Oriented responses of carrot fly larvae, Psila rosae, to plant odours, carbon dioxide and carrot root volatiles

ABSTRACT. The responses of carrot fly larvae, Psila rosae , to host plant volatiles were studied. Two criteria for an oriented response were used: one based on whether an individual reached within 1.5 cm of the odour source and one involving analysis of the track patterns of larvae within 3 cm of the odour source. All larval instars were attracted to both host and non-host plant material, though to a lesser degree by the latter; they were also attracted to CO₂, but not to N₂. A steam volatile fraction of carrot roots, and methyl eugenol, a volatile component of this fraction, also attracted the larvae, differentially at different concentrations. The possible roles of both CO₂ and the host-specific secondary plant volatiles in the host plant finding behaviour of soil inhabiting arthropods are discussed.     

Behavioural responses of the carrot fly larva, Psila rosae, to carrot root volatiles

ABSTRACT. The behaviour of the carrot fly larva, Psila rosae F. (Diptera, Psilidae), was investigated in the presence of six concentrations of thirty-four volatiles associated with carrot root and of trans -methyl-iso-eugenol, a constituent of carrot herb oil. Bomyl acetate, 2,4-dimethyl styrene, α-ionone, SbT-ionone and biphenyl were the most consistently preferred compounds. Klinotaxis and klinokinesis were the orientation responses near the stimulus source. Trans -2-nonenal was the most consistently avoided compound. Extracts derived by steam distillation of carrot roots and by concentration of vapour from roots were resolved, by gas liquid chromatography, into forty-five and twenty-two major constituents, respectively. The five preferred compounds are micro-components of these extracts, collectively representing 1% and 0.6% of root extract oil and vapour, respectively. It is suggested that these secondary plant constituents are specific host finding cues for the larva, and that frara-2-nonenal is a carrot defence compound.     

Electroantennogram responses of the carrot fly, Psila rosae, to volatile plant components

ABSTRACT. Electroantennogram (EAG) responses of male and female carrot flies, Psila rosae F. (Diptera: Psilidae), were recorded to thirty-six volatile plant constituents. The most distinct EAG responses were obtained to: (1) the general green leaf volatiles 1-hexanol, trans-2-hexen-1-ol and cis-3-hexen-1-ol, their isomers cis-2-hexen-1-ol and trans-3-hexen-1-ol, the alcohol 1-heptanol, the ester cis-3-hexenyl acetate and the leaf aldehydes hexanal and trans-2-hexenal, and (2) from four compounds associated with the umbelliferous host plants of this insect, namely trans-methyl-iso-eugenol, β-caryophyllene, linalool and trans-2-nonenal. Higher responses were elicited by the leaf aldehydes than by the corresponding alcohols. Although the absolute amplitude of the female response was over twice that of the male, there were no differences between the relative responses to the compounds tested in both sexes, with the exception of a much higher response to the leaf aldehydes in the male. The shape of the EAG evoked by the various compounds was consistently different, with the slowest recovery being recorded for trans-methyl-iso-eugenol. While the antennal olfactory receptors of the carrot fly are sensitive to the closely related general green leaf volatiles, they are most specifically tuned to the aldehyde component of this green odour complex. In addition, the ability of this insect to discriminate between different plants may be augmented by the perception of a group of more host specific volatiles. The conformity of the responses of males and females to the compounds tested may indicate that host plant volatiles plays an additional role as an aggregation cue for both sexes.     

The responses of carrot fly larvae, Psila rosae, to components of their physical enrivonment

Abstract. 1. The responses of third instar Psila rosae (F.) larvae to light, temperature, humidity and soil moisture were investigated in the laboratory.
2. Larvae were photonegative and preferred a temperature of about 15°C. Temperatures between 30 and 40°C adversely affected movement and over 40° C were lethal.
3. In choice chambers, larvae preferred humidities of 70–100% r.h. and larvae in sand avoided dry conditions (2.5% field capacity). The latter response became more marked as larvae approached the pre-pupal stage when moistures of 40% field capacity and lower were avoided.
4. Most larvae were found at a depth of 8 cm in sand of uniform moisture content and temperature, but variation in moisture content could alter this preference.
5. In August, most larval damage in the field occurred near the tip of the carrot tap root but was more evenly distributed over the roots in November. It is uncertain whether this was due to soil near the surface being drier in August or whether it was caused by behavioural differences between the two generations of carrot fly larvae.
6. During the summer of 1975, low soil moisture levels resulted in the total absence of larval mines on the carrot roots even though pupae were found at depths of 20–30 cm in the soil. Temperature had no effect on the distribution of mines on carrot roots except at the top 2 cm of the soil profile.     

The contribution of gustatory input to larval acceptance and female oviposition choice of potential host plants in Papilio hospiton (Géné)

The Lepidopteran Papilio hospiton uses only plants belonging to the Apiaceae and the Rutaceae families as hosts. Both adult females and larvae are equipped with gustatory receptor neurons (GRNs) capable of detecting sugars, bitters and salts, thus providing information for evaluating the chemical composition of the plant. Since the activation of these neurons may affect insect behavior, the aim of this study were: (a) to study the gustatory sensitivity of both females and larvae to the sap of two Apiaceae, Foeniculum vulgare (fennel) and Daucus carota (carrot), that are not used as host plants; (b) to cross‐compare the spike activity evoked from these two plants with that evoked by Ferula communis (ferula), the host plant preferred by ovipositing females of P. hospiton and where the larvae perform best; (c) finally, to confirm that the gustatory system can provide the central nervous system with the necessary information to evaluate differences between plant saps. The results show that: (a) fennel and carrot both evoke a higher neural activity from the bitter‐sensitive neurons and lower from the sugar‐sensitive neurons with respect to ferula, in both adult females and larvae; (b) on the basis of the different patterns of neural activity generated in tarsal, lateral and medial sensilla by fennel and carrot versus ferula, both adult and larvae possess enough information to discriminate among these plants; (c) adult females of P. hospiton lay eggs where the larvae have the greatest growth success and this confirms the importance of taste sensitivity in host plants selection.     

An investigation of the host range of the carrot fly

The historical records of the earliest reports of umbelliferous and other hosts of carrot fly ( Psila rosae ) are presented and their validity discussed. In addition, the results are reported of tests made between 1972 and 1980 on 27 species of Umbelliferae and three sub-species of Daucus carota to determine whether they would support the carrot fly. Techniques were developed for identifying plant species as hosts by determining the number of adult flies that emerged from root and soil samples obtained from plants exposed to carrot fly in the field. Experiments in 1979 and 1980 indicating the importance of co-ordinating the life cycles of plant and insect. The results showed that certain annual species of Umbelliferae were unsuitable as hosts in the autumn when they has flowered and senesced. Valid records could only be obtained for these species by exposing the plants to first generation carrot fly attack. Of the 27 species tested, Anthriscus sylvestris, Ferula communis, and Smyrnium olusatrum failed to support carrot fly and the following 13 species were new host records: Aethusa cynapium, Anthriscus caucalis, Apium inundatum, Apium nodiflorum, Bupleurum tenuissimum, Chaerophyllum temulentum, Cicuta virosa, Daucus capillifolius, Daucus glochidiatus, Heracleum mantegazzianum, Ligusticum scoticum, Oenanthe crocata and Sison amomum . From two species, Chaerophyllum temulentum and Torilis japonica , more than two carrot flies/root were recovered. These species are numerous and widespread in carrot-growing districts. The significance of these and other wild host plants in relation to the ecology and control of carrot fly is discussed.     

Carrot fly cultivar preferences: some influencing factors

Abstract. 1. Factors affecting cultivar preferences by the carrot fly Psila rosae F. were examined in choice tests using foliage from carrot lines representing extremes of resistance and susceptibility to attack.
2. Flies were offered a choice to oviposit on foliage, artificial substrates impregnated with leaf surface extracts or enclosed in vapours of different cultivars to establish the importance of contact and olfactory stimuli. Susceptible cv. Danvers Half Long 126 foliage was preferred over that of resistant cvs. Clause's Sytan Original and Tip-Top. But, whereas the Sytan leaf surface extract was as effective as that of Danvers, the surface extract of Tip-Top was very much inferior as an oviposition stimulant. By contrast, Sytan and Tip-Top foliar vapours were both more attractive to the fly than that from Danvers.
3. Headspace vapours over Sytan foliage evoked significantly higher electroantennogram responses than those from Danvers.
4. Cold-trapped foliar volatiles of Sytan and Danvers were analysed by gas chromatography linked with antennographic detection. Foliage of Sytan released, among other chemo-stimulants, higher levels of host plant attractants, i.e. green leaf aldehydes and the phenylpropanoids, trans-asarone and trans-methylisoeugenol.
5. These findings indicate that olfactory and contact chemostimuli may be involved in preferences shown by the carrot fly for carrot cultivars, but these factors alone do not fully account for the preferences observed.     

Foliar form, colour and surface characteristics influence oviposition behaviour of the carrot fly

Various leaf models made of paper were presented to carrot flies, Psila rosae (F.) (Diptera: Psilidae) in choice assays to investigate the effect of non-chemical plant traits on oviposition behaviour. The surrogate leaves differed in colour, shape, surface coating, size and stem length. In the presence of host-plant extracts, physical factors strongly influenced oviposition. Green, yellow and orange three-dimensional models similar in shape to host-plant leaves (pinnately or ternately compound or dissected) and with a thin cover of paraffin wax were most acceptable to the females. Egg-laying was not affected by leaf size, but was negatively correlated with stem length. The results obtained by testing models with simple leaf silhouettes were confirmed in an experiment using more lifelike imitations of real host and non-host leaves. The findings are discussed by an extensive review of similar studies in three other phytophagous fly species (cabbage root fly, onion fly, Hessian fly).     

Host-plant susceptibility to the carrot fly, Psila rosae. 2. Suitability of various host species for larval development

Several apiaceous and two asteraceous species were tested for their suitability to support larval development of the carrot fly. Plants grown in pots or transplanted from seed beds into pots, were inoculated with a specific number of eggs. Pupae and non-pupated larvae were collected 6–7 wk after inoculation. Both the number and weights of pupae produced varied widely among the species. Cultivated carrots Daucus carota sativus often gave rise to only moderate numbers of pupae, but these invariably attained the highest weights. Pimpinella major was the only apiaceous plant tested that did not yield any carrot flies. The two asteraceous plants Cichorium intybus and Tanacetum vulgare failed to support larval development. Total carrot fly biomass produced per plant was influenced by both the host species and the root weight. Emergence rates of adult flies were positively correlated with pupal weights. Small individuals tended to have a longer total developmental time from egg to adult fly.     

Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta

Many plants employ induced responses against generalist herbivores. Specialist herbivores, however, may employ several mechanisms to overcome the negative effects of induced plant defenses. Here we test how the behavior and development of specialist Manduca sexta larvae are affected by induced responses in their natural host plant Nicotiana attenuata. On a spatial scale relevant to both the plant and the herbivore, we first determined how methyl jasmonate (MeJA)-induced responses, such as increased nicotine production, affect the tendency of larvae to leave induced plants. When larvae were allowed to move between two plants planted in one pot, they left an MeJA-treated plant faster than a control plant. When both plants in the pot were MeJA-treated, the larvae developed more slowly than when both plants were uninduced, or when the larvae had the opportunity to move to an uninduced neighbor. The sooner larvae moved from an MeJA-treated plant to an untreated neighbor, the larger the body mass they attained. This demonstrates that M. sexta larvae can compensate behaviorally for the deleterious effects of induced plant responses. These effects were observed in plants grown under both low and high N supply rates, though the effects were more pronounced under high N. To examine the consequences of the timing and the direction of the host plant switching behavior for larval development, neonate larvae were fed leaves excised from induced and uninduced plants. Larvae confined to MeJA-treated leaves had higher mortality rates and grew slower than larvae fed only control leaves. This demonstrates that MeJA-induced responses decrease growth and development of specialist herbivores that do not have the behavioral option of moving to an uninduced plant. The sooner the larvae were switched to MeJA-treated leaves, the slower their development compared to larvae fed only uninduced leaves. In contrast, the sooner larvae fed MeJA-treated leaves were switched to control leaves, the faster they developed. Again the effects of MeJA treatment were stronger in plants grown under high N supply. We propose that induced plants growing in close competition with an uninduced conspecific may offset the fitness costs of these induced responses and perhaps obtain a fitness benefit by motivating herbivores to move to their neighboring competitors. Received: 25 March 1999 / Accepted: 8 October 1999     

Differences in host plant selection among three Athalia sawflies feeding on crucifers in Japan

Abstract 1. The ways of using host plants were compared among the three Athalia sawflies [ A. japonica (Klug), A. rosae ruficornis Jakovlev, and A. infumata (Marlatt)] feeding on crucifers in Japan to determine whether host specialisation can explain the difference in their life-history traits. The occurrence of their larvae was examined on each crucifer species in the field, and the suitability of each crucifer species for the three successive steps of host use by the sawflies was evaluated: microhabitat selection by adult females, female oviposition, and larval growth.
2. There were 11 species of crucifer in the study area, and A. japonica , A. rosae , and A. infumata used nine, seven, and eight species respectively. Thus, sawfly host ranges overlapped.
3. Adult females of A. japonica , A. rosae , and A. infumata preferred shady clumps of crucifers, sunny clumps of crucifers, and disturbed areas respectively.
4. Unsuitable hosts for larval performance such as Brassica oleracea and Arabis plants were eliminated from the host ranges of the three sawflies.
5. Once they chose microhabitats, the suitability of each host plant for female oviposition and larval growth was similar.
6. Because of the divergent preferences for microhabitats, the host plants that were suitable for all the three steps were restricted to different sets of plants among the sawflies: Cardamine for A. japonica , cultivated crucifers ( Raphanus and Brassica ) for A. rosae , and Rorippa for A. infumata . These plants could be recognised as the respective primary host plants.
7. The spatio-temporal distributions of primary hosts were consistent with and explained the pattern of diapause and migration of each sawfly, suggesting that host specialisation caused their life-history traits to differentiate.     

Effects of plant odor on oviposition by the black swallowtail butterfly,Papilio polyxenes (Lepidoptera: Papilionidae)

Black swallowtail females laid more eggs on plant models treated with contact stimulants and volatiles from carrot leaves than on models treated only with contact stimulants. The volatiles enhanced landing rates and females alighted more frequently on artificial leaves treated with host volatiles than on adjacent control leaves. Volatiles from cabbage, a nonhost, inhibited landing rates on artificial leaves treated with carrot contact stimulants. Examination of antennae revealed two major types of sensilla, believed to be olfactory in function. Electroantennogram preparations responded more strongly to carrot volatiles than to cabbage volatiles and several shared responses at particular retention times to carrot volatile components eluting from a gas chromatograph. Our results are consistent with a long-standing hypothesis that behavioral responses to essential oil components characteristic of the larval food plants have facilitated host shifts in the genus Papilio.     

Uptake and turn-over of glucosinolates sequestered in the sawfly Athalia rosae

Larvae of the sawfly Athalia rosae sequester glucosinolates from their various host plants of the Brassicaceae into their hemolymph for defensive purposes. We found that the glucosinolate concentration in the insect varies in a fluctuating manner during larval development. Analyses of larvae which had been offered diets with different glucosinolate profiles showed that there is an equilibrium between a rapid uptake of glucosinolates into the hemolymph and a continuous turn-over. Injection of glucotropaeolin into the hemolymph and ingestion of the same amount resulted in similar levels of intact glucosinolates recovered from larvae after different periods of time. This indicates that hemolymph glucosinolates are the principal source for glucosinolate degradation. Feeding experiments with [14C]-labeled glucotropaeolin revealed that the majority of the ingested glucosinolate is excreted as one or more unidentified metabolite(s) within 14 h. We found no indication for the presence of an insect myrosinase, or sulfatase in A. rosae, which have been shown to be involved in glucosinolate metabolism in other specialists feeding on Brassicaceae. Furthermore, the metabolism of sinalbin in A. rosae seems to result in different products than its metabolism in the caterpillar Pieris rapae. Obviously, A. rosae has yet another way of coping with the glucosinolates.     

The effects of host age and superparasitism by the parasitoid, Microplitis rufiventris on the cellular and humoral immune response of Spodoptera littoralis larvae

To study the dynamics of stage-dependent immune responses in Spodoptera littoralis (Boisd.) larvae (Lepidoptera: Noctuidae), single and superparasitism experiments were carried out using the parasitoid Microplitis rufiventris Kok. (Braconidae: Hymenoptera). Compared to younger (preferred) host larvae, the older (non-preferred) host larvae displayed a vigorous humoral response that often damaged and destroyed the single wasp egg or larva. Superparasitism and host age altered both the cellular and humoral immune responses. Younger host larvae showed a stronger encapsulation response compared to older host larvae. Moreover encapsulation rates in younger hosts (e.g., second instar) decreased with increasing numbers of parasitoid eggs deposited/larvae. In older larvae, the encapsulation rate was low in fourth, less in fifth and absent in sixth instar hosts. Conversely, the order and magnitude of the cellular immune response in S. littoralis hosts were highest in second instar larvae with the first instar larvae being a little lower. The immune response steadily decreased from the third through to the fifth instar and was least obvious in the sixth instar. In contrast, the general humoral immune response was most pronounced in sixth instar larvae and diminished towards younger stages. The results suggest that both cellular and humoral responses are stage-dependent. Wasp offspring in younger superparasitized host larvae fought for host supremacy with only one wasp surviving, while supernumerary wasp larvae generally survived in older superparasitized larvae, but were unable to complete development. Older instars seem to have a method for immobilizing/killing wasp larvae that is not operating in the younger instars.     

Host plant odor extracts with strong effects on oviposition behavior in Papilio polyxenes

Ovipositing females of the black swallowtail butterfly, Papilio polyxenes Fabricius (Lepidoptera: Papilionidae: Papilioninae), have an innate response to contact chemical cues, but it was not known how naïve females would respond to volatile host plant chemicals. Naïve and experienced females were tested in a free-flight experiment using model plants and volatile extracts from two hosts, carrot [ Daucus carota L. (Apiaceae)] and poison hemlock [ Conium maculatum L. (Apiaceae)], and one non-host, fava bean [ Vicia faba L. (Fabaceae)]. Naïve females responded to both host plant extracts with more approaches and landings than to non-host extracts, with poison hemlock receiving more responses than carrot. Females experienced with one of the two host plants also approached and landed frequently on extracts of host plants, but poison hemlock again received more approaches and landings, regardless of a female's host plant experience. Female P. polyxenes thus respond specifically to volatile extracts of their host plants, even in the absence of both relevant contact chemical cues and adult host plant experience.     

Effectiveness of the defence mechanism of the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae), against predation by lizards

The turnip sawfly, Athalia rosae Linnaeus, is a pest on cruciferous crops. Larvae sequester secondary plant compounds, namely glucosinolates, in their haemolymph. When attacked, their integument is easily disrupted and a droplet of haemolymph is exuded ('easy bleeding'). This has been shown to be an effective, chemical-based, defence against invertebrate predators. The efficiency of this proposed defence was tested against a vertebrate predator, using groups of the iguanid lizard Anolis carolinensis Voigt as a model predator. Caterpillars of Pieris rapae Linnaeus and Pieris brassicae Linnaeus served as control prey species that do not sequester glucosinolates. Lizards attacked far fewer sawfly larvae than pierid caterpillars. Several of the sawfly larvae were rejected after an initial attack, demonstrating unpalatability to the lizards, while the Pieris larvae were not rejected. However, P. rapae larvae topically treated with extracts of haemolymph of A. rosae had no deterrent effect on the lizards and no avoidance learning occurred over a period of two weeks. Adult sawflies do not easy bleed but have glucosinolates carried over from the larval stage. Lizards attacked them at a higher rate than larvae and they were never rejected. The results suggest that for the defensive effectiveness of the pest sawfly species against vertebrates the chemical cue is not necessarily sufficient. Movement and colour may be important additional factors triggering the behaviour of vertebrate predators.     

Consumption of carrot weevil,Listronotus oregonensis, [Coleoptera: Curculionidae] by four species of carabids on host plants in the laboratory

Four carabid species,Anisodactylus santaecrucis, Bembidion quadrimaculatum oppositum, Pterostichus lucublandus andPterostichus melanarius, abundant in carrot fields in southwestern Quebec, were tested for predation against the carrot weevil,Listronotus oregonensis, on host plants. The largest species,Pterostichus melanarius, consumed the greatest number of carrot weevil larvae and pupae.Bembidion quadrimaculatum oppositum did not prey on carrot weevil eggs laid on carrot leaves.      

Maintenance of narrow diet breadth in the monarch butterfly caterpillar: response to various plant species and chemicals

In order to better understand the maintenance of a fairly narrow diet breadth in monarch butterfly larvae, Danaus plexippus L. (Lepidoptera: Nymphalidae: Danainae), we measured feeding preference and survival on host and non-host plant species, and sensitivity to host and non-host plant chemicals. For the plant species tested, a hierarchy of feeding preferences was observed; only plants from the Asclepiadaceae were more or equally preferred to Asclepias curassavica, the common control. The feeding preferences among plant species within the Asclepiadaceae are similar to published mean cardenolide concentrations. However, since cardenolide data were not collected from individual plants tested, definitive conclusions regarding cardenolide concentrations and plant acceptability cannot be made. Although several non-Asclepiadaceae were eaten in small quantities, all were less preferred to A. curassavica. Additionally, these non-Asclepiadaceae do not support continued feeding, development, and survival of first and fifth-instar larvae. Preference for a host versus a non-host (A. curassavica versus Vinca rosea) increased for A. curassavica reared larvae as compared to diet-reared larvae suggesting plasticity in larval food preferences. Furthermore, host species were significantly preferred over non-host plant species in bioassays using a host plant or sucrose as a common control. Larval responses to pure chemicals were examined in order to determine if host and non-host chemicals stimulate or deter feeding in monarch larvae. We found that larvae were stimulated to feed by some ubiquitous plant chemicals, such as sucrose, inositol, and rutin. In contrast, several non-host plant chemicals deterred feeding: caffeine, apocynin, gossypol, tomatine, atropine, quercitrin, and sinigrin. Additionally the cardenolides digitoxin and ouabain, which are not in milkweed plants, were neutral in their influence on feeding. Another non-milkweed cardenolide, cymarin, significantly deterred feeding. Extracts of A. curassavica leaves were tested in bioassays to determine which components of the leaf stimulate feeding. Both an ethanol extract of whole leaves and a hexane leaf-surface extract are phagostimulatory, suggesting the involvement of both polar and non-polar plant compounds. These data suggest that the host range of D. plexippus larvae is maintained by both feeding stimulatory and deterrent chemicals in host and non-host plants.     

The role of pre- and post-imaginal experience in the host-finding and oviposition behaviour of the cabbage moth

The influence of pre- and post-imaginal experience on the orientation, landing, and oviposition of the female cabbage moth, Mamestra brassicae (L.) (Lepidoptera: Noctuidae) was studied in a wind tunnel. The results of experiments on the influence of pre-imaginal experience do not support the Hopkins host selection hypothesis because the females’ responses to host plants were not affected by the plant species used for feeding the larvae. The females were initially attracted to and landed on chrysanthemum whether or not they were fed on this plant species. In addition, the oviposition preference for cabbage plants was not changed by the larval feeding regimen. Imaginal experience influenced the females’ subsequent orientation/landing responses: exposure of the females to chrysanthemum plants for 5 min decreased their subsequent responses to this species, but subsequent responses to cabbage were not changed when the females were exposed to cabbage plants. Overnight exposure of females to a chrysanthemum or cabbage plant decreased the subsequent orientation/landing on the same species offered in non-choice tests. A similar effect was observed in responses to chrysanthemum plants after overnight contact, and possibly to cabbage plants, in the two-choice tests. Overnight exposure to cabbage or chrysanthemum had no effect on subsequent oviposition: females from both treatments oviposited more often on cabbage.