Winter Moth Populations Research Articles

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.

Cyzenis albicans(Diptera: Tachinidae) Does Not Prevent the Outbreak of Winter Moth (Lepidoptera: Geometridae) in Birch Stands and Blueberry Plots on the Lower Mainland of British Columbia

In the late 1980s, a new outbreak of the introduced winter moth, Operophtera brumata (L.), occurred in Richmond, on the lower mainland of British Columbia. This was accompanied by the introduced parasitoid, Cyzenis albicans (Fallen). Populations were monitored at 2 birch woodlands and 2 blueberry plots between 1989 and 1993. Parasitism by C. albicans and predation by generalist predators were important mortality factors during the outbreak. Predation of moth pupae increased at all sites between 1989 and 1990. Parasitism by C. albicans caused significant mortality each year reaching a maximum in 1991 and remaining high through to 1993 at birch sites. The winter moth populations collapsed simultaneously in 1992 at all study sites, despite different levels of parasitism and 2 very different host plants. As the outbreak collapsed at Richmond, the moth continued to increase in numbers and cause severe defoliation of birch at new sites in southern Vancouver where parasitism remained low. C. albicans is unable to prevent the initial outbreak of winter moth even when the 2 species are introduced simultaneously. The parasitoid requires high density host populations before becoming well established, but may contribute sufficient additional mortality to prevent subsequent prolonged outbreaks. The control of high density winter moth populations in North America by C. albicans supports the hypothesis that natural enemies that are rare in their native habitat will be effective control agents when released into exotic habitats without competitors or their own natural enemies.

Top-down versus bottom-up and the Ruritanian bean bug.

In a recent article, Hunter uses the late George Varley and George Gradwell's long-term data on the winter moth (Operophtera brumata) and green tortrix (Tortrix viridana) populations to propose a method of quantifying the relative importance of top-down effects (because of natural enemies) and bottom-up effects (because of resource competition) in influencing population dynamics. We believe this approach is deeply flawed. Using Varley and Gradwell's winter moth study, we show that the problems with Hunter's analysis lie in his misinterpretation of the population dynamics and his inappropriate use of statistical techniques. We also emphasize the importance of distinguishing clearly between two quite different things: firstly, top-down and bottom-up regulation of populations and secondly, the much simpler task of categorizing factors affecting changes in population density as either top-down or bottom-up processes.

Identifying Density-Dependent Processes: A Comment on the Regulation of Winter Moth

Long-term population studies provide the foundation against which ecological hypotheses on mechanisms of population regulation can be accepted or refuted. One of the classic long-term population studies has focused on the winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae) and its associated natural enemies. Detailed population studies have been carried out in a native area at Wytham Wood, Oxfordshire (Varley & Gradwell 1963, 1968; Varley, Gradwell & Hassell 1973) and in regions where the moth has been introduced into Canada (Embree 1965, 1991; Roland 1986, 1988). Different regulatory mechanisms have emerged from these studies. At Wytham Wood, mortality occurring in the soil, mainly due to pupal predators, acts in a density-dependent manner and seems to be the primary regulatory process (Varley et al. 1973). In Canada, however, pupal predation seemed much less important and an introduced tachinid parasitoid, Cyzenis albicans (Fall.) (Diptera: Tachinidae), was identified as the main density-dependent process (Embree 1966). More recently, Roland (1986, 1988 1990, 1994) has presented yet further interesting interpretations of the winter moth population dynamics based on his studies at Mount Tolmie Park, British Columbia, Canada. In his most recent paper (Roland 1994), data are presented on the relationships between mortality and the estimated density at different stages in the life cycle between 1982 and 1990 (Fig. 1). During this period the winter moth population declined from initial high levels to relatively low levels (for the final 7 years). In order to determine the importance of these mortalities to the winter moth dynamics, Roland selected only the final six 'equilibrium' years of data for his analysis (Fig. 2). On the basis of this, he concluded that egg and larval mortality (k fec and klarv) were not densitydependent and therefore not important in regulating the winter moth population. Pupal predation by ground beetles, however, did appear to be strongly density-dependent and was thus inferred as the primary cause of stability in the British Columbia winter moth population. In this note, we question this conclusion. In particular, we caution against looking for specific densitydependent processes from relatively stationary populations. By considering all the available data (198290), we show that egg and larval mortality (k fec and klarv), in contrast to pupal mortality (kpred), are densitydependent and could have a major impact on the winter moth population regulation.

Response to Bonsall & Hassell `Identifying Density-Dependent Processes: A Comment on the Regulation of Winter Moth'

The re-analysis by Bonsall & Hassell (1995) questions the validity of analysing population data over a limited range of population densities rather than analysing the entire data set. My use of a restricted set of data points for analysis of winter moth populations in British Columbia, Canada (Roland 1994) was not done with respect to density per se, but rather was restricted to a given time interval which happens to

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

Abstract. 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. 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. 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. 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. 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.

After the Decline: What Maintains Low Winter Moth Density after Successful Biological Control?

Life-table data for winter moth are analysed for an 8-year period following introduction of parasitoids for biological control in British Columbia, Canada. Winter moth density declined in 1984, and has remained low since 1985 at an average density of approximately 1.20 adults per m 2 . Introduced parasitoids contributed to mortality during the decline, and have a weak, delayed density-dependent effect at the new low density. Mortality of unparasitized pupae in the soil (primarily by predation) is strongly, and directly density-dependent at the new low density, and is the factor which is most strongly regulatory. Analysis indicates that the strong regulation of winter moth numbers by generalist predators allows parasitism levels to vary greatly after suppression without the eruption of winter moth populations; if parasitism were absent, winter moth populations would erupt to pre-biocontrol levels

Decline in Winter Moth Populations in North America: Direct Versus Indirect Effect of Introduced Parasites

Decline in Winter Moth Populations in North America: Direct Versus Indirect Effect of Introduced Parasites

Density dependence and the stabilization of animal numbers : 3. The winter moth reconsidered.

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.

POPULATION STUDIES ON THE WINTER MOTH OPEROPHTERA BRUMATA (L.) (LEPIDOPTERA: GEOMETRIDAE) IN APPLE ORCHARDS IN NOVA SCOTIA

AbstractThe winter moth Operophtera brumata (L.) is a serious introduced pest of apple trees in Nova Scotia. It spread westward through orchards of the Annapolis Valley in the 1950’s and to other deciduous trees throughout Nova Scotia later. The parasites Cyzenis albicans (Fall.) and Agrypon flaveolatum (Grav.) were liberated during 1961 in Nova Scotia and gradually spread throughout the winter moth population. Population dynamics studies were conducted in insecticide-free orchards and corroborated with observations in neglected unsprayed apple trees over a wide area. The winter moth population reached a balanced level in unsprayed orchards at varying densities below the limits of its food supply, but well above an acceptable level for commercial apple production. In young orchards, where trees cover a small percentage of the ground, natural dispersal of larvae appeared to be a suppressing factor. In mature orchards mortality was density dependent during the prepupal to adult stage; mortality was partly due to parasitism and predation but also to other factors.

Use of a sex attractant and an inhibitor for monitoring winter moth and bruce spanworm populations

A single sex pherormone component was isolated from abdominal tip extracts of female Bruce spanworm.Operophtera bruceata (Hulst). This was identified as (Z,Z,Z)-1,3,6,9-nonadecatetraene by capillary gas chromatography (GC), electroantennography, and mass spectrometry. In addition, hexane extracts of female abdominal tips from Bruce spanworm and the winter moth.O. brumata L., were analyzed by GC coupled to an electroantennographic detector (GC-EAD). The extracts ofO. bruceata andO. brumata females elicited only a single response, at the same retention time, from antennae of their conspecific and reciprocal males. In field tests conducted in Saskatchewan, traps baited with the synthetic tetraene captured Bruce spanworm males. In tests carried out on Vancouver Island, British Columbia, where the two species coexist, both Bruce spanworm and winter moth males were captured. The attractancy of lures containing the synthetic pheromone alone and in combination with several structurally related analogs was field tested at both locations. One of these, an isomer of the natural pheromone, (E,Z,Z)-1,3,6,9-nonadecatetraene, inhibited the capture of Bruce spanworm males but had no effect upon the number of winter moth males which were taken. Thus, populations of these two very similar species can be distinguished by employing traps baited with pheromone ± the inhibitor. Coneorifice Hara traps were found useful for field trapping males of both species.

Foraging pattern of pine siskins and its influence on winter moth survival in an apple orchard.

Foraging by migratory pine siskins in an apple orchard infested with varying densities of winter moth was observed, and winter moth mortality in the presence and absence of birds was recorded. Time spent foraging in a tree and number of birds foraging per tree was positively related to larval density but number of larvae removed per leaf cluster or per unit time was not. Level of defoliation was a better predictor of the number of clusters searched per tree than was prey density. Despite poor predictability in allocation of search effort with respect to prey density, siskins acted as a source of strong compensatory mortality on the winter moth population.

Herbivory in Forested Ecosystems

Forest canopies support a complex assemblage of herbivores that are usually inconspicuous except when population outbreaks of one or more species pro­ duce noticeable defoliation or other signs of herbivore activity. Little is known about the ecological impacts of herbivores during non-outbreak phases (52, 109, 137, 141). Foliage consumption during non-outbreak periods has been measured as 5-15 % of leaf area production in temperate forests (109), but the techniques used may underestimate actual herbivory (88). Foliage loss may reach 100% of foliage production during herbivore population outbreaks (33, 89, 168). In the last five years there has been an explosion of information on both the process of herbivory and the nature of inseCt/plant relationships. Recent com­ pendia include volumes by Ahmad (2), Bell & Carde (10), Crawley (34), Denno & McClure (37), Edwards & Wratten (42), Hedin (65), Rosenthal & Janzen ( 130), and Strong et al (147). Ecological chemistry has been a fun­ damental organizing theme for many of these works. As recently as 1960, Hairston et al (57) based their world hypothesis on the premise that all green foliage was equally available to herbivores. Secondary metabolites were considered to be metabolic by-products with no known function. The emergence of ecological chemistry can be traced from Fraenkel' s (49) concept of plant chemical defense to Feeny's (46) classic study of plant regulation of winter moth (Operophtera brumata L.) populations. More recently, the induc-

Density Dependence and the Stabilization of Animal Numbers 2. the Pine Looper

To test the hypothesis that the density-dependent mortality of advanced larvae of the pine looper kept density within limits (i.e. regulated), the fluctuations of numbers in the field population studied by Klomp are compared with those in the null model in which, on average, this mortality of older larvae is kept at the field level, but the density dependence is removed. It is concluded that the density-dependent mortality of advanced larvae, whether or not in concert with the following density-dependent reduction of fecundity, did not regulate density, but rather had a somewhat destabilizing influence by increasing the chance that very low densities are reached. In an earlier paper the same effect was shown to occur in the winter moth population studied by Varley and Gradwell. It is suggested that this destabilizing tendency may result from the fact that the action of a significantly density-dependent factor can be frustrated by correlations with other, more independent and mutually non-randomly interrelated, mortality factors, by which the potentially stabilizing effect can get lost, and may even turn into the reverse.

The Role of Alternative Host-Plant Species in the Life of a Polyphagous Moth, Operophtera brumata (Lepidoptera: Geometridae)

The Role of Alternative Host-Plant Species in the Life of a Polyphagous Moth, Operophtera brumata (Lepidoptera: Geometridae)

Foraging Strategies, Population Models and Biological Control: A Case Study

SUMMARY (4) A population model based on that of May (1978), but with k from the negative binomial now a function of host density as observed for Cyzenis, is analysed and the stability properties displayed. (5) This general model for parasitism is included in a more detailed model for the winter moth and Cyzenis at Wytham Wood. It shows Cyzenis to play a minor part in the winter moth population dynamics, which is largely governed by the destabilizing effects of the key-factor and the stabilizing effects of the density dependent soil mortality. (6) A model for the winter moth and CyzeMis in Nova Scotia is developed. Cyzenis is assumed to search in the manner found for Wytham Wood, but the other components are derived from the studies of Embree (1965, 1966). The model predicts the successful biological control of the winter moth that has been observed in Nova Scotia following the introduction of Cyzenis. The reasons for the very different performances of Cyzenis at Wytham Wood and Nova Scotia are discussed.

Further Elaboration of the Winter Moth Population Models

where a = area of discovery; kp = k-value for mortality caused by the parasite; and P = parasite density, and the whole model used to test the theoretical implications of variations in area of discovery of the parasite and/or the strength of the density-dependent mortality. Of several limitations in the model the inclusion of k5 the pupal mortality, as a simple linear relationship between the density of healthy fifth instar larvae (in logs) and the mortality of pupae (expressed as a k-value), presented a considerable over simplification of the complex process of predation. The model is unsatisfactory because it neither seeks to describe predator behaviour, nor generates a predator population estimate which can be compared with observed figures. k5 was expressed in the form:

A Study of the Mortality Factors Acting upon Cyzenis albicans (Fall.), a Tachinid Parasite of the Winter Moth (Operophtera brumata (L.))

In an earlier paper (Hassell 1968) the behavioural responses of the adult population of Cyzenis albicans (Fall.) at Wytham Woods, Berkshire towards uneven spatial distributions of hosts were considered. To explain the part played by Cyzenis in the natural control of the winter moth population it is the intergeneration relationships that are most important. Only from these can firm conclusions be drawn about the ability of natural enemies to regulate their hosts or prey. An intergeneration relationship is detected when a plot of the yearly mean percentage host mortality (or k-values) caused by the enemy population against the yearly mean host density (or its logarithm) reveals a linear, curvilinear or some form of spiral relationship. Each of these has, of course, very different implications. A curvilinear or rectilinear relationship indicates a superproportional or subproportional relationship depending on whether the slope is positive or negative. Such relationships imply a relatively constant parasite or predator density. A tendency for 'spiralling' to occur when the points are joined serially implies some form of delayed relationship, resulting from changes in the parasite or predator density, which can be caused only by changes in their reproductive rate and/or survival (Hassell 1966). Cyzenis is a specific parasite of the winter moth with a single annual emergence moreor-less synchronized with the availability of host larvae, and so may be expected to play an important part in the control of the winter moth population at Wytham. However, the intergeneration relationship between Cyzenis and the winter moth (Varley & Gradwell 1968) reveals no sign of delayed density-dependency, and the variation in the winter moth mortality due to Cyzenis is clearly insignificant when compared with the variation in generation mortality of the winter moth. The mean density of adult Cyzenis in the area of oak studied at Wytham since 1950 is 0 96/m2 (having varied between 7-2 and 0 1/Im2). In only three of these years has there been more than 700 parasitism of winter moth larvae. In contrast, in Nova Scotia, Canada, where Cyzenis was first introduced in 1954 (Graham 1958), adult parasite densities rapidly increased and in 1960 were causing a mean of 58% parasitism (Embree 1965, 1966). Clearly some unfavourable factor(s) are operating at Wytham and cause Cyzenis to be less effective than in Canada. This paper is concerned with the mortality factors acting upon the Cyzenis population, and a subsequent paper will deal with the construction of a population model describing the fluctuations in parasite density observed in the field.

The Role of Introduced Parasites in the Control of the Winter Moth in Nova Scotia

AbstractThe history of the winter moth, Operophtera brumata (Linnaeus), a geometrid introduced into Nova Scotia, is reviewed and an assessment is made of two introduced parasites: a tachinid, Cyzenis albicans (Fallen), and an ichneumonid, Agrypon flaveolatum (Gravenhorst). Functional response curves of both species are discussed, particularly the atypical S-shaped curve of C. albicans, which demonstrates regulatory properties. Biological control efforts to date have been successful but a virus that appeared in winter moth populations may change initial relationships between the introduced parasites and the host.