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.     

Predation potential of the earwig Euborellia annulipes on fruit fly larvae and trophic interactions with the parasitoid Diachasmimorpha longicaudata

The earwig Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae), a generalist predator, has been observed in fruits infested with fruit fly larvae, which are frequently parasitized by parasitoid wasps. Neither the capacity of earwigs to predate on fruit flies nor intraguild interactions between earwigs and fruit fly parasitoids have been investigated. Here, we studied in laboratory conditions the predation on the fruit fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) by the earwig E. annulipes, and whether parasitism of fruit fly larvae by the parasitoid wasp Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) influences predation by the earwig. We evaluated the predation capacity, functional response and prey preference of E. annulipes for parasitized and non-parasitized fruit fly larvae in choice and no-choice tests. We found that earwigs prey on second- and third-instar larvae and pupae of C. capitata and consumed larger numbers of second-instar larvae, followed by third-instar larvae and pupae. Females prey on larger numbers of fruit flies than did males, regardless of the prey developmental stage, but both sexes exhibited a type II functional response. Interestingly, males killed but did not consume fruit fly larvae more than did females. In no-choice tests, earwig females consumed equal numbers of parasitized and non-parasitized fruit fly larvae. However, in choice tests, the females avoided feeding on parasitized larvae. Subsequent tests with hexane-washed parasitized and non-parasitized larvae showed that putative chemical markings left on fruit flies by parasitoids did not drive the earwig preference towards non-parasitized larvae. These findings suggest that E. annulipes is a potential biological control agent for C. capitata, and that, because the earwig avoids consuming larvae parasitized by D. longicaudata, a combination of the two natural enemies could have an additive effect on pest mortality.     

Generalist predators in organically and conventionally managed grass‐clover fields: implications for conservation biological control

Organically managed agroecosystems rely in part on biological control to prevent pest outbreaks. Generalist predators (Araneae, Carabidae and Staphylinidae) are a major component of the natural enemy community in agroecosystems. We assessed the seasonal dynamics of major generalist predator groups in conventionally and organically managed grass–clover fields that primarily differed by fertilisation strategy. We further established an experiment, manipulating the abundant wolf spider genus Pardosa, to identify the importance of these predators for herbivore suppression in the same system and growth period. Organic management significantly enhanced ground‐active spider numbers early and late in the growing season, with potentially positive effects of plant cover and non‐pest decomposer prey. However, enhancing spider numbers in the field experiment did not improve biological control in organically managed grass–clover fields. Similar to the survey results, reduced densities of Pardosa had no short‐term effect on any prey taxa; however, spider guild structure changed in response to Pardosa manipulation. In the presence of fewer Pardosa, other ground‐running spiders were more abundant; therefore, their impact on herbivore numbers may have been elevated, possibly cancelling increases in herbivore numbers because of reduced predation by Pardosa. Our results indicate positive effects of organic farming on spider activity density; however, our survey data and the predator manipulation experiment failed to find evidence that ground‐running spiders reduced herbivore numbers. We therefore suggest that a positive impact of organic fertilisers on wolf spiders in grass–clover agroecosystems may not necessarily improve biological control when compared with conventional farming.     

Role of plant phenology in mediating interactions between two biological control agents for spotted knapweed

The role of spotted knapweed phenology on the attack rate of two seed-head insects Urophora affinis and Larinus minutus was assessed in a series of field studies at four study sites in south-eastern British Columbia, Canada. Slow or later developing knapweed plants had more seed heads that contained only single or multiple U. affinis whereas early or faster developing plants had more seed heads containing L. minutus alone or in combination with U. affinis. L. minutus did not distinguish between seed heads with or without U. affinis larvae when laying eggs. However, seed heads with multiple U. affinis present, produced fewer L. minutus adults than expected. The probability of single or multiple U. affinis galls being present increased with seed-head diameter but was not affected by seed-head height. Attack by L. minutus increased with seed-head diameters >5 mm and was lower at plant heights above 50 cm. These results demonstrate two mechanisms that enable U. affinis to successfully coexist with L. minutus: differences between the species in their response to the developmental phenology of knapweed heads, and increased survivorship of U. affinis in heads with multiple U. affinis galls through niche interference competition. These mechanisms provide a possible explanation for the persistence of U. affinis populations on spotted knapweed, in spite of high levels of within seed-head mortality that have been observed with increasing L. minutus populations.     

Intraguild predation and competitive displacement between Nesidiocoris tenuis and Dicyphus maroccanus,two biological control agents in tomato pests

Dicyphus maroccanus Wagner and Nesidiocoris tenuis Reuter (Hemiptera: Miridae) are 2 biological control agents in tomatoes. Through the crop seasons, a natural shift in the occurrence of both mirids in favor of N. tenuis has been observed at the end of the cropping cycle in eastern Spain. To better optimize their conservation, the reasons for the observed change, such as intraguild interactions (IGP) or the influence of environmental conditions, are worth elucidating. To do this, we first studied the IGP of adult females on heterospecific nymphs in the laboratory. We next studied exploitative competition between adults and nymphs of each species when feeding on Ephestia kueniella Zeller (Lepidoptera: Pyralidae) eggs in the laboratory. Finally, to analyze the competitive displacement between both mirids, we conducted a semifield experiment in which both predators were released together. All experiments were conducted at 2 temperature regimes (20 and 25°C). Adult‐to‐nymph intraguild interactions occurred only at 25 ºC at very low levels, showing that N. tenuis attacked and consumed a greater proportion of heterospecific nymphs. Nesidiocoris tenuis was a better competitor than D. maroccanus when feeding on the shared prey in the presence of its heterospecific nymph at 25 ºC. In semifield conditions, N. tenuis showed a competitive advantage over D. maroccanus at both temperatures. We conclude that there is not direct interference between both species, however, N. tenuis has a greater ability to outcompete, since it is best adapted to higher temperatures and it is able to remove food sources for D. maroccanus.     

Combined use of the larvo‐pupal parasitoids Diachasmimorpha longicaudata and Aganaspis daci for biological control of the medfly

In biological control programmes, it is very common to employ multiple species to manage a single insect pest. However, the beneficial effects of natural enemies are not always additive because of several factors, including interspecific competition between these biocontrol agents. For this reason, in the present study we assessed several biological parameters (percentage parasitism, fertility, induced mortality and population reduction) of the parasitoids Diachasmimorpha longicaudata and Aganaspis daci when used together against the medfly Ceratitis capitata under laboratory and greenhouse conditions. Our results showed that, under laboratory conditions, fertility and percentage parasitism corresponded to a different functional response for each species (D. longicaudata: type II; A. daci: type III), whilst under greenhouse conditions, and unlike what occurs with single releases, both parasitoids showed a type III functional response; this is the only response which may lead to direct density dependence when host densities are low. Our results also revealed that when both species acted together, they produced a very high total percentage parasitism compared to that reported for single releases under both laboratory (64–76%) and greenhouse (21–51%) conditions. The parasitism was also higher for A. daci except when medfly larvae were provided in an artificial diet. Furthermore, host mortality induced by the two parasitoids acting together was very high, especially at low‐host densities; medfly population was almost completely reduced under greenhouse conditions. In summary, the data reported here supports the combined use of these species in biological control programmes against the medfly and highlights the importance of several factors, such as climatic conditions and host density, when planning their field releases.     

Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control

In agroecosystems, parasitoids and predators may exert top-down regulation and predators for different reasons may avoid or give preference to parasitised prey, i.e., become an intraguild predator. The success of pest suppression with multiple natural enemies depends essentially on predator–prey dynamics and how this is affected by the interplay between predation and parasitism. We conducted a simple laboratory experiment to test whether predators distinguished parasitised prey from non-parasitised prey and to study how parasitism influenced predation. We used a host-parasitoid system, Spodoptera frugiperda and one of its generalist parasitoids, Campoletis flavicincta, and included two predators, the stinkbug Podisus nigrispinus and the earwig Euborellia annulipes. In the experiment, predators were offered a choice between non-parasitised and parasitised larvae. We observed how long it took for the predator to attack a larva, which prey was attacked first, and whether predators opted to consume the other prey after their initial attack. Our results suggest that, in general, female predators are less selective than males and predators are more likely to consume non-parasitised prey with this likelihood being directly proportional to the time taken until the first prey attack. We used statistical models to show that males opted to consume the other prey with a significantly higher probability if they attacked a parasitised larva first, while females did so with the same probability irrespective of which one they attacked first. These results highlight the importance of studies on predator–parasitoid interactions, as well as on coexistence mechanisms in agroecosystems. When parasitism mediates predator choice so that intraguild predation is avoided, natural enemy populations may be larger, thus increasing the probability of more successful biological control.     

Spatial interactions between sympatric carnivores: asymmetric avoidance of an intraguild predator

Interactions between intraguild species that act as both competitors and predator–prey can be especially complex. We studied patterns of space use by the black-footed ferret (Mustela nigripes), a prairie dog (Cynomys spp.) specialist, and the American badger (Taxidea taxus), a larger generalist carnivore that competes for prairie dogs and is known to kill ferrets. We expected that ferrets would spatially avoid badgers because of the risk of predation, that these patterns of avoidance might differ between sexes and age classes, and that the availability of food and space might influence these relationships. We used location data from 60 ferrets and 15 badgers to model the influence of extrinsic factors (prairie dog density and colony size) and intrinsic factors (sex, age) on patterns of space use by ferrets in relation to space use by different sex and age categories of badgers. We documented asymmetric patterns of avoidance of badgers by ferrets based on the sex of both species. Female ferrets avoided adult female badgers, but not male badgers, and male ferrets exhibited less avoidance than female ferrets. Additionally, avoidance decreased with increasing densities of prairie dogs. We suggest that intersexual differences in space use by badgers create varying distributions of predation risk that are perceived by the smaller carnivore (ferrets) and that females respond more sensitively than males to that risk. This work advances understanding about how competing species coexist and suggests that including information on both intrinsic and extrinsic factors might improve our understanding of behavioral interactions between sympatric species.     

Plant-mediated interactions: Considerations for agent selection in weed biological control programs

Plant-mediated indirect interactions among herbivores (arthropods and pathogens) are common and extensively reported in the ecological literature. However, they are not well-documented with respect to weed biological control. Such interactions between biological control agents can have net positive or negative impacts on total weed suppression depending on the strength of the interaction(s), the relative importance of the agent indirectly impacted, and the combined weed suppression that results. A better understanding of plant-mediated interactions may improve decision-making about which agents to introduce in classical biological control programs for greatest impact on invasive weeds. This paper reviews the subject, including examples from the biological control literature; outlines the need for research on indirect effects of herbivores on other herbivores; discusses how such knowledge may strengthen classical biological control programs for invasive weeds; and provides recommendations for the kind of studies that should be done and how information about plant-mediated interactions could be integrated into agent evaluation protocols, to assist in decision-making about agents for importation and release.     

Interactions between two biological control agents and their target weed: a beetle,a bug and a cactus weed

ABSTRACT

Pereskia aculeata Miller (Cactaceae) is an invasive alien shrub introduced into South Africa from Brazil. The leaf-feeding beetle, Phenrica guerini Bechyne (Chrysomelidae), was released as a biological control agent in South Africa in 1991 followed by the stem-wilting bug, Catorhintha schaffneri Brailovsky & Garcia (Coreidae), in 2014. This study investigated the interactions between the two agents under laboratory conditions. Potted plants were exposed to one of four treatments: control (no agents), P. guerini only, C. schaffneri only and both species together. Four densities, ranging from 2 to 12 insects per plant were used. Cathorhitha schaffneri alone at low to moderate densities resulted in the same reduction in number of leaves and shoot length as when combine with P. guerini. At the highest density, C. schaffneri reduced the number of leaves significantly more than any treatment. Mortality of P. guerini was significantly higher than C. schaffneri at the highest density when in combination. The antagonistic interaction between P. guerini and C. schaffneri suggests that these agents should not be released together because this would impact negatively on the overall biocontrol programme against P. aculeata. It is recommended that C. schaffneri should be released at sites where P. guerini is not present. Extrapolation of laboratory-based studies into the field is often challenging, so mass-rearing and releases of P. guerini should continue until there is convincing proof that C. schaffneri alone is more effective than P. guerini in the field.     

Intraguild predation in biological control: consideration of multiple resource species

Theoretical models of intraguild predation (IGP) predict that IGP decreases the effectiveness of biological control while many empirical studies do not agree with this prediction. In this study, I discuss the importance of explicit consideration of multiple resource species that has been neglected in most theoretical IGP models. In the previous models of IGP, a single resource species represented the pest species. However, there are multiple resource species (e.g., multiple pest species or aggregates of pest and non-pest species) in real systems. This study shows that models with multiple resource species can predict a variety of outcomes including those consistent with the empirical observations. The explicit consideration of resource species is useful for the future development of theories in biological control. Handling Editor: Helen Roy     

Parasitism and dispersal potential of Sirex noctilio: implications for biological control

1 Sirex noctilio F. (Hymenoptera: Siricidae) is a wood‐boring wasp that attacks many pine species, including commercial trees planted throughout the world. Management of its populations is largely based on biological control using the nematode Beddingia siricidicola. Adult females are sterilized by the nematode, but are free to move and attack new trees, promoting nematode dispersal. Although generally successful, wasp management through nematode introductions has sometimes been inadequate. 2 We evaluated the effect of parasitism by B. siricidicola on flight performance of woodwasps under laboratory conditions. Using flight mills, we recorded a total of 46 flight trials over 23 h, obtained from infected and control (uninfected) females. 3 Although all wasps lost weight during flight, parasitized females were significantly smaller and suffered larger weight losses than uninfected females. In addition, total flight distance and velocity were lower in parasitized females. 4 Because nematode infection transmission relies on healthy wasps attacking trees previously visited by nematode‐bearing females, differential dispersal capacity could limit biological control success.     

Evidence for intraguild predation by Podisus maculiventris on a ladybeetle, Coleomegilla maculata: Implications for biological control of Colorado potato beetle, Leptinotarsa decemlineata

The potential for intraguild predation (IGP) between larval and adult life stages of twopolyphagous arthropod predators common in NorthAmerican agroecosystems was studied in thelaboratory. Predators examined were the spinedsoldier bug, Podisus maculiventris Say,and the twelve-spotted ladybeetle, Coleomegilla maculata Lengi. A shared preyitem, eggs of the Colorado potato beetle (CPB),Leptinotarsa decemlineata Say, was alsoprovided to the predators, both to provide analternate food source and to quantify theimpact of IGP on the potential for pestsuppression by these two predators. Experimentswere conducted on single potato leaves inplastic cup arenas, and, subsequently, in cagesenclosing whole potato plants. IGP occurredasymmetrically, with P. maculiventrisadults and nymphs only attacking C. maculata larvae. Even though ladybeetle adultswere generally smaller than soldier bug adults,they were never preyed upon. This appears to bethe first documented case of a coccinellidshowing differential larval and adult immunityto attack by a larger invertebrate predator.The impact of IGP, when it did occur, on CPBegg consumption was equivocal. IGP did notconsistently influence levels of predation onthe eggs. Conversely, even when IGP did notoccur, predation on CPB eggs by both predatorstogether did not increase significantly overlevels inflicted by either predator alone. Theimplications for biological control of CPB bythese predators, which are being considered foraugmentative release in potato and tomato cropsin the United States, are discussed.     

Web-site selection strategies of linyphiid spiders in alfalfa: implications for biological control

Site-specific foraging can enhance the ability of generalist predators to provide effective and sustainable levels of pest control in agroecosystems. This can result from increased growth rates, higher population densities, and improved capture frequencies of pests at high prey density microsites. We tested the hypothesis that linyphiid spiders would exhibit microhabitat-specific web-site selection strategies in alfalfa. This was predicted to result in high prey densities at web-sites compared to paired non-web-sites through direct, or indirect, selection of prey-rich habitats. A total of 22,242 potential prey items were collected from mini-sticky traps located at 896 microsites. Web-centered mini-sticky traps on the ground, representative of Erigone autumnalis Emerton (Araneae: Linyphiidae) webs, captured similar numbers of potential prey as paired non-web-centered traps nearby. However, aerial sticky traps at web-sites of Bathyphantes pallidus (Banks) (Araneae: Linyphiidae) contained significantly more Diptera and Empoasca fabae (Harris) (Homoptera: Cicadellidae) than paired non-web-centered sticky-traps. Prey activity-densities also varied between web-sites of E. autumnalis and B. pallidus. Diptera were dominant at aerial microsites of B. pallidus whilst Collembola were abundant on ground-based traps of E. autumnalis. These results suggest that in alfalfa, the pressure for selecting prey-rich web-sites by erigonine spiders is low, but B. pallidus exhibits a selective web-location strategy targeted towards high quality dipteran prey. These sites also captured large numbers of E. fabae, a major pest of alfalfa, thus implicating aerial-based linyphiines as valuable predators in biological control.     

Indirect nontarget effects of host-specific biological control agents: Implications for biological control

Classical biological control of weeds currently operates under the assumption that biological control agents are safe (i.e., low risk) if they do not directly attack nontarget species. However, recent studies indicate that even highly host-specific biological control agents can impact nontarget species through indirect effects. This finding has profound implications for biological control. To better understand the causes of these interactions and their implications, we evaluate recent case studies of indirect nontarget effects of biological control agents in the context of theoretical work in community ecology. We find that although particular indirect nontarget effects are extremely difficult to predict, all indirect nontarget effects of host specific biological control agents derive from the nature and strength of the interaction between the biological control agent and the pest. Additionally, recent theoretical work suggests that the degree of impact of a biological control agent on nontarget species is proportional to the agent’s abundance, which will be highest for moderately successful control agents. Therefore, the key to safeguarding against indirect nontarget effects of host-specific biological control agents is to ensure the biological control agents are not only host specific, but also efficacious. Biological control agents that greatly reduce their target species while remaining host-specific will reduce their own populations through density-dependent feedbacks that minimize risks to nontarget species.     

Cross mating studies among five fruit fly parasitoid populations: potential biological control implications for tephritid pests

The reproductive compatibility between four different species/populations of the tephritid parasitoid Psyttalia (Walker) species from Kenya and individuals of the morphologically identical Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) from a laboratory culture in Italy used in augmentative biological control of olive fly, Bactrocera oleae (Gmelin) (Diptera: Tephritidae) was assessed through cross mating tests using single-pair and group mating methods. Reciprocal crosses among the species resulted in the production of viable offsprings up to the second generation. In spite of the successful production of viable offspring in the laboratory, Psyttalia species are known to have specific host fruit and/or host fly preferences and populations/species may be isolated in one way or the other. However, it is not known whether these populations/species interbreed in the field. We discuss the ability of these parasitoids to interbreed and the potential effects of that on their use as biological control agents, especially in environments where other closely related species are present or in situations where multiple parasitoid introductions are intended.     

Intraguild interactions between Euseius stipulatus and the candidate biocontrol agents of Tetranychus urticae in Spanish clementine orchards: Phytoseiulus persimilis and Neoseiulus californicus

Spanish clementine orchards are frequently infested by the two-spotted spider mte Tetranychus urticae. Natural control of T. urticae is insufficient despite the presence of Neoseiulus californicus and Phytoseiulus persimilis. The phytoseiid community is dominated by the generalist Euseius stipulatus which is poorly adapted to exploit T. urticae. Having the intention to promote biological control of T. urticae by augmentative releases we were interested whether P. persimilis and N. californicus are negatively affected by intraguild (IG) interactions with E. stipulatus. Two experiments were conducted. Firstly, we assessed female aggressiveness (quantified as combination of attack probability and latency) in IG predation on larvae. Secondly, we measured mortality, escaping rate and developmental time of immature IG prey in presence and absence of an adult IG predator female. Euseius stipulatus appeared the strongest IG opponent but microhabitat structure modulated the IG interactions and the advantage of E. stipulatus was partially offset when spider mite webbing was present. Implications of these IG interactions for natural and biological control of T. urticae in clementine orchards are discussed.     

Possible indirect interactions between transient and resident killer whales: implications for the evolution of foraging specializations in the genus Orcinus

Summary Two distinct forms of killer whale (Orcinus orca) occur off the coast of British Columbia, Alaska and Washington State. These have different diets, and may be reproductively isolated. Because the primary food of transient whales (pinnipeds) is a potential competitor for the primary food of resident whales (salmon), or for the smaller fishes on which salmon feed, there should be an indirect interaction between the two forms of killer whale. We use simple mathematical models to show that this interaction will be either of a plus-minus type, or a plus-plus type (indirect mutualism), depending on whether or not pinnipeds and residents are on the same trophic level. In the case of the plus-minus interaction, increasing the population density or improving the environmental conditions of transients will increase the population density of residents, while increasing resident populations will reduce the equilibrium population size of transients. In the case of the plus-plus interaction, increasing the population density or improving the environmental conditions of transients will increase the population density of residents, while increasing resident populations will reduce the equilibrium population size of transients. In the case of the plus-plus interaction, increasing the population density or improving the environmental conditions of transients will increase the population density of residents, and vice versa. Such effects may not be currently manifest due to reduced populations at most levels in the food web. Regardless, considering such indirect interactions may be important for the management of many of the species involved, and can also provide a valuable framework for examining the evolution of the two forms of killer whales. Frequency-dependent indirect interactions, acting in concert with density-dependence within populations and disruptive selection on prey-type specific foraging characteristics, may have favoured reproductive isolation of the two forms of killer whales. We suggest that these two forms of whale are in the process of speciating, i.e., the two forms are incipient species.     

Complex interactions among fish, snails and macrophytes: implications for biological control of an invasive snail

The golden apple snail (Pomacea canaliculata), a native of freshwater wetlands of South America, has invaded many Asian countries and grazed heavily in agricultural and wild areas. Common carp (Cyprinus carpio) has been proposed as a biological control agent against this snail, but little is known about its impact on non-target aquatic plants and animals. In a 8-week enclosure experiment, we quantified the impact of common carp on three species of aquatic macrophytes and nine species of snails, including the apple snail, in a shallow pond. The results showed that the apple snail or carp alone significantly reduced the plant biomass, although the apple snail had a stronger overall herbivorous effect than the carp. The carp completely removed juvenile apple snails, but had only a weak predatory effect on larger apple snails and no effect on the adults’ oviposition frequency. Furthermore, the carp significantly reduced the populations of most species of other snails that occurred naturally in the pond. Our results thus indicate that common carp can be an effective biological control agent against the invasive apple snail, but caution should be taken about its potential to reduce wetland floral and faunal diversity.