Daniel R Papaj

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Chapters

• Leonard, A. S., Dornhaus, A. R., & Papaj, D. R. (2012). Why are floral signals complex? An outline of functional hypotheses. In EVOLUTION OF PLANT-POLLINATOR RELATIONSHIPS. Cambridge University Press.
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  S. Patiny, ed.

Journals/Publications

• Moore Brusca, W., Carriere, Y., Smith, R. L., Papaj, D. R., Davidowitz, G., & Schaller, J. (2018). Molecular phylogeny, ecology and multispecies aggregation behaviour of bombardier beetles in Arizona. PLoS ONE, 13(10), e0205192.
• Papaj, D. R., Davidowitz, G., Eran, L., & Nielsen, M. E. (2018). Color alters thermoregulatory behavior in Battus philenor caterpillars by modifying the cue received. Animal Behavior, 140, 93-98.
• Bronstein, J., Papaj, D. R., Alarcon, R., Davidowitz, G., & Smith, G. P. (2020). Sex differences in the foraging behavior of a generalist hawkmoth. Oecologia.
• Dunlap, A. S., Nielsen, M. E., Dornhaus, A. R., & Papaj, D. R. (2016). Foraging bumble bees weigh the reliability of personal and social information. CURRENT BIOLOGY.
• Mitra, C., Davidowitz, G., & Papaj, D. R. (2016). Fitness effects of male salt puddling. Ecological Entomology.
• Mitra, C., Reynoso, E., Davidowitz, G., & Papaj, D. R. (2015). Passing the salt: Effects of salt puddling on reproductive and flight behaviour of a swallowtail butterfly. ANIMAL BEHAVIOUR.
• Muth, F., Papaj, D. R., & Leonard, A. S. (2016). Multiple floral rewards have asymmetric effects on bee learning. FUNCTIONAL ECOLOGY.
• Nielsen, M. E., & Papaj, D. R. (2016). Why have multiple plastic responses? Interactions between color change and thermoregulatory behavior in Battus philenor larvae. THE AMERICAN NATURALIST.
• Papaj, D. R., Leonard, A. S., Gillette, H., & Russell, A. L. (2016). Concealed floral rewards and the role of experience in floral sonication by bees. ANIMAL BEHAVIOUR.
• Russell, A. L., & Papaj, D. R. (2016). Artificial pollen dispensing flowers and feeders for bee behaviour experiments. JOURNAL OF POLLINATION ECOLOGY.
• Russell, A. L., Newman, C. R., & Papaj, D. R. (2016). White flowers finish last: Pollen-foraging bumble bees show biased learning in a floral color polymorphism. EVOLUTIONARY ECOLOGY.
• Schaller, J., Davidowitz, G., Papaj, D. R., Smith, R. L., Carriere, Y., & Moore Brusca, W. (2018). Multispecies aggregation behavior and molecular phylogeny of bombardier beetles Brachinus WEBER (Carabidae: Brachininae). In prep for Proceedings of the National Academy of Sciences.
• Francis, J., Muth, F., Papaj, D., & Leonard, A. (2016). Nutritional complexity and the structure of bee foraging bouts. BEHAVIORAL ECOLOGY. doi:doi:10.1093/beheco/arv229
• Mitra, C., Reynoso, E., Davidowitz, G., & Papaj, D. R. (2016). Effects of sodium-puddling on male mating success, courtship, and flight in a swallowtail butterfly. Animal Behavior, 114, 203-210.
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  Mitra, C., E. Reynoso, G. Davidowitz, D. Papaj. (2015). Effects of sodium-puddling on male mating success, courtship, and flight in a swallowtail butterfly. Animal Behavior (in press).
• Muth, F., Papaj, D. R., & Leonard, A. (2016). Bees remember flowers for more than one reason: pollen mediates associative learning. ANIMAL BEHAVIOUR, 111, 93-100.
• Davis, J. M., Coogan, L. E., & Papaj, D. R. (2015). Big maggots dig deeper: size-dependent larval dispersal in flies. OECOLOGIA, 179(1), 55-62.
• Essenberg, C. J., Easter, R. A., Simmons, R. A., & Papaj, D. R. (2015). The value of information in floral cues: bumblebee learning of floral size cues. BEHAVIORAL ECOLOGY, 26(5), 1335-1344.
• Kandori, I., Tsuchihara, K., Suzuki, T. A., Yokoi, T., & Papaj, D. R. (2015). Long frontal projections help Battus philenor (Lepidoptera: Papilionidae) larvae find host plants. PLOS ONE, 10(7).
• Muth, F., Papaj, D. R., & Leonard, A. S. (2015). Colour learning when foraging for nectar and pollen: bees learn two colours at once. BIOLOGY LETTERS, 11, 20150628.
• Nielsen, M. E., & Papaj, D. R. (2015). Effects of developmental change in body size on ectotherm body temperature and behavioral thermoregulation: caterpillars in a heat-stressed environment. OECOLOGIA, 177(1), 171-179.
• Papaj, D. R. (2015). Bees learn preferences for plant species that offer only pollen as a reward. BEHAVIORAL ECOLOGY. doi:doi:10.1093/beheco/arv213
• Jones, B. M., Leonard, A. S., Papaj, D. R., & Gronenberg, W. (2013). Plasticity of the worker bumblebee brain in relation to age and rearing environment. BRAIN, BEHAVIOR AND EVOLUTION, 82, 250-261. doi:doi: 10.1159/000355845
• Leonard, A. S., Brent, J., Papaj, D. R., & Dornhaus, A. (2013). Floral nectar guide patterns discourage nectar robbing by bumble bees. PLOS ONE, 8(2), e55914.
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  featured in PLoS Author SpotlightPMID: 23418475;PMCID: PMC3572167;Abstract: Floral displays are under selection to both attract pollinators and deter antagonists. Here we show that a common floral trait, a nectar guide pattern, alters the behavior of bees that can act opportunistically as both pollinators and as antagonists. Generally, bees access nectar via the floral limb, transporting pollen through contact with the plant's reproductive structures; however bees sometimes extract nectar from a hole in the side of the flower that they or other floral visitors create. This behavior is called "nectar robbing" because bees may acquire the nectar without transporting pollen. We asked whether the presence of a symmetric floral nectar guide pattern on artificial flowers affected bumble bees' (Bombus impatiens) propensity to rob or access nectar "legitimately." We discovered that nectar guides made legitimate visits more efficient for bees than robbing, and increased the relative frequency of legitimate visits, compared to flowers lacking nectar guides. This study is the first to show that beyond speeding nectar discovery, a nectar guide pattern can influence bees' flower handling in a way that could benefit the plant. © 2013 Leonard et al.
• Snell-Rood, E. C., Davidowitz, G., & Papaj, D. R. (2013). Plasticity in learning causes immediate and trans-generational changes in allocation of resources. INTEGRATIVE AND COMPARATIVE BIOLOGY, 53(2), 329-339.
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  PMID: 23624867;Abstract: Plasticity in the development and expression of behavior may allow organisms to cope with novel and rapidly changing environments. However, plasticity itself may depend on the developmental experiences of an individual. For instance, individuals reared in complex, enriched environments develop enhanced cognitive abilities as a result of increased synaptic connections and neurogenesis. This suggests that costs associated with behavioral plasticity - in particular, increased investment in "self" at the expense of reproduction - may also be flexible. Using butterflies as a system, this work tests whether allocation of resources changes as a result of experiences in "difficult" environments that require more investment in learning. We contrast allocation of resources among butterflies with experience in environments that vary in the need for learning. Butterflies with experience searching for novel (i.e., red) hosts, or searching in complex non-host environments, allocate more resources (protein and carbohydrate reserves) to their own flight muscle. In addition, butterflies with experience in these more difficult environments allocate more resources per individual offspring (i.e., egg size and/or lipid reserves). This results in a mother's experience having significant effects on the growth of her offspring (i.e., dry mass and wing length). A separate study showed this re-allocation of resources comes at the expense of lifetime fecundity. These results suggest that investment in learning, and associated changes in life history, can be adjusted depending on an individual's current need, and their offspring's future needs, for learning. © The Author 2013.
• Kaczorowski, R. L., Leonard, A. S., Dornhaus, A., & Papaj, D. R. (2012). Floral signal complexity as a possible adaptation to environmental variability: A test using nectar-foraging bumblebees, Bombus impatiens. ANIMAL BEHAVIOUR, 83(4), 905-913.
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  Abstract: Floral signals are typically emitted across multiple sensory modalities, although why they are multimodal is unclear. One possible explanation is that multimodal signalling ensures that at least one signal component will be transmitted effectively under varying environmental conditions (the 'efficacy backup' hypothesis). For example, by transmitting both component A and B, a signaller can communicate under environmental conditions where transmission of component A is reduced; component B 'backs up' A. To test this hypothesis, we determined whether a floral scent could back up a floral colour signal when light levels were low. We trained nectar-foraging bumblebees to discriminate rewarding and unrewarding targets that differed in colour, scent, or both colour and scent, and then presented the targets at different levels of illumination. We measured bees' accuracy at distinguishing the two targets and their rate of visits to the trained target. Performance on both measures declined under low light when targets were unscented. The presence of scent reduced the loss of accuracy under low light, supporting the efficacy backup hypothesis, but this effect depended upon the colour of the previously rewarded target. In contrast, the presence of scent did not affect the overall rate of correct visits under low light (correct visits/foraging time). A backup mechanism that maintains accuracy, but not rate of nectar collection, does not necessarily benefit the pollinator. However, it most likely benefits the plant through reduced pollen wastage. In short, multimodal floral signals may benefit the plant by improving pollen transfer, while not benefiting the pollinator. © 2012 The Association for the Study of Animal Behaviour.
• Nufio, C. R., & Papaj, D. R. (2012). Aggregative behavior is not explained by an Allee effect in the walnut infesting fly, Rhagoletis juglandis. JOURNAL OF INSECT BEHAVIOR, 25(2), 166-182.
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  Abstract: Component Allee effects are considered to be a driving force in the origin and maintenance of aggregative behavior. In this study, we examine whether a pattern of active host reuse by the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), involves an Allee effect. We examined how the density of clutches deposited within a fruit, the temporal pattern in which successive clutches are deposited and the spatial distribution of clutches over a fruit's surface influences survival to pupation and pupal size. Within the density range used in this experiment (1 to 7 clutches), increases in larval density strongly reduced pupal weight but not larval survival to pupation. The temporal staggering of clutches into a host strongly reduced offspring survival and, probably owing to competitive release, increased the pupal weight of survivors. Offspring survival and pupal weight were affected relatively little by whether two clutches were deposited within the same oviposition punctures or were evenly spaced. In contrast, in three-clutch treatments offspring survival was higher when clutches were placed within the same oviposition cavity. However, pupal weights did not significantly increase when clutches were placed together and this relatively higher survival rate was not greater than that associated with hosts that contained fewer clutches. The results of the study failed to provide evidence of an Allee effect. We put forward a scenario under which females appear to reuse larval hosts to maximize their own reproductive success, albeit at the expense of the per capita fitness of their offspring. © 2011 Springer Science+Business Media, LLC.
• Papaj, D. R. (2012). Review: An Introduction to Animal Behaviour: An Integrative Approach, by Michael J. Ryan and Walter Wilczynski. ANIMAL BEHAVIOUR, 83, 905-913.
• Davis, J. M., Nufio, C. R., & Papaj, D. R. (2011). Resource quality or competition: Why increase resource acceptance in the presence of conspecifics?. BEHAVIORAL ECOLOGY, 22(4), 730-737.
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  Abstract: Some animal species increase resource acceptance rates in the presence of conspecifics. Such responses may be adaptive if the presence of conspecifics is a reliable indicator of resource quality. Similarly, these responses could represent an adaptive reduction in choosiness under high levels of scramble competition. Although high resource quality and high levels of scramble competition should both favor increased resource acceptance, the contexts in which the increase occurs should differ. In this paper, we tested the effect of social environment on egg-laying and aggressive behavior in the walnut fly, Rhagoletis juglandis, in multiple contexts to determine whether increased resource acceptance in the presence of conspecifics was better viewed as a response to increased host quality or increased competition. We found that grouped females oviposit more readily than isolated females when provided small (low-quality) artificial hosts but not when provided large (high-quality) artificial hosts, indicating that conspecific presence reduces choosiness. Increased resource acceptance was observed even when exposure to conspecifics was temporally or spatially separate from exposure to the resource. Finally, we found that individuals showed reduced aggression after being housed in groups, as expected under high levels of scramble competition. These results indicate that the pattern of resource acceptance in the presence of conspecifics may be better viewed as a response to increased scramble competition rather than as a response to public information about resource quality. © 2011 The Author.
• Leonard, A. S., & Papaj, D. R. (2011). 'X' marks the spot: The possible benefits of nectar guides to bees and plants. FUNCTIONAL ECOLOGY, 25(6), 1293-1301.
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  Abstract: 1.Many floral displays are visually complex, transmitting multi-coloured patterns that are thought to direct pollinators to nectar rewards. These 'nectar guides' may be mutually beneficial, if they reduce pollinators' handling time, leading to an increased visitation rate and promoting pollen transfer. Yet, many details regarding how floral patterns influence foraging efficiency are unknown, as is the potential for pollinator learning to alter this relationship. 2.We compared the responses of bumblebee (Bombus impatiens Cresson) foragers to artificial flowers that either possessed or lacked star-like patterns. By presenting each bee with two different foraging scenarios (patterned flowers rewarding/plain flowers unrewarding, plain flowers rewarding/patterned flowers unrewarding) on different days, we were able to assess both short- and long-term effects of patterns on bee foraging behaviour. 3.Bees discovered rewards more quickly on patterned flowers and were less likely to miss the reward, regardless of whether corollas were circular or had petals. Nectar guides' effect on nectar discovery was immediate (innate) and persisted even after experience, although nectar discovery itself also had a learned component. We also found that bees departed patterned flowers sooner after feeding. Finally, when conditions changed such that flowers no longer provided a reward, bees visited the now-unrewarding flowers more persistently when they were patterned. 4.On the time-scale of a single foraging bout, our results provide some of the first data on how pollinators learn to forage efficiently using this common floral trait. Our bees' persistent response to patterned flowers even after rewards ceased suggests that, rather than being consistently mutually beneficial to plant and pollinator, nectar guide patterns can at times promote pollen transfer for the plant at the expense of a bee's foraging success. © 2011 The Authors. Functional Ecology © 2011 British Ecological Society.
• Leonard, A. S., Dornhaus, A., & Papaj, D. R. (2011). Flowers help bees cope with uncertainty: signal detection and the function of floral complexity. THE JOURNAL OF EXPERIMENTAL BIOLOGY, 214, 113-121.
• Leonard, A. S., Dornhaus, A., & Papaj, D. R. (2011). Forget-me-not: Complex floral displays, inter-signal interactions, and pollinator cognition. CURRENT ZOOLOGY, 57(2), 215-224.
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  Abstract: Flowers are multisensory displays used by plants to influence the behavior of pollinators. Although we know a great deal about how individual signal components are produced by plants and detected or learned by pollinators, very few experiments directly address the function of floral signal complexity, i.e. how the multicomponent nature of these signals benefits plant or pollinator. Yet, experimental psychology suggests that increasing complexity can enhance subjects' ability to detect, learn and remember stimuli, and the plant's reproductive success depends upon ensuring that pollinators learn their signals and so transport pollen to other similar (conspecific) flowers. Here we explore functional hypotheses for why plants invest in complex floral displays, focusing on hypotheses in which floral signals interact to promote pollinator learning and memory. Specifically, we discuss how an attention-altering or context-providing function of one signal may promote acquisition or recall of a second signal. Although we focus on communication between plants and pollinators, these process-based hypotheses should apply to any situation where a sender benefits from enhancing a receiver's acquisition or recall of information. © 2011 Current Zoology.
• Marek, P., Papaj, D., Yeager, J., Molina, S., & Moore, W. (2011). Bioluminescent aposematism in millipedes. CURRENT BIOLOGY, 21, R680-R681.
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  PMID: 21959150;PMCID: PMC3221455;Abstract: Bioluminescence - the ability of organisms to emit light - has evolved about 40-50 times independently across the tree of life [1]. Many different functions for bioluminescence have been proposed, for example, mate recognition, prey attraction, camouflage, and warning coloration. Millipedes in the genus Motyxia produce a greenish-blue light at a wavelength of 495 nm that can be seen in darkness [2]. These detritivores defend themselves with cyanide, which they generate internally and discharge through lateral ozopores [3]. Motyxia are an ideal model system to investigate the ecological role of bioluminescence because they are blind, thus limiting their visual signalling to other organisms, for example predators. While the biochemical mechanisms underlying Motyxia bioluminescence have been studied in detail [2,4], its adaptive significance remained unknown [5,6]. We here show that bioluminescence has a single evolutionary origin in millipedes and it serves as an aposematic warning signal to deter nocturnal mammalian predators. Among the numerous examples of bioluminescence, this is the first field experiment in any organism to demonstrate that bioluminescence functions as a warning signal. Video Abstract: The editors of Current Biology welcome correspondence on any article in the journal, but reserve the right to reduce the length of any letter to be published. All Correspondence containing data or scientific argument will be refereed. Queries about articles for consideration in this format should be sent by e-mail to cbiol@current-biology.com © 2011 Elsevier Ltd. All rights reserved.
• Snell-Rood, E. C., Davidowitz, G., & Papaj, D. R. (2011). Reproductive tradeoffs of learning in a butterfly. BEHAVIORAL ECOLOGY, 22(2), 291-302.
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  Abstract: The evolution of learning has long been hypothesized to be limited by fitness trade-offs such as delays in reproduction. We explored the relationship between host learning and reproduction in the cabbage white butterfly, Pieris rapae. The cabbage white female is innately biased to search for common green hosts but can learn to search for rare red hosts. Host learning was shown previously to vary among full-sibling families and to incur costs in terms of host search efficiency and brain size. In the present study, we show that butterflies from full-sib families with relatively better learning performance on red hosts tend to emerge as adults with relatively fewer and less-developed eggs. We also used methoprene, a juvenile hormone mimic, to advance reproduction in female cabbage whites. We found that methoprene-treated butterflies improved host-finding ability less with experience, relative to controls, providing independent evidence of a link between learning and timing of reproduction. Finally, we show that the learning experience itself is associated with additional decreases in lifetime fecundity. These results support a range of theoretical and comparative studies highlighting the importance of fitness tradeoffs in the evolution of learning and cognition. © 2011 The Author.
• Carsten-Conner, L. D., Papaj, D. R., & O'Brien, D. M. (2010). Resource allocation to testes in walnut flies and implications for reproductive strategy. Journal of Insect Physiology, 56(11), 1523-1529.
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  PMID: 20451528;Abstract: Testes size often predicts the winner during episodes of sperm competition. However, little is known about the source of nutrients allocated to testes development, or testes plasticity under varying nutrient availability. Among many holometabolous insects, metabolic resources can derive from the larval or adult diet. Distinguishing the source of nutrients allocated to testes can shed light on life history factors (such as maternal influences) that shape the evolution of male reproductive strategies. Here we used an experimental approach to assess resource allocation to testes development in walnut flies (Rhagoletis juglandis) from differing nutritional backgrounds. We fed adult male walnut flies on sugar and yeast diets that contrasted with the larval diet in carbon and nitrogen stable isotope ratios. This design allowed us to assess the dietary source of testes carbon and nitrogen and its change over time. We found significant incorporation of adult dietary carbon into testes, implying that walnut flies are income breeders for carbon (relying more on adult resources). In contrast, we found little evidence that walnut flies incorporate adult dietary nitrogen into testes development. We discuss the implications of these allocation decisions for life history evolution in this species. © 2010 Elsevier Ltd.
• Papaj, D. R. (2009). Learning. Encyclopedia of Insects, 552-555.
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  Abstract: This chapter focuses on the learning process of insects. Learning involves an enduring change in behavior with experience, the change usually progressing gradually with continued experience to some asymptote. Learned behavior is often modified by novel experiences, and effects of experience eventually wane if not reinforced. Learning can be categorized as nonassociative or associative. Nonassociative learning includes habituation and sensitization. Habituation involves the waning of a response to a stimulus upon repeated presentation of that stimulus. Associative learning involves pairing a stimulus with another stimulus, or with a motor pattern, such that the response to the first stimulus is altered as a consequence of the pairing. Associative learning is typically evaluated in two kinds of paradigms: classical, Pavlovian, conditioning, and instrumental conditioning. Additionally, in a sense, the function of associative learning is obvious. Animals learn by association to orient toward stimuli predicting positively rewarding resources such as sugar, pollen, food plants, hosts, and away from stimuli predicting negatively rewarding events, shock, heat, toxins, predators. Likewise, habituation is a means for reducing energy-wasteful, time-consuming responses to meaningless stimuli. In either case, however, learning is needed only if the appropriate responses cannot be predicted without benefit of experience, else an insect could respond (or not respond) innately. © 2009 Elsevier Inc. All rights reserved.
• Peterson, B. K., Hare, E., Iyer, V. N., Storage, S., Conner, L., Papaj, D. R., Kurashima, R., Jang, E., & Eisen, M. B. (2009). Big genomes facilitate the comparative identification of regulatory elements. PLoS ONE, 4(3), e4688.
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  PMID: 19259274;PMCID: PMC2650094;Abstract: The identification of regulatory sequences in animal genomes remains a significant challenge. Comparative genomic methods that use patterns of evolutionary conservation to identify non-coding sequences with regulatory function have yielded many new vertebrate enhancers. However, these methods have not contributed significantly to the identification of regulatory sequences in sequenced invertebrate taxa. We demonstrate here that this differential success, which is often attributed to fundamental differences in the nature of vertebrate and invertebrate regulatory sequences, is instead primarily a product of the relatively small size of sequenced invertebrate genomes. We sequenced and compared loci involved in early embryonic patterning from four species of true fruit flies (family Tephritidae) that have genomes four to six times larger than those of Drosophila melanogaster. Unlike in Drosophila, where virtually all non-coding DNA is highly conserved, blocks of conserved non-coding sequence in tephritids are flanked by large stretches of poorly conserved sequence, similar to what is observed in vertebrate genomes. We tested the activities of nine conserved non-coding sequences flanking the even-skipped gene of the teprhitid Ceratis capitata in transgenic D. melanogaster embryos, six of which drove patterns that recapitulate those of known D. melanogaster enhancers. In contrast, none of the three non-conserved tephritid non-coding sequences that we tested drove expression in D. melanogaster embryos. Based on the landscape of non-coding conservation in tephritids, and our initial success in using conservation in tephritids to identify D. melanogaster regulatory sequences, we suggest that comparison of tephritid genomes may provide a systematic means to annotate the non-coding portion of the D. melanogaster genome. We also propose that large genomes be given more consideration in the selection of species for comparative genomics projects, to provide increased power to detect functional non-coding DNAs and to provide a less biased view of the evolution and function of animal genomes.
• Roitberg, B. D., Lauzon, C. R., Opp, S. B., & Papaj, D. R. (2009). Functional and behavioural ecology of tree-fruit pests: The four Fs of fruit flies (Diptera: Tephritidae). Biorational Tree Fruit Pest Management, 56-84.
• Snell-Rood, E. C., & Papaj, D. R. (2009). Patterns of phenotypic plasticity in common and rare environments: a study of host use and color learning in the cabbage white butterfly Pieris rapae. American Naturalist, 173(5), 615-631.
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  PMID: 19302028;Abstract: Phenotypic Plasticity is Adaptive in Variable Environments But, Given Its Costs, May be Disfavored if only One Environ. is Commonly Encountered. Yet Species in Relatively Constant Environments Often Adjust Phenotypes Successfully in Rare or Novel Environments. Devmtl. Biases May Reduce the Costs of Plasticity in Com. Environments, Favoring the Maintenance of Plasticity. We Explored This Proposition by Studying the Flexibility of Visually Guided Host-Sel. Behav. in Cabbage White Butterflies (Vieris Rapae), Wherein Com. and Rare Environments Consisted of Gn. and Red Host Types, Respectively. We Demonstrated in Greenhouse Assays That Adult Females Display an Innate Bias Toward Gn. Color during Host Search but Alter That Bias Through Lrng. in Red-host Assemblages Such That, after Several Hours of Experience, Red Hosts Are Located as Efficiently as Gn. Hosts. Full-sib Analyses Suggested There Was Genetic Variation in Host and Color Choice That Was More Pronounced in the Red-host Environ.. We Found no Evidence of Genetic Correlations in Behav. Across Host Environments or of Fitness Costs of Plasticity in Color Choice. Our Results Support the Idea That Lrng. May Persist in Less Variable Environments Through the Evol. of Innate Biases That Reduce Operating Costs in Com. Environments. 2009 by the Univ. of Chicago.
• Snell-Rood, E. C., & Papaj, D. R. (2009). Patterns of phenotypic plasticity in common and rare environments: a study of host use and color learning in the cabbage white butterfly Pieris rapae. The American Naturalist, 173(5), 615–631.
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  Phenotypic plasticity is adaptive in variable environments but, given its costs, may be disfavored if only one environment is commonly encountered. Yet species in relatively constant environments often adjust phenotypes successfully in rare or novel environments. Developmental biases may reduce the costs of plasticity in common environments, favoring the maintenance of plasticity. We explored this proposition by studying the flexibility of visually guided host-selection behavior in cabbage white butterflies (Pieris rapae), wherein common and rare environments consisted of green and red host types, respectively. We demonstrated in greenhouse assays that adult females display an innate bias toward green color during host search but alter that bias through learning in red-host assemblages such that, after several hours of experience, red hosts are located as efficiently as green hosts. Full-sib analyses suggested there was genetic variation in host and color choice that was more pronounced in the red-host environment. We found no evidence of genetic correlations in behavior across host environments or of fitness costs of plasticity in color choice. Our results support the idea that learning may persist in less variable environments through the evolution of innate biases that reduce operating costs in common environments.
• Snell-Rood, E. C., Papaj, D. R., & Gronenberg, W. (2009). Brain size: A global or induced cost of learning?. Brain, Behavior and Evolution, 73(2), 111-128.
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  PMID: 19390176;Abstract: The role of brain size as a cost of learning remains enigmatic; the nature and timing of such costs is particularly uncertain. On one hand, comparative studies suggest that congenitally large brains promote better learning and memory. In that case, brain size exacts a global cost that accrues even if learning does not take place; on the other hand, some developmental studies suggest that brains grow with experience, indicating a cost that is induced when learning occurs. The issue of how costs are incurred is an important one, because global costs are expected to constrain the evolution of learning more than would induced costs. We tested whether brain size represented a global and/or an induced cost of learning in the cabbage white butterfly, Pieris rapae. We assayed the ability of full sibling families to learn to locate either green hosts, for which butterflies have an innate search bias, or red hosts, which are more difficult to learn to locate. Naïve butterflies were sacrificed at emergence and congenital brain volume estimated as a measure of global costs; experienced butterflies were sacrificed after learning and change in brain volume estimated as a measure of induced costs. Only for the mushroom body, a brain region involved in learning and memory in other insects, was volume at emergence related to learning or host-finding. Butterfly families that emerged with relatively larger mushroom bodies showed a greater tendency to improve their ability to find red hosts across the two days of host-search. The volume of most brain regions increased with time in a manner suggesting host experience itself was important: first, total number of landings during host-search was positively related to mushroom body calyx volume, and, second, experience with the red host was positively related to mushroom body lobe volume. At the family level, the relative volume of the mushroom body calyx and antennal lobes following learning was positively related to overall success in finding red hosts. Overall, our results suggest that within species, brain size might act as a small global cost of learning, but that environment-specific changes in brain size might reduce the overall costs of neural tissue in the evolution of learning. Copyright © 2009 S. Karger AG, Basel.
• Kulahci, I. G., Dornhaus, A., & Papaj, D. R. (2008). Multimodal signals enhance decision making in foraging bumble-bees. Proceedings of the Royal Society B: Biological Sciences, 275(1636), 797-802.
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  PMID: 18198150;PMCID: PMC2596894;Abstract: 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. © 2008 The Royal Society.
• Kulahci, I. G., Dornhaus, A., & Papaj, D. R. (2008). Multimodal signals enhance decision making in foraging bumble-bees. Proceedings of the Royal Society of London, Series B, 275(1636), 797–802.
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  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.
• Kulahci, I. G., Dornhaus, A., & Papaj, D. R. (2008). Multimodal signals enhance decision-making in foraging bumble-bees. Proceedings of the Royal Society B: Biological Sciences, 275, 797-802.
• Papaj, D. R., & Snell-Rood, E. C. (2007). Memory flies sooner from flies that learn faster. Proceedings of the National Academy of Sciences of the United States of America, 104(34), 13539-13540.
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  PMID: 17699627;PMCID: PMC1959415;
• Papaj, D. R., Mallory, H. S., & Heinz, C. A. (2007). Extreme weather change and the dynamics of oviposition behavior in the pipevine swallowtail, Battus philenor. Oecologia, 152(2), 365-375.
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  PMID: 17277928;Abstract: Prospects of global increases in extreme weather change provide incentive to examine how such change influences animal behavior, for example, behavior associated with resource use. In this study, we examined how oviposition behavior in a southern Arizona population of pipevine swallowtails (Battus philenor L.) responded to changes in their Aristolochia host resource and vegetative background caused by the North American monsoon system. Summer monsoon rains resulted in a flush of non-host vegetation and a more than doubling in rate of landings by host-searching females on non-host vegetation. Rates of discovery of the host species A. watsoni Woot. Standl. decreased by 50% after monsoon rains. Rains did not alter host density appreciably, but resulted in significant increases in host plant size and new growth, two indicators of host suitability for B. philenor larvae. After the rains, mean clutch size on individual host plants increased by a factor of 2.5; the mean proportion of host plants encountered on which a female laid eggs also increased significantly. Females were discriminating about the host plants on which they laid eggs after alightment; plants accepted for oviposition were larger, bore more new growth, and bore fewer larvae than rejected plants. Contrary to predictions from foraging theory, degree of discrimination did not change seasonally. Finally, the rate at which eggs were laid increased seasonally, suggesting that oviposition rates were limited more before monsoon rains by the relatively low quality of hosts than they were after the rains by the relatively low rate at which hosts were found. This latter result suggests that, while butterflies possess behavioral flexibility to respond to extreme weather change, such flexibility may have limits. In particular, expected increases in the severity and frequency of droughts may result in reduced oviposition rates, reductions that could have adverse demographic consequences. © 2007 Springer-Verlag.
• Prudic, K. L., Skemp, A. K., & Papaj, D. R. (2007). Aposematic coloration, luminance contrast, and the benefits of conspicuousness. Behavioral Ecology, 18(1), 41-46.
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  Abstract: Many organisms use warning, or aposematic, coloration to signal their unprofitability to potential predators. Aposematically colored prey are highly visually conspicuous. There is considerable empirical support that conspicuousness promotes the effectiveness of the aposematic signal. From these experiments, it is well documented that conspicuous, unprofitable prey are detected sooner and aversion learned faster by the predator as compared with cryptic, unprofitable prey. Predators also retain memory of the aversion longer when prey is conspicuous. The present study focused on the elements of conspicuousness that confer these benefits of aposematic coloration. Drawing on current understanding of animal vision, we distinguish 2 features of warning coloration: high chromatic contrast and high brightness, or luminance, contrast. Previous investigations on aposematic signal efficacy have focused mainly on the role of high chromatic contrast between prey and background, whereas little research has investigated the role of high luminance contrast. Using the Chinese mantid as a model predator and gray-painted milkweed bugs as model prey, we found that increased prey luminance contrast increased detection of prey, facilitated predator aversion learning, and increased predator memory retention of the aversive response. Our results suggest that the luminance contrast component of aposematic coloration can be an effective warning signal between the prey and predator. Thus, warning coloration can even evolve as an effective signal to color blind predators. © The Author 2006. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved.
• Cnaani, J., Thomson, J. D., & Papaj, D. R. (2006). Flower choice and learning in foraging bumblebees: Effects of variation in nectar volume and concentration. Ethology, 112(3), 278-285.
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  Abstract: Bees collect food from flowers that differ in morphology, color, and scent. Nectar-seeking foragers can rapidly associate a flower's cues with its profitability, measured as caloric value or 'net energy gain,' and generally develop preferences for more profitable species. If two flower types are equally easy to discover and feed from, differences in profitability will arise from differences in the volume or the sugar concentration of their nectar crops. Although there has been much study of how bees respond to one or the other of these two kinds of nectar variation, few studies have considered both at once. We presented free-foraging bumblebees with two different types of equally rewarding artificial flowers. After a period of familiarization, we made one type more rewarding than the other by increasing its nectar concentration, volume, or both. Bees responded more rapidly to a change in the reward's sugar concentration than to a change in its volume, even if the profitability differences were approximately equal. Sucrose concentration differences (40% vs. 13%) caused bees to virtually abandon the more dilute flower type, whether both types offered the same volume (2 μl) or the less concentrated reward offered higher volume (7 μl vs. 0.85 μl). When the two types of flower differed only in nectar volume (7 μl vs. 0.85 μl), the less rewarding type continued to receive 22% of the visits. We propose three different hypotheses to explain the stronger response of the bees to changes in sugar concentration: (i) their response threshold to sucrose concentration might change; (ii) less time is needed to assess the concentration of a reward than its volume; and (iii) a smaller sample size may be needed for reliable estimation of profitability when flowers differ in concentration. © 2006 Blackwell Verlag.
• Snell-Rood, E. C., & Papaj, D. R. (2006). Learning signals within sensory environments: Does host cue learning in butterflies depend on background?. Animal Biology, 56(2), 173-192.
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  Abstract: Insects must detect and interpret stimuli embedded in a sensory environment of competing stimuli. While sensory environments vary in time and space, individuals may be able to learn local background characteristics, facilitating perceptual learning. This study on host search in butterflies examines the following questions in an ecologically relevant context: i) does cue learning depend on the sensory environment in which learning occurs; and ii) are background characteristics learned, such that performance on novel tasks in the same sensory environment is facilitated? Females of Battus philenor (Papilionidae: Lepidoptera) were trained to different coloured and shaped oviposition targets, against different background colours. Individuals trained to colours on a brown background but tested on a green background performed significantly worse than control individuals which were trained to the same colours but on a green background. Females pre-trained to discriminate green targets from red targets on a green background colour performed significantly better in a novel task (shape learning) involving green shapes on a green background than did individuals trained to discriminate the same colours on a brown background. These two results were unique to particular cue-background combinations, in particular cryptic conditions. Taken together, our results suggest that cue learning depends on an insect's sensory environment, and that learning characteristics of local backgrounds may confer benefits to habitat-faithful individuals. © Koninklijke Brill NV 2006.
• Carsten, L. D., & Papaj, D. R. (2005). Effects of reproductive state and host resource experience on mating decisions in a walnut fly. Behavioral Ecology, 16(3), 528-533.
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  Abstract: Prior experience with conspecifics or essential resources, as well as physiological condition, can have important influences on an animal's reproductive behavior. While effects of experience and physiological state (such as reproductive condition) are generally treated separately in theoretical discussions, they often interact. No previous study has attempted to distinguish effects of experience on physiological state from other effects of experience in the context of mating behavior. In a study of a walnut-infesting tephritid fly (Rhagoletis juglandis), we examined the effects of host fruit experience on mating behavior. We manipulated physiological state in terms of egg load (defined as the number of mature oocytes in a female's ovaries) independently of fruit experience to distinguish the effects of these variables. We found that females with high egg loads were significantly more likely to copulate than low-egg load females; the level of fruit experience had no effect on propensity to copulate, except via effects on egg load. In contrast, females with prior exposure to fruit copulated for a significantly shorter duration than control females, while egg load had no effect on copulation duration. These results suggest that female reproductive condition and exposure to essential resources can have important, albeit diverse effects on mating behavior. We discuss how distinguishing different types of variables may provide insight into sexual conflict over mating decisions, as well as which sex controls specific aspects of behavior. © The Author 2005. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved.
• Hebets, E. A., & Papaj, D. R. (2005). Complex signal function: Developing a framework of testable hypotheses. Behavioral Ecology and Sociobiology, 57(3), 197-214.
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  Abstract: 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. © Springer-Verlag 2004.
• Lynn, S. K., Cnaani, J., & Papaj, D. R. (2005). Peak shift discrimination learning as a mechanism of signal evolution. Evolution, 59(6), 1300-1305.
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  PMID: 16050106;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 sender's reproductive success. © 2005 The Society for the Study of Evolution. All rights reserved.
• Lynn, S. K., Cnaani, J., & Papaj, D. R. (2005). Peak shift discrimination learning as a mechanism of signal evolution. Evolution, 59(6).
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  "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 sender's reproductive success.
• Papaj, D. R. (2005). Ovarian dynamics in relation to host quality in the Walnut-infesting Fly, Rhagoletis juglandis. Functional Ecology, 19(3), 396-404.
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  Abstract: 1. Reproductive behaviour is routinely studied with a view towards characterizing how an animal responds to variation in resource abundance and quality. This characterization is less commonly made with respect to reproductive physiology. 2. In the Walnut-infesting Fly, Rhagoletis juglandis, ovarian development is cued by the presence of the host fruit resource. In this study, I examined how ovarian development was affected by two host characteristics that relate to competition in the juvenile stages: fruit size and presence of conspecific larvae. 3. Large fruit promoted egg maturation more than small fruit, and uninfested fruit promoted maturation more than larval-infested fruit. Both effects were reproduced with artificial models of fruit. 4. The functional significance of these effects and ramifications for individual-level dynamics in oviposition behaviour are discussed. © 2005 British Ecological Society.
• Papaj, D. R., & Newsom, G. M. (2005). A within-species warning function for an aposematic signal. Proceedings of the Royal Society B: Biological Sciences, 272(1580), 2519-2523.
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  PMID: 16271978;PMCID: PMC1599780;Abstract: Aposematic, or warning, signals are generally interspecific in form: one species advertises noxiousness to a predator or parasite species. In a study of the pipevine swallowtail butterfly (Battus philenor), we show that a pattern of colouration in the caterpillars that is considered to be aposematic in the context of attack by natural enemies also deters oviposition by conspecific females. In field and laboratory assays, females avoided oviposition on plants bearing live conspecific larvae. Females avoided oviposition on plants bearing artificially constructed models identical to larvae in shape, size and colour pattern. Finally, oviposition on plants harbouring a model bearing the larval colour pattern was reduced relative to plants bearing a leaf-green model, suggesting that the larval colour pattern was essential for avoidance. We discuss how intraspecific and interspecific processes might interact in the evolution of an aposematic signal. © 2005 The Royal Society.
• Papaj, D., Papaj, D. R., & Worden, B. D. (2005). Flower choice copying in bumblebees. Biology Letters, 1(4).
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  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.
• Papaj, D., Papaj, D. R., Worden, B. D., & Skemp, A. K. (2005). Learning in two contexts: the effects of interference and body size in bumblebees. The Journal of Experimental Biology, 208(Pt 11).
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  We examined the effect of learning a new task on the performance of a previously learned task with the same set of visual cues in bumblebees, Bombus impatiens. Previous studies have shown that given a binary choice at each task, bumblebees do not show retroactive interference, or mistakes in the first task, if the two tasks are in different contexts, feeding and nest location. Here we tested whether adding a third, unrewarded choice to each task affects the performance of bees learning in two contexts. In addition, we examined whether workers differ in their expression of interference and learning ability based on size. Performance of workers at a feeder task was degraded by the introduction of training to a second task at the nest entrance. Mistakes at the feeder were biased toward the color cue that was not rewarding in both tasks; suggesting that irrelevant or background stimuli are more prone to decay or forgetting during interference. With respect to interference, we did not find an effect of body size on the amount of interference; however, size was related to how quickly interference occurred. Among individuals showing retroactive interference, larger bees showed interference earlier in phase 2 than did smaller bees. Overall, larger workers learned each task more rapidly than smaller workers. We conclude that the timing of interference is a tradeoff between acquisition of the new task and performance at a previously learned task. Given that foragers in nature tend to be larger than nest workers, we suggest that size-related learning differences be considered as a factor in division of labor between large and small bumblebees.
• Worden, B. D., & Papaj, D. R. (2005). Flower choice copying in bumblebees. Biology Letters, 1(4), 504-507.
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  PMID: 17148244;PMCID: PMC1626359;Abstract: 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. © 2005 The Royal Society.
• Worden, B. D., Skemp, A. K., & Papaj, D. R. (2005). Learning in two contexts: The effects of interference and body size in bumblebees. Journal of Experimental Biology, 208(11), 2045-2053.
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  PMID: 15914648;Abstract: We examined the effect of learning a new task on the performance of a previously learned task with the same set of visual cues in bumblebees, Bombus impatiens. Previous studies have shown that given a binary choice at each task, bumblebees do not show retroactive interference, or mistakes in the first task, if the two tasks are in different contexts, feeding and nest location. Here we tested whether adding a third, unrewarded choice to each task affects the performance of bees learning in two contexts. In addition, we examined whether workers differ in their expression of interference and learning ability based on size. Performance of workers at a feeder task was degraded by the introduction of training to a second task at the nest entrance. Mistakes at the feeder were biased toward the color cue that was not rewarding in both tasks; suggesting that irrelevant or background stimuli are more prone to decay or forgetting during interference. With respect to interference, we did not find an effect of body size on the amount of interference; however, size was related to how quickly interference occurred. Among individuals showing retroactive interference, larger bees showed interference earlier in phase 2 than did smaller bees. Overall, larger workers learned each task more rapidly than smaller workers. We conclude that the timing of interference is a tradeoff between acquisition of the new task and performance at a previously learned task. Given that foragers in nature tend to be larger than nest workers, we suggest that size-related learning differences be considered as a factor in division of labor between large and small bumblebees.
• Nufio, C. R., & Papaj, D. R. (2004). Host-marking behaviour as a quantitative signal of competition in the walnut fly Rhagoletis juglandis. Ecological Entomology, 29(3), 336-344.
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  Abstract: 1. Walnut-infesting flies in the Rhagoletis suavis species group actively re-use hosts for oviposition despite engaging in a genus-typical host-marking behaviour which, in other Rhagoletis groups, deters oviposition. In a study of the walnut fly, R. juglandis (Cresson), alternative hypotheses for the putative marking behaviour were evaluated. 2. The oviposition site attraction hypothesis proposes that the host mark guides females to oviposition sites on occupied fruit. The competition intensity signal hypothesis proposes that the host mark is an indicator of the level of competition to be incurred if fruit are re-used. 3. In a field cage, females were presented simultaneously with fruit previously exposed to 25 females that were also allowed to oviposit and engage in the putative marking behaviour, and control fruit on which females were allowed only to oviposit. The occurrence of host marking reduced a female's propensity to oviposit from 46% to just over 10%, consistent with the competition intensity signal hypothesis only. 4. In a laboratory assay, the duration of host marking was correlated positively with the size of a female's clutch. This result, also consistent with the competition intensity signal hypothesis, suggests that the amount of marking pheromone on a fruit is a reliable indicator of the number of eggs already deposited within. 5. In a second field-cage experiment, females were allowed to mark on fruit for 0, 10, 20, or 30 min and fruit were presented to test females. Whether or not females alighted on a particular host was not affected by the duration of marking; however, the frequency of both ovipositor probing and egg deposition decreased with increasing duration of marking. Consistent with the competition intensity signal hypothesis, this result suggests that the host mark permits females to assess the level of competition that a clutch will incur within re-used fruit.
• Nufio, C. R., & Papaj, D. R. (2004). Superparasitism of larval hosts by the walnut fly, Rhagoletis juglandis, and its implications for female and offspring performance. Oecologia, 141(3), 460-467.
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  PMID: 15300487;Abstract: The oviposition-preference-offspring-performance hypothesis predicts that female insects should prefer to deposit clutches on or in hosts that maximize offspring performance. An important assumption behind this prediction is that female fitness is tightly correlated with the fitness of any one offspring. In this study, we evaluate offspring performance in the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), in relation to a previously described oviposition preference for previously exploited host fruit. In particular, we examined how superparasitism of walnut hosts influences offspring survival and weight at pupation under field conditions. We found that superparasitism was common and that increases in larval densities within fruit were associated with reduced larval survival and weight at pupation. In a laboratory experiment, female size was correlated with lifetime fecundity. In this system, oviposition preference is therefore negatively, not positively, correlated with offspring performance. We argue that patterns of female preference in this system reflect direct benefits to females that are traded off against costs in terms of offspring fitness. Because female fitness is a product not only of offspring quality but also of the total number of offspring produced, female walnut flies may be optimizing their fitness by producing many less fecund offspring. Studies examining the preference-performance hypothesis should consider the reproductive conflicts between parents and offspring as potential factors that influence the congruence between parental preference and offspring performance. © Springer-Verlag 2004.
• Papaj, D., Nufio, C. R., & Papaj, D. R. (2004). Superparasitism of larval hosts by the walnut fly, Rhagoletis juglandis, and its implications for female and offspring performance. Oecologia, 141(3).
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  The oviposition-preference-offspring-performance hypothesis predicts that female insects should prefer to deposit clutches on or in hosts that maximize offspring performance. An important assumption behind this prediction is that female fitness is tightly correlated with the fitness of any one offspring. In this study, we evaluate offspring performance in the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), in relation to a previously described oviposition preference for previously exploited host fruit. In particular, we examined how superparasitism of walnut hosts influences offspring survival and weight at pupation under field conditions. We found that superparasitism was common and that increases in larval densities within fruit were associated with reduced larval survival and weight at pupation. In a laboratory experiment, female size was correlated with lifetime fecundity. In this system, oviposition preference is therefore negatively, not positively, correlated with offspring performance. We argue that patterns of female preference in this system reflect direct benefits to females that are traded off against costs in terms of offspring fitness. Because female fitness is a product not only of offspring quality but also of the total number of offspring produced, female walnut flies may be optimizing their fitness by producing many less fecund offspring. Studies examining the preference-performance hypothesis should consider the reproductive conflicts between parents and offspring as potential factors that influence the congruence between parental preference and offspring performance.
• Cnaani, J., Schmidt, J. O., & Papaj, D. R. (2003). The effect of octopamine on behavioral responses of free-foraging bumblebees to a change in food source profitability. Naturwissenschaften, 90(4), 185-188.
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  PMID: 12712253;Abstract: The invertebrate neuromodulator octopamine is known to be involved in bees' associative learning, enhancing the responsiveness of a bee to a conditioned stimulus. In this study, we tested the effect of octopamine on the choice behavior of free-flying bumblebees using a two-phase experiment in an array of artificial flowers. During the first phase of the experiment, the bee was allowed to collect octopamine-laden sugar water from two types of equally rewarding flowers (yellow versus blue). In the second phase, one type of flower was set to be unrewarding. The behavior of the bee (proportion of visits to the unrewarding flowers) over the two phases was fitted to a sigmoid regression model. Our results show that octopamine had no significant effect on the bees' equilibrium choice or on the overall rate of the behavioral change in response to the change in reward. Rather, octopamine significantly affected the time interval between the change in reward status and the initiation of behavioral change in the bee.
• Weiss, M. R., & Papaj, D. R. (2003). Colour learning in two behavioural contexts: How much can a butterfly keep in mind?. Animal Behaviour, 65(3), 425-434.
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  Abstract: Here we examine the ability of butterflies to learn colour cues in two different behavioural contexts, nectar foraging and oviposition, more or less simultaneously. We first trained female Battus philenor (Papilionidae) butterflies to associate a given colour with the presence of host plant leaf extract and assayed their colour preference; we then trained a subset of these butterflies to associate a second colour with the presence of sucrose solution and assayed colour preference once more. When offered an array of four unscented and unrewarding coloured models, 'single-trained' butterflies consistently alighted most frequently on their oviposition training colour. Green-trained butterflies landed on nontrained colours only about 4% of the time, while butterflies trained to red, yellow or blue made about 23% of their landings on nontrained colours; of those nontrained landings, most were on green. The majority of 'dual-trained' butterflies made the greatest number of visits to both training colours in the appropriate behavioural context; that is, they probed the models of their sucrose-associated colour and alighted on the models of their oviposition-associated colour. Landings or probes on nontrained colours in one context were consistently biased towards what was learned in the alternative context, suggesting an information-processing constraint in the butterflies. This paper provides a clear demonstration that butterflies can learn in two behavioural contexts within a short span of time. A capacity for such dual conditioning presumably permits female butterflies to forage effectively for egg-laying sites and nectar resources even when those activities are intermingled in time. © 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.
• Aluja, M., Díaz-Fleischer, F., Papaj, D. R., Lagunes, G., & Sivinski, J. (2001). Effects of age, diet, female density, and the host resource on egg load in Anastrepha ludens and Anastrepha obliqua (Diptera: Tephritidae). Journal of Insect Physiology, 47(9), 975-988.
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  Abstract: Oocyte counts, used as a measure of egg load, were compared among three different age groups (15, 30 and 45 days) of two polyphagous species of tephritid fruit flies, Anastrepha ludens and Anastrepha obliqua, which were exposed to varying conditions of diet (sucrose vs sucrose and protein), availability of oviposition substrate (present vs absent), adult female density (1, 2 and 4 females/cage), and semiochemical context (presence vs absence of male pheromones and fruit volatiles). In both species, oocyte counts were higher in older females and for females fed sucrose and protein than for females fed sucrose only. The presence of artificial oviposition substrates influenced oocyte counts in A. obliqua, but not in A. ludens. Female density influenced oocyte counts in both species. Females maintained in groups had higher egg loads than isolated females. Finally, preliminary evidence suggests that semiochemical context influenced oocyte counts. Counts were highest for females in a room containing both fruit volatiles and male pheromone, lowest for females in a room containing neither volatiles nor pheromone, and intermediate for females in rooms containing either volatiles or pheromone but not both. Our results suggest that egg load is influenced by environmental factors in different ways in these two species. Egg load in A. obliqua, a species whose host fruits are highly ephemeral, is responsive to access to the host resource. By contrast, in A. ludens, a species infesting less ephemeral fruit, female density and age played a more important role than host stimuli. The role of ovarian maturation and oviposition in mediating these effects, as well as implications for mass rearing and pest management, are discussed. © 2001 Elsevier Science Ltd.
• Dukas, R., Prokopy, R. J., Papaj, D. R., & Duan, J. J. (2001). Egg laying behavior of Mediterranean fruit flies (Diptera: Tephritidae): Is social facilitation important?. Florida Entomologist, 84(4), 665-671.
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  Abstract: In a set of three experiments, we were unable to verify earlier reports of social facilitation of oviposition-associated behavior in Mediterranean fruit flies, Ceratitis capitata (Wiedemann). In our first 2 experiments, we placed a focal fly on a kumquat (Experiment 1) or artificial fruit (Experiment 2) either occupied by an ovipositing resident fly or alone. The frequency of oviposition attempts by the focal fly was slightly, but not significantly, lower in the social than solitary case. In the third experiment, which was carried out in a large field enclosure, we found that focal flies did not prefer to alight on a kumquat occupied by an ovipositing fly compared with a similar but unoccupied kumquat. Our results suggest that social facilitation of oviposition-associated behavior may not be a ubiquitous phenomenon in medflies.
• Lachmann, A. D., & Papaj, D. R. (2001). Effect of host stimuli on ovariole development in the walnut fly, Rhagoletis juglandis (Diptera, Tephritidae). Physiological Entomology, 26(1), 38-48.
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  Abstract: Although examples of non-nutritive effects of host resources on ovarian development in insects are known, precise descriptions of effects on ovariole formation and development are rare. In this study, we provide a description with respect to the enhancement of egg production, or egg load, by surrogate fruit stimuli (yellow plastic spheres) in the walnut fly, Rhagoletis juglandis Cresson. A system for staging developing ovarioles was established, and cohorts of females held from emergence with or without surrogate fruit were sampled over time with respect to number of ovarioles as well as number and stage of follicles within ovarioles. As found previously, the presence of surrogate fruit strongly enhanced production of eggs in the first maturation cycle. The effect was probably not due to oosorption in the ovaries of females held without surrogates; in fact, oosorption was never observed in ovaries of females in either treatment. The effect was due in part to an increase in ovariole number in females held with surrogates; in each of two trials, mean ovariole number was slightly but significantly greater for females held with vs. without spheres. However, the main effect was also due in part to an earlier onset and increased rate of vitellogenesis in the first and second follicles of females held with spheres.
• Nufio, C. R., & Papaj, D. R. (2001). Host marking behavior in phytophagous insects and parasitoids. Entomologia Experimentalis et Applicata, 99(3), 273-293.
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  Abstract: 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.
• Alonso-Pimentel, H., Spangler, H. G., Rogers, R., & Papaj, D. R. (2000). Acoustic component and social context of the wing display of the walnut fly Rhagoletis juglandis. Journal of Insect Behavior, 13(4), 511-524.
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  Abstract: Courtship signaling via wing vibration, accompanied by sound production, has been reported in several species of tephritids. In this large family of flies, sound communication as well as complex courtship displays appears to be restricted to species with lekking mating systems (i.e., Mediterranean fruit fly, Anastrepha and Dacus species). In contrast, in tephritid species with resource-defense mating systems, such as species in the genus Rhagoletis, little or no courtship behavior, acoustical or otherwise, has been described. Wing displays in Rhagoletis species have been considered to play a visual role. This study describes a distinctive wing display performed by males of the walnut fly, Rhagoletis juglandis. Laboratory experiments and field observations demonstrate that the male wing display plays a role in courtship. We used sound and vibration detectors to record the signals produced by this wing display. Using a combination of techniques, we were able to record both the very low-frequency vibration and its accompanying airborne infrasound (12-22 Hz) produced by the males.
• Nufio, C. R., Papaj, D. R., & Alonso-Pimentel, H. (2000). Host utilization by the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Environmental Entomology, 29(5), 994-1001.
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  Abstract: Rhagoletis juglandis Cresson is a specialist that deposits its eggs into the husks of developing walnut fruit. Like other walnut infesting flies in the R. suavis group, R. juglandis actively superparasitizes its larval hosts. However, little is known regarding the degree to which hosts are reused and the ecological context under which host reuse occurs. This field study examined the pattern of host utilization by R. juglandis and how fruit variables such as volume and penetrability affect the degree that hosts are reused. Fruit on four of five study trees were synchronously infested and within 2-2.5 wk all fruit on these trees were infested. Fruit on a fifth tree were significantly less penetrable than those found among the other trees in the study and this may explain why fruit on this tree were rarely used throughout the season. Walnut hosts were commonly multiply infested and reuse of hosts occurred in as few as 1-2 d after first infestion. Infestation levels within fruit appeared to stabilize 4-5 d after fruit were first used. Fruit volume was positively correlated with both the number of punctures on hosts and the infestation levels within hosts that had been infested for either 1-2 or 4-9 d. Large fruit were infested more quickly than small fruit, although this trend was stronger on some trees than others. Finally, despite a size-penetrability correlation among two of the five trees, penetrability itself did not explain either which fruit were preferentially used throughout the season or the infestation levels within fruit.
• Papaj, D. R. (2000). Ovarian dynamics and host use. Annual Review of Entomology, 45, 423-448.
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  PMID: 10761584;Abstract: Oviposition behavior in herbivorous and frugivorous insects and parasitoids is dynamic at the level of the individual, responding to variation in host quality and availability. Patterns of variation in egg load in response to host presence and quality suggest that ovarian development also responds to variation in the host environment. Ovarian dynamics are mediated by feedback from oviposition, by host feeding, and by sensory input from the host. The last of these mechanisms, host sensory cuing, is known to occur in three major orders and provides strong evidence that ovarian dynamics are adaptive by design. Conditions favoring host effects on ovarian development include trade-offs between egg production and either survival or dispersal, uncertainty in the host environment, and a correlation in host conditions between the time that oogenesis is initiated and the time that eggs are laid. Some host defenses block ovarian development, suggesting that ovarian dynamics in host-specific insects should be viewed from a coevolutionary perspective.
• Alonso-Pimentel, H., & Papaj, D. R. (1999). Resource presence and operational sex ratio as determinants of copulation duration in the fly Rhagoletis juglandis. Animal Behaviour, 57(5), 1063-1069.
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  Abstract: The effects of the interaction between the operational sex ratio (OSR) and a resource (i.e. oviposition site) on mating dynamics have rarely been considered. We examined the effect of the resource presence and its interaction, with the effect of OSR on copulation duration in Rhagoletis juglandis, a tephritid fly species characterized by a resource-defence mating system in which males defend territories on Walnut fruit. In this species, copulation duration varies from 30 s to over 1 h and was shown previously to respond strongly to changes in OSR. In the field, short copulations tended to begin and end on fruit, whereas most long copulations generally began on fruit but ended in the foliage, suggesting a possible effect of resource presence on the copulation duration. In laboratory assays of isolated pairs, copulations were significantly shorter in the presence of a surrogate fruit, confirming the effect of resource presence. In another laboratory assay, in which we manipulated OSR independently of resource presence, resource presence and OSR were additive in their effects. Results are discussed in the context of sperm competition theory.
• Henneman, M. L., & Papaj, D. R. (1999). Role of host fruit color in the behavior of the walnut fly Rhagoletis juglandis. Entomologia Experimentalis et Applicata, 93(3), 249-258.
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  Abstract: Observations and sticky-trap tests were used to assess the effect of fruit color on the behavior of adult male and female Rhagoletis juglandis Cresson (Diptera: Tephritidae), a tephritid that infests husks of Arizona walnut in southeastern Arizona. In the first experiment, during which flies were observed foraging among walnut models suspended from small walnut trees, models were painted green to appear ripe and uninfested or yellow with brown patches to appear ripe and infested. Flies used for this first experiment were also of two types: prior to observations, one group of flies had access to real walnuts for 1.5 days (prior experience) while the other group of flies was held without real walnut fruits (no prior experience). Regardless of prior experience with real walnut fruits, female flies landed on green models more than yellow/brown models. Experienced males also were more likely to land on green models than on yellow/brown models. More interactions also occurred on green models, because there were more landings. In the field behavioral assay, flies from a natural population given a choice of green, yellow, and yellow/brown models landed most often on green models, and all interactions and oviposition attempts occurred on green models. Flies also distinguished models by color in field sticky trap assays. These results suggest that female response to ripeness cues is innate, while males develop a preference for green based on their encounter rate with females.
• Alonso-Pimentel, H., Korer, J. B., Nufio, C., & Papaj, D. R. (1998). Role of colour and shape stimuli in host-enhanced oogenesis in the walnut fly, Rhagoletis juglandis. Physiological Entomology, 23(2), 97-104.
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  Abstract: This study aimed to quantify effects of the host plant on oogenesis in the walnut-husk-infesting fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), and to assess the role of physical cues in those effects. In laboratory assays, the presence of fruit was manipulated independently of the presence of foliage for newly emerged females, After eight days, in each of two trials, females with fruit were found to have significantly higher egg loads than females without fruit. Foliage presence had little effect. In a second experiment, females held with fruit or a fruit model (plastic yellow sphere of a size similar to fruit) had significantly higher egg loads than females held with neither fruit nor model. Egg loads of females with fruit were not significantly different from those of females with models. In a third experiment, females were held with spheres of various colours or no sphere at all. Females with yellow or green spheres (similar to the colour of walnut fruit) had significantly higher egg loads than females with black, blue or red spheres of other colours or females without spheres. In a fourth experiment, females held with spheres had significantly higher egg loads than females held with cubes of equivalent surface area or females held without a model. Finally, cohorts of newly emerged females held with yellow spheres or without spheres were sampled periodically. In the sphere treatment, mean egg load increased sharply from negligible levels between days 8 and 10. The pattern was similar in the no-sphere treatment, although the increase in egg load appeared to occur a day later. From these experiments, we conclude that physical host fruit stimuli known to be important in host selection in Rhagoletis flies, including colour and shape, also enhance oogenesis in the first egg maturation cycle, and that enhancement of oogenesis via these stimuli requires neither nutritional input from the fruit nor prior egg deposition.
• Papaj, D. R., & Messing, R. H. (1998). Asymmetries in physiological state as a possible cause of resident advantage in contests. Behaviour, 135(9-10), 1013-1030.
• Vet, L. E., Jong, A. D., Franchi, E., & Papaj, D. R. (1998). The effect of complete versus incomplete information on odour discrimination in a parasitic wasp. Animal Behaviour, 55(5), 1271-1279.
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  Abstract: We studied the function of learning in the parasitoid Leptopilina heterotoma by looking at discrimination of odour stimuli used in foraging for a host. To optimize the rate of encounters with hosts, these parasitoids are expected to assess the extent to which variation in host-substrate odours is reliably associated with variation in the presence of hosts, that is, substrate profitability. Where the association is reliable, parasitoids should attend to variation in odours and discriminate between them; where it is not, they should ignore it. We hypothesized that foraging decisions are based on the completeness of information the animal has about differences in substrate profitabilities. Our laboratory studies showed that discrimination and non-discrimination of odour stimuli are dynamic behavioural decisions that can be related to the degree of substrate variation and to an animal's informational state. In wind-tunnel studies, females learned to discriminate between odours from substrates that were qualitatively different, for example, between odours from apple and pear substrates or between yeast substrates with different C6 compounds added. They did not discriminate when differences were small (e.g. between odours from two apple varieties or between yeast patches with different concentrations of ethyl acetate), unless unrewarding experiences provided evidence of the absence of hosts in one of the substrates. Hence, we suggest that non-discrimination between odour stimuli in L. heterotoma is not a lack of ability to discriminate but a functional decision by the parasitoid.
• Papaj, D. R., & Alonso-Pimentel, H. (1997). Why walnut flies superparasitize: Time savings as a possible explanation. Oecologia, 109(1), 166-174.
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  Abstract: This study evaluated a possible fitness advantage, specifically time savings, that might account for an unusual propensity in walnut flies (Rhagoletis spp.) to superparasitize their walnut hosts and to place eggs into existing egg-laying cavities. The first part of this study demonstrated that, in laboratory assays, females of two walnut fly species, R. boycei and R. juglandis, save time when cavities are reused and that in R. juglandis, where it was examined in detail with in vivo staining of eggs, time saving was not an artifact of differences in the size of clutches deposited at new versus existing sites. We further demonstrated that time savings reflected a reduction in the time required to generate the cavity itself. In the second part of the study, we evaluated the possibility that, in the field, time saved by reusing existing cavities is nullified by extra time spent mating associated with a previously described tendency for males to guard these cavities. Field observations of R. juglandis indicated that use of existing sites was, as expected, associated with increased mating. Yet, despite the added time spent mating, in observations of similar length females attempting to lay eggs at existing sites deposited clutches more often than females attempting to lay eggs at new sites. We discuss these results in the context of the more common pattern of superparasitism avoidance observed in hostspecific insects. © Springer-Verlag 1997.
• Allard, R. A., & Papaj, D. R. (1996). Learning of leaf shape by pipevine swallowtail butterflies: A test using artificial leaf models. Journal of Insect Behavior, 9(6), 961-967.
• Alonso-Pimentel, H., & Papaj, D. R. (1996). Operational sex ratio versus gender density as determinants of copulation duration in the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Behavioral Ecology and Sociobiology, 39(3), 171-180.
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  Abstract: In laboratory and field studies of the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), we assessed the effect of operational sex ratio on copulation duration and partitioned the sex ratio effect into component effects due to male density and female density. In our first laboratory experiment, results were clearly consistent with theoretical expectation: increases in male density were associated with significant increases in copulation duration while increases in female density were associated with significant decreases in copulation duration. These component effects yielded a striking composite effect of operational sex ratio (OSR) on copulation duration in which male-biased ratios were associated with low frequencies of short copulations and female-biased ratios were associated with high frequencies of short copulations. Consistent with a priori expectations concerning costs of territorial behavior, the effect of male density on copulation duration was stronger than that of female density. There was no significant interaction between the effects of gender density on copulation duration: each gender density contributed additively to the composite OSR effect on copulation duration. In contrast to the effect of OSR, overall density had little effect. Field data corroborated these findings fully and showed additionally that OSR in the vicinity of fruit tended in nature to be male-biased. In a second laboratory experiment, we measured copulation duration for individuals exposed alternately to male-biased and female-biased ratios. Individual flies consistently copulated for longer in male-biased environments than in female-biased ones. We propose that this plasticity permits individuals to track changes in local sex ratio over space and time and respond appropriately.
• Alonso-Pimentel, H., & Papaj, D. R. (1996). Patterns of egg load in the walnut fly Rhagoletis juglandis (Diptera: Tephritidae) in nature and their possible significance for distribution of sexes. Annals of the Entomological Society of America, 89(6), 875-882.
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  Abstract: In a field study of the tephritidd fly Rhagoletis Juglandis Cresson on its host Juglans major (Torrey) Heller, the density of both sexes on host foliage remained more or less constant throughout the season. The density of each sex on fruit, by contrast, increased steadily over the course of several weeks. The density of mals on fruit increased much more sharply than that of females. Associeted with the temporal increase in relative fly density on fruit was an increase in the mean number of eggs in a female's ovaries (i.e., egg load). this pattern in egg load was not caused by an increase in the mean egg load of individuals carrying eggs (which remained more or less constant over the season), but rather by an increase in the number of individuals that carried any eggs (i.e., the number of reproductively mature individuals). Late in the season, mean egg load of females in the foliage was lower than that of females on fruit for each of 2 yr, but the difference was not statistically significant. Within a given location (fruit versus foliage), egg load was associated with female activity. Females attempting to oviposit on fruit and females found in mating pairs on foliage had high mean egg loads, whereas females feeding on foliage and females dragging their ovipositor (indicative of recent clutch deposition) on fruit had low mean egg loads. We discuss how results for this species conform to a generally held scenario for the distribution of frugivorous tephritied flies in time and space.
• Papaj, D. R., & Messing, R. H. (1996). Functional shifts in the use of parasitized host by a tephritid fly: The role of host quality. Behavioral Ecology, 7(3), 235-242.
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  Abstract: Superparasitism a phenomenon in which parasitic insects lay eggs in already-exploited hosts, provides a useful context in which to examine the dynamics of parental investment. This study explored conditions under which female Mediterranean fruit flies (Cerati capitata) shift from avoiding superparasitism of hot fruit to preferring it, even placing eggs directly into existing egg laying. An a prior hypothesis of costs and benefits was use to predict how to use and avoidance of parasitized fruit would change in response to changes in fruit size and ripeness. We predicted that avoidance would decrease with increasing fruit size, while use would increase with decreasing ripeness. Using a field-cage assay, ripeness was held constant and the size host coffee berries manipulated. Avoidance of parasitized berries was significantly less pronounced on large berries than on small ones. In a second experiment, size was held constant and ripeness manipulated. On unripe berries, females deposited the majority of clutches directly into existing egg-laying cavities. On ripe berries, by contrast, the same female deposited most clutches in previously unparasitized fruit. Parallel in the patterns in the frequency of female-female contests were observed, supporting the notion that a fruit's value is determined by an interaction between fruit size or ripeness, on one hand the prior occurrence of egg, on the other. Laboratory assays suggested that use of exiting site had-advantages inn terms of time savings; female behavior thus constitute a relatively uncommon example of adaptive superparasitism in which parasitized hosts are actually preferred over unparasitized ones.
• Papaj, D. R., García, J., & Alonso-Pimentel, H. (1996). Marking of host fruit by male Rhagoletis boycei Cresson flies (Diptera: Tephritidae) and its effect on egg-laying. Journal of Insect Behavior, 9(4), 585-598.
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  Abstract: Male Rhagoletis boycei flies (Cresson) have been shown previously to guard egg-laying punctures on host walnut (Juglans major) fruit. During their tenure, R. boycei moles were observed to dip the posterior portion of their abdomen repeatedly toward the fruit surface. Closeup video analysis revealed that, during this dipping behavior, a clear viscous substance emanating from the cercus was deposited directly on the fruit. Laboratory assays indicated that the rate of abdomen-dipping was significantly higher on fruit bearing simulated egg-laying punctures than on control fruit and significantly higher in the area of the puncture than elsewhere on the fruit. In a final experiment, the occurrence of abdomen-dipping in the vicinity of a puncture was manipulated independently on separate punctures on the same fruit. On such fruit and in the absence females, previously mated, reproductively mature females attempted oviposition significantly more often in or near a puncture exposed to males than in or near an unexposed control puncture. Possible functions of the putative male-marking behavior from the perspectives of both male and female are discussed.
• Papaj, D. R. (1994). Oviposition site guarding by male walnut flies and its possible consequences for mating success. Behavioral Ecology and Sociobiology, 34(3), 187-195.
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  Abstract: Field studies showed that male Rhagoletis juglandis and R. boycei flies guard egg-laying punctures (and the eggs within) on host walnut (Juglans major) fruit and defend those sites from conspecific and heterospecific males. In field experiments with artificially punctured fruit,as well as field observations on unmanipulated fruit, males were consistently more likely to be sighted and stayed longer on damaged fruit than on undamaged fruit. On artificially punctured fruit, they consistently spent more time in the vicinity of a puncture than expected by chance alone. Males together on damaged fruit were more likely to engage in contests over those fruit than males together on undamaged fruit. Copulations were consistently more frequent for either species on damaged than undamaged fruit, both in observations of unmanipulated fruit and in artificial puncture experiments. Analyses which controlled for the longer male residence time on damaged fruit suggested strongly that copulations were consistently achieved at higher per capita rates on damaged than on undamaged fruit, indicating that puncture-guarding functions to increase access to females. An exception to the pattern in male mating success was noted at a site where both species used host fruit on the same trees. In this case, R. juglandis males were only slightly more common on punctured fruit than on control fruit and male success in copulation did not differ significantly between the two types of fruit. This anomalous result was apparently due to an almost absolute advantage enjoyed by R. boycei males in on-fruit contests with R. juglandis males. A likely basis for improvements in mating success associated with puncture guarding was a propensity for females to deposit eggs into existing punctures. Both in observations of unmanipulated fruit and in artificial puncture experiments, females consistently attempted oviposition more often in damaged than undamaged fruit. In artificial puncture experiments, both species at both sites deposited most clutches in damaged fruit. Mating generally took place as females initiated oviposition. The possible functions of puncture use by females as well as alternative functions of puncture guarding by males are discussed. © 1994 Springer-Verlag.
• Papaj, D. R., Snellen, H., Swaans, K., & Vet, L. E. (1994). Unrewarding experiences and their effect on foraging in the parasitic wasp Leptopilina heterotoma (Hymenoptera: Eucoilidae). Journal of Insect Behavior, 7(4), 465-481.
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  Abstract: The host-foraging behavior of female entomophagous parasitoids is commonly modified by positive associative learning. Typically, a rewarding experience (e.g., successful oviposition in a host) increases a female's foraging effort in a host microhabitat of the type associated with that experience. Less well understood are the effects of unrewarding experiences (i.e., unsuccessful foraging). The influence of unrewarding experience on microhabitat choice and residence time within a microhabitat was examined for the eucoilid parasitoid, Leptopilina heterotoma, in laboratory and greenhouse assays. As determined previously, females which oviposited successfully in either of two microhabitat types (fermenting apple or decaying mushroom) strongly preferred to forage subsequently on that microhabitat type. However, failure to find hosts in the formerly rewarding microhabitat caused females to reverse their preference in favor of a novel microhabitat type. The effect, though striking, was transient: within 1-2 h, the original learned preference was nearly fully restored. Similar effects of unrewarding experiences were observed with respect to the length of time spent foraging in a microhabitat. As determined previously, oviposition experience in a particular microhabitat type increased the time spent foraging in a patch of that microhabitat type. However, failure to find hosts in the patch caused the time a wasp spent in the next unoccupied patch of that type to decrease to almost nothing. In addition, there was a tendency for an unrewarding experience on a formerly rewarding microhabitat type to extend the time spent in a patch of a novel type. The function of the observed effects of unrewarding experiences is discussed. © 1994 Plenum Publishing Corporation.
• Papaj, D. R., & Aluja, M. (1993). Temporal dynamics of host-marking in the tropical tephritid fly, Anastrepha ludens. Physiological Entomology, 18(3), 279-284.
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  Abstract: Time spent marking increased as A. ludens females deposited clutches in a given fruit previously marked zero, one, two or three times. This trend was paralleled by an increase in the number of pauses in marking behaviour within the host-marking bout. Within any given marking bout, the length of a sub-bout diminished progressively. Host-marking pheromone (while deterrent to females prior to egg-laying) actually stimulates continued host-marking behaviour after egg-laying. -from Authors
• Prokopy, R. J., Cooley, S. S., & Papaj, D. R. (1993). How well can relative specialist Rhagoletis flies learn to discriminate fruit for oviposition?. Journal of Insect Behavior, 6(2), 167-176.
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  Abstract: We show that blueberry maggot females [Rhagoletis mendax (Curran)], apple maggot females [Rhagoletis pomonella (Walsh)], and walnut husk fly females [Rhagoletis suavis (Loew)], all relative specialists in range of fruit species attacked in nature, are able to learn to discriminate between types of fruit in which they oviposit. It appears, however, that these relative specialists express less capacity to learn fruit characters than relative generalist tephritids. This difference in expression of learning ability may be associated in part with differences in assignments species are asked to learn. Apparent differences in learning capability between relative specialist and relative generalist tephritids may therefore depend as much upon differences in the physical and chemical nature of host fruit as upon species differences in the adaptive value of learning. © 1993 Plenum Publishing Corporation.
• Papaj, D. R., Averill, A. L., Prokopy, R. J., & Wong, T. T. (1992). Host-marking pheromone and use of previously established oviposition sites by the mediterranean fruit fly (Diptera: Tephritidae). Journal of Insect Behavior, 5(5), 583-598.
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  Abstract: Under controlled conditions, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) preferred to initiate oviposition into preexisting, naturally formed oviposition punctures in a host fruit, kumquat (Fortunella japonica), over establishing new sites on the fruit. This preference was expressed despite the presence of naturally deposited host-marking pheromone (HMP)shown previously to deter oviposition. An almost-identical preference for existing punctures was expressed when females were presented with fruit bearing artificially made punctures on which HMP had been naturally deposited. Using artificial punctures and HMP extracts, the occurrence of punctures was manipulated independently of the presence of HMP. Under field-cage conditions, we found that (1) punctures stimulated egg-laying on kumquats, regardless of HMP treatment; (2) HMP extract inhibited egg-laying, regardless of the occurrence of punctures; and (3) the extent to which HMP inhibited egg-laying was greater on fruit free of punctures than on fruit bearing them. The physiological, evolutionary, and pest management implications of these results are discussed. © 1992 Plenum Publishing Corporation.
• Papaj, D. R., Feeny, P., Sachdev-Gupta, K., & Rosenberry, L. (1992). d-(+)-Pinitol, an oviposition stimulant for the pipevine swallowtail butterfly, Battus philenor. Journal of Chemical Ecology, 18(5), 799-815.
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  PMID: 24253972;Abstract: Oviposition by females of the pipevine swallowtail butterfly, Battus philenor, was stimulated by contact with alcoholic extracts of host foliage. d-(+)-Pinitol was isolated and identified from leaf material of one host species, Aristolochia macrophylla (Aristolochiaceae). In combination with chloroform-soluble components of host leaf material, this compound was comparable to the parent extract in stimulating oviposition. © 1992 Plenum Publishing Corporation.
• Prokopy, R. J., Papaj, D. R., Hendrichs, J., & Wong, T. T. (1992). Behavioral responses of Ceratitis capitata flies to bait spray droplets and natural food. Entomologia Experimentalis et Applicata, 64(3), 247-257.
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  Abstract: In studies carried out on field-caged non-fruiting host trees, we examined effects of environmental and adult physiological and experiential state factors on responses of released Mediterranean fruit flies, Ceratitis capitata (Wiedemann), to droplets of proteinaceous bait (PIB-7) with or without 20% insecticide (malathion). We confirmed that fresh PIB-7 is both attractive and phagostimulatory to protein-deprived medflies and found that presence of 20% malathion ultra low volume concentrate (ULVC) in PIB-7 droplets does not significantly repel medflies from approaching droplets but does significantly deter feeding on them. A single relatively fresh deposit of bird feces, an important source of protein for medflies in natural environments, attracted several times more laboratory-cultured and wild medflies than 20 droplets of 80% PIB-7/20% malathion ULVC (about the average number of droplets per m2 of plant canopy in aerial bait spray programs). Attraction to protein was significantly greater among wild medflies deprived of protein continuously from eclosion than among wild medflies that had recent (within 3 days) or continuous access to protein. Attraction to protein increased significantly with increasing age (2, 7 and 12 days) of protein-deprived wild medflies. But we found no significant positive impact of recent brief experience of wild medflies with protein on degree of subsequent attraction to protein. In final experiments that mimicked the size, density and distribution of bait spray droplets on tree foliage typical for an aerial medfly control program, very few (4%) or no released protein-deprived wild medflies found a bait droplet within the 15 min test period even though most found a single deposit of bird feces. We conclude that the effectiveness of aerial bait sprays against medflies might be enhanced substantially (and the proportion of infested area treated with bait spray reduced considerably) by (1) including synthetic equivalents of attractive components of bird feces in the spray mixture, and (2) adjusting spatial and temporal patterns of bait spray applications according to estimates of the composition and abundance of natural medfly food and the age structure of medfly adult populations in infested regions. © 1992 Kluwer Academic Publishers.
• Vet, L. E., & Papaj, D. R. (1992). Effects of experience on parasitoid movement in odour plumes. Physiological Entomology, 17(1), 90-96.
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  Abstract: The effect of oviposition experience on upwind movement of the parasitoid Leptopilina heterotoma (Hymenoptera: Eucoilidae), in odour plumes of host microhabitats, was quantified. A 2 h exposure to host Drosophila melanogaster larvae in either fermenting apple-yeast or decaying mushroom substrate had a number of effects on movement in plumes of each substrate. Females experienced with a particular substrate walked faster and straighter, made narrower turns and spent more time in upward movement in a plume of odour from that substrate than in odour from an alternative substrate. Inexperienced females generally showed little or no significant difference in responses to alternative odours. In addition to affecting the mean values of movement parameters, experience also affected variability around those means. When walking speed or path straightness in an odour plume was increased by experience, variability among individuals was correspondingly decreased. The consequences of odour learning for microhabitat choice is discussed briefly. -from Authors
• Hendrichs, J., Katsoyannos, B. I., Papaj, D. R., & Prokopy, R. J. (1991). 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). Oecologia, 86(2), 223-231.
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  Abstract: Systematic 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. © 1991 Springer-Verlag.
• Papaj, D. R. (1991). Interference with learning in pipevine swallowtail butterflies: behavioural constraint or possible adaptation?. Insects-plants '89. Proc. 7th symposium on insect-plant relationships, Budapest, 1989, 89-101.
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  Abstract: Ovipositing Battus philenor learned host leaf shape when Aristolochia host species were presented singly in outdoor enclosure arrays. When species were presented together, however, learning of one leaf shape interfered with learning of another. For two of three Aristolochia species presented singly, females found hosts at higher rates overall than when all host species were presented together. Host-finding rates increased with successive encounters when those two species were presented singly, but not when all three species were presented together. Improvement in host-finding with experience was associated only weakly with increases in oviposition rate. Females that find hosts at higher rates will be more selective about the plants on which they deposit eggs, placing more progeny on plants on which they are more likely to survive. -from Author
• Papaj, D. R. (1990). Fruit size and clutch size in wild Ceratitis capitata. Entomologia Experimentalis et Applicata, 54(2), 195-198.
• Papaj, D. R., & Vet, L. E. (1990). Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. Journal of Chemical Ecology, 16(11), 3137-3150.
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  PMID: 24263300;Abstract: A brief 2-hr experience with host Drosophila larvae in artificial apple-yeast or mushroom microhabitats had three effects on the foraging behavior of female Leptopilina 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 or D. 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. © 1990 Plenum Publishing Corporation.
• Papaj, D. R., Roitberg, B. D., Opp, S. B., Aluja, M., Prokopy, R. J., & Wong, T. T. (1990). Effect of marking pheromone on clutch size in the Mediterranean fruit fly. Physiological Entomology, 15(4), 463-468.
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  Abstract: Female Ceratitis capitata laid fewer eggs per clutch in fruit previously infested with eggs than in uninfested fruit, an effect apparently attributable to marking pheromone deposited by females after oviposition. -from Authors
• Vet, L. E., Lewis, W. J., Papaj, D. R., & Lenteren, J. v. (1990). A variable-response model for parasitoid foraging behavior. Journal of Insect Behavior, 3(4), 471-490.
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  Abstract: An important factor inducing variability in foraging behavior in parasitic wasps is experience gained by the insect. Together with the insect's 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 parasitoid's 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 insect's 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. © 1990 Plenum Publishing Corporation.
• Papaj, D. R., & Prokopy, R. J. (1989). Ecological and evolutionary aspects of learning in phytophagous insects. Annual review of entomology. Vol. 34, 315-350.
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  Abstract: In phytophagous insects, emphasis has been on learning in relation to the acquisition of food, but there is also an array of work on mate acquisition, recognition of competitors and establishment of home range. Host stimuli involved in learning are noted. Types of learning include habituation, associative learning, aversion learning and induction of preference. Ecological implications of each type are examined, and the possible integration of learning mechanisms is indicated. There are a number of programmed elements of learning, eg imprinting, where restriction to a limited set of stimuli and motor patterns in highly specific contexts probably has an adaptive function. The adaptive functions of learning and memory are embraced by the non-mutually exclusive neural economy and environmental unpredictability hypotheses. There is little evidence that learning has undergone adaptive evolutionary change in phytophagous insects, though the potential for such change probably exists. -P.J.Jarvis
• Papaj, D. R., Katsoyannos, B. I., & Hendrichs, J. (1989). Use of fruit wounds in oviposition by Mediterranean fruit flies. Entomologia Experimentalis et Applicata, 53(3), 203-209.
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  Abstract: Casual observations suggested that female Mediterranean fruit flies (Ceratitis capitata Wiedemann) exploit fruit wounds (including pre-existing oviposition punctures) as oviposition sites. This behaviour was quantified under field conditions in a citrus grove on the Greek island of Chios. Fruit wounds influenced oviposition behaviour in three ways. First, females were more likely to land on oranges (Citrus sinensis) that were artificially wounded than into unwounded control oranges. Second, having landed, females were more likely to attempt oviposition into a wounded orange than into control oranges. Third, females that attempted oviposition into wounded oranges usually did so directly into or very near the wound. The diameter and depth of the wound significantly influenced the tendency for female flies to land on a fruit but not their propensity, having landed, to attempt oviposition in or near the wound. The significance of this behavior in nature and implications for management of the Mediterranean fruit fly are discussed. © 1989 Kluwer Academic Publishers.
• Papaj, D. R., Opp, S. B., Prokopy, R. J., & Wong, T. T. (1989). Cross-induction of fruit acceptance by the medfly Ceratitis capitata: The role of fruit size and chemistry. Journal of Insect Behavior, 2(2), 241-254.
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  Abstract: Groups of female Mediterranean fruit flies, Ceratitis capitata (Wiedemann), were exposed for several days to one of three host fruit species. Oviposition-site acceptance behavior was subsequently assayed on five fruit species. Females accepted most often the fruit to which they were exposed. Females exposed to a small fruit, mock orange, accepted other fruit species less often as the size of the fruit increased; females exposed to a large fruit, sweet orange, accepted other fruit species more often as the size of the fruit increased. This tendency for experience with one host fruit species to alter differentially behavioral responses to alternative host fruit species has been defined as cross-induction. In contrast, females exposed to a medium fruit, kumquat, were not cross-induced: females accepted the medium fruit very often and rejected all other fruit species to approximately the same degree regardless of size. When females were exposed to small, medium, or large fruit and tested on spherical wax fruit models of a variety of sizes, patterns similar to those with real fruit were observed. Whereas naive females generally accepted a given model as frequently as real fruit of a similar size, experienced females generally accepted models much less frequently than real fruit. In a final experiment, females were exposed to different fruits and tested on spherical wax models treated with fruit chemicals. Experienced females generally accepted fruit-treated spheres more often than untreated spheres. In addition, females usually accepted most often models treated with chemicals from the fruit to which they were exposed. Two hypotheses about the mechanism by which experience alters fruit acceptance- termed the "sliding template" and "closing window" hypotheses- are presented. Results of fruit and model acceptance by naive and experienced females support the latter hypothesis. © 1989 Plenum Publishing Corporation.
• Papaj, D. R., Roitberg, B. D., & Opp, S. B. (1989). Serial effects of host infestation on egg allocation by the Mediterranean fruit fly: a rule of thumb and its functional significance. Journal of Animal Ecology, 58(3), 955-970.
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  Abstract: Prior infestation of host kumquats Fortunella japonica with the eggs of Ceratitis capitata had a number of effects on the oviposition behaviour of conspecific flies. Overall, infestation markedly reduced the rate at which clutches were laid by a female searching within a host tree. Egg infestation decreased the probability that a female 1) bored with her ovipositor after landing on a fruit and 2) deposited a clutch once oviposition-boring was initiated, and 3) deposited additional clutches at new sites on the fruit before leaving. Egg infestation also decreased duration of an oviposition (and thus probably clutch size) and tended to decrease the persistence with which a female foraged on fruit. Infestation had no effect on the persistence with which a female foraged within a tree or on the rate at which a female landed on fruit. A simple rule of thumb for response by Mediterranean fruit flies to egg infestation is presented. This rule implies that different foraging traits such as clutch size and giving up time are mechanistically related and should not be treated independently in foraging theory. Both survival to pupation and the expected fecundity of survivors decreased progressively as egg density in host fruit was artificially increased, suggesting that progeny deposited in egg-infested fruit have lower fitness than progeny deposited in uninfested fruit. -from Authors
• Papaj, D. R., & Prokopy, R. J. (1988). The effect of prior adult experience on components of habitat preference in the apple maggot fly (Rhagoletis pomonella). Oecologia, 76(4), 538-543.
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  Abstract: Numerous authors have suggested that genetic subdivision within a population in a heterogeneous environment is more likely if individuals tend, through prior experience, to breed in the same habitat in which they developed. Under semi-field conditions we demonstrate that prior adult experience alters habitat preference in the apple maggot fly, Rhagoletis pomonella (Tephritidae), a frugivorous parasitic insect thought to have undergone sympatric divergence in host use in historical times. Females exposed to a particular host fruit species - apple (Malus pumila) or hawthorn (Crataegus mollis) - in a field cage oviposited at a higher rate in test fruit of that species than did inexperienced females or females exposed to the other species. Females exposed to a particular host fruit species also tended to remain longer in test trees harboring fruit of that species than did inexperienced females or females exposed to the other species. Prior adult experience thus alters two components of habitat preference in the apple maggot fly: oviposition preference and habitat fidelity. We discuss how these effects of experience on habitat preference should increase the likelihood that individuals mate assortatively and may further increase the likelihood that apple maggot populations become genetically subdivided. © 1988 Springer-Verlag.
• Prokopy, R. J., & Papaj, D. R. (1988). Learning of apple fruit biotypes by apple maggot flies. Journal of Insect Behavior, 1(1), 67-74.
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  Abstract: Previously, we showed that after a female apple maggot fly, Rhagoletis pomonella, arrives on a host hawthorn or apple fruit, its propensity to accept (bore into) or reject that fruit prior to egg deposition can be modified by previous ovipositional experience with one or the other species and, hence, involves learning. Here, we present both field and laboratory evidence indicating that females also are able to learn characteristics of three different apple biotypes or cultivars: "Early Macintosh," "Red Delicious," and "Golden Delicious." We suspect that females learn to discriminate among these three cultivars on the basis of differences in chemical stimuli among cultivars. The effect of fruit cultivar learning was not as strong as the effect of fruit species learning. © 1988 Plenum Publishing Corporation.
• Papaj, D. R., & Rausher, M. D. (1987). Components of conspecific host discrimination behavior in the butterfly Battus philenor.. Ecology, 68(2), 245-253.
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  Abstract: Pipevine swallowtail butterflies discriminated among Aristolochia reticulata host plants differing in leaf quality both before and after landing. Host plants on which females landed and oviposited were smaller, possessed longer buds, and bore a higher percentage of high-quality leaves than host plants on which females landed but left without deposition eggs. Plants on which butterflies alighted bore a higher percentage of high-quality leaves, a lower percentage of low-quality leaves, and longer buds than their nearest neighbors that were not landed upon. These characteristics were associated with differences in expected larval growth and survival. -from Authors
• Papaj, D. R., & Rausher, M. D. (1987). Genetic differences and phenotypic plasticity as causes of variation in oviposition preference in Battus philenor. Oecologia, 74(1), 24-30.
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  Abstract: Bradshaw (1965) proposed that phenotypic plasticity would be more common than adaptive genetic variability in species for which environmental fluctuations occur over periods roughly equal to that species' generation time. In an effort to examine this notion, sources of seasonal variation in two components of oviposition behavior in an east Texas population of pipevine swallowtail butterflies (Battus philenor) were investigated under natural and seminatural conditions. Variability in a visually-based prealighting component involving orientation to leaf shape was primarily due to phenotypic plasticity in the form of adult learning; no seasonally-based genotypic differences in leaf-shape discrimination behavior were observed. By contrast, a chemotactile post-alighting component involving elicitation of oviposition after landing on the host plant was not phenotypically plastic, i.e., not susceptible to learning. In addition, only slight and nonsignificant seasonally-based differences in post-alighting responses to different host species were observed. © 1987 Springer-Verlag.
• Papaj, D. R., Prokopy, R. J., McDonald, P. T., & Wong, T. T. (1987). Differences in learning between wild and laboratory Ceratitis capitata flies. Entomologia Experimentalis et Applicata, 45(1), 65-72.
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  Abstract: Laboratory-reared and wild-collected adult female Mediterranean fruit flies, Ceratitis capitata Wiedemann, were exposed to two host fruit species, sweet orange (Citrus sinensis L.) and mock orange (Murraya paniculata Jack: Rutaceae). The effect of experience with a fruit species on acceptance of these fruit species (i.e., learning) differed between lab and wild females, but only for flies that were exposed to mock orange. Similar differences in fruit acceptance between lab and wild females were observed when individuals experienced with one fruit species were exposed to the other fruit species (i.e., switching). Finally, when each group was exposed to sweet orange, wild flies subsequently deprived of host fruit retained the effect of exposure on acceptance of mock orange 1 day longer than did lab flies subsequently deprived of host fruit. An hypothesis is presented by which selection under artificial culture gave rise to these differences. © 1987 Dr W. Junk Publishers.
• Prokopy, R. J., Papaj, D. R., Opp, S. B., & Wong, T. T. (1987). Intra-tree foraging behavior of Ceratitis capitata flies in relation to host fruit density and quality. Entomologia Experimentalis et Applicata, 45(3), 251-258.
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  Abstract: We examined the intra-tree foraging behavior of individually-released, wild-population Mediterranean fruit flies (medflies), Ceratitis capitata (Wiedemann), on field-caged host trees bearing each of three different densities (0, 3, or 12 per tree) of non-infested host fruit (kumquat) or each of two levels of fruit quality (12 non-infested fruit or 12 fruit infested with eggs and covered with host marking pheromone). With increasing density of non-infested fruit, medflies tended to remain longer in trees, visit more fruit before leaving, oviposit more often, accept a proportionately smaller number of fruit visited, and emigrate sooner after the last egg was laid (i.e. have a shorter Giving-Up-Time). Medflies spent much less time, oviposited much less often, and exhibited a longer Giving-Up-Time on trees harboring pheromone-marked fruit than non-infested fruit. Variation in temperature within the range at which experiments were conducted (25-36°C) had little detectable influence on foraging behavior. We compare our findings with published findings on the intra-tree foraging behavior of another tephritid fly, Rhagoletis pomonella (Walsh), and with current foraging behavior theory. We discuss implications of our findings with respect to medfly management strategies, particularly fruit stripping in eradication programs and use of synthetic marking pheromone for control. © 1987 Dr W. Junk Publishers.
• Papaj, D. R. (1986). Conditioning of leaf-shape discrimination by chemical cues in the butterfly, Battus philenor. Animal Behaviour, 34(5), 1281-1288.
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  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. © 1986.
• Papaj, D. R. (1986). Interpopulation differences in host preference and the evolution of learning in the butterfly, Battus philenor.. Evolution, 40(3), 518-530.
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  Abstract: Host-discrimination behaviour of adult female pipevine swallowtail butterfly was investigated for an E Texas population that uses 2 host species with different leaf shapes and a Virginia montane population that uses 1 host species with a single leaf shape. While Texas and Virginia females exhibited similar chemotactile responses after landing on various host species, butterflies from each population landed more frequently on certain host species used by that particular population. Despite this difference in searching behaviour, Texas and Virginia populations were equally capable of learning to search for the leaf shape of a particular host species in artificial enclosure arrays. Selection for restriction of learning of leaf-shape preference in the Virginia montane population may be constrained by selection for learning of other types of discrimination behaviour.-from Author
• Papaj, D. R. (1986). Leaf buds, a factor in host selection by Battus philenor butterflies.. Ecological Entomology, 11(3), 301-307.
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  Abstract: Identified a character intrinsic to Aristolochia reticulata host plants, the terminal leaf bud, that is involved in host-selection behaviour by female pipevine swallowtail butterflies searching for oviposition sites. -from Author
• Papaj, D. R. (1986). Shifts in foraging behavior by a Battus philenor population: field evidence for switching by individual butterflies. Behavioral Ecology and Sociobiology, 19(1), 31-39.
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  Abstract: A bivoltine east Texas population of the pipevine swallowtail butterfly (Battus philenor) exhibits a seasonal shift in the shapes of non-host leaves upon which ovipositing females land. Field mark-recapture studies and analysis of the behavior of wild females of different ages were used to distinguish between two alternative mechanisms for the shift in the populations's predominant leaf-shape search mode: seasonal differences in the outcome of learning for successively emerging naive foragers which exhibit one preference for most of their lives vs. synchronous switching by experienced foragers from one learned preference to another. Results supported each hypothesis: (1) Since wild butterflies are short-lived, the seasonal shift in searching behavior must reflect at least partly the successive emergence of naive females that learn to prefer host species with different leaf shapes. The leaf-shape preferences of older females were, in fact, stronger and less variable than those of younger individuals. About 80% of 51 marked individuals maintained stable leaf-shape search modes over recapture events, exhibiting slightly stronger preferences in later observation periods. (2) Almost 16% of marked females switched search modes across recapture events. Unmarked females sometimes switched search modes within an observation period; switching occurred only after the discovery of the host species with a leaf shape differing from that originally preferred. Switching by individual butterflies was generally more frequent at the time an adult brood shifted from one dominant search mode to another. Individual switching within an adult brood was more common in those years in which the population's shift in predominant search mode occurred during that brood. The evolution of rapid learning by naive females and conservative switching by experienced females is discussed in relation to a quantitative model of switching dynamics. © 1986 Springer-Verlag.
• Papaj, D. R., & Prokopy, R. J. (1986). Phytochemical basis of learning in Rhagoletis pomonella and other herbivorous insects. Journal of Chemical Ecology, 12(5), 1125-1143.
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  PMID: 24307051;Abstract: 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 insect's 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. © 1986 Plenum Publishing Corporation.
• Prokopy, R. J., Papaj, D. R., Cooley, S. S., & Kallet, C. (1986). On the nature of learning in oviposition site acceptance by apple maggot flies. Animal Behaviour, 34(PART 1), 98-107.
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  Abstract: In a previous study, we found that after a female apple maggot fly, Rhagoletis pomonella, had arrived on a host fruit, its propensity to accept (bore into) or reject that fruit prior to egg deposition was modifiable through experience, and hence involved learning. Here, we aimed to determine whether the true nature of the learned response was either (a) one in which a conditioned female, as a result of having become familiar with a particular fruit type, formed a greater propensity to accept that type in a future encounter than had a naive female, or (b) one in which a conditioned female formed no greater propensity to accept a particular fruit type but simply was less prone than a naive female to accept a novel fruit type. The results of two experiments supported the latter mechanism, while the results of a third experiment provided evidence for both mechanisms. The possible adaptive significance of learning to refuse a novel resource type is discussed. © 1986.
• Rausher, M. D., & Papaj, D. R. (1983). Demographic consequences of discrimination among conspecific host plants by Battus philenor butterflies.. Ecology, 64(6), 1402-1410.
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  Abstract: Discrimination has no detectable effect on larval growth rates or on predispersal mortality but does appear to enhance larval survival by increasing larval size at dispersal. The effects of discrimination among conspecific hosts on larval survival are similar in magnitude to analogous effects of discrimination between host species.-from Authors
• Rausher, M. D., & Papaj, D. R. (1983). Host plant selection by Battus philenor butterflies: Evidence for individual differences in foraging behaviour. Animal Behaviour, 31(2), 341-347.
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  Abstract: A previous study reported that individual females of the pipevine swallowtail butterfly, Battus philenor, exhibit different search modes when searching for host plants on which to oviposit. However, an alternative explanation for the results of that study exists: apparent differences in searching behaviour may simply represent differences in the composition of the vegetation over which females fly. The results from the present study rule out this alternative explanation and indicate that apparent differences in search mode reflect underlying differences among females in response to leaf shape. © 1983.

Presentations

• Bronstein, J., Papaj, D. R., Alarcon, R., Davidowitz, G., & Smith, G. (2018, January). Intraspecific variation in nectar use by foraging hawkmoth. American Society of Naturalists. Asilomar, CA: American Society of Naturalists.
• Essenberg, C. J., & Papaj, D. R. (2014, April). Bumblebee patch departure decisions at two spatial scales. Entomological Society of America, Pacific Branch, Annual Meeting. Tucson, AZ, USA: Entomological Society of America.
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  Symposium Title: Pollination Biology: Ecological, Evolutionary, and Behavioral Perspectives.
• Essenberg, C. J., Easter, R. A., Simmons, R. A., Benzing, K. R., McKay, A. M., & Papaj, D. R. (2014, August). Do bees prefer flowers with informative cues indicating rewards?. Animal Behavior Society, Annual Meeting. Princeton, NJ: Animal Behavior Society.
• Francis, J., Papaj, D. R., & Leonard, A. S. (2014, April). Constancy in bees with respect to floral rewards. Entomological Society of America, Pacific Branch, Annual Meeting. Tucson, AZ, USA: Entomological Society of America.
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  Symposium Title: Pollination Biology: Ecological, Evolutionary, and Behavioral Perspectives.
• Mitra, C., Davidowitz, G., & Papaj, D. R. (2014, August). Passing the salt: Nuptial gifts in a swallowtail butterfly. International Society for Behavioral Ecology (ISBE).
• Mitra, C., Davidowitz, G., & Papaj, D. R. (2014, July). Puddling behavior by male butterflies: who, where and what. International Society of Behavioral Ecology, Triennial Meeting. New York, NY, USA: International Society of Behavioral Ecology.
• Muth, F., Papaj, D. R., & Leonard, A. (2014, April). Bees learn floral cues using only pollen rewards.. Entomological Society of America, Pacific Branch Annual Meeting. New York, NY, USA: Entomological Society of America.
• Muth, F., Papaj, D. R., & Leonard, A. (2014, July). Bees learn floral cues using only pollen rewards.. International Society of Behavioral Ecology, Triennial Meeting. New York, NY, USA: International Society of Behavioral Ecology.
• Nielsen, M. E., & Papaj, D. R. (2014, July). Interactions among different forms of phenotypic plasticity: how caterpillars stay cool. 2014. Evolution 2014 Conference. Raleigh, NC, USA: Society for Evolution.
• Papaj, D. R., Buchmann, S., Muth, F., Russell, A., Francis, J., & Leonard, A. S. (2014, July). Multiple signals, multiple outcomes: Do bumble bees learn floral color signals in multiple reward contexts?. International Society of Behavioral Ecology, Triennial Meeting. New York, NY, USA: International Society of Behavioral Ecology.
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  Symposium Title: Color Signals in Terrestrial Invertebrates: Integrating Senders and Receivers
• Papaj, D. R., Leonard, A. S., Buchmann, S., Muth, F., Russell, A., & Francis, J. (2014, April). Multiple signals, multiple outcomes: Do bumble bees learn floral color signals in multiple reward contexts?. Entomological Society of America, Pacific Branch, Annual Meeting. Tucson, AZ, USA: Entomological Society of America.
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  Symposium Title: Pollination Biology: Ecological, Evolutionary, and Behavioral Perspectives.
• Russell, A., Leonard, A. S., Buchmann, S., & Papaj, D. R. (2014, April). Bringing big data to small bees: patterns of reward specialization. Entomological Society of America, Pacific Branch, Annual Meeting. Tucson, AZ, USA: Entomological Society of America.
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  Symposium Title: Pollination Biology: Ecological, Evolutionary, and Behavioral Perspectives.
• Essenberg, C. J., & Papaj, D. R. (2013, August). Do bumblebees match their foraging movements to the scale of resource patchiness?. 2nd International Conference on Pollinator Biology, Health and Policy. College Station, PA, USA: Penn State University.
• Nielsen, M. E., & Papaj, D. R. (2013, June). Interaction between size and behavioral plasticity in Battus philenor: how caterpillars stay cool. Society for Evolution Annual Meeting. Snowbird, UT: Society for Evolution.
• Papaj, D. R. (2013, April). Learning and uncertainty in plant-insect interactions: Studies with butterflies and bees. University of Nevada, Reno, Department Seminar Series. Reno, NV: University of Nevada, Reno.
• Papaj, D. R. (2013, November). Resource uncertainty in plant-pollinator interactions: Studies with butterflies and bees. ASU West, Department Seminar Series. Arizona State University, West Campus, Glendale, AZ: Arizona State University, West Campus.
• Papaj, D. R., & Papaj, D. R. (2013, August). Resource uncertainty in plant-pollinator interactions: Studies with bumble bees. 2nd International Conference on Pollinator Biology, Health and Policy. College Station, PA, USA: Penn State University.
• Nielsen, M. E., & Papaj, D. R. (2012, July). Size and thermal refuge seeking behavior in Battus philenor caterpillars. Animal Behavior Society National Meeting. University of New Mexico, Albuquerque, NM: Animal Behavior Society.
• Papaj, D. R. (2012, April). Signal uncertainty in plant-insect interactions: Studies with butterflies and bees. University of Illinois, Department Seminar Series. Champagne-Urbana, Illinois: University of Illinois.
• Dunlap, A. S., Dornhaus, A. R., & Papaj, D. R. (2011, June). Effects of reliability on whether to follow social or floral signals in foraging bumblebees. International Conference, Social Decision Making: Bridging Economics and Evolutionary Biology. Monte Verita, Switzerland.
• Dunlap, A. S., Dornhaus, A. R., & Papaj, D. R. (2011, June). When to acquire new information? How persistence and reward affect sampling and tracking in foraging bumblebees. 18th Annual International Conference on Comparative Cognition. Melbourne, FL.
• Dunlap, A. S., Dornhaus, A., & Papaj, D. R. (2011, August). When should bumblebees use social information? Effects of reliability of floral and social cues.. Animal Behavior Society, Annual Meeting. Bloomington, IN: Animal Behavior Society.
• Leonard, A. S., & Papaj, D. R. (2011, August). The possible benefits of nectar guides to plants and bees. Animal Behavior Society, Annual Meeting. Bloomington, IN: Animal Behavior Society.
• Leonard, A. S., Dornhaus, A. R., & Papaj, D. R. (2010, July). Odors facilitate perception of color cues in bumble bees. International Society of Behavioral Ecology, Triennial Meeting. Perth Australia: International Society of Behavioral Ecology.
• Papaj, D. R. (2011, April). Floral complexity, signal uncertainty and learning. University of California, San Diego, Department Seminar Series. San Diego, CA: UC San Diego, Section of Ecology & Evolutionary Biology.
• Leonard, A. S., Dornhaus, A. R., & Papaj, D. R. (2010, August). Signal detectability and the function of complex floral signals. Animal Behavior Society, Annual Meeting. Williamsburg, VA: Animal Behavior Society.
• Papaj, D. R. (2010, January). Floral complexity, signal uncertainty and learning. University of California, Davis, Department Seminar Series. Davis, CA: UC Davis, Section of Ecology & Evolutionary Biology.
• Papaj, D. R. (2010, January). Signal complexity, uncertainty and learning. University of Massachussetts Alexander Speaker Series. Amherst, MA: UMass Amherst Department of Plant and Insect Science.
• Papaj, D. R. (2010, July). Use of red hosts by butterflies: The challenge of low detectability. International Conference on the Biology of Butterflies. University of Edmonton, Edmonton, Canada.
• Papaj, D. R., Dornhaus, A. R., & Dunlap, A. S. (2010, July). When to acquire new information? How persistence and reward affect sampling, tracking, and constancy in bumblebees. Meeting, International Union for the Study of Social Insects. Copenhagen, Denmark: International Union for the Study of Social Insects.
• Papaj, D. R., Leonard, A. S., & Dornhaus, A. R. (2010, August). Floral complexity, speed-accuracy tradeoffs, and the neuroeconomics of nectar-foraging in bees. Animal Behavior Society, Annual Meeting. Williamsburg, VA: Animal Behavior Society.
• Papaj, D. R. (2009, July). Signal uncertain and learning plant-insect interactions. Insect Learning Workshop. Roscoff, France.

Poster Presentations

• Russell, A., & Papaj, D. R. (2015, January). The role of experience in floral sonication behavior by a bumble bee. Society for Integrative and Comparative Biology. West Palm Beach, FL: Society for Integrative and Comparative Biology.
• Francis, J. S., Muth, F., Papaj, D. R., & Leonard, A. S. (2014, Augus). Separating pollinator constancy into flowers and rewards: A new look at an old phenomenon. Ecological Society of America National Meeting. Sacramento, CA: Ecological Society of America.
• Nielsen, M., & Papaj, D. R. (2014, January). Interactions between behavioral thermoregulation and color change in pipevine swallowtail caterpillars (Battus philenor). Society for Integrative and Comparative Biology. Austin, TX: Society for Integrative and Comparative Biology.
• Nielsen, M., & Papaj, D. R. (2014, July). Interactions between behavioral thermoregulation and color change in pipevine swallowtail caterpillars (Battus philenor). Entomological Society of America, Pacific Branch Annual Meeting. Tucson, AZ: Entomological Society of America.
• Russell, A. L., Morrison, S. J., & Papaj, D. R. (2014, July). Bringing big data to small bees: patterns of reward specialization.. Sigma Xi International Research Conference. Tempe, AZ: Sigma Xi.
• Russell, A. L., Morrison, S. J., Leonard, A. S., Papaj, D. R., & Buchmann, S. (2014, July). Bringing big data to small bees: patterns of reward specialization.. International Society of Behavioral Ecology, Triennial Meeting. New York, NY, USA: International Society of Behavioral Ecology.
• Essenberg, C. J., & Papaj, D. R. (2013, July). Do bumblebees match their foraging movements to the scale of resource patchiness?. Animal Behavior Society National Meeting. University of Colorado: Animal Behavior Society.
• Mitra, C., Davidowitz, G., & Papaj, D. R. (2013, July). Puddling behavior in butterflies: effects on male mating success. Animal Behavior Society National Meeting. University of Colorado: Animal Behavior Society.
• Nielsen, M. E., & Papaj, D. R. (2013, October). Interactions between behavioral thermoregulation and color change in pipevine swallowtail caterpillars (Battus philenor).. Symposium on Research Insights in Semiarid Ecosystems (RISE).. Tucson, AZ: University of Arizona.
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  Won Best Poster competition
• Russell, A., & Papaj, D. R. (2013, March). Bringing big data to small bees.. Entomology and Insect Science GIDP Showcase Poster Competition. Tucson, AZ: University of Arizona GIDP.
• Wang, D. I., & Papaj, D. R. (2013, January). The role of larval dietary carotenoids in an adult butterfly’s foraging behavior. Society for Integrative and Comparative Biology. San Francisco, CA: Society for Integrative and Comparative Biology.
• Wang, D. L., & Papaj, D. R. (2013, April). Color preference in the pipevine swallowtail, Battus philenor: is hue or brightness more important?. 1st Annual School of Mind, Brain, and Behavior Poster Session. Tucson, AZ: University of Arizona.
• Papaj, D. R., Wang, D. I., Nielsen, M. E., & Kaczorowski, R. (2012, July). Pollinator behavior and the persistence of rare floral morphs. Animal Behavior Society National Meeting. University of New Mexico, Albuquerque, NM: Animal Behavior Society.
• Wang, D. L., & Papaj, D. R. (2012, January). Color preference in the pipevine swallowtail, Battus philenor: is hue or brightness more important?. Society for Integrative and Comparative Biology. Charleston, SC: Society for Integrative and Comparative Biology.
• Wang, D. L., & Papaj, D. R. (2012, July). Color preference in the pipevine swallowtail, Battus philenor: is hue or brightness more important?. Animal Behavior Society. University of New Mexico, Albuquerque, NM: Animal Behavior Society.
• Jones, B., Leonard, A. S., Papaj, D. R., & Gronenberg, W. (2011, August). The role of multimodal experience in bumble bee brain development. Animal Behavior Society, Annual Meeting. Bloomington, IN: Animal Behavior Society.
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  won Honorable Mention for Best Poster
• Papaj, D. R., Leonard, A. S., & Dornhaus, A. R. (2011, July). Speed-accuracy tradeoffs and nectar-foraging in bees: merging neuroeconomics with optimality theory. Gordon Conference on Neuroethology and Evolution. Eaton, MA: Gordon Conferences.
• Wang, D. I., & Papaj, D. R. (2011, July). Color preference in the pipevine swallowtail, Battus philenor: Is hue or brightness more important?. Animal Behavior Society National Meeting. Bloomington, IN: Animal Behavior Society.
• Dunlap, A. S., Papaj, D. R., & Dornhaus, A. R. (2010, May). Tracking of a variable environment: experiments with bees. Workshop on Social Biomimicry: Insect Societies and Human Design,. Tempe, AZ: Arizona State University.
• Kaczorowski, R. L., Leonard, A. S., Dornhaus, A. R., & Papaj, D. R. (2010, July). Do bumblebees match their foraging movements to the scale of resource patchiness?. Animal Behavior Society National Meeting. Bloomington, IN: Animal Behavior Society.

Others

• Russell, A. L., Leonard, A. S., & Papaj, D. R. (2015, APR). The role of experience in floral sonication behavior by a bumble bee. INTEGRATIVE AND COMPARATIVE BIOLOGY.