Outbreaks of the winter moth on Sitka Spruce in Scotland are not influenced by nutrient deficiencies of trees,tree budburst,or pupal predation

Summary Since the early 1980s, the winter moth, Operophtera brumata L. (Lepidoptera: Geometridae) has emerged as a serious pest of Sitka Spruce, Picea sitchensis Bong. plantations in southern Scotland. Outbreaks are characterised by susceptible sites within plantations which can occur immediately adjacent to resistant sites. We investigated the level of some nutrients in the trees, the date of budburst of the trees, and the numbers of some potential predators of winter moth pupae. None could satisfactorily explain outbreak patterns. Although foliage analysis demonstrated that many trees were marginal or deficient in phosphorus, nitrogen and potassium, these deficiencies were not related to the susceptibility of a site. Within sites, the numbers and weights of O. brumata were positively related to phosphorus content and negatively related to calcium content of foliage. Other evidence suggests, however, that these correlations may not represent direct effects of phosphorus and calcium on larval growth and survival. Date of budburst, which commonly determines susceptibility of deciduous hosts to O. brumata, was unrelated to density, and pupal predators were more, not less, abundant in susceptible sites. Although it is difficult to distinguish between factors that initiate outbreaks and those that maintain them, these data suggest that nutrient deficiencies of trees, budburst date, and the distribution of pupal predators of the winter moth cannot explain patterns of outbreak of the winter moth on spruce.     

Phenology and abundance in relation to climatic variation in a sub-arctic insect herbivore–mountain birch system

The two forest-defoliating geometrid moth species Operophtera brumata and Epirrita autumnata are known to exhibit different altitudinal distribution patterns in northern birch forests. One possible explanation for this is that altitudinal climatic variation differentially affects the performance of two species through mismatching larval and host plant phenology. We explored this hypothesis by investigating the relationship between larval phenology and leaf phenology of Betula pubescens, which is the main host plant of both moth species, along ten replicate altitudinal transects during two springs with contrasting climate in northern Norway. There was a distinct monotonous cline in host plant phenology with increasing altitude in both years of the study, but the development of the leaves were generally 14 days later in the first of the 2 years due to cold spring weather. We found that larval development of both species closely tracked host plant leaf phenology independent of altitude and year. However, at the time of sampling, E. autumnata was approximately one instar ahead of O. brumata at all altitudes, probably reflecting that E. autumnata has faster early instar growth than O. brumata. The abundance of O. brumata was lowest at the altitudinal forest-line, while E. autumnata was lowest near sea level. Our results do not indicate that the altitudinal distribution patterns of the two moth species is due to any phenological mismatch between larval and host plant phenology. We suggest rather that natural enemies at low altitudes limit larval survival and thus abundance of E. autumnata, while an early onset of winter at the forest limit reduces survival of late eclosing adults of O. brumata.     

A new species of Rhynchoidomonas Patton, 1910 (Kinetoplastida: Trypanosomatina) from Operophtera brumata (Lepidoptera: Geometridae)

Summary A new species of Rhynchoidomonas Patton was observed in a single adult male winter moth, Operophtera brumata (L.) from England. Intracellular amastigotes, and extracellular epimastigotes and trypomastigotes with an undulating membrane and free flagellum, were present. All stages had a large, reniform kinetoplast. As transmission of the flagellate between generations of winter moths by ingestion of infected faeces is a virtual impossibility, it is suggested that the flagellate's true host may have been a dipteran parasitoid and that an egg, surface-contaminated with the flagellate, was oviposited into or ingested by a winter moth larva. If the parasitoid had died, this flagellate infection could have been carried over to the adult moth. ac]19830601     

Interactions between Operophtera brumata and Tortrix viridana on oak: new evidence from time-series analysis

1. Yearly population estimates of the green oak leaf roller moth, Tortrix viridana (Lepidoptera: Tortricidae), and the winter moth, Operophtera brumata (Lepidoptera: Geometridae), were taken from the pedunculate oak, Quercus robur, from 1951 to 1966 in Wytham Woods, Oxfordshire, U.K. Larval mortality from parasitoids was recorded for both species over the same period. 2. Operophtera brumata population density fluctuated around a constant mean, whereas T. viridana population density exhibited a linear decline over the sampling period. Population counts were subjected to time-series analysis after the linear decline was removed from the T. viridana data by detrending. Multiple regression models were built so that variation in the per capita rate of increase of each population could be partitioned among (a) current and previous population density, (b) current and previous population density of the second moth species, and (c) rates of larval parasitism. 3. Multiple regression analysis suggested that variation in the per capita rate of increase of O. brumata could be explained by negative feedback from O. brumata density at T–2 (32%), a negative relationship with T. viridana density at T–1 (18%), and a positive relationship with parasitism suffered by T. viridana at T–1 (24%). 4. The T. viridana population time-series was dominated by a rapid feedback process such that per capita rate of increase at time T was negatively related to population density at time T–1, explaining 53% of variance in population growth rate. Per capita rate of increase was unrelated to larval parasitism or densities of O. brumata. 5. In light of previous life-table and experimental studies on O. brumata and T. viridana, the current analyses suggest that pupal predation (data not presented) and interspecific competition are significant determinants of O. brumata population growth rates in Wytham Woods. In contrast, T. viridana population growth rates appear to be dominated by rapid negative feedback consistent with intraspecific competition.     

Predicted changes in the synchrony of larval emergence and budburst under climatic warming

Summary The impact of climatic warming on the synchrony of insect and plant phenologies was modelled in the case of winter moth (Operophtera brumata) and Sitka spruce (Picea sitchensis) in the Scottish uplands. The emergence of winter moth larvae was predicted with a thermal time requirement model and the budburst of Sitka spruce was predicted from a previously published model (Cannell and Smith 1983) based on winter chilling and thermal time. The date of emergence of winter moth larvae was predicted to occur earlier under climatic warming but the date of budburst of Sitka spruce was not greatly changed, resulting in decreased synchrony between larval emergence and budburst. The general question of how a change of climate might affect phenological synchrony and insect abundance is discussed.     

Parasitism and predation as agents of mortality of winter moth populations in neglected apple orchards in Nova Scotia

Abstract.

• 1 This study compared the roles of pupal mortality and parasitism in winter moth (Operophtera brumata) population dynamics in Nova Scotian apple orchards and assessed the importance of beetles as pupal predators.
• 2 The component of pupal mortality termed predation accounted for greater stage-specific mortality of winter moth than parasitism by Cyzenis albicans in four neglected orchards.
• 3 Parasitism by Cyzenis albicans was not spatially density-dependent in any orchard, whereas the predation component of pupal mortality was spatially density-dependent in the two orchards most densely populated by winter moth.
• 4 Field experiments indicated that over 60% of pupal predation may be attributed to beetles, and that about 46% of pupal predation occurred within 4 weeks after pupal drop.
• 5 Mortality of introduced populations of winter moth in Nova Scotia resembles that of native populations in England where density-dependent predation regulates the winter moth population and reduces the parasitoid population to minimal levels. The situation in Nova Scotia appears to have changed appreciably since the establishment of parasitoids into the system in the 1950s.

     

Expansion of the winter moth outbreak range: no restrictive effects of competition with the resident autumnal moth

1. Both direct and indirect competition can have profound effects on species abundance and expansion rates, especially for a species trying to strengthen a foothold in new areas, such as the winter moth (Operophtera brumata) currently in northernmost Finland. There, winter moths have overlapping outbreak ranges with autumnal moths (Epirrita autumnata), who also share the same host, the mountain birch (Betula pubescens ssp. czerepanovii). Competitive interactions are also possible, but so far unstudied, are explanations for the observed 1–3 years phase lag between the population cycles of the two moth species. 2. In two field experiments, we studied host plant‐mediated indirect inter‐specific competition and direct interference/exploitation competition between autumnal and winter moths. The experimental larvae were grown either with the competing species or with the same number of conspecifics until pupation. Inter‐specific competition was judged from differences in pupal mass (reflecting lifespan fecundity), larval development time and larval survival. 3. Larval performance measurements suggested that neither direct nor indirect inter‐specific competition with the autumnal moth reduce the growth rate of winter moth populations. Winter moths even had a higher probability of survival when reared together with autumnal moths. 4. Thus, we conclude that neither direct nor indirect inter‐specific competition is capable of suppressing the spread of the winter moth outbreak range and that both are also an unlikely cause for the phase lag between the phase‐locked population cycles of the two moth species.     

Insect parasites of the winter moth,Operophtera brumata (L.) (Lepidoptera: Geometridae) in western Europe

Summary Sixty-three species of insect parasites of the winter moth,Operophtera brumata (L.) (Lepidoptera: Geometridae), including 26 reared in the present investigation and 37 recorded only in the literature, are listed. Eleven of those reared in the present study are new parasite records for winter moth. Thirteen of the records from the literature are questionable because in each case the identity of either the parasite or host in uncertain. Notes on distribution and life-history are given for species reared in the present study.

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Zusammenfassung In vorliegender Untersuchung wurden insgesamt 63 Insekten als Parasiten des Frostspanner,Operophtera brumata (L.), behandelt. Von diesen sind 37 Arten nur aus der Literatur bekannt. Die übrigen 26 Arten wurden aus dem gesammelten Material gezüchtet. Von letzteren waren 11 Arten bis jetzt noch nicht als Parasiten der Frostspanner bekannt. 13 in der Literatur genannte Arten sind mit einem Fragezeichen zu versehen, weil die Bestimmung der Parasiten-Arten oder des Wirtes zweifelhaft erscheint. Bemerkungen über die Biologie und Verbreitung der von uns gezüchteten Arten werden gegeben.

     

Local outbreaks of Operophtera brumata and Operophtera fagata cannot be explained by low vulnerability to pupal predation

• 1 One of the unresolved questions in studies on population dynamics of forest Lepidoptera is why some populations at times reach outbreak densities, whereas others never do. Resolving this question is especially challenging if populations of the same species in different areas or of closely‐related species in the same area are considered.
• 2 The present study focused on three closely‐related geometrid moth species, autumnal Epirrita autumnata, winter Operophtera brumata and northern winter moths Operophtera fagata, in southern Finland. There, winter and northern winter moth populations can reach outbreak densities, whereas autumnal moth densities stay relatively low.
• 3 We tested the hypothesis that a lower vulnerability to pupal predation may explain the observed differences in population dynamics. The results obtained do not support this hypothesis because pupal predation probabilities were not significantly different between the two genera within or without the Operophtera outbreak area or in years with or without a current Operophtera outbreak.
• 4 Overall, pupal predation was even higher in winter and northern winter moths than in autumnal moths. Differences in larval predation and parasitism, as well as in the reproductive capacities of the species, might be other candidates.

     

Responses of generalist invertebrate predators to pupal densities of autumnal and winter moths under field conditions

• 1 Generalist natural enemies are usually not considered as being capable of causing population cycles in forest insects, but they may influence the population dynamics of their prey in the low density cycle phase when specialist enemies are largely absent.
• 2 In the present field study, the total response of the generalist invertebrate predator community to experimentally established pupal densities of the closely related autumnal (Epirrita autumnata) and winter moths (Operophtera brumata) was analysed.
• 3 Due to the high amount of variation in the dataset, the exact shape of the response curve could not be convincingly estimated. Nevertheless, two important conclusions can be drawn from the analyses.
• 4 Firstly, the natural invertebrate predator community seems to become saturated at rather low densities of both autumnal and winter moth pupae. Secondly, the predator community seems to become saturated at much lower densities of autumnal than of winter moth pupae.
• 5 Furthermore, pupal mass was significantly negatively correlated with invertebrate predation probability in autumnal moth pupae.
• 6 These results indicate that differences in the predator assemblage being able to consume pupae of the two moth species, as well as different handling times, could be responsible for the substantially higher predation rates in winter than in autumnal moth pupae.
• 7 As a consequence, the population dynamics of autumnal moths might be less affected by generalist invertebrate predators than those of winter moths, as autumnal moths seem able to escape from the regulating influence of generalist predators at much lower population densities than winter moths.

     

Genetically variable nucleopolyhedroviruses isolated from spatially separate populations of the winter moth Operophtera brumata (Lepidoptera: Geometridae) in Orkney

Here we report a lepidopteran system in which a pathogen is both abundant and genotypically variable. Geographically separate populations of winter moth (Operophtera brumata L.) were sampled in heather habitats on the Orkney Isles to investigate the prevalence of a pathogen, O. brumata Nucleopolyhedrovirus (OpbuNPV), within the natural system. Virus was recorded in 11 of the 13 winter moth populations sampled, with two populations suffering mortality due to virus at levels of 50%. The virus genome from 200 single insect isolations was investigated for variation using restriction endonuclease digests. Twenty-six variants of OpbuNPV were detected using SalI. The polyhedrin gene of the virus was partially sequenced, allowing the relationship between the 26 variants to be portrayed as a cladogram. The phylogenetic relationship between OpbuNPV and other known baculovirus polyhedrin gene sequences was also established. The discovery of virus at such high prevalence is discussed with reference to occurrence and genetic variation of pathogens in other lepidopteran host populations. This study shows encouraging results for further studies into the role of pathogens in the regulation of host insect populations.     

Population genetic structure of the winter moth,Operophtera brumata Linnaeus,in the Orkney Isles suggests long‐distance dispersal

1. The application of population genetic analysis and molecular ecological approaches allows us to examine the invasion of species in the wild. In particular, we can gain an insight into the role of dispersal, a key determinant of the invasion and population dynamics of important pest species. Since the 1980s, severe outbreaks of the winter moth, Operophtera brumata (Linnaeus), have caused extensive damage to heather moorlands in the Orkney Isles. The population genetic structure of O. brumata in Orkney was examined in order to establish whether the widely dispersed outbreaking populations are connected. 2. Amplified fragment length polymorphism (AFLP) analysis showed a high level of genetic diversity within subpopulations. This is consistent with an initial mass colonisation event and/or continuing dispersal between populations of O. brumata in Orkney. 3. Genetic differentiation among populations is low, and although some weak isolation by distance is detectable, no effect of isolation as a result of a sea barrier was found. High gene flow between populations is consistent with the low genetic differentiation observed, although there is evidence to suggest that the populations are not panmictic. 4. Given the limited dispersal of adults, the present results suggest that larvae may disperse over considerable distances by ballooning on strong winds across the Orkney Isles.     

Invading and resident defoliators in a changing climate: cold tolerance and predictions concerning extreme winter cold as a range‐limiting factor

1. Winter temperatures in northern latitudes are predicted to increase markedly as a result of ongoing climate change, thus making the invasion of new insect defoliators possible. The establishment of new outbreak pest species may have major effects on northern ecosystems that are particularly sensitive to disturbances. 2. Effects of winter minimum temperatures under field and laboratory conditions were examined and limitations by minimum temperatures on future range expansion were investigated for invasive [Operophtera brumata (Lepidoptera: Geometridae)] and potentially invasive [Agriopis aurantiaria (Lepidoptera: Geometridae)] birch‐feeding forest pests. The results for the studied invasive and potentially invasive moths were compared with the parameters of the resident moth species Epirrita autumnata (Lepidoptera: Geometridae). 3. The results showed tolerated critical temperatures of the invader (O. brumata) and the resident (E. autumnata) were more similar (differing only by 1 °C), whereas the potential invader (A. aurantiaria) was much less tolerant of cold temperatures. Although describing different stages of overwintering, results were consistent between laboratory and field studies except for those at one field location, at which other abiotic conditions are suggested to have significant influence on moth egg survival. 4. Based on the present results and expected changes in winter temperatures over the next 30 years, the range expansion of an established invasive species may be predicted. No limitations were found regarding the possible future invasion of a new pest species to northern Fennoscandia. The importance of studying a species' whole overwintering period is highlighted and further studies devoted to the effects of other abiotic factors in addition to the effects of temperature are suggested.     

Identification of winter moth (Operophtera brumata) refugia in North Africa and the Italian Peninsula during the last glacial maximum

Numerous studies have shown that the genetic diversity of species inhabiting temperate regions has been shaped by changes in their distributions during the Quaternary climatic oscillations. For some species, the genetic distinctness of isolated populations is maintained during secondary contact, while for others, admixture is frequently observed. For the winter moth (Operophtera brumata), an important defoliator of oak forests across Europe and northern Africa, we previously determined that contemporary populations correspond to genetic diversity obtained during the last glacial maximum (LGM) through the use of refugia in the Iberian and Aegean peninsulas, and to a lesser extent the Caucasus region. Missing from this sampling were populations from the Italian peninsula and from North Africa, both regions known to have played important roles as glacial refugia for other species. Therefore, we genotyped field‐collected winter moth individuals from southern Italy and northwestern Tunisia—the latter a region where severe oak forest defoliation by winter moth has recently been reported—using polymorphic microsatellite. We reconstructed the genetic relationships of these populations in comparison to moths previously sampled from the Iberian and Aegean peninsulas, the Caucasus region, and western Europe using genetic distance, Bayesian clustering, and approximate Bayesian computation (ABC) methods. Our results indicate that both the southern Italian and the Tunisian populations are genetically distinct from other sampled populations, and likely originated in their respective refugium during the LGM after diverging from a population that eventually settled in the Iberian refugium. These suggest that winter moth populations persisted in at least five Mediterranean LGM refugia. Finally, we comment that outbreaks by winter moth in northwestern Tunisia are not the result of a recent introduction of a nonnative species, but rather are most likely due to land use or environmental changes.     

Some factors that affect the annual cycle of the winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae) in western Europe

Egg development rate in the winter moth (Operopbtera brumata (L.)) is increased by higher temperatures between at least 6.0° C and 18° C. Pupal development rate is, in general, reduced by higher temperatures. Therefore, lower temperatures in northern localities and at high altitudes in Europe increase the duration of the egg stage and decrease that of the pupa. Inherent differences in the eggs and pupae from different localities increase the effect of temperature differences.

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Resume La température affecte directement le taux de développement des oeufs et inversement celui des pupes chez la phalène hiémale, Operopbtera brumata (L.). Dans le nord de l'Europe, une température relativement basse a pour effet de prolonger la durée du stade de l'oeuf et de raccourcir proportionnellement celle du stade de la pupe, tandis que dans le sud de l'Europe avec de plus hautes températures, l'effet est contraire. Les différences inhérentes aux oeufs et aux pupes dans diverses localités augmentent l'effet des différences de température.

     

Delayed density-dependent parasitism of eggs and pupae as a contributor to the cyclic population dynamics of the autumnal moth

Many populations of forest Lepidoptera exhibit 10-year cycles in densities, with impressive outbreaks across large regions. Delayed density-dependent interactions with natural enemies are recognized as key factors driving these cyclic population dynamics, but emphasis has typically been on the larval stages. Eggs, pupae and adults also suffer mortality from predators, parasitoids and pathogens, but little is known about possible density relationships between mortality factors and these non-feeding life stages. In a long-term field study, we experimentally deployed autumnal moth (Epirrita autumnata) eggs and pupae to their natural enemies yearly throughout the 10-year population cycle in northern Norway. The abundance of another geometrid, the winter moth (Operophtera brumata), increased in the study area, permitting comparisons between the two moth species in predation and parasitism. Survival of autumnal moth eggs and pupae was related to the moth abundance in an inverse and delayed manner. Egg and pupal parasitoids dominated as density-dependent mortality factors and predicted the subsequent growth rate of the host population size. In contrast, effects of egg and pupal predators were weakly density dependent, and generally predation remained low. Parasitism rates did not differ between the autumnal and winter moth pupae, whereas predators preferred winter moth pupae over those of the autumnal moth. We conclude that parasitism of the autumnal moth by egg and pupal parasitoids can be related to the changes of the moth density in a delayed density-dependent manner. Furthermore, egg and pupal parasitoids cannot be overlooked as causal factors for the population cycles of forest Lepidoptera in general.     

Long-term dynamics of <Emphasis Type="Italic">Operophtera brumata</Emphasis> L. in the oak stands of forest-steppe

The study overviews contemporary investigations on Operophtera brumata L. and its outbreak series in the oak stands of the southern forest-steppe zone over the recent 60 years. Autumnal flight of the moth has been studied.     

Using the SSU,ITS, and Ribosomal DNA Operon Arrangement to Characterize Two Microsporidia Infecting Bruce Spanworm,Operophtera bruceata (Lepidoptera: Geometridae)

Research pertaining to the two closely‐related microsporidian genera Nosema and Vairimorpha is hindered by inconsistencies in species differentiation within and between the two clades. One proposal to better delimit these genera is to restructure the Nosema around a “True Nosema” clade, consisting of species that share a characteristic reversed ribosomal DNA operon arrangement and small subunit (SSU) ribosomal DNA sequences similar to that of the Nosema type species, N. bombycis. Using this framework, we assess two distinct microsporidia recovered from the forest insect Bruce spanworm (Operophtera bruceata) by sequencing their SSU and internal transcribed spacer regions. Phylogenetic analyses place one of our isolates within the proposed True Nosema clade close to N. furnacalis and place the other in the broader Nosema/Vairimorpha clade close to N. thomsoni. We found that 25% of Bruce spanworm cadavers collected over the four‐year study period were infected with microsporidia, but no infections were detected in cadavers of the Bruce spanworm's invasive congener, the winter moth (O. brumata), collected over the same period. We comment on these findings as they relate to the population dynamics of the Bruce spanworm‐winter moth system in this region, and more broadly, on the value of ribosomal DNA operon arrangement in Nosema systematics.     

Postglacial recolonization shaped the genetic diversity of the winter moth (Operophtera brumata) in Europe

Changes in climate conditions, particularly during the Quaternary climatic oscillations, have long been recognized to be important for shaping patterns of species diversity. For species residing in the western Palearctic, two commonly observed genetic patterns resulting from these cycles are as follows: (1) that the numbers and distributions of genetic lineages correspond with the use of geographically distinct glacial refugia and (2) that southern populations are generally more diverse than northern populations (the “southern richness, northern purity” paradigm). To determine whether these patterns hold true for the widespread pest species the winter moth (Operophtera brumata), we genotyped 699 individual winter moths collected from 15 Eurasian countries with 24 polymorphic microsatellite loci. We find strong evidence for the presence of two major genetic clusters that diverged ~18 to ~22 ka, with evidence that secondary contact (i.e., hybridization) resumed ~ 5 ka along a well‐established hybrid zone in Central Europe. This pattern supports the hypothesis that contemporary populations descend from populations that resided in distinct glacial refugia. However, unlike many previous studies of postglacial recolonization, we found no evidence for the “southern richness, northern purity” paradigm. We also find evidence for ongoing gene flow between populations in adjacent Eurasian countries, suggesting that long‐distance dispersal plays an important part in shaping winter moth genetic diversity. In addition, we find that this gene flow is predominantly in a west‐to‐east direction, suggesting that recently debated reports of cyclical outbreaks of winter moth spreading from east to west across Europe are not the result of dispersal.