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.     

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.

     

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.     

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.

     

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.

     

Invasion spread of Operophtera brumata in northeastern United States and hybridization with O. bruceata

We used five methods to estimate the rate of spread of the winter moth, Operophtera brumata L., a European Lepidoptera, invading the northeastern USA and occasionally hybridizing with the closely related O. bruceata. These two species utilize the same sex attractant and pheromone traps capture both species. We estimated spread based on the ratio of the two species captured in pheromone-baited traps. Population boundaries were derived from captures in a grid of traps and spread was estimated as 6.6 km/year based on displacement of population boundaries between 2005 and 2008. Radial spread rate was also estimated as 6.9 km/year from the displacement of boundaries using logistic regression of trap captures along a single east–west transect of traps deployed yearly from 2007 to 2011. We also estimated the rate of spread from the expansion of defoliation mapped during aerial surveys. Based on the displacement of defoliation boundaries from 2005 to 2008, spread rate was estimated as 6.0 km/year. Based on the year of first defoliation, spread was estimated as 4.8 km/year and regression of the square-root of the cumulative area/π versus time yielded an estimate of 4.7 km/year. All five estimates were similar, and differences reflect the nuances of the data from which they were derived. We discuss here how the occasional hybridization with O. bruceata may be either retarding or enhancing O. brumata spread.     

Identification of a nucleopolyhedrovirus in winter moth populations from Massachusetts

Winter moth, Operophtera brumata, originally from Europe, has invaded eastern Massachusetts causing widespread defoliation and damage to many deciduous tree species and a variety of crop plants in the infested area. We identified O. brumata nucleopolyhedrovirus (OpbuNPV) in winter moth larvae collected from field sites in Massachusetts by using PCR to amplify a 482 bp region of the baculovirus polyhedrin gene. Viral sequences were also detected in winter moth pupae that failed to emerge, suggesting that these insects may have died as a result of viral infection. This represents the first report of OpbuNPV in winter moth populations in the US.     

Behavioural responses of the leaf-chewing guild to the presence of Eriocrania mines on silver birch (Betulapendula)

1. Interactions between early season leaf-miners from the genus Eriocrania Zeller (Eriocraniidae: Lepidoptera), and the leaf-chewing guild of silver birch (Betula pendula Roth) were investigated. 2. Field observations indicated that a negative association between damage caused by Eriocrania, and leaf-chewers could be observed under certain conditions, namely at higher damage densities in the final week of mine development on trees with relatively high densities of mines. 3. Experimental manipulation of Operophtera brumata L. (Geometridae: Lepidoptera) densities in the field confirmed the negative association between established mines of Eriocrania, and this species of free-living folivore. 4. The behaviour of O. brumata was modified further in the presence of mines. On branches where mined leaves were present, O. brumata larvae consumed a larger proportion of leaf tissue, by continuing to feed on the same leaf longer rather than shifting to a new leaf. Increased consumption may indicate some modification of leaf quality beyond the leaves occupied by Eriocrania. Alternatively, it may indicate an association between Eriocrania, and higher quality leaf material.     

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.     

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.     

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.     

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.     

The potential for interspecific competition between two abundant defoliators on oak: leaf damage and habitat quality

Abstract. 1. The pedunculate oak, Quercus robur L., suffers high annual levels of spring defoliation in Wytham Woods, Oxon. The two major defoliators, Tortrix viridana L. and Operophtera brumata L., sometimes reach high enough densities to completely defoliate trees.
2. Experiments with larvae of both species enclosed on oak trees in Wytham Woods suggest considerable potential for intra- and interspecific competition between T. viridana and O. brumata.
3. T. viridana and O. brumata consume equivalent amounts of leaf tissue per unit caterpillar density. Despite this, O. brumata is the superior competitor, measured by mortality during the larval feeding period.
4. Evidence is presented that T. viridana larvae depend upon the protected microclimate of leaf rolls to maintain water balance, and that leaf damage may disrupt the construction of, and microclimate within, leaf rolls. O. brumata may therefore be competitively superior because it indirectly interferes with the water balance of T. viridana.
5. The importance of interspecific competition in the dynamics of T. viridana and O. brumata populations is discussed. Stochastic mortality factors acting on first instar larvae of both species probably make intense competition a rare event.     

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.     

Spatially patterned guild structure in larval parasitoids of cyclically outbreaking winter moth populations

1. Wide temporal fluctuations in host abundance are a potential source of instability and stochasticity in the spatiotemporal population dynamics of associated parasitoid species. Within parasitoid guilds (i.e. parasitoids with similar modes of host utilisation), a conceivable outcome is guild organisation according to a lottery model, in which guild members attain local dominance by colonising previously emptied habitats during increasing host density, before other guild members. In the spatial dimension, an expected manifestation of such dynamics is variable guild structure even across homogeneous habitats. 2. We examined the extent of large‐scale spatial patterning of guild characteristics in larval parasitoid wasps associated with cyclically outbreaking populations of the geometrid moth Operophtera brumata in northern Fennoscandia. The study was performed at the onset of the crash‐phase of the geometrid's outbreak cycle, along a 70‐km transect in costal northern Norway, characterised by largely homogeneous environmental conditions, except for a small climatic gradient. 3. There was a distinct large‐scale spatial turnover in dominance among the major parasitoid groups (i.e. guild structure) in O. brumata along the transect, whereas the total prevalence rate of the guild and its diversity showed no consistent variation. Guild structure was unrelated to host density. 4. Although group‐specific responses to a slight spatial climatic gradient cannot be rejected as a causal mechanism, we conclude that our results are consistent with the expectation from large‐scale stochastic extinction‐recolonisation dynamics among functionally equivalent parasitoids relying on a host with strongly cyclic population fluctuations.     

How rapidly do invasive birch forest geometrids recruit larval parasitoids? Insights from comparison with a sympatric native geometrid

Two related issues in studies of biological invasions are how quickly the enemy complexes of invasive species become as species-rich and efficient as those of native species and how important enemy release is for the establishment and spread of invaders. We addressed these issues for the geometrid moths Operophtera brumata and Agriopis aurantiaria, who invaded the coastal mountain birch forest of northern Norway by range expansion approximately a century and 15 years ago, respectively. This was done by comparing larval parasitoid species richness and prevalence among the invaders and the native geometrid Epirrita autumnata. We found that E. autumnata and O. brumata both hosted seven parasitoid species groups, whereas A. aurantiaria hosted only one. Several parasitoid groups were shared between two or more of the geometrids. Total larval parasitism rates were similar in all three geometrid species, and comparison with published studies on larval parasitism in Western Europe suggested that O. brumata and A. aurantiaria do not suffer lower parasitism rates in our study region than in their native ranges. Our results indicate that accumulation of larval parasitoids on invasive geometrids in coastal mountain birch forest may reach completion within a few decades to at least a century after the invasion, and that establishment and spread of such invaders is unlikely to be facilitated by release from larval parasitism. Our investigations also uncovered a high degree of spatiotemporal synchrony between the total larval parasitism rates of O. brumata and A. aurantiaria, suggesting that larval parasitism of different geometrid species in the study system is governed by some common external factor.     

Manipulation of oviposition patterns of the parasitoidCyzenis albicans (Tachinidae) in the field using plant extracts

We examine the oviposition behavior of the parasitic fly Cyzenis albicans(Fall.) to determine if long-distance or contact chemical cues given off by damaged oak and apple foliage influences the attack of their host the winter moth Operophtera brumata(L.). Wind-tunnel experiments indicate the presence of an attractive odor in oak leaves and the absence of an attractant in apple leaves. The application of oak foliage extracts to apple trees increased the number of parasitoid eggs laid and the level of parasitism of winter moths in the field. The impact of altered host-seeking behavior by the parastoid is discussed in the context of the population ecology of its host.     

Density-dependent effects of larval dispersal mediated by host plant quality on populations of an invasive insect

The success of invasive species is often thought to be due to release from natural enemies. This hypothesis assumes that species are regulated by top-down forces in their native range and are likely to be regulated by bottom-up forces in the invasive range. Neither of these assumptions has been consistently supported with insects, a group which includes many destructive invasive species. Winter moth (Operophtera brumata) is an invasive defoliator in North America that appears to be regulated by larval mortality. To assess whether regulation was caused by top-down or bottom-up forces, we sought to identify the main causes of larval mortality. We used observational and manipulative field and laboratory studies to demonstrate that larval mortality due to predation, parasitism, and disease were minimal. We measured the response of larval dispersal in the field to multiple aspects of foliar quality, including total phenolics, pH 10 oxidized phenolics, trichome density, total nitrogen, total carbon, and carbon–nitrogen ratio. Tree-level declines in density were driven by density-dependent dispersal of early instars. Late instar larvae dispersed at increased rates from previously damaged as compared to undamaged foliage, and in 2015 field larval dispersal rates were related to proportion of oxidative phenolics. We conclude that larval dispersal is the dominant source of density-dependent larval mortality, may be mediated by induced changes in foliar quality, and likely regulates population densities in New England. These findings suggest that winter moth population densities in New England are regulated by bottom-up forces, aligning with the natural enemy release hypothesis.     

Do multitrophic interactions override N fertilization effects on <Emphasis Type="Italic">Operophtera</Emphasis> larvae?

We examined how performance of Operophtera brumata (Lepidoptera) larvae was affected by nitrogen (N) fertilization of boreal forest understorey vegetation. We monitored larval densities on Vaccinium myrtillus plants for a period of 7 years in a field experiment. Preliminary results indicated that the N effect on larval densities was weak. To examine if this was due to indirect interactions with a plant pathogen, Valdensia heterodoxa, that share the same host plant, or due to top-down effects of predation, we performed both a laboratory feeding experiment (individual level) and a bird exclusion experiment (population level) in the field. At the individual level, altered food plant quality (changes in plant concentration of carbon, N, phenolics, or condensed tannins) due to repeated infection by the pathogen had no effect on larval performance, but both survival to the adult stage and adult weight were positively affected by N fertilization. Exclusion of insectivorous birds increased the frequency of larval damage on V. myrtillus shoots, indicating higher larval densities. This effect was stronger in fertilized than in unfertilized plots, indicating higher bird predation in fertilized plots. Predation may thus explain the lack of fertilization effect on larval densities in the field experiment. Our results suggest that top-down effects are more important for larval densities than bottom-up effects, and that bird predation may play an important role in population regulation of O. brumata in boreal forests.Electronic Supplementary Material Supplementary material is available for this article at     

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