Oviposition-deterring Pheromone Research Articles

Substrate-Borne Marking in the Parasitoid Wasp Urolepis rufipes (Hymenoptera: Pteromalidae).

Many animals use pheromone marking as a way to identify their territory or other resources. Among insects, substrate-borne marking is frequently reported for females, which in many species make marks containing oviposition-deterring pheromone, which other females avoid. However, there are fewer reports of substrate-borne marking for males. Here, marking in males of the parasitoid wasp Urolepis rufipes (Ashmead) is described. The conditions under which males mark and whether males and females respond to the males' marks were examined using behavioral observations. Males marked by dragging the tips of their abdomens across a substrate. They marked much more after mating and after consuming honey. They also marked more when with a female, irrespective of copulation, although not when with a male. Females spent more time on or near marked substrates, and males also responded to their own marks. Although males aggressively and successfully defended areas that they had marked against other males, males did not respond to another male's marks in the conspecific's absence. In contrast to males, females did not mark, either on the surface of hosts or on other surfaces, and males showed no detectable response to surfaces which females had recently occupied.

Behavioural evidence for a putative oviposition-deterring pheromone in the butterfly, Phengaris (Maculinea) teleius (Lepidoptera: Lycaenidae)

Larvae of the endangered Scarce Large Blue butterfly, Phengaris (Maculinea) teleius, are initially endophytic, feeding upon developing seeds of Sanguisorba officinalis, but complete their development as social parasites preying on the brood of Myrmica ants. Females show very specific preferences, laying eggs exclusively in young flower heads of the food plant. In the present contribution we report the results of a detailed study of female behaviour at three sites differing in size and abundance of S. officinalis. Tracked individuals switched between feeding on nectar (nectaring), flight and oviposition. They fed exclusively on flowers of reddish, pink or violet colouration, favouring Viccia cracca and S. officinalis. However, females spent about one fifth of the time they were active ovipositing and laid about 20 eggs per hour. Oviposition visits to flower heads were highly stereotyped and followed a specific ritual. Examination of accepted, rejected and randomly sampled flower heads showed that females avoided those containing conspecific eggs and at a site where this was difficult due to a shortage of suitable flower heads, they tended to distribute their eggs evenly among the available flower heads. Our results indirectly indicate the existence of an oviposition-deterring pheromone (ODP) in P. teleius. This hypothetical marking ensures a more even distribution of eggs and possibly increases the chances of survival of caterpillars by reducing competition during both the phytophagous and myrmecophagous stages of development. There are few reports of butterflies producing ODPs and to our knowledge this is the first evidence of their presence in the family Lycaenidae.

Evolution of cannibalism and female’s response to oviposition‐deterring pheromone in aphidophagous predators

1. Egg cannibalism by larvae is common in Coccinellidae and is known to be advantageous for the cannibals. Furthermore, larvae of aphidophagous ladybirds usually produce an oviposition-deterring pheromone (ODP), which inhibits oviposition by adult females. It has been proposed that the response to ODP has evolved because of the high costs of cannibalism. However, this has never been formally proved. 2. In this paper, we study the theoretical evolution of this system. We first look at the conditions under which cannibalism and the response to ODP can evolve. Subsequently, we examine the occurrence of polymorphism both in the production of larval tracks and in the sensitivity of females to specific pheromones. 3. The models predict that the amount of cannibalism should not depend on prey density and that evolution should lead to a continuous increase in cannibalism, and consequently larvae should always cannibalize eggs when possible. In response to the cost of cannibalism, ODP recognition can evolve, so that females avoid laying eggs in patches of prey already occupied by conspecific larvae. The result is an arms race between larvae and adult females, which favours a diversification of ODP pheromones. Our models show that: (i) females should be able to recognize mixtures of hydrocarbons rather than a single molecule; and (ii) females should be more sensitive to the tracks of their own offspring than those of non-related larvae.

(Z)-Pentacos-12-ene, an Oviposition-deterring Pheromone of Cheilomenes sexmaculata

Larvae of the coccinellid beetle Cheilomenes sexmaculata (F.) produce an oviposition-deterring pheromone that inhibits egg laying of conspecific females on oviposition sites walked over by first-instar larvae. By use of bioassay-guided fractionation of larval extracts, (Z)-pentacos-12-ene was identified as an active component of the cuticular hydrocarbons of the larvae. Other compounds that occur in the active fractions, such as the alkaloid coccinelline and saturated hydrocarbons, were individually tested but proved to be inactive. The synthesis of (Z)-pentacos-12-ene is reported.

Oviposition-deterring pheromone deposited on blueberry fruit by the parasitic wasp, Diachasma alloeum

Insect parasitoids are known to deposit chemical signals on utilized hosts following oviposition. It is believed that these chemical signals alert future conspecifics of an exploited and thus sub-optimal host alleviating potential suffering among brood that would otherwise compete over a limited resource. Diachasma alloeum (Muesebeck) is a braconid wasp that specifically attacks two species of fruit-parasitic flies in the genus Rhagoletis . Female wasps lay a single egg into a second or third instar fly maggot developing in blueberry, hawthorn, or apple fruit. Following oviposition, female wasps press and drag their ovipositor across the fruit surface depositing a clear liquid; this has been termed 'excreting' behaviour. In this report, we describe excreting behaviour in a field population of D. alloeum attacking the blueberry maggot fly, Rhagoletis mendax Curran. Subsequently, we demonstrate in a series of laboratory assays that D. alloeum females deposit a substance on blueberry fruit directly following egg laying that deters subsequent naïve females from ovipositing into the marked fruit. Marking fruit with this putative oviposition-deterring pheromone without associated egg laying was sufficient to induce the deterring effect, while oviposition alone without subsequent marking had no effect. The oviposition-deterring effect was removed by rinsing fruit with a solution of 50% ethanol in water. Spraying unmarked fruit with an ethanol-water rinsate of previously-marked berries induced the oviposition-deterring effect. Significant deterrence of oviposition lasted up to 7 days after marking. To our knowledge, this is the first demonstration of a hymenopteran oviposition-deterring pheromone that is deposited externally on the surface of the fruit skin rather than on the surface of the parasitized larva. Female D. alloeum maximally parasitize second-instar R. mendax larvae during a short 4-5 d window. The length of activity of the oviposition-deterring pheromone described here should be sufficient to prevent multiple egg-laying into a host that cannot support more than one parasitoid larva, and thus reduce intraspecific competition. Insect parasitoids are known to deposit chemical signals on utilized hosts following oviposition. It is believed that these chemical signals alert future conspecifics of an exploited and thus sub-optimal host alleviating potential suffering among brood that would otherwise compete over a limited resource. Diachasma alloeum (Muesebeck) is a braconid wasp that specifically attacks two species of fruit-parasitic flies in the genus Rhagoletis . Female wasps lay a single egg into a second or third instar fly maggot developing in blueberry, hawthorn, or apple fruit. Following oviposition, female wasps press and drag their ovipositor across the fruit surface depositing a clear liquid; this has been termed 'excreting' behaviour. In this report, we describe excreting behaviour in a field population of D. alloeum attacking the blueberry maggot fly, Rhagoletis mendax Curran. Subsequently, we demonstrate in a series of laboratory assays that D. alloeum females deposit a substance on blueberry fruit directly following egg laying that deters subsequent naïve females from ovipositing into the marked fruit. Marking fruit with this putative oviposition-deterring pheromone without associated egg laying was sufficient to induce the deterring effect, while oviposition alone without subsequent marking had no effect. The oviposition-deterring effect was removed by rinsing fruit with a solution of 50% ethanol in water. Spraying unmarked fruit with an ethanol-water rinsate of previously-marked berries induced the oviposition-deterring effect. Significant deterrence of oviposition lasted up to 7 days after marking. To our knowledge, this is the first demonstration of a hymenopteran oviposition-deterring pheromone that is deposited externally on the surface of the fruit skin rather than on the surface of the parasitized larva. Female D. alloeum maximally parasitize second-instar R. mendax larvae during a short 4-5 d window. The length of activity of the oviposition-deterring pheromone described here should be sufficient to prevent multiple egg-laying into a host that cannot support more than one parasitoid larva, and thus reduce intraspecific competition.

The Immediate Source of the Oviposition-Deterring Pheromone Produced by Larvae of Adalia bipunctata (L.) (Coleoptera, Coccinellidae)

As is the case for other insects ovipositing on or in resources that are limited in time and/or space, the two-spot ladybird beetle, Adalia bipunctata (L.) produces an oviposition-deterring pheromone (ODP), which is produced by the larval stages. Foraging larvae touch the substrate with their tarsi and the anal disk on the tenth abdominal segment. The aim of this paper was to determine whether the ODP produced by larvae was deposited by the tarsi or the anal disk. Fourth instar larvae either had their anal disk and tarsi, or anal disk, or tarsi coated with a water-soluble mounting medium. Larvae so treated were allowed to walk on filter paper that was subsequently presented to gravid females. The tracks of larvae that had both their tarsi and anal disk masked did not inhibit oviposition. However, the tracks of larvae that had only their tarsi masked significantly inhibited oviposition but those of larvae that had only their anal disk masked did not. It is concluded that the ODP is deposited on the substrate by the anal disk on the tenth abdominal segment of larvae.

Catalytic Glycosylation with Rhodium(III)‐Triphos Catalysts.

AbstractFor Abstract see ChemInform Abstract in Full Text.

Catalytic Glycosylation with Rhodium(III)-Triphos Catalysts

The formation of glycosides in high yield from 1-hydroxy sugars using catalytic amounts (0.5mol%) of Rh(III)Cl3(triphos) (1a) or [Rh(III)(MeCN)3(triphos)](TfO)3 (1b) is described. High stereocontrol at the anomeric center is achieved by neighboring group participation. In addition, an application of this new glycosylation procedure for the synthesis of a derivative of the oviposition-deterring pheromone of the cherry fruit fly Rhagoletis cerasi is presented.

Natural oviposition-deterring chemicals in female cotton bollworm, Helicoverpa armigera (Hubner)

Observation of the oviposition behavior of cotton bollworm demonstrated the existence of substances that can act as oviposition deterrents. The scales, abdomens and tarsi of the moths, the most likely carrier, were extracted for the substances. An acetone extract exhibiting an oviposition deterrent effect was analyzed using gas chromatography and combined gas chromatography–mass spectroscopy. Three components, 4-methyl-4-hydroxyl-pentanone-2, hexadecanoic acid and (Z)-9-octadecenoic acid, were identified, being present in the ratio 1:2:2. Experiments with synthetic mixtures indicated that a mixture of equal amounts of the two organic acids exhibited similar repellent and deterrent activity to a synthetic mixture of all three components. It is concluded that the natural oviposition-deterring pheromone is a mixture of hexadecanoic acid and (Z)-9-octadecenoic acid.

Effects of conspecific and heterospecific larval tracks on the oviposition behaviour of the predatory ladybird, Harmonia axyridis (Coleoptera: Coccinellidae)

The effect of the oviposition deterring pheromone (ODP) in the larval tracks of conspecific and heterospecific ladybirds on oviposition in Harmonia axyridis Pallas was studied in semi natural conditions. Gravid females of H. axyridis were deterred from ovipositing on plants contaminated with conspecific larval tracks, but not on those with heterospecific tracks. H. axyridis females spent significantly less time on plants contaminated with conspecific ODP than on those with heterospecific ODP. This behaviour may account for why fewer eggs were laid on plants contaminated with conspecific ODP.

Identification of the gland secreting oviposition-deterring pheromone in the cabbage seed weevil, Ceutorhynchus assimilis, and the mechanism of pheromone deposition

After laying an egg into a pod of Brassica napus, the female cabbage seed weevil, Ceutorhynchus assimilis, brushes the caudal setae of the eighth abdominal tergite (VIII UT) on the host pod as she walks along it, depositing oviposition-deterring pheromone (ODP). The VIII UT is periodically extended and withdrawn, thus repeatedly rubbing against the posterior fold of the seventh urotergite (VII UT) which bears the individual outlets of glandular epidermal cells. In post-diapause, sexually mature, gravid (i.e. oviferous) females (virgin or mated) the cells of this VII UT gland were hypertrophic, showing intense secretory activity. Extracts of VII UT from these individuals elicited strong electrophysiological responses from antennal club gustatory sensilla and deterred oviposition. In pre-diapause (sexually immature) females, the cells of the VII UT gland were neither hypertrophic nor active and an extract of their VII UT elicited no significant electrophysiological or behavioural response. Extract of female rectum was a less potent oviposition deterrent than VII UT extract and elicited an electrophysiological response similar to male rectum extract. An extract of ovarian calyces and ovaries elicited no behavioural response. We conclude that ODP is secreted by the epidermal cells of the VII UT posterior fold.

Perception of oviposition-deterring pheromone by cabbage seed weevil (Ceutorhynchus assimilis )

Following oviposition into a pod of oilseed rape (Brassica napus), the female cabbage seed weevil (Ceutorhynchus assimilis) marks the pod with oviposition-deterring pheromone (ODP) by brushing it with her eighth abdominal tergite. On an unmarked pod, oviposition site selection was always accompanied by intensive antennation of the pod. Females approaching a freshly ODP-marked pod brought their antennae within 1 mm of the pod but usually did not antennate it before rejecting it for oviposition. Females with the clubs of their antennae amputated continued to discriminate pods from stems or petioles as oviposition sites but showed no behavioral response to ODP. Extracts of volatiles air-entrained from ovipositing weevils failed to inhibit oviposition. Air passed over a behaviorally active extract of ODP did not elicit a detectable electroantennogram response. By contrast, when presented as a gustatory stimulus to the sensilla chaetica of the antennal club, a behaviorally active extract of ODP from postdiapause, gravid females elicited a strong electrophysiological response. This response usually involved more than one cell and displayed a phasic–tonic time course over the recording period of 10 sec. Extract from prediapause (and hence sexually immature) females elicited neither behavioral nor electrophysiological (contact) responses. Thus the ODP of the cabbage seed weevil is sensed primarily by contact chemoreception at the sensilla chaetica of the antennae, and the electrophysiological responses recorded from these gustatory sensilla are of value as the basis of a bioassay to assist identification of the active constituent(s) of the pheromone.

Assessment of patch quality by ladybirds: role of larval tracks.

Gravid females of the two-spot ladybird, Adalia bipunctata (L.), were deterred from ovipositing when kept in petri dishes that had previously contained conspecific larvae but not conspecific adults, or the larvae of another two species of ladybird, Adalia decempunctata (L.) and Coccinella septempunctata L. The deterrent effect was density dependent and mediated via a chloroform-soluble contact pheromone present in the larval tracks. Similarly, gravid females of C. septempunctata were deterred from ovipositing by conspecific larval tracks and chloroform extracts of these tracks, but not by the tracks or extracts of tracks of A. bipunctata larvae. That is, in ladybirds the larvae produce a species-specific oviposition-deterring pheromone. In the field, the incidence of egg cannibalism in ladybirds increases very rapidly with the density of conspecific eggs or larvae per unit area. Thus, in responding to the species specific oviposition deterring pheromone female ladybirds reduce the risk of their eggs being eaten and spread their offspring more equally between patches.

Enantiomeric synthesis of the key synthon of the oviposition-deterring pheromone of Rhagoletis cerasi L

A convenient and enantioselective synthesis of ethyl (8 RS, 15 R)-8-acetoxy-15-hydroxyhexadecanoate 15 via a chemoenzymatic approach has been described. The salient features of the synthesis were operational simplicity, use of easily accessible materials, and excellent enantiocontrol via lipase catalyzed acetylation of 2-alkanol.

The role of larval food resources and adult movement in the population dynamics of the orange-tip butterfly (Anthocharis cardamines).

Numbers of the orange-tip butterfly were recorded on a permanent transect in Monks Wood National Nature Reserve between 1982 and 1993, together with numbers of its only larval food plant in the wood, Cardamine pratensis. Females of the butterfly lay their eggs on the newly opened flower heads of Cardamine and the larvae feed on the developing seed pods. They are extremely selective in their choice of plant for egg laying, choosing mainly large flower heads growing in open sunny locations. Larval survival is greatly reduced if the flower head is more than 8 days old at the time of egg laying, because the seed pods become too tough for feeding. Earlier studies showed that only one larva can survive on a flower head, because larvae are cannibalistic, but females tend to avoid plants carrying more than one egg, in response to an oviposition-deterring pheromone laid down at the time of egg laying. The numbers of flower heads of Cardamine fluctuate enormously between years, and the numbers of eggs follow these closely. There is a strong correlation between number of eggs laid and the availability of suitable flower heads, and this correlation was shown to be real and causal by the experimental provision of extra flower heads, which resulted in more eggs, laid over an extended period of oviposition. The main causes of mortality of the butterfly's young stages were egg infertility, cannibalism, predation, starvation, the grazing of flower heads by deer, and possibly the failure of the newly hatched larvae to feed adequately. Adult numbers were only weakly correlated with the numbers of young stages in the wood, and there appears to be a considerable amount of movement by the butterfly through the wood and surrounding farmland.

Oviposition and feeding preferences of a flower‐feeding weevil, Coelocephalapion aculeatum, in relation to conspecific damage to its host‐plant

AbstractThe oviposition and feeding preferences of Coelocephalapion aculeatum Fall (Coleoptera: Apionidae), a host specific florivore of Mimosa pigra L. (Mimosaceae), were studied in relation to conspecific damage to its host‐plant. Adults of C. aculeatum cease ovipositing in inflorescences when the egg load reaches a number consistent with the larval carrying capacity of the inflorescence. The basis for this oviposition deterrence was examined by offering inflorescences damaged by adult feeding alone, larval feeding alone and a combination of adult feeding and oviposition. Adults preferred to oviposit on inflorescences which are not damaged by either adult feeding, larval feeding, or oviposition. No evidence for the existence of an oviposition deterring pheromone (ODP) was found. I suggest that the ability of a single host inflorescence to support the development of many larvae causes selection for the use of these oviposition deterring cues which can convey more quantitative information about the level of previous infestation than can ODPs. Adults fed a similar amount on damaged compared to undamaged inflorescences. These results assisted in the design of host range testing trials and allows predictions to be made about the effectiveness of this insect as a biological control agent.

Tarsal contact chemoreceptor for the host marking pheromone of the cherry fruit fly, Rhagoletis cerasi: responses to natural and synthetic compounds

Abstract. The European cherry fruit fly (Rhagoletis cerasi L.; Diptera, Tephritidae) marks cherries (Prunus avium L.) after oviposition with a host marking pheromone (HMP). The marking trail prevents additional oviposition by the same or other females into the same fruit. On the ventral side of the tarsi of both sexes, contact‐chemoreceptor sensilla were identified which contain a receptor cell selectively sensitive to HMP. The HMP receptors of males were slightly more sensitive than those of females, suggesting that the more general term ‘host‐marking pheromone’ is more appropriate than the previously used ‘oviposition deterring pheromone (ODP)’.The four structural isomers of the HMP, N(15R, S(β‐glucopyranosyl)‐oxy‐8RS‐hydroxypalmitoyl)‐taurine, and various derivatives were synthesized and tested in an electrophysiological bioassay. Both the 8R,15R and the 8S,15RS isomers of the HMP were equally active with a threshold of about 2 times 10‐10M, and were shown to be present in the female faeces in similar proportions. The two 15S HMP isomers were about 13 times less active.Testing synthetic derivatives of the HMP molecule revealed that the presence of the four moieties of the molecule are important for the activity: taurine, palmitic acid, C(8) hydroxyl group, and glucose (C(15)). The chain length of the fatty acid, the hydroxyl group at C(8) and the position of glucose at C(15) also influenced the activity. Only minor loss of activity (factor 2) relative to the natural molecule was observed when the methyl group in the C(15) position was removed. The removal of the β‐glycosidically linked glucose (replaced by a hydroxyl group) resulted in about a 4‐fold loss of activity. The cation of the HMP molecule seemed to have no effect on its activity, whereas both low and high pH reduced it significantly.Based on these results, field experiments have been initiated to control oviposition by cherry fruit flies on cherries applying the 15‐desmethyl‐HMP derivative.

Pheromone synthesis, CLX. A new synthesis of the oviposition-deterring pheromone of the European cherry fruit flyRhagoletis cerasi L.

A new synthesis of the ammonium salt 1c of (8RS,15R)-N-[(β-D-glucopyranosyloxy)-8-hydroxypalmitoyl]taurine, the oviposition-deterring pheromone of the European cherry fruit fly Rhagoletis cerasi L., was achieved by starting from 2,3,4,6-tetra-O-pivaloyl-α-D-glucopyranosyl bromide (2), taurine (4), ethyl (R)-3-hydroxybutanoate (5), propargyl alcohol (6), methyl acetoacetate (7), and 1,6-hexanediol (8).

Tandem mass spectrometry in the structural analysis of an oviposition-deterring pheromone

The potential of tandem mass Spectrometry (MS/MS) as a stand-alone technique in the structural analyses of an oviposition-deterring pheromone (ODP, 1) is reviewed. Two facets of the salt-like glycolipid structure of 1 were of major interest in this context: the substitution pattern of the lipid backbone (15-glucosyioxy-8-hydroxypalmitate) and, more specifically, the configurational identity of the sugar portion (glucopyra nose). Throughout this study, trideuterioacetyl derivatives of ODP (1 → pentakis(trideuterioacetyl)-ODP la) and the reference substrates were used. Probing of the sugar moiety by fast atom bombardment (FAB) and both low- and high-energy collision-induced dissociation (CID) of B2-type sugar ions surprisingly failed as a single exception within a larger number of glycosidic substrates subjected to this approach. However, electrospray ionization (ESI) of la with the formation of the sugar ions in the gas phase by ‘first-stage’ CID before mass selection circumvented this difficulty and provided an unambiguous and sensitive probe for sugar stereochemistry. When studying the ODP molecule as a whole, FAB-generated M-like ions such as [M − H]−, [M + Na]+ and [M − H + 2Na]+ were subjected to high-energy CID using a four-sector tandem mass spectrometer. Analyses of simple model substrates such as the 12-trideuterioacetoxystearate anion facilitated the interpretation of the distinct charge-remote fragmentation (CRF) behaviour of la. Whereas all M-like species provided complete records of the lipid portion of la and its oxygenation pattern, only the sodiated cations allowed reliable location of the individual substituents. In these latter species complementary series of ‘sequence ions’ were observed that incorporated either the taurine or the sugar terminus and thus reflected CRF for both alternatives of terminal charge fixation.

Biological evidence of an oviposition-deterring pheromone inLobesia botrana Den. et Schiff. (Lepidoptera, Tortricidae)

Females of the European grapevine moth (Lobesia botrana Den. et Schiff.) usually deposit isolated eggs on flowers and berries of the grapevine (Vitis vinifera L.). We have investigated whether an epideictic pheromone could be present on the egg surface to explain this spacing behavior. About 21,000 eggs ofL. botrana were washed in cold methanol, and the biological activity was tested in a two-choice bioassay offering treated and nontreated areas. Different dilutions of the extract were tested in methanol, which was inactive alone. At the dose of four egg equivalents per microliter of extract, the number of eggs laid by theL. botrana females was reduced by as much as 57% on the treated areas compared to nontreated areas. A longer-term suppression of oviposition (at least 24 hr) following an exposure to the extract occurred for two doses (0.6 and 4.0 eggs/μl) of egg extract. Our results strongly suggest the occurrence of an oviposition-deterring pheromone (ODP) on the eggs ofL. botrana. The ecological value of these results is discussed.