Review

17 pages, 1778 KiB

Open AccessReview

Analysis of Synaptic Microcircuits in the Mushroom Bodies of the Honeybee

by Claudia Groh and Wolfgang Rössler

Insects 2020, 11(1), 43; https://doi.org/10.3390/insects11010043 - 07 Jan 2020

Cited by 31 | Viewed by 6076

Mushroom bodies (MBs) are multisensory integration centers in the insect brain involved in learning and memory formation. In the honeybee, the main sensory input region (calyx) of MBs is comparatively large and receives input from mainly olfactory and visual senses, but also from [...] Read more.

Mushroom bodies (MBs) are multisensory integration centers in the insect brain involved in learning and memory formation. In the honeybee, the main sensory input region (calyx) of MBs is comparatively large and receives input from mainly olfactory and visual senses, but also from gustatory/tactile modalities. Behavioral plasticity following differential brood care, changes in sensory exposure or the formation of associative long-term memory (LTM) was shown to be associated with structural plasticity in synaptic microcircuits (microglomeruli) within olfactory and visual compartments of the MB calyx. In the same line, physiological studies have demonstrated that MB-calyx microcircuits change response properties after associative learning. The aim of this review is to provide an update and synthesis of recent research on the plasticity of microcircuits in the MB calyx of the honeybee, specifically looking at the synaptic connectivity between sensory projection neurons (PNs) and MB intrinsic neurons (Kenyon cells). We focus on the honeybee as a favorable experimental insect for studying neuronal mechanisms underlying complex social behavior, but also compare it with other insect species for certain aspects. This review concludes by highlighting open questions and promising routes for future research aimed at understanding the causal relationships between neuronal and behavioral plasticity in this charismatic social insect. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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12 pages, 548 KiB

Open AccessReview

The Waggle Dance as an Intended Flight: A Cognitive Perspective

by Randolf Menzel

Insects 2019, 10(12), 424; https://doi.org/10.3390/insects10120424 - 25 Nov 2019

Cited by 14 | Viewed by 4340

Abstract

The notion of the waggle dance simulating a flight towards a goal in a walking pattern has been proposed in the context of evolutionary considerations. Behavioral components, like its arousing effect on the social community, the attention of hive mates induced by this [...] Read more.

The notion of the waggle dance simulating a flight towards a goal in a walking pattern has been proposed in the context of evolutionary considerations. Behavioral components, like its arousing effect on the social community, the attention of hive mates induced by this behavior, the direction of the waggle run relative to the sun azimuth or to gravity, as well as the number of waggles per run, have been tentatively related to peculiar behavioral patterns in both solitary and social insect species and are thought to reflect phylogenetic pre-adaptations. Here, I ask whether these thoughts can be substantiated from a functional perspective. Communication in the waggle dance is a group phenomenon involving the dancer and the followers that perform partially overlapping movements encoding and decoding the message respectively. It is thus assumed that the dancer and follower perform close cognitive processes. This provides us with access to these cognitive processes during dance communication because the follower can be tested in its flight performance when it becomes a recruit. I argue that the dance message and the landscape experience are processed in the same navigational memory, allowing the bee to fly novel direct routes, a property understood as an indication of a cognitive map. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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13 pages, 647 KiB

Open AccessReview

Acetylcholine and Its Receptors in Honeybees: Involvement in Development and Impairments by Neonicotinoids

by Bernd Grünewald and Paul Siefert

Insects 2019, 10(12), 420; https://doi.org/10.3390/insects10120420 - 22 Nov 2019

Cited by 37 | Viewed by 8259

Abstract

Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh receptors (AChR), the existence of non-neuronal AChR in honeybees is plausible. The cholinergic system is a popular target of insecticides because the [...] Read more.

Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh receptors (AChR), the existence of non-neuronal AChR in honeybees is plausible. The cholinergic system is a popular target of insecticides because the pharmacology of insect nicotinic acetylcholine receptors (nAChRs) differs substantially from their vertebrate counterparts. Neonicotinoids are agonists of the nAChR and are largely used in crop protection. In contrast to their relatively high safety for humans and livestock, neonicotinoids pose a threat to pollinating insects such as bees. In addition to its effects on behavior, it becomes increasingly evident that neonicotinoids affect developmental processes in bees that appear to be independent of neuronal AChRs. Brood food (royal jelly, worker jelly, or drone jelly) produced in the hypopharyngeal glands of nurse bees contains millimolar concentrations of ACh, which is required for proper larval development. Neonicotinoids reduce the secreted ACh-content in brood food, reduce hypopharyngeal gland size, and lead to developmental impairments within the colony. We assume that potential hazards of neonicotinoids on pollinating bees occur neuronally causing behavioral impairments on adult individuals, and non-neuronally causing developmental disturbances as well as destroying gland functioning. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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17 pages, 1078 KiB

Open AccessReview

Spatial Vision and Visually Guided Behavior in Apidae

by Almut Kelber and Hema Somanathan

Insects 2019, 10(12), 418; https://doi.org/10.3390/insects10120418 - 22 Nov 2019

Cited by 17 | Viewed by 4439

Abstract

The family Apidae, which is amongst the largest bee families, are important pollinators globally and have been well studied for their visual adaptations and visually guided behaviors. This review is a synthesis of what is known about their eyes and visual capabilities. There [...] Read more.

The family Apidae, which is amongst the largest bee families, are important pollinators globally and have been well studied for their visual adaptations and visually guided behaviors. This review is a synthesis of what is known about their eyes and visual capabilities. There are many species-specific differences, however, the relationship between body size, eye size, resolution, and sensitivity shows common patterns. Salient differences between castes and sexes are evident in important visually guided behaviors such as nest defense and mate search. We highlight that Apis mellifera and Bombus terrestris are popular bee models employed in the majority of studies that have contributed immensely to our understanding vision in bees. However, other species, specifically the tropical and many non-social Apidae, merit further investigation for a better understanding of the influence of ecological conditions on the evolution of bee vision. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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9 pages, 221 KiB

Open AccessReview

A Multiscale Review of Behavioral Variation in Collective Foraging Behavior in Honey Bees

by Natalie J. Lemanski, Chelsea N. Cook, Brian H. Smith and Noa Pinter-Wollman

Insects 2019, 10(11), 370; https://doi.org/10.3390/insects10110370 - 25 Oct 2019

Cited by 25 | Viewed by 4123

Abstract

The emergence of collective behavior from local interactions is a widespread phenomenon in social groups. Previous models of collective behavior have largely overlooked the impact of variation among individuals within the group on collective dynamics. Honey bees (Apis mellifera) provide an excellent model [...] Read more.

The emergence of collective behavior from local interactions is a widespread phenomenon in social groups. Previous models of collective behavior have largely overlooked the impact of variation among individuals within the group on collective dynamics. Honey bees (Apis mellifera) provide an excellent model system for exploring the role of individual differences in collective behavior due to their high levels of individual variation and experimental tractability. In this review, we explore the causes and consequences of individual variation in behavior for honey bee foraging across multiple scales of organization. We summarize what is currently known about the genetic, developmental, and neurophysiological causes of individual differences in learning and memory among honey bees, as well as the consequences of this variation for collective foraging behavior and colony fitness. We conclude with suggesting promising future directions for exploration of the genetic and physiological underpinnings of individual differences in behavior in this model system. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

11 pages, 246 KiB

Open AccessReview

Honey Bee Alarm Pheromone Mediates Communication in Plant–Pollinator–Predator Interactions

by Zhengwei Wang and Ken Tan

Insects 2019, 10(10), 366; https://doi.org/10.3390/insects10100366 - 21 Oct 2019

Cited by 11 | Viewed by 7337

Abstract

Honey bees play a crucial role in pollination, and in performing this critical function, face numerous threats from predators and parasites during foraging and homing trips. Back in the nest, their defensive behavior drives some individuals to sacrifice themselves while fighting intruders with [...] Read more.

Honey bees play a crucial role in pollination, and in performing this critical function, face numerous threats from predators and parasites during foraging and homing trips. Back in the nest, their defensive behavior drives some individuals to sacrifice themselves while fighting intruders with their stingers or mandibles. During these intense conflicts, bees release alarm pheromone to rapidly communicate with other nest mates about the present danger. However, we still know little about why and how alarm pheromone is used in plant–pollinator–predator interactions. Here, we review the history of previously detected bee alarm pheromones and the current state of the chemical analyses. More new components and functions have been confirmed in honey bee alarm pheromone. Then, we ask how important the alarm pheromones are in intra- and/or inter-species communication. Some plants even adopt mimicry systems to attract either the pollinators themselves or their predators for pollination via alarm pheromone. Pheromones are honest signals that evolved in one species and can be one of the main driving factors affecting co-evolution in plant–pollinator–predator interactions. Our review intends to stimulate new studies on the neuronal, molecular, behavioral, and evolutionary levels in order to understand how alarm pheromone mediates communication in plant–pollinator–predator interactions. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

16 pages, 2004 KiB

Open AccessReview

Effects of the Herbicide Glyphosate on Honey Bee Sensory and Cognitive Abilities: Individual Impairments with Implications for the Hive

by Walter M. Farina, M. Sol Balbuena, Lucila T. Herbert, Carolina Mengoni Goñalons and Diego E. Vázquez

Insects 2019, 10(10), 354; https://doi.org/10.3390/insects10100354 - 18 Oct 2019

Cited by 76 | Viewed by 13075

Abstract

The honeybee Apis mellifera is an important pollinator in both undisturbed and agricultural ecosystems. Its great versatility as an experimental model makes it an excellent proxy to evaluate the environmental impact of agrochemicals using current methodologies and procedures in environmental toxicology. The increase [...] Read more.

The honeybee Apis mellifera is an important pollinator in both undisturbed and agricultural ecosystems. Its great versatility as an experimental model makes it an excellent proxy to evaluate the environmental impact of agrochemicals using current methodologies and procedures in environmental toxicology. The increase in agrochemical use, including those that do not target insects directly, can have deleterious effects if carried out indiscriminately. This seems to be the case of the herbicide glyphosate (GLY), the most widely used agrochemical worldwide. Its presence in honey has been reported in samples obtained from different environments. Hence, to understand its current and potential risks for this pollinator it has become essential to not only study the effects on honeybee colonies located in agricultural settings, but also its effects under laboratory conditions. Subtle deleterious effects can be detected using experimental approaches. GLY negatively affects associative learning processes of foragers, cognitive and sensory abilities of young hive bees and promotes delays in brood development. An integrated approach that considers behavior, physiology, and development allows not only to determine the effects of this agrochemical on this eusocial insect from an experimental perspective, but also to infer putative effects in disturbed environments where it is omnipresent. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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13 pages, 1173 KiB

Open AccessReview

Genetics in the Honey Bee: Achievements and Prospects toward the Functional Analysis of Molecular and Neural Mechanisms Underlying Social Behaviors

by Hiroki Kohno and Takeo Kubo

Insects 2019, 10(10), 348; https://doi.org/10.3390/insects10100348 - 16 Oct 2019

Cited by 13 | Viewed by 6415

Abstract

The European honey bee is a model organism for studying social behaviors. Comprehensive analyses focusing on the differential expression profiles of genes between the brains of nurse bees and foragers, or in the mushroom bodies—the brain structure related to learning and memory, and [...] Read more.

The European honey bee is a model organism for studying social behaviors. Comprehensive analyses focusing on the differential expression profiles of genes between the brains of nurse bees and foragers, or in the mushroom bodies—the brain structure related to learning and memory, and multimodal sensory integration—has identified candidate genes related to honey bee behaviors. Despite accumulating knowledge on the expression profiles of genes related to honey bee behaviors, it remains unclear whether these genes actually regulate social behaviors in the honey bee, in part because of the scarcity of genetic manipulation methods available for application to the honey bee. In this review, we describe the genetic methods applied to studies of the honey bee, ranging from classical forward genetics to recently developed gene modification methods using transposon and CRISPR/Cas9. We then discuss future functional analyses using these genetic methods targeting genes identified by the preceding research. Because no particular genes or neurons unique to social insects have been found yet, further exploration of candidate genes/neurons correlated with sociality through comprehensive analyses of mushroom bodies in the aculeate species can provide intriguing targets for functional analyses, as well as insight into the molecular and neural bases underlying social behaviors. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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12 pages, 1447 KiB

Open AccessReview

The Neurophysiological Bases of the Impact of Neonicotinoid Pesticides on the Behaviour of Honeybees

by Amélie Cabirol and Albrecht Haase

Insects 2019, 10(10), 344; https://doi.org/10.3390/insects10100344 - 14 Oct 2019

Cited by 28 | Viewed by 5827

Abstract

Acetylcholine is the main excitatory neurotransmitter in the honeybee brain and controls a wide range of behaviours that ensure the survival of the individuals and of the entire colony. Neonicotinoid pesticides target this neurotransmission pathway and can thereby affect the behaviours under its [...] Read more.

Acetylcholine is the main excitatory neurotransmitter in the honeybee brain and controls a wide range of behaviours that ensure the survival of the individuals and of the entire colony. Neonicotinoid pesticides target this neurotransmission pathway and can thereby affect the behaviours under its control, even at doses far below the toxicity limit. These sublethal effects of neonicotinoids on honeybee behaviours were suggested to be partly responsible for the decline in honeybee populations. However, the neural mechanisms by which neonicotinoids influence single behaviours are still unclear. This is mainly due to the heterogeneity of the exposure pathways, doses and durations between studies. Here, we provide a review of the state of the science in this field and highlight knowledge gaps that need to be closed. We describe the agonistic effects of neonicotinoids on neurons expressing the different nicotinic acetylcholine receptors and the resulting brain structural and functional changes, which are likely responsible for the behavioural alterations reported in bees exposed to neonicotinoids. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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16 pages, 412 KiB

Open AccessReview

The Role of Landscapes and Landmarks in Bee Navigation: A Review

by Bahram Kheradmand and James C. Nieh

Insects 2019, 10(10), 342; https://doi.org/10.3390/insects10100342 - 12 Oct 2019

Cited by 13 | Viewed by 4081

Abstract

The ability of animals to explore landmarks in their environment is essential to their fitness. Landmarks are widely recognized to play a key role in navigation by providing information in multiple sensory modalities. However, what is a landmark? We propose that animals use [...] Read more.

The ability of animals to explore landmarks in their environment is essential to their fitness. Landmarks are widely recognized to play a key role in navigation by providing information in multiple sensory modalities. However, what is a landmark? We propose that animals use a hierarchy of information based upon its utility and salience when an animal is in a given motivational state. Focusing on honeybees, we suggest that foragers choose landmarks based upon their relative uniqueness, conspicuousness, stability, and context. We also propose that it is useful to distinguish between landmarks that provide sensory input that changes (“near”) or does not change (“far”) as the receiver uses these landmarks to navigate. However, we recognize that this distinction occurs on a continuum and is not a clear-cut dichotomy. We review the rich literature on landmarks, focusing on recent studies that have illuminated our understanding of the kinds of information that bees use, how they use it, potential mechanisms, and future research directions. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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16 pages, 3275 KiB

Open AccessReview

Neuroethology of the Waggle Dance: How Followers Interact with the Waggle Dancer and Detect Spatial Information

by Hiroyuki Ai, Ryuichi Okada, Midori Sakura, Thomas Wachtler and Hidetoshi Ikeno

Insects 2019, 10(10), 336; https://doi.org/10.3390/insects10100336 - 11 Oct 2019

Cited by 11 | Viewed by 4510

Abstract

Since the honeybee possesses eusociality, advanced learning, memory ability, and information sharing through the use of various pheromones and sophisticated symbol communication (i.e., the “waggle dance”), this remarkable social animal has been one of the model symbolic animals for biological studies, animal ecology, [...] Read more.

Since the honeybee possesses eusociality, advanced learning, memory ability, and information sharing through the use of various pheromones and sophisticated symbol communication (i.e., the “waggle dance”), this remarkable social animal has been one of the model symbolic animals for biological studies, animal ecology, ethology, and neuroethology. Karl von Frisch discovered the meanings of the waggle dance and called the communication a “dance language.” Subsequent to this discovery, it has been extensively studied how effectively recruits translate the code in the dance to reach the advertised destination and how the waggle dance information conflicts with the information based on their own foraging experience. The dance followers, mostly foragers, detect and interact with the waggle dancer, and are finally recruited to the food source. In this review, we summarize the current state of knowledge on the neural processing underlying this fascinating behavior. Full article

(This article belongs to the Special Issue Honeybee Neurobiology and Behavior)

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