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.

     

Density dependence and the stabilization of animal numbers

Summary Latto and Hassell (1987) disagree with the conclusion of Den Boer (1986), that the winter moth population at Wytham Wood, studied by Varley and Gradwell, was not regulated. They attempt to demonstrate regulation by means of a simulation model. In the present paper the validity of this model is tested step by step. The fixing of the initial and final densities, as practised by Den Boer and rejected by Latto and Hassell, did not prevent population explosions and extinctions, as was assumed by Latto and Hassell. It is shown that the deterministic formulation of the density dependence of pupal predation, as used by Latto and Hassell, deviates systematically from the field data. Replacing the values of the key-factor (k₁) by random values drawn from a normal distribution (Latto and Hassell) affects the dynamics such that the ability of pupal predation to govern density is improved in the model. Changing mortalities other than the key-factor does not significantly influence the pattern of fluctuations nor the limits of density. Models should leave intact the essentials of the reality under study, while removing distracting elements (Levins 1968). As both the timing of the key-factor, and its correlation with pupal predation are essential features of the winter moth population at Wytham Wood between 1950 and 1968, the model of Latto and Hassell does not apply to this population. By simply changing log₁₀ (eggs/female) it is shown that the power of the density dependence of pupal predation to govern possible trends in density of the winter moth population at Wytham Wood is weak. On the other hand, the model of Latto and Hassell gives insight into the conditions that might favour regulation of numbers. Although the model of Poethke and Kirchberg (1987) preserves more features of the pertinent winter moth population than that of Latto and Hassell (1987) it still deviates in one essential aspect: the succession in time of both the (coupled) mortalities and the deviations from the deterministic density dependence are taken at random. Therefore, also this model is still too far from the field population to be a sound base for the statistical speculation proposed by Poethke and Kirchberg.Communication No. 339 of the Biological Station, Wijster     

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.     

Escape from pupal predation as a potential cause of outbreaks of the winter moth, Operophtera brumata

The winter moth, Operophtera brumata , shows varying population dynamics in different host plant habitats. Populations in Sitka spruce, Picea sitchensis, plantations and in Scottish moorlands have a tendency to outbreak that is not shown by winter moth in lowland oak woods. Since pupal predators have previously been identified as being important for the regulation of winter moth in a lowland oak wood it was hypothesized that invertebrate pupal predators were failing to control winter moth in outbreak populations. This hypothesis was tested by comparing the abundance of invertebrate predators and patterns of spatially density dependent pupal predation across habitats. Several results supported this hypothesis. Carabid predators of winter moth were one or two orders of magnitude more abundant in oak woods than in moorland or spruce habitats. Staphylinid predators were also more abundant in high winter moth density oak woods than in any other habitat. Beetle predation of tagged cocoons in the field was inversely density dependent in Highland moors in experiments in 1999 and 2000, and in Sitka spruce in 1999. However, in opposition to our hypothesis, pupal predation was also inversely density dependent in oak woods in 2000, although this result may be explained by the low range of winter moth densities in the field that year. These results are discussed in relation to the role of natural enemies in regulating winter moth populations and the differences in life-history of the beetle predators in different habitats.     

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.

     

Predation of codling moth Cydia pomonella L. by the Silvereye Zosterops lateralis (Latham)

Predation of cocooned larvae of codling moth Cydia pomonella by silvereyes Zosterops lateralis was studied in an apple orchard in Nelson, New Zealand. Apple logs with known larval densities were made available to the birds for known periods of time, either in cages or exposed in the apple orchard. The numbers of silvereyes and the natural predation of codling moth were recorded in the same orchard. Predation was density dependent. On caged logs with an initial high density of 32 larvae, 1.1 larvae were consumed per bird‐hour; in contrast, one larva was consumed per 34.5 bird‐hours at three larvae per log. A curvilinear relationship was demonstrated between larval density and the bird‐hours required for predation; this relationship was consistent with the known density dependence of silvereye predation of codling moth. A regression of the total annual winter bird predation of larvae in the orchard on bird numbers was significant. However, the density dependence of predation resulted in declining rates of predation over the winter as larval density declined; the first birds to arrive in the orchard benefitted from particularly high predation rates. As a consequence, fluctuations in bird numbers during the winter had only a secondary influence on predation rates. The numbers of silvereyes in the orchard showed no relationship to the density of the codling moth population present. This study confirmed the importance of silvereyes in the predation of codling moth and a functional, not numerical, rseponse of these birds to codling moth density.     

Resources and dispersal as factors limiting a population of the tussock moth (Orgyia vetusta), a flightless defoliator

The western tussock moth (Orgyia vetusta) is very abundant on one stand of bush lupine (Lupinus arboreus) at the Bodega Marine Reserve (Sonoma Co, Calif., USA), but is sparse or absent on nearby stands. To determine what controls its abundance, both within the outbreak area and more globally, I performed experimental manipulations of resource availability and dispersal. To measure resource limitation, I inoculated 30 caged and 30 uncaged bushes with a realistic range of numbers of tussock moth eggs. On caged bushes, starvation led to density-dependent reductions in survival, pupal weight and fecundity. Larvae on uncaged bushes experienced density-independent ant predation on early instars and density-dependent emigration by late instars. From the results of this experiment, I predicted the density of a resource-limited tussock moth population. The predictions agreed fairly well with data from the outbreak area in 1992. To measure dispersal by the moth, which has flightless adult females, I released 30,000 tussock moth eggs at a central point in each of two uninfested lupine stands, and censused larvae weekly in a circle of radius 16 m until pupation. Median displacement over one entire generation was only 2 m, or about 2 bush radii. Rearing experiments indicated that bushes outside the out-break area are fully nutritionally suitable for the moth. I conclude that two major factors limiting the population are resources (within the outbreak area) and inefficient dispersal (more globally).     

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.     

Integrated control of apple pests in New Zealand 10. Population dynamics of codling moth in Nelson

Abstract

Sampling methods are described for estimating the population density, mortality, and natality of a univoltine population of codling moth attacking mature apple trees (cv. ‘Delicious’) at Nelson, New Zealand. These methods were used to construct life tables for the species over eight generations (1967–68 to 1974–75) on trees variously sprayed and not sprayed with ryania in an integrated control programme. Bait traps provided a sensitive measure of seasonal adult population density. Analysis of the life tables shows that migration of adults was the main key factor and that overwintering larval mortality (particularly that due to bird predation), fecundity, and ryania also made a major contribution to variation in generation mortality. In the absence of ryania the resident population usually increased between generations, whereas it usually decreased when ryania sprays were applied. The density dependence of overwintering larval mortality was due to bird predation, and the inverse density dependence of larval mortality from ryania was due to changes in the site of fruit entry with larval population density. Fecundity was density independent, and inconclusive evidence was obtained on the density dependence of migration. The wide variation in fecundity is attributed primarily to weather conditions. The impact on control strategy of the above key factors, density dependence, and total natural mortality is discussed. Ryania is found to be uneconomic, whereas the granulosis virus of codling moth and male removal with pheromone traps show promise as future control methods. The need to eliminate reservoirs of codling moth close to orchards under integrated pest control is emphasised. Regulation of codling moth populations at Nelson on neglected, unsprayed trees appears to result from intraspecific competition for fruits and cocooning sites, and weakly density-dependent mortality of mature larvae when seeking cocooning sites and while overwintering in their cocoons. Variation in fecundity also cohtributes to fluctuations in abundance of the species. In contrast, at low density in an integrated control programme no intraspecific competition was evident; migration, winter mortality, and fecundity were the main determinants of abundance. This illustrates the need to study pest populations at densities similar to those tolerable commercially.     

Interspecific predation as a mortality factor among overwintering spiders

Summary Results from field experiments indicate that predation occurs among spruce-living spiders during winter in SW Sweden. Field observations of natural activity showed that Philodromus spp and Pityohyphantes phrygianus together make up 80% of the spiders active on spruce in winter. They are therefore potential predators on other overwintering spiders. Laboratory experiments were performed at +4° C to assess the importance of such predation between spiders. Small spiders (length <2.5 mm) had a mean winter mortality of 58% when kept together with large spiders (2.5 mm) which had a mean mortality of 3% only. Among the small spiders the Erigninae spp seemed to be more vulnerable to predation than other taxonomic groups. Predation also occurred when large P. phrygianus were kept together, but such predation caused mortality of less importance to the spider populations than the mortality among small spiders. Differences in spider density and food availability did not change this pattern. Considerable weight increase occurred in subadult P. phrygianus when fed during winter. This suggests that winter foraging specimens increase their fitness. Interspecific predation among spiders is suggested to be an important mortality factor in natural populations at high spider densities in November and December, when the ambient temperature often is above 0° C and when the density of large spiders is not yet substantially reduced by bird predation.     

Supply-side control over the survivorship of Chthamalus spp. recruits in northern Baja California

The constant supply of larvae to coastal habitats is important for the persistence of populations and can vary depending on oceanic conditions that may affect physical transport processes. We evaluated the survivorship of Chthamalus recruits in Playa San Miguel, Baja California, for over a year to evaluate if the supply of new recruits was of greater importance than the post-recruitment factors of competition and predation in determining adult population size. We hypothesized that the number of Chthamalus recruits would predict the number of adults present and that predation and competition would not play a significant role in determining adult densities. Recruit density was a robust predictor of adult density despite the presence of weak density-dependent mortality. Neither predation nor competition significantly affected the survivorship of recruits and did not decouple the relationship between recruit and adult densities, suggesting that these post-recruitment controls did not play an important role in determining the population size of Chthamalus barnacles at this site. The data support the hypothesis that supply-side control is the primary factor structuring the population of Chthamalus in the intertidal community at Playa San Miguel.     

Biology ofhyphantria cunea drury (lepidoptera : Arctiidae) in Japan. IX. population dynamics

Fluctuations in population density of Hyphantria cunea in Japan are characterized by a gradation-like pattern. Analysis of the life table data taken from two stations during eight successive generations showed that (1) mortality during egg and early larval stages was density-independent, (2) mortality during later larval stages was inversely density-dependent, and (3) mortality during prepupal and pupal stages was density-independent. Thus the overall mortality process from egg to adults eclosion was inversely density-dependent. The inverse density-dependence in mortality process during later larval instars was mainly attributed to the ‘escape’ (VOÛTE, 1946) of H. cunea populations from the predation pressure of polyphagous predators such as birds and Politses wasps. This inverse density-dependence was considered to be a cause of gradation-like fluctuation. Field collection of egg-masses showed that the mean number of eggs per egg-mass, which was believed to be a good representation of mean fecundity, varied from 425 to 1050 during 4 years. Density-dependent reduction in the mean number of eggs per egg-mass was demonstrated, and this reduction was a factor regulating the population density. Assuming fixed sex ratio and survival rate of adults, a preliminary population model was constructed. The number of eggs laid in the survey station could be predicted well by the model based on the number of eggs laid in the previous generation, in 9 out of 13 cases. An attempt to apply a model of the same type to mimic the fluctuation of abundance (peak number of larval colonies per tree) on road-side trees suggested another density-dependent process, that is, insecticide application by man. Discussion was also presented on the causes responsible for the turn of population trend from decreasing to increasing in the 1st generation of 1968.     

Temporal and spatial variation of larval parasitism in non-outbreaking populations of a folivorous moth

In order to assess the role of parasitoids in the regulation of non-outbreaking populations of Epirrita autumnata, a geometrid lepidopteran with outbreaking populations in northern Europe, we examined the temporal and spatial variation of larval parasitism in southwestern Finland during 6 successive years. The study was carried out on two spatial scales, among trees within sites of about 1 ha and among sites separated by distances of 2–10 km, using experimental and observational approaches respectively. The overall percent parasitism was independent of host density on both spatial scales, while temporally it fluctuated only little. Of the two main parasitoids, the commoner one, Protapanteles immunis, showed a variable response to host density on the larger spatial scale and negative density dependence on the smaller scale. Temporally, parasitism caused by this species was independent of host density. Another parasitoid, Phobocampe bicingulata, showed positive density dependence on the smaller spatial scale and had a variable response on the larger scale, but exhibited negative density dependence over time. The results of this study caution against drawing conclusions concerning population regulation on the grounds of spatial density dependence alone. Larval parasitoids apparently do not maintain low densities in the E. autumnata populations studied. However, they may suppress E. autumnata densities to a level low enough for density-dependent mortality factor(s) to become regulating. Among other mortality factors of E. autumnata, pupal predation has been found to be temporally positively density-dependent. Received: 19 October 1999 / Accepted: 10 January 2000     

Seasonal variation in the functional response of a coral-reef piscivore alters the inverse density-dependent mortality of its prey

Density-dependent processes are critical for regulating species’ populations, and piscivory of coral-reef fishes is frequently density dependent. However, the mechanism driving this density-dependent mortality is poorly understood, but may be caused by changes in a predator’s feeding rate at different prey densities (its functional response). An aquarium experiment replicated in winter and summer examined the functional response after 22 and 47 h of Cephalopholis cruentata feeding on Halichoeres pictus. With the exception of summer data after 47 h (density-independent mortality), mortality was inversely density dependent across all prey densities and increased with higher summer temperatures. The absence of an asymptotic pattern of inverse density-dependent mortality was caused by type II (summer) or dome-shaped type IV (winter) functional responses, with the benefits of schooling likely to cause the low mortality rates at higher prey densities. Predators’ functional responses may underlie the inverse density-dependent mortality reported in field studies of aggregating fishes.     

Can predation cause the 10-year hare cycle?

Summary We relate causes of mortality of snowshoe hares to density of hares over an 8-year period that included a peak in numbers. We then use simulation modeling to examine whether these density-dependent relationships could produce changes in hare density similar to those observed in our study are in Yukon, Canada.Predation during winter was the largest source of mortality for snowshoe hares at Kluane, Yukon during 1978–84. There was a one-year lag in the response of winter predation mortality rate to hare density. There was a two-year lag in the response of winter mortality not caused by predators to hare density.A simple simulation model with density-dependent predation produced 8–11 year cycles only within a narrow range of parameters that are inconsistent with data from the Kluane region. However, a simulation model that predicted winter mortality rates using a delayed density-dependent numerical response and a Type II functional response by predators, produced 8–11 year cycles within the range of parameter values measured in our study. Yet another simulation model that predicted both summer and winter mortality rates using a delayed density-dependent numerical response and a Type II functional response by predators, did not produce 8–11 year cycles within the range of parameter values measured in our study. Lack of data on juvenile mortality may be one reason for this result.     

THE NATURAL CONTROL OF POPULATIONS OF BUTTERFLIES AND MOTHS

1. Life-table data for 14 species of Lepidoptera are analysed by the k -factor technique of Varley & Gradwell (1960). Two factors are shown to be of particular importance in determining fluctuations in abundance from one generation to the next. These key factors are predators and the failure of females to lay their full complement of eggs.
2. Data from 24 studies are reviewed to identify any density-dependent factors that would be capable of regulating the populations about an equilibrium density. In eight studies no density-dependent relationships could be identified, and in a further 13 the only density dependence demonstrated was due to intraspecific competition for resources. It is argued that competition is incapable of regulating populations at low density. In the other three studies, natural enemies are thought to be acting in a density-dependent manner, but their ability to regulate the populations is questioned.
3. The frequency of over-population and of extinction is reviewed and both appear to occur frequently in Lepidoptera. This, coupled with the failure of most studies to demonstrate the existence of density-dependent processes capable of regulating populations, leads the author to reject the model of regulation about an equilibrium density in favour of a model of population limitation by a ceiling set by resources.
4. Fluctuations in resource availability may be important in determining variations in the abundance of many Lepidoptera, but at present too few ecologists have quantified the carrying capacity of habitats occupied by the species they study to generalize about this.     

Dispersion pattern and mortality of seeds and seedlings ofFagus crenata Blume in a cool temperate forest in western Japan

The seed and seedling mortality ofFagus crenata Blume after a mast year (1993) was examined in relation to density and distance from the nearest conspecific adult tree in a mixed conifer-hardwood forest in Ohdaigahara, western Japan. The mortality of fallen seeds during winter amounted to 93.7%, and 79.2% of the current-year seedlings died in the first growing season. The most important factor of death for both seeds and seedlings was predation by vertebrates. The mortality of seeds during winter was positively correlated with sound seed density. The mortality of seedlings was positively correlated with density but not significantly related to the distance from the nearest crown edge of a conspecific adult tree. Mortality patterns varied with stages and spatial scales due to the behavior of predators; it is thus important to investigate the spatial pattern of seeds and seedling mortality at various temporal and spatial scales. After the first growing season, the difference in seedling density between distance classes was not significant at <4m from the nearest adult trees due to density-dependent mortality. However, seedling density was significantly lower in the ≥4 m class than in the <4 m classes.     

A note on key factor analysis

Various aspects of a model for key factor analysis (Manly , 1977a) are discussed. Equations for estimating the parameters of the model are given. The jackknife method is suggested for obtaining standard errors for estimators. The case of circular populations (where the adults in one generation produce all the individuals alive at the start of the next, generation) is considered. A computer program is described. Varley et al.'s (1973) data on the winter moth is used for illustrative purposes.     

Density-related mortality of the flour beetle,Tribolium confusum duval

Life tables were constructed to assess the relative importance of some factors causing mortality of Tribolium confusum and to gauge their response to increasing population density. Observations focussed on three population densities (100, 400 and 800 individual/8 g medium) from the egg to the adult stage. The medium was not renewed in order to maximize predatory interactions. Generation mortality at densities 100, 400 and 800 was 42%, 50% and 74% respectively, i. e. density-dependent. Mortality in the first 10 days was also density-dependent reaching a maximum of 27% at density 800: predation by small larvae on eggs seemed the principal causative factor. The overall pattern of larval mortality was density-independent. Data on the mortality of pupae and callows were ultimately consistent with an inversely density-dependent pattern. Apparently, only mortality occurring within the first 10 days was capable of population regulation.