Jay A. Rosenheim

Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population.

We evaluated the influence of intraguild predation among generalist insect predators on the suppression of an herbivore, the aphid Aphis gossypii, to test the appropriateness of the simple three trophic level model proposed by Hairston, Smith, and Slobodkin (1960). We manipulated components of the predator community, including three hemipteran predators and larvae of the predatory green lacewing Chrysoperla carnea, in field enclosure/exclosure experiments to address four questions: (1) Do generalist hemipteran predators feed on C. carnea? (2) Does intraguild predation (IGP) represent a substantial source of mortality for C. carnea? (3) Do predator species act in an independent, additive manner, or do significant interactions occur? (4) Can the experimental addition of some predators result in increased densities of aphids through a trophic cascade effect? Direct observations of predation in the field demonstrated that several generalist predators consume C. carnea and other carnivorous arthropods. Severely reduced survivorship of lacewing larvae in the presence of other predators showed that IGP was a major source of mortality. Decreased survival of lacewing larvae was primarily a result of predation rather than competition. IGP created significant interactions between the influences of lacewings and either Zelus renardii or Nabis predators on aphid population suppression. Despite the fact that the trophic web was too complex to delineate distinct trophic levels within the predatory arthropod community, some trophic links were sufficiently strong to produce cascades from higher-order carnivores to the level of herbivore population dynamics: experimental addition of either Z. renardii or Nabis predators generated sufficient lacewing larval mortality in one experiment to release aphid populations from regulation by lacewing predators. We conclude that intraguild predation in this system is wide-spread and has potentially important influences on the population dynamics of a key herbivore.

Egg load as a major source of variability in insect foraging and oviposition behavior

Foraging and oviposition behavior of insects directly influences offspring production and fitness, and is therefore particularly amenable to analysis with optimization models. These models have identified two general constraints on female fitness: host availability and egg complement. Research on insect oviposition has thus far focused on external, environmentally-derived cues such as host density and quality. Here we review recent studies and suggest that insects adjust their foraging and oviposition behavior in response to their perceived risk of becoming egg limited

Adult feeding and lifetime reproductive success in the parasitoid Aphytis melinus

The diet of adult females of the parasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae) includes host insects and sugar‐rich foods such as nectar and honeydew. We compared the contributions of host feeding to longevity and fecundity in A. melinus females in the presence and in the absence of honey meals. First, we assessed the longevity of females that were not allowed to oviposit. While the longevity of females fed honey was significantly increased by host feeding (median ages were 30.5 days for host‐fed females and 17 days for females not allowed to host feed), the lifespan of parasitoids not fed honey did not exceed 3 days for any individual and there was no effect of host feeding on longevity in this group. In the second set of experiments, we assessed the fecundity and longevity of females allowed to oviposit. We conducted two experiments, one in which honey was continuously available, and one in which honey was not available. In both experiments, daily observations were made of females that were either allowed to host feed or manually prevented from host feeding. In the presence of honey, host feeding significantly increased both fecundity and longevity, and in the absence of honey, parasitoids died within 2 days and host feeding had no significant effect on either fecundity or longevity. The lifetime fecundity of females fed honey but not hosts exceeded the initial egg complement by 60% on average. Approximately one host per day was used for host feeding whether honey was supplied or not, and each host‐feeding meal contributed approximately 3.9 eggs to the lifetime fecundity of honey‐fed females. In the last experiment, we compared the rate of egg resorption over a 36‐h period in A. melinus females that were deprived of hosts and either fed honey or starved. While no egg resorption was detected in honey‐fed females over this time period, starved females resorbed approximately 9 eggs. Thus, the availability of a sugar‐rich food interacts strongly with host feeding in influencing longevity and fecundity and has a strong direct effect on egg resorption.

Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis : distinguishing the influences of egg load and experience

(1) We used an experimental protocol that allowed us to distinguish the relative influences of egg load and experience with host contact on foraging behaviour and clutch size decisions in the gregarious parasitoid Aphytis lingnanensis Compere. Egg load was manipulated without concurrent changes in experience by exploiting sizerelated variation in fecundity and by holding parasitoids at different temperatures to vary the rate of egg production. (2) Egg load influenced the intensity of searching behaviour. Parasitoids with smaller egg loads required more time within a foraging arena to discover hosts. (3) Parasitoids with smaller egg loads and parasitoids with a prior experience with host contact deposited smaller clutches. (4) Total host handling time was inversely related to parasitoid egg load. Increased egg load had a similar accelerating influence on each of the component activities that comprise host handling, including preparation for oviposition, oviposition, and postoviposition grooming and resting. (5) The probability of successful parasitoid egg to adult development was independent of clutch size. Progeny size, however, decreased with increasing number of competing sibs. (6) A. lingnanensis clutch size decisions do not conform to the static expectations of a forager maximizing the fitness gained per egg, per host, or per unit time. Rather, clutch size decisions appeared to be fundamentally dynamic, responding to changes in parasitoid physiology (egg load) and the parasitoids perception of host availability (experience).

Intraguild interactions in aphid parasitoids

We reviewed the literature on aphid parasitoids to determine the occurrence, nature and outcome of intraguild interactions. Intraguild interactions were described for larval, pupal and adult aphid parasitoids and by the type of natural enemy (fungus, predator, or parasitoid). They appear to be prevalent in most aphid parasitoid systems and, except for parasitoid‐parasitoid interactions, they are mostly asymmetric, with aphidophagous predators and pathogens killing parasitoids. The limited experimental evidence from field studies is insufficient to provide a comprehensive pattern of the consequences of intraguild interactions for aphid parasitoid populations in general and, more specifically, for the efficacy of biological control. However, because intraguild interactions are widespread in aphid‐natural enemy communities and mostly detrimental to aphid parasitoids, we conclude that intraguild interactions have a primary effect in driving fluctuations in aphid parasitoid populations. Drawing on case studies, we further argue that intraguild interactions can substantially alter the effectiveness of aphid parasitoids as biological‐control agents.

Impact of a natural enemy overwintering refuge and its interaction with the surrounding landscape

1. Egg parasitoids in the genus Anagrus (Hymenoptera: Mymaridae) are important mortality factors for grape leafhoppers (Erythroneura elegantula; Homoptera: Cicadellidae) in California vineyards, yet must overwinter in habitats external to these vineyards. Existing evidence suggests that French prune trees, which harbour the overwintering host Edwardsiana prunicola, planted adjacent to vineyards may enhance early‐season abundance of Anagrus.

The influence of intraguild predation on prey suppression and prey release: a meta-analysis

Intraguild predation (IGP) occurs when one predator species consumes another predator species with whom it also competes for shared prey. One question of interest to ecologists is whether multiple predator species suppress prey populations more than a single predator species, and whether this result varies with the presence of IGP. We conducted a meta-analysis to examine this question, and others, regarding the effects of IGP on prey suppression. When predators can potentially consume one another (mutual IGP), prey suppression is greater in the presence of one predator species than in the presence of multiple predator species; however, this result was not found for assemblages with unidirectional or no IGP. With unidirectional IGP, intermediate predators were generally more effective than the top predator at suppressing the shared prey, in agreement with IGP theory. Adding a top predator to an assemblage generally caused prey to be released from predation, while adding an intermediate predator caused prey populations to be suppressed. However, the effects of adding a top or intermediate predator depended on the effectiveness of these predators when they were alone. Effects of IGP varied across different ecosystems (e.g., lentic, lotic, marine, terrestrial invertebrate, and terrestrial vertebrate), with the strongest patterns being driven by terrestrial invertebrates. Finally, although IGP theory is based on equilibrium conditions, data from short-term experiments can inform us about systems that are dominated by transient dynamics. Moreover, short-term experiments may be connected in some way to equilibrium models if the predator and prey densities used in experiments approximate the equilibrium densities in nature.

PREDATORS REDUCE PREY POPULATION GROWTH BY INDUCING CHANGES IN PREY BEHAVIOR

The ability of predators to reduce prey populations is generally ascribed to the consumption of prey individuals. However, predators may also induce behavioral chang- es in prey individuals, which can reduce prey survival and reproduction. Pea aphid pop- ulations are impacted by a variety of predators, many of which induce escape responses in individual aphids. We created disturbance-only predators (surgically manipulated pred- ators that were unable to consume prey, but were still able to forage and interact with prey) and measured their ability to suppress aphid population growth over a six-day period. The greatest reduction in aphid population growth was caused by normal predators that were able to both consume and disturb aphids, but aphid population growth was also strongly reduced by nonconsumptive, disturbance-only predators. These field experiments are the first to show that predators reduce prey population growth partly through predator-induced changes in prey behavior, as well as through consumption of prey individuals.

SEX RATIOS AND MULTIFACETED PARENTAL INVESTMENT

Although theories of parental investment and sex ratio generally assume that a single resource limits reproduction, many organisms invest two or more qualitatively different types of resources in the production of offspring. We examine the consequences of multifaceted parental investment for offspring provisioning and sex allocation, building our argument around a study of the nest-building Hymenoptera (wasps, bees, and ants). We review empirical studies that demonstrate that lifetime reproductive success may be constrained not only by resources used to provision offspring but also by the supply of mature oocytes or, in some cases, by the availability of space within nest sites or the time required to defend nests. Under multifaceted parental investment, the factor limiting parental fitness determines the currency of the optimization problem; parents are predicted to adjust reproductive behavior to maximize fitness returns per unit of the limiting resource. We develop simple models that predict that a greater availability of resources used for provisions will lead to an increase in the amount provisioned per offspring and an increase in the numerical or biomass proportion of females produced. These predictions explain widely observed patterns of variation in offspring provisioning and sex allocation in the nest-building Hymenoptera.

Predation on immature parasitoids and its impact on aphid suppression

Many predatory arthropods eat both unparasitized herbivores and herbivores that are parasitized and contain the immature stages of endoparasitoids, a form of intraguild predation. Thus, the biological control of herbivorous arthropods can be either enhanced or disrupted by introducing a predator species to an existing host-parasitoid system. We evaluate the impact of introducing a predator, the convergent ladybird beetle, Hippodamia convergens, on the biological control of the cotton aphid, Aphis gossypii, by the parasitoid Lysiphlebus testaceipes, under field conditions. Predation on immature parasitoids by H. convergens was intense: 98–100% of aphid mummies were consumed by the end of the experiment, and H. convergens substantially reduced immature parasitoid populations. Despite the negative impact of H. convergens on aphid parasitoids, aphid population suppression was greatest in treatments containing both H. convergens and parasitoids. The parasitoid alone or in combination with H. convergens suppressed cotton aphids in a density-dependent manner and increased total plant leaf area and biomass, H. convergens did not substantially alter the percentage of aphids mummified by parasitoids and showed a partial feeding preference for unparasitized aphids over aphid mummies. We conclude that under conditions where a predator shows both a partial preference for unparasitized hosts and high levels of predation on unparasitized hosts, we may expect the predator to improve suppression of herbivores even if it produces high levels of intraguild predation. While intraguild predation is an important ecological interaction in the early-season cotton agroecosystem, it does not disrupt cotton aphid biological control.