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Abstract

Maeterlinck did not mean to suggest that honeybees rival humans in intelligence — rather he saw in the bee a qualitatively different form of intelligence, tailored to the challenges of a profoundly different kind of society and lifestyle. Insects are strange “aliens from inner space”, with sensory and cognitive worlds wholly different from our own. The 19th century discovery that ants can detect ultraviolet light triggered a golden age in the exploration of the diversity of sensory systems of insects (and indeed other animals), identifying such abilities as magnetic compasses, electrosensitivity, polarization vision, and peculiar locations for sense organs such as the infrared sensors on the abdomens of some beetles or photoreceptors on the genitalia of some butterflies. Could insect minds be equally strange and diverse?

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... The optimization of such relations will be reflected in the amount of assimilates that the sink structures receive for growth, including flower development and fertilization. Besides, since tomato does not produce nectar, pollinating insects will feed on pollen produced by flowers and will take successive foraging decisions based on the quantity and quality of food that they receive during their visits (Chittka 2017;Borghi and Fernie 2018). Therefore, the pollinator's preference determined by foraging decisions could be used as an indicator of the physiological status of the plant and, ultimately, of yield under any environmental conditions. ...
... The experimental rootstocks include five introgression lines (ILs, #3, 4, 5, 6) derived from crosses between Solanum lycopersicum cv M82 with Solanum pennellii LA716 (Eshed and Zamir 1995), and with S. habrochaites LA1777 (rootstock #8), five domestic (rootstocks #7, 10, 13, 16, 18) and two wild (rootstocks #15, 17) accessions and three mutant lines affected in abscisic acid (rootstock #14) and ethylene (rootstocks #11, 12) production. Those hormones have been involved in rootstock-mediated responses to salinity and nutrient stress in tomato (Martínez-Andújar et al. 2016, 2017 The sowing of scion and rootstock seeds was synchronized to obtain the appropriate stem diameter to ensure grafting viability and homogenous grafted plants. The graft was performed using the splicing method at the 2-3 true leaf stage (3-4 weeks after sowing), and the scion was attached at the first node of the rootstock. ...
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Aims Since producing more with less is required for increasing agricultural sustainability and reducing its environmental impact, breeding varieties with increased yield stability under reduced fertilizer application is an important goal, particularly in high valued horticultural crops such as tomato (Solanum lycopersicum L.). However, because of the difficulties to conciliate yield and fertilizer use efficiency through breeding, the graft-compatible genetic biodiversity existing in horticultural species offers the possibility to directly approach this objective in high-yielding elite varieties through improving nutrient capture and promoting ecosystem services such as insect pollination. We hypothesized that rootstocks affect pollinator foraging decisions through the nutritional status that impacts yield. Methods Fifteen genetically diverse experimental rootstocks were grafted to a scion tomato variety and cultivated under optimal and reduced (25% of optimal) P and NPK fertilization in the presence of managed bumblebee pollinators (Bombus terrestris). Results Up to twofold yield variability between rootstocks was associated with leaf nutrition and photosynthesis of the scion. Interestingly, fertilization regime and the rootstock genotype influenced the pollinator foraging decisions since bumblebees showed feeding preference for plants cultivated under low P, and for the most yielding and nutritious graft combinations under reduced but not under optimal fertilization. Bumblebees can sense plant nutritional status through source-sink relations, as supported by the consistent relationship between pollinator preferences and leaf carbon concentration. Conclusions This study opens new perspectives for using pollinators as “phenotypers” to select the most resilient plants under suboptimal conditions and/or genotypes that synergistically increase crop productivity by promoting the ecosystem service provided by the insects.
... For example, different workers within a colony would likely have a diverse knowledge of profitable resource patches, or safe foraging routes. Foraging hymenopterans are known to return to rewarding locations and show different motivation to forage for particular resources 46,47 . Hence, individuals might leave the colony aiming to collect a specific resource. ...
... Within insect colonies, the mechanisms causing differential task allocation can operate at multiple levels, and be genetic, maturational, nutritional, or of environmental nature 13,44 . Also in insects, learning processes, long term memories, and deliberate choices seem to play a very important role throughout life 13,44,46,47 . We do know that individual experience alone can shape behavioural differentiation in ants 48 or the individual performance of wasps 45 . ...
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A widely held assumption in ecology is that specialists are more efficient than generalists. However, empirical evidence for this fundamental assumption is surprisingly scarce and often contradictory. Theoretically, the evolution of alternative life history strategies is underpinned by a trade-off between activity levels and survival. We investigated the consequences of specialization in a foraging context, by comparing the performance and longevity of closely related individuals in a social insect, the common wasp (Vespula vulgaris). Using radio-frequency identification technology, we monitored the lifetime foraging activity of individual wasps from three colonies kept under natural foraging conditions. Returning foragers were video-recorded as they passed the nest entrance so that their foraging load could be assessed. There were substantial differences in foraging activity and survival within and between colonies. At the colony level, foraging specialization was weak. Yet, workers within each nest demonstrated a remarkable range of foraging specialization levels (defined as the degree of overlap between individual and colony-level task allocation) and efficiencies (defined by the number of successful trips and trip duration). We found that specialist foragers were less efficient than generalist siblings within the same colony. Behavioural specialists accomplished fewer successful trips per foraging day, and their trips were typically relatively longer. Specialized foragers also showed reduced life expectancy. The mortality risk was higher for individuals spending relatively more time in the field, yet we found no link between the level of specialization and relative field exposure. Our extensive dataset of unprecedented detail provides strong empirical evidence that behavioural specialization is not associated with a better lifetime performance, on the contrary, the opposite appears true for the common wasp. We also show that the survival of genetically similar individuals can be linked to life-long differences in behaviour according to classical life-history theory predictions.
... Thus, pollination is a key insect-plant interaction for human needs and for terrestrial ecosystems more fundamentally. Pollinators select flowers using a variety of chemical and visual cues (odours, colour/pattern and flower shape) through learned or innate preferences (Dafni et al. 1997;Daly & Smith 2000;Chittka 2017;Giurfa et al. 1995;Goyret et al. 2008). Alternatively, flowers may filter out preferred pollinators through specialist adaptations of floral morphology and chemistry that limit access to nectar (Brosi 2016). ...
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The homoterpenes 4,8‐dimethyl‐1,3,7‐nonatriene (DMNT) and 4,8,12‐trimethyl‐1,3,7,11‐tridecatetraene (TMTT) are volatile products of plant metabolism reported from diverse plant taxa and multiple plant tissues. As such, they have a range of potential ecological functions. Here, we review the key literature to assess evidence for roles in contrasting plant–arthropod interactions. TMTT, and DMNT especially, have been reported as sometimes dominant constituents of floral scents from angiosperm taxa ranging from primitive Magnoliales to more advanced, taxonomic orders of economic significance such as Fabales and Sapindales. Although all taxa producing TMTT and DMNT in floral scents are entomophilous (‘insect pollinated’), experimental evidence for an assumed role of these homoterpenes in pollinator attraction is limited. Representing a trade‐off, in some cases, homoterpenes in floral scents have been shown to act as kairomones, attracting herbivores. Additionally, both TMTT and DMNT are released by plant foliage in response to arthropod feeding, mechanical damage simulating feeding, or even egg deposition. Evidence for a functional role in herbivore‐induced plant volatile (HIPV) blends comes from a wide range of angiosperm orders, including anemophilous (‘wind pollinated’) taxa, as well as from gymnosperms. We conclude by considering how TMTT and DMNT function in community‐level interactions and highlighting research priorities that will reveal how plants avoid trade‐offs from contrasting ecological functions of DMNT and TMTT release and how homoterpene production might be exploited to develop improved crop varieties.
... Social insects offer a great opportunity to study inter-individual cognitive differences due to their impressive cognitive capabilities (Dornhaus and Franks 2008;Avarguès-Weber et al. 2011;Giurfa 2013Giurfa , 2019Chittka 2017;Perry et al. 2017;Howard et al. 2018;Simons and Tibbetts 2019). Interindividual variability has been described in a wide range of behaviors and is considered as a major factor for their ecological success, adding to division of labor and flexible responses to environmental changes (Thomson and Chittka 2001;Chittka and Muller 2009;Jeanson and Weidenmüller 2014;Bengston and Jandt 2014;Jandt and Gordon 2016;Walton and Toth 2016;Jeanson 2019). ...
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The question of whether individuals perform consistently across a variety of cognitive tasks is relevant for studies of comparative cognition. The honey bee (Apis mellifera) is an appropriate model to study cognitive consistency as its learning can be studied in multiple elemental and non-elemental learning tasks. We took advantage of this possibility and studied if the ability of honey bees to learn a simple discrimination correlates with their ability to solve two tasks of higher complexity, reversal learning and negative patterning. We performed four experiments in which we varied the sensory modality of the stimuli (visual or olfactory) and the type (Pavlovian or operant) and complexity (elemental or non-elemental) of conditioning to examine if stable correlated performances could be observed across experiments. Across all experiments, an individual's proficiency to learn the simple discrimination task was positively and significantly correlated with performance in both reversal learning and negative patterning, while the performances in reversal learning and negative patterning were positively, yet not significantly correlated. These results suggest that correlated performances across learning paradigms represent a distinct cognitive characteristic of bees. Further research is necessary to examine if individual cognitive consistency can be found in other insect species as a common characteristic of insect brains.
... This high variability could be associated with the quantity of nAChRs in the brain, which is much greater than in the flight muscle and may therefore explain why there is lower variance among the flight muscles of imidacloprid-exposed bees and among control groups. Cognitive ability such as learning and memory varies among individual bees; this suggests that the brain is particularly susceptible to interspecific variation (30,31). Hence, a possible variation in the number of neonicotinoid target sites among individual bees may lead to more variability in the response of imidacloprid on mitochondrial function. ...
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Mitochondria are intracellular organelles responsible for cellular respiration with one of their major roles in the production of energy in the form of ATP. Activities with increased energetic demand are especially dependent on efficient ATP production, hence sufficient mitochondrial function is fundamental. In bees, flight muscle and the brain have particularly high densities of mitochondria to facilitate the substantial ATP production required for flight activity and neuronal signalling. Neonicotinoids are systemic synthetic insecticides that are widely utilised against crop herbivores but have been reported to cause, by unknown mechanisms, mitochondrial dysfunction, decreasing cognitive function and flight activity among pollinating bees. Here we explore, using high-resolution respirometry, how the neonicotinoid imidacloprid may affect oxidative phosphorylation in the brain and flight muscle of the buff-tailed bumblebee, Bombus terrestris. We find that acute exposure increases routine oxygen consumption in the flight muscle of worker bees. This provides a candidate explanation for prior reports of early declines in flight activity following acute exposure. We further find that imidacloprid increases the maximum electron transport capacity in the brain, with a trend towards increased overall oxygen consumption. However, intra-individual variability is high, limiting the extent to which apparent effects of imidacloprid on brain mitochondria are shown conclusively. Overall, our results highlight the necessity to examine tissue-specific effects of imidacloprid on respiration and energy production.
... contains supplementary material, which is available to authorized users. off to optimize and improve their cognition capacity e.g. by focusing only on the most rewarding flower types and by rejecting flowers that they have learned to be poorly rewarding (Niggebrügge and De Ibarra 2003;Chittka 2017). Honey bees for example show a mechanism of unsuccessful attempt avoidance which means that they recognize rewardable flowers and discard unrewardable ones. ...
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Plants may use different strategies to attract pollinators in long distance (e.g. floral display) and in short distance (e.g. ratio between differentially colored flowers) scales. The Verbenaceae Lantana canescens Kunth is a wide spread species in open sites of the Brazilian Pantanal wetland. Individuals of this generalist species can produce a variable number of open inflorescences with yellow and white flowers that are organized in whorls. In this study we tested the hypothesis that increased floral display (long distance attraction) and the ratio between yellow and white flowers (short distance attraction) enhances the number of pollinator species and individuals. We observed flower visitors and calculated floral parameters in 38 plots of 1 m2 each, that contained a varying number of flowering L. canescens individuals. Non-metric multidimensional scaling and Bray-Curtis distances were used to account for flower visitor composition and the relative visitation rate, respectively. We used a structural equation model to test the power of each predictor variable on the visitation rate and a covariance analysis to disentangle the effect of each independent variable on the frequency of plant-pollinator interactions. We found that the number of flower visitors and the visitation rate increased with increasing number of inflorescences. Disentangling long and short distance attraction indicated that the number of inflorescences (per plot) and the number of yellow flowers (yellowing effect) contributed most to flower visitation at long and short distance, respectively.
... Similar to vertebrate studies, a very limited number of species largely drives our understanding of insect learning and memory. The fruit fly (Drosophila melanogaster), honey bee (Apis mellifera), and bumble bees (Bombus spp.) have become robust and influential insect model systems because they are amenable to highly controlled experimental manipulations [5,6], such as the proboscis extension reflex (PER), sting extension reflex (SER), artificial flower patch, shuttle box, and Y-maze techniques [7][8][9][10][11]. In bees, the proboscis extension reflex (PER), proposed first by [12] wild bee species. ...
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Olfactory learning and floral scents are co-adaptive traits in the plant–pollinator relationship. However, how scent relates to cognition and learning in the diverse group of Neotropical stingless bees is largely unknown. Here we evaluated the ability of Melipona eburnea to be conditioned to scent using the proboscis extension reflex (PER) protocol. Stingless bees did not show PER while harnessed but were able to be PER conditioned to scent when free-to-move in a mini-cage (fmPER). We evaluated the effect of: 1) unconditioned stimulus (US) reward, and 2) previous scent–reward associations on olfactory learning performance. When using unscented-US, PER-responses were low on day 1, but using scented-US reward the olfactory PER-response increased on day 1. On day 2 PER performance greatly increased in bees that previously had experienced the same odor and reward combination, while bees that experienced a different odor on day 2 showed poor olfactory learning. Bees showed higher olfactory PER conditioning to guava than to mango odor. The effect of the unconditioned stimulus reward was not a significant factor in the model on day 2. This indicates that olfactory learning performance can increase via either taste receptors or accumulated experience with the same odor. Our results have application in agriculture and pollination ecology.
... However, a clear next step would be to test our finding over a broader range of stimuli. Given that generalist bees rely on a broad range of cognitive abilities [56], moving towards assays that measure cognition in more naturalistic settings is critical to fully understand these pesticides' effects on bees. ...
Article
Neonicotinoid pesticides can impair bees’ ability to learn and remember information about flowers, critical for effective foraging. Although these effects on cognition may contribute to broader effects on health and performance, to date they have largely been assayed in simplified protocols that consider learning in a single sensory modality, usually olfaction. Given that real flowers display a variety of potentially useful signals, we assessed the effects of acute neonicotinoid exposure on multimodal learning in freeflying bumblebees. We found that neonicotinoid consumption differentially impacted learning of floral stimuli, impairing scent, but not colour, learning. These findings raise questions about the mechanisms by which pesticides might differentially impair sensory systems, with implications for how neonicotinoids affect multiple aspects of bee ecology.
... For example, honeybees reared under sub-optimal environmental conditions have 47 exhibited reduced brain volumetric growth and altered neuronal architecture ( Groh et al., 2004;Steijven 48 et al., 2017). Impeded brain development and structural plasticity may impact on behaviours such as 49 learning ability, that require detection, assimilation and processing of sensory input from the environment 50 (Cabirol et al., 2018;Chittka, 2017;Galizia et al., 2011). Knowledge of how pesticide contaminated food 51 inside bee colonies can affect individual physiological development however, is limited ( Gregorc et al., 52 2012; Wu et al., 2012Wu et al., , 2011). ...
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Understanding the risk to biodiversity from pesticide exposure is a global priority. For bees, an understudied step in evaluating pesticide risk is understanding how pesticide contaminated foraged food brought back to the colony can affect developing individuals. Provisioning bumblebee colonies with pesticide (neonicotinoid) treated food, we investigated how exposure during two key developmental phases (brood and/or early-adult), impacted brain growth and assessed the consequent effects on adult learning behaviour. Using micro-computed tomography (micro-CT) scanning and 3D image analysis, we compared brain development for multiple neuropils in workers 3 and 12-days post-emergence. Mushroom body calyces were the neuropils most affected by exposure during either of the developmental phases, with both age cohorts showing smaller structural volumes. Critically, reduced calyces growth in pesticide exposed workers was associated with lower responsiveness to a sucrose reward and impaired learning performance. Furthermore, the impact from brood exposure appeared irrecoverable despite no exposure during adulthood.
... By activating 'reward' and 'punishment' neurons in closed-loop using different behavioral contingencies, the optoPAD system should allow the design of new operant conditioning paradigms in which the animal learns to associate the consequences of its own behavior with specific outcomes or the statistical structure of its environment. Learning such abstract environmental structures is a fundamental ability animals use to optimize their foraging strategies (Chittka, 2017;Glimcher and Fehr, 2013). The extent to which Drosophila is able to perform such proto-cognitive computations is currently an important frontier in fly systems neuroscience. ...
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The regulation of feeding plays a key role in determining the fitness of animals through its impact on nutrition. Elucidating the circuit basis of feeding and related behaviors is an important goal in neuroscience. We recently used a system for closed-loop optogenetic manipulation of neurons contingent on the feeding behavior of Drosophila to dissect the impact of a specific subset of taste neurons on yeast feeding. Here, we describe the development and validation of this system, which we term the optoPAD. We use the optoPAD to induce appetitive and aversive effects on feeding by activating or inhibiting gustatory neurons in closed-loop – effectively creating virtual taste realities. The use of optogenetics allowed us to vary the dynamics and probability of stimulation in single flies and assess the impact on feeding behavior quantitatively and with high throughput. These data demonstrate that the optoPAD is a powerful tool to dissect the circuit basis of feeding behavior, allowing the efficient implementation of sophisticated behavioral paradigms to study the mechanistic basis of animals’ adaptation to dynamic environments.
... By activating "reward" and "punishment" neurons in closed loop using different behavioral contingencies, the optoPAD system should allow the design of new operant conditioning paradigms in which the animal learns to associate the consequences of its own behavior with specific outcomes or the statistical structure of its environment. Learning such abstract environmental structures is a fundamental ability animals use to optimize their foraging strategies (Chittka, 2017;Glimcher et al., 2009). The extent to which Drosophila is able to perform such proto-cognitive computations is currently an important frontier in fly systems neuroscience. ...
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The regulation of feeding plays a key role in determining the fitness of animals through its impact on nutrition. Elucidating the circuit basis of feeding and related behaviors is an important goal in neuroscience. We recently used a system for closed-loop optogenetic manipulation of neurons contingent on the fly’s feeding behavior to dissect the impact of a specific subset of taste neurons on yeast feeding (Steck et al., 2018). Here we describe the development and validation of this system, which we term the optoPAD. We use the optoPAD to induce appetitive and aversive effects on feeding by activating or inhibiting gustatory neurons in closed loop – effectively creating virtual taste realities. The use of optogenetics allowed us to vary the dynamics and probability of stimulation in single flies and assess the impact on feeding behavior quantitatively and with high throughput. These data demonstrate that the optoPAD is a powerful tool to dissect the circuit basis of feeding behavior, allowing the efficient implementation of sophisticated behavioral paradigms to study the mechanistic basis of animals’ adaptation to dynamic environments.
... Awareness of a goal or the presence of feelings clearly plays no role in the courtship ritual, since this complex behavior can be performed by headless flies (Pan et al., 2011). There is no evidence that complex learning in insects involves sentience (Giurfa, 2013;Chittka, 2017). There is no need to assume conscious awareness in either insects or molluscs in order to explain complex behaviors when non-conscious neural networks can effectively account for such abilities (Ardin et al., 2016;Faghihi et al., 2017;Goldschmidt et al., 2017;Müller et al., 2017;Peng and Chittka, 2017;Perry et al., 2017;Roper et al., 2017). ...
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There is compelling evidence that the “what it feels like” subjective experience of sensory stimuli arises in the cerebral cortex in both humans as well as mammalian experimental animal models. Humans are alone in their ability to verbally communicate their experience of the external environment. In other species, sensory awareness is extrapolated on the basis of behavioral indicators. For instance, cephalopods have been claimed to be sentient on the basis of their complex behavior and anecdotal reports of human-like intelligence. We have interrogated the findings of avoidance learning behavioral paradigms and classical brain lesion studies and conclude that there is no evidence for cephalopods feeling pain. This analysis highlighted the questionable nature of anthropometric assumptions about sensory experience with increased phylogenetic distance from humans. We contend that understanding whether invertebrates such as molluscs are sentient should first begin with defining the computational processes and neural circuitries underpinning subjective awareness. Using fundamental design principles, we advance the notion that subjective awareness is dependent on observer neural networks (networks that in some sense introspect the neural processing generating neural representations of sensory stimuli). This introspective process allows the observer network to create an internal model that predicts the neural processing taking place in the network being surveyed. Predictions arising from the internal model form the basis of a rudimentary form of awareness. We develop an algorithm built on parallel observer networks that generates multiple levels of sensory awareness. A network of cortical regions in the human brain has the appropriate functional properties and neural interconnectivity that is consistent with the predicted circuitry of the algorithm generating pain awareness. By contrast, the cephalopod brain lacks the necessary neural circuitry to implement such an algorithm. In conclusion, we find no compelling behavioral, functional, or neuroanatomical evidence to indicate that cephalopods feel pain.
... A. S. Dunlap et al. / Animal Behaviour xxx (2018) 1e10 flag model can be used in conjunction with natural history to predict learning differences in a model organism of cognitive ecology, bumblebees (Bombus spp.). While bumblebees have long been models of cognition due to the tractability of their foraging (Chittka, 2017;Goulson, 2010), their generation time and social structure make experimental evolution with bumblebees problematic. However, the ability to track change in the foraging environments of bumblebees lends itself to being mapped onto the flag model's parameters of change, thereby providing a method for merging bumblebee natural history with theory on when learning should evolve. ...
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Theoretical treatments of the evolution of learning have a long and rich history, and although many aspects remain unresolved, the consensus is that the predictability and timescale of environmental change play a crucial role in when learning evolves. Directly testing these ideas has proven difficult because comparative experiments must assume many often unknowable aspects of an evolutionary past. Even within the present, identifying and accurately quantifying the relevant types of change can be problematic. Controlling or manipulating change can be difficult in many taxa. Within the theory, what is meant by change can markedly vary between models. Here, we present a targeted comparison of models to show this variation, and argue that standardizing measures of change can add tractability to models. We first review how change is emphasized in models of learning evolution and then describe the still small literature that directly tests the evolution of learning via digital evolution and experimental evolution. We then give an example of how to tie specific natural history to larger theory on learning evolution using the flag model of reliability and certainty and foraging in bumblebees. Learning, by its nature, is of fundamental importance to many fields. Theoretical treatments of learning evolution have been growing at a rapid pace, often with limited empirical applicability to natural systems and little congruence on what is meant by change across models. By explicitly defining change and tying models to natural systems, we can greatly increase our ability to not only understand when learning should evolve, but also when learning does evolve.
... 36 Chittka remarks of the bee which cooperates to build an elaborate geometrical structure, the hive, evaluates food sources, maps its territory, remembers threats, communicates information to its fellows, provisions its young, enters into seemingly emotional states, and can solve novel problems under laboratory conditions, that references to 'instinct' fail to do justice to the behavioural complexity of social insects. 37 But why have qualia? Gerald Edelman and colleagues argue that the organism needs to be faced with a scene in order to extract and employ information. ...
... Honey bee foraging has been one of the most fruitful behavioral paradigms in the study of sensory and cognitive capabilities of insects and animals in general (von Frisch, 1967;Giurfa, 2007;Chittka, 2017). Foragers continue to visit a highly rewarding food source for days and weeks till it gets exhausted. ...
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In honey bees, continuous foraging is accompanied by a sustained up-regulation of the immediate early gene Egr-1 (early growth response protein-1) and candidate downstream genes involved in learning and memory. Here, we present a series of feeder training experiments indicating that Egr-1 expression is highly correlated with the time and duration of training even in the absence of the food reward. Foragers that were trained to visit a feeder over the whole day and then collected on a day without food presentation showed Egr-1 up-regulation over the whole day with a peak expression around 14:00. When exposed to a time-restricted feeder presentation, either 2 h in the morning or 2 h in the evening, Egr-1 expression in the brain was up-regulated only during the hours of training. Foragers that visited a feeder in the morning as well as in the evening showed two peaks of Egr-1 expression. Finally, when we prevented time-trained foragers from leaving the colony using artificial rain, Egr-1 expression in the brains was still slightly but significantly up-regulated around the time of feeder training. In situ hybridization studies showed that active foraging and time-training induced Egr-1 up-regulation occurred in the same brain areas, preferentially the small Kenyon cells of the mushroom bodies and the antennal and optic lobes. Based on these findings we propose that foraging induced Egr-1 expression can get regulated by the circadian clock after time-training over several days and Egr-1 is a candidate transcription factor involved in molecular processes underlying time-memory.
... Being capable of interval timing, bumblebees can predict future events (Boisvert and Sherry, 2006;Skorupski and Chittka, 2006). There is evidence that insects might at some level predict the outcomes of their own actions (Webb, 2004;Kim et al., 2015;Mischiati et al., 2015), or perceive a desirable outcome and then to explore possibilities to achieve this goal (Chittka, 2017;Menzel, 2017). In view of this, a re-evaluation of some behavioral routines traditionally thought to be entirely governed by instinct is in order (Bateson and Mameli, 2007). ...
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The wax-made comb of the honeybee is a masterpiece of animal architecture. The highly regular, double-sided hexagonal structure is a near-optimal solution to storing food and housing larvae, economizing on building materials and space. Elaborate though they may seem, such animal constructions are often viewed as the result of ‘just instinct,’ governed by inflexible, pre-programmed, innate behavior routines. An inspection of the literature on honeybee comb construction, however, reveals a different picture. Workers have to learn, at least in part, certain elements of the technique, and there is considerable flexibility in terms of how the shape of the comb and its gradual manufacture is tailored to the circumstances, especially the available space. Moreover, we explore the 2-century old and now largely forgotten work by François Huber, where glass screens were placed between an expanding comb construction and the intended target wall. Bees took corrective action before reaching the glass obstacle, and altered the ongoing construction so as to reach the nearest wooden wall. Though further experiments will be necessary, these results suggest a form of spatial planning skills. We discuss these findings in the context of what is now known about insect cognition, and ask if it is possible that the production of hexagonal wax combs is the result of behavioral heuristics where a complex structure emerges as the result of simple behavioral rules applied by each individual, or whether prospective cognition might be involved.
Chapter
Despite abundant evidence to the contrary, non-avian reptiles are widely considered as behavioural and cognitive underachievers. The persistent myth of the sluggish, primitive, stupid reptile can be traced, at least in part, to long-standing misconceptions about reptilian brain size and organisation. Historically, reptile brains have been considered small and lacking the neural structures that support complex cognition in other vertebrates. In particular, the notion that reptiles lack a cerebral cortex has led to expectations that their behaviour and cognition should be simple and unsophisticated in comparison with birds and mammals. However, it was shown several decades ago that reptiles possess a large pallium comprising three–four distinct cortical areas and a dorsal ventricular ridge that may be functionally equivalent to parts of mammalian neocortex. In fact, forebrain organisation conforms to a common plan in birds and reptiles, which may seem surprising given the recent trend to put the cognitive achievements of birds above those of reptiles yet on a par with mammals. Moreover, the view that reptiles do not exhibit complex cognition faces a growing list of exceptions. Reptiles are capable of spatial, social, reversal, problem-solving, and many other types of learning and cognitively demanding behaviours provided that experimental designs account for some peculiarities of their biology involving their morphology, physiology, and ecology. Unlike frequent caricatures that depict reptiles as clumsy, inflexible, and instinct-driven, much reptile behaviour is precisely performed, delicate in appearance, readily modified, and contextually determined. Recent work has shown that reptiles can show elaborate communication and social systems, parental care, social learning, and play. Although such research is sparse compared to endothermic vertebrates, and the diversity among them immense, captive reptiles also benefit from enrichment, recognise their caretakers individually and form bonds with them, and are affected by early social isolation in ways similar to birds and mammals. Still, the gap between what we know and what we would like to know about reptilian behaviour and cognition is enormous.KeywordsBrainBrain sizeCerebral cortexCognitionLearningBehaviourComplex behaviourSocial behaviourParental carePlay
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Unlabelled: Stingless bees are among the most dominant pollinators in the south tropics. As such, the rational beekeeping of stingless bee species, called meliponiculture, is an ancient and relevant activity, related to sustainable agricultural development, and which connects traditional knowledge to innovation and novelty. Given the relevance of this topic, this paper discusses the possibilities of a semiotically mediated communication between humans and Meliponini (stingless bees). Zoosemiotics, as the studies of animal views of the world, is the ideal modelling system for the investigation of the possibilities of mutual understanding between these two species. Starting from the premise that, for there to be inter-specific communication, there must be a shared code, and that this depends on the biological makeup and sensory apparatus of both organisms involved in the communication process, this research suggests that a possible way to communicate with stingless bees is with the use of olfactory (chemical) signals, since this channel seems to be common to both humans and bees. Considering that for human-animal relations one party must be able to recognize the other (iconic learning), it is revealed that chemical signals do allow bees to recognize individual humans, even going so far as profiling this person as 'not a threat'. Finally, bees are seen to act cooperatively while the beekeeper is taking action to protect and maintain the nest, something that can be interpreted as an opening of semiotic relations, where the bees are deeming the beekeeper as part of their social group. Supplementary information: The online version contains supplementary material available at 10.1007/s12304-022-09519-2.
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The question of whether individuals perform consistently across a variety of cognitive tasks is relevant for studies of comparative cognition. The honey bee ( Apis mellifera ) is an appropriate model to study cognitive consistency as its learning can be studied in multiple elemental and non-elemental learning tasks. We took advantage of this possibility and studied if the ability of honey bees to learn a simple discrimination correlates with their ability to solve two tasks of higher complexity, reversal learning and negative patterning. We performed four experiments in which we varied the sensory modality of the stimuli (visual or olfactory) and the type (Pavlovian or operant) and complexity (elemental or non-elemental) of conditioning to examine if stable correlated performances could be observed across experiments. Across all experiments, the individual’s proficiency to learn the simple discrimination task was positively correlated with the performance in both reversal learning and negative patterning, while the performances in reversal learning and negative patterning were not correlated. These results suggest that this pattern of correlated and independent performances across the learning paradigms tested represent a distinct cognitive characteristic of bees. Further research is necessary to examine if this pattern of individual cognitive consistency can be found in other insect species as a common characteristic of insect brains.
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Being able to abstract relations of similarity is considered one of the hallmarks of human cognition. While previous research has shown that other animals (e.g. primates) can attend to relational similarity, they struggle to focus on object similarity. This is in contrast with humans. And it is precisely the ability to attend to objects that it is argued to make relational reasoning uniquely human. What about invertebrates? Despite earlier studies indicating that bees are capable of learning abstract relationships (e.g. ‘same’ and ‘different’), no research has investigated whether bees can spontaneously attend to relational similarity and whether they can do so when relational matches compete with object matches. To test this, a spatial matching task (with and without competing object matches) previously used with children and great apes was adapted for use with wild-caught bumblebees. When object matches were not present, bumblebees spontaneously used relational similarity. Importantly, when competing object matches were present, bumblebees still focused on relations over objects. These findings indicate that the absence of object bias is also present in invertebrates and suggest that the relational gap between humans and other animals is due to their preference for relations over objects.
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‘‘Ecological intelligence’’ hypotheses posit that animal learning and memory evolve to meet the demands posed by foraging and, together with social intelligence and cognitive buffer hypotheses, provide a key framework for understanding cognitive evolution.1–5 However, identifying the critical environments where cognitive investment reaps significant benefits has proved challenging.6–8 Here, we capitalize upon seasonal variation in forage availability for a social insect model (Bombus terrestris audax) to establish how the ben- efits of short-term memory, assayed using a radial arm maze (RAM), vary with resource availability. Following a staggered design over 2 years, whereby bees from standardized colonies at identical life-history stages underwent cognitive testing before foraging in the wild, we found that RAM performance predicts foraging efficiency—a key determinant of colony fitness—in plentiful spring foraging conditions but that this relation- ship is reversed during the summer floral dearth. Our results suggest that the selection for enhanced cognitive abilities is unlikely to be limited to harsh environments where food is hard to find or extract,5,9–11 highlighting instead that the challenges of rich and plentiful environments, which present multiple options in short succession, could be a broad driver in the evolution of certain cognitive traits.
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The concept of culture and its consideration on comparative evolutionary grounds have elicited contradictory opinions in sociology and anthropology. An anthropomorphic view would be reducing its presence to human and nonhuman primate species. Here we adopt an evolutionary standing on this issue and consider that culture represents a universal social expression of the history of interaction in gregarious species. Its evolution would depend on species-specific constructs and the ecological environment, thus, expressing aliquots of a variable, complex, interactive social construction and its material and conceptual output. Biosocial interactions continue to model social, behavioral trends or social phenotypes, in addition to the basic, deeply entrenched, survival, and occasionally prevalent drives that conform to the basic structure of the ancestral animal nature. These interactions may be best summarized by the probability of continuous frictions between the neurobiological and cultural tectonic plates, described here.
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Interest in studying cognitive ecology has moved the field of animal cognition into the wild. Animals face many challenges such as finding food and other resources, avoiding and deterring predators and choosing the best mate to increase their reproductive success. To solve these dilemmas, animals need to rely on a range of cognitive abilities. Studying cognition in natural settings is a powerful approach revealing the link between adaptive form and biological function. Recent technological and analytical advances opened up completely new opportunities and research directions for studying animal cognition. Such innovative studies were able to disclose the variety in cognitive processes that animals use to survive and reproduce. Cognition indeed plays a major role in the daily lives of wild animals, in which the integration of many different types of information using a diverse range of cognitive processes enhances fitness.
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Previous research looking at expectancy in animals has used various experimental designs focusing on appetitive and avoidance behaviors. In this study, honey bees (Apis mellifera) were tested ina series of three proboscis extension response (PER) experiments to determine to what degree honey bees’ form a cognitive-representation of an unconditioned stimulus (US). Tthe first experiment, bees were presented with either a 2 sec. sucrose US or 2 sec. honey US appetitive reward and the proboscis-extension duration was measured under each scenario. The PER duration was longer for the honey US even though each US was presented for just 2 sec. Honey bees in the second experiment were tested during extinction trials on a conditioned stimulus (CS) of cinnamon or lavender that was paired with either the sucrose US or honey US in the acquisition trials. The proportion of bees showing the PER response to the CS was recorded for each extinction trial for each US scenario, as was the duration of the proboscis extension for each bee. Neither measure differed between the honey US and sucrose US scenarios, In experiment three, bees were presented with a cinnamon or lavender CS paired with either honey US or sucrose US in a set of acquisition trials, but here the US was not given until after the proboscis was retracted. The PER duration after the CS, and again subsequent after the US, were recorded. While the PER duration after the US was longer for honey, the PER duration after the CS did not differ between honey US and sucrose US.
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Mapping animal performance in a behavioral task to underlying cognitive mechanisms and strategies is rarely straightforward, since a task may be solvable in more than one manner. Here, we show that bumblebees perform well on a concept-based visual discrimination task but spontaneously switch from a concept-based solution to a simpler heuristic with extended training, all while continually increasing performance. Bumblebees were trained in an arena to find rewards on displays with shapes of different sizes where they could not use low-level visual cues. One group of bees was rewarded at displays with larger shapes and another group at displays with smaller shapes. Analysis of total choices shows bees increased their performance over 30 bouts to above chance. However, analyses of first and sequential choices suggest that after approximately 20 bouts, bumblebees changed to a win-stay/lose-switch strategy. Comparing bees’ behavior to a probabilistic model based on a win-stay/lose-switch strategy further supports the idea that bees changed strategies with extensive training. Analyses of unrewarded tests indicate that bumblebees learned and retained the concept of relative size even after they had already switched to a win-stay, lost-shift strategy. We propose that the reason for this strategy switching may be due to cognitive flexibility and efficiency.
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Some floral visitors collect nectar by piercing flower external whorls, acting as nectar robbers. They leave robbery vestiges, which can cause changes in floral characteristics, including physical and chemical signals that may influence flower recognition by pollinators. If pollinating bees associate these changes with absence or reduction in nectar volume, they can avoid these flowers, negatively affecting pollination. We aimed to investigate the effect of robbery on primary and secondary attractants. Additionally, we experimentally investigated if the visual signs present in robbed flowers affect the bee pollination of this plant species by discouraging pollinator visits. This study was performed in a very common pollinator-plant-cheaters system comprised by a bee-pollinated Bignoniaceae species and a nectar-robber bee that lands on the corolla tube and makes slits at its base during the nectar robbery. We experimentally isolated the effect of nectar consumption by this nectar-robber and investigated if the slits caused by the nectar-robbers affected the floral scent emission. In addition, we experimentally evaluated the effect of visual signs (slits) associated to the nectar robbery and the effect of nectar depletion on the pollination of Jacaranda caroba (Bignoniaceae). The robbers visited around 75% of the flowers throughout the day and removed significant amounts of nectar from them. However, the damages the robbers cause did not affect floral scent emission and we did not verify significant differences on pollen deposition neither when comparing flowers with slits and control nor when comparing flowers with and without nectar. We showed that even though nectar-robbers visually honestly signal the robbery and deplete high amounts of nectar, they did not affect pollinator visitation. These results showed that presumably antagonistic interactions might in fact not be so.
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Understanding how animals learn is crucial to interpreting animal behaviour. Flower-visiting insects, such as bees and parasitoids, are excellent animal models to study visual and olfactory learning, including memory phenomena. The diversity of resources flower-visiting insects exploit predisposes them to learn and remember the colours, shapes and odours associated with rewarding experiences (e.g. flowers), allowing them to focus on the most rewarding resources. Recent research has shown that nectar-living microbes release volatile organic compounds (VOCs) that contribute to overall flower scent. Nevertheless, little is known about the extent to which nectar microbiota mediate insect learning of floral preferences. In this study, we investigated whether VOCs produced by nectar microbes serve as a learning cue to parasitoids and how long any developed preference is maintained. Experiments were performed using the generalist aphid parasitoid Aphidius ervi and three nectar yeasts, including the nectar specialist Metschnikowia reukaufii and the generalist species Hanseniaspora uvarum and Sporobolomyces roseus. Results showed that naïve parasitoids had an innate preference for nectar fermented by the nectar specialist M. reukaufii, but not by the other two yeasts which had either a neutral (H. uvarum) or deterrent (S. roseus) effect. When parasitoids were conditioned with yeast-fermented nectar, they were strongly attracted to their odours 2 and 24 h after conditioning, but not after 48 h. Furthermore, when parasitoids were conditioned to one yeast-fermented nectar, they also showed increased attraction to other yeast-fermented nectars. This generalization suggests that their learning ability may have broader ecological consequences. However, this generalized response to other yeast VOCs lasted for only 2 h. We conclude that parasitoids show conditioned responses to the scent of yeastfermented nectar, and yeasts, therefore, may play an important but understudied role in shaping their foraging behaviour.
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Social insects show complex behaviors and master cognitive tasks. The underlying neuronal mechanisms, however, are in most cases only poorly understood due to challenges in monitoring brain activity in freely moving animals. Immediate early genes (IEGs) that get rapidly and transiently expressed following neuronal stimulation provide a powerful tool for detecting behavior-related neuronal activity in vertebrates. In social insects, like honey bees, and in insects in general, this approach is not yet routinely established, even though these genes are highly conserved. First studies revealed a vast potential of using IEGs as neuronal activity markers to analyze the localization, function, and plasticity of neuronal circuits underlying complex social behaviors. We summarize the current knowledge on IEGs in social insects and provide ideas for future research directions.
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Mushroom bodies (MBs), a higher-order center in the honeybee brain, comprise some subtypes/populations of interneurons termed as Kenyon cells (KCs), which are distinguished by their cell body size and location in the MBs, as well as their gene expression profiles. Although the role of MBs in learning ability has been studied extensively in the honeybee, the roles of each KC subtype and their evolution in hymenopteran insects remain mostly unknown. This mini-review describes recent progress in the analysis of gene/protein expression profiles and possible functions of KC subtypes/populations in the honeybee. Especially, the discovery of novel KC subtypes/populations, the “middle-type KCs” and “KC population expressing FoxP,” necessitated a redefinition of the KC subtype/population. Analysis of the effects of inhibiting gene function in a KC subtype-preferential manner revealed the function of the gene product as well as of the KC subtype where it is expressed. Genes expressed in a KC subtype/population-preferential manner can be used to trace the differentiation of KC subtypes during the honeybee ontogeny and the possible evolution of KC subtypes in hymenopteran insects. Current findings suggest that the three KC subtypes are unique characteristics to the aculeate hymenopteran insects. Finally, prospects regarding future application of genome editing for the study of KC subtype functions in the honeybee are described. Genes expressed in a KC subtype-preferential manner can be good candidate target genes for genome editing, because they are likely related to highly advanced brain functions and some of them are dispensable for normal development and sexual maturation in honeybees.
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Very clever bees use tools One hallmark of cognitive complexity is the ability to manipulate objects with a specific goal in mind. Such “tool use” at one time was ascribed to humans alone, but then to primates, next to marine mammals, and later to birds. Now we recognize that many species have the capacity to envision how a particular object might be used to achieve an end. Loukola et al. extend this insight to invertebrates. Bumblebees were trained to see that a ball could be used to produce a reward. These bees then spontaneously rolled the ball when given the chance. Science , this issue p. 833
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Social insects make elaborate use of simple mechanisms to achieve seemingly complex behavior and may thus provide a unique resource to discover the basic cognitive elements required for culture, i.e., group-specific behaviors that spread from " innovators " to others in the group via social learning. We first explored whether bumblebees can learn a nonnatural object manipulation task by using string pulling to access a reward that was presented out of reach. Only a small minority " innovated " and solved the task spontaneously, but most bees were able to learn to pull a string when trained in a stepwise manner. In addition, naïve bees learnt the task by observing a trained demonstrator from a distance. Learning the behavior relied on a combination of simple associative mechanisms and trial-and-error learning and did not require " insight " : naïve bees failed a " coiled-string experiment, " in which they did not receive instant visual feedback of the target moving closer when tugging on the string. In cultural diffusion experiments, the skill spread rapidly from a single knowledgeable individual to the majority of a colony's foragers. We observed that there were several sequential sets (" generations ") of learners, so that previously naïve observers could first acquire the technique by interacting with skilled individuals and, subsequently, themselves become demonstrators for the next " generation " of learners, so that the longevity of the skill in the population could outlast the lives of informed foragers. This suggests that, so long as animals have a basic toolkit of associative and motor learning processes, the key ingredients for the cultural spread of unusual skills are already in place and do not require sophisticated cognition. Author Summary Social insects make use of simple mechanisms to achieve many seemingly complex behaviors and thus may be able to provide a unique resource for uncovering the basic cognitive PLOS Biology |
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Whether invertebrates exhibit positive emotion-like states and what mechanisms underlie such states remain poorly understood. We demonstrate that bumblebees exhibit dopamine-dependent positive emotion-like states across behavioral contexts. After training with one rewarding and one unrewarding cue, bees that received pretest sucrose responded in a positive manner toward ambiguous cues. In a second experiment, pretest consumption of sucrose solution resulted in a shorter time to reinitiate foraging after a simulated predator attack. These behavioral changes were abolished with topical application of the dopamine antagonist fluphenazine. Further experiments established that pretest sucrose does not simply cause bees to become more exploratory. Our findings present a new opportunity for understanding the fundamental neural elements of emotions and may alter the view of how emotion states affect decision-making in animals. © 2016, American Association for the Advancement of Science. All rights reserved.
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Insect pollinators such as bumblebees play a vital role in many ecosystems, so it is important to understand their foraging movements on a landscape scale. We used harmonic radar to record the natural foraging behaviour of Bombus terrestris audax workers over their entire foraging career. Every flight ever made outside the nest by four foragers was recorded. Our data reveal where the bees flew and how their behaviour changed with experience, at an unprecedented level of detail. We identified how each bee's flights fit into two categories-which we named exploration and exploitation flights-examining the differences between the two types of flight and how their occurrence changed over the course of the bees' foraging careers. Exploitation of learned resources takes place during efficient, straight trips, usually to a single foraging location, and is seldom combined with exploration of other areas. Exploration of the landscape typically occurs in the first few flights made by each bee, but our data show that further exploration flights can be made throughout the bee's foraging career. Bees showed striking levels of variation in how they explored their environment, their fidelity to particular patches, ratio of exploration to exploitation, duration and frequency of their foraging bouts. One bee developed a straight route to a forage patch within four flights and followed this route exclusively for six days before abandoning it entirely for a closer location; this second location had not been visited since her first exploratory flight nine days prior. Another bee made only rare exploitation flights and continued to explore widely throughout its life; two other bees showed more frequent switches between exploration and exploitation. Our data shed light on the way bumblebees balance exploration of the environment with exploitation of resources and reveal extreme levels of variation between individuals.
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Ants, like many other animals, use visual memory to follow extended routes through complex environments, but it is unknown how their small brains implement this capability. The mushroom body neuropils have been identified as a crucial memory circuit in the insect brain, but their function has mostly been explored for simple olfactory association tasks. We show that a spiking neural model of this circuit originally developed to describe fruitfly (Drosophila melanogaster) olfactory association, can also account for the ability of desert ants (Cataglyphis velox) to rapidly learn visual routes through complex natural environments. We further demonstrate that abstracting the key computational principles of this circuit, which include one-shot learning of sparse codes, enables the theoretical storage capacity of the ant mushroom body to be estimated at hundreds of independent images.
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Primates can analyse visual scenes extremely rapidly, making accurate decisions for presentation times of only 20ms. We asked if bumblebees, despite having potentially more limited processing power, could similarly detect and discriminate visual patterns presented for durations of 100ms or less. Bumblebees detected stimuli and discriminated between differently oriented and coloured stimuli even when presented as briefly as 20ms but failed to identify ecologically relevant shapes (predatory spiders on flowers) even when presented for 100ms. This suggests a profound difference between primate and insect visual processing, so that while primates can capture entire visual scenes 'at a glance', insects might have to rely on continuous online sampling of the world around them, using a process of active vision which requires longer integration times.
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Significance Here we show that honey bees ( Apis mellifera ) can adaptively alter their behavior in a choice test in response to trial difficulty. Bees preferentially opt out of difficult trials and by doing so, improve their success rate. We discuss whether this choice involves assessing degree of uncertainty (considered a definition of basic metacognition) or whether this task might be solved by associative mechanisms. We propose a hypothesis for how uncertainty might be processed within the known circuitry of the insect brain to frame the concept of uncertainty as a topic for neurobiological analysis.
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Insects process and learn information flexibly to adapt to their environment. The honeybee Apis mellifera constitutes a traditional model for studying learning and memory at behavioural, cellular and molecular levels. Earlier studies focused on elementary associative and non-associative forms of learning determined by either olfactory conditioning of the proboscis extension reflex or the learning of visual stimuli in an operant context. However, research has indicated that bees are capable of cognitive performances that were thought to occur only in some vertebrate species. For example, honeybees can interpolate visual information, exhibit associative recall, categorize visual information and learn contextual information. Here we show that honeybees can form `sameness' and `difference' concepts. They learn to solve `delayed matching-to-sample' tasks, in which they are required to respond to a matching stimulus, and `delayed non-matching-to-sample' tasks, in which they are required to respond to a different stimulus; they can also transfer the learned rules to new stimuli of the same or a different sensory modality. Thus, not only can bees learn specific objects and their physical parameters, but they can also master abstract inter-relationships, such as sameness and difference.
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We demonstrate that the evolution of facial recognition in wasps is associated with specialized face-learning abilities. Polistes fuscatus can differentiate among normal wasp face images more rapidly and accurately than nonface images or manipulated faces. A close relative lacking facial recognition, Polistes metricus, however, lacks specialized face learning. Similar specializations for face learning are found in primates and other mammals, although P. fuscatus represents an independent evolution of specialization. Convergence toward face specialization in distant taxa as well as divergence among closely related taxa with different recognition behavior suggests that specialized cognition is surprisingly labile and may be adaptively shaped by species-specific selective pressures such as face recognition.
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Whether animals experience human-like emotions is controversial and of immense societal concern [1–3]. Because animals cannot provide subjective reports of how they feel, emotional state can only be inferred using physiological, cognitive, and behavioral measures [4–8]. In humans, negative feelings are reliably correlated with pessimistic cognitive biases, defined as the increased expectation of bad outcomes [9–11]. Recently, mammals [12–16] and birds [17–20] with poor welfare have also been found to display pessimistic-like decision making, but cognitive biases have not thus far been explored in invertebrates. Here, we ask whether honeybees display a pessimistic cognitive bias when they are subjected to an anxiety-like state induced by vigorous shaking designed to simulate a predatory attack. We show for the first time that agitated bees are more likely to classify ambiguous stimuli as predicting punishment. Shaken bees also have lower levels of hemolymph dopamine, octopamine, and serotonin. In demonstrating state-dependent modulation of categorization in bees, and thereby a cognitive component of emotion, we show that the bees' response to a negatively valenced event has more in common with that of vertebrates than previously thought. This finding reinforces the use of cognitive bias as a measure of negative emotional states across species and suggests that honeybees could be regarded as exhibiting emotions. Video Abstract
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