93. Zappia, SPW; Hoi, AG; Roitberg, BD. (2015) Energy-State Dependent Response of Anopheles gambiae to DEET-Protected, Simulated Blood-Hosts.Journal of Insect Behavior 28: 67-76 Energy-State Dependent Response of Anopheles gambiae to DEET-Protected, Simulated Blood-Hosts
Energy level; malaria; mosquito; repellent
Understanding how mosquito host-seeking behavior changes according to different energy levels in Anopheles gambiae (Diptera: Culicidae) when confronted with a known chemical barrier (N,N-Diethyl-3-methylbenzamide; DEET) is of interest for vector control strategies. We used two identical straight-tube olfactometers to mimic domiciles containing a simulated blood host (human foot odor from a recently-used sock) wrapped in a DEET impregnated net (1 or 0.1 %) and a sugar source (honey) placed some distance away. The energy level of the mosquitoes was manipulated by depriving females of sugar for 6, 24 and 48 h, and we monitored their responses in the olfactometer. Energy level did not have a significant impact on behavior. However, significant differences in residence time at the sock and overall activity level of the mosquito were recorded wherein mosquitoes exposed to DEET responded less readily to the blood-host scent, almost never probing its source. We propose that DEET is perceived by the mosquito as such a strong risk that energy levels do not affect its behavioral outcome. This study, along with previous work showing DEET efficacy, suggests that DEET is an important asset in mosquito control campaigns. DOI
92. Bannerman, JA; Roitberg, BD. (2014) Impact of extreme and fluctuating temperatures on aphid-parasitoid dynamics.Oikos 123: 89-98 Impact of extreme and fluctuating temperatures on aphid-parasitoid dynamics
Climate change is predicted to increase the occurrence of extreme temperature events. We constructed a stage-structured Leslie matrix model with intra-generational dynamics to explore the impact of extreme and fluctuating temperatures on host-parasitoid dynamics. We varied three temperature parameters to generate a range of temperature regimes that varied in their daily maximum temperatures, the number of warmer-than-average days and the autocorrelation of those warmer-than-average days. All three temperature parameters influenced host-parasitoid dynamics. Increasing the frequency of warmer than average days and the degree of autocorrelation only exerted significant impacts on host- parasitoid dynamics when daily maximum temperatures were sufficient to produce temperature-dependent mortality. The effects of increasing autocorrelation of daily temperatures were dependent on the maximum daily temperatures and the frequency of warmer than average days. When daily maximum temperatures were severely warm, but the frequency of those severely warm days was low, increasing autocorrelation increased the probability that the aphids and parasitoids will persist, but when the frequency of severely warm days is increased, increasing autocorrelation decreases the probability that the populations will persist. These temperature phenomena exert significant effects on host-parasitoid dynamics in addition to those effects produced by changes in mean temperatures and warrant further investigation at the community level. DOI
91. Chubaty, AM; Ma, BO; Stein, RW; Gillespie, DR; Henry, LM; Phelan, C; Palsson, E; Simon, FW; Roitberg, BD. (2014) On the evolution of omnivory in a community context.Ecology and Evolution 4: 251-265 On the evolution of omnivory in a community context
Community structure; density-dependent; diet choice; evolutionary game; frequency-dependent; genotype-environment interaction; omnivory; optimal foraging; phenotype
Omnivory is extremely common in animals, yet theory predicts that when given a choice of resources specialization should be favored over being generalist. The evolution of a feeding phenotype involves complex interactions with many factors other than resource choice alone, including environmental heterogeneity, resource quality, availability, and interactions with other organisms. We applied an evolutionary simulation model to examine how ecological conditions shape evolution of feeding phenotypes (e.g., omnivory), by varying the quality and availability (absolute and relative) of plant and animal (prey) resources. Resulting feeding phenotypes were defined by the relative contribution of plants and prey to diets of individuals. We characterized organisms using seven traits that were allowed to evolve freely in different simulated environments, and we asked which traits are important for different feeding phenotypes to evolve among interacting organisms. Carnivores, herbivores, and omnivores all coexisted without any requirement in the model for a synergistic effect of eating plant and animal prey. Omnivores were most prevalent when ratio of plants and animal prey was low, and to a lesser degree, when habitat productivity was high. A key result of the model is that omnivores evolved through many different combinations of trait values and environmental contexts. Specific combinations of traits tended to form emergent trait complexes, and under certain environmental conditions, are expressed as omnivorous feeding phenotypes. The results indicate that relative availabilities of plants and prey (over the quality of resources) determine an individual's feeding class and that feeding phenotypes are often the product of convergent evolution of emergent trait complexes under specific environmental conditions. Foraging outcomes appear to be consequences of degree and type of phenotypic specialization for plant and animal prey, navigation and exploitation of the habitat, reproduction, and interactions with other individuals in a heterogeneous environment. Omnivory should not be treated as a fixed strategy, but instead a pattern of phenotypic expression, emerging from diverse genetic sources and coevolving across a range of ecological contexts. DOI
90.Roitberg, BD; Gillespie, DR. (2014) Natural enemies on the landscape - Integrating life-history theory and landscapes.Biological Control 75: 39-47 Natural enemies on the landscape - Integrating life-history theory and landscapes
Model; State dependent life history; Patch exploitation; Theory; Structure function
The relationship between patch exploitation by individual parasitoids and landscape levels of control by such parasitoids is complex and not well understood. Here we build on a classic concept of the structure function as a way of describing the landscape of a biological control agent from the agent's perspective. We include such structure functions into patch exploitation theory as way of connecting the two aforementioned levels. An important feature is that for any given focal individual, its resource-specific structure functions can differ dramatically in the environment; we explain how one might employ multivariate functions into our theory. Further, rather than employ these functions in a strictly descriptive manner we embed them in state-dependent life history. Parasitoid states include, eggload, energy state, mass and their impacts on the Darwinian fitness from patch exploitation. When taken together, our approach allows us to determine optimal exploitation decisions for agents across various landscapes and more importantly, to predict response of biocontrol agents to changes in landscape as a function of changes in agricultural practices. Finally, we show how these optimal decisions can be used to calculate pest-killing rates for biological control agents, and ultimately to facilitate the selection and management of agents. (C) 2014 Elsevier Inc. All rights reserved. DOI
89. Jannat, KNE; Roitberg, BD. (2013) Effects of larval density and feeding rates on larval life history traits in Anopheles gambiae s.s. (Diptera: Culicidae).Journal of Vector Ecology 38: 120-126 Effects of larval density and feeding rates on larval life history traits in Anopheles gambiae s.s. (Diptera: Culicidae)
AEDES-AEGYPTI; TREEHOLE MOSQUITO; TIME CONSTRAINTS; WESTERN KENYA; SIZE; GROWTH; METAMORPHOSIS; SURVIVAL; COMPETITION; FOOD
Mosquito larval habitat determines the fitness, survivorship, fecundity, and vector capacity of emerging adults. We manipulated larval density and food provisioning in the laboratory to determine their effects on a number of life history parameters of Anopheles gambiae. Larval mortality was positively correlated with larval density. In addition, increased density skewed sex ratios that favored females. DOI
88. Wogin, MJ; Gillespie, DR; Haye, T; Roitberg, BD. (2013) Female-biased sex ratio shifts in a solitary parasitoid and their effects on virginity, population dynamics, and biological control.Entomologia Experimentalis et Applicata 146: 165-176 Female-biased sex ratio shifts in a solitary parasitoid and their effects on virginity, population dynamics, and biological control
Nicholson-Bailey; mating failures; competition; search efficiency; Hymenoptera; Pteromalidae; Trichomalus perfectus; cabbage seedpod weevil; Ceutorhynchus obstrictus; Coleoptera; Curculionidae
Mated female parasitic wasps can control the sex of their offspring by controlling which eggs are exposed to sperm. Females that have failed to mate, however, are restricted to producing only male offspring, as all their eggs are unfertilized. We incorporated the effects of these sometimes constrained, sometimes flexible parasitoid sex ratios into a basic NicholsonBailey population model. We found that the less common case of an increasing female bias in response to competition can destabilize dynamics and have both positive and negative effects on host suppression. We also incorporated the effects of virginity due to a lack of males into the model. Virginity had stabilizing effects on parasitoid-host population dynamics, and prevented runaway female bias in a parasitoid population. We found that the changes in host suppression caused by these new behaviours can be either positive or negative, and are highly dependent on the search efficiency of the parasitoid. DOI
87. Cook, MA; Fitzpatrick, SM; Roitberg, BD. (2012) Phenology of Dasineura oxycoccana (Diptera: Cecidomyiidae) on Cranberry and Blueberry Indicates Potential for Gene Flow.Journal of Economic Entomology 105: 1205-1213 Phenology of Dasineura oxycoccana (Diptera: Cecidomyiidae) on Cranberry and Blueberry Indicates Potential for Gene Flow
phenology; cryptic species; Dasineura oxycoccana; Vaccinium macrocarpon; Vaccinium corymbosum
Dasineura oxycoccana (Johnson) (Diptera: Cecidomyiidae) is a pest of cranberry, Vaccinium macrocarpon (Aiton) (Ericales: Ericaceae), and highbush blueberry, Vaccinium corymbosum (L.) (Ericales: Ericaceae), in North America. In British Columbia, Canada, D. oxycoccana was first found on highbush blueberry in 1991 and then on cranberry seven years later. Because many cranberry and highbush blueberry farms are adjacent to one another, we hypothesized that D. oxycoccana was moving from highbush blueberry onto cranberry. Cranberry and highbush blueberry differ in phenology, and adaptation to these different phenologies may result in host races or cryptic species on these two crops. We recognized the alternative hypothesis that D. oxycoccana had arrived as immature stages with cranberry vines imported from another region of North America. During spring and summer, we recorded the phenology of D. oxycoccana and the development of plant shoots from three cranberry and three highbush blueberry farms to determine whether the opportunity exists for successful movement of D. oxycoccana between the two crops. Our results show that D. oxycoccana from cranberry and highbush blueberry overlap in phenology for much of the season, indicating a high potential for movement and gene flow. However, differences were seen in number of larvae per shoot, location of pupae, and heat unit accumulation during larval development suggesting that instead there may be the potential for host race or cryptic species formation. DOI
86. Gillespie, DR; Nasreen, A; Moffat, CE; Clarke, P; Roitberg, BD. (2012) Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species.Oikos 121: 149-159 Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species
Heat waves extended periods of abnormally hot weather are predicted to increase in severity and frequency under climate change. The severity of heat waves should impact communities and food webs through effects on performance of individual species and through changes in the strength of interactions between them. This study tested the effects of severity of simulated heat waves, with daily maxima of either 32 degrees C or 40 degrees C, on a tritrophic food web consisting of plants, Capsicum anuum, aphids, Myzus persicae and two parasitoids, Aphidius matricariae and Aphelinus abdominalis. Osmolarity of plant sap (concentration of dissolved solids) was highest under 40 degrees C heat waves, suggesting the presence of secondary plant compounds involved with stress responses. Population growth of aphids was lower under heat waves (both 32 degrees C and 40 degrees C daily maxima), compared to environments with periodic hot days. Development time of parasitoids was longer under heat waves. Heat waves decreased the proportion of winged aphids in the population. When both parasitoid species were present, impacts on aphid populations were greater in heat wave environments than environments with periodic hot days. When either parasitoid species was by itself, heat waves did not affect the interaction between parasitoids and aphids. Numbers of A. matricariae were reduced in heat wave environments, whereas numbers of A. abdominalis were not. In addition to direct effects on individual species, we also obtained indirect evidence for the effects of heat waves on the bottomup effects of plant stress compounds on herbivore performance, and on the strength of inter and intra-specific competition. Our results demonstrate that heat waves could have important effects on community structure, and on important, community-level processes such as intra-guild interactions and trophic cascades. DOI
83. Zappia, SPW; Roitberg, BD. (2012) Energy-state dependent responses of Anopheles gambiae (Diptera: Culicidae) to simulated bednet-protected hosts.Journal of Vector Ecology 37: 172-178 Energy-state dependent responses of Anopheles gambiae (Diptera: Culicidae) to simulated bednet-protected hosts
Anopheles gambiae; behavior; energy state; biting rate; foraging theory; olfactometer
In nature, Anopheles gambiae mosquitoes are found at various energy levels and such females must choose between seeking somatic energy from sugar sources and obtaining both somatic and gametic energy from blood hosts. We used a straight-tube olfactometer containing a simulated unobtainable blood host (human foot smell protected by a net) as well as a sugar source (honey odor). We assessed female probing rate and residence time at the net as a function of energy state (0, 24, 48, 72-h starved). In our trials, 0-h starved females showed low response to human odor, low probing rate, and residence time at the human odor site. By contrast, both 48 and 72-h individuals showed high response to foot odor, longer residence time, and higher probing rates. Seventy-two-h females also flew towards the honey source less often than other groups. Our findings suggest that managing sugar sources might be a viable strategy for influencing mosquito biting behavior. DOI
82. Bannerman, JA; Gillespie, DR; Roitberg, BD. (2011) The impacts of extreme and fluctuating temperatures on trait-mediated indirect aphid-parasitoid interactions.Ecological Entomology 36: 490-498 The impacts of extreme and fluctuating temperatures on trait-mediated indirect aphid-parasitoid interactions
Aphidius matricariae; climate change; heat stress; Myzus persicae; non-consumptive effects; trait-mediated indirect effects; trophic interactions
1. Global climate change models predict an increase in the frequency and magnitude of extreme temperature events. These temperature events, heatwaves for example, will impact a wide range of physiological and behavioural processes, particularly in ectotherms, and may therefore influence interactions between species. 2. Anti-predator responses may be more costly under more severe temperature regimes and therefore trait-mediated disturbance could lead to high mortality or reduced reproduction under extreme and fluctuating temperature regimes. 3. We examined the impacts of extreme and fluctuating temperatures on trait-mediated indirect interactions in an aphid-parasitoid community. 4. In treatments that isolated the effects of trait-mediated disturbance from the effects of foraging parasitoids we found that an increase in both the amplitude and frequency of peak temperatures reduced aphid numbers and provided evidence that the cost of trait-mediated disturbance could increase under frequent periods of high temperature. Aphid dispersal also increased with more frequent periods of high temperature. 5. In treatments where female wasps were allowed to freely forage (direct + trait-mediated effects), there was no evidence that extreme and fluctuating temperatures influenced the wasp's foraging ability. Exposure to extreme fluctuating temperatures did not influence the offspring production of exposed wasps or the position of the mummies within the plots. DOI
81. Cook, MA; Ozeroff, SN; Fitzpatrick, SM; Roitberg, BD. (2011) Host-associated differentiation in reproductive behaviour of cecidomyiid midges on cranberry and blueberry.Entomologia Experimentalis et Applicata 141: 8-14 Host-associated differentiation in reproductive behaviour of cecidomyiid midges on cranberry and blueberry
gall midge; host race; assortative mating; host shift; cryptic species; Dasineura oxycoccana; Vaccinium corymbosum; Vaccinium macrocarpon; Diptera; Cecidomyiidae; Ericaceae
In British Columbia, Canada, Dasineura oxycoccana Johnson (Diptera: Cecidomyiidae) was initially found on highbush blueberry, Vaccinium corymbosum L. (Ericaceae) and has recently become a pest of cranberry, Vaccinium macrocarpon Aiton, a crop that is often found in close proximity with blueberry. Previous work has shown no temporal isolation and a potential for gene flow between these two D. oxycoccana populations. However, important behavioural differences were observed suggesting the potential for host races or cryptic species. Host races and cryptic species differ in their degree of assortative mating and reproductive isolation from partial to complete. We assessed whether populations of adult D. oxycoccana on these two crops would discriminate against mates from different natal hosts. Mating experiments were conducted within the greenhouse in 2010 using small glass vials without host plants present. Our results show D. oxycoccana from cranberry and blueberry hosts displayed complete assortative mating in the absence of their host plants. Behavioural data collected from the different crosses suggest these two D. oxycoccana populations differ in sex pheromones and close-range 'courtship pheromones'. We conclude that D. oxycoccana populations on cranberry and blueberry in British Columbia are reproductively isolated and probably represent cryptic species. DOI
80. Jumean, Z; Ma, BO; Chubaty, AM; Ellenor, CW; Roitberg, BD; Gries, G. (2011) A Theoretical Approach to Study the Evolution of Aggregation Behavior by Larval Codling Moth, Cydia pomonella (Lepidoptera: Tortricidae).Journal of Insect Behavior 24: 249-263 A Theoretical Approach to Study the Evolution of Aggregation Behavior by Larval Codling Moth, Cydia pomonella (Lepidoptera: Tortricidae)
Codling moth larva; aggregation; evolution; genetic algorithm
Pupation site-seeking larvae of the codling moth, Cydia pomonella, aggregate in response to aggregation pheromone produced by cocoon-spinning conspecific larvae. Larvae that pupate in an aggregation rather than in solitude may experience a lower rate of parasitism by the parasitoid Mastrus ridibundus. Additionally, adults eclosing from a larval aggregation may encounter mates more rapidly at the site of eclosion (on-site) than away from that site (off-site). We employed an evolutionary simulation to determine the effect of several ecological parameters on the evolution of larval aggregation behavior. These parameters included (i) the probability of mate encounter off-site; (ii) the time available for finding a mate; and (iii) the population density of parasitoids and their rate of larval parasitism. The model predicts that larval aggregation behavior is selected for when the probability of off-site mate encounter is low, the time to locate mates is short, and egg-limited parasitoids are at high population levels. We also show that aggregations reduce the risk of parasitism through dilution effects. The parameters found to favour the evolution of larval aggregation behavior are consistent with life history traits exhibited by C. pomonella. DOI
79. Alma, CR; Gillespie, DR; Roitberg, BD; Goettel, MS. (2010) Threat of Infection and Threat-Avoidance Behavior in the Predator Dicyphus hesperus Feeding on Whitefly Nymphs Infected with an Entomopathogen.Journal of Insect Behavior 23: 90-99 Threat of Infection and Threat-Avoidance Behavior in the Predator Dicyphus hesperus Feeding on Whitefly Nymphs Infected with an Entomopathogen
Feeding behavior; greenhouse whitefly; intraguild interaction; entomopathogen; generalist predator
The nature and severity of intraguild interactions between predators and entomopathogens will be determined, in part, by a combination of threat of infection, and avoidance of that threat by the predator. We determined the threat of infection posed by the entomopathogen, Paecilomyces fumosoroseus (as PFR-97 (TM)) to the generalist predator, Dicyphus hesperus. We then asked if D. hesperus displays behavioral avoidance of infection while foraging for whitefly nymphs at different stages of infection by the pathogen. When exposed to leaf surfaces treated with the pathogen, 28% of adult female predators died due to infection. Consumption of Ephestia kuehniella eggs by surviving predators over 6 d was significantly reduced, suggesting effects of a sublethal infection. Whitefly nymphs that had been treated with P. fumosoroseus 3 d prior were acceptable as prey to D. hesperus but whitefly nymphs that had been treated with P. fumosoroseus 5 days prior were not. When foraging for whitefly nymphs, adult D. hesperus females rejected infected nymphs 96% of the time, compared to 39% of non-infected nymphs. Paecilomyces fumosoroseus therefore presents a measurable threat to D. hesperus through mortality and reduced prey consumption. Dicyphus hesperus does not avoid initial contact with infected prey but does not feed on such prey. The mechanism underlying these rejections could be due to either avoidance of infection or rejection of prey already consumed by the infectious agent. These results suggest that predation by D. hesperus foraging among infected whitefly nymphs under greenhouse or natural conditions could be reduced through a combination of pathogenicity and reduced efficiency of foraging. DOI
78. Henry, LM; Bannerman, JA; Gillespie, DR; Roitberg, BD. (2010) Predator identity and the nature and strength of food web interactions.Journal of Animal Ecology 79: 1164-1171 Predator identity and the nature and strength of food web interactions
adaptive behaviour; Aphelinus abdominalis; Aphidius matricariae; Aulacorthum solani; community dynamics; food web; host-parasitoid interactions; indirect effects
P>1. Most trophic interaction theory assumes that all predators are an abstract form of risk to which prey respond in a quantitatively similar manner. This conceptualization can be problematic because recent empirical work demonstrates that variation in the responses of prey to different predators can play a key role in structuring communities and regulating ecosystem function. 2. Predator identity - the species specific response of prey to a predator - has been proposed as an ultimate mechanism driving the relative contribution of indirect effects in food webs; however few studies have explicitly tested this hypothesis. 3. This study explores the impact of predator identity on direct consumptive (CE) and non-consumptive effects (NCEs), and on the relative contribution of indirect, density and trait-mediated effects in trophic cascades within host-parasitoid communities. 4. We systematically compared the individual, host-parasitoid-plant interactions of two actively foraging parasitoid species with disparate foraging styles, one aggressive and one furtive, a common aphid host and plant. Our results demonstrate that the degree of risk aversion by prey to each particular predator species (i.e. predator identity) is a key factor driving the nature and strength of direct and indirect transmission pathways. 5. Both parasitoid species, in general, had a negative impact on plants. The magnitude of the aphid anti-predator dispersal response was positively correlated with plant infestation and plant damage. The qualitative effect of predator-induced infestation of new plants superseded the quantitative effects of predator-mediated reductions in aphid numbers. 6. The greatest indirect impact on plants was generated by the aggressively foraging parasitoid, and the strength of the aphids anti-predator response (a NCE) antagonistically traded-off with CEs due to an increased investment in attempting to capture risk-sensitized prey. In contrast, the furtive parasitoid did not elicit a strong anti-predator response, had little indirect impact on plants, but generated very high CEs due to the advantage of ovipositing into a sedentary prey population. 7. Our data suggest the responses of prey to different predatory cues may be an important mechanism driving the relative contribution of transmission pathways in trophic cascades. We conclude that predator identity is a key factor influencing the nature and strength of food web interactions. DOI
77. Henry, LM; May, N; Acheampong, S; Gillespie, DR; Roitberg, BD. (2010) Host-adapted parasitoids in biological control: Does source matter?Ecological Applications 20: 242-250 Host-adapted parasitoids in biological control: Does source matter?
Acyrthosiphon pisum; adaptive evolution; Aphidius ervi; Aulacorthum solani; biological control; foxglove aphid; heritability; parasitoid; pea aphid; reciprocal transplant; selection experiment
It has been hypothesized that the success of a biological control introduction is, in part, dependent oil the ability of the control agent to become established in its new environment or to its new population of hosts through local adaptation. Despite this, few studies have investigated the influence of the recent coevolutionary history of pest species and natural enemies oil the efficacy of biological control agents, especially for agents that arc mass-reared for release in agriculture. We investigate the evolutionary potential of a biological control agent Aphidius ervi to adapt to a key pest species, the foxglove aphid Aulacorthum solani, through components essential to the evolution of parasitoid Virulence. We explored (1) the influence of genetic variation front natural Source populations Oil the ability to parasitize natal and non-natal host species, (2) the heritability of key traits related to parasitoid fitness; and (3) the efficacy of parasitoid host-selection lilies in a greenhouse system. Source Populations maintained genetic variation in the ability to utilize natal and non-natal host species; however. Only some of the traits sampled suggested local adaptation of parasitoid Populations. The ability to parasitize a host was found to be genetically determined and strongly heritable, irrespective of host species. The greenhouse study demonstrated the potential of parasitoid selection lilies to substantially increase performance of parasitoids for target pest species. This research provides insight into novel techniques that can be used to increase the quality of biological control agents through the development of lilies of natural enemies adapted to particular pest species.
76. Peterson, JH; Roitberg, BD. (2010) Egg maturation, nest state, and sex ratios: a dynamic state variable model.Evolutionary Ecology Research 12: 347-361 Egg maturation, nest state, and sex ratios: a dynamic state variable model
dynamic state variable model; Hymenoptera; nest provisioning decisions; offspring sex ratio; optimizing multiple resources
Background: Parents can invest in offspring through a variety of behaviours. Optimization models of these behaviours are usually based on determination of the single 'factor' parents optimize for a given set of conditions. Interactions between factors are rarely considered. Question: Do mothers optimize a single factor related to the investment in offspring (e.g. current nest state or mature egg state), or do mothers find an optimal balance between these two in relation to maximizing lifetime reproduction? Methods and key assumptions: A dynamic state variable model. We develop a 'hybrid' model that examines mothers' allocation decisions to offspring by considering mature egg and nest state as well as other environmental/ecological factors. We assume that mothers alter reproductive decisions based on their perception of costs and benefits of brood cell and nest construction. Some of these construction behaviours determine investment in one or a few offspring within a brood but others affect the entire brood. Egg maturation rate is a constant. Conclusions: Our results demonstrate that there is no single limiting factor; instead, there is some 'optimal balance' between mature egg and nest state that determines the optimal reproductive decision.
75.Roitberg, BD; Keiser, S; Hoffmeister, T. (2010) State-dependent attacks in a mosquito.Physiological Entomology 35: 46-51 State-dependent attacks in a mosquito
Anopheles gambiae; body size; dynamic; energy state; foraging theory; persistence; residence time
Mosquito biting frequency and meal size are considered to be important parameters in the epidemiology of insect-vectored diseases such as malaria. Because both parameters are likely to depend on the size and energetic state of adult mosquitoes, the present study investigates the effects of body size and energy state on attack behaviours in the malaria mosquito, Anopheles gambiae. Attack rates are measured as well as total time spent before giving up for individual females when provided with an unobtainable human hand (i.e. mosquitoes are dislodged every time that they land). The factorial design considers two body sizes, small and large, as well as three sugar deprivation states, 0, 1 and 2 days. The results reveal a positive effect of size on attack rate and a nonlinear effect of energy state, where mosquitoes of intermediate energy state show lower attack rates than either 2-day food-deprived or nondeprived mosquitoes. Moreover, attack rate is negatively associated with persistence time in nondeprived and 2-day food-deprived Anopheles but is unrelated to persistence time in 1-day food-deprived mosquitoes, Interestingly, although persistence times are generally inversely related to attack rates, they are not significantly influenced by either energetic or size states. DOI
74.Roitberg, BD; Mangel, M. (2010) Mosquito Biting and Movement Rates as an Emergent Community Property and The Implications for Malarial Interventions.Israel Journal of Ecology & Evolution 56: 297-312 Mosquito Biting and Movement Rates as an Emergent Community Property and The Implications for Malarial Interventions
Mosquito; malaria; Anopheles; bednet; dynamic state variable; biting rate; Monte Carlo
Malaria, a mosquito-vectored disease, continues to be one of the most important scourges afflicting humankind. In this paper, we take a mosquito-centric approach by studying mosquito states (i.e., energy, neurological health, and toxin information state) to demonstrate how key parameters of malaria, biting and movement rates and mosquito survival, are all emergent properties of those states when considered in the context of the background community interactions. We do so as follows: First, we develop a dynamic state variable model of mosquito biting and movement decisions that maximize mosquito expected reproductive success (fitness), and then we embed those optimal policies in a Monte Carlo simulation wherein mosquitoes attempt to feed on human hosts at domiciles where insecticide-treated bednets (ITNs) and insecticidal residual wall sprays (IRSs) are used. We find that biting rates, at the domicile level, are not impacted by mosquito state but that emigration rates from domiciles are determined by an interaction between mosquito energy state, information state, and risk of predation. This means that malaria incidence, at the village level at least, may be best understood as a response of mosquitoes to their ecological community that includes nectar-bearing plants, predators, the spatial arrangement of homes, and the protection of humans in those homes. DOI
73.Roitberg, BD; Zimmermann, K; Hoffmeister, TS. (2010) Dynamic response to danger in a parasitoid wasp.Behavioral Ecology and Sociobiology 64: 627-637 Dynamic response to danger in a parasitoid wasp
Patch leaving; State-dependent model; Fear; Bayesian updating
Despite the multitude of work on patch time allocation and the huge number of studies on patch choice in the face of danger, the patch leaving response of foragers perceiving cues of danger has received relatively little attention. We investigated the response of parasitoid insects to cues of danger both theoretically and experimentally. Using stochastic dynamic theory, we demonstrate that patch-leaving responses in response to the detection of danger should be seen as a dynamic decision that depends upon reproductive options on the current host patch and on alternative patches that might be found after leaving the current patch. Our theory predicts a sigmoidal response curve of parasitoids, where they should accept the danger and stay on the patch when patch quality is high and should increasingly avoid the risk and emigrate from the patch with decreasing patch quality and decreasing costs of traveling to an alternative host patch. Experiments with females of the drosophilid parasitoid Asobara tabida that were exposed to a puff of formic acid (a danger cue) at different times through their patch exploitation confirmed the theoretical predictions (i.e., a sigmoid response curve); however, the predicted curve was significantly steeper than observed. We discuss the impact of dynamic patch-exit decisions of individual foragers on population and community dynamics. DOI
72. van Herk, WG; Vernon, RS; Harding, C; Roitberg, BD; Gries, G. (2010) Possible aversion learning in the Pacific Coast wireworm.Physiological Entomology 35: 19-28 Possible aversion learning in the Pacific Coast wireworm
aversion learning; behaviour; insecticide; Limonius canus; repellency; wireworm
The effects of carbon dioxide and the induction of morbidity on aversion learning in larvae of the Pacific Coast wireworm Limonius canus LeConte (Coleoptera: Elateridae) are discussed. Wireworms preconditioned by exposing them one or four times to odour of Tefluthrin 20SC and Dividend XLRTA [Syngenta Crop Protection (Canada), Inc., Canada] during the induction of temporary morbidity subsequently contact tefluthrin-treated wheat seeds in soil bioassays for as long as naive (i.e. not preconditioned) larvae but are repelled four to five-fold more frequently by Dividend-treated seeds in soil bioassays than naive wireworms, suggesting that wireworms are capable of associating a novel odour (i.e. Dividend) with morbidity but require a minimum of 10-15 min subsequent contact time with treated seeds before being repelled. Wireworms preconditioned by exposure to peppermint odour during the induction of morbidity are not subsequently repelled by peppermint odour in soil bioassays, suggesting that wireworms are either not capable of aversion learning or that the presence of a CO2 source and/or a suitable host plant may override a negative cue (i.e. peppermint odour). In studies conducted in the absence of soil, a host plant and CO2 production, wireworms are repelled slightly by droplets of 1.0% but not 0.1% peppermint oil. Previous exposure to peppermint odour or contact with peppermint oil-treated filter paper during one induction of morbidity does not increase the repellency of wireworms to 1.0% peppermint oil significantly. Repellency to 1.0% peppermint oil is almost eliminated when morbidity is induced five times in the absence of peppermint odour but is restored when peppermint odour is present during preconditioning. These findings suggest that wireworm sensitivity to repellent compounds decreases when repeatedly made moribund, although the results are not sufficient to conclude that wireworms are capable of associative learning. DOI
71. Chubaty, AM; Roitberg, BD; Li, C. (2009) A dynamic host selection model for mountain pine beetle, Dendroctonus ponderosae Hopkins.Ecological Modelling 220: 1241-1250 A dynamic host selection model for mountain pine beetle, Dendroctonus ponderosae Hopkins
IDEAL FREE DISTRIBUTION; MARGINAL VALUE THEOREM; DOUGLAS-FIR BEETLE; HABITAT SELECTION; LODGEPOLE PINE; BARK BEETLES; COLONIZATION BEHAVIOR; POPULATION-DYNAMICS; TIME ALLOCATION; ECOLOGY
The link between individual habitat selection decisions (i.e., mechanism) and the resulting population distributions of dispersing organisms (i.e., outcome) has been little-studied in behavioural ecology. Here we consider density-dependent habitat (i.e., host) selection for an energy- and time-limited forager: the mountain pine beetle (Dendroctonus ponderosae Hopkins). We present a dynamic state variable model of individual beetle host selection behaviour, based on an individual's energy state. Field data are incorporated into model parameterization which allows us to determine the effects of host availability (with respect to host size, quality, and vigour) on individuals' decisions. Beetles choose larger trees with thicker phloem across a larger proportion of the state-space than smaller trees with thinner phloem, but accept lower quality trees more readily at low energy- and time-states. In addition, beetles make habitat selection decisions based on host availability, conspecific attack densities, and beetle distributions within a forest stand. This model provides a framework for the development of a spatial game model to examine the implications of these results for attack dynamics of beetle populations. (C) 2009 Elsevier B.V. All rights reserved. DOI
70. Henry, LM; Ma, BO; Roitberg, BD. (2009) Size-mediated adaptive foraging: a host-selection strategy for insect parasitoids.Oecologia 161: 433-445 Size-mediated adaptive foraging: a host-selection strategy for insect parasitoids
MONOCTONUS-PAULENSIS HYMENOPTERA; APHIDIUS-ERVI HYMENOPTERA; BODY-SIZE; INDIVIDUAL BEHAVIOR; SEX ALLOCATION; HABITAT USE; PREY SIZE; POPULATION-DYNAMICS; INSTAR SELECTION; DIET CHOICE
Foraging models are useful tools for generating predictions on predator-prey interactions, such as habitat or diet choice. However, the majority of studies attempting to explain adaptive behaviour using optimality criteria have assumed that there is no trait (e.g. size) variation among individual consumers or their prey. Hymenopteran parasitoids that attack the free-living stages of their host are an ideal system for studying the influence of body size on host selection because of the wide range of adult parasitoid sizes coupled with the defensive capabilities of their hosts. We report here our application of an experimentally parameterized host selection model to investigate the influence of parasitoid body size on the range of acceptable host instar classes. Using a demographic model, we compared the efficiency of parasitoids using an optimal host selection strategy against parasitoids using an indiscriminate host selection strategy over a range of different parasitoid body sizes. Net fitness accrual of parasitoids and the impact of host instar selection on aphid recruitment were assessed on different stage-structured aphid populations. Our results demonstrate that optimal host selection allows larger parasitoids to utilize a wider range of hosts. However, smaller parasitoids receive the greatest benefits from selecting hosts optimally by utilizing a restricted range of small, poorly defended hosts when they are abundant. We argue that the correlation between flexible host selection behaviour and adult body size may be a general phenomenon that applies to the majority of hymenopteran parasitoids that attack free-living, well-defended hosts. The potential of within-generation behavioural interactions to impact between-generation dynamics in host-parasitoid populations are discussed. DOI
69. Jenner, WH; Roitberg, BD. (2009) Foraging Behaviour and Patch Exploitation by Campoplex dubitator (Hymenoptera: Ichneumonidae), a Parasitoid of Bark-mining Larvae.Journal of Insect Behavior 22: 257-272 Foraging Behaviour and Patch Exploitation by Campoplex dubitator (Hymenoptera: Ichneumonidae), a Parasitoid of Bark-mining Larvae
IMPERFECT HOST DISCRIMINATION; INSECT PARASITOIDS; TIME ALLOCATION; BIOLOGICAL-CONTROL; SIZE; SUPERPARASITISM; MECHANISMS; STRATEGY; ECOLOGY; TORTRIX
This study examines the foraging behaviour of Campoplex dubitator Horstmann (Hymenoptera: Ichneumonidae), a parasitoid of the highly concealed bark-mining host, Enarmonia formosana Scopoli (Lepidoptera: Tortricidae), and how this foraging behaviour is affected by host density. The ultimate aim was to determine whether foraging behaviour and patch fidelity could explain patterns of parasitism in the field. An ethogram was first constructed to portray C. dubitator behaviour prior to and immediately following host attacks. The pre-attack behavioural sequence was highly structured whereas behavioural transitions became less predictable after a sting event. Females spent more time on patches with higher host densities and host encounters caused a significant reduction in the leaving tendency. The giving up time was only slightly affected by host encounters. Campoplex dubitator did not demonstrate the ability to distinguish between occupied and empty host mines. The results show that C. dubitator forages more efficiently at lower host densities and this behavioural phenomenon may result in the patterns of parasitism observed in the field. DOI
68. Senger, SE; Tyson, R; Roitberg, BD; Thistlewood, HMA; Harestad, AS; Chandler, MT. (2009) Influence of Habitat Structure and Resource Availability on the Movements of Rhagoletis indifferens (Diptera: Tephritidae).Environmental Entomology 38: 823-835 Influence of Habitat Structure and Resource Availability on the Movements of Rhagoletis indifferens (Diptera: Tephritidae)
APPLE MAGGOT DIPTERA; FRUIT-FLY; LANDSCAPE CONNECTIVITY; BACTROCERA-CUCURBITAE; OLFACTORY STIMULI; FLIES DIPTERA; POMONELLA; RESPONSES; ECOLOGY; DISTANCE
Habitat structure and resources availability may differentially influence movement between habitat patches. We examined fly movement decisions (stay or leave) at the scale of individual trees by measuring the response of marked Rhagoletis indifferens (Diptera: Tephritidae) to sweet cherry trees (Prunus avium) that were manipulated by changing the shape of the tree (structure treatment = normal or reduced) and the fruit load (fruit treatment = augmented, normal, or reduced). More than 600 observations were made at two field sites that differed in the average inter-tree distance: Senger site, 10.1 +/- 4.5 m; Tuemp site, 29.0 +/- 19.3 m. At the Senger site, flies were resighted most often in the normal structure-augmented fruit trees. At the Tuemp site, however, there were fewer transfers between trees, unusual tree preferences, and significant treatment interaction terms. Using a first principles diffusion model of attraction and by varying fly perceptual range to limit tree choice, we generated unusual tree preferences based on differential attraction to individual trees. Our results suggest that manipulating tree attractiveness may be a viable pest management strategy for closely spaced trees but not for dispersed trees. Further study into the relationship between the spatial arrangement of trees and the flies' ability to detect specific tree characteristics is warranted.
67. Stone, CM; Taylor, RM; Roitberg, BD; Foster, WA. (2009) Sugar Deprivation Reduces Insemination of Anopheles gambiae (Diptera: Culicidae), Despite Daily Recruitment of Adults, and Predicts Decline in Model Populations.Journal of Medical Entomology 46: 1327-1337 Sugar Deprivation Reduces Insemination of Anopheles gambiae (Diptera: Culicidae), Despite Daily Recruitment of Adults, and Predicts Decline in Model Populations
WESTERN KENYA; FEEDING-BEHAVIOR; MALARIA VECTORS; BODY-SIZE; SURVIVAL; MOSQUITOS; FEMALE; BLOOD; DISPERSAL; FUNESTUS
Our research tests the hypothesis that the inability to sugar-feed reduces the insemination rate in mosquito populations. To test this, we measured the effects of sugar availability oil cumulative insemination performance of male Anopheles gambiae Giles s.s. (Diptera:Culicidae) during 10-d periods of continual emergence of equal numbers of both sexes, and we evaluated the implications at the population level with a matrix population model. Oil each day of each of four replicates, 20 newly emerged mosquitoes of each sex were recruited into the populations within two mesocosms, large walk-in enclosures with simulated natural conditions. Each mesocosm contained a cage to replicate the experiment oil a small scale. Scented sucrose was absent or present (control). A human host was available nightly as a bloodmeal source in both mesocosms. Sugar availability and enclosure size significantly influenced female insemination. In the mesocosms, with sugar 49.7% of the females were inseminated, compared with 10.9% of the females without sugar. In the small cages, the insemination rates were 76.0 and 23.5%, respectively. In the mesocosms, cumulative survival of females after 10 d was 51.6% with sugar and 25.6% without sugar. In the cages, female survival was 95 and 73%, respectively. Sensitivity analysis of the population projection matrix shows that both reduced male survival and reduced mating capability due to a lack of sugar contributed to lower insemination rates in females, and in the absence of sugar the insemination rate was lowered to all extent that led to population decline.
66. Henry, LM; Roitberg, BD; Gillespie, DR. (2008) Host-range evolution in Aphidius parasitoids: Fidelity, virulence and fitness trade-offs on an ancestral host.Evolution 62: 689-699 Host-range evolution in Aphidius parasitoids: Fidelity, virulence and fitness trade-offs on an ancestral host
Acyrthosiphon pisum; Aphidius ervi; Aulacorthum solani; fitness trade-offs; host adaptation; local adaptive peak; population differentiation
The diversity of parasitic insects remains one of the most conspicuous patterns on the planet. The principal factor thought to contribute to differentiation of populations and ultimately speciation is the intimate relationship parasites share with hosts and the potential for disruptive selection associated with using different host species. Traits that generate this diversity have been an intensely debated topic of central importance to the evolution of specialization and maintenance of ecological diversity. A fundamental hypothesis surrounding the evolution of specialization is that no single genotype is uniformly superior in all environments. This "trade-off" hypothesis suggests that negative fitness correlations can lead to specialization on different hosts as alternative stable strategies. In this study we demonstrate a trade-off in the ability of the parasitoid, Aphidius ervi, to maintain a high level of fitness on an ancestral and novel host, which suggests a genetic basis for host utilization that may limit host-range expansion in parasitoids. Furthermore, behavioral evidence suggests mechanisms that could promote specialization through induced host fidelity. Results are discussed in the context of host-affiliated ecological selection as a potential source driving diversification in parasitoid communities and the influence of host species heterogeneity on population differentiation and local adaptation. DOI
65. Leighton, BJ; Roitberg, BD; Belton, P; Lowenberger, CA. (2008) Host antibodies in mosquito bloodmeals: A potential tool to detect and monitor infectious diseases in wildlife.Journal of Medical Entomology 45: 470-475 Host antibodies in mosquito bloodmeals: A potential tool to detect and monitor infectious diseases in wildlife
mosquito; enzyme-linked immunosorbent assay; bloodmeal; antibody; wildlife disease
When a female mosquito bites, it carries away a blood sample containing specific antibodies that can provide a history of the immune responses of its vertebrate host. This research examines the limits and reliability of a technique to detect antibodies in blood-fed mosquitoes in the laboratory. Mosquitoes were fed on blood containing a specific antibody, and then they were assayed using an enzyme-linked immunosorbent assay to determine the limits of detection of antibody over time, at different temperatures and initial antibody concentrations. The antibody, at an initial concentration of 1 mu g/ml, could be detected in mosquitoes for 24-48 h after feeding. Blind tests simulating the assay of feral mosquitoes were used to test the reliability of the method and detected positive mosquitoes with few false negatives and no false positives. Specific antibodies also could be detected in mosquitoes that had been air-dried or preserved in ethanol. This research indicates that, in theory, the collection and immunological assay of blood-fed mosquitoes could be developed to detect and monitor infectious disease in wildlife.
64. Ma, BO; Roitberg, BD. (2008) The role of resource availability and state-dependence in the foraging strategy of blood-feeding mosquitoes.Evolutionary Ecology Research 10: 1111-1130 The role of resource availability and state-dependence in the foraging strategy of blood-feeding mosquitoes
Aedes aegypti; Anopheles gambiae; dynamic state variable model; foraging behaviour; mosquitoes; omnivores; resource availability; state-dependence; vector-borne disease control
Background: Blood-feeding female mosquitoes are omnivores that face trade-offs and constraints between taking blood meals, sugar meals, and ovipositing their eggs. Questions: (1) How does a mosquito allocate her time and energy to blood and sugar feeding? (2) How does the availability of sugar and/or blood influence her decisions? Methods and key assumptions: We use a dynamic state variable model to address this question. The model is parameterized from primary literature using Anopheles gambiae for reference where possible. The model assumes that female mosquitoes have evolved to make decisions that maximize their lifetime reproductive success. Conclusions: Blood and sugar have important roles in the life history of blood-feeding female mosquitoes. In the presence of blood hosts, the decision to search for a blood meal is almost always chosen over the search for sugar. However, away from the blood host microhabitat, sugar is readily used. Survivorship and fecundity are increased with an increase in sugar availability. Frequency of blood feeding, mosquito fecundity, and survivorship are only marginally decreased with decreases in blood availability.
63.Roitberg, B and Roitberg, G. (2008) Foraging.The Encyclopedia of Life. Article A3228 (Wiley Press) Foraging
DOI
62. Senger, SE; Roitberg, BD; Thistlewood, HMA. (2008) Ovarian response to resource availability in female Rhagoletis indifferens.Entomologia Experimentalis et Applicata 129: 26-31 Ovarian response to resource availability in female Rhagoletis indifferens
fitness trade-offs; dispersal; egg load; crowding; factorial design; Diptera; Tephritidae; Rosaceae
Fitness trade-offs in behavioural ecology theory suggest that the costs associated with dispersal can impact reproductive output, but evidence of dispersal-reproduction trade-offs is often lacking. We present evidence of Rhagoletis indifferens Curran (Diptera: Tephritidae) developing its egg load in response to host availability [Prunus avium L. (Rosaceae)] and link this to our previous work on flight behaviour through the common methodology of these two studies. We replicated the study design from the flight mill experiment, such that females were maintained in one of six possible treatments combining two factors: social interactions (crowded vs. isolated) and resources (food = food only; leaf = food + leaf; and cherry = food + leaf + fruit), and then dissected the females to determine egg load. Egg counts varied significantly with 'crowded' females and those in the 'cherry' resource treatments producing the most mature eggs. Although the average mature egg count for females from the 'leaf' and 'food' resource treatments was similar, these two groups differed in the proportion of females that produced no mature eggs at all. No significant interaction terms between the factors tested were generated. We conclude that the effect of social interactions and resources on the maturation of eggs is additive in R. indifferens. These results support those of an earlier flight mill experiment and provide evidence that egg load may trade off with dispersal ability in R. indifferens. DOI
60. Alma, CR; Goettel, MS; Roitberg, BD; Gillespie, DR. (2007) Combined effects of the entomopathogenic fungus, Paecilomyces fumosoroseus Apopka-97, and the generalist predator, Dicyphus hesperus, on whitefly populations.Biocontrol 52: 669-681 Combined effects of the entomopathogenic fungus, Paecilomyces fumosoroseus Apopka-97, and the generalist predator, Dicyphus hesperus, on whitefly populations
biological control; interaction; interference competition; Trialeurodes vaporariorum
The effects of intraguild interactions between Dicyphus hesperus Knight (Hemiptera: Miridae) and Paecilomyces fumosoroseus Apopka-97 (PFR-97 (TM)) (Wize) Brown and Smith (Ascomycota: Hypocreales) on Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) populations were investigated in tomato greenhouse microcosms. Conditions were established in which interference or synergy would most likely occur; namely, a high number of available whiteflies were combined with large numbers of both D. hesperus and PFR-97 (TM). We measured live whitefly density in a factorial repeated measures experiment where plants were provided or withheld releases of D. hesperus and/or applications of PFR-97 (TM) for 6 weeks. Releases of D. hesperus were made at a rate of 10 adults/plant during the first and third week and PFR-97 (TM) suspensions were applied with a backpack sprayer at a rate of 18 x 10(7), 1.3 x 10(7) and 1.2 x 10(7) viable blastospores/ml during the first, third and fourth week, respectively. Results revealed a non-significant interaction effect between D. hesperus and PFR-97 (TM), indicating that their actions were independent. Individual whitefly reductions of 48% and 35% were achieved by PFR-97 (TM) and D. hesperus, respectively. Collectively, the natural enemies reduced whitefly densities by 62% relative to the controls. The density of D. hesperus adults was unaffected by multiple applications of PFR-97 (TM). These results suggest that the combination of generalist entomopathogenic fungi and generalist predators has the potential to cause increased pest mortality despite evidence of minimal interference. DOI
57. Peterson, JH; Roitberg, BD; Ydenberg, RC. (2007) When nesting involves two sequential, mutually exclusive activities: what's a mother to do?Evolutionary Ecology Research 9: 1187-1197 When nesting involves two sequential, mutually exclusive activities: what's a mother to do?
dynamic state variable model; Hymenoptera; nest provisioning decisions; offspring sex ratio; resource allocation; solitary bee
Background: Parents can invest in offspring through a variety of behaviours, some of which trade off against each other, such as investment in the current brood versus investment in a future one. Question: When should hymenopteran parents stop provisioning the current nest and decide whether to seal the entrance to the nest (e.g. with a number of leaf pieces)? Method and key assumptions: A dynamic state variable model. We assume that mothers alter reproductive decisions based on their perception of costs and benefits of brood cell and nest construction. Some of these construction behaviours allocate investment at one or a few offspring in a brood but others affect the entire brood. Conclusions: Several factors impact the decisions of when to cease provisioning new offspring and whether to seal the nest. Higher current nest value and greater risk of mortality increase the likelihood of both ceasing provisioning earlier and sealing the nest. The greater the benefit of sealing, either because of increased benefits or decreased negative impacts, the earlier and the more frequently it occurs.
55.Roitberg, B. (2007) Why pest management needs behavioral ecology and vice versa (INVITED REVIEW).Entomological Research 37 (2007) 14–18 Why pest management needs behavioral ecology and vice versa (INVITED REVIEW)
Behavior manipulation is becoming an accepted tactic in pest management, however, there are many ways in which the approach can be improved. In this review, I explain how and why insect behavioral response to various stimuli can vary dramatically under different conditions and that it is this variable response that must be understood before behavior manipulation becomes widely accepted in pest management programs. I propose that entomologists use concepts from behavioral ecology to manipulate pest behavior in a predictable manner. The key is to study behaviors that maximize fitness in natural environments and then exploit these behaviors in agriculture. I provide examples from a range of behavior manipulation tactics, including use of attracticides, kairomone-mediated biological control, use of marking pheromones, and push-pull manipulation. DOI
54.Roitberg, B. and Bernard, P. (2007) State dependent problems for parasitoids.In: Behavioral Ecology of Parasitoids. (E. Wijnberg, J. Van Alphen, Eds.) Cabi Press.State dependent problems for parasitoids.
52. Senger, SE; Roitberg, BD; Thistlewood, HMA. (2007) Relative flight responses of Rhagoletis indifferens as influenced by crowding, sex, and resources.Entomologia Experimentalis et Applicata 123: 91-100 Relative flight responses of Rhagoletis indifferens as influenced by crowding, sex, and resources
Western cherry fruit fly; dispersal; flight mill; foraging; distance; velocity; behaviour; Diptera; Tephritidae
Although flight is believed to be the primary mechanism for dispersal in the Western cherry fruit fly, Rhagoletis indifferens Curran (Diptera: Tephritidae), an orchard pest of both sweet (Prunus avium L.) and sour (Prunus cerasus L.) (Rosaceae) cherry crops, the movement of these flies between host patches is difficult to quantify in the field. A tethered flight mill system was used in the laboratory to examine the flight behaviour of sexually mature flies exposed to different levels of conspecific contact and resource availability. A complete 2 x 2 x 3 factorial design compared the relative influence of the factors 'context' (crowded, isolated), 'sex' (female, male), and 'resources' (low = food only; medium = food + leaf; high = food + leaf + cherries) on flight performance measures including distance flown, net trial time, and stopping patterns. Rather than using a minimum time or distance to determine trial length, flight observations were continued for each fly until a behavioural protocol based on stopping time was met. In this protocol each successful trial was composed of three consecutive flight intervals and included a minimum of three stops lasting a combined total of 5 min. Of the 160 flies tested, 86.9% flew < 500 m on the flight mill. Individuals from both sexes were capable of maximum flights in the same order of magnitude, ca. 3 km on the flight mill. Distance flown was significantly influenced by 'context' such that crowded individuals flew > 1.5-fold farther than isolated individuals. Sex influenced the frequency and duration of stops made, with females stopping more often and longer than males. Although females and males in high resource treatments had the shortest net trial times, the factor 'resources' did not produce any highly significant main effects, but did generate significant interaction terms with the factors 'context' and 'sex', suggesting that past experience with 'resources' modifies individual flight behaviour. We have shown for the first time using a tethered flight mill system that R. indifferens flight behaviour is context dependent and sensitive to adult crowding. The implications of this study for improved field experiments on dispersal are discussed. DOI
51. Henderson, AE; Roitberg, BD. (2006) Microhabitat location of Exophthalmus jekelianus (White) (Coleoptera : Curculionidae): Is there a preference for shade-grown coffee?Environ Entomol 35: 1603-1609 Microhabitat location of Exophthalmus jekelianus (White) (Coleoptera : Curculionidae): Is there a preference for shade-grown coffee?
shade preference; microhabitat; coffee agroecosystem; Exophthalmus jekelianus
The Costa Rican weevil, Exophthalmus jekelianus (White) (Coleoptera: Curculionidae) I is an economically important defoliator of coffee, Coffea arabica, in the Turrialba region of Costa Rica. Preliminary observations of E. jekelianus behavior suggest a preference for shaded microhabitat, which could have important implications for E. jekelianus management. Our results support that E. jekelianus prefer shade to sun microhabitat in a controlled environment, and furthermore, that E. jekelianus location within the coffee agroecosystem is strongly influenced by both shade and the amount and type of fertilizer applied. We postulate that temperature and humidity of the microclimate surrounding a coffee plant and coffee plant nutritional quality are the key factors in determining microhabitat. location for E. jekelianus. Our findings contribute to knowledge of curculionid microhabitat selection and provide novel approaches to monitoring and management of E. jekelianus on Costa Rican coffee.
50. Henry, LM; Roitberg, BD; Gillespie, DR. (2006) Covariance of phenotypically plastic traits induces an adaptive shift in host selection behaviour.Proc R Soc B 273: 2893-2899 Covariance of phenotypically plastic traits induces an adaptive shift in host selection behaviour
host size preference; body size; adaptive behaviour; linked traits; capture efficiency; evolution
Flexibility in adult body size allows generalist parasitoids to use many host species at a cost of producing a range of adult sizes. Consequently, host selection behaviour must also maintain a level of flexibility as adult size is related to capture efficiency. In the present study, we investigated covariance of two plastic traits-size at pupation and host size selection behaviour-using Aphidius ervi reared on either Acyrthosiphon pisum or Aulacorthum solani, generating females of disparate sizes. Natal host was shown to change the ranking of perceived host quality with relation to host size. Parasitoids preferentially attacked hosts that corresponded to the size of the second instar of their natal host species. This resulted in optimal host selection behaviour when parasitoids were exposed to the same host species from which they emerged. Parasitoid size was positively correlated with host size preference, indicating that females use relative measurements when selecting suitable hosts. These coadapted gene complexes allow generalist parasitoids to effectively use multiple host species over several generations. However, the fixed nature of the behavioural response, within a parasitoid's lifetime, suggests that these traits may have evolved in a patchy host species environment.
49. Lalonde, RG; Roitberg, BD. (2006) Chaotic dynamics can select for long-term dormancy.American Naturalist 168: 127-131 Chaotic dynamics can select for long-term dormancy
chaos; diapause; dormancy; risk spreading; demographic; bet hedging
Extended dormancy in a population is evolutionarily costly unless some variance in season-to-season fitness (usually driven by variance in environmental quality) makes bet hedging useful. Consequently, dormancy in a population is usually accepted as evidence of environmental variance. Using a Ricker-type model with heritable variation in dormancy, we show that this need not be so. Intrinsic population dynamics can generate chaotic fluctuations in the absence of environmental variance. Chaotic dynamics increase the frequency of a range of dormant strategists under natural selection, even when mortality during dormancy is relatively high. The buffering effect of dormant individuals then eliminates chaotic dynamics or generates periodic orbits of relatively low amplitude. These stabilized populations harbor a high frequency of dormant individuals that express a range of propensities to enter dormancy.
48. Perry, JC; Roitberg, BD. (2006) Trophic egg laying: hypotheses and tests.Oikos 112: 706-714 Trophic egg laying: hypotheses and tests
Trophic egg-laying - wherein mothers provide non-developing eggs for offspring to eat - has attracted much empirical attention to diverse taxa (e.g. amphibians, non-social and eusocial insects, fish, and marine gastropods). However, there has been been only a limited exchange of ideas among studies of different taxa. We advocate a unified approach to the study of trophic eggs within an evolutionary ecological framework. In this paper, we stress the importance of elucidating the adaptive function of trophic eggs through explicit hypothesis testing, and our primary objective is to outline key experiments that can test adaptive and functional hypotheses. Currently, some cases of hypothesized trophic eggs may simply represent offspring consumption of eggs that failed to develop for non-adaptive reasons (e.g. sperm limitation). Furthermore, in many trophic egg-laying species, it is unclear whether trophic eggs have evolved to provision offspring or to reduce cannibalism among offspring. With increased focus on theory and hypothesis testing, the study of trophic eggs can offer important insight into topics such as sibling rivalry, parent-offspring conflict, and parental care.
47. Peterson, JH; Roitberg, BD. (2006) Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, Megachile rotundata.Behavioral Ecology and Sociobiology 59: 589-596 Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, Megachile rotundata
sex ratio; flight distance; central-place-forager; Megachile rotundata; leafcutter bee
Fisher's theoretical prediction of equal investment in each sex for a panmictic population (The genetical theory of natural selection. Clarendon, Oxford, 1930) can be altered by a number of factors. For example, the sex ratio theory predicts variation in equal investment in each sex when the maternal fitness gains from increased investment differ between sexes. Changing sex allocation because of changing payoffs may result from different ecological situations, such as foraging conditions. We investigated the impact of foraging travel cost on relative investment in sons vs daughters. Field studies were carried out with the central-place-foraging leafcutter bee Megachile rotundata (Fabricius), which has smaller males than females. Therefore, less investment is required to produce a viable son compared with a daughter. We found that with increased flight distance to resources, females produced a greater proportion of sons. Females also invested fewer resources in individual sons and daughters and produced fewer offspring with increased flight distance.
46. Peterson, JH; Roitberg, BD. (2006) Impact of resource levels on sex ratio and resource allocation in the solitary bee, Megachile rotundata.Environ Entomol 35: 1404-1410 Impact of resource levels on sex ratio and resource allocation in the solitary bee, Megachile rotundata
sex ratio; resource allocation; Megachile rotundata; leafcutter bee; food availability
Maternal investment is strongly influenced by the availability of resources. A mother is expected to trade-off allocation to size, number, and sex of offspring to maximize her lifetime reproductive success. Optimal allocation is likely affected by ecological conditions that can alter the costs and benefits of different allocation decisions. When resources are rare, mothers have fewer resources to invest in offspring, likely altering optimal resource allocation. We examined maternal resource allocation to progeny under three different resource levels in semifield conditions for the solitary bee Megachile rotundata (Fabricius). We found that females with access to low resource levels invested less per individual daughter, but the same per individual son, and produced fewer total offspring compared with females with access to greater resource levels. Resource limitation had no impact on sex ratio.
45. VanLaerhoven, SL; Gillespie, DR; Roitberg, BD. (2006) Patch retention time in an omnivore, Dicyphus hesperus is dependent on both host plant and prey type.J Insect Behav 19: 613-621 Patch retention time in an omnivore, Dicyphus hesperus is dependent on both host plant and prey type
heteroptera; Miridae; biological control; retention; arrestment
We examined patch residence times for an omnivorous predator, Dicyphus hesperus on a variety of plants and prey. Individual D. hesperus were placed in cages containing either mullein, tomato, pepper or chrysanthemum plants, and either no prey, Mediterranean flour moth eggs, greenhouse whitefly pupae or two-spotted spider mite adults. Patch residence times were typically greater than 24 h. The probability of remaining on the patch was greatest on mullein and tomato, followed by chrysanthemum and least on pepper, whereas probability of remaining on the patch was greatest when flour moth eggs were present, and least when no prey were available. Patch residence time in D. hesperus was determined by both the prey, and the species of plant, in an independent fashion. Our results reinforce the notion that for omnivores, the patch itself is as important as the prey that it harbors.
44. Henry, LM; Gillespie, DR; Roitberg, BD. (2005) Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi.Entomologia Experimentalis et Applicata 116: 167-174 Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi
Aulacorthum solani; host quality; host preference; host value; host transfer; Hymenoptera; Aphidiidae
The reproductive success of female parasitoids is dependent on their ability to accurately assess the suitability of a host for larval development. For generalist parasitoids, which utilize a broad range of species and instars as hosts, a set of assessment criteria determines whether a host is accepted or rejected. The suitability of a host, however, can only be imperfectly assessed by the female parasitoid, which can result in the selection of lesser quality hosts for oviposition. In this study we explored the disparity between host quality and host preference using the generalist koinobiotic parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) and the host Aulacorthum solani (Harris) (Homoptera: Aphididae), the foxglove aphid. The second instar hosts produced the highest level of reproductive success, while third and fourth instars resulted in a substantially reduced reproductive performance. When given a choice of host instars, parasitoids preferred the older hosts for oviposition disregarding their reduced suitability for larval development. Results are discussed in context of mechanisms involved in A. ervi host selection and biases in the criteria used to assess hosts that may arise when parasitoids transfer host species between generations.
43. Hoffmeister, TS; Roitberg, BD; Vet, LEM. (2005) Linking spatial processes to life-history evolution of insect parasitoids.American Naturalist 166: E62-E74 Linking spatial processes to life-history evolution of insect parasitoids
clutch size; density dependence; competition; foraging behavior; spatial heterogeneity; multitrophic interactions
Understanding the evolutionary transition from solitary to group living in animals is a profound challenge to evolutionary ecologists. A special case is found in insect parasitoids, where a tolerant gregarious larval lifestyle evolved from an intolerant solitary ancestor. The conditions for this transition are generally considered to be very stringent. Recent studies have aimed to identify conditions that facilitate the spread of a gregarious mutant. However, until now, ecological factors have not been included. Host distributions and life-history trade-offs affect the distribution of parasitoids in space and thus should determine the evolution of gregariousness. We add to current theory by using deterministic models to analyze the role of these ecological factors in the evolution of gregariousness. Our results show that gregariousness is facilitated through inversely density-dependent patch exploitation. In contrast, host density dependence in parasitoid distribution and patch exploitation impedes gregariousness. Numerical solutions show that an aggressive gregarious form can more easily invade a solitary population than can a tolerant form. Solitary forms can more easily invade a gregarious, tolerant population than vice versa. We discuss our results in light of exploitation of multitrophic chemical cues by searching parasitoids and aggregative and defensive behavior in herbivorous hosts.
42. Jenner, WH; Kuhlmann, U; Cossentine, JE; Roitberg, BD. (2005) Reproductive biology and small-scale rearing of cherry bark tortrix and its candidate biological control agent.Journal of Applied Entomology 129: 437-442 Reproductive biology and small-scale rearing of cherry bark tortrix and its candidate biological control agent
Campoplex dubitator; Enarmonia formosana; mating; oviposition; rearing
The larval parasitoid, Campoplex dubitator (Hym.,: Ichneumonidae), is under consideration as an agent for classical biological control of cherry bark tortrix (CBT), Enarmonia formosana (Lep.,: Tortricidae), in North America. A comprehensive risk analysis of the candidate agent will require prosperous cultures of both the pest and its parasitoid. We present a rearing method for small-scale production of both species using a bean-based artificial diet, with additional information on the reproductive biology of C. dubitator. Based on estimated survivorship probabilities, a CBT egg had a 70% chance of developing completely to the adult stage under this system. The success of parasitism, however, was very dependent on the instar of the CBT host larva at the time of oviposition. All parasitised first instar larvae died shortly after the attack, rendering them unsuitable for oviposition, while 50% of parasitised second instar larvae died prematurely. In contrast, early mortality was 15-30% for larvae parasitised in the third to fifth instars. Regardless of the instar at oviposition, approximately 90% of the surviving hosts yielded parasitoids, showing a high acceptance by C. dubitator of second to fifth instars for oviposition.
41. Perry, JC; Roitberg, BD. (2005) Ladybird mothers mitigate offspring starvation risk by laying trophic eggs.Behavioral Ecology and Sociobiology 58: 578-586 Ladybird mothers mitigate offspring starvation risk by laying trophic eggs
Coccinellidae; Harmonia axyridis; hatching synchrony; sibling cannibalism; trophic eggs
A large proportion of ladybird beetle (Coleoptera: Coccinellidae) eggs are apparently infertile-they do not develop an embryo and are consumed by larvae hatching within the egg batch. The predicted benefits of egg consumption for larvae are empirically well supported. An important question, however, remains: are these eggs a maternal strategy to feed offspring (i.e., trophic eggs) or did egg eating evolve to exploit unavoidably infertile eggs? We investigated the adaptive value of infertile eggs in laboratory experiments with multicoloured Asian ladybirds (Harmonia axyridis). Female H. axyridis were assigned to low and high resource environments for brief intervals; we predicted that tactics to facilitate egg cannibalism, such as infertile egg production and hatching asynchrony, would be adopted in low food environments in which starvation risk for offspring is greater. We conducted two experiments in this manner that provided females with information about resource levels through prey feeding or scent. We also observed female oviposition patterns and tested for infertile egg distributions that departed from random. Females produced 56% more infertile eggs in the low vs. the high food treatment; however, hatching synchrony did not change. We consider a potential confound between information and nutrition state unlikely because ladybirds are well able to tolerate low food for 24 h, the duration of trials, and because females were in good condition when trials began. Results suggest that ladybirds use information from prey encounter to manipulate the proportion of trophic eggs in a manner consistent with the adaptive hypothesis, the first evidence of trophic egg plasticity in a non-eusocial insect.
40. Perry, JC; Roitberg, BD. (2005) Games among cannibals: competition to cannibalize and parent-offspring conflict lead to increased sibling cannibalism.J Evolution Biol 18: 1523-1533 Games among cannibals: competition to cannibalize and parent-offspring conflict lead to increased sibling cannibalism
game interactions; parent-offspring conflict; sibling cannibalism; sibling rivalry; trophic eggs
Sibling cannibalism occurs in many species, yet understanding of sibling cannibalism as an adaptation currently lags behind understanding of other antagonistic interactions among siblings. Observed sibling cannibalism phenotypes likely reflect the interaction between competitive games among siblings and parent-offspring conflict. Using a game-theoretic approach, we derive optimal offspring cannibalism behaviour and parental modifiers that limit or facilitate cannibalism. The results are compared to contemporary frequency-independent analysis. With the addition of game interactions among siblings or parent-offspring co-evolution, our model predicts increased cannibalism (compared to the frequency-independent prediction), as offspring compete to eat siblings. When infertile eggs are present - strengthening competition - offspring risk eating viable siblings in order to gain access to infertile eggs, intensifying parent-offspring conflict. We use the results to make new predictions about the occurrence of sibling cannibalism. Additionally, we demonstrate the utility of trophic egg laying as a maternal mechanism to promote egg eating.
39.Roitberg, BD; Gillespie, DR; Quiring, DMJ; Alma, CR; Jenner, WH; Perry, J; Peterson, JH; Salomon, M; VanLaerhoven, S. (2005) The cost of being an omnivore: mandible wear from plant feeding in a true bug.Naturwissenschaften 92: 431-434 The cost of being an omnivore: mandible wear from plant feeding in a true bug
Evolutionary and ecological transitions from carnivorous to omnivorous feeding may be constrained by the ability of the animal to cope with disparate types of foods, even if preadaptations for such behaviour exist. The omnivorous true bug, Dicyphus hesperus (Hemiptera: Miridae) requires both animals (small, soft-bodied insects) and plants in its diet and obtains the majority of its dietary and metabolic water from plant feeding. Serrations on the lateral margins of the mandibular stylets wear with age, and this wear is exacerbated when the insects feed on plants compared to those provided free water and no plants. D. hesperus that feed on plants attack fewer prey but consumed similar amounts of prey tissue compared to individuals that were provided free water. Although others have shown mandible wear for plant-chewing animals we show for the first time that plant feeding can impose similar wear on plant-piercing animals as well.
38.Roitberg, BD; Gordon, I. (2005) Does the Anopheles blood meal - fecundity curve, curve?J Vector Ecol 30: 83-86 Does the Anopheles blood meal - fecundity curve, curve?
Anopheles; blood meal; fecundity curve; body size
We determined the blood meal size - fecundity relationship in Anopheles gambiae in the laboratory. Our primary interest was to determine whether the fecundity curve has a non-linear component, i.e., does it decelerate towards an asymptote? Small and large adult females in their second gonotrophic cycle were fed on human hosts for predetermined lengths of time. Blood meal size was ascertained by weight and subsequent fecundity was detertmined by the number of eggs laid on filter paper. In both small and large-bodied females there was a significant curvilinear component. We used this relationship to show that marginal returns from feeding decline as a function of current blood load. This means that further fecundity payoff for continued feeding declines over time.
37. Choi, MY; Khaskin, G; Gries, R; Gries, G; Roitberg, BD; Raworth, DA; Kim, DH; Bennett, RG. (2004) (2R,7S)-diacetoxytridecane: Sex pheromone of the aphidophagous gall midge, Aphidoletes aphidimyza.Journal of Chemical Ecology 30: 659-670 (2R,7S)-diacetoxytridecane: Sex pheromone of the aphidophagous gall midge, Aphidoletes aphidimyza
Aphidoletes aphidimyza; Cecidomyiidae; sex pheromone; stereoisomers; (2R,7S)-diacetoxytridecane; (2S,7R)-diacetoxytridecane; (2R,7R)-diacetoxytridecane; (2S,7S)-diacetoxytridecane
In a recent study, evidence was presented that females of the aphidophagous midge Aphidoletes aphidimyza (Rondi) (Diptera: Cecidomyiidae) release a sex pheromone to attract mates. Our objectives were to identify and bioassay the pheromone. Coupled gas chromatographic-electroantennographic detection (GC-EAD) analyses of untreated and hydrogenated pheromone extract on three fused-silica columns (DB-5, DB-23, DB-210) revealed a single compound that elicited responses from male antennae. Retention index calculations of this candidate pheromone (CP) suggested that it was a di-acetate. Considering that most of the presently identified cecidomyiid pheromones consist of a 13-carbon chain with (at least) one acetate group in C2, we synthesized 2,6-, 2,7-, 2,8-, 2,9-, 2,10-, 2,11-, and 2,12-diacetoxytridecane. In GC analyses of these compounds, only 2,7- diacetoxytridecane cochomatographed with CP on all columns. In laboratory two-choice experiments with stereospecifically synthesized stereoisomers, only (2R, 7S)-diacetoxytridecane elicited significant anemotatic responses by male A: aphidimyza. In trapping experiments in greenhouse compartments, only traps baited with (2R, 7S)-diacetoxytridecane captured significant numbers of male A. aphidimyza, clearly revealing the absolute configuration of the pheromone. Failure of the stereoisomeric mixture (containing all four stereoisomers including the pheromone) to attract males is due to inhibitory characteristics of the (2R, 7R)- and (2S, 7R)-stereoisomers. The pheromone of zoophagous A. aphidimyza resembles those from phytophagous cecidomyiid midges, suggesting a common, diet-independent pathway for pheromone biosyntheses.
36. Choi, MY; Roitberg, BD; Shani, A; Raworth, DA; Lee, GH. (2004) Olfactory response by the aphidophagous gall midge, Aphidoletes aphidimyza to honeydew from green peach aphid, Myzus persicae.Entomologia Experimentalis et Applicata 111: 37-45 Olfactory response by the aphidophagous gall midge, Aphidoletes aphidimyza to honeydew from green peach aphid, Myzus persicae
Aphidoletes aphidimyza; Diptera; Cecidomyiidae; honeydew; Myzus persicae; oviposition; olfactory response; Hemiptera; Aphididae
Female adults of the aphidopagous gall midge, Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), showed an olfactory response to honeydew excreted by the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) under laboratory conditions. The response was only elicited by treatments with honeydew, whereas aphids, aphids with pepper plants or leaves, and pepper plants or leaves were not attractive to the midges. Dose-dependent responses were observed from whole honeydew, honeydew volatiles extracted in pentane, and honeydew volatiles captured on Porapak Q(R). When honeydew was eluted with three sequential pentane washes, a positive response was only observed from the midges for the first wash. Female midges laid more eggs on pepper plants infested with higher densities of M. persicae. The olfactory response of midges to honeydew is discussed with respect to prey location.
35. Jenner, WH; Kuhlmann, U; Cossentine, JE; Roitberg, BD. (2004) Phenology, distribution, and the natural parasitoid community of the cherry bark tortrix.Biological Control 31: 72-82 Phenology, distribution, and the natural parasitoid community of the cherry bark tortrix
campoplex dubitator; Enarmonia formosana; biological control; parasitoid community; parasitism; spatial distribution; phenology
The aim of this study was to investigate the ecology and phenology of the cherry bark tortrix (CBT), Enarmonia formosana Scopoli (Lepidoptera: Tortricidae), as well as its previously unknown parasitoid community, in Central Europe. The CBT is univoltine, overwintering primarily in the fourth or fifth (ultimate) larval instars. This bark-boring pest, found on cherry trees throughout the surveyed regions of France, Germany, and Switzerland, had a highly skewed within-tree distribution, with most larvae aggregated near the bases of trees. The natural parasitoid community of the CBT consisted of 13 species (12 ichneumonids and 1 pteromalid), which fall into four parasitoid guilds: larval-pre-pupal, late larval (ecto), larval-pupal, and pupal. Although parasitism was recorded from each region studied, only one larval parasitoid and three pupal parasitoids were collected on more than one occasion. Of these, the larval parasitoid, Campoplex dubitator Horstmann (Hymenoptera: Ichneumonidae), was clearly dominant, representing 85% of all the parasitoids emerging from CBT hosts. This paper discusses the relevance of these and other features of the CBT parasitoid community for biological control. (C) 2004 Elsevier Inc. All rights reserved.
34. Mondor, EB; Roitberg, BD. (2004) Inclusive fitness benefits of scent-marking predators.Proceedings of the Royal Society of London Series B-Biological Sciences 271: S341-S343 Inclusive fitness benefits of scent-marking predators
alarm pheromone; aphid; cornicle droplet; inclusive fitness; predation risk; scent mark
Because relatedness is high and dispersal is limited, one would expect to see higher levels of altruistic behaviour among clonal organisms than among animals of lesser relatedness. Enigmatically, however, parthenogenetic aphids do not emit alarm signals when a predator first enters a colony but only after being captured. Here, we report that an aphid smearing alarm pheromone directly onto a predator decreases the predation risk for clone-mates as the predator continues to search for additional prey. Adult multicoloured Asian ladybird beetles, Harmonia axyridis, daubed with alarm pheromone caused a greater proportion of aphids to drop off a plant and escape predation than did predators lacking pheromone droplets. Thus, along with direct fitness benefits of individual protection, aphid alarm signalling behaviour may have evolved through inclusive fitness benefits of protecting clone-mates by scent-marking predators.
33.Roitberg, BD. (2004) From parasitoid behavior to biological control: applied behavioral ecology.Canadian Entomologist 136: 289-297 From parasitoid behavior to biological control: applied behavioral ecology
A hypothetical parasitoid mass rearing facility is used to unite principles from behavioral ecology and biological control. The key to the problem is variation in the tendency of solitary parasitoids to superparasitize. Superparasitism affects individual and population parasitoid productivity, though not necessarily to the same degree. Herein, the interest is in determining conditions that will maximize parasitoid population productivity when superparasitism varies. To accomplish this, a combination of graphical marginal analysis (to provide an economic context), dynamic optimization models (to determine individual parasitoid superparasitism tendency), and functional response models (to determine parasitoid population productivity) has been used. Marginal analysis shows that marginal returns decrease with an increase in the number of parasitoids released but that the slope of the marginal returns curve depends upon the sensitivity of superparasitism to environmental conditions. In addition, results show that parasitoid responses can be highly nonlinear and, as such, can greatly affect optimal numbers of parasitoids released in a nonintuitive manner. This behavioral ecology approach greatly increases efficiency and predictability of parasitoid production.
32. Sinia, A; Roitberg, B; McGregor, RR; Gillespie, DR. (2004) Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus.Entomologia Experimentalis et Applicata 110: 243-248 Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus
biological control; Dicyphus hesperus; generalist predator; Heteroptera; Miridae; omnivory; plant feeding; tomato; zoophytophagous predator
The effects of water stress (produced by water deprivation and prey feeding) on plant feeding were investigated in the omnivorous predator Dicyphus hesperus Knight (Hemiptera: Miridae). The objective was to determine if prey feeding aggravated water deficits and thus increased plant feeding. We measured plant feeding in a factorial experiment where female D. hesperus were prepared for experiments by providing or withholding water and/or prey for 24 h. We then evaluated the amount of plant feeding on Nicotiana tabacum seedlings by the direct observation of insects at three different densities of the prey, Ephestia kuehniella eggs. The amount of plant feeding, as measured by frequency of plant feeding bouts and time spent plant feeding during observation, was significantly greater for water-deprived individuals than for those that had been provided with water. Individuals that had been provided with prey fed on plants at a significantly higher frequency than prey-deprived individuals at two of the prey densities used in the experiment. These results support the hypothesis that plant feeding in zoophytophagous Hemiptera facilitates prey feeding by providing water that is essential for predation.
31. Tyerman, JG; Roitberg, BD. (2004) Factors affecting soldier allocation in clonal aphids: a life-history model and test.Behavioral Ecology 15: 94-101 Factors affecting soldier allocation in clonal aphids: a life-history model and test
colony defense; dynamic programming model; eusocial aphids; Pemphigus spyrothecae; soldier allocation strategies; tradeoffs
Aphid species using a defensive soldier caste offer us the opportunity to study allocation decisions by eusocial groups, without the hindrance of genetic dissimilarity between colony members, which often impair studies involving Hymenopteran or Isopteran systems. When the entire aphid clone is considered the adaptive unit of organization, understanding soldier allocation strategies is tantamount to understanding the outcome of the tradeoff between clonal growth (i.e., asexual reproduction) and clonal defense. Under this framework, we present the results of a dynamic programming effort aimed at determining the optimal ontogeny of defensive allocation strategies by eusocial clonal organisms. We consider the allocation decision for clones with both obligately and facultatively sterile soldiers, under various levels of predation, and favorable and unfavorable ecological conditions. We test predictions of the model with the cusocial aphid, Pemphigus spyrothecae. Our model predicts that defensive investment should be dependent on the time of the season, with clones discounting defense nearer the end of season. Defensive investment should also vary inversely with clonal productivity and be sensitive to the current state (e.g., level of defense) of the clone. Census data collected in Burnaby, British Columbia, Canada, conform to patterns of clonal composition derived from allocation decisions generated in the model. Finally, qualitative predictions about patterns of clonal organization under "good" and "poor" ecological conditions were upheld by comparing clones in preferred and less-preferred galling sites.
30. Mondor, EB; Roitberg, BD. (2003) Age-dependent fitness costs of alarm signaling in aphids.Canadian Journal of Zoology-Revue Canadienne de Zoologie 81: 757-762 Age-dependent fitness costs of alarm signaling in aphids
For an alarm signal to evolve, the benefits to the signaler must outweigh the costs of sending the signal. Research has largely focused on the benefits of alarm signaling, and the costs to an organism of sending an alarm signal are not well known. When attacked by a predator, aphids secrete cornicle droplets, containing an alarm pheromone, for individual protection and to warn clonemates. As aphid alarm pheromone is synthesized de novo in a feedback loop with juvenile hormone, we hypothesized that the secretion of cornicle droplets may result in a direct fitness cost to the emitter. We show that the secretion of a single cornicle droplet by pre-reproductive (third- and fourth-instar) pea aphids, Acyrthosiphon pisum, directly altered the timing and number of offspring produced. Third-instar pea aphids delayed offspring production but produced more offspring overall than non-secreting aphids, demonstrating a life-history shift but no significant fitness cost of droplet secretion. Fourth-instar pea aphids also delayed offspring production but produced the same number of offspring as non-secretors, resulting in a direct fitness cost of droplet secretion. Offspring production by adult, reproductive pea aphids that secreted a cornicle droplet did not differ from that of non-secretors. Thus, the fitness costs of secreting cornicle droplets containing an alarm signal are age-dependent.
29.Roitberg, BD; Mondor, EB; Tyerman, JGA. (2003) Pouncing spider, flying mosquito: blood acquisition increases predation risk in mosquitoes.Behavioral Ecology 14: 736-740 Pouncing spider, flying mosquito: blood acquisition increases predation risk in mosquitoes
Anopheles; escape; feeding; flight; mass; mosquitoes; predation risk; spiders
Female mosquitoes dramatically increase their mass when blood feeding on their hosts. Such an increase could impact mosquito mortality risk by reducing escape speed and/or agility. We used two laboratory-based experiments to test this notion. In the first, we allowed mature female Anopheles gambiae mosquitoes to feed from 0 to 4 min and then attacked those females with an artificial predator. We videotaped subsequent escape response of each mosquito. Analysis of those responses clearly demonstrated an inverse relationship between increased mass and escape speed. In the second experiment, we exposed both blood-engorged and unfed A.gambiae females to single zebra spiders (Salticus scenicus) in small plexiglass cages. Here, we focused on mosquito escapes from searching and pouncing spiders. We found that engorged mosquitoes were three times less likely to escape searching spiders compared to unfed conspecifics. Thus we conclude that blood feeding has substantial state-dependent risk both at the host (experiment 1) and after feeding (experiment 2). Such risk can be extended to a broad range of taxa.
28. VanLaerhoven, SL; Gillespie, DR; Roitberg, BD. (2003) Diel activity pattern and predation rate of the generalist predator Dicyphus hesperus.Entomologia Experimentalis et Applicata 107: 149-154 Diel activity pattern and predation rate of the generalist predator Dicyphus hesperus
Heteroptera; Miridae; nocturnal; omnivore; biological control; foraging behaviour; Dicyphus hesperus
This study examined the diel activity pattern and the effect of diel activity pattern on predation rate and prey finding of Dicyphus hesperus Knight (Heteroptera:Miridae). To determine the diel activity pattern of D. hesperus, starved females were placed on tomato leaflets Lycopersicon esculentum Mill. (Solanaceae) under zero, low, or high light intensities at 02:00, 08:00, and 14:00 h, respectively, and the amount of time spent walking or resting during a 30-min interval was recorded. Predation rates of D. hesperus females on Ephestia kuehniella Zeller (Lepidoptera:Pyralidae) egg patches were determined under either a L16:D8 (long day) or L8:D16 (short day) diel period. Egg patches were removed from D. hesperus females after either 8 or 16 h of dark or 16 or 8 h of light, and the number of eggs consumed was counted. Dicyphus hesperus females spent more time searching for prey at night than during the day. Females ate eggs at a higher rate during the night than during the day. Overall, D. hesperus females had higher predation rates when reared under a long day diel cycle compared with females reared under a short day diel cycle. More females reared at the L16:D8 diel cycle found the egg patch during the night than during the day. There was no difference in egg patch finding between night and day for females reared at L8:D16. Overall, L16:D8 reared females found more egg patches than females reared at L8:D16. Therefore, D. hesperus females are more active and find and consume prey at a higher rate at night than day.
27. Krupke, CH; Roitberg, BD; Judd, GJR. (2002) Field and laboratory responses of male codling moth (Lepidoptera : Tortricidae) to a pheromone-based attract-and-kill strategy.Environmental Entomology 31: 189-197 Field and laboratory responses of male codling moth (Lepidoptera : Tortricidae) to a pheromone-based attract-and-kill strategy
Cydia pomonella; attracticide; behavior; pheromone; orchard
A case study of a pheromone-based attract-and-kill management strategy for codling moth, Cydia pomonella (L.), was conducted to examine key insect behavioral factors mitigating the possible effectiveness of this strategy. Last Call CM is a newly registered attracticide product that combines the primary component of codling moth sex pheromone with the insecticide permethrin. Studies of competition between pheromone point sources within caged trees showed individual attracticide droplets were significantly more attractive to male moths than calling females. In commercial orchard blocks, marked male moths were recaptured after visiting attracticide droplets applied at rates of 50, 100, and 200 droplets/ha, although no marked moths were recaptured in plots with 500 droplets/ha. This experiment also revealed no significant differences among 0, 50, 100, and 200 droplets/ba in suppressing total catch in female-baited traps, nor were total numbers of females attracting at least one male reduced significantly. In plots with 500 droplets/ha applied, male moth catch was suppressed significantly compared with catches in untreated control plots, and the number of females attracting at least one male was reduced significantly as well. Experiments investigating sublethal physiological effects of attracticide exposure upon mating competency of male codling moths demonstrated male leg autotomy at 1, 24, 48, and 72 h after exposure. Male codling moth at 1, 24, 48, and 72 h after exposure placed near calling virgin females exhibited significant behavioral differences from sham-treated males in courtship and mating. These results clarify some of the possible mechanisms, and strengths and weaknesses of this attract-and-kill management strategy for codling moth.
26. Mondor, EB; Roitberg, BD. (2002) Pea aphid, Acyrthosiphon pisum, cornicle ontogeny as an adaptation to differential predation risk.Canadian Journal of Zoology-Revue Canadienne de Zoologie 80: 2131-2136 Pea aphid, Acyrthosiphon pisum, cornicle ontogeny as an adaptation to differential predation risk
Aphids possess unique anatomical structures called cornicles through which a defensive secretion containing alarm pheromone is often emitted when a predator attacks an aphid. The levels of alarm pheromone in cornicle droplets from the pea aphid, Acyrthosiphon pisum (Harris), vary considerably during development; however, it is not clear how the length of the cornicle changes during ontogeny. The length of the cornicle relative to the lengths of other body structures may have profound effects on aphid defense and alarm signal diffusion. Using previously published morphological measurements of pea aphids and observing interactions between pea aphids and multicolored Asian ladybird beetles, Harmonia axyridis Pallas, it was observed that pea aphid cornicles elongate proportionally more than other body parts during the first four instars, when alarm-pheromone levels have peaked, than during the fifth (adult) instar, when pheromone levels decline. Pea aphids also are more likely to emit cornicle droplets and daub them onto a predator when the cornicles are undergoing such rapid growth. We suggest that because of a high risk of predation, rapid cornicle growth in juveniles has evolved both for individual defense and for the inclusive fitness benefits of alarm signaling.
25. Mondor, EB; Roitberg, BD; Stadler, B. (2002) Cornicle length in Macrosiphini aphids: a comparison of ecological traits.Ecological Entomology 27: 758-762 Cornicle length in Macrosiphini aphids: a comparison of ecological traits
aphid; Aphidinae; cornicle; evolution; Macrosiphini
1. Aphids often emit cornicle droplets when attacked by predators. While the function of cornicle droplets has long been debated (i.e. mechanical protection vs. chemical signalling), it is not understood why aphid species have cornicles of different lengths. 2. It was hypothesised that aphids living in more scattered colonies have longer cornicles to scent-mark predators with cornicle droplets containing alarm pheromone, so that clone-mates are provided with advanced warning of a threat, even if not at the predation site. To test this hypothesis, multiple regression analyses were used, due to a lack of phylogenetic information on these taxa, to address which ecological traits (amount of wax on an aphid, degree of colony aggregation, feeding shelter, ant attendance) are correlated with cornicle length. 3. Aphids living in dense colonies tended to have shorter cornicles than aphids living in more scattered colonies. Also, aphids with more protection (i.e. wax) on their bodies had shorter cornicles. Aphids also tended to have shorter cornicles when tended by ants. The presence of a feeding shelter was not a good predictor of cornicle length. 4. It is suggested that longer cornicles function to scent-mark predators with alarm pheromone to increase the inclusive fitness of a clone; however the negative correlation between the amount of individual protection, and also ant attendance, and cornicle length argues for a trade-off between different forms of defence.
24. Prasad, RP; Roitberg, BD; Henderson, DE. (2002) The effect of rearing temperature on parasitism by Trichogramma sibericum Sorkina at ambient temperatures.Biological Control 25: 110-115 The effect of rearing temperature on parasitism by Trichogramma sibericum Sorkina at ambient temperatures
Trichogramma sibericum; parasitism; temperature acclimation; biological control
Parasitism activity of Trichogramma sibericum Sorkina tested in laboratory bioassays at different ambient temperatures was not dependent on the rearing temperature of the wasps. Trichogramma sibericum parasitized more Ephestia kuelmiella Zeller eggs as ambient temperature increased from 16 to 26 degreesC. Rearing temperature had a significant effect on potential fecundity (measured as egg load) and on parasitism rate. Insects reared at 21 degreesC laid significantly more eggs than wasps reared at 16, 26 degreesC or fluctuating temperatures between 16 and 26 degreesC. Computer generated simulations with laboratory derived data suggest that rearing T. siberician at 16 degreesC will improve biological control efficacy when ambient temperatures are expected to be cool (<210 &DEG;C). Marginal analysis also indicates that rearing at 16 &DEG;C is more cost effective, again when ambient temperatures are expected to be cool. (C) 2002 Elsevier Science (USA). All rights reserved.
23. Petrescu, AS; Mondor, EB; Roitberg, BD. (2001) Subversion of alarm communication: Do plants habituate aphids to their own alarm signals?Canadian Journal of Zoology-Revue Canadienne de Zoologie 79: 737-740 Subversion of alarm communication: Do plants habituate aphids to their own alarm signals?
When attacked by a predator, pea aphids, Acyrthosiphon pisum, emit an alarm pheromone, (E)-beta -farnesene, which causes nearby conspecifics to disperse from the area. However, herbivore-damaged plants also emit (E)-beta -farnesene. We hypothesized that plants release farnesene to habituate aphids, i.e., to disrupt their alarm-pheromone responses, perhaps to reduce herbivory by increasing parasitoid or predator efficacy. Thus, we addressed two questions: (1) Do aphids habituate to (E)-beta -farnesene, and (2) Are they habituated at levels produced by aphid-infested plants? On an artificial diet devoid of farnesene, aphids were exposed to 10 ng/cm(3) of (E)-beta -farnesene or a hexane control over 24 h. Habituation was achieved, as dropping responses to 50 ng/cm(3) of (E)-beta -farnesene decreased after exposure. We then exposed aphids to 0.8 ng/cm(3) of (E)-beta -farnesene, a pheromone concentration emitted by plants, or a hexane control for 24 h. Their reaction to 38 ng/cm(3) of (E)-beta -farnesene, the maximum pheromone concentration found in aphid-cornicle droplets, was not significantly different before and after exposure. Thus, our hypothesis that plants emit farnesene to disrupt aphid alarm communication remains unsupported.
22. Prokopy, RJ; Roitberg, BD. (2001) Joining and avoidance behavior in nonsocial insects.Annual Review of Entomology 46: 631-665 Joining and avoidance behavior in nonsocial insects
fitness; inhibition; facilitation; grouping; spacing
Groups of two or more consexual conspecific adults of many kinds of nonsocial insects have been observed to form at feeding, mating, ovipositional, or sheltering sites. Conversely, adults of these same insects have been observed to avoid joining consexual conspecifics (or their progeny) and to place themselves (or their progeny) at some distance that results in spacing. Examples from various taxa illustrate that mechanisms underlying joining or avoidance behavior differ among species, as do types of benefits and costs to individuals who decide to join or avoid others. Moreover, within a given species, the decision to join or avoid others can be affected markedly by the physiological and informational state of the individual and by contextual response thresholds to resource availability. Decisions that benefit the individual may or may not affect the group in terms of total reproductive output.
21. Gillespie, DR; Opit, G; Roitberg, B. (2000) Effects of temperature and relative humidity on development, reproduction, and predation in Feltiella acarisuga (Vallot) (Diptera : Cecidomyiidae).Biological Control 17: 132-138 Effects of temperature and relative humidity on development, reproduction, and predation in Feltiella acarisuga (Vallot) (Diptera : Cecidomyiidae)
Feltiella acarisuga; Tetranychus urticae; biological control; greenhouse; tomato; temperature; relative humidity; predation; development; fecundity; survival
The predatory gall midge Feltiella acarisuga (Vallot) (Diptera: Cecidomyiidae) is a biological control agent for twospotted spider mites on greenhouse vegetable crops. Effects of temperature and relative humidity (RH) on development of immatures, reproduction, and prey capture were determined in order to confirm the suitability of F. acarisuga for use in greenhouses. Developmental time ranged from 10 days at 27 degrees C to 34 days at 15 degrees C. At 20 degrees C, developmental time was significantly shorter at 96% RH than at 84% RH. There was very poor survival of immatures at 64% RH and none at 36%. Lifespan of adult females decreased with increasing temperature, but temperature had no significant effect on number of eggs laid. At 20 degrees C, lifespan was longer at 84 and 96% RH than at 64 or 36% RH. The number of spider mites attacked by 3-day-old larvae over 8 h increased with increasing temperature from 15 to 27 degrees C. The number of mites attacked also increased with increasing RR at 27 degrees C. We conclude that F. acarisuga will complete its life cycle and reproduce under conditions typically found in vegetable greenhouses in northern temperate climates. However, extended periods of low RH (<60% RH) could reduce reproduction and survivorship sufficiently to impair the predator's action against spider mite populations. (C) 2000 Academic Press.
20. Hoffmeister, TS; Roitberg, BD; Lalonde, RG. (2000) Catching Ariadne by her thread: how a parasitoid exploits the herbivore's marking trails to locate its host.Entomologia Experimentalis et Applicata 95: 77-85 Catching Ariadne by her thread: how a parasitoid exploits the herbivore's marking trails to locate its host
parasitoid host location; marking pheromone; contact kairomone; directed search; Rhagoletis basiola; Halticoptera rosae
Chemical signals that can be associated with the presence of a host insect often work as arrestants in close range host location by parasitoids, leading to longer searching times on patches where such signals are present. Our current view of parasitoid host location is that by prolonging the search times in patches, randomly searching parasitoids enhance their chance of detecting host insects. However, prolonged search times are not necessarily the only modification in parasitoid behaviour. In this study, we examine the exploitation of host-fruit marking pheromone of rose-hip flies, Rhagoletis basiola Osten-Sacken (Diptera: Tephritidae) by the specialized egg-larval parasitoid Halticoptera rosae Burks (Hymenoptera: Pteromalidae). We provide evidence that the instantaneous probability that a host egg will be located by a searching parasitoid wasp differs markedly between pheromone-marked and unmarked fruits. The arresting response to the marking pheromone, i.e., the prolonged time a wasp is willing to search on marked fruits, can only account for a small fraction of the difference in successful host location on marked and unmarked fruits. We further demonstrate that the time wasps require to locate the host egg is independent of the size of the rose-hip harbouring the fly egg, and thus is independent of the area the wasp potentially has to search. A comparison of our findings with results of different search algorithms for parasitoid wasps suggests that wasps use the fly's pheromone marking trail as a guide way to the fly's oviposition site and thus the host egg.
19. McGregor, RR; Roitberg, BD. (2000) Size-selective oviposition by parasitoids and the evolution of life-history timing in hosts: fixed preferences vs frequency-dependent host selection.Oikos 89: 305-312 Size-selective oviposition by parasitoids and the evolution of life-history timing in hosts: fixed preferences vs frequency-dependent host selection
The influence of size-selective oviposition behaviour by parasitoids on the evolution of life-history timing in their hosts was examined using an optimization model of a two-stage life history similar to a genetic algorithm. Host populations with varying durations of early-larval development were subjected to selection in scenarios where parasitoids had fixed preferences for oviposition on late-stage larvae, or those where parasitoid attack was dependent on the relative frequencies of the two life stages present in the population. Fixed preference for oviposition on late-stage larvae caused positive directional selection on the duration of early-larval development. Surviving individuals remained for as long as possible in the first stage of development in order to avoid parasitoid attack. Frequency-dependent parasitoid attack, in contrast. caused maintenance of variation ih the duration of early-larval development. The influence of the fitness payoffs of different life stages on the plasticity of size-selective oviposition behaviour is discussed, as are possible implications of the model results for parasitoid-host population dynamics.
18. Mondor, EB; Baird, DS; Slessor, KN; Roitberg, BD. (2000) Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum.J. Chem. Ecol. 26: 2875-2882 Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum
Alarm pheromone; signaling; (E)-beta-farnesene; pea aphid; cornicle; ontogeny; defense
When attacked by a predator, an aphid may secrete a droplet of fluid from its cornicles containing a volatile alarm pheromone component, (E)-beta -farnesene. This study investigated both qualitative and quantitative aspects of alarm pheromone production in the pea aphid. Acyrthosiphon pisum. The best predictor of cornicle droplet emission was reproductive phase, rather than instar, as prereproductive aphids were more likely to secrete cornicle droplets than either reproductive or postreproductive individuals. Analogously, alarm pheromone amounts were highest in prereproductive aphids. (E)-beta -Farnesene quantities (mean +/- SE) increased significantly from first instar (1.5 +/- 0.6 ng) to second instar (11.2 +/- 3.7 ng) and did not significantly change during third (12.8 +/- 3.0 ng) or fourth instars (11.0 +/- 3.7 ng). Alarm pheromone amounts then decreased significantly in adults (4.8 +/- 2.3 ng). We suggest that prereproductive aphids have been selected to produce higher levels of pheromone because of their more clustered colony structure and higher levels of predation, as compared with adult aphids. DOI
17. Mondor, EB; Roitberg, BD. (2000) Has the attraction of predatory coccinellids to cornicle droplets constrained aphid alarm signaling behavior?Journal of Insect Behavior 13: 321-329 Has the attraction of predatory coccinellids to cornicle droplets constrained aphid alarm signaling behavior?
kairomone; searching; predator-prey interactions; pheromone; E-B-farnesene
When attacked by a predator, aphids of many species secrete cornicle droplets, containing an alarm pheromone, that results in the dispersal of nearby conspecifics. As females are parthenogenetic, alarm signaling functions to enhance the survival of clone-mates. Enigmatically, however, aphids are physically able to, but usually do not emit alarm pheromone when initially detecting a predator but rather signal only when captured by a predator We hypothesized that cornicle droplets may be attractive to natural enemies and result in an increased risk of predation for the signaler thereby selecting for prudent alarm signalers. We tested this hypothesis by investigating the olfactory cues that the multicolored Asian ladybird beetle, Harmonia axyridis Pallas, uses to locate pea aphids, Acyrthosiphon pisum. In choice tests, H. axyridis were am-acted to odors from pea aphid colonies, whether feeding or nor feeding on a host plant leaf; but were not attracted to cornicle droplets containing alarm pheromone. Further individual pea aphids emitting cornicle droplets were not located more often or in a shorter period of time by beetles than aphids nor emitting cornicle droplets. Thus, the cost of emitting early alarm signals is not prohibitively high in regards to the attraction of predators such as H. axyridis.
16. Sargent, RD; Roitberg, BD. (2000) Seasonal decline in male-phase duration in a protandrous plant: a response to increased mating opportunities?Functional Ecology 14: 484-489 Seasonal decline in male-phase duration in a protandrous plant: a response to increased mating opportunities?
Chamerion angustifolium; dichogamy; Epilobium; hermaphrodite; pollinator visitation
1. We examined the effects of pollinator visitation and time of season on male- and female-phase duration, using experimental manipulation and survey data from naturally occurring populations of Chamerion (= Epilobium) angustifolium (L.) J. Holub (Onagraceae). 2. Based on the observation that male mating opportunity (numbers of female flowers/numbers of male flowers) increases seasonally, we predicted that individual flowers should spend more time in the male phase early in the season when mating opportunity is low. We predicted that if seasonal changes in mating opportunity select for phase duration, male-phase duration should decline when pollinator effects are experimentally controlled. 3. A comparison of phase duration in naturally pollinated and pollinator-excluded plants supported this prediction: male-phase duration in the pollinator-exclusion treatment was longer and declined faster than in the naturally pollinated group. 4. A population survey revealed that once the effects of temperature were controlled for, male-phase duration was negatively correlated with date, while female-phase duration was positively correlated with date. 5. These findings suggest that seasonal variation in mating opportunity, and not just pollination rate or temperature, may play a significant role in phase duration in dichogamous plants.
15. Tenhumberg, B; Tyre, AJ; Roitberg, B. (2000) Stochastic variation in food availability influences weight and age at maturity.Journal of Theoretical Biology 202: 257-272 Stochastic variation in food availability influences weight and age at maturity
Variation in mean food availability, and in the variance around the mean, affects the growth rate during development. Previous theoretical work on the influence of environmental quality or growth rates on the phenotypic traits age and size at maturation assumed that there is no variation in growth rate or food availability within a generation. We develop a stochastic dynamic programming (SDP) model of the foraging behaviour of aphidophagous syrphids, and use this model to predict when syrphids should pupate (mature) when average food availability changes, or varies stochastically, during development. The optimal strategy takes into account not only the availability of food, but also the timing of its availability. Food availability, when small, influences developmental time, but not weight at pupation. Food availability, when large, influences weight at pupation, but not developmental time. When the food supply is low, the optimal strategy adjusts the size at pupation downwards for stochastic as opposed to deterministic availability of food. The conclusions reinforce the need for life-history studies to consider state dependence and short-term variability in growth rates. (C) 2000 Academic Press.
14. Anderson, RA; Roitberg, BD. (1999) Modelling trade-offs between mortality and fitness associated with persistent blood feeding by mosquitoes.Ecology Letters 2: 98-105 Modelling trade-offs between mortality and fitness associated with persistent blood feeding by mosquitoes
blood feeding; fecundity; models; mortality; mosquitoes; trade-offs
Feeding persistence of mosquitoes (that tendency to attack again within a short period ii a first meal is incomplete) is a key determinant of feeding success (defined here as blood-meal volume), especially with regard to mosquitoes that attack defensive hosts. Mortality risk from the vertebrate host is one cost that may be expected to create a trade-off against increased fecundity from second and subsequent meals depending on the availability of blood sources and on the probability of survival until the next gonotrophic cycle. We initially used stochastic simulation models to examine potential trade-offs in fecundity and survival for persistent and nonpersistent lines of mosquitoes that acquire blood from potentially dangerous hosts. In these models, a given strategy, i.e. persistence or the lack thereof, was fixed for the lifetime of the mosquito. Persistent blood feeding paid off relative to nonpersistent mosquitoes when feeding-associated mortality was relatively low to moderate and when the probability of obtaining blood on a given attempt was relatively low. On the ether hand, the nonpersistent strategy tended to give relatively higher fecundity when the chances of obtaining blood were high. We also examined the implications of persistence as a feeding strategy for mosquitoes that could exhibit this behaviour in a flexible manner over their lifetime in response to state. We solved for optimal feeding behaviours with a stochastic dynamic programming model set up along similar lines to the simulation model. Results from this approach lend support to the idea that the threshold blood-meal size at which mosquitoes should continue to feed should change relative to the age of the mosquito. The modelling approaches used in this study identified important areas of future study for mosquito blood-feeding behaviour.
12. Bouskila, A; Robinson, ME; Roitberg, BD; Tenhumberg, B. (1998) Life-history decisions under predation risk: Importance of a game perspective.Evolutionary Ecology 12: 701-715 Life-history decisions under predation risk: Importance of a game perspective
development; frequency dependence; genetic algorithm; ontogenetic shifts; predation risk
We model ontogenetic shifts (e.g. in food or habitat use) during development under predation risk. We ask whether inclusion of slate and frequency dependence will provide new insights when compared with game-free life-history theory. We model a simple biological scenario in which a prey animal must switch from a low-predation, low-growth habitat to a high-predation, high-growth habitat, To assess the importance of frequency dependence, we compare the results of four scenarios of increasing complexity: (1) no predation; (2) constant predation; (3) frequency-dependent predation (predation risk diluted at high prey density), and (4) frequency-dependent predation as in (3) but with predators allowed to respond adaptively to prey behaviour. State dependence is included in all scenarios through initial size, assumed to be environmental. A genetic algorithm is used to search for optimal solutions to the scenarios. We find substantially different results in the four different scenarios and suggest a decision tree by which biological systems could be tested to ascertain which scenario is most applicable.
11. Hoffmeister, TS; Roitberg, BD. (1998) Evolution of signal persistence under predator exploitation.Ecoscience 5: 312-320 Evolution of signal persistence under predator exploitation
host marking pheromone; herbivore-parasitoid interaction; signal persistence; optimality model
We investigated the problem of the optimal persistence of a chemical signal as an evolutionary game between conspecifics when such signals can be exploited by natural enemies. We used a plant-herbivore-parasitoid system as a model to determine the optimal decay rate of a contact pheromone used by a herbivore to signal the presence of an herbivore's egg to the marking female and conspecifics. These pheromones are also exploited by a specialized parasitoid of the herbivore offspring. We used a series of models with increasing complexity to elucidate the optimal decay rates of marking pheromones. As long as the mark had no associated costs, the population evolved towards the lowest possible decay rates, independent of herbivore oviposition response towards marked sites. When marking behaviour had some associated cost, increasingly higher decay rates evolved with physiological cost of marking and increasing levels of parasitoid attack. However, the degree of change depended on competition for, and the probability of re-encounters with, exploited oviposition sites. Additionally, we tested the effect of the time of onset of parasitoid attack (representing early instar to late instar parasitoids) on the evolution of optimal decay rates and found decay rates to decrease in a non-linear fashion with increasing time lag between herbivore egg deposition and parasitoid attack. We discuss our findings with respect to chemical communication and signals in general that might be exploited by natural enemies, and stress the importance of an evolutionary ecological perspective towards an understanding of signal quality.
10. Robertson, IC; Robertson, WG; Roitberg, BD. (1998) A model of mutual tolerance and the origin of communal associations between unrelated females.Journal of Insect Behavior 11: 265-286 A model of mutual tolerance and the origin of communal associations between unrelated females
communal breeding; game theory; genetic algorithm; mutual tolerance; Nicrophorus; reproductive skew
We use a genetic algorithm model employing game theory to explore the ecological conditions favoring reproductive tolerance between two unrelated females that meet at a nesting site (i. e., breeding resource). Each female adopts one of three strategies: (I) fight for exclusive use of the nest, (2) tolerate the other female and breed communally: but fight back if attacked, or (3) leave in search of new breeding opportunities. Nests vary in the number of offspring they can support and their probability of failure due to discovery by competitors. The model predicts that communal associations are most likely to arise when (I) the benefits of nest sharing to females exceed the losses to individual reproduction, (2) additional nesting sires are rare, (3) females have limited clutch sizes, and (4) dominant females are able to skew reproduction in their favor. The amount of reproductive skew a dominant (larger) female can acquire while maintaining a communal association is predicted to increase when the asymmetry infighting ability between females increases, and at nests that have a relatively high probability of nesting success for solitary females. When the losers of fights can parasitize the winner's brood, dominant females must reduce reproductive skew to promote a communal relationship. We discuss the ability of our model to predict patterns of facultative communal behavior in burying beetles (Silphidae; Nicrophorus spp.), as well as the absence of communal behavior in dung beetles (Scarabaeidae).
9. Robertson, IC; Roitberg, BD. (1998) Duration of paternal care in pine engraver beetles: why do larger males care less?Behavioral Ecology and Sociobiology 43: 379-386 Duration of paternal care in pine engraver beetles: why do larger males care less?
Ips pini; marginal-value theorem; mate desertion; parental care; Scolytidae
Male pine engravers, Ips pini (Coleoptera: Scolytidae), assist their mates during reproduction by removing the debris that accumulates while females excavate oviposition tunnels in the phloem tissue of host tree bark. Although duration of paternal care and male reproductive success are positively correlated, large males leave their mates and brood sooner than small males. We address two hypotheses to explain the earlier departure of larger males from their breeding galleries: (1) females oviposit most rapidly when paired with large males, thereby reducing the length of time that paternal care increases male reproductive success, (2) larger males have better prospects for future reproduction, and thus leave their galleries in search of new breeding opportunities sooner than smaller males. Contrary to the first hypothesis, when females were paired either with large or small males, there was no effect of male size on their rate of oviposition. Consistent with the second hypothesis, males that initiated breeding galleries were larger than males from the general population. In addition, large males flew farther and faster on flight mills than small males, which may indicate that large males have an advantage in locating suitable breeding sites. Thus, we suggest chat large male pine engravers leave their galleries earlier than small males because large individuals have better prospects for future reproduction.
7. Hoffmeister, TS; Roitberg, BD. (1997) To mark the host or the patch: Decisions of a parasitoid searching for concealed host larvae.Evolutionary Ecology 11: 145-168 To mark the host or the patch: Decisions of a parasitoid searching for concealed host larvae
evolution; Halticoptera laevigata; host-marking pheromone; parasitoids; patch mark; Tephritidae
We found evidence for patch marking in the parasitic wasp Halticoptera laevigata (Hymenoptera: Pteromalidae) foraging for concealed hosts. Wasps attack larvae of the fruit fly Myoleja lucida (Diptera: Tephritidae) in fruits of honeysuckle. A special feature of this host-parasitoid system is the limited food supply of a patch (i.e. a fruit of honeysuckle), which allows the successful development of only a single host try larva. Females of the parasitoid H. laevigata were found to mark the host patch with a pheromone and to abandon the patch following oviposition into a single host larva. Field data revealed that eggs of the parasitoid were spread out evenly among infested patches, with several larvae of the host fly left unparasitized in those patches that contained more than one host. Since many parasitic insects mark the parasitized host after oviposition, we assumed host marking to be the ancestral character state and studied the patch-marking behaviour of H. laevigata as a derived character state as an alternative foraging strategy. We used stochastic dynamic modelling to investigate under what conditions mutant (patch) markers would be able to invade a population of normal (larval) markers. The models suggested that, under a variety of conditions, wasps marking the patch obtained higher fitness than wasps only marking the larva. Consequently, the results from our model predict the evolution of the patch-marking behaviour found in the empirical investigation. Finally, we discuss alternative pathways to the evolution of patch marking and point out under what circumstances the evolution of a patch-marking behaviour can generally be expected.
6. Li, C; Roitberg, BD; Mackauer, M. (1997) Effects of contact kairomone and experience on initial giving-up time.Entomologia Experimentalis et Applicata 84: 101-104 Effects of contact kairomone and experience on initial giving-up time
giving up time; patch residence time; kairomone; Aphelinus asychis; honeydew
5. Onyabe, DY; Roitberg, BD. (1997) The effect of conspecifics on oviposition site selection and oviposition behaviour in Aedes togoi (Theobold) (Diptera : Culicidae).Canadian Entomologist 129: 1173-1176 The effect of conspecifics on oviposition site selection and oviposition behaviour in Aedes togoi (Theobold) (Diptera : Culicidae)
Two opposing hypotheses are tested regarding the choice of oviposition sires by female Aedes togoi (Theobold) mosquitoes: (i) conspecific avoidance-females discriminate against sites harboring conspecifics to reduce intraspecific competition for their offspring and (ii) conspecific attraction-females prefer sites with conspecifics because their presence indicates suitable conditions for larvae. Under laboratory conditions, A. togoi females laid many more eggs on rearing water (LRW) containing conspecific larvae, their waste, bacteria, and food supplements than on rearing water alone (RM). In another experiment, females showed an oviposition preference for LRW sites that were devoid of A. togoi eggs compared with those harboring 50 (0.3 eggs/mL) conspecific eggs. Further, it was discovered that females laid their eggs at several sites rather than at a single suitable site. Possible reasons for such choices are discussed.
4. Onyabe, DY; Roitberg, BD; Friend, WG. (1997) Feeding and mating strategies in anopheles (Diptera : Culicidae): Theoretical modeling approach.Journal of Medical Entomology 34: 644-650 Feeding and mating strategies in anopheles (Diptera : Culicidae): Theoretical modeling approach
Anopheles; mating; simulation; reproductive strategies; mosquitoes; fitness
The effects of various ecological factors, such as the probability of finding mates and hosts and of successfully obtaining a blood meal, on the mating and feeding strategies of domestic female anopheline mosquitoes was investigated using theoretical models. The models calculated the mean fitness of 1,000 nonblood-fed, anautogenous, virgin anophelines. One model simulated females that always mate before blood feeding, whereas another simulated females that are able to feed opportunistically if a host was detected before they mated. The models demonstrated highest fitness for mosquitoes capable of opportunistic feeding under nearly all simulated conditions. This advantage increased as the probability of finding hosts and mates decreased as a function of host and mate availability.
3.Roitberg, BD; Mangel, M. (1997) Individuals on the landscape: behavior can mitigate landscape differences among habitats.Oikos 80: 234-240 Individuals on the landscape: behavior can mitigate landscape differences among habitats
We present a case study of the rose hip fly, Rhagoletis basiola, to demonstrate how one can connect landscape to population and evolutionary dynamics through the responses of individuals. Survey data from six different isolated rose habitats (Rosa sp.) near Vancouver, Canada were analyzed to determine the spatial distribution of rose hips within and among bushes. Rose hips were clumped at all sites; there was statistically significant variation in degree of clumping among sires. However, analyses using dynamic life history theory suggest that much of this variation may be mitigated by oviposition and movement response of individual flies to fruit distribution: sites that differ structurally may not differ evolutionarily. With this in mind, we provide five different indices that could be used to evaluate fly performance on different landscapes: 1) the probability that a cell r units away contains resource, given that the current cell contains resource, 2) the probability that a cell I units away contains resource, given that the current cell is de-void of resource. 3) the optimal distance to move from a cell that harbors Fruit, 4) the optimal distance to move ii om a cell that is devoid of fruit, and 5) the Expected Reproductive Success of a fly in a particular habitat. Those indices provide the link between landscape and individual behavior and suggest another way of addressing habitat conservation issues.
2. Carriere, Y; Roitberg, BD. (1996) Optimality modelling and quantitative genetics as alternatives to study the evolution of foraging behaviours in insect herbivores.Evolutionary Ecology 10: 289-305 Optimality modelling and quantitative genetics as alternatives to study the evolution of foraging behaviours in insect herbivores.
fitness function; gene flow; heterogeneous environments; host acceptance; host specificity; insect foraging behaviours; physiological state; rank order of preference
Although the evolution of large-scale dispersal has received considerable attention, we know very little about how natural selection influences foraging behaviours in herbivorous insects. Host-selection behaviours and within-habitat movements jointly determine foraging behaviours, since host selection affects the allocation of time spent on a particular host versus moving between these hosts. However, host selection is generally a labile trait, whose expression is influenced by the physiological state of the forager and hence, by characteristics of the habitat. We discuss how the quantitative genetic concepts can be used to study the evolution of such labile behaviours. Since host responses depend on the physiological state of the forager, it is argued that the state of the forager must be explicitly considered when estimating the additive genetic basis of host-selection behaviours. The lability of foraging behaviours increases the difficulty of measuring the fitness consequence of variation in the foraging phenotype in specific habitats, Therefore, it may be difficult to rely exclusively on quantitative genetic methods to test hypotheses about adaptive change in foraging behaviours across different habitats. We provide a novel approach based on optimality modelling to calculate the fitness consequence of variation in the foraging phenotype across different habitats. This method, in conjunction with quantitative genetics, can be used to test hypotheses concerning the evolution of foraging behaviours.
1. vanRanden, EJ; Roitberg, BD. (1996) The effect of egg load on superparasitism by the snowberry fly.Entomologia Experimentalis et Applicata 79: 241-245 The effect of egg load on superparasitism by the snowberry fly
egg load; adaptive superparasitism; Rhagoletis zephyria; host marking pheromone; snowberry
In studies conducted with fruits of the host plant, Symphoricarpus albus (L.), we examine the influence of egg load on the oviposition behaviour of Rhagoletis zephyria Snow (Diptera:Tephritidae). By altering the availability of exogenous protein, three classes of females with progressively increasing egg loads were produced, while keeping confounding factors such as age, experience, and mating status constant. Flies from all three classes were randomly presented with either a pheromone marked fruit, or with an unmarked fruit. Results indicate that increased egg load led to a greater propensity to accept, or superparasitize, the pheromone marked fruit. Upon dissection it was revealed that females which superparasitized had a mean egg load of 19.5 eggs (n=22), while females which rejected marked fruit had a mean egg load of 13.5 eggs (n=26). These results are consistent with the theory of adaptive superparasitism.
