Geographic variation in clutch size and a realized benefit of aggregative feeding

We investigated one causal explanation for geographic variation in clutch size and aggregative feeding of the pipevine swallowtail, Battus philenor. Populations in California lay larger clutches than those in Texas, and larger feeding aggregations grow at an accelerated rate on the California host plant. Using reciprocal transplant experiments with larvae from California and Texas populations, we found that the benefit of increased growth rate associated with feeding in larger groups occurred only on the California host plant and was observed for larvae from both populations. These results are consistent with the hypothesis that larger clutch size and aggregative feeding are adaptations to characteristics of the California host plant. Future studies on the evolution of clutch size and aggregative feeding of herbivorous insects should consider how these life-history traits affect host plant suitability.     

Temporal dynamics of herbivore‐induced responses in Brassica juncea and their effect on generalist and specialist herbivores

Herbivore feeding may induce an array of responses in plants, and each response may have its own temporal dynamics. Precise timing of these plant responses is vital for them to have optimal effect on the herbivores feeding on the plant. This study measured the temporal dynamics of various systemically induced responses occurring in Brassica juncea (L.) Czern. (Brassicaceae) leaves after insect herbivory in India and The Netherlands. Morphological (trichomes, leaf size) and chemical (glucosinolates, amino acids, sugars) responses were analysed. The effects of systemic responses were assessed using a specialist [Plutella xylostella L. (Lepidoptera: Plutellidae)] and a generalist [Spodoptera litura Fabricius (Lepidoptera: Noctuidae)] herbivore. We tested the hypotheses that morphological responses were slower than chemical responses and that generalist herbivores would be more affected by induced responses than specialists. Glucosinolates and trichomes were found to increase systemically as quickly as 4 and 7 days after herbivore damage, respectively. Amino acids, sugars, and leaf size remained unaffected during this period. The generalist S. litura showed a significant feeding preference for undamaged leaves, whereas the specialist herbivore P. xylostella preferred leaves that were damaged 9 days before. Performance bioassays on generalist S. litura revealed that larvae gained half the weight on leaves from damaged plants as compared to larvae feeding on leaves from undamaged plants. These studies show that although morphological responses are somewhat slower than chemical responses, they also contribute to induced plant resistance in a relatively short time span. We argue that before considering induced responses as resistance factors, their effect should be assessed at various points in time with both generalist and specialist herbivores.     

Crocidolomia pavonana larval foraging: behavior and feeding site preferences on cabbage, Brassica oleracea

Experiments were conducted to determine feeding site preferences of Crocidolomia pavonana (Fabricius) (Lepidoptera: Crambidae) larvae within cabbage plants, Brassica oleracea L. var. capitata cv. Warrior (Brassicaceae), and to determine whether induced plant responses to herbivory affect the behavior of larvae. In the first experiment, intra-plant damage and larval distribution were recorded to account for the spreading pattern of damage and larval feeding behavior on a plant; larvae initially fed on the base of leaves and moved progressively to the bud, leaf tips were avoided. In the second experiment, larval performance (the duration of the first instar, survival to the second instar, and weight of second instars) was assessed when larvae fed on the bud, the base, and the tip of the youngest fully expanded leaf on a plant. Crocidolomia pavonana larvae performed best when they fed on bud leaf tissue and most poorly when they fed on leaf tissue at the base of leaves. In the third experiment, expression of induced resistance was tested on each of the three plant parts using a first-instar bioassay. Negative impacts on larval growth and development were not detected when larvae fed on the bud or base tissue when plants were damaged prior to the assay. However, negative effects were detected in larvae feeding on tip leaf tissue when the base of the leaf was damaged prior to the assay or if the bud tissue was damaged simultaneously with the assay. The findings indicate that resource heterogeneity for C. pavonana within-cabbage plants is determined by both the initial quality of food at a location and by subsequent induced changes as a result of larval feeding; both contribute to the feeding pattern observed in these gregarious larvae.     

Does group feeding by toxic prey confer a defensive benefit? Aristolochic acid content,group size and survival of first‐instar pipevine swallowtail (Battus philenor L.) larvae

1. Aggregative feeding of larvae is widespread in the Lepidoptera, and many hypotheses have been proposed to explain the adaptive significance of this trait. Group feeding occurs disproportionately more in species with aposematic, chemically defended larvae compared with species with cryptic, non‐chemically defended larvae, consistent with the hypothesis that group feeding provides an enhanced aposematic signal to natural enemies. Most species characterised as having chemically defended larvae are cryptic during the first instar, when they are most highly aggregated and most vulnerable to predation. 2. The benefits of group feeding in terms of decreased predation were explored for first‐instar larvae of the pipevine swallowtail, Battus philenor, a species that sequesters aristolochic acids from its Aristolochia host plant and exhibits aposematism in later instars and as adults. We found that groups of larvae with experimentally enhanced aristolochic acid content had significantly lower survivorship due to predation both in the field and in laboratory experiments compared with groups of larvae without enhanced chemical defence. 3. A laboratory experiment found that aristolochic acid does not deter the generalist predator Hippodamia convergens. 4. No evidence was found that was consistent with the hypothesis that group feeding and increased sequestered chemical defence interact to decrease rates of larval mortality in non‐aposematic, first‐instar larvae. Future research on chemical defence, aposematism, and aggregative feeding should continue to appreciate that particular chemical defences and feeding behaviours are not universally effective against all natural enemies.     

The consequences of larval aggregation in the butterfly Chlosyne lacinia

1. Females of Chlosyne lacinia (Geyer) (Lepidoptera: Nymphalidae, Melitaenae), the bordered patch butterfly, clump eggs in a few large clusters on their host plant, Helianthus annuus. Resulting larvae form sibling aggregations to at least the third instar.
2. The effect of group size on survival and development of C. lacinia larvae was tested experimentally in the field. Larvae developed faster and survived better in larger groups.
3. The effects of various predator guilds (ground-dwelling arthropods, aerial arthropods and avian predators) on survival of larvae was then tested while controlling group size. Ground-dwelling arthropods, mainly fire ants Solenopsis xyloni , reduced larval survival greatly but other solitary invertebrate and avian predators did not alter survival. Group defences and aposematism of C. lacinia larvae are probably ineffective against predatory ants that attack en masse and recruit other colony members.
4. In laboratory experiments, two possible mechanisms underlying faster development of larvae in larger groups were tested: (i) overcoming the physical toughness of host plant leaves, and (ii) social stimulus to feed. Results support the physical toughness hypothesis but not the social stimulus hypothesis.
5. Feeding in large groups by C. lacinia larvae confers multiple advantages, including protection from solitary predators and increased feeding efficiency because grouped, early-instar larvae can initiate feeding wounds on tough sunflower leaves. These advantages of larval gregariousness, coupled with reduced desiccation at the egg stage, apparently outweigh disadvantages of aggregation, such as interference and exploitative competition among larvae.     

Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does not induce plant indirect defences

Abstract.  1. Recent research has addressed the function of herbivore-induced plant volatiles in attracting natural enemies of feeding herbivores. While many types of insect herbivory appear to elicit volatile responses, those triggered by gall insects have received little attention. Previous work indicates that at least one gall insect species induces changes in host-plant volatiles, but no other studies appear to have addressed whether gall insects trigger plant indirect defences.
2. The volatile responses of wheat to feeding by larvae of the Hessian fly Mayetiola destructor (Say) (Diptera: Cecidomyiidae) were studied to further explore indirect responses of plants to feeding by gall insects. This specialist gall midge species did not elicit a detectable volatile response from wheat plants, whereas a generalist caterpillar triggered volatile release. Moreover, Hessian fly feeding altered volatile responses to subsequent caterpillar herbivory.
3. These results suggest that Hessian fly larvae exert a degree of control over the defensive responses of their host plants and offer insight into plant-gall insect interactions. Also, the failure of Hessian fly larvae to elicit an indirect defensive response from their host plants may help explain why natural enemies, which often rely on induced volatile cues, fail to inflict significant mortality on M. destructor populations in the field.     

Plant‐mediated interactions among above‐ground and below‐ground life stages of a root‐feeding weevil

1. Interactions among herbivores mediated by plant responses to herbivore injury may have large impacts on herbivore population densities. Responses may persist for weeks after injury and may affect not only the initial (inducing) herbivore, but also herbivores that are spatially or temporally separated from the initial attacker. 2. In many plant–insect interactions, multiple life stages of the insect may be associated with the same plant, and these various stages may interact indirectly with one another via induced responses. The rice water weevil (RWW), Lissorhoptrus oryzophilus, a serious global pest of rice, is one such insect. A series of experiments were performed with root‐feeding larvae and leaf‐feeding adults of the RWW using three conventional rice varieties. 3. The first objective of this study was to test whether RWW adult feeding on rice leaves resulted in altered oviposition by subsequent adults. The hypothesis for the first objective was that RWW adult feeding would decrease plant suitability, resulting in reduced oviposition by subsequent adults. 4. The second objective was to test whether injury by RWW larvae to rice roots resulted in altered oviposition by subsequent adults. The hypothesis for the second objective was that below‐ground RWW larval feeding would decrease plant suitability of rice to above‐ground RWW adults, resulting in decreased oviposition. 5. Results provided inconsistent support for the first hypothesis, indicating that responses differed among combinations of variety and injury level. Conversely, consistent support for the second hypothesis was found, indicating that larval feeding on roots decreased suitability of rice plants for oviposition.     

Species-specific herbivore–herbivore interactions and plant responses to sequential attack by multiple herbivores on a perennial woody plant

When plants are sequentially attacked by multiple herbivores, herbivore identity and host specialization can greatly influence the patterns of herbivore–herbivore and plant–herbivore interactions. However, how prior herbivory and the resulting induced plant responses potentially affect subsequent herbivores deserves further investigation. In this study, we conducted a common-garden experiment that manipulated sequential herbivory by the specialist caterpillar Gadirtha fusca Pogue (Lepidoptera: Nolidae) and the generalist caterpillar Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) on Chinese tallow, Triadica sebifera (L.) Small (Euphorbiaceae). We tested how prior exposure to herbivores with different levels of host specialization affected the performance of subsequently arriving con- and heterospecifics, as well as plant growth and defense responses under subsequent herbivory. We found that prior exposure to the specialist G. fusca facilitated the performance of subsequent conspecifics, resulting in a significant decrease in the growth (height and stem diameter at ground level) of tallow plants. However, prior exposure to the generalist S. litura did not affect the feeding of subsequent con- or heterospecifics or the growth of tallow plants. Sequential herbivory by specialist and generalist conspecifics resulted in lower levels of tannins and flavonoids, respectively, in leaves of tallow plants, whereas sequential herbivory by the two species did not affect the levels of tannins or flavonoids, compared to a single damage event. We conclude that herbivore species-specific plant responses appear to be more important than herbivore identity or specialization in determining herbivore–herbivore interactions and plant responses to sequential herbivore attack.     

The alkaloidal responses of wild tobacco to real and simulated herbivory

Summary I compared the induced alkaloidal response in undamaged leaves of plants subjected to herbivory by the larvae of Manduca sexta and to different simulations of this herbivory; all herbivory treatments removed similar amounts of leaf mass. Although larval feeding induced a significant increase (2.2x) in alkaloid concentrations compared to undamaged plants, the alkaloid responses to larval feeding were significantly lower than the responses to an herbivory simulation (4x controls) which involved removing the same amount of leaf area from the same positions on the leaf, over a similar time period. Moreover, another herbivory simulation, identical in amount of leaf mass removed and duration of damage to the larval feeding, but without regard to spatial array of leaf damage, resulted in an alkaloidal response (5.5x controls) higher still than the previous herbivory simulation. In a second experiment the importance of leaf vein damage on the induced alkaloidal response was examined. Here, leaf removal that involved cutting leaf tissues from between secondary veins before removing the midrib, resulted in alkaloidal responses that were significantly lower (1.7x controls) than responses from leaf removal that involved cutting both veins and midribs along with the intervein tissues (2.6x controls). Vein damage alone did not produce a significant response. These results indicate that herbivory is difficult to simulate: that how a leaf is damaged can be as important as the magnitude of leaf damage in determining a plant's response to damage.     

Effects of elicitation treatment and genotypic variation on induced resistance in Populus: impacts on gypsy moth (Lepidoptera: Lymantriidae) development and feeding behavior

We examined the effects of various wounding treatments and genotypic variation on induced resistance in Populus (Salicales: Salicaceae) against herbivory by the gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae). Second-instar larvae grew and consumed less on leaves from induced than non-induced trees. Likewise, larvae preferred leaf disks from non-induced trees. Among induction treatments, gypsy moth feeding had the strongest and most consistent effect in behavioral choice tests. Mechanical wounding of leaves and mechanical wounding plus application of gypsy moth regurgitant had intermediate effects, while application of jasmonic acid had the weakest overall effect. Under no-choice conditions, there were no consistent trends across clones in the ability of various treatments to elicit plant responses affecting the herbivore. Levels of constitutive and inducible resistance to herbivory varied significantly among 12 Populus clones. Larvae grew up to 30-fold more, and consumed up to 250-fold more on the most suitable than the least suitable clone. Prior feeding by gypsy moths reduced larval feeding up to 71.4% on the most highly inducible clone, but it had little or no effect for the least inducible clones. There was no evidence for a relationship between levels of inducible and constitutive resistance, or between inducible resistance and phylogenetic relatedness among clones. We discuss implications for the ecology and evolution of plant-insect interactions and the management of insect pests. Received: 12 October 1998 / Accepted: 22 March 1999     

Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus

Aims Although ecological interactions are often conceptualized and studied in a pairwise framework, ecologists recognize that the outcomes of these interactions are influenced by other members of the community. Interactions (i) between plants and insect herbivores and (ii) between plants and mycorrhizal fungi are ubiquitous in terrestrial ecosystems and may be linked via common host plants. Previous studies suggest that colonization by arbuscular mycorrhizal fungi (AMF) can modify plants' induced responses to herbivore attack, but these indirect effects of fungal symbionts are poorly understood. I investigated the role of AMF in induced plant response to a generalist herbivore.Methods I manipulated AMF status and herbivory in Cucumis sativus L. (cucumber, Cucurbitaceae) in a greenhouse to investigate induced responses in the presence and absence of the mycorrhizal fungus Glomus intraradices (Glomeraceae). Spodoptera exigua Hübner (Noctuidae) were used to manipulate prior damage and later as assay caterpillars. I also measured G. intraradices and herbivory effects on plant N and effects on plant growth.Important findings AMF status affected the induced response of C. sativus, underscoring the importance of incorporating the roles of plant symbionts into plant defense theory. Assay caterpillars ate significantly more leaf tissue only on mycorrhizal plants that had experienced prior damage. Despite more consumption, biomass change in these caterpillars did not differ from those feeding on plants with other treatment combinations. Leaf N content was reduced by G. intraradices but unaffected by herbivory treatments, suggesting that the observed differences in assay caterpillar feeding were due to changes in defensive chemistry that depended on AMF.     

Aggregation facilitates larval growth in the neotropical nymphalid butterfly Chlosyne janais

1. Larvae of Chlosyne janais (Lepidoptera: Nymphalidae) feed gregariously as early instars on the shrub Odontonema callistachyum (Acanthaceae). During the fourth instar, aggregations break up and larvae feed as solitary individuals.
2. The hypothesis that aggregation increases growth rate was tested by raising larvae on intact plants in the field in different group sizes and measuring their daily growth.
3. There was a striking effect of group size on larval growth whereby larvae more than doubled their weight gain by feeding in large rather than small aggregations on intact plants in the field.
4. This group-feeding advantage was lost altogether if larvae were raised on excised leaves in the laboratory, suggesting that large aggregations may facilitate growth either by inducing a nutrient sink or by overwhelming an induced allelochemical response in the plant.
5. Although larval survival was higher in cages that excluded enemies than in exposed aggregations, there was no influence of group size (experimentally manipulated) on short-term survival in the field. However, there was a weak positive relationship between short-term survival and the size of naturally occurring larval aggregations in the field. These data provide mixed support for the notion that gregarious feeding promotes defence against natural enemies.
6. Although the group defence hypothesis warrants further investigation, feeding facilitation is clearly an important factor contributing to the aggregation behaviour of C. janais larvae.     

Comparative processing of allelochemicals in the Papilionidae (Lepidoptera)

Within the family Papilionidae (Lepidoptera), species display a broad range of feeding patterns, from oligophagy on a single hostplant family to polyphagy on over a dozen families. Accompanying this diversity of feeding strategies is a diversity of physiological mechanisms for processing hostplant allelochemicals. Studies on members of this family as well as other Lepidoptera suggest that oligophagy is associated with high activity, in addition to high substrate specificity, of detoxicative enzymes.     

Herbivore‐induced plants do not affect oviposition but do affect fitness of subsequent herbivores on canola

The diamondback moth (DBM), Plutella xylostella (L.) (Lepidoptera: Plutellidae), is oligophagous on plants in the Brassicaceae, and is considered one of the most significant insect pests of canola (Brassica napus L.), a major oilseed crop grown in the Prairie Provinces of Canada. The bertha armyworm (BAW), Mamestra configurata Walker (Lepidoptera: Noctuidae), is a generalist herbivore that preferentially feeds on canola plants. In the canola growing season in the Prairie Provinces of Canada, DBM feeding occurs prior to BAW herbivory. In this study, we test the effect of DBM herbivory on subsequent host use by BAW. Oviposition by female BAW was not influenced by previous DBM‐herbivory or mechanical damage of canola plants. Bertha armyworm larvae were deterred from feeding on canola previously damaged by DBM and larvae developed into lighter pupae when reared on DBM‐damaged plants. Bertha armyworm pupae that developed from larvae fed on mechanically damaged plants had similar pupal weights to those fed undamaged plants. Adult BAW reared on canola with previous DBM feeding damage had marginally smaller wings than moths reared on canola treated differently. The combination of these results suggests that herbivory by the brassicaceous specialist, DBM, negatively influences host use and larval performance by the generalist, BAW, on canola.     

Solar ultraviolet-B radiation alters the attractiveness of Arabidopsis plants to diamondback moths (Plutella xylostella L.): impacts on oviposition and involvement of the jasmonic acid pathway

Solar ultraviolet-B radiation (UV-B) can have large impacts on the interactions between plants and herbivorous insects. Several studies have documented effects of UV-B-induced changes in plant tissue quality on the feeding performance of insect larvae. In contrast, the effects of UV-B-induced plant responses on the behavior of adult insects have received little attention. We carried out a series of field and glasshouse experiments using the model plant Arabidopsis thaliana L. and the crucifer-specialist insect Plutella xylostella L. (diamondback moth) to investigate the effects of UV-B on natural herbivory and plant–insect interactions. Natural herbivory under field conditions was less severe on plants exposed to ambient UV-B than on plants grown under filters that attenuated the UV-B component of solar radiation. This reduced herbivory could not be accounted for by effects of UV-B on larval feeding preference and performance, as P. xylostella caterpillars did not respond to changes in plant quality induced by UV-B. In contrast, at the adult stage, the insects presented clear behavioral responses: P. xylostella moths deposited significantly more eggs on plants grown under attenuated UV-B levels than on plants exposed to ambient UV-B. The deterring effect of UV-B exposure on insect oviposition was absent in jar1-1, a mutant with impaired jasmonic acid (JA) sensitivity, but it was conserved in mutants with altered ethylene signaling. The jar1-1 mutant also presented reduced levels of UV-absorbing phenolic compounds than the other genotypes that we tested. Our results suggest that variations in UV-B exposure under natural conditions can have significant effects on insect herbivory by altering plant traits that female adults use as sources of information during the process of host selection for oviposition. These effects of natural UV-B on plant quality appear to be mediated by activation of signaling circuits in which the defense-related hormone JA plays a functional role.     

Bird predation on herbivorous insects: indirect effects on sugar maple saplings

Insectivorous birds have been shown to have direct effects on abundances of herbivorous arthropods, but few studies have tested the indirect effects of birds on plant performance through consumption of herbivorous insects. In a 3-year study at the Hubbard Brook Experimental Forest, New Hampshire, we tested whether bird predation indirectly affects leaf herbivory levels and leaf and shoot biomass production of understory sugar maple (Acer saccharum) saplings. Trees were randomly assigned to one of four treatments: an insecticide application to reduce herbivory levels, exclosures that prevented bird access, addition of Lepidoptera larvae, and controls. Trees sprayed with an insecticide supported significantly fewer Lepidoptera larvae than other treatments throughout the study. Also, trees in exclosures supported more Lepidoptera larvae than controls during one count each year, and pooled across all counts during the second year. As predicted, the mean proportion of leaf area consumed varied significantly among treatments and was least in the insecticide treatment, followed by controls, exclosures, and Lepidoptera additions. Significant differences among treatments in herbivory levels, however, did not lead to differences in leaf or shoot biomass production. Thus, bird predation decreased Lepidoptera abundances and decreased herbivory levels, but did not increase biomass production during the following year. Over 85% of the herbivores in our study were Homoptera nymphs that were not folivorous and are not important bird prey items, potentially dampening the indirect effects of bird predation on biomass production. A comparison of these results with previous studies suggests that the indirect effects of bird predation on plant biomass production may depend on the plant species, abundance and composition of the herbivore community, and primary productivity of the ecosystem.     

Gregariousness and repellent defences in the survival of phytophagous insects

Group living has both costs and benefits for plant‐feeding insects, but defence against predators is the most widely acknowledged benefit. Gregarious folivores typically have warning coloration and elaborate anti‐predator defences. Do these defences protect these species from predation? To see if protection from predators generally results from gregariousness, I compared the shapes of published survivorship curves of externally feeding, gregarious and solitary Lepidoptera and Symphyta. Gregarious species are less likely than solitary species to die in the larval stages. However, solitary species that have anti‐predator defences do not have higher larval survival compared to gregarious species. This result, along with evidence from experimental manipulations of group size, suggests that repellent defences per se do not increase survival of gregarious larvae. Group behaviour is undoubtedly important in affecting the higher larval survival of gregarious species, but we currently cannot determine whether predator learning, dilution of risk, or rapid development contribute most to increasing survival.     

Superparasitism in Cotesia glomerata does not benefit the host plant by reduction of herbivory caused by Pieris brassicae

Superparasitism occurs in Cotesia glomerata L. (Hymenoptera: Braconidae), a gregarious endoparasitoid of Pieris spp. (Lepidoptera: Pieridae). The responses of Pieris brassicae L. larvae to superparasitism were examined in order to elucidate the ecological significance of this behaviour. Models of tritrophic interactions often imply that attraction of herbivore natural enemies by the plant constitutes a defence. Parasitoid attack on herbivores is assumed to result in a reduction in herbivory and or an increase in plant fitness. Coupled with the active involvement of the plant in producing signals, this can be seen as an indirect mediation of wound induced defence. The results show that superparasitism of P. brassicae by the parasitoid C. glomerata reduced survivorship but increased food consumption and weight growth in P. brassicae larvae. The duration of host larval development was found prolonged as the number of oviposition increased and superparasitized larvae (three to five time parasitized) grew slower than unparasitized larvae or larvae parasitized one or two times.