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. Received: 8 October 1996 / Accepted: 3 April 1997     

The population biology of the Orange Tip butterfly Anthocharis cardamines in Britain

ABSTRACT.

• 1 The population biology of Anthocharis cardamines (L.) is described and shown to vary with locality. Southern and Western populations emerge earlier than Northern ones, but Western and Northern populations occupy similar, wetter habitats and are associated primarily with Cardamine pratensis (L.). Southern populations are recorded mostly from Alliaria petiolata (Bieb.).
• 2 Studies on egg and larval survival indicate that host plant-induced death and parasitization by a tachinid are important mortality factors. However, a key-factor analysis on one population indicates that the major determinant of population size may be the number of eggs laid by ovipositing females, itself dependent upon weather during the oviposition period. Populations in different localities do show similar trends in abundance, corroborating the effect of weather.
• 3 Human effects on distribution and abundance are discussed, and some conservation strategies suggested.

     

Host plant conspicuousness and the distribution of eggs and larvae in the butterfly,Anthocharis scolymus (Lepidoptera: Pieridae)

We investigated how the distribution pattern of eggs and larval on the host plant, Turritus glabra, was influenced by the oviposition behavior of the pierid butterfly Anthocharis scolymus. Females searched for the host plants visually and they frequently approached taller host plants with sparse surrounding vegetation. After encountering host plants, oviposition behavior of females was independent of host plant characteristics such as height, density, and type of surrounding vegetation. A female laid eggs singly on a host plants. Most females appeared to lay their eggs regardless of the presense of eggs on the host plant. Consequently egg and larva tended to be abundant on conspicuous host plants as measured by height or relative isolation from other plants. However, overcrowding of eggs on an individual host decreased the survival rate of larvae.     

Evidence for an oviposition-deterring pheromone in Tephritis bardanae (Schrank) (Diptera: Tephritidae)

Summary Female Tephritis bardanae (Schrank) exhibit a characteristic ovipositor-dragging behaviour immediately after laying eggs into a flowerbud of Arctium minus (Hill) Bernh. To establish whether this behaviour is associated with an oviposition-deterring pheromone (ODP), female T. bardanae were presented with clean, unattacked flowerbuds and fly activity was monitored using video recording equipment. The distribution of oviposition and fly behaviour were analysed. Avoidance of attacked buds was revealed by the oviposition pattern becoming overdispersed. Spacing out of eggs continued until, on average, each bud contained one egg-batch, after which the distribution became more random or clumped. Analysis of fly behaviour showed that attacked and unattacked buds received similar numbers of visits, but fewer oviposition attempts were made on attacked buds. This behaviour was consistent with use of a contact pheromone deterring repeated oviposition and applied to the bud surface during ovipositor-dragging. Avoidance of attacked buds should increase the efficiency of resource use by T. bardanae populations in the field; however, distributions of egg-batches in flowerhead samples collected from Monks Wood NNR, Cambridgeshire, during 1983–1985, were highly clumped and did not provide supportive evidence. This suggests that the effectiveness of oviposition deterrence in the field is reduced, because the active life of ODP under natural conditions is short, and/or because wild females frequently experience high oviposition drive due to scarcity of suitable flowerbuds.     

The 'edgeeffect' in butterfly oviposition: causality in Anthocharis cardarnines and related species

Abstract. 1. An 'edge-effect', where outlying host plants receive proportionately most attention from insect herbivores, is described from the literature, and from data on Anthochoris cardamines (L.), in northern England.
2. Six hypotheses are examined as explanations for the effect in A.curdamines . Four are shown to be refuted by studies on female behaviour and the survival of larvae.
3. It is argued that the 'edge-effect' comes about due to two or more aspects of the searching behaviour of females. The effect may be seen as an outcome of behaviour adapted to searching for host plants of low density.     

Effects of time-dependent intraspecific competition on offspring survival in the butterfly, Anthocharis scolymus (L.) (Lepidoptera: Pieridae)

Effects of mothers' eclosion and oviposition timing on the survival of their offspring in the pierid butterfly Anthocharis scolymus (L.) was examined. I recorded the performance of individual eggs and larvae that differed in their mother's eclosion and oviposition timing in a natural population, where A. scolymus feeds on Turritis glabra (L.) Bernh. Eggs laid early in the season, and larvae emerging from these eggs, had higher survival than eggs laid later, and larvae emerging from eggs that were laid later in the season, the causal factor being egg cannibalism by larvae on the same host plant. Logistic regression showed that females eclosing early in the season had higher offspring survival than females eclosing later. I conclude that optimal timing of adult eclosion in A. scolymus is a trade-off between eclosing early with associated higher offspring survival but lower egg-laying rate, and eclosing later with associated lower offspring survival but higher egg-laying rate. Received: 4 August 1997 / Accepted: 19 October 1997     

Morphological and electrophysiological mapping of tarsal chemoreceptors of oviposition-deterring pheromone in Rhagoletis pomonella flies

Light microscopy and S.E.M. observations revealed that Rhagoletis pomonella female tarsi, bearing the principal receptors of oviposition-deterring fruit marking pheromone (ODP), have 3 types of chemosensilla: B, C and D. Using electrophysiological hair tip-recording techniques, we found that D chemosensilla located in pairs on distal ventrolateral portions of the 2nd, 3rd and 4th tarsomeres of each leg were highly sensitive to stimulation by the pheromone. D chemosensilla located in pairs on the 5th tarsomere of each leg were moderately sensitive to the pheromone, while the B and C chemosensilla of all tarsi were nearly or completely insensitive to it. For reasons discussed, the D chemosensilla on the prothoracic tarsi may be the most important in providing sensory input eliciting oviposition deterrence.     

Deposition and longevity of oviposition-deterring pheromone in the cabbage seed weevil

Abstract The cabbage seed weevil ( Ceutorhynchus assimilis Payk.) lays eggs singly into pods of oilseed rape ( Brassica napus L.) through punctures bored with the mouthparts, preferring pods not recently used for oviposition. A simple new choice test has been used to test individual components of egg-laying behaviour for their effect on oviposition site selection. It is confirmed that an oviposition-deterring pheromone (ODP) is deposited during abdomen brushing of the pod which follows egg-laying. Neither pin punctures, weevil feeding punctures, oviposition punctures nor eggs had any deterrent effect. Pods walked on by female weevils were not avoided by those laying eggs. Observations suggest that the ODP is sensed by contact chemoreceptors on the antennae. The deterrent effect lasted only 1–2 h. The implications of these findings on the adaptive significance of the pheromone and its possible use in pest control are discussed.     

Site of production of an oviposition-deterring pheromone component in Rhagoletis pomonella flies

Using behavioural and electrophysiological assay techniques, we identified the posterior half of the midgut as being a principal site of production of a major component of the oviposition-deterring, fruit-marking pheromone of female Rhagoletis pomonella flies. Following secretion into, and accumulation in, the gut lumen, this component is released, together with other gut contents, in the marking trail deposited during dragging of the ovipositor on the fruit surface after egg-laying, as well as in the faeces. Other components of the pheromone may be produced elsewhere.     

Courtship and male discrimination between virgin and mated females in the orange tip butterfly Anthocharis cardamines

Recent evidence implies that male butterflies incur non-trivial costs in producing ejaculate, and that the number of ejaculates they can produce is limited. Therefore males should be expected to show some mate discrimination. In butterflies, the reproductive value of females, by necessity, decreases with age and, therefore, males should be expected to court young virgin females more intensively than old mated females. In the orange tip butterfly, Anthocharis cardamines, we show that males exhibit behaviour consonant with this hypothesis. They court unreceptive virgin females for approximately 60 s before giving up, whereas unreceptive mated females are courted for only about 3 s before the male departs. We also show that receptive virgin females usually detain courting males by performing an ‘elevated abdomen’ display for about 4 s before accepting the male, and that this display is identical in form to that used by mated females to reject courting males.     

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.     

Response of the sandfly Lutzomyia longipalpis to an oviposition pheromone associated with conspecific eggs

Response of female Lutzomyia longipalpis Lutz & Neiva (Diptera: Psychodidae) to an oviposition attractant and/or stimulant associated with conspecific eggs was investigated in the laboratory. Females of two populations laid significantly higher mean number of eggs on sites with 160 eggs already present than on bare control sites. This response was lost when eggs placed on test sites were previously washed in organic solvents and distilled water. Age of eggs placed on test sites, 1-6 days after being laid, did not seem to affect the oviposition response of the females. Comparing effects of different numbers of eggs, positive responses were obtained when 80, 160 or 320 eggs were placed on test sites. No significant differences between mean egg numbers laid on test sites and controls were detected when batches of only 20 or 40 eggs were used.     

Correlation between glycerolipids and pheromone aldehydes in the sex pheromone gland of female tobacco hornworm moths,Manduca sexta (L.)

Analysis by TLC and HPLC revealed that the triacylglycerols comprise the most abundant lipid class in the sex pheromone glands of Manduca sexta females. Also, conjugated olefinic acyl analogs of the major pheromone aldehydes occur principally in the triacylglycerols. The amount of triacylglycerols with conjugated diene acyl moieties significantly decreased when the period of pheromone production was extended by 7 h beyond the normal period of pheromone production by 3 injections of pheromone biosynthesis activating neuropeptide (PBAN) at 3 h intervals. This decrease indicates that the triacylglycerols stored in the gland may serve as major sources of pheromone precursors in the biosynthesis of the sex pheromone aldehydes. Furthermore, analysis of pheromone aldehydes and triacylglycerols in the gland from moths treated with PBAN showed that the proportions of the triacylglycerols with conjugated diene moieties were closely correlated with the proportions of aldehydes found in the same gland. This correlation suggests that the proportions of fatty acids bound to certain triacylglycerols regulates the proportions of aldehydes in biosynthesis of the pheromone blend in M. sexta. © 1995 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, is in the public domain in the United States of America.

     

Coevolution of pierid butterflies and their cruciferous foodplants IV. Crucifer apparency and Anthocharis cardamines (L.) oviposition

Summary The oviposition behaviour of the butterfly Anthocharis cardamines has been examined, using the methods of strong inference to investigate foodplant choice. Adaptive explanations for females ovipositing mainly on unshaded, young and large individuals of Alliaria petiolata are rejected in favour of explanations based on apparency to searching females. Floral characters shown to influence intraspecific foodplant apparency are then examined in comparisons between crucifer species, and are shown to explain well the observed deposition of A. cardamines eggs. Cruciferae such as Barbarea vulgaris and Hesperis matronalis, although poor for larval survival, receive many butterfly eggs as a result of large, persistent inflorescences. The contrasting and opposing effects of hostplant apparency and defence are discussed.     

Evidence for a host-marking pheromone in Chaetorellia australis

Experiments and observations on the oviposition behavior of Chaetorellia australis Hering (Diptera, Tephritidae) females, caged in the laboratory with their natural oviposition substrates, floral buds of the yellow starthistle (YST) Centaurea solstitialis L. and Centaurea cyanus L. (Asteraceae: Cardueae) revealed that females of that species deposit a contact host-marking pheromone immediately after oviposition by dragging their extended ovipositor over the floral bud surface. The function of this pheromone is the prevention of repeated oviposition in already infested oviposition sites. Apparently it also plays a role in sexual behavior by functioning as a male arrestant. The pheromone was found to be soluble in water but insoluble in methanol, ethanol, diethyl ether and acetone. Under laboratory conditions, its effectiveness persisted for at least 10 days. By preventing oviposition on already infested buds the pheromone apparently contributes to uniform egg dispersion among available resources for larval development. By functioning as a male arrestant, which causes aggregations of males on places visited frequently by females such as the floral buds of host plants, it also contributes to overall fertility by facilitating encounters of the sexes. The potential practical application for biocontrol of the YST through introducing and releasing C. australis flies into areas infested by the weed is discussed.

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Zusammenfassung Versuche und Beobachtungen über das Eiablageverhalten von im Labor mit ihren natürlichen Eiablagesubstraten, d.h. Blütenknospen von Centaurea solstitialis L. und Centaurea cyanus L. (Asteraceae: Cardueae) gehaltenen Chaetorellia australis Hering (Diptera: Tephritidae) zeigten, dass C. australis Weibchen sofort nach der Eiablage die Oberfläche der Blütenknospe mit einem eiablageverhindernden Pheromon markieren, indem sie ihren ausgestellten Ovipositor über die Oberfläche der Blütenknospe ziehen. Das Pheromon, das auch als Männchen-Arrestans wirkt, ist wasserlöslich, jedoch unlöslich in Methanol, Äthanol, Diethyläther und Aceton. Unter Laborbedingungen hält seine Wirkung mindestens 10 Tage an. Da das Pheromon die Eiablage an bereits infestierten Blütenknospen verhindert, trägt es zu einer gleichmässigen Eiverteilung in den für die Larvenentwicklung zur Verfügung stehenden Futtequellen bei. Als Männchen arretierendes Pheromon führt es zur Aggregation von Männchen an den Blütenknospen, die oft von Weibchen besucht werden und versichert somit eine hohe Fertilität, indem es das Zusammentreffen der Geschlechter erleichtert. Die praktische Anwendung der Ergebnisse für die biologische Bekämpfung von Centaurea solstitialis durch Einfuhr und Freilassung von C. australis in die mit dem Unkraut verseuchten Gebiete wird diskutiert.

     

Possible Age-Dependent Variation in Egg-Loaded Host Selectivity of the Pierid Butterfly, Anthocharis scolymus (Lepidoptera: Pieridae): A Field Observation

To understand better the effects of age on host selection through conspecific egg detection by Anthocharis scolymus females, field observations were performed at a graveyard where the insect population was isolated and the host plant was limited to the cruciferous plant, Turritis glabra. We chased females and recorded their oviposition behaviors and the conditions of plants which females approached. Older females tended to avoid ovipositing on egg-loaded host plants and selectively laid eggs on nonloaded host plants. This result was not confounded by other factors such as seasonality, air temperature, plant height, plant phenological stage, surrounding vegetation, host plant density, and extent of plant damage. We discuss the possibility that females make an oviposition decision on how to lay their limited number of eggs during their remaining lifetime.     

Persistence of the oviposition-deterring pheromone inChrysopa oculata (Neur.: Chrysopidae)

Paper previously exposed for short periods to first instar larvae ofChrysopa oculata Say (Neur.: Chrysopidae) deters conspecific females from ovipositing. The deterrent effect was not reduced by keeping the substrates at temperatures of up to 140°C for one hour. The oviposition-deterring pheromone is volatile. If contaminated substrates were kept in the open air for 3–4 weeks they no longer deterred females from ovipositing. However, the deterrent effect did not decrease significantly when the substrates were kept for 20 weeks in small Petri dishes. Clean paper substrates enclosed for one day above glass previously walked over by larvae also deterred females from ovipositing.     

Venom as an interspecific sex pheromone, and species recognition by a cuticular pheromone in Paper Wasps (Polistes, Hymenoptera: Vespidae)

ABSTRACT. The venoms of Polistes fuscatus (subspecies fuscatus) (F.) and P. exclamans Viereck from sympatric populations in North Carolina, U.S.A., contain a pheromone which attracts males and stimulates sexual behaviour in both conspecific and heterospecific males. Males of P. fuscatus (subspecies variatus Cresson), a subspecies from Wisconsin, respond to venom of P. fuscatus fuscatus, P. exclamans, and Vespula maculifrons (Buysson) from North Carolina, although the levels of response to P. exclamans and V. maculifrons venom are less than that to P. fuscatus variatus venom.
Caged Wisconsin P. fuscafus males do not attempt to mate with P. exclamans females, but will attempt to mate with conspecifics. A series of bioassays indicates that males discriminate between females of P. fuscatus and P. exclamans on the basis of chemical, rather than behavioural or visual cues. The venom apparently is not important in species recognition. Instead, the results of two sets of bioassays suggest that species recognition is mediated by a surface pheromone on the cuticle of females.     

Sex pheromone levels in pheromone glands and identification of the pheromone and hydrocarbons in the hemolymph of the moth Scoliopteryx libatrix L. (Lepidoptera: Noctuidae)

The hydrocarbon sex pheromone (13-methyl-Z6-heneicosene) of Scoliopteryx libatrix L. (Lepidoptera: Noctuidae) was found to reach its highest levels on pheromone glands of 3-day-old females. Pheromone levels were not different between the time of maximum calling (end of scotophase) and at the middle of photophase. Overwintering females collected in October had sex pheromone present. Decapitation did not lower the amount of pheromone present, indicating that a head factor is not involved in maintaining pheromone titers. Hemolymph also contained the pheromone, indicating that it is made by oenocytes and transported to the sex pheromone gland. Longer chain length hydrocarbons were also identified from the hemolymph and on the cuticular surface. Quantitative differences in hydrocarbon profiles were found with more methyl-branched hydrocarbons found in the hemolymph than on the cuticular surface. Arch.     

Isolation of oviposition pheromone from the eggs of the sandfly Lutzomyia longipalpis

Abstract. Semiochemical components of eggs of the sandfly Lutzomyia longipalpis (Diptera: Psychodidae) were separated by high performance liquid chromatography. HPLC fractions were examined quantitatively and qualitatively by gas chromatography (GC). A bioassay was used to determine the oviposition attraction of gravid L. longipalpis to each of the fractions separately and a peak responsible for the semiochemical activity was identified. Gravid flies were placed in individual oviposition tubes to determine if the peak of interest was an oviposition stimulant. The active semiochemical fraction attracted gravid flies for oviposition. Furthermore, egg laying was enhanced: gravid flies exposed to the pheromone oviposited earlier and laid more eggs than control flies. GC analysis indicated that 1200 eggs (2 days old) gave a yield of 12.75 ug of active pheromone. This fraction had similar HPLC and GC retention times to caryophyllene oxide, suggesting comparable polarity and molecular weight.