Abstract
Foraging theory assumes that animals assess value based on objective payoffs; however, animals often evaluate rewards comparatively, forming expectations based on recent experience. This ...form of evaluation may be particularly relevant for nectar foragers such as bumblebees, where individuals can visit thousands of flowers daily that vary in nectar quality. While many animals, including bees, demonstrate reference-based evaluation in experimental contexts, it is unclear whether this occurs in the wild. Here, we asked how daily experience with wildflower nectar influenced wild bumblebees’ reward evaluation. We measured the daily nectar concentration of bee-visited wildflowers (Penstemon spp.), before presenting foragers with conspecific flowers filled with a range of artificial nectar concentrations. We recorded bees’ acceptance of artificial nectar, the probability of subsequent visits to flowers on the same plant, and residence time. While bees had a minimum threshold of nectar acceptability that was unaffected by experience, when there was higher-concentration environmental nectar, they were less likely to accept lower-quality rewards on manipulated plants. Bees also visited more flowers and stayed longer on plants with higher-concentration nectar. This study shows evidence for both absolute and reference-based evaluation in wild bees and points towards differences between bees’ behavior in lab- and wild-foraging contexts.
While classic models of animal decision-making assume that individuals assess the absolute value of options, decades of research have shown that rewards are often evaluated relative to recent ...experience, creating incentive contrast effects. Contrast effects are often assumed to be purely sensory, yet consumer and experimental psychology tell us that label-based expectations can affect value perception in humans and rodents. However, this has rarely been tested in non-model systems. Bumblebees forage on a variety of flowers that vary in their signals and rewards and show contrast when rewards are lowered. We manipulated bees' expectations of stimulus quality, before downshifting the reward to induce incentive contrast. We found that contrast effects were not solely driven by experience with a better reward, but also influenced by experience with associated stimuli. While bees' initial response did not differ between treatments, individuals were faster to accept the lower-quality reward when it was paired with a novel stimulus. We explored the boundaries of these label-based expectations by testing bees along a stimulus gradient and found that expectations generalized to similar stimuli. Such reference-dependent evaluations may play an important role in bees' foraging choices, with the potential to impact floral evolution and plant community dynamics.
Over a century of research on pollinator cognition has shown that pollinators such as bees perceive and learn a multitude of floral stimuli and are capable of sophisticated decision-making using a ...variety of cognitive abilities.Research on pollinator cognition usually focuses on a single reward aspect in isolation, which does not reflect the complexity of reward types, chemistries, and attributes many pollinators encounter while foraging.Reward complexity can impact pollinators’ perception, learning, and decision-making in interesting and sometimes unexpected ways.A cognitive perspective can shed new insight into the functions of floral reward complexity and bridge the fields of animal behavior and plant ecology.
The cognitive ecology of pollination is most often studied using simple rewards, yet flowers often contain multiple types of chemically complex rewards, each varying along multiple dimensions of quality. In this review we highlight ways in which reward complexity can impact pollinator cognition, demonstrating the need to consider ecologically realistic rewards to fully understand plant–pollinator interactions. We show that pollinators’ reward preferences can be modulated by reward chemistry and the collection of multiple reward types. We also discuss how reward complexity can mediate pollinator learning through a variety of mechanisms, both with and without reward preference being altered. Finally, we show how an understanding of decision-making strategies is necessary to predict how pollinators’ evaluation of reward options depends on the other options available.
The cognitive ecology of pollination is most often studied using simple rewards, yet flowers often contain multiple types of chemically complex rewards, each varying along multiple dimensions of quality. In this review we highlight ways in which reward complexity can impact pollinator cognition, demonstrating the need to consider ecologically realistic rewards to fully understand plant–pollinator interactions. We show that pollinators’ reward preferences can be modulated by reward chemistry and the collection of multiple reward types. We also discuss how reward complexity can mediate pollinator learning through a variety of mechanisms, both with and without reward preference being altered. Finally, we show how an understanding of decision-making strategies is necessary to predict how pollinators’ evaluation of reward options depends on the other options available.
Mating signals have evolved to attract target receivers, even to the point of exploiting receivers through perceptual manipulation. Signals, however, can also expose signalers to nontarget receivers, ...including predators and parasites, and thus have also evolved to decrease enemy attraction. Here we show that male tree frogs (Smilisca sila) reduce their attractiveness to eavesdropping enemies (bats and midges) by overlapping their calls at near-perfect synchrony with the calls of neighboring conspecifics. By producing calls that closely follow those of other males, synchronizing S. sila take advantage of an auditory illusion where enemies are more attracted to the leading call. Female S. sila, however, are less susceptible to this illusion. Thus, synchronization among signaling males can result in acoustic crypsis from predators without affecting female attraction. Given the widespread use of conspicuous mating signals and eavesdropping enemies, perceptual exploitation of eavesdroppers is likely a common driver of signal evolution.
Emitting conspicuous signals into the environment to attract mates comes with the increased risk of interception by eavesdropping enemies. As a defence, a commonly described strategy is for ...signallers to group together in leks, diluting each individual's risk. Lekking systems are often highly social settings in which competing males dynamically alter their signalling behaviour to attract mates. Thus, signalling at the lek requires navigating fluctuations in risk, competition and reproductive opportunities. Here, we investigate how behavioural defence strategies directed at an eavesdropping enemy have cascading effects across the communication network. We investigated these behaviours in the túngara frog (
), examining how a calling male's swatting defence directed at frog-biting midges indirectly affects the calling behaviour of his rival. We found that the rival responds to swat-induced water ripples by increasing his call rate and complexity. Then, performing phonotaxis experiments, we found that eavesdropping fringe-lipped bats (
) do not exhibit a preference for a swatting male compared to his rival, but females strongly prefer the rival male. Defences to minimize attacks from eavesdroppers thus shift the mate competition landscape in favour of rival males. By modulating the attractiveness of signalling prey to female receivers, we posit that eavesdropping micropredators likely have an unappreciated impact on the ecology and evolution of sexual communication systems.
Decisions tend to become more challenging as the number of available options increases and choice sets become more complex. Choosing between multiple options may require additional information ...processing time and effort. Here, we asked if response time increases with stimulus number and attractiveness by female frogs (Physalaemus pustulosus) and their predators, frog-eating bats (Trachops cirrhosus), when comparing the mating calls of male túngara frogs. We found that frogs’ response time is significantly longer when presented with two calls, compared with one. Bats also take longer to respond when presented with two calls but only when they were complex calls. Although the frogs and bats behave somewhat similarly in this experiment, the decisions that these animals are making are occurring in different domains (mating vs. foraging) and have different fitness consequences. Given these differences, we find it especially interesting that for both frogs and bats, we see similar temporal patterns in response times as a function of information load.
Most models of animal behavior assume rationality in animal's decisions, with animals maintaining strict preferences for different options (e.g., optimal foraging theory). In the wild, however, ...animals often choose among several options simultaneously, and their evaluation of each prey type may depend on the perceived relative values of other choices. Fringe-lipped bats (Trachops cirrhosus) are promising subjects for studying how animals make decisions. When given a choice between the calls of two species of frogs, T. cirrhosus will choose the more salient call that is associated with the higher capture rate. Although in the wild T. cirrhosus often choose among multiple call options, most tests of prey preferences in this system include only two options. In this experiment, we tested whether T. cirrhosus alters relative preference for two call types that differ along two acoustic dimensions (amplitude and complexity) when presented with a third, "decoy" option, inferior to the two original options along either one or both dimensions. Results from this study demonstrate that under these circumstances, T. cirrhosus evaluates all three options independently of one another, and thus, preferences remain consistent and rational in both the presence and absence of a decoy. These results counter many other experiments suggesting irrationality in animal decision-making.
Humans and other animals have been shown to exhibit preferences for options previously associated with greater past need. Such studies indicate that animals are sensitive to both the physical ...properties of choices and their own state-dependent gains at the time of learning. Because this behaviour appears to occur across divergent taxonomic groups, it most likely reflects a common way that animals learn about food. Here we study this phenomenon in the frog-eating bat, Trachops cirrhosus. This carnivorous bat hunts by eavesdropping on frog and insect mating calls and its diet is both broad and seasonally variable. As a result, these bats must learn about new sources of food and possibly the state-dependent gains associated with those sources. In this experiment we trained bats to associate two different acoustic cues (ringtones) to two identical food rewards. Each ringtone was encountered in one of two nutritional states: hungry or pre-fed. We then tested preferences between these cues under both nutritional states. We found that bats overwhelmingly preferred the ringtone associated with previous greater deprivation regardless of their condition during testing. We argue that it is most likely adaptive for frog-eating bats to place a higher value on food rewards that are obtained when internal reserves are low.
•Properties of prey and state-dependent gains of predators may affect learning.•We tested whether bats' nutritional state during learning affects food preferences.•Bats preferred cues that they learned when they were in a hungry state.•Reliance on internal state as a cue to food availability is most likely adaptive.
Animals are expected to optimize energy intake when choosing between different foraging options. A common explanation for deviations from optimal economic decisions is that there is an imperfect ...relationship between physical reality and an animal's perceptual processes, which can constrain assessment of profitability. One such phenomenon that is apparently ubiquitous across taxa is proportional processing, where a perceived change in a stimulus is proportional to the change in stimulus magnitude. In this study, we investigated whether proportional processing explains how frog-eating bats, Trachops cirrhosus, discriminate between patches of frog choruses that vary in their number of calling frogs. To test this, we created artificial choruses consisting of one to six calling frogs. In the flight cage, we then tested the preference of bats (N=17) with every pairwise combination of chorus size. We found that while bats generally preferred larger choruses, preferences for larger choruses were better explained by the relative, not absolute, differences in chorus sizes. This indicates that T. cirrhosus is perceptually limited in its ability to discriminate between choruses of varying size as the choruses increase in size. Foragers are likely to be less choosy when choosing among larger patches.
•We investigated perceptual limitations in patch size assessment in frog-eating bats.•Frog-eating bats preferred larger choruses, with more calling frogs.•Bats attended to relative, not absolute, differences when choosing larger chorus sizes.
Most models of animal foraging assume that individuals make decisions rationally. One expectation of rationality theory is that preferences should be hierarchical or transitive. For many animals, ...including humans, making decisions about what to eat can become difficult when various parameters of choices are not positively related to one another and no single option may be considered the best. These complex decisions can result in irrational behaviour, suggesting that the value of any particular option may vary depending on the other available options. Here, we tested whether frog-eating bats, Trachops cirrhosus, are transitive in their preferences for frog calls. These bats attend to several attributes of the calls, such as call amplitude and complexity, when choosing a frog to target in their attack. While acoustic preferences are largely understood in isolation, we have a limited understanding of how bats choose between calls that vary along several important acoustic dimensions. Here, we conducted a series of binary choice experiments manipulating amplitude and complexity both separately and together to evaluate whether these bats make transitive foraging decisions. We found that bats are transitive in their rankings of calls based on these acoustic dimensions, with preferences reflecting a trade-off between both amplitude and complexity. Overall, our results add support to the notion that bats' preferences obey the general principles of rational behaviour and support the use of optimality approaches to the study of animal behaviour and decision making.
•Animal foraging models assume hierarchical preferences, but evidence is mixed.•Frog-eating bats showed linear preferences for calls that varied in amplitude.•Bats preferred calls with chucks and calls with more chucks up to a threshold.•When chucks and amplitude were varied, bats showed transitive preferences.
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