A study on the emergence sequence of pupal parasitoids of the pine processionary moth,Thaumetopoea pityocampa

The emergence of pupal parasitoids from collected pupae of Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae) was recorded over a 2-year period. The moths and the parasitoid species Villa brunnea (Diptera: Bombylidae), Phryxe caudata (Diptera: Tachinidae), Coelichneumon rudis (Hymenoptera: Ichneumonidae) emerged sequentially. The ecological implications of such parasitism are discussed.     

Prepupal diapause synchronizes adult emergence in the pine processionary moth Thaumetopoea pityocampa (Lepidoptera: Notodontidae)

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Sex pheromone biosynthesis in the processionary moth Thaumetopoea pityocampa by delta-13 desaturation

In vivo treatments of female sex pheromone glands of the processionary moth, Thaumetopoea pityocampa, with mass-labeled fatty acids showed that (Z)-13-hexadecen-11-ynyl acetate, the main sex pheromone component, is biosynthesized from palmitic acid by the combined action of delta-11 and delta-13 desaturases. The involvement of this unusual delta-13 has been proven by application of [16,16,16-2H3] [1,2-13C2]-hexadecanoic acid to the glands with a resultant incorporation of all labeled atoms into the pheromone and each one of the corresponding intermediates. These results seem to exclude alternative biosynthetic pathways, such as chain shortening and elongation combined with delta-11 desaturation. The delta-11 desaturase responsible for the formation of the triple bond in both the 11-hexadecynoyl and (Z)-13-hexadecen-11-ynoyl intermediates is also an unusual enzyme not previously reported in lepidopteran sex pheromone biosynthesis.     

Host-plant use in the range expansion of the pine processionary moth, Thaumetopoea pityocampa

Abstract.  1. During range expansions of phytophagous insects, secondary or novel hosts may allow colonisation of areas without primary hosts. Because plant species often differ in their relative attractiveness and suitability for insects, insect preference for, and performance on, these hosts can determine recruitment potential in the current and future expansion areas.
2. This study explores the relative roles of female preference and larval performance in an important pine defoliator, Thaumetopoea pityocampa (Denis & Schiffermüller) (Lepidoptera, Notodontidae), which colonises three Pinus species at its current range margin in the Italian Alps: P. nigra (primary host), P. sylvestris (secondary host), and P. mugo (novel host).
3. Host use patterns in multiple insect populations were studied through choice and no-choice oviposition experiments in cages, field surveys of mixed stands, and laboratory and field monitoring of larval growth and mortality. It was predicted that a specific life-history trait – time limitation of short-lived females to lay a single batch of eggs – would act as a component of female performance, and lead to similar rates of host acceptance in no-choice settings.
4. In the choice experiment, P. nigra was accepted the most frequently while P. sylvestris was accepted the least frequently, confirming nest density patterns in the field. Contrary to prediction, females remained discriminating in no-choice settings in spite of time limitation. In contrast, relative growth rate (RGR) and mortality of larvae did not differ significantly among the three hosts, highlighting a discrepancy between female preference and larval performance.
5. Recruitment potential of T. pityocampa in future expansion into stands of P. sylvestris and P. mugo is evaluated by combining host quality, conservatism in oviposition behaviour, habitat suitability, and the opportunity for local adaptation.     

Deciphering the demographic history of allochronic differentiation in the pine processionary moth Thaumetopoea pityocampa

Understanding the processes of adaptive divergence, which may ultimately lead to speciation, is a major question in evolutionary biology. Allochronic differentiation refers to a particular situation where gene flow is primarily impeded by temporal isolation between early and late reproducers. This process has been suggested to occur in a large array of organisms, even though it is still overlooked in the literature. We here focused on a well‐documented case of incipient allochronic speciation in the winter pine processionary moth Thaumetopoea pityocampa. This species typically reproduces in summer and larval development occurs throughout autumn and winter. A unique, phenologically shifted population (SP) was discovered in 1997 in Portugal. It was proved to be strongly differentiated from the sympatric “winter population” (WP), but its evolutionary history could only now be explored. We took advantage of the recent assembly of a draft genome and of the development of pan‐genomic RAD‐seq markers to decipher the demographic history of the differentiating populations and develop genome scans of adaptive differentiation. We showed that the SP diverged relatively recently, that is, few hundred years ago, and went through two successive bottlenecks followed by population size expansions, while the sympatric WP is currently experiencing a population decline. We identified outlier SNPs that were mapped onto the genome, but none were associated with the phenological shift or with subsequent adaptations. The strong genetic drift that occurred along the SP lineage certainly challenged our capacity to reveal functionally important loci.     

Survival at low temperature of larvae of the pine processionary moth Thaumetopoea pityocampa from an area of range expansion

1 Larvae of Thaumetopoea pityocampa (Lepidoptera: Notodontidae) develop throughout the winter, although their feeding activity and survival can be impaired by adverse climatic factors. The present study investigated the survival at low temperature of larvae originating from a population with range expansion in an alpine valley in Northern Italy.
2 The supercooling point of individually analysed larvae averaged at −7 °C. This value insufficiently described the cold hardiness of the larvae; 39% of the tested larvae were alive when returned to room temperature immediately after freezing. When larval colonies inside their nest were exposed to −17 °C for 1 h after gradual temperature decrease, survival was 70.4%.
3 Rearing of larvae in the laboratory at different day/night temperatures indicated an effect of cumulative chill injury on larvae. A logistic regression explained the relationship between negative thermal sum (h°C below 0 °C) received in the laboratory experiment and larval survival. A similar relationship was demonstrated between negative thermal sum and survival of larval colonies in the field.
4 In the laboratory experiment, some tested larvae were able to survive for up to 8 weeks without feeding depending on rearing temperature. As expected, feeding occurred only when larvae were reared at temperatures of 9 °C day/0 °C night.
5 We classify the larvae of T. pityocampa as being moderate freezing tolerant. The winter behaviour allows this species to track climate warming by a rapid expansion into those areas that become compatible with the insect's development.     

Effects of climate on pine processionary moth fecundity and on its egg parasitoids

Climate change may be affecting the fecundity of phytophagous insects as well as impacting their natural enemies. However, temperature impacts these two insect groups differently, disrupting population regulation mechanisms, and ultimately, possibly culminating in an outbreak of the host. The pine processionary moth (PPM) is one of the most harmful insects of the Mediterranean basin. Not only are PPM larvae harmful to plants, but they are also dangerous to humans because of their urticating hairs. Although some information is available on climate change effects on the PPM, little is known about its potential effects on PPM egg parasitoids, especially on their distribution range or on their role in controlling PPM populations. The aim of this article was to verify the effects of climate on PPM fecundity and on its egg parasitoids. Our results show that climate warming may affect the PPM positively, but not its egg parasitoids. Specifically, during our study mild winters directly favored the PPM, while increasing summer temperatures (over 30°C) also favored the PPM indirectly, by decreasing parasitism rates. We predict that ever‐milder winters will not only favor PPM development, but also encourage it to spread in otherwise previously inhospitable environments.     

Impact of climatic variation on populations of pine processionary moth Thaumetopoea pityocampa in a core area of its distribution

• 1 There is growing appreciation of climatic effects on insect population dynamics at the margins of distribution limits. Climatic effects might be less important and/or involve different drivers and processes near the centre of distributions.
• 2 We evaluated the effects of interannual variation in temperatures, radiation and precipitation on populations of pine processionary moth Thaumetopoea pityocampa in Central–South Portugal, a low altitude area with a relatively mild Mediterranean climate near the centre of the north–south range of the species.
• 3 We tested for effects of climate on mortality of young larvae, growth rates, final larval mass and fecundity.
• 4 Results indicated high mortality of early instars associated with low minimum and maximum daily temperatures and low precipitation. Low minimum temperatures were further associated with high parasitism by the larval parasitoid Phryxe caudata (Rondani) (Diptera, Tachinidae). Furthermore, larval growth rates were higher with high solar radiation during December and January, which was itself negatively related to precipitation and air temperature. Slow larval growth rates led to lower final mass at pupation in the spring, and smaller egg masses and smaller initial colony sizes during the next autumn.
• 5 Thus climatic factors, and temperature in particular, apparently contributed to population dynamics of T. pityocampa in the core of its distribution, as well as at its northern limits. The most specific climatic parameters of importance, however, and the connections between climate, physiology and insect demographics in the core area were clearly different from northern areas.

     

Incipient allochronic speciation in the pine processionary moth (Thaumetopoea pityocampa, Lepidoptera, Notodontidae)

A plausible case of allochronic differentiation, where barrier to gene flow is primarily attributable to a phenological shift, was recently discovered in Portugal for the pine processionary moth Thaumetopoea pityocampa. Previous results suggested that the observed 'summer population' (SP) originated from the sympatric winter population (WP). Our objectives were to finely analyse these patterns and test their stability in time, through field monitoring and genetic analyses of larvae and adults across different years. Reproductive activity never overlapped between SP and WP. Microsatellites showed a clear differentiation of the SP, consistent with a strong reduction in gene flow owing to the phenological shift. Assignment tests suggested that some individuals shift from the SP to the WP phenology, causing some hybridization. We discuss these patterns and their maintenance over time. This could be a first stage of allochronic speciation, and SP should be considered as a distinct phenological race.     

Host utilisation by moth and larval survival of pine processionary caterpillar Thaumetopoea pityocampa in relation to food quality in three Pinus species

Abstract 1. The work reported here analysed host utilisation by the pine processionary moth Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae), the relationship between moth oviposition patterns and larval performance, the chemical characteristics of the plant in relation to the performance of different larval instars, and the role of these factors in the outbreak capacity of the species. In order to do this, a combination of field and laboratory techniques was used to study three pine species differing in nutritional characteristics.
2. Moths oviposited in the three pine species analysed, although cluster pine received a lower number of batches. Late-instar larvae were able to feed on all three pine species, however first-instar larvae developed on Scots and black pine but died on cluster pine. Consequently, oviposition in cluster pine can be considered an oviposition mistake, and indicates that moths are rather unselective when ovipositing on different pine species.
3. Chemical analysis of needles suggested that the quantity of nitrogen was the main factor responsible for the difference in survival of larvae.
4. The oviposition pattern of the moth and the larval susceptibility to food quality in Thaumetopoea pityocampa agree with the theory that unselective oviposition of the moth is a precondition for eruptive dynamics in phytophagous insects.
5. The success of the larvae depends mainly on the probability of the moth finding a suitable host. This probability is determined strongly by the changes of structure and coverage in Mediterranean pine woodlands, due to human management.     

Spatial patterns at host and forest stand scale and population regulation of the pine processionary moth Thaumetopoea pityocampa

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Sex pheromone precursors in the processionary moth Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeae)

The fatty acid composition of Thaumetopoea pityocampa female sex pheromone gland was determined. In addition to the common C16 and C18 fatty acids, the glandular tissue contains large amounts of (Z)-11-hexadecenoate, (Z,Z)-11,13-hexadecadienoate, (Z)-13-hexadecen-11-ynoate and 11-hexadecynoate, as well as some unusual C18 fatty acids, such as (Z)-11 and (Z)-13-octadecenoic acids. From these results, different biosynthetic pathways are discussed for the formation of (Z)-13-hexadecen-11-ynyl acetate, the main component of the sex pheromone of the processionary moth.     

Needle terpene concentrations and emissions of two coexisting subspecies of Scots pine attacked by the pine processionary moth (Thaumetopoea pityocampa)

Mediterranean pine forests are often attacked by caterpillars of Thaumetopoea pityocampa (Lep., Thaumetopoidae), one of the most important defoliators in the Mediterranean region causing large economic losses and ecological effects. The needle terpene concentrations and emissions may play a key role in the defense of pines. We studied two subspecies of Pinus sylvestris, nevadensis (an endemic and relict subspecies) and iberica , with different levels of caterpillar attack in Sierra Nevada mountains (Spain). GC–MS analyses showed large total concentrations of terpenes (6 to 39 mg g^?1 of dry weight) in the needles of both subspecies under field conditions. Concentrations were 25 % higher in “Non-Attacked Trees” (NATs) of the iberica than in the nevadensis subspecies. The branches of NATs had terpene concentrations 20 % higher than those of “Attacked Branches of attacked trees” (ABs). Within attacked trees, the “Non-Attacked Branches” (NABs) also had terpene concentrations 20 % higher than those of ABs. Mainly α-pinene and germacrene D had higher concentrations in NATs and NABs than in ABs. Some terpenes had higher concentrations in NABs than in NATs, indicating possible systemic reactions. In subsp. nevadensis, the percentage of monoterpenes relative to total terpenes was higher in ABs than in other attack states. The rates of emission in nevadensis (standardized to 30 °C) were ca. three times higher in ABs than in NABs and NATs. These results suggest that the lower terpene concentrations and high percentages of monoterpenes in ABs were produced by a combination of emission losses and terpene induction in response to herbivorous attack.     

Phylogeography of the pine processionary moth Thaumetopoea wilkinsoni in the Near East

Phylogeographic structure of the eastern pine processionary moth Thaumetopoea wilkinsoni was explored in this study by means of nested clade phylogeographic analyses of COI and COII sequences of mitochondrial DNA and Bayesian estimates of divergence times. Intraspecific relationships were inferred and hypotheses tested to understand historical spread patterns and spatial distribution of genetic variation. Analyses revealed that all T. wilkinsoni sequences were structured in three clades, which were associated with two major biogeographic events, the colonization of the island of Cyprus and the separation of southwestern and southeastern Anatolia during the Pleistocene. Genetic variation in populations of T. wilkinsoni was also investigated using amplified fragment length polymorphisms and four microsatellite loci. Contrasting nuclear with mitochondrial data revealed recurrent gene flow between Cyprus and the mainland, related to the long-distance male dispersal. In addition, a reduction in genetic variability was observed at both mitochondrial and nuclear markers at the expanding boundary of the range, consistent with a recent origin of these populations, founded by few individuals expanding from nearby localities. In contrast, several populations fixed for one single mitochondrial haplotype showed no reduction in nuclear variability, a pattern that can be explained by recurrent male gene flow or selective sweeps at the mitochondrial level. The use of both mitochondrial and nuclear markers was essential in understanding the spread patterns and the population genetic structure of T. wilkinsoni, and is recommended to study colonizing species characterized by sex-biased dispersal.     

Influence of trap type, trap colour, and trapping location on the capture of the pine moth, Thaumetopoea pityocampa

Studies were conducted to evaluate the effect of type, location, and colour of traps baited with 1 mg of the sex pheromone (Z)‐13‐hexadecen‐11‐ynyl acetate in polyethylene vials on the capture of the pine processionary moth, Thaumetopoea pityocampa (Denis & Schiffermüller) (Lepidoptera: Thaumetopoeidae), males. The experiments were carried out during two flight seasons in 2002 and 2003 at a low elevation Mediterranean pine forest on the hill of Goritsa (Magnesia, Thessaly, Central Greece). The hill is covered by approximately 120 ha of pines, among which Pinus brutia Ten. (Pinaceae) is predominant with Pinus halepensis Mill. (Pinaceae) as second most common species. Among the commercially available trap types used, the Delta and Pherocon II captured significantly more males than the Funnel trap. Furthermore, pine density had a significant effect on trap type and trap colour catches. Delta traps caught significantly more adults than the other two trap types in the low density pine stand, while in the medium and high‐density pine stands no significant differences were noted between Delta and Pherocon II traps. In addition, trap colour performance varied according to pine density; white‐ and yellow‐coloured traps caught significantly more males than the other two trap colours in the high‐density stand. The first adults were captured in traps during May, and traps continued to capture adults in low numbers (< two individuals per trap) until mid‐June. A period of 3–4 weeks of no trap captures followed until mid‐July, when captures restarted, at low numbers. The peak of T. pityocampa flight was observed during late August–September.     

A cytoplasmic polyhedrosis virus isolated from the pine processionary caterpillar, Thaumetopoea pityocampa

A cytoplasmic polyhedrosis virus (CPV) was isolated from the larvae of Thaumetopoea pityocampa and shown to cause an infection of midgut cells. This viral infection revealed several important diagnostic symptoms, including discoloration of the posterior midgut, reduced feeding, and extended development time of the larvae. The virus infection is lethal to Thaumetopoea pityocampa, and with the increasing doses kills the larvae within 4-5 days post infection. Electron microscopy studies showed typical cytoplasmic polyhedral inclusion bodies that are icosahedral, and ranged from 2.4 to 5.3 microm in diameter. Electrophoretic analysis of the RNA genome showed that the virus has a genome composed of 10 equimolar RNA segments with the sizes of 3,907, 3,716, 3,628, 3,249, 2,726, 1,914, 1,815, 1,256, 1,058, and 899 bp, respectively. Based on morphology and nucleic acid analysis, this virus was named Thaumetopoea pityocampa cytoplasmic polyhedrosis virus (TpCPV), and belongs to the genus Cypovirus, family Reoviridae.     

The role of topography in structuring the demographic history of the pine processionary moth,Thaumetopoea pityocampa (Lepidoptera: Notodontidae)

Aim We investigated the Quaternary history of the pine processionary moth, Thaumetopoea pityocampa, an oligophagous insect currently expanding its range. We tested the potential role played by mountain ranges during the post‐glacial recolonization of western Europe. Location Western Europe, with a focus on the Pyrenees, Massif Central and western Alps. Methods Maternal genetic structure was investigated using a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene. We analysed 412 individuals from 61 locations and performed maximum likelihood and maximum parsimony phylogenetic analyses and hierarchical analysis of molecular variance, and we investigated signs of past expansion. Results A strong phylogeographic pattern was found, with two deeply divergent clades. Surprisingly, these clades were not separated by the Pyrenees but rather were distributed from western to central Iberia and from eastern Iberia to the Italian Peninsula, respectively. This latter group consisted of three shallowly divergent lineages that exhibited strong geographic structure and independent population expansions. The three identified lineages occurred: (1) on both sides of the Pyrenean range, with more genetically diverse populations in the east, (2) from eastern Iberia to western France, with a higher genetic diversity in the south, and (3) from the western Massif Central to Italy. Admixture areas were found at the foot of the Pyrenees and Massif Central. Main conclusions The identified genetic lineages were geographically structured, but surprisingly the unsuitable high‐elevation areas of the main mountainous ranges were not responsible for the spatial separation of genetic groups. Rather than acting as barriers to dispersal, mountains appear to have served as refugia during the Pleistocene glaciations, and current distributions largely reflect expansion from these bottlenecked refugial populations. The western and central Iberian clade did not contribute to the northward post‐glacial recolonization of Europe, yet its northern limit does not correspond to the Pyrenees. The different contributions of the identified refugia to post‐glacial expansion might be explained by differences in host plant species richness. For example, the Pyrenean lineage could have been trapped elevationally by tracking montane pines, while the eastern Iberian lineage could have expanded latitudinally by tracking thermophilic lowland pine species.     

Genetic differentiation in the winter pine processionary moth (Thaumetopoea pityocampa--wilkinsoni complex), inferred by AFLP and mitochondrial DNA markers

The winter pine processionary moth has become an important pine pest in the last century, as a consequence of the spread of pine cultivation in the Mediterranean region. The pattern of genetic differentiation of this group, that includes two sibling species (Thaumetopoea pityocampa and Th. wilkinsoni), has been studied in nine populations using amplified fragment length polymorphism (AFLP) and single strand conformation polymorphism-sequence analysis (SSCP) of the mitochondrial cytochrome oxidase 1 (COI) and cytochrome oxydase 2 (COII). Results indicate the existence of strong genetic differentiation between the two species that became separated before the Quaternary ice ages. Moreover data indicate that Th. pityocampa has a strong geographical structure, particularly evident at the nuclear level, where all pairwise phiST resulted to be highly significant and individuals from the same population resulted to be strongly clustered when an individual tree was reconstructed. The estimates of the absolute number of migrants between populations (Nm), obtained from mitochondrial and nuclear DNA markers, suggest that gene flow is low and that a gender-related dispersal could occur in this species. The males appear to disperse more than females, contributing to the genetic diversity of populations on a relatively wide range, reducing the risks of inbreeding and the genetic loss associated with bottlenecks occurring in isolated populations.     

Termination of diapause in the Cinnabar moth (Tyria jacobaeae) by chilling

The effect of chilling time on the termination of pupal diapause was studied in the Cinnabar moth, Tyria jacobaeae L., Lepidoptera: Arctiidae. Chilling followed by a temperature of 20°C was effective in terminating diapause. Chilling for 120 days immediately after pupation yielded the highest percentage emergence and resulted in the shortest total pupal development time (162 days). A more natural treatment, a warm period before cold treatment, did not result in a higher percentage of emergence or in a shorter total pupal development time.During hibernation this species experiences two successive processes: diapause development during the first three to four months of cold, followed by a period of quiescence. Application of high temperatures in this latter period immediately starts morphogenesis. The impact of a relative humidity of 70% during the pupal stage for complete wing unfolding is demonstrated. The underlying mechanism of diapause is discussed.

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Résumé L'effet sur la levée de la diapause de différents régimes de température infligés aux chrysalides est étudié chez Tyria jacobaeae L. (Lepidoptera: Arctiidae). Une mise au froid suivie de hautes températures lève efficacement la diapause. Un refroidissement pendant 120 jours immédiatement après la nymphose entraîne le plus grand pourcentage d'éclosions et la durée totale du développement des chrysalides la plus courte (162.3 j). Un traitement plus naturel, une période chaude avant la période froide, n'entraîne pas un plus grand pourcentage d'éclosions ni une durée plus courte de développement.Il est proposé que durant l'hibernation cette espèce passe par deux processus successifs: un diapause durant les premiers trois ou quatre mois de froid, suivie d'une période de quiescence. Le transfert à des hautes températures pendant cette derpériode déclanche immédiatement la morphogénèse. L'influence d'un taux élevé d'humidité relative durant le stade chrysalide sur le déploiement complet des ailes est démontré. Le méchanisme de diapause sous-jacent est discuté.