Daniel R. Papaj

Complex signal function: developing a framework of testable hypotheses

The basic building blocks of communication are signals, assembled in various sequences and combinations, and used in virtually all inter- and intra-specific interactions. While signal evolution has long been a focus of study, there has been a recent resurgence of interest and research in the complexity of animal displays. Much past research on signal evolution has focused on sensory specialists, or on single signals in isolation, but many animal displays involve complex signaling, or the combination of more than one signal or related component, often serially and overlapping, frequently across multiple sensory modalities. Here, we build a framework of functional hypotheses of complex signal evolution based on content-driven (ultimate) and efficacy-driven (proximate) selection pressures (sensu Guilford and Dawkins 1991). We point out key predictions for various hypotheses and discuss different approaches to uncovering complex signal function. We also differentiate a category of hypotheses based on inter-signal interactions. Throughout our review, we hope to make three points: (1) a complex signal is a functional unit upon which selection can act, (2) both content and efficacy-driven selection pressures must be considered when studying the evolution of complex signaling, and (3) individual signals or components do not necessarily contribute to complex signal function independently, but may interact in a functional way.

A variable-response model for parasitoid foraging behavior

An important factor inducing variability in foraging behavior in parasitic wasps is experience gained by the insect. Together with the insects genetic constitution and physiological state, experience ultimately defines the behavioral repertoire under specified environmental circumstances. We present a conceptual variable-response model based on several major observations of a foraging parasitoids responses to stimuli involved in the hostfinding process. These major observations are that (1) different stimuli evoke different responses or levels of response, (2) strong responses are less variable than weak ones, (3) learning can change response levels, (4) learning increases originally low responses more than originally high responses, and (5) hostderived stimuli serve as rewards in associative learning of other stimuli. The model specifies how the intrinsic variability of a response will depend on the magnitude of the response and predicts when and how learning will modify the insects behavior. Additional hypotheses related to the model concern how experience with a stimulus modifies behavioral responses to other stimuli, how animals respond in multistimulus situations, which stimuli act to reinforce behavioral responses to other stimuli in the learning process, and finally, how generalist and specialist species differ in their behavioral plasticity. We postulate that insight into behavioral variability in the foraging behavior of natural enemies may be a help, if not a prerequisite, for the efficient application of parasitoids in pest management.

Host marking behavior in phytophagous insects and parasitoids

Oviposition behavior in phytophagous insects and entomophagous parasitoids is often modified by the presence of conspecific brood (eggs and larvae). Often, females avoid laying eggs on or in hosts bearing brood, a behavior that acts to reduce the level of competition suffered by their offspring. Avoidance of occupied hosts is typically mediated by cues and/or signals associated with brood. In this article, we review the role of Marking Pheromones (MPs) as signals of brood presence in both phytophagous and entomophagous insects. We place information about the function and evolution of MPs in the context of recent theory in the field of animal communication. We highlight the dynamics of host‐marking systems and discuss how effects of MPs vary according to factors such as female experience and egg load. We also examine variation in the form and function of MP communication across a variety of insect taxa. While studies of MP communication in phytophagous insects have focused on the underlying behavioral mechanisms and chemistry of MP communication, studies in entomophagous insects have focused on the functional aspects of MPs and their role in ‘decision‐making’ in insects. We argue that an approach that incorporates the important contributions of both of these somewhat independent, but complementary areas of research will lead to a more complete understanding of MPs in insects. Finally, we suggest that MP systems are model systems for the study of animal signaling and its evolution.

Odor learning and foraging success in the parasitoid, Leptopilina heterotoma.

A brief 2-hr experience with hostDrosophila larvae in artificial apple-yeast or mushroom microhabitats had three effects on the foraging behavior of femaleLeptopilina heterotoma (Hymenoptera: Eucoilidae) parasitoids under field conditions. First, experienced females released at the center of circular arrays of apple-yeast and mushroom baits were more likely to find a microhabitat over the course of a daily census than naive ones. Second, for those females that found a microhabitat, experienced ones found it faster than naive ones (i.e., experience reduced travel times). Third, females experienced with a particular microhabitat were more likely to find that micro-habitat than an alternative one. Learned preferences were retained for at least one day and possibly as many as seven. Results generally did not depend on the host species (D. melanogaster orD. simulans) with which females were given experience. Females tended to arrive at baits upwind of the point of release, suggesting that odor is involved in finding host microhabitats and, in particular, in learning to find them more effectively. The implications of these results for the application of semiochemicals in biological control are discussed briefly.

Sex differences in movement between natural feeding and mating sites and tradeoffs between food consumption, mating success and predator evasion in Mediterranean fruit flies (diptera : tephritidae)

SummarySystematic quantitative observations of the location and diel pattern of adult Mediterranean fruit fly, Ceratitis capitata (Wiedemann), activities were carried out in an orange grove and surroundings on the island of Chios in Greece. Natural fly foods were assessed for their contribution to fly longevity, fecundity and fertility. There were diel shifts in male and female location. Females required a substantial and varied diet to realize peak fecundity. This diet was acquired away from the primary host, orange. Foraging for food throughout most of the day on fig and non-host foliage (including feeding on bird droppings) as well as on fig fruit and grapes, females dispersed and fed more than males. A diet of grapes alone did not support any fecundity, contributing only to longevity. A diet of figs alone, on the other hand, sustained both longevity and egg production. Bird feces alone supported neither egg production nor longevity. However, when added to a diet of figs, bird feces significantly increased fly fecundity. Throughout most of the day, males aggregated in leks within the inner canopy of the primary host, orange. The arrival here during the warmest hours of the day of receptive females, followed by pair formation, reinforced the lek mating system on host foliage. In the afternoon, females shifted to orange fruit where they suffered from high predation mortality while ovipositing. Soon after, males also shifted to orange fruit, where they attempted matings with non-receptive ovipositing females. Male feeding on fig fruit occurred late in the day, a time when they were least likely to find a mate. Male survival did not differ between the natural diets. Tradeoffs between food consumption, mating success and predator evasion are discussed for each sex and related to fruit fly mating systems.

Multimodal signals enhance decision making in foraging bumble-bees

Multimodal signals are common in nature and have recently attracted considerable attention. Despite this interest, their function is not well understood. We test the hypothesis that multimodal signals improve decision making in receivers by influencing the speed and the accuracy of their decisions. We trained bumble-bees (Bombus impatiens) to discriminate between artificial flowers that differed either in one modality, visual (specifically, shape) or olfactory, or in two modalities, visual plus olfactory. Bees trained on multimodal flowers learned the rewarding flowers faster than those trained on flowers that differed only in the visual modality and, in extinction trials, visited the previously rewarded flowers at a higher rate than bees trained on unimodal flowers. Overall, bees showed a speed–accuracy trade-off; bees that made slower decisions achieved higher accuracy levels. Foraging on multimodal flowers did not affect the slope of the speed–accuracy relationship, but resulted in a higher intercept, indicating that multimodal signals were associated with consistently higher accuracy across range of decision speeds. Our results suggest that bees make more effective decisions when flowers signal in more than one modality, and confirm the importance of studying signal components together rather than separately.

Peak shift discrimination learning as a mechanism of signal evolution

Abstract “Peak shift” is a behavioral response bias arising from discrimination learning in which animals display a directional, but limited, preference for or avoidance of unusual stimuli. Its hypothesized evolutionary relevance has been primarily in the realm of aposematic coloration and limited sexual dimorphism. Here, we develop a novel functional approach to peak shift, based on signal detection theory, which characterizes the response bias as arising from uncertainty about stimulus appearance, frequency, and quality. This approach allows the influence of peak shift to be generalized to the evolution of signals in a variety of domains and sensory modalities. The approach is illustrated with a bumblebee (Bombus impatiens) discrimination learning experiment. Bees exhibited peak shift while foraging in an artificial Batesian mimicry system. Changes in flower abundance, color distribution, and visitation reward induced bees to preferentially visit novel flower colors that reduced the risk of flower‐type misidentification. Under conditions of signal uncertainty, peak shift results in visitation to rarer, but more easily distinguished, morphological variants of rewarding species in preference to their average morphology. Peak shift is a common and taxonomically widespread phenomenon. This example of the possible role of peak shift in signal evolution can be generalized to other systems in which a signal receiver learns to make choices in situations in which signal variation is linked to the senders reproductive success.

Flower choice copying in bumblebees

We tested a hypothesis originating with Darwin that bees outside the nest exhibit social learning in flower choices. Naive bumblebees, Bombus impatiens, were allowed to observe trained bees or artificial bees forage from orange or green flowers. Subsequently, observers of bees on green flowers landed more often on green flowers than non-observing controls or observers of models on orange flowers. These results demonstrate that bumblebees can change flower choice by observations of non-nest mates, a novel form of social learning in insects that could provide unique benefits to the colony.

Phytochemical basis of learning inRhagoletis pomonella and other herbivorous insects

Examples of phytochemically-based learning of host preference in herbivorous insects are reviewed in the context of traditionally important issues: the number and kinds of chemicals involved; which sensory modalities are affected; whether peripheral or central nervous processing is altered; and whether learning is associative or not. A fifth issue addressed here— whether experience enhances a feeding or ovipositing insects propensity to accept familiar chemical stimuli or to reject novel chemical stimuli-has been ignored in previous studies. Following the review, evidence is presented indicating that female apple maggot flies (Ragoletis pomonella) learn to reject both novel physical and novel chemical stimuli.

Conditioning of leaf-shape discrimination by chemical cues in the butterfly, Battus philenor

Abstract In a large outdoor screened enclosure, female pipevine swallowtail butterflies ( Battus philenor ) were trained to search selectively for leaves of a shape similar to that of the Aristolochia host species to which they were exposed as adults. Conditioning was reversed by exposure to an alternative host species with a different leaf shape. Results indicated that contact with a host plant without oviposition was sufficient to induce a change in alighting responses to leaves of different shapes. Enclosure assays employing non-host species possessing leaves of different shapes and treated with host extracts demonstrated that females associate the shape of their alighting substrate with host chemicals present on the surface of that substrate. Results suggested that contact with host extracts without oviposition can induce changes in alighting responses to leaves of different shapes. A hypothesis is presented in which the primary host species for which females in an east Texas population learn to search varies seasonally with changes in host leaf chemistry.