Abstracts of selected (pre)prints
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n Abstract This review focuses on five key evolutionary issues pertaining to animal cognition, defined as the neuronal processes concerned with the acquisition, retention, and use of information. Whereas the use of information, or decision making, has been relatively well examined by students of behavior, evolutionary aspects of other cognitive traits that affect behavior, including perception, learning, memory, and attention, are less well understood. First, there is ample evidence for genetically based individual variation in cognitive traits, although much of the information for some traits comes from humans. Second, several studies documented positive association between cognitive abilities and performance measures linked to fitness. Third, information on the evolution of cognitive traits is available primarily for color vision and decision making. Fourth, much of the data on plasticity of cognitive traits appears to reflect nonadaptive phenotypic plasticity, perhaps because few evolutionary analyses of cognitive plasticity have been carried out. Nonetheless, several studies suggest that cognitive traits show adaptive plasticity, and at least one study documented genetically based individual variation in plasticity. Fifth, whereas assertions that cognition has played a central role in animal evolution are not supported by currently available data, theoretical considerations indicate that cognition may either increase or decrease the rate of evolutionary change.
Male fruit flies learn to avoid interspecific courtship
Reuven Dukas
Experimental data suggest, and theoretical models typically assume, that males of many fruit flies (Drosophila spp) are at least partially indiscriminate while searching for mates, and that it is mostly the females who exert selective mate choice, which can lead to incipient speciation. Evidence on learning by male D. melanogaster in the context of courtship, however, raises the possibility that the initially indiscriminate males become more selective with experience. I tested this possibility by comparing the courtship behavior of male D. melanogaster experienced at courting females of the closely related species, D. simulans, and inexperienced males. I found that, compared to the inexperienced males, the males experienced with courting D. simulans females showed significantly lower courtship towards female D. simulans. Both male treatments, however, showed virtually identical courtship durations with female D. melanogaster. These results indicate that male fruit flies adaptively refine their courtship behavior with experience and suggest that the males contribute more to assortative mating and incipient speciation than commonly assumed.
Causes and consequences of limited attention
Reuven Dukas
This review focuses on the evolutionary causes and consequences of limited attention, defined as the restricted rate of information processing by the brain. The available data suggest, first, that limited attention is a major cognitive constraint determining animals’ search for cryptic food, and, second, that limited attention reduces animals’ ability to detect predators while involved in challenging tasks such as searching for cryptic food. These two effects of limited attention probably decrease animal fitness. Furthermore, a simulated evolutionary study provides empirical support for the prediction that focused attention by predators selects for prey polymorphism. The neurobiological mechanisms underlying limited attention have been widely studied. A recent incorporation of that mechanistic knowledge into an ecological model suggests that limited attention is an optimal strategy that balances effective yet economical search for cryptic objects. The review concludes with a set of testable predictions aimed to expand the currently limited empirical knowledge on the evolutionary ecology of limited attention.
Environmental enrichment improves mating success in fruit flies
REUVEN DUKAS AND ARNE ø MOOERS
Environmental enrichment, defined as housing conditions that include a combination of complex inanimate and social stimulation, has strong positive effects on brain and behaviour in various species. Here we extend previous studies to evaluate how enrichment affects mating success. In a series of experiments, we found that male fruit flies (Drosophila melanogaster) reared in an enriched environment were twice as successful in acquiring mates as were males from standard rearing conditions. The dominant factor increasing mating success was the larger space available per fly. Flies from enriched and standard environments showed no significant behavioural differences, leading us to suggest that different social environments at high and low per capita spaces are associated, on average, with either subtle behavioral differences or distinct pheromonal profiles to which females are sensitive while choosing mates.
Behavioural and ecological consequences of limited attention
Reuven Dukas
Ecological research in the past few decades has shown that most animals acquire and respond adaptively to information that affects survival and reproduction. At the same time, neurobiological studies have established that the rate of information processing by the brain is much lower than the rate at which information is encountered in the environment, and that attentional mechanisms enable the brain to focus only on the most essential information at any given time. Recent integration of the ecological and neurobiological approaches helps us understand key behaviours with broad ecological and evolutionary implications. Specifically, current data indicate that limited attention affects diet choice and constrains animals’ ability to simultaneously feed and attend to predators. Recent experiments also suggest that limited attention influences social interactions, courtship and mating behaviour.
The behavioral ecology of a cognitive constraint: limited attention
Colin W. Clark and Reuven Dukas
Limited attention may constrain animal behavior in situations where the rate of relevant information exceeds the brain’s threshold processing capacity. Here we examine why attention is limited by quantifying how attention affects the ubiquitous problem of balancing foraging and antipredator activity. We analyze how a given attentional capacity affects feeding requirements, the optimal attentional focus during predator scanning, and the probability of detecting predators. Our model indicates that, because of the complex interplay between the costs and benefits associated with a given attentional capacity, limited attention can be an optimal strategy, which allows effective and economical search for cryptic objects.
Crab spiders affect flower visitation by bees
Reuven Dukas and Douglass H. Morse
In a field experiment, the bumblebee, B. ternarius, visited milkweed patches harboring crab spiders, Misumena vatia, at a lower frequency than patches free of crab spiders, and honeybees showed a similar trend. Two other bumblebee species, B. terricola and B. vagans, did not avoid the spider patches. The latter two species are larger than B. ternarius and honeybees and suffer lower crab-spider predation. As far as we know, this is the first field study documenting negative effects of predators on flower visitation rate by pollinator populations. Our study suggests that pollinator response to predation may influence pollinator-plant interactions.
EFFECTS OF PERCEIVED DANGER ON FLOWER CHOICE BY BEES
REUVEN DUKAS
Studies on animal-flower interactions have mostly neglected the third trophic level of pollinators’ predators even though anti-predatory behavior of pollinators may affect patterns of pollinator visitation, pollen transfer and floral traits. In three experiments, I found that honeybees showed sensitivity to perceived danger at flowers by preferring apparently safe flowers over equally rewarding alternatives harboring either a dead bee or a spider, and avoiding revisitation of a site where the bees have escaped a simulated predation attempt. These results suggest that bees, like other animals, take anti-predatory measures, which may have far reaching effects on animal-flower interactions.
Reuven Dukas
Almost all pollination studies neglect the possible effects of predation on flower visitors. Various authors have even claimed that predation is too infrequent to influence pollinator behavior (Pyke 1979; Miller & Gass 1985; Morse 1986; Schmid-Hempel 1991). It is tempting to dismiss the role of predation because it is rarely observed. In the past two decades, however, ecologists have learned to appreciate the central role that predation risk plays in animal behavior and ecology, mostly through a variety of measures animals take to minimize predation. Studies on a wide variety of animals from zooplankton to mammals have suggested that predation risk affects: diurnal patterns of activity; choice of diet, habitat, food patches and food type; ways of handling food items; social organization; choice of nest sites; and various physiological factors such as diurnal and seasonal levels of fat reserves and respiration patterns (Price et al. 1980; Lawton 1986; Bernays & Graham 1988; Lima & Dill 1990; Clark 1993; Martin 1995; Lima 1998a, b; Ydenberg 1998).
Are flower visiting animals really immune to predation, or does the prevailing view about the unimportance of predation in pollination systems merely reflect researchers’ inattention? In this chapter, I shall review some of the literature and argue that pollination ecologists have mostly overlooked a central factor influencing pollinator traits and pollination systems. Specifically, I ask: (1) Are there significant levels of predation on pollinators? (2) How might predation affect pollinator traits? And, (3) how might predation influence pollinator-plant interactions?
CONCLUSIONS
The available evidence suggests significant levels of predation on pollinators. Hence the effect of predation risk should be integrated into future studies on pollinator behavior and pollinator-plant ecology and evolution. Currently, there are only few detailed accounts on attack and predation rates on pollinators, so further quantitative studies will be useful. Perhaps more important would be studies evaluating how predation affects pollinator behavior and plants. Throughout this chapter, I presented numerous ideas for the necessary experiments.
Limited attention: the constraint underlining search image
Reuven Dukas* and Alan C. Kamil
Recent models of predator search behavior integrate proximate neurobiological constraints with ultimate economic considerations. These models are based on two assumptions, which we have critically examined in a series of experiments with blue jays searching for artificial prey images presented on a computer monitor. We found, first, that when jays had to switch between searching for two or three distinct prey types, they showed no reduction in detection rates compared to no-switching conditions, and second, that when jays divided attention between searching for two prey types at the same time, they had lower detection rates than when they focused attention on one prey type at a time. Our results suggest that limited attention strongly affects predator search patterns and diet choice, including the ubiquitous tendency to form search images.
Learning improves growth rate in grasshoppers
Reuven Dukas*# & Elizabeth A. Bernays+
To quantify the adaptive significance of insect learning, we documented the behavior and growth rate of grasshoppers in an environment containing two artificial food types, one providing a balanced diet of protein and carbohydrate and the other being carbohydrate-deficient. Grasshoppers in the Learning treatment experienced a predictable environment, where the spatial location, taste and color of each food source remained constant throughout the experiment. In contrast, grasshoppers of the Random treatment developed in a temporally varying environment, where the spatial location, taste and color of the balanced and deficient food types randomly alternated twice each day. Our results show that the grasshoppers that could employ associative learning for diet choice experienced higher growth rates than individuals of the Random treatment, demonstrating the adaptive significance of learning in a small, short lived insect.
Fitness Consequences of Learning in a parasitoid wasp
Reuven Dukas and Jian Jun Duan
Several studies have documented associative learning in insects but the adaptive significance of such learning is not yet well understood. To evaluate this issue, we quantified long-term fitness consequences of learning in the parasitoid wasp, Biosteres arisanus. We compared individual wasps that were allowed to choose host substrate based on experience to wasps that could only make random substrate choice in an environment where only one out of two substrates contained host eggs. In two experiments, the lifetime number of host eggs parasitized and number of adult offspring was larger for the learning than random wasps. This is the first study documenting long term fitness consequences of learning.
The cost of limited attention in blue jays
Reuven Dukas and Alan C. Kamil
Experiments with fish and birds suggest that animals are unable to simultaneously allocate sufficient attention to tasks such as the detection of an approaching predator while searching for cryptic prey. We quantified the effects of limited attention on performance in controlled laboratory settings and report here the first direct evidence that attending to a difficult central task simulating foraging deters a bird's ability to detect a peripheral target, which could be a predator. Our results fill a gap between ecological and neurobiological studies by illustrating that although attention is an efficient filtering mechanism, limited attention may be a major cause of mortality in nature.
COSTS OF MEMORY: IDEAS AND PREDICTIONS
REUVEN DUKAS
Studies on the ecology of animal memory have focused on the benefits of memory while implicitly assuming that there are costs as well. Here I discuss probable costs of memory by relying on knowledge from molecular biology and physiology, which indicates that the maintenance of accurate information in animals is an active and costly process of maintenance and repair. Redundancy probably plays a key role in ensuring a high level of accuracy; its cost is in terms of additional tissue, which increases body mass and energetic expenditure. Examining the magnitude and cost of redundancy at the neurobiological and behavioral levels can help us understand the cost of memory in particular and cognitive abilities in general.
Ecological relevance of associative learning in fruit fly larvae
REUVEN DUKAS
A few invertebrate models have been used for studying neurobiological and molecular aspects of associative learning. The ecological and evolutionary aspects of associative learning in these invertebrates are not yet well understood. To further this knowledge, fruit fly larvae were tested for their ability to learn to associate odours with preferred environmental conditions. The larvae learned to avoid odours associated with predation and to prefer odours associated with high quality food, but they failed to learn about odours associated with optimal temperature. Further experiments are needed for establishing how well the larvae can learn about different environmental factors and distinct stimuli. It appears likely, however, that the larvae possess a general ability to evaluate a suite of environmental parameters and to associate preferred conditions with relevant stimuli.
THE SPATIAL DISTRIBUTION OF COLONIAL FOOD PROVISIONERS
REUVEN DUKAS* and LEAH EDELSTEIN-KESHET
We present spatially explicit models to predict the optimal distribution of numerous food provisioners that share a nesting aggregation. We compare predictions for solitary and social provisioners, and for three foraging currencies. When distinct food patches with identical food parameters are considered, fewer provisioners use the farther patches. The rate of decline in number of provisioners depends on the currency used. With net rate of energy intake (net energy gain over time), the rate of decline is relatively small under a wide range of realistic parameter values and distances; with efficiency (net energy gain over energy cost) and empirically derived energetic costs, the rate of decline is much higher. With lifetime fitness (lifetime food delivery under predation risk), outcomes depend on the ratio of mortality risk during flight and during food collection at the patch. With all currencies, there is a difference between the optimal spatial distribution of solitary and social provisioners, with a larger proportion of social provisioners being farther from the central place. The optimal distribution of solitary provisioners in a two dimensional field of uniformly distributed food such as a flowering meadow is such that the density of solitary provisioners (number per unit area) declines monotonically with distance, and provisioner number peaks at half the maximum area used.
3. Constraints on Information Processing and their Effects on Behavior
REUVEN DUKAS
Chapter 3 In: Cognitive Ecology: The Evolutionary Ecology of Information Processing and Decision Making (Ed. by R. Dukas). Chicago: University of Chicago Press.
SUMMARY
Various constraints limit the brain’s capacity to process information. Here I integrated neurobiological and psychological knowledge on such constraints with theory from behavioral ecology in order to (i) evaluate how cognitive constraints affect ecologically relevant behaviors of animals in their natural settings, and (ii) examine how evolutionary and ecological theory can help investigate the fundamental neuronal constraints, costs and tradeoffs that shape cognitive systems. First, the brain has a limited capacity to process information simultaneously and effectively. Increasing the amount of information a subject attends to may decrease the quality of information processing and the associated performance. Visual attention may be focused either on a small spatial portion of the visual field, or along various dimensions such as color and shape. While searching for cryptic prey, it is optimal to have a narrower spatial focus of attention than when searching for conspicuous food. This may be associated with a reduced rate of search for cryptic prey. That prediction is supported by experimental evidence. In addition, it may be beneficial to attend to a single visual attribute while searching for cryptic prey. This may imply searching for only one of several available prey types simultaneously; such phenomenon has been widely observed in numerous species. Limited attention restricts also the capacity of animals to monitor predator behavior and to search for food simultaneously.
Second, animals cannot sustain a high quality of information processing for extended periods. The consequent decrement in vigilance reduces performance on various behavioral tasks. This may affect temporal patterns of activity and rest. Third, working memory has a very limited capacity; however, it is still unclear whether that limitation constrains animal behavior. It is possible that animals, like human experts, can overcome this constraint. Fourth, it is commonly believed that long term memory is unlimited. But it is likely that maintaining memories is costly. One probable cost is due to interference between various items in memory. Interference, together with limited attention, most likely affects the tendency of animals to concentrate on a single activity at a time. Current theory and evidence illustrate the potential importance of cognitive constraints for the behavior of animals in the field. However, this knowledge must still be supplemented with rigorous experimental data. Moreover, further research is required in order to establish the neuronal foundations of cognitive constraints.
Evolutionary Ecology of Learning
REUVEN DUKAS
Chapter 4 In: Cognitive Ecology: The Evolutionary Ecology of Information Processing and Decision Making (Ed. by R. Dukas). Chicago: University of Chicago Press.
SUMMARY
This chapter addresses two aspects of learning. First, learning is discussed within the ecological framework of phenotypic plasticity. Studies of phenotypic plasticity have focused on a narrow range of plastic traits, where there is a consistent phenotypic response to some environmental variable. Such research has not evaluated complex types of reversible plasticity, such as learning, where animals record experience in memory and alter their responses to the environment throughout life. Here I assessed learning in relation to simpler forms of plasticity. Simple forms of reversible plasticity are effective as long as an identical phenotypic response is a sufficient adaptation to some frequent environmental change. An example is changes in pupil diameter in response to varying light intensities. By contrast, learning is favored where feedback from interactions with an environmental event can be used to improve the phenotypic response to subsequent occurrences of that event
The second issue addressed here is that various life history traits could have selected for different learning abilities. I examined the relative effects on learning of aspects of foraging, predation, mate choice, parental care, sociality, and life span. Rich learning capacities already appear even in short lived solitary species. However, the transition toward more complex learning appears to be associated with parental care and the lengthening of life span. I concluded by stressing the potential of comparative experimental studies, detailed in the section on life history and learning. Such empirical research could reveal critical steps in the evolution of learning. I also outlined further promising theoretical directions that would help place learning within a broader framework of phenotypic plasticity.