Delineating the effects of a plant trait on interactions among associated insects

Plant traits can affect ecological interactions between plants, herbivores, and predators. Our study tests whether reduced leaf wax in peas alters the interaction between the pea aphid ( Acyrthosiphon pisum), a foliar-foraging predator (a lady beetle, Hippodamia convergens) and a ground-foraging predator (a ground beetle, Poecilus scitulus). We performed a 2×2×2 factorial experiment in which wax level, presence of H. convergens, and presence of P. scitulus were manipulated. Experimental arenas consisted of a cage surrounding three pea plants. One plant in each cage was stocked with 15 pea aphids. In greenhouse and field cage experiments, we assessed the effect of each factor and their interactions on aphid density. As in previous studies, H. convergens foraged for aphids more effectively on reduced wax peas than on normal peas. Other interactions among H. convergens, P. scitulus , and A. pisum were the same on both types of peas. We consider how aphid movement, plant growth, and a high frequency of predation by P. scitulus on H. convergens influenced pea aphid density.     

Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids

Summary The nature and relative strengths of intra versus interspecific interactions among foraging ladybeetle larvae were studied experimentally by measuring short-term growth rates of predators and reductions in population sizes of prey in laboratory microcosms. In these microcosms, ladybeetle larvae foraged singly or as conspecific or heterospecific pairs, for pea aphids on bean plants over a two-day period. Similarly sized third instar larvae ofHippodamia convergens andH. tredecimpunctata, H. convergens andH. sinuata, andH. convergens andCoccinella septempunctata, were tested in experiments designed to ensure that paired larvae experienced moderate competition. Interspecific competition in these experiments did not differ significantly from intraspecific competition, in that an individual's weight gain did not depend on whether its competitor was heterospecific or conspecific. Furthermore, aphid populations were reduced equally by heterospecific and conspecific pairs. These results suggest that there is little or no difference between intra and interspecific interactions among larvae of these ladybeetles when two similarly sized individuals co-occur on a host plant. Thus, the species diversityper se of assemblages of ladybeetle larvae may have little influence over the short term on the reduction of aphid populations by ladybeetle predation.     

Predators mediate host plant resistance to a phytophagous pest in cabbage with glossy leaf wax

This study examined the role of generalist predators in producing higher mortality ofPlutella xylostella L. (Plutellidae) larvae on glossy vs. normal-wax cabbage,Brassica oleracea var.capitata L. To test this, survival and feeding ofP. xylostella were measured on individually caged glossy and normal-wax plants with and without each of three generalist predators,Chrysoperla carnea (Stephens) (Chrysopidae),Orius insidiosus (Say) (Anthocoridae), andHippodamia convergens Guerin-Meneville (Coccinellidae). In the greenhouse, predators always significantly reduced survival ofP. xylostella larvae on glossy plants, but never on normal-wax plants. In the field, predators significantly reducedP. xylostella survival on glossy plants, but onlyC. carnea was effective on normal-wax plants. In similar experiments with excised leaves,O. insidiosus andC. carnea were more effective predators on the glossy leaves, whileH. convergens was equally effective on both kinds of leaves. Patterns for feeding were similar, but significance levels differed from those forP. xylostella survival. The greater effectiveness of predators on glossy plants is apparently due to the reported improved mobility of these animals on glossy leaf surfaces. The data also suggest that reduced mining byP. xylostella exposes the larvae to more predation on glossy plants and contributes some to the resistance. Regardless of the mechanism, resistance toP. xylostella on glossyB. oleracea appears to depend on the action of generalist predators for its full expression. This dependence on predation must be considered in the development and deployment of glossy insect-resistantB. oleracea.     

Coccinellid interactions mediated by vegetation heterogeneity

Environmental heterogeneity can have profound effects on agroecosystem function and it is important for improving ecosystem services such as biological control. Promoting system diversity via non‐crop plants is one method for increasing habitat heterogeneity within farmscapes. Non‐crop plants provide access to refuges and alternative food resources provide multiple benefits to enhance populations of arthropod predators. In this study, we examined the effects of small‐scale spatial structure on life‐stage specific interactions between the native coccinellid, Hippodamia convergensGuérin‐Méneville, and the exotic Harmonia axyridis (Pallas) (both Coleoptera: Coccinellidae), which overlap in spatial distribution in many crop systems. Squash [Cucurbita pepo L. (Cucurbitaceae)] and non‐crop mugwort [Artemisia vulgaris L. (Asteraceae)] plants with and without aphids were used as a model of spatial heterogeneity in micro‐ and mesocosm experiments. In response to factorial treatment combinations, we evaluated oviposition behavior, egg predation, larval survival, and larval predator‐prey and predator‐predator interactions. Adult H. convergens displayed higher foraging activity on aphids when exposed to complex habitats containing a non‐crop plant. In the presence of the exotic coccinellid, H. convergens preferred to deposit eggs on the non‐crop plant. Furthermore, a combination of spatial heterogeneity and prey availability reduced larval intraguild predation and cannibalism, and improved reproductive output of H. convergens by reducing intra‐ and interspecific egg predation. Our results provide evidence that life‐stage‐specific intraguild interactions are mediated by access to non‐crop plants. Thus, the introduction or maintenance of non‐crop plants has the potential to enhance coexistence of multiple natural enemies and improve top‐down control of pests.     

Mobility of three generalist predators is greater on cabbage with glossy leaf wax than on cabbage with a wax bloom

Adult coccinellids Hippodamia convergens Guerrin-Menneville, adult minute pirate bugs Orius insidiosus (Say), and larval lacewings Chrysoperla carnea (Stephens) have been reported to more effectively reduce populations of Plutella xylostella (L.) (Plutellidae: Lepidoptera) larvae on a cabbage with glossy surface waxes than on a standard cabbage variety. To examine the mechanisms, the behavior of each predator species was quantified on the two cabbage types. All three predators spent less time walking on the standard variety and more time in other activities, including grooming and scrambling (ineffective forward locomotion). In addition, walking by each predator was distributed more evenly among the parts of the leaf on the glossy cabbage than on the standard variety. In small enclosures, C. carnea and O. insidiosus found and attacked individual first instar P. xylostella more quickly on the glossy cabbage. Scanning electron micrographs showed debris, probably wax, on the tarsae of C. carnea and O. insidiosus that had walked on the standard variety, but not on those that had walked on glossy cabbage. H. convergens tarsae did not accumulate debris on either cabbage type. Predator mobility and effectiveness were apparently impeded by wax crystals, which are present only on the standard variety. This mechanism can explain the greater effectiveness of these generalist predators against P. xylostella larvae on glossy vs normal-wax cabbage.     

Attachment to plant surface waxes by an insect predator

Insects foraging on plant surfaces must attach to the layerof lipophilic materials known as epicuticular waxes (EW) thatcover these surfaces. In this paper, we briefly review the evidencethat variation in EW morphology can influence the ecology ofherbivorous insects directly, by affecting their attachmentto plant surfaces, and indirectly by affecting attachment byactively foraging predatory insects to plant surfaces. We thenpresent new data examining how EW micromorphology and chemicalcomposition of Brassica oleracea influence attachment by thepredatory beetle, Hippodamia convergens (Coccinellidae). Bioassayswith genotypes of B. oleracea differing in wax characteristics,and with EW extracts from these plants applied to glass, showthat wax crystals disrupt attachment. In addition, bioassaysshow that attachment by H. convergens differs among EW extractsprepared to have smooth surfaces without crystals. The differencesin attachment under these conditions are evidently due to thechemical composition of the waxes. Bioassays with two pure waxconstituents show that wax composition can significantly affectattachment by H. convergens. The study opens the way for usinga similar approach to understand attachment by insects to waxyplant surfaces.     

Intraguild predators and the spatial distribution of a parasitoid

An experimental plot of the aphid Aphis fabae on various host plant species was colonized by natural populations of the aphidiine parasitoid Lysiphlebus fabarum and insect predators, especially coccinellids. Parasitism of A. fabae by L. fabarum was significantly depressed on plants bearing coccinellids. The number of parasitized aphids increased with aphid abundance on three plant species (Papaver dubium, Rumex obtusifolius, Vicia faba), but not on the plant species (Chenopodium album) which bore very high numbers of coccinellids. In complementary laboratory experiments, L. fabarum offered a choice between odours of plants infested with A. fabae and/or coccinellids selected the odour fields from coccinellid treatments at significantly lower frequency than the odour fields of other treatments. It is concluded that avoidance of coccinellids by L. fabarum contributes to the negative association between the abundance of coccinellids and parasitoids in the field. Received: 22 March 1999 / Accepted: 22 March 2000     

Response of coccinellids to their aphid prey at different spatial scales

Predators that have an increasing numerical response for aggregation, attack and oviposition to increasing prey density are thought to be ideal for biological control. However density-dependent processes are infrequently detected and explanations include differences in the scales at which observations are made, behavioral differences among species, and habitat features. We examined the aggregation of four species of colonizing adult coccinellids to varying prey densities at two spatial scales in a maize system. Three of the species, Adalia bipunctata, Hippodamia tredecimpunctata, and Hippodamia convergens, responded to aphid abundance at the plant scale, and one species, Coleomegilla maculata, responded to the average aphid density at the plot (10×10 m) scale. In addition, H. convergens responded to individual plants with high aphid abundance in those plots with many plants of high aphid abundance. These results suggests that C. maculata (and possibly H. convergens) may be better able to colonize fields before aphid populations reach high levels, whereas A. bipunctata and H. tredecimpunctata may only be able to respond to high aphid abundance at the plant scale. This study suggests that spatial scale can affect predator–prey dynamics in a species-specific manner. However, the differences among coccinellid species in the community appear to be complementary, potentially contributing to greater aphid suppression.An erratum to this article can be found at     

Effects of Brassica oleracea waxblooms on predation and attachment by Hippodamia convergens

Four mutations that reduce waxbloom in Brassica oleracea L. were examined for their effects on predation, mobility, and adhesion to the plant surface by the general predator Hippodamia convergens (Guérin-Menéville) (Coleoptera: Coccinellidae). The mutations reduce waxbloom to different degrees, but all produce a glossy phenotype. Plants tested were inbred lines, near isogenic lines, or segregating F₂ populations, depending on the mutation. In an experiment on caged leaves, predation of Plutella xylostella L. larvae by H. convergens adult females was significantly greater on glossy types as compared with normal-wax or wild-type counterparts. Although the trend was the same for each mutation, individual comparisons between glossy and normal-wax lines or segregants were only significant for two of them, those producing mutant alleles gl_a and gl_d. Individual H. convergens were observed to spend more time walking on leaf edges and less time walking on leaf surfaces of normal-wax plants than glossy plants. Hippodamia convergens also obtained better adhesion to the surfaces of glossy plants than to normal-wax plants when tested using a centrifugal device. Two of the mutations produced similarly strong effects on predation, behaviour, and adhesion by H. convergens. These two are the same previously determined by us to provide the strongest similar effects on another generalist predator, Chrysoperla plorabunda (Fitch). The results indicate that waxbloom variation in nature could affect herbivore populations through its effects on generalist predators.     

Behavioral responses of hybrid lacewings (Neuroptera: Chrysopidae) to courtship songs

The study of hybrid courtship songs and the behavioral responses of hybrids and parental individuals to hybrid songs can be useful in understanding the origin of reproductive isolation among species that differ mainly in their courtship songs. Here we test the hypotheses (a) that hybrid lacewings prefer hybrid songs to either of the parental songs from a cross betweenChrysoperla plorabunda andC. johnsoni, and (b) that parental individuals prefer their own song over those of hybrids. Analysis of songs showed that most features of hybrid songs are intermediate between the two parents. Hybrids organize their songs with a series of simple volleys like those ofC. plorabunda. Female hybrids from two reciprocal crosses and females and males of the parental species were presented with choices of hybrid and parental songs. Hybrids responded more to recordings of hybrid songs than to recordings ofC. plorabunda but did not differ in the responses given toC. johnsoni and hybrid songs. In contrast, males and females of both parental lines preferred to duet with recordings of their own song types and did not respond to hybrid songs. Our results demonstrate that hybrids would be at a disadvantage in nature, because neitherC. plorabunda norC. johnsoni will respond to their songs.     

A protein‐based approach to mark arthropods for mark‐capture type research

A series of studies was conducted to test methods for marking a wide variety of arthropods with inexpensive proteins for mark‐capture dispersal research. The markers tested included egg albumin protein in chicken egg whites and casein protein in bovine milk. The first study qualified the effectiveness of the two marks on more than 50 arthropod species inhabiting cotton via two application procedures. The application methods included: (1) a topical plus residue protein application, and (2) a residue‐only protein application. Both protein marks, regardless of the method of application, were readily retained on the arthropod assemblage over the duration of the study. The second study determined how rapidly insects acquire chicken egg albumin protein after contact exposure to cotton tissue sprayed with an egg whites solution. Under laboratory conditions, the vast majority of adult Hippodamia convergens Guérin‐Méneville (Coleoptera: Coccinellidae) and Lygus hesperus Knight (Heteroptera: Miridae) acquired the mark after 5 min, and immature Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae) acquired the marker after 40 min. The third study determined how rapidly H. convergens and L. hesperus acquire bovine casein protein after contact exposure to either alfalfa, Medicago sativa L. (Fabaceae), or lesquerella, Lesquerella fendleri (Watson) (Brassicaceae), plants sprayed with a bovine milk solution. These insects rapidly acquired the casein mark from the plant residue under field conditions. A final study determined how long H. convergens retain casein protein after 24‐h exposure to alfalfa and lesquerella plants containing a 7‐day‐old residue of bovine milk. Approximately 95% of the H. convergens maintained the casein mark for 2 days after removal from each type of plant.     

Competitive interactions among two specialist predators and a generalist predator of hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae) in south-western Virginia

1 Competitive interactions among two specialist predators, Laricobius nigrinus and Sasajiscymnus (Pseudoscymnus) tsugae, and a generalist predator, Harmonia axyridis Pallas, of hemlock woolly adelgid, Adelges tsugae were evaluated in hemlock stands in south‐western Virginia. The two specialist predators are part of a biological control program for A. tsugae, and the potential for competition among these species and previously established generalist predators in the field is unknown. 2 Adult predators were evaluated in branch cages during spring and summer at two field sites infested with A. tsugae. Using females only in 2003 and sexual pairs in 2004, predator survival and net reproduction were examined, as well as their feeding and impact on A. tsugae when present alone and in conspecific and heterospecific groupings. 3 Predator survival was not affected by the presence of additional predators. Total feeding was greater for all species when placed in predator groupings, suggesting that interactions do not significantly interfere with feeding activity. Net reproduction per predator was negatively affected by conspecifics, but unaffected by heterospecifics, indicating that direct or indirect intraspecific interference may occur. In spring, L. nigrinus showed the greatest impact on A. tsugae, and H. axyridis had the greatest impact during summer. 4 These results suggest that it would be beneficial to utilize multiple predator species combinations over single species when implementing biological control for A. tsugae. Low‐density releases are also recommended to reduce intraspecific interference.     

Continental dispersal of the cassava green mite,an exotic pest in Africa,and implications for biological control

The continental dispersal of an exotic spider mite species is described for the first time. The cassava green mite,Mononychellus tanajoa (Bondar) (Acari: Tetranychidae), has been found to be dispersed across the cassava belt of Africa in less than 10 years after first being discovered in 1971. This mite disperses within plants by walking, and within and between fields by drifting aerially. Widespread transportation of mite-infested plant material, however, is proposed to explain the rapid spread ofM. tanajoa in Africa. Observations of mite-infested plant material being transported in the field, and laboratory evidence of mite populations surviving up to 60 days on cassava stems removed from the field and isolated from external contaminates, support this hypothesis. The spread ofM. tanajoa in Africa as a model for future introductions on cassava suggests a pattern of movement at species-specific rates. Exotic natural enemies ofM. tanajoa, especially phytoseiid predators, are expected to spread at a rate slower than their host; consequently, large-scale and long-range releases will be needed to accelerate their spread.     

The role of vision and color in the close proximity foraging behavior of four coccinellid species

The role of vision and color in close-proximity foraging behavior was investigated for four species of lady beetles: Coccinella septempunctata, Hippodamia convergens, Harmonia axyridis, and Coleomegilla maculata. The effect of light level and color cues on consumption rates varied among the four predator species. The consumption rates of these predators on the pea aphid Acyrthosiphon pisum (Harris) was measured under light and dark conditions. C. septempunctata,H. convergens, and Ha. axyridis consumed significantly more aphids in the light than in the dark, while the consumption rate of Col. maculata was not affected by light level. Foraging ability was also measured on red and green color morphs of the pea aphid on red, green, and white backgrounds. C. septempunctata consumed significantly more of the aphid morph that contrasted with the background color, and showed no difference between morphs on the white background. H. axyridis consumed significantly more red morph aphids regardless of background. The remaining two species showed no difference in consumption rates on the two color morphs. The variation in the use of visual cues demonstrates how different species of predators can exhibit different foraging behaviors when searching for the same prey. Received: 4 August 1997 / Accepted: 3 February 1998     

The role of predators and parasites in controlling populations ofEarias insulana,heliothis armigera andBemisia tabaci on cotton in the Syrian Arab Republic

Studies on the relationship between insect pests and their predators and parasites were conducted in the Syrian cotton agro-ecosystem from 1980 up to 1983.Earias insulana (Boisduval) was found to be the most damaging pest, whileHeliothis armigera (Hübner) was not an annual returning problem. Among the entomophagous insects found, coccinellids were most numerous during the months June and July and the hemipterous predators were more abundant during August and September. When predator numbers were reduced with insecticide applications, a significant increase in the bollworm populations occurred, resulting in significant reductions in seed cotton yields. Parasites were relatively not important for the control of lepidopterous pests on cotton. Egg and larva populations ofE. insulana andH. armigera were parasitized byTrichogramma spp. andHabrobracon brevicornis Wesmael respectively. Populations ofBemisia tabaci (Gennadius) were heavily parasitized byEretmocerus mundus Mercet.      

Interaction ofManduca sexta resistance in tomato with insect predators ofHelicoverpa zea

Resistance in accession PI 134417 ofLycopersicon hirsutum f.glabratum toManduca sexta L. results from the presence of the methyl ketones 2-tridecanone and 2-undecanone in the type VI trichome glands on foliage of these plants. Short (24 h) and long term (neonate to adult) laboratory experiments usingM. sexta-resistant and susceptible foliage and methyl ketone treated filter paper disks were conducted to evaluate the direct (plant-mediated), and indirect (prey-mediated) effects of this resistance on two predators ofHelicoverpa zea eggs,Coleomegilla maculata (DeGeer) andGeocoris punctipes (Say). Direct effects of resistance were manifest as reduced egg consumption and increased mortality for both predators. Indirect effects were manifest as reduced egg consumption byG. punctipes, but were not observed forC. maculata. Results of experiments using methyl ketone-treated filter paper disks instead of foliage were similar.     

Variation in aluminum resistance among arbuscular mycorrhizal fungi

Arbuscular mycorrhizal (AM) fungi mediate interactions between plants and soils, and are important where nutrient or metal concentrations limit plant growth. Variation in fungal response to edaphic conditions may influence the effectiveness of the plant-mycorrhizal association in some soil environments. Andropogon virginicus (broomsedge) colonizes disturbed sites in the eastern United States, including acidic mine soils where aluminum (Al) is phytotoxic, and Al resistance in broomsedge has been associated with colonization by the AM fungus Glomus clarum. In the present study, inter- and intra-specific variation to confer Al resistance to broomsedge was assessed among selected species of AM fungi. Broomsedge seeds were grown in sand culture inoculated with one of five isolates of three species of fungi (G. clarum, Acaulospora morrowiae, and Scutellospora heterogama). Plants were exposed to 0 or 400 µM Al in nutrient solution and harvested after 4 or 9 weeks of growth. Mean infection percentage, plant biomass, and plant tissue Al and phosphorus (P) concentrations were measured. G. clarum conferred the greatest Al resistance to broomsedge, with the lowest variability among isolates for colonization and growth inhibition by Al [tolerance indices (TI) between 22.4 and 92.7%]. Broomsedge plants colonized by A. morrowiae were consistently the most sensitive to Al, with little variation among isolates (TI between 1.6 and 12.1%). Al resistance by S. heterogama isolates was intermediate and wide-ranging (TI between 3.9 and 40.0%). Across all AM fungal isolates, resistance was associated with high rates of colonization and low tissue Al concentrations of broomsedge plants. The functional diversity in Al resistance displayed by these AM fungi reflect variation in acclimation mechanisms operating in the mycorrhizal symbiosis under environmental stress.     

Field cage performance of two tachinid parasitoids of the tomato fruitworm on insect resistant and susceptible tomato lines

Rates of parasitism ofHelicoverpa (=Heliothis) zea (Boddie) (Lepidoptera: Noctuidae) by two tachinid parasitoid species differing in larviposition habits were measured in field cages on tomato plant lines with or without methyl-ketone (2-tridecanone and 2-undecanone)-mediated insect resistance. Hosts were placed on resistant or susceptible plants, exposed to parasitoids for 24–48 h, then held on artificial diet for parasitoid emergence. Rates of parasitism byArchytas marmoratus (Townsend) (Diptera: Tachinidae), which larviposits on its host's food plant, were significantly reduced on the resistant plants, relative to those on the susceptible plants. Parastism by another Tachinid,Eucelatoria bryani Sabrosky, which larviposits directly into its host and does not directly contact the foliage of its hosts' food plant as a small larva, was not affected by the methyl-ketone mediated resistance.     

Reduction of black vine weevil larval growth by vesicular-arbuscular mycorrhizal infection

Larvae ofOtiorhynchus sulcatus (black vine weevil) were reared at three densities (zero, two or eight), on plants ofTaraxacum officinale (dandelion) with and without infection by the mycorrhizal fungusGlomus mosseae. On plants without the fungus, survival of larvae to late final instar was 84%, but this was only 43% on infected plants. The differential survival of larvae was evident in their effects on plant biomass. Significant interactions were found between larval density and infection, indicating that mycorrhizal presence mitigated the effects of herbivory at the low larval density. Infection byG. mosseae thus conferred some degree of resistance in roots to this insect and the consequences of this for horticultural and natural situations are discussed.     

Field evaluation of insect resistance in a wild tomato and its effects on insect parasitoids

Populations ofHelicoverpa (=Heliothis) zea (Boddie),Heliothis virescens (F.),Manduca sexta (L.) andM. quinquemaculata (Haw.) and their egg and larval parasitoids were sampled in field plots of the: insect-resistant wild tomato,Lycopersicon hirsutum f. glabratum C. H. Mull, accession PI 134417; susceptible commercial tomato cultivar ‘Better Boy’; F₁ hybrid; and selected, moderately resistant backcross genotype. Densities ofH. zea andH. virescens eggs and small larvae were higher on resistant genotypes than on susceptible genotypes, but densities of large larvae were similar on all genotypes. Densities ofManduca spp. larvae were too low to permit similar analyses of the effects of plant genotype. Rates of egg parasitism byTrichogramma spp. andTelenomus sphingis (Ashmead) were reduced on insect-resistant genotypes. Rates of parasitism by the larval parasitoidsCampoletis sonorensis (Cameron) andCotesia congregata (Say) were reduced on resistant genotypes. No consistent effects on parasitism rates byCotesia marginiventris (Cresson) were observed and parasitism rates byCardiochiles nigriceps Viereck were unaffected.