Intra-tree variation in foliage quality drives the adaptive sex-biased foraging behaviors of a specialist herbivore.

Some herbivorous insects enhance their fitness using foraging strategies that allow them to find and colonize the best of available resources within heterogeneous plants. The yellowheaded spruce sawfly, Pikonema alaskensis (Roh.) (Hymenoptera: Tenthredinidae), is a common defoliator that oviposits and feeds on the developing foliage of young open-grown black spruce [Picea mariana (Mills) B.S.P.]. While female and male eggs are both laid throughout the crown, most eggs laid in the upper crown are female, and more female than male late-instar larvae disperse acropetally, from the lower and mid-crown to the upper crown, to complete juvenile development. Here we present results from 4 years of manipulative sleeve-cage experiments that were carried out to evaluate the hypothesis that sex-biased oviposition-site selection and acropetal dispersal by P. alaskensis are adaptive responses to intra-tree variation in foliage quality. Survival and proportion of survivors that were female were either the same (2 years) or significantly higher (2 years) for groups placed in the lower or mid-crown during early instars, and then transferred acropetally during late instars to complete development in the upper crown, compared with those forced to feed exclusively in the lower crown. This suggests that females benefited most from acropetal dispersal. Sex ratios of survivors that had been forced to develop exclusively in the upper crown were usually more female biased than those of survivors that developed exclusively in the lower crown, suggesting higher survival for female than for male larvae emerging from eggs laid in the upper crown. Sex-biased egg allocation and larval dispersal appear to increase the survival of P. alaskensis by accounting for differential effects on male versus female larvae of phenology-independent temporal and spatial variations in the quality of foliage within the heterogeneous crown of black spruce.

Suppression of Ennomos subsignaria (Lepidoptera: Geometridae) on Acer pseudoplatanus (Aceraceae) in an urban forest with bole-implanted acephate.

Trees in an urban forest are highly valued because they have esthetic appeal, provide shade, and improve air quality. During the past 5 yr (2002-2006) in St. John's, Newfoundland and Labrador, Canada, the elm spanworm, Ennomos subsignaria (Hübner) (Lepidoptera: Geometridae), has reached outbreak densities. Each year, hundreds of trees have been completely defoliated, and many more trees have been partially defoliated. Adding to this problem, the larvae, their silk strands, and their frass are a considerable nuisance to property owners in areas of high larval densities. In this study, we evaluated the efficacy of three doses of bole-implanted acephate (AceCap 97) for reducing densities and associated defoliation of E. subsignaria on sycamore maple, Acer pseudoplatanus L. (Aceraceae). During the treatment year (2005), all three doses significantly reduced E. subsignaria larval and pupal density; full or two-thirds doses significantly reduced defoliation compared with control trees. During the posttreatment year (2006), bole-implanted acephate did not affect E. subsignaria egg mass density, survival (= adult emergence), or defoliation. Bole-implanted acephate is an effective and practical way of suppressing E. subsignaria densities and herbivory in an urban forest where the protection of high-value trees and the reduction of environmental contamination are of utmost importance.

Opposing effects of mortality factors on progeny operational sex ratio may thwart adaptive manipulation of primary sex ratio.

Despite extensive research on mechanisms generating biases in sex ratios, the capacity of natural enemies to shift or further skew operational sex ratios following sex allocation and parental care remains largely unstudied in natural populations. Male cocoons of the sawfly Neodiprion abietis (Hymenoptera: Diprionidae) are consistently smaller than those of females, with very little overlap, and thus, we were able to use cocoon size to sex cocoons. We studied three consecutive cohorts of N. abietis in six forest stands to detect cocoon volume-associated biases in the attack of predators, pathogens, and parasitoids and examine how the combined effect of natural enemies shapes the realized operational sex ratio. Neodiprion abietis mortality during the cocoon stage was sex-biased, being 1.6 times greater for males than females. Greater net mortality in males occurred because male-biased mortality caused by a pteromalid parasitic wasp and a baculovirus was greater and more skewed than female-biased mortality caused by ichneumonid parasitic wasps. Variation in the susceptibility of each sex to each family of parasitoids was associated with differences in size and life histories of male and female hosts. A simulation based on the data indicated that shifts in the nature of differential mortality have different effects on the sex ratio and fitness of survivors. Because previous work has indicated that reduced host plant foliage quality induces female-biased mortality in this species, bottom-up and top-down factors acting on populations can affect operational sex ratios in similar or opposite ways. Shifts in ecological conditions therefore have the potential to alter progeny fitness and produce extreme sex ratio skews, even in the absence of unbalanced sex allocation. This would limit the capacity of females to anticipate the operational sex ratio and reliably predict the reproductive success of each gender at sex allocation.

Paradigms in Eastern Spruce Budworm (Lepidoptera: Tortricidae) Population Ecology: A Century of Debate.

Three main hypotheses have been postulated over the past century to explain the outbreaking population dynamics of eastern spruce budworm, Choristoneura fumiferana (Clemens). The Silviculture Hypothesis first arose in the 1920s, with the idea that outbreaks were driven by forestry practices favoring susceptible softwood species. In the 1960s, it was proposed that populations were governed by Multiple Equilibria, with warm weather conditions releasing low-density populations from the regulatory control of natural enemies. Dispersal from outbreak foci, or "epicenters," was seen as causing widespread outbreaks that eventually collapsed following resource depletion. However, in the 1980s, following the re-analysis of data from the 1940s outbreak in New Brunswick, this interpretation was challenged. The alternative Oscillatory Hypothesis proposed that budworm population dynamics were governed by a second-order density-dependent process, with oscillations being driven by natural enemy-victim interactions. Under this hypothesis, weather and resource availability contribute to secondary fluctuations around the main oscillation, and weather and moth dispersal serve to synchronize population cycles regionally. Intensive, independent population studies during the peak and declining phases of the 1980s outbreak supported the principal tenet of the Oscillatory Hypothesis, but concluded that host plant quality played a more important role than this hypothesis proposed. More recent research on the early phase of spruce budworm cycles suggests that mate-finding and natural-enemy-driven Allee effects in low-density populations might be overcome by immigration of moths, which can facilitate the onset of outbreaks. Even more recent research has supported components of all three hypotheses attempting to explain spruce budworm dynamics. In the midst of a new rising outbreak (2006-present), we discuss the evolution of debates surrounding these hypotheses from a historic perspective, examine gaps in current knowledge, and suggest avenues for future research (e.g., intensive studies on low-density populations) to better understand and manage spruce budworm populations.

Interactions between size and temperature influence fecundity and longevity of a tortricid moth, Zeiraphera canadensis.

Females of Zeiraphera canadensis Mut. & Free., the spruce bud moth, were reared in the laboratory at constant and alternating temperatures, and in an outdoor insectary, to (1) determine the effects of temperature, age and size on several reproductive parameters and, (2) to test the hypothesis that body size-temperature interactions influence longevity and realized fecundity. Egg maturation was linearly related to age and large moths developed eggs at a higher rate than small ones. Mcan lifetime oviposition rate reached a maximum and remained stable at temperatures ≥20° C while the mean lifetime rate of egg maturation increased linearly with temperature, indicating that higher temperatures adversely affect oviposition. The production of nonviable eggs increased with age but also with temperature, suggesting high temperature (≥25° C) reduces egg quality and/or hinders fertilization. The realized fecundity and longevity of females reared under an alternating temperature regime (mean 20° C) was significantly less than that of females reared at constant 20° C. Similar realized fecundity, longevity and mean lifetime oviposition rates for females reared at temperatures alternating between 10 and 25° C (mean 20° C) and those at constant 25° C reflected the inability of females to recover from elevated diurnal temperatures. Longevity was positively related to female body size at constant 15 and 20° C but the relationships were negative for moths exposed to diurnal temperatures equal to or exceeding 25° C. Due to the reduced longevity of large moths at high temperatures, linear regressions between size and realized fecundity were only significant at constant temperatures ≤20° C. At higher temperatures, the size-fecundity relationship became curvilinear as a result of the diminished reproductive output of large individuals. Reduced fecundity and longevity of large females at high temperatures may have been due to elevated internal temperatures of large-bodied moths. Large females in a controlled-environment chamber maintained at 25° C developed an internal temperature excess (i.e. temperature above ambient) of nearly 2° C while small-bodied females exceeded ambient by only 0.3° C. However, when held at 20° C, the temperature excess of large-bodied moths was much less than 1° C and small-bodied females did not differ from ambient. Such interactions between temperature and body size suggest that there should be stabilizing selection toward moderate-sized individuals and may explain the absence of size-related effects on fecundity and longevity previously reported for several other lepidopterans.

Evaluating seasonal variation in bottom-up and top-down forces and their impact on an exotic wood borer, Tetropium fuscum (Coleoptera: Cerambycidae).

It is well understood that forces from multiple trophic levels simultaneously influence herbivore performance, but how the relative strength of these forces vary over space and time is less clear. We evaluated seasonal variation in the impact of bottom-up forces (host condition), top-down forces (natural enemies), and competition on the performance of an exotic wood borer. Tetropium fuscum (F.) (Coleoptera: Cerambycidae) eggs that were either protected or exposed were placed on healthy and stressed red spruce, Picea rubens Sargent, trees at three different times during the natural T. fuscum flight period. We also measured the length of necrotic lesions (i.e., an induced hypersensitive response) that developed in response to attacking T. fuscum. As predicted, T. fuscum performance was usually greater, and induced host defenses lower, on stressed than on healthy trees, but the impact of host condition on T. fuscum performance varied seasonally. Timing of attack was critical, influencing the strength of bottom-up forces and consequently all measures of T. fuscum performance. Survival was reduced when T. fuscum attacked too early (late-May) or too late (late-June), which may result in stabilizing selection for attack time in this species. Parasitism and competition were generally negligible during this study. Our results suggest that timing of attack is critical for this wood borer and that temporal variation in the impact of top-down and bottom-up forces should be considered in other systems.

Spread of a Gammabaculovirus within Larval Populations of Its Natural Balsam Fir Sawfly (Neodiprion abietis) Host Following Its Aerial Application.

Field trials and assessments of the balsam fir sawfly (Neodiprion abietis) nucleopolyhedrovirus (NeabNPV: Baculoviridae, Gammabaculovirus) against its natural host were conducted in July and August 2002 near Corner Brook, Newfoundland and Labrador, Canada, in naturally regenerated, precommercially thinned stands dominated by balsam fir (Abies balsamea). Two experimental blocks, each with its own untreated control, were established. The purpose of the Island Pond block was to examine the spread of NeabNPV from a 313-ha aerial treatment block out into adjacent populations of balsam fir sawflies. The purpose of the Old Man's Pond block (2,093 ha) was to determine whether NeabNPV could disperse into populations of balsam fir sawflies within a 200-m zone between spray swaths. NeabNPV was applied to treatment blocks by a Cessna 188B AgTruck aircraft equipped with MicronAir AU4000 rotary atomizers at an application rate equivalent to 1 × 108 NeabNPV occlusion bodies/ha in 2.5 L of 20% aqueous molasses. At Island Pond, NeabNPV infection increased with time following the spray, especially for individuals close to the treatment block, and infection rate decreased to a measured distance of 400 m from the treatment block. At Old Man's Pond, NeabNPV infection rose higher (80% vs. 15%) and sawfly densities declined more (84% vs. 60%) in the area between spray swaths than in the control block.

Transmission of a Gammabaculovirus within Cohorts of Balsam Fir Sawfly (Neodiprion abietis) Larvae.

Nucleopolyhedroviruses (NPV: Gammabaculovirus: Baculoviridae) of diprionid sawflies (Diprionidae: Hymenoptera) are highly host specific and only infect the midgut epithelium. While still alive, infected sawfly larvae excrete NPV-laden diarrhea that contaminates food sources. The diarrhea can then be consumed by conspecific larvae, resulting in rapid horizontal transmission of the virus. To better understand the efficacy of Gammabaculovirus-based biological control products, the horizontal spread of such a virus (NeabNPV) within cohorts of balsam fir sawfly (Neodiprion abietis) larvae was studied by introducing NeabNPV-treated larvae into single-cohort groups at densities similar to those observed during the increasing (field study) and peak (laboratory study) phases of an outbreak. In field studies (~200 N. abietis larvae/m² of balsam fir (Abies balsamea) foliage), NeabNPV-induced mortality increased positively in a density-dependent manner, from 23% (in control groups) to 51% with the addition of one first-instar NeabNPV-treated larva, to 84% with 10 first-instar-treated larvae. Mortality was 60% and 63% when one or 10 NeabNPV-treated third-instar larva(e), respectively, were introduced into groups. Slightly higher levels of NeabNPV-induced mortality occurring when NeabNPV-treated larvae were introduced into first- rather than third-instar cohorts suggests that early instars are more susceptible to the virus. In the laboratory (~1330 N. abietis larvae/ m² of foliage), NeabNPV-caused mortality increased from 20% in control groups to over 80% with the introduction of one, five or 10 NeabNPV-treated larvae into treatment groups of first-instar larvae.

Influence of host tree condition on the performance of Tetropium fuscum (Coleoptera: Cerambycidae).

Tetropium fuscum (F.) attacks weakened Norway spruce, Picea abies (L.) Karst., in its native Europe and may colonize healthy spruce in Nova Scotia, Canada. We used manipulative field experiments to evaluate: 1) the development of T. fuscum on apparently healthy red spruce (Picea rubens Sarg.) in Nova Scotia; 2) the influence of red spruce physiological condition (healthy, girdled or cut) on T. fuscum performance; and 3) the impact of natural enemies and competitors on T. fuscum performance when developing on trees of varying condition. Tetropium fuscum successfully developed on healthy red spruce. Survival was higher on healthy than on girdled or cut trees when larvae were exposed to natural enemies and competitors. The benefits of reduced competition and parasitism on healthy trees appeared to compensate for any reductions in nutritional quality, increase in host resistance, or both. In contrast, when T. fuscum were protected from natural enemies, apparent survival was highest on girdled trees. Tetropium fuscum development took longer on healthy than on cut or girdled trees, and emerged adults were largest on healthy trees. The disparities in adult sizes among the three treatments may mean that healthy trees are more nutritious. Alternatively, the differences may indicate that a greater amount of time was spent feeding in healthy than in girdled or cut trees. Tree condition appears to have a direct impact on the success of T. fuscum, influencing survival, development time, and adult size, and may mediate the impact of natural enemies and competitors, further affecting T. fuscum performance.

A phloem-sap feeder mixes phloem and xylem sap to regulate osmotic potential.

Phloem-sap feeders (Hemiptera) occasionally consume the dilute sap of xylem, a behaviour that has previously been associated with replenishing water balance following dehydration. However, a recent study reported that non-dehydrated aphids ingested xylem sap. Here, we tested the hypothesis that the consumption of xylem sap, which has a low osmolality, is a general response to osmotic stresses other than dehydration. Alate aphids were subjected to different treatments and subsequently transferred onto a plant, where electrical penetration graph (EPG) was used to estimate durations of passive phloem sap consumption and active sucking of xylem sap. The proportion of time aphids fed on xylem sap (i.e., time spent feeding on xylem sap/total time spent feeding on phloem plus xylem sap) was used as a proxy of the solute concentration of the uptake. The proportion of time alate aphids fed on xylem sap increased: (1) with the time spent imbibing an artificial diet containing a solution of sucrose, which is highly concentrated in phloem sap and is mainly responsible for the high osmotic potential of phloem sap; (2) with the osmotic potential of the artificial diet, when osmotic potential excess was not related to sucrose concentration; and (3) when aphids were deprived of primary symbionts, a condition previously shown to lead to a higher haemolymph osmotic potential. All our results converge to support the hypothesis that xylem sap consumption contributes to the regulation of the osmotic potential in phloem-sap feeders.

Role of xylem consumption on osmoregulation in Macrosiphum euphorbiae (Thomas).

Aphids are phloem feeders that occasionally ingest xylem sap. The duration of xylem consumption by Macrosiphum euphorbiae (Hemiptera: Aphididae) was positively correlated with the level of dehydration of alate aphids of different ages after a period of starvation, supporting the hypothesis that aphids ingest xylem sap to replenish their water balance. However, the duration of xylem sap ingestion but not phloem sap consumption varied in unstarved alate adults of different ages. Furthermore, both alate and apterous aphids ingested xylem sap at the end of their life, when aphids were not dehydrated but when fecundity started to decrease. Fecundity was negatively correlated with the proportion of time spent ingesting xylem sap, and that over the entire reproductive life of alate and apterous aphids. The lower proportion of xylem ingested by apterous than by alate aphids during the first few days of adult life may be related to a higher symbiont density in apterous morphs. As previous studies have demonstrated a relationship between sucrose assimilation, which is directly influenced by fecundity and symbiont density, and osmoregulation, we suggest that xylem consumption may play a role in the osmoregulation of haemolymph of aphids.

Ecosystem alteration modifies the relative strengths of bottom-up and top-down forces in a herbivore population.

1. Ecosystem alterations can affect the abundance, distribution and diversity of plants and animals, and thus potentially change the relative strength of bottom-up (the plant resource) and top-down (natural enemies) trophic forces acting on herbivore populations. 2. The hypothesis that alterations of the forest ecosystem associated with precommercial thinning have contributed to the increased severity of outbreaks of Neodiprion abietis (Harris), a sawfly defoliator, through the reduction of trophic forces acting on N. abietis larvae, was tested using exclusion techniques. 3. The relative contributions to N. abietis larval mortality of bottom-up and top-down forces both increased with increasing levels of defoliation and were both reduced by thinning. The reduction of bottom-up and top-down forces caused a 58% mean increase in N. abietis larval survival in thinned compared with untreated stands, which is less than would be expected by the sum of the effects of thinning on each source of mortality. Evidence indicates that the partly compensatory, partly additive nature of the mortality associated with trophic forces in the system under study is responsible for this discrepancy. 4. To our knowledge, this is the first study to show the impact of ecosystem alterations on the balance between bottom-up and top-down forces acting on an eruptive herbivore population along a gradient of host-plant defoliation, and how this can lead to increased outbreak severity. It is stressed that accurate estimates of the relative contributions of bottom-up and top-down forces to mortality cannot be obtained if the additive or compensatory nature of the mortality associated with these trophic forces is overlooked.

Herbivory modifies conifer phenology: induced amelioration by a specialist folivore.

Herbivory by Zeiraphera canadensis Mut. & Free. (Lepidoptera: Tortricidae), an early season folivore of white spruce [ Picea glauca(Moench) Voss], has been associated with a shift in the timing of bud burst by its host during the subsequent year. We tested the hypothesis that a herbivory-induced shift in the phenology of bud development improves the window for colonisation of white spruce buds by Z. canadensis. Feeding on cortical tissue of elongating shoots caused the destruction of apical buds and an interruption of apical dominance in the year following herbivory. White spruce compensated for damage with the activation of dormant buds; mainly at proximal positions along shoots. As a result, half of all active buds on previously damaged branches were located immediately adjacent egg sites (i.e. previous year's bud scales), whereas <10% of active buds on intact shoots were situated there. More than 40% of newly emerged larvae colonised the basal buds of damaged shoots versus just 10% for intact shoots. Previous herbivory also influenced the initiation of bud burst. All buds flushed 2 days earlier on damaged shoots and date of bud burst was inversely correlated to bud density, indicating that short damaged shoots with large numbers of buds were stronger sinks for nutrients required for bud development. Egg hatch was best synchronized with early bursting buds on damaged branches. As a consequence, 89% of first-instar larvae successfully colonised buds on damaged branches while only 55% were successful on undamaged branches. Improved survival of larvae in the year following herbivory was a direct result of the evolved response by white spruce to the interruption of apical dominance. The pattern of herbivory by Z. canadensis may have evolved as a strategy to enhance the quality of white spruce for their offspring.

Advantages of a mixed diet: feeding on several foliar age classes increases the performance of a specialist insect herbivore.

Two field studies were carried out to determine the influence of Abies balsamea foliage age on the preference and performance of larvae of Neodiprion abietis, a specialist Diprionid sawfly. Preference was determined by examining N. abietis defoliation on all age classes of foliage. Performance was estimated using larval survival, cocoon weights and the percentage of adults that were females. Neodiprion abietis preference for, and performance on, current-year foliage was very low, peaked on 2 or 3-year-old foliage, and declined on older foliage. Thus, sawfly feeding preference was adaptive. However, survival and cocoon weight were highest when sawflies were allowed to feed on all age classes of foliage, demonstrating that an insect specialist may perform better when feeding on several age classes of foliage from a single host plant species. These results indicate that either different larval instars have different nutritional requirements, or that food mixing provides the best diet, permitting the herbivore to obtain needed nutrients while avoiding ingestion of toxic doses of secondary metabolites. In addition, our results suggest that limited availability of varied foliage has more negative consequences for N. abietis females than for males, as the percentage of survivors that were females decreased when juvenile mortality was high. Our results emphasize the importance of considering non-linear changes in foliar quality as leaves age on herbivore preference and performance, and demonstrate how a herbivore can use this variability to maximize its fitness.