) or not (raised on pure medium). Ladybird performance (survival, growth and development) is poor on the pure fly larvae diets, and also reduced when given mixed diets compared with the pure aphid diet. Nutrient enrichment of the fly larvae has no positive effects. The physiological background for the differences in food value, as indicated by performance in life‐history parameters, is a strong pre‐ingestive effect (i.e. reduced consumption of fly larvae compared with aphids) and a post‐ingestive effect (i.e. reduced utilization of assimilated larval fly tissue), whereas the assimilation efficiency of the consumed fly larvae is as high as that of aphids. The results show a physiological trade‐off resulting from prey specialization that reduces the possibility of utilizing alternative prey when the availability of aphids is scarce. Connected with this is a high robustness against variation in prey nutrient diversity and composition; the ladybird shows little positive response to dietary mixing (i.e. neither mixing of adequate aphids, nor of aphids and alternative prey) or to nutrient enrichment of prey. This contrasts with the results from generalist predators (spiders), where similar treatments lead to strong effects on life‐history parameters.     

Effects of prey aphid species on the abundance of a parasitoid and two predator species in aphid colonies attended by ants on citrus

This study focused on three species of enemies, the parasitoid wasp Lysiphlebus japonicus Ashmead (Hymenoptera: Aphidiidae), the ladybird Scymnus posticalis Sicard (Coleoptera: Coccinellidae) and the predatory gall midge Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), all of which are able to exploit aphids attended by ants. I experimentally evaluated the effects of prey aphid species on the abundance of each of the three enemy species in ant‐attended aphid colonies on citrus. The aphids compared were Aphis gossypii Glover versus Aphis spiraecola Patch in late spring, and Toxoptera citricidus (Kirkaldy) versus A. spiraecola in late summer (all, Hemiptera: Aphididae). Colonies of the three aphid species were attended by the ant Pristomyrmex punctatus Smith (Hymenoptera: Formicidae). The initial number of attending ants per individual aphid did not differ significantly between the colonies of the two aphid species compared in each season. Between A. gossypii and A. spiraecola, there was no significant difference in the number of mummies formed by the parasitoid or foraging larvae of each of the two predators per aphid colony. A significant difference was detected between T. citricidus and A. spiraecola for each of the three enemy species, with a far greater number of L. japonicus mummies in T. citricidus colonies and distinctly more larvae of each of the two predators in A. spiraecola colonies. Thus, the abundance of each of the three enemy species in ant‐attended aphid colonies was significantly influenced by the species of the prey aphids, with the three enemies showing different responses to the three aphid species.     

Intraguild interactions of aphidophagous predators in fields: effect of Coccinella septempunctata and Episyrphus balteatus occurrence on aphid infested plants

Intraguild relations between beneficial insects have become a major research topic in biological pest control. In order to understand the intraguild competitions between aphidophagous populations in natural conditions, a field experiment was carried out in the experimental farm of the Gembloux Agricultural University. As biological control of pests involve a community of diverse natural enemies, this experiment firstly aimed to assess the aphidophagous predator diversity and abundance in green pea (Pisum sativum) field and secondly to investigate the impact of the large natural occurrence of C. septempunctata on the aphidophagous beneficial dispersion and efficiency as aphid biological control agents in pea field. Visual observations were weekly performed throughout the 2006 growing season. The pea aphids were attacked by several predatory groups, mainly ladybird beetles and hoverflies. Higher densities of ladybirds and hoverflies were recorded in the beginning of July, associated with an aphid occurrence peak. Using net cage system in the field, the particular intraguild relations between added C. septempunctata or E. balteatus and the natural beneficial arrivals and dispersion were observed. The E. batteatus (eggs and larvae) presence inhibited other aphidophagous predators presence on the aphid infested plants. Lower abundance of E. balteatus was observed on aphid infested plants already colonised by C. septempunctata. To explore more accurately the oviposition and predation behaviours of ladybirds and hoverflies and to determine the chemical factors that could influence these behaviours, current researches are performed in laboratory and will be discussed to promote efficient biological control of aphids by natural enemies.     

Effects of mixed prey on the development and demographic attributes of a generalist predator,Coccinella septempunctata (Coleoptera: Coccinellidae)

Coccinella septempunctata Linnaeus, 1758 (Coleoptera: Coccinellidae) is an aphidophagous ladybird beetle species with cosmopolitan distribution. However, it may also thrive on arthropods other than aphids, when the latter are not readily available. Certain life history traits and demographic attributes of C. septempunctata were determined using seven different diets with different alternations and proportions of an aphid, Lipaphis erysimi (Kaltenbach,1843) and a mite, Tetranychus urticae Koch, 1836, in the laboratory (at 25±0.5°C, 65±5% RH and a photoperiod of 16 h L:8 h D).The larval duration was longest (12.61±6.17 days) when fed an alternating diet of two days aphid/two days mite. Adult longevity was longest (78.65±1.09 days) when fed aphids only and shortest (3.17±1.25 days) when fed mites only. Life expectancy (e_x) was highest (111 days) when adults were fed only aphids and lowest (11.3 days) when fed only mites. Survival rates of ladybird beetles were positively related to an increasing ratio of aphids in their diet. Their ability to prey on both aphids and mites indicates the effectiveness of C. septempunctata as a biological control agent on plants infested with these two pests.     

The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain

Abstract.  1. The harlequin ladybird, Harmonia axyridis , has recently arrived in Britain.
2. This species has been introduced from Asia into many parts of the world for biological control purposes.
3. In many parts of North America it has become the predominant aphidophagous coccinellid in less than 20 years, and in north-western Europe it is spreading and increasing in number rapidly.
4. Since establishment in North America and continental Europe, reports of its effectiveness as a biological control agent of aphids and coccids have been accompanied by accounts of negative effects on other aphidophagous species and humans.
5. Here the potential impacts of the arrival of the harlequin ladybird in Britain are assessed.     

Overlapping oviposition and chemical defense of eggs in two co-occurring species of ladybird predators of aphids

Oviposition behavior in two co-occurring species of predatory ladybirds of aphids were investigated. The two species of beetles often shared the same aphid colonies in bean plants in space and time and showed a similar oviposition pattern in response to aphid abundance. Overlapping oviposition presents potential risks of interspecific predation of eggs in unstable aphid colonies. Eggs in clusters by two ladybird species, Menochilus sexmaculatus and Coccinella transversalis, were defended from reciprocal predation and the defense was found to be chemical. Eggs occurring singly were found to be highly vulnerable to predation. Strength of chemical defense significantly increased from single eggs to eggs in mixed clusters and eggs in pure clusters. Results are not only consistent with the hypothesis that eggs in clusters are better protected from natural enemies but also extend the ambit of the hypothesis that coexisting ladybird predators have evolved to avoid the risks of heterospecific predation of eggs in a patch. Received: September 11, 2000 / Accepted: November 13, 2000     

Effect of stinging nettle habitats on aphidophagous predators and parasitoids in wheat and green pea fields with special attention to the invader Harmonia axyridis Pallas (Coleoptera: Coccinellidae)

The relative occurrence and seasonal abundance of aphids and their natural enemies were visually assessed between May and July 2005–2006 in four types of habitats located in Gembloux (Namur province, Belgium): green pea, wheat and stinging nettle either planted in or naturally growing in woodland adjacent to these crops. Results showed that: (i) Acyrthosiphon pisum Harris, Sitobion avenae F. and Microlophium carnosum Buckton were the most common aphid species, respectively, on green pea, wheat and stinging nettle either in or near field crops; (ii) stinging nettle and field crops shared several important aphidophagous insect species such as the ladybird Coccinella septempunctata L., hoverfly Episyrphus balteatus De Geer and braconid wasp Aphidius ervi Haliday; (iii) the shared beneficial species were typically recorded earlier on stinging nettles than on crops; and (iv) the spatial occurrence of the invasive ladybird Harmonia axyridis Pallas was distinctly associated with stinging nettles, particularly in 2005. Stinging nettles and field crops partially coincide in time, enabling the movement of natural enemies among them. These findings suggest that the presence of stinging nettles in landscapes seems to enhance the local density of aphidophagous insect communities necessary for aphid biocontrol in field crops.     

Why do neonates of aphidophagous ladybird beetles preferentially consume conspecific eggs in presence of aphids?

The neonates of aphidophagous ladybird beetles, Propylea dissecta, Coccinella transversalis and Coelophora saucia preferentially consumed conspecific eggs in presence of essential aphid prey, Aphis gossypii. This preference was strongest in P. dissecta and recorded in all density combinations of conspecific eggs and aphids. The neonates of all three species developed faster resulting in heavier second instars with lower mortality when fed on conspecific eggs as compared to mobile or defenceless aphids. In addition, they required less dry biomass of conspecific eggs than that of aphids. These results reveal that neonates are benefitted intrinsically when they feed on conspecific eggs. The neonates of P. dissecta exhibited discrimination for more nutritious food, as they contacted and ate conspecific eggs more frequently than aphids as their first meal. This discrimination was not found in Coccinella transversalis and Coelophora saucia possibly due to their bigger sizes and possible higher energy requirements. Although, the major effect of chemical cues was only noticed in P. dissecta, it could be concluded that chemicals (surface and within) of conspecific eggs possibly attract neonates for egg-cannibalism, as both eggs and aphids were consumed in greater numbers when coated with egg extracts. The reverse occurred when eggs and aphids were coated with aphid extracts.     

Influence of host density and population structure on egg production in the coccidophagous ladybird,Chilocorus nigritus F. (Coleoptera: Coccinellidae)

1 Studies on aphidophagous coccinellids have indicated that patch quality, and, in particular, the age structure of the prey or the phenological age of the plant, may play an important role in stimulating oviposition behaviour. However, little is known about the egg‐laying tactics of coccidophagous species. 2 When restricted to a single, large colony of overlapping generations of their diaspid host Abgrallaspis cyanophylli (Signoret), adult females of the coccidophagous ladybird Chilocorus nigritus F. varied their egg production rate in a cyclic pattern that lasted for approximately 22 days. This information was used to generate hypotheses relating to eliciting cues for oviposition. 3 Two experiments were carried out in the absence of conspecific larvae to assess: (i) whether changes in host density at levels above those needed to sustain egg production in the females affected egg output and (ii) the effect of restricting beetles to various homogeneous prey population structures on daily egg production. 4 Changes in host density caused a significant but transient decline in egg production whereas a heterogeneous prey population elicited significantly higher levels of oviposition than homogeneous ones with similar host densities, irrespective of the growth stage of the prey. 5 Beetles were fed to satiation throughout the experiments but the data obtained suggest that cues for eliciting oviposition operated in a density‐dependent fashion. The results of the study are used to discuss the possibility that visual and chemical cues are quantitatively used by ovipositing beetles to assess patch suitability.     

Effect of cannibalism and predation on the larval performance of two ladybird beetles

The relative impact of cannibalism and predation on the development and survival of fourth instar larvae was assessed in two species of aphidophagous ladybird beetles, Coccinella septempunctata and Harmonia axyridis. The effect of eating aphids, conspecific larvae or heterospecific larvae on larval performance differed in the two species: aphids were the best food for C. septempunctata and survival of C. septempunctata larvae was significantly lower when offered heterospecific larvae rather than conspecific larvae or aphids as food, indicating that H. axyridis larvae were not suitable food for C. septempunctata. However, as the different foods did not affect the larval performance of H. axyridis, this species appears to be more polyphagous. Both intraguild predation by the aggressive larvae of H. axyridis and the polyphagous food habit of this species may account for its dominance in ladybird assemblages and its displacing other ladybird beetles in several places in the world.     

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.     

Physiological mechanism governing slow and fast development in predatory ladybirds

Aphidophagous and coccidophagous ladybirds, similar to their prey, show marked differences in their pace of life (Dixon, 2000), in particular in their rate of development, with all stages of aphidophagous species developing much faster than those of coccidophagous species. Two hypotheses are proposed to account for the large difference in the pace of life of these two groups. These are that differences in the rate of development are a result of differences in lower temperature thresholds for development or the quality of their respective prey as food (Dixon et al., 2011). Analysis of published results on the rates of development of the eggs of ladybirds indicates that the inverse relationships between the number of day‐degrees required for development (K) and the lower temperature threshold for development (td_min) of these two groups are significantly different. In particular, the respective td_min overlap and K of the aphidophagous and coccidophagous species with a similar td_min are, on average, 38 and 117 day‐degrees (D^o). The relationship between the rate of development (R) and temperature (T) for aphids reared on poor‐ or high‐quality foods indicates that, although the value of td_min of a species depends on food quality, K does not, showing that it is unlikely that K is governed by food quality. Thus, there is little support for differences in either the td_min or food quality governing the difference in the pace of life of these two groups of ladybirds. The results indicate that the physiological mechanism that may govern the difference in the pace of life between these two groups is the number of day‐degrees (K) needed to complete their development. The possible evolutionary reason for this is discussed.     

Discrimination of parasitized aphids by a hoverfly predator: effects on larval performance, foraging, and oviposition behavior

The choice of oviposition site by female aphidophagous predators is crucial for offspring performance, especially in hoverflies whose newly hatched larvae are unable to move over large distance. Predator and parasitoid interactions within the aphidophagous guild are likely to be very important in influencing the choices made by predatory hoverfly females. In the present study, the foraging and oviposition behavior of the aphidophagous hoverfly Episyrphus balteatus DeGeer (Diptera: Syrphidae) was investigated with respect to the parasitized state of its aphid prey, Acyrthosiphon pisum Harris (Homoptera: Aphididae), that were parasitized by Aphidius ervi Haliday (Hymenoptera: Aphidiidae). We also recorded the number of eggs laid by hoverfly females when subjected to parasitized aphids. Furthermore, we studied the influence of being fed with parasitized aphids on hoverfly larval performance. Hoverfly females did not exhibit any preference for plants infested with unparasitized or aphids parasitized for 7 days. On the other hand, plants infested with mummies or exuvia were less attractive for E. balteatus . These results were correlated with (i) the number of eggs laid by E. balteatus females and (ii) larval performance. Thus, our results demonstrate that E. balteatus behavior is affected by parasitoid presence through their exploitation of aphid colonies. Indeed, hoverfly predators select their prey according to the developmental state of the parasitoid larvae.