Does Mutual Interference Affect the Feeding Rate of Aphidophagous Coccinellids? A Modeling Perspective

Mutual interference involves direct interactions between individuals of the same species that may alter their foraging success. Larvae of aphidophagous coccinellids typically stay within a patch during their lifetime, displaying remarkable aggregation to their prey. Thus, as larvae are exposed to each other, frequent encounters may affect their foraging success. A study was initiated in order to determine the effect of mutual interference in the coccinellids’ feeding rate. One to four 4^th larval instars of the fourteen-spotted ladybird beetle Propylea quatuordecimpunctata were exposed for 6 hours into plastic containers with different densities of the black bean aphid, Aphis fabae, on potted Vicia faba plants. The data were used to fit a purely prey-dependent Holling type II model and its alternatives which account for interference competition and have thus far been underutilized, i.e. the Beddington-DeAngelis, the Crowley-Martin and a modified Hassell-Varley model. The Crowley-Martin mechanistic model appeared to be slightly better among the competing models. The results showed that although the feeding rate became approximately independent of predator density at high prey density, some predator dependence in the coccinellid’s functional response was observed at the low prey—high predator density combination. It appears that at low prey densities, digestion breaks are negligible so that the predators do waste time interfering with each other, whereas at high prey densities time loss during digestion breaks may fully accommodate the cost of interference, so that the time cost may be negligible.     

Predation rate and numerical response of Aphidoletes aphidimyza feeding on different densities of Aphis craccivora

Predation rate and numerical response are basic to any investigation of predator–prey relationships and key components in the selection of predators for biological control. The density-dependent predation rate and numerical response of Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae) to varying densities (5, 10, 20, 40, 60 and 80) of third-instar Aphis craccivora (Koch) (Hemiptera: Aphididae), were studied in laboratory conditions [23±1°C, 70 ± 5% relative humidity (RH), and a photoperiod of 16:8 h L:D. Predation rate data were analysed using the age-stage, two-sex consumption rate software. Net consumption rate (C₀) increased by increasing prey density. The lowest and highest net consumption rates were 20.75 and 190.8 prey nymphs at densities of 5 and 80 A. craccivora. The transformation rate from prey population to predator offspring (Q_p) increased by increasing prey density. The reproductive numerical response, in terms of eggs laid, increased curvilinearly with increasing prey density. Females laid 121.375 ± 4.301 eggs when exposed to the highest prey density (80) and 52.5 ± 1.544 eggs at lowest prey density (5). It can be concluded that different densities of A. craccivora influenced the reproductive performance of A. aphidimyza in terms of predation rate and numerical response.     

Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus

Introductions of the harlequin ladybird Harmonia axyridis into Belgium for aphid biological control have been followed by declines in native aphid natural enemies. We first examined, in laboratory and field conditions, the impact of larval mobility of either H. axyridis or Episyrphus balteatus, the most abundant native hoverfly in central Europe, on aphid suppression. The hoverfly larvae consumed more aphids (Megoura viciae) in a short term, whereas the ladybird ones were more efficient in a long term. We second investigated the intraguild interactions between H. axyridis and E. balteatus larvae and adults. In larva pairings between the two species in laboratory microcosms containing aphid (M. viciae) infested broad bean (Vicia faba) plants, H. axyridis had an intraguild predation (IGP) advantage over the hoverfly. When conspecific larvae were paired together on aphid‐infested plants, no cannibalism between them was detected. The presence of either H. axyridis or E. balteatus larvae on aphid‐infested plants negatively influenced the ovipositional behaviour of H. axyridis and E. balteatus females; lower numbers of laid eggs were recorded compared to control treatment. Moreover, eggs laid by E. balteatus females were also dropped as victims of predation mainly by H. axyridis larvae. Our results suggest that while the exotic ladybird was more efficient in aphid biological control, larvae and eggs of the native hoverfly species face increased IGP by H. axyridis, which would contribute, as a consequence, to the decline in E. balteatus population following invasion.     

Functional response of Euseius concordis to densities of different developmental stages of the cassava green mite

Both prey density and developmental stage of pests and natural enemies are known to influence the effectiveness of biological control. However, little is known about the interaction between prey density and population structure on predation and fecundity of generalist predatory mites. Here, we evaluated the functional response (number of prey eaten by predator in relation to prey density) of adult females and nymphs of the generalist predatory mite Euseius concordis to densities of different developmental stages of the cassava green mite Mononychellus tanajoa, as well as the fecundity of adult females of the predator. We further assessed the instantaneous rate of increase, based on fecundity and mortality, of E. concordis fed on eggs, immatures and adults of M. tanajoa. Overall, nymphs and adults of E. concordis feeding on eggs, immatures and females of M. tanajoa had a type III functional response curve suggesting that the predator increased prey consumption rate as prey density increased. Both nymphs and adult females of the predator consumed more eggs than immatures of M. tanajoa from the density of 20 items per leaf disc onwards, revealing an interaction between prey density and developmental stage in the predatory activity of E. concordis. In addition, population growth rate was higher when the predator fed on eggs and immatures in comparison with females. Altogether our results suggest that E. concordis may be a good candidate for the biological control of M. tanajoa populations. However, the efficiency of E. concordis as a biological control agent of M. tanajoa is contingent on prey density and population structure.     

Intraguild Predation among the Hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and Other Aphidophagous Predators

Aphidophagous predators compete for the same prey species. During their foraging activity they frequently encounter heterospecific aphid predators. These situations can lead to intraguild predation and may disrupt biological control efforts against aphids where more than one predator species is present. We investigated the behavior of larvae of the hoverfly Episyrphus balteatus de Geer and its interaction with three other aphid predators: the ladybird Coccinella septempunctata L., the lacewing Chrysoperla carnea Stephens, and the gall midge Aphidoletes aphidimyza (Rondani). Interspecific interactions between predators were examined in arenas of different sizes and in the presence of extraguild prey. The outcome of interactions between E. balteatus larvae and the other predators depended predominantly on the relative body size of the competitors. Relatively large individuals acted as intraguild predators, while relatively smaller individuals became intraguild prey. Eggs and first- as well as second-instar larvae of E. balteatus were highly susceptible to predation by all other predators, whereas pupae of E. balteatus were preyed upon only by the larvae of C. carnea. Interactions between A. aphidimyza and E. balteatus were asymmetric and always favored the latter. Eggs and first- as well as second-instar larvae of E. balteatus sustained intraguild predation irrespective of the size of the arena or the presence of extraguild prey. However, the frequency of predation on third-instar larvae of E. balteatus was significantly reduced. This study indicated that the same species can be both intraguild predator and intraguild prey. It is suggested that combinations of predators must be carefully chosen for success in biological control of aphids.     

Predator-prey responses in an acarine system

Summary This study examines the responses of the predatory mite,Phytoseiulus persimilis, to the density and distribution of its prey,Tetranychus urticae. It is divided into three parts. Firstly, the functional responses of protonymph, deutonymph and adult females towards different prey stages are displayed. The great majority of the responses are of the type II form, and the variations in the values of attack ratea′ and handling timeT _h are discussed. Experiments are then described in which individual protonymph, deutonymph and adult female predators are presented with varying ratios of two prey age-classes (eggs and deutonymphs, and larvae and deutonymphs). Any observed preference for one of the prey stages is discussed in relation to the predicted preference on the basis of the separate functional response experiments. Finally, the response of different densities of adult female predators to a non-random distribution of deutonymph prey on bean leaflets is examined. The predators show a clear tendency to aggregate on the leaflets of high prey density, counteracted to some extent by interference increasing the probability of dispersal to other leaflets.     

Numerical response of ladybird beetles (Col., Coccinellidae) to aphid prey (Hom., Aphididae) in a field bean in north-east India

Two predaceous species of Coccinellidae, Menochilus sexmaculatus and Coccinella transversalis , occurred abundantly in bean crops infested with the aphid, Aphis craccivora Koch in north-east India. The number of eggs and adults of the two coccinellids increased in response to the increase in the population of aphid prey. Reproductive numerical responses were found to be synchronous to prey density whereas aggregative numerical responses appeared asynchronous in the later part of the aphid cycle on beans. Menochilus sexmaculatus oviposited smaller clusters of eggs at lower density of aphids than C. transversalis which laid larger clusters and showed greater numerical response at higher densities of aphids. Within a species cluster the size of the eggs seems to be directly related to aphid density. The two coccinellid species of this study seem to be efficient predators of A. craccivora in terms of their reproductive and aggregative numerical responses.     

Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management

Trichome-based tomato resistance offers the potential to reduce pesticide use, but its compatibility with biological control remains poorly understood. We evaluated Episyrphus balteatus De Geer (Diptera, Syrphidae), an efficient aphidophagous predator, as a potential biological control agent of Myzus persicae Sulzer (Hemiptera, Aphididae) on trichome-bearing tomato cultivars. Episyrphus balteatus’ foraging and oviposition behavior, as well as larval mobility and aphid accessibility, were compared between two tomato cultivars (Lycopersicon esculentum Mill. ‘Moneymaker’ and ‘Roma’) and two other crop plants; broad bean (Vicia faba L.) and potato (Solanum tuberosum L.). Hoverfly adults landed and laid more eggs on broad beans than on three species of Solanaceae. Hoverfly larval movement was drastically reduced on tomato, and a high proportion of hoverfly larvae fell from the plant before reaching aphid prey. After quantifying trichome abundance on each of these four plants, we suggest that proprieties of the plant surface, specifically trichomes, are a key factor contributing to reduced efficacy of E. balteatus as a biological agent for aphid control on tomatoes. Handling editor: Stanislaw Gorb     

Potential of adultOrius insidiosus [Hemiptera: Anthocoridae] as a predator of the fall armyworm,Spodoptera frugiperda [Lepidoptera: Noctuidae]

Orius insidiosus (Say) was observed to successfully prey on eggs and earlier instar larvae of the fall armyworm (FAW),Spodoptera frugiperda (J. E. Smith). Significantly more neonates of FAW were killed per 24 h than either 1, 2 or 3 d old larvae. Female and male predators exhibited a typical type-II functional response when preying on varying densities of eggs or neonates of FAW.      

Influence of intraguild predation between Episyrphus balteatus and Hippodamia variegata on their prey

Intraguild predation (IGP) is an interaction that frequently occurs in natural enemy communities, especially aphidophagous predators. This research investigated IGP intensity between Episyrphus balteatus De Geer (Diptera: Syrphidae), with Hippodamia variegata Goeze (Coleoptera: Coccinellidae). Five predator combinations including second and third larvae of H. variegata and third instar larvae of E. balteatus plus control treatment (totally six treatments) were tested. The effect of IGP on cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae) population density was investigated on sweet pepper seedlings under laboratory microcosms. In most combinations, the third instar larvae of E. balteatus alone reduced an A. gossypii population more efficiently than ladybird larvae and their combinations. Furthermore, IGP between third instar of E. balteatus and second larvae of H. variegata was asymmetrical; second instar H. variegata larvae were always the intraguild prey for third instar E. balteatus. The obtained result showed that outcome of IGP interaction on cotton aphid density was non-additive.     

Functional and numerical responses of Propylea dissecta (Col., Coccinellidae)

The functional response of a ladybeetle, Propylea dissecta, to increasing density of aphid, Aphis gossypii, was of the curvilinear shape depicting Holling's type II response with fourth instar larva being the most voracious stage when compared with adult male and female. Prey handling time by different predatory stages decreased from 65.45 to 8.72 min with increase in prey density from 25 to 800. The predator aggregation and high prey density reduces the searching efficiency of the predator. Area of discovery was highest (1.4437) when a single predator was searching at minimum aphid density (25) and lowest (0.0366) when eight predators were searching at a constant aphid density (200). Mutual interference and quest constants were 0.75 and 0.40, respectively. The reproductive numerical response, in terms of eggs laid, increased curvilinearly with prey density and female laid 70.5 ± 5.55 eggs when exposed to highest prey density (400) and 12.3 ± 0.79 eggs at lowest prey density (10). The similar shapes of both functional and reproductive responses indicate that both responses are interlinked and function simultaneously.     

Prey stage preference and functional response of the predatory mite Galendromus flumenis to Oligonychus pratensis

The Banks grass mite, Oligonychus pratensis (Banks) (Acari: Tetranychidae), is a serious pest in dates (Phoenix dactylifera L.) in the New World. Currently O. pratensis is managed using the miticide, Savey, and alternative strategies are necessary to remove pressure from a single control method due to the risk of resistance evolution. For this purpose, studies are underway to develop biological control strategies using the predatory mite, Galendromus flumenis (Chant) (Acari: Phytoseiidae). The current study determined the consumption rate of G. flumenis at constant densities of O. pratensis eggs, larvae, protonymphs and deutonymphs, and defined the functional response of predator females. The predator consumed significantly more eggs than other prey stages, and displayed a type II functional response on all prey stages. The highest attack rate and shortest handling time were obtained for predators feeding on prey larvae and eggs, respectively. The proportions of prey consumed by G. flumenis were higher at lower densities for all stages of Banks grass mite, implying that G. flumenis should be more effective at suppressing Banks grass mite populations at lower densities. Therefore, in an augmentative release program, G. flumenis would need to be released early in the infestation.     

Oviposition Behavior of the Predatory Midge Aphidoletes aphidimyza in Response to Aphid Patch Quality

Female Aphidoletes aphidimyza confronts serious challenges from both aphid prey and conspecifics. These challenges constitute strong selective pressures on the predatory midge to have an adaptive oviposition strategy. We did laboratory experiments to investigate clutch size of A. aphidimyza in response to the aphid Rhopalosiphum padi (density and age) and the presence of conspecific eggs (density) and larvae (age) in aphid colonies. The results of our study show that A. aphidimyza female adjusts its foraging effort by assessing the quality of prey patches. The number of eggs laid increased in response to aphid density. However, patches consisting of older aphids received fewer eggs. The number of eggs laid decreased in response to the presence of conspecific eggs, and in response to the presence of 2-day old conspecific larvae. Our study reveals deterrent effects on A. aphidimyza oviposition decisions on clutch size in response to older aphids and the presence of more conspecific eggs and older larvae.     

Functional responses of two chrysopid predators feeding onHelicoverpa armigera (lep.: noctuidae) and aphis gossypii (hom.: aphididae)

Predation onHelicoverpa armigera (Hubner) eggs andAphis gossypii (Glover) nymphs by 3rd instar larvae ofMallada desjardinsi (Navas) andChrysoperla congrua (Walker) was studied under laboratory conditions. Single predators that had been starved for 24 hours were isolated for 1 hour in 9 cm Petri dishes containing prey at densities of 5, 10, 15, 20 and 25 per dish. A type II functional response model gave a satisfactory fit to the data in case ofM. desiardinsi preying onH. armigera. However, with C.congrua, a type III model gave a slightly better fit. ForA. gossypii, functional responses of both predators did not differ from type II, withM. desjardinsi showing a significantly lower search rate and shorter handling time thanC. congrua. Implications of these findings are discussed     

Predation,oviposition and longevity of the predacious mite,Agistemus exsertus Gonzalez at different prey densities of Tetranychus urticae Koch (Acari: Stigmaeidae,Tetranychidae)

The relation between some biological aspects of the predatory mite, Agistemus exsertus Gonzalez and nymph densities of Tetranychus urticae Koch was studied in the laboratory. Predation and oviposition of A. exsertus showed Holling's Type II functional and numerical responses to changes in prey density. The total predation by A. exsertus females initially averaged 79.42 nymphs/female at 2 prey nymphs/day, significantly increased to a maximum average of 208.92 nymphs/female at 10 nymphs/day and gradually decreased to 90.92 nymphs/female at 30 prey items/day. Similarly, the predator significantly deposited total averages of 14.75, 76.42 and 34.33 eggs/female at 2, 10 and 30 nymph densities/day, respectively. The preoviposition and oviposition periods as well as longevity of A. exsertus significantly shortened with increasing prey densities.     

Effect of tomato leaf hairiness on functional and numerical response of Neoseiulus californicus (Acari: Phytoseiidae)

The objective of this study was to determine whether differences in hairiness of tomato plants affect the functional and numerical response of the predator Neoseiulus californicus McGregor attacking the two-spotted spider mite, Tetranychus urticae Koch. Two tomato hybrids with different density of glandular hairs were used. The functional response was measured by offering eggs and adults of T urticae at densities ranging from 4 to 64 items per tomato leaflet (surface ca. 6.3 cm2); eggs were offered to predator protonymphs and deutonymphs, adult spider mites to adult predators. The number of spider mites eaten as a function of initial density was fitted to the disc equation. Predator densities were regressed against initial prey densities to analyze the numerical response. The number of eggs and adults of T. urticae eaten by N. californicus was extremely low in both hybrids. The nymphal stage of N. californicus and prey density had a significant effect on the number of T urticae eggs eaten by the predator, while hybrid had no effect. The functional response fitted reasonably well to the Holling model. The handling time (Th) and the attack rate (a) were very similar among the two hybrids. The numerical response indicated that the absolute density of predators increased with changes in spider mite densities but the relative predator/prey density decreased in both hybrids. Tomato hairiness prevented N. californicus from exhibiting a strong numerical response and the predator functional response was much lower than observed in other host plants and other phytoseiids. This result shows the need to consider plant attributes as an essential and interactive component of biological control practices.     

Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi （Hymenoptera： Aphidiinae）

Intraguild predation （IGP） can be an important factor influencing the effective- ness of aphid natural enemies in biological control. In particular, aphid parasitoid foraging could be influenced by the presence of predators. This study investigated the effect of larvae of the predatory hoverfly Episyrphus balteatus DeGeer （Diptera： Syrphidae） and the multicolored Asian ladybird Harmonia axyridis Pallas （Coleoptera： Coccinellidae） on the foraging behavior of the aphid parasitoid, Aphidius ervi Haliday （Hymenoptera： Aphidiidae） in choice experiments using a leaf disc bioassay. Wasp response to chemical tracks left by those predator larvae was also tested. Parasitoid behavior was recorded using the Observer （Noldus Information Technology, version 5.0, Wageningen, the Netherlands）. The experiments were conducted under controlled environmental conditions using leaves of the broad bean plant, Viciafaba L. （Fabaceae） with Myzus persicae Sulzer （Homoptera： Aphididae） as the host complex. A. ervi females avoided aphid patches when larvae of either predator were present. A similar avoidance response was shown by A. ervi to aphid patches with E. balteatus larval tracks, whereas no significant response was observed to tracks left by H. axyridis larvae. It was concluded that IG predator avoidance shown by the aphid parasitoid A. ervi may be a factor affecting their distribution among host patches.     

Effect of size,extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis> and the hoverfly <Emphasis Type="Italic">Episyrphus balteatus</Emphasis>

Intraguild predation (IGP) is a widespread interaction between predatory arthropods, and is influenced by several factors. The harlequin ladybird, Harmonia axyridis (Coleoptera: Coccinellidae), has frequently been reported as an intraguild predator of other Coccinellidae, but little is known about its interactions with other aphidophagous predators, including syrphids. This study investigated the incidence of IGP between H. axyridis and Episyrphus balteatus (Diptera: Syrphidae), the most abundant hoverfly species in Europe and a commercially available aphid biocontrol agent. The influence of size, presence of extraguild prey and habitat complexity were investigated through laboratory experiments in Petri dishes and on potted broad bean plants. In both types of arenas, IGP between H. axyridis and E. balteatus was found to be asymmetric, with the coccinellid in the majority of cases being the intraguild predator. There was a significant effect of size on the frequency of IGP. The efficiency of H. axyridis as an intraguild predator increased with the developmental stage. Early instars of E. balteatus were the most vulnerable to IGP. Pupae of either species were not attacked. In the presence of extraguild prey, the frequency of IGP was substantially reduced. However, IGP still occurred, mainly in combinations of older larvae of H. axyridis with first or second instars of E. balteatus. The size of the arena affected the incidence of IGP in combinations with second instars of E. balteatus, but not in combinations with third instars. Field research is needed to elucidate the ecological relevance of IGP among these predators.     

Prey‐mediated changes in the selectivity of the predator Macrolophus pygmaeus (Heteroptera: Miridae)

When foraging in communities with mixed prey, generalist predators may be confronted with prey species that differ in quality, size and mobility and interact with one another. To examine prey selection, predation by Macrolophus pygmaeus (Heteroptera: Miridae) was recorded by providing a diet of either one or two prey species of Myzus persicae (third‐instar nymphs), Aphis gossypii (fourth‐instar nymphs), Trialeurodes vaporariorum (third‐instar nymphs) and Ephestia kuehniella (eggs). In the experiments, prey mobility, prey quality and prey biomass were considered. The biomass consumed by the predator was dependent on the combination of prey species and the quantity of biomass offered. In choice experiments with diets mixed of two prey species at equal densities, the predation to A. gossypii was significantly reduced in the presence of E. kuehniella but the rate of consumption of M. persicae, T. vaporariorum and E.kuehniella was not significantly affected by the coexistence of any other species in the mixed prey diet. When equal amounts of biomass from two prey species were provided in combination, the total consumed biomass was significantly reduced in the mixed prey diets composed of E. kuehniella eggs and aphid nymphs. Thus, under the mixed‐prey situation, prey selection by predators may be affected by interactions among prey species differing in traits such as quality, mobility and size.     

Foraging behaviour of Scymnus coccivora Ayyar against cotton mealybug Phenacoccus solenopsis Tinsley

Predation is one of the significant biotic mortality factors reducing the insect pest population as functional response and the numerical response of the predator are the key factor regulating the population dynamics of predator prey species. This study is aimed to evaluate the functional response of all the developmental stages of Scymnus coccivora Ayyar (Coleoptera: Coccinellidae) against the different densities of cotton mealybug, Phenacoccus solenopsis (Tinsley) (Hemiptera: Pseudococcidae) and the numerical response of female predator. Experiments were carried out in controlled environment laboratory conditions at 25 ± 1 °C temperature, 60 ± 5% relative humidity and photoperiod of 16 h. Number of eggs consumed, number of eggs laid and the Efficiency of Conversion of Ingested food (ECI) were recorded daily. Results from the study revealed that all the developmental stages of S. coccivora exhibited a Type II response. Different parameters such as attack rate (a’), handling time (T_h) and the maximum rate of predation were estimated using Roger’s random attack equation and Holling Disc equation in which Rogers random attack equation was found best fit. Female has shown the highest attack rate (a’) followed by IV^th instar grub, male, III^rd, II^nd and I^st instar grub. With low handling time, IV^th instar grub has shown maximum predation rate of 76.40 per day followed by female (75.86), male (58.79), III^rd (22.84), II^nd (19.65) and I^st instar grub (15.39). The numerical response increase was curvilinearly related to different prey densities with the highest number of eggs (11.8 ± 3.44) produced at highest prey density (160). The Efficiency of Conversion of Ingested food (ECI) was highest (64.49 ± 8.03) at prey density of 10. Understanding the factors that lead to variation in functional response of predator in natural population will advance our understanding of the effects of predation on individual and the effectiveness of coccinellid predators as biocontrol agent against cotton mealybug.