The Foraging Behavior of the Honey Bee (Apis mellifera, L.)

The Foraging Behavior of the Honeybee (Apis mellifera, L.) provides a scholarly resource for knowledge on the regulation, communication, resource allocation, learning and characteristics of honeybee foraging behavior at the individual and colony level. Foraging, in this context, is the exploration of the environment around a honey bee hive and the collection of resources (pollen, nectar, water, etc.) by bees in the worker caste of a colony. Honeybees have the unique ability to balance conflicting and changing resource needs in rapidly changing environments, thus their characterization as “superorganisms made up of individuals who act in the interest of the whole.

This book explores the fascinating world of honey bees in their struggle to obtain food and resources in the ecosystem and environment around the hive. Written by a team of international experts on honey bee behavior and ecology, this book covers current and historical knowledge, research methods and modeling used in the field of study and includes estimates of key parameters of energy utilization, quantities of materials collected, and identifies inconsistencies or gaps in current knowledge in the field.

• Establishes a basis of current knowledge on honeybees to build and advance understanding of their foraging behavior
• Addresses stressors such as habitat loss, climate change, pesticides, pests and diseases
• Presents concise concepts that facilitate direct traceability to the original underlying research

• Language: English
• Publisher: Academic Press
• Release date: Oct 25, 2023
• ISBN: 9780323986199

Book preview

Chapter 1: Introduction

John Purdy    Abacus Consulting Services Ltd., Campbellville, ON, Canada

Abstract

This chapter describes the purpose and scope of the book, the approach taken in assembling literature, and a perspective on honey bees and bee research related to their foraging for food, water, nesting materials and new nest sites. The intent is to provide a brief overview of current science as a basis for understanding the specialist chapters that follow. Terminology is introduced in more detail than provided in the Glossary. A review of honey bee systematics and evolution, and an overview of major aspects of honey bees as social insects are included. The complex interplay of individual sensory inputs, genetics, learning, motivation and colony level influences on individual bee behavior is described. Major theories and concepts, including central place foraging are described. The individual agent hypothesis, which has emerged as the consensus view of social order is included. The significance of individual variability within the colony, which provides resilience to the colony in a rapidly changing environment and enables the stochastic problem-solving process that optimizes colony level behavior in the absence of a central command structure. The importance of computer modeling to enable simulation and prediction of foraging behavior is introduced, but the unprecedented success of the bee-foraging-inspired Artificial Bee Colony algorithm in finding optimal solutions to intractable problems is also noted. The influences of the state of the colony and the motivational state of individual bees on foraging are described.

A discussion of ecosystem level perspectives is provided as an introduction to the review in Chapter 6. Although there is a small persistent population of feral honey bees in many parts of the world, honey bees are primarily present as managed livestock. The population for bees in an area depends on how many colonies the beekeepers decide to put there regardless of the carrying capacity of the landscape. Chapter 8 discusses managed foraging for honey and crop pollination.

Keywords

Apis mellifera; behavior; carrying capacity; caste; central place foraging; cognition; eusocial; evolution; individual agent hypothesis; learning; memory modeling; orientation; ontogeny; optimization; phylogeny; quorum; state of the colony; stochastic

Chapter outline

Historical perspective

Scope and approach

Evolution and taxonomy

Methodology

Honey bee species

A. mellifera clades and subspecies

Genetic changes in evolution

Evolution of sociality

Social order—Population dynamics and self-assembly

The colony and the role of the worker caste

The self-assembled eusocial order of honey bees

Seasonal colony size and division of labor

Concepts of social order

Ontogeny—The making of a forager bee

Physical changes on transition to foraging

Regulation of the transition to foraging

Nutrition and provisioning of foragers

Regulation of foraging activity

Division of labor

Genetics and variability among bees

Sensory inputs to foraging

Resource selection

Cognition, motivation, and memory

Motivation and integration of cues—The state of the colony

Terminology related to the state of the colony

Ecosystem-level interactions of honey bee pollinators

Feral and managed honey bees

Adaptability

Conclusions

References

Historical perspective

The significance of honey bees for mankind is documented in prehistoric cave drawings and included in the literature from ancient civilizations to the present time (Crane, 1992). Honey bees form colonies of individuals that work together to build nests (hives) of wax and plant resin (propolis); they store honey and pollen as food. Even the earliest humans used these materials in diverse ways (Dunne et al., 2021) and marveled at the organized social behavior of these insects. The species of importance for human societies include Apis cerana, Apis dorsata, Apis florea, and Apis mellifera of the tribe Apini (Crane, 2004) as well as the stingless bees of the tribe Meliponini (Vit et al., 2013). The continued importance of honey bees for mankind appears in most publications related to bees. A detailed history of honey bees and beekeeping is beyond the scope of this book, but there are excellent reviews on the topic, which also provide profound insights into the gains and retreats involved in the advancement of beekeeping and the science of bees (Crane, 1983, 1999; Jones, 2013; Carlson, 2015).

The formal study of honey bees in science is quite recent. Early work centered on the observation and description of bees. It began in the 16th century (Crane, 1992) within the same mid-renaissance culture that gave rise to the scientific method itself (Klein and Giglioni, 2020). Early work centered on the observation and description of bees. The production of the European honey bee queen from eggs or young larvae was reported in 1568 by Nickel Jacob (Crane, 1992). The Melipona bees and bee culture in Brazil were first described in 1557 by Hans Staden and brought to light by recent historical reviews (Engels, 2009). The study of honey bees continues to grow with each technological advance, particularly with molecular biology, neurobiology, genomics, and the use of computer modeling. It is the study of a highly successful species with a magnificently intricate evolutionary design that is both efficient and resilient. However, the foraging of honey bees is, in itself, a complex and interesting topic, and few works focus specifically on this aspect of honey bee behavior. In summary, this book presents an exploration of how a honey bee is well suited to foraging, knows what to search for, finds what it seeks, and returns to the hive.

Scope and approach

This book focuses on the foraging behavior of A. mellifera at a level appropriate for university-level teaching and professional research. As such, a basic knowledge of honey bee science is helpful for the reader to take the best advantage of it. Fieldwork experience with honey bees is also beneficial. This introductory chapter gives an overview of honey bee biology, evolution, and ecology, and introduces some basic terminology and concepts. A glossary of technical terms is included at the end of the book.

For honey bees, foraging is not for the consumption of food by the forager, it is the search for and collection of food, water, minerals, or plant resins, or the identification of other resources such as nest sites for a reproductive swarm (Seeley and Visscher, 2003). Foraging is a complex pattern of innate and learned behaviors which is required to sustain both an individual colony and the entire species on an evolutionary timescale. Foraging behavior needs to be regulated to meet colony needs, efficient and well integrated into the anatomy and physiology of the honey bee. Honey bees have multiple adaptations to support this behavior at the individual and colony levels (see Chapters 2 and 3). Chapter 4 covers cognition learning and memory related to navigation, Chapter 5 describes the energetics of foraging, Chapter 6 discusses honey bee pollination ecology, Chapter 7 covers modeling applied to honey bee foraging, and Chapter 8 considers honey bees from the perspective of their use as agricultural livestock. A discussion of knowledge gaps and future directions is provided in Chapter 9.

The approach used in compiling the information for this book is based on searches of the peer-reviewed literature supplemented by searches in the noncurated media including Google Scholar. Publications that present original data and concepts have been preferred except in reference to fields outside the scope of honey bee foraging, or where the original work is no longer easily accessible. The basic quality of research on honey bees has been widely criticized (Cushnie and Lamb, 2005; Page, 2011; Menzel, 2019; Monks et al., 2019). While the study of honey bees has been widely pursued in diverse fields of study, it is uniquely challenging, because bees are tiny, live in large colonies, and fly well beyond a line of sight. Most aspects of bee behavior are influenced by multiple factors operating at the level of individual bees, colonies, or ecological communities. True replication may be difficult or impossible, and many reports are based on very few (<5) repetitions in a single area at one time of the year despite known high variability. Important aspects of the condition of colonies used in research reports are often unreported, such as the genetic lineage or the adequacy of food resources (carrying capacity) in the area of a field study; the occurrence of queen supersession; or the presence of parasites, viruses, or other diseases (Delaplane et al., 2013a,b; Human et al., 2013; Scheiner et al., 2013). Artifacts of experimental conditions abound, including seasonal effects, handling stress on bees (Havard et al., 2020), enhanced feeding at artificial feeders (Fernandez and Farina, 2005), unexpected metabolic linkages (Mayack et al., 2020), or increased pollen collection in response to the use of a pollen trap (Delaplane et al., 2013a). There is also confusion due to the imprecise use of terminology (Boomsma and Gawne, 2018). A critical and objective reading of reports in this field is particularly important.

As background reading, there are chapters on foraging among the textbooks and reviews that cover honey bee biology, ecology, and behavior (see, for example, Winston, 1987; Graham et al., 1992; Willmer, 2011a,b,c; Galizia et al., 2012). Earlier reviews that include honey bee foraging include van der Steen (2015) and Rodney and Purdy (2020).

Evolution and taxonomy

Methodology

The evolutionary history and phylogeny beginning from Hymenoptera to honey bees provide insights into the traits that sustain social foraging behavior and the taxonomic relationships give us many opportunities for comparisons (Engel, 1998; Weinstock et al., 2006; Raffiudin and Crozier, 2007). These fields of study and the ongoing progress of systematics are in a time of major changes brought about by combining a growing body of genomic data and advances in the methodology for analyzing it (Grafen, 1989; Danforth et al., 2013; Meixner et al., 2013). The results may change with the inclusion of additional samples. Fig. 1.1 provides a consensus overview of the major evolutionary transitions leading to A. mellifera based on the ITIS and the available literature on the evolution of honey bees (Ascher, 2020; Pulawski, 2021).

Fig. 1.1

Fig. 1.1 Phylogeny of evolutionary changes leading to the genus Apis and A. mellifera . This line drawing shows a consensus of the major division points in the current evolutionary lineage leading to the honey bees (genus Apis ) from a Hymenopteran ancestor based on literature up to 2021. The main sister taxa are included at each stage, along with some broader phylogenetic names and sister groups. No timescale is implied, but the suggested dates for the numbered nodes are given in Table 1.1.

The most important consideration in reviewing phylogenies is that the included species may represent entire lineages. For example, the separation of A. cerana and A. mellifera is the final genus level separation for the latter (Node 14 in Fig. 1.1) but only the beginning of the lineage of all other Apis (Node 15 in Fig. 1.1). Thus, the separation of A. cerana from other Apis lineages may be as recent as early workers indicated (Arias and Sheppard, 2005; Bossert et al., 2019). The key dates for the numbered nodes in Fig. 1.1 are given in Table 1.1.

Table 1.1

This table provides the proposed geological times and descriptions of the events at the numbered nodes in Fig. 1.1.

Hymenoptera and pollination: Based on estimates from fossils an association of insects with the pollination of plants occurred approximately 300 million years ago (MYA) (Scott and Taylor, 1983; Willmer, 2011a). This association developed through a long period of coevolution, particularly between angiosperms and bees (Apoidea). For more detail refer to Willmer (2011a), which includes four hypotheses for the causal relationship between the floral specialization of pollinators and rapid species diversification in the evolution of bees.

With this early and very successful association with Angiosperms, the bees obtained a completely balanced diet of sugar for energy from nectar and protein, lipids, minerals, and other nutrients from pollen, so the bees could regulate the amounts of these two foods collected separately according to their needs (Wright et al., 2018). The sugars in most nectars are glucose, fructose, and sucrose (De Groot, 1953) in mixtures that inhibit crystallization. Assuming this has not changed, this would have made more concentrated nectar feasible in the competition among plants for pollinators. For the bees, it would make nectar easier to handle and ingest. Nectar offers significant advantages in addition to being easily accessible. It is almost completely digestible. Hydrolysis of sucrose by salivary invertase is essentially complete before uptake in the foregut and in the conversion to honey for storage. Dietary sugars are ingested from the foregut distributed in the hemolymph and metabolized at the cellular level. Reserves are stored as trehalose (diglucose), which reduces the contribution to osmolarity and supports energy regulation (Crailsheim, 1988; Blatt and Roces, 2001). Metabolism of sugars produces only carbon dioxide and water, which can be exhaled or excreted as liquid (Suarez et al., 1996). Metabolic water with the water already in the nectar provides much of the water needed by bees (Nicolson, 2009; see Chapter 5, Energetics).

An important feature of pollen often overlooked is its stability. While pollen can spoil, as it loses nutritional value by air oxidation and contains antimicrobial compounds (Pacini and Hesse, 2005), it is sufficiently stable, particularly when mixed with saliva and nectar to be stored as food for larvae in a nest. The nectar adds energy and metabolic water to the provisions, but it is possible that ancient pollen, like the pollen of extant species, was hygroscopic and collected water from the air (Cane and Love, 2021). The availability of a complete diet from a seasonal but reliable and accessible source greatly simplifies the search for food compared to the predatory or parasitic ancestors of bees and this supported central place foraging (Orians and Pearson, 1979) and nest building, which protected offspring during development. On the other hand, it made the Anthophila entirely dependent on pollen and nectar from plants (Willmer, 2011a).

Honey bee species

There are currently eight species and three subgenera in Apis accepted by Integrated Taxonomic Information System (ITIS) (Ascher, 2020). The relationships among these species are shown in Fig. 1.1, and the current phylogeny of the genus Apis is presented in Table 1.2.

Table 1.2

Based on Ascher, J.S., 2020. Taxonomic Hierarchy of Apis (Linnaeus, 1758). Taxonomic Serial No.: 154395 Retrieved 11/08/21, from the Integrated Taxonomic Information System (ITIS), www.itis.gov, CC0 https://doi.org/10.5066/F7KH0KBK.

Three additional taxa have been suggested at the species level: Apis nuluensis (Arias and Sheppard, 2005), Apis breviligula, and Apis indica (Lo et al., 2010). Apis binghami, considered a species by Arias and Sheppard, was taken to be a subspecies of A. dorsata (Raffiudin and Crozier, 2007; Ascher, 2020) and omitted from Fig. 1.1.

Geographical origins for A. mellifera in many areas have been suggested but the most recent work supports the idea that the species originated in Asia, with multiple expansions into Africa and Europe. It is now considered to be endemic in Africa, Europe, and parts of Asia as far East as Mongolia and North West China (Dogantzis et al., 2021).

A. mellifera clades and subspecies

There is a remarkable diversity of behavior, form, and genetics within the species A. mellifera. Adaptability to survive in tropical to subarctic climates, using the local floral resources, and overcome competition, predation, and disease in these varied regions are other remarkable traits of this species. Much of this adaptability arises from the eusocial lifestyle and cavity nesting, which provides the controlled atmosphere within the hive and optimal harvesting of a reliable food supply from foraging on flowering plants (see Chapter 3).

The concept of geographic specialization or biogeography was introduced by Ruttner using statistical clustering of traits now referred to as classical morphometry (Ruttner, 1988). The major lineages have been confirmed (Ilyasov et al., 2020), but even with the introduction of genomics, progress in defining a minimal set of distinct lineages has been slow (Garnery et al., 1992; Alburaki et al., 2011). Only with a combination of advanced methods of statistical morphometry and molecular biology has it been possible to bring order to the complex array of subspecies and the intergrades among them. There are currently seven regional lineages in the phylogeny of A. mellifera, each designated by a single letter acronym: A (African), C (Eastern Europe), L (A. m. lamarckii, Egypt), M (Western Europe and Asia), O (Middle East), U (A. m. unicolor, Madagascar), and Y (Arabia). The phylogeny and biogeography of these lineages are illustrated in Fig. 1.2. Two lineages (S and Z) that were based on morphometry and mitochondrial DNA have been resolved as admixtures using nuclear DNA single-nucleotide polymorphisms (SNPs) (Dogantzis et al., 2021).

Fig. 1.2

Fig. 1.2 Biogeography and phylogeny of A. mellifera lineages. (A) Map of the native distribution of the seven genetically distinct lineages. (B) Evolutionary relationships among A. mellifera samples constructed with a neighbor-joining tree using single nucleotide polymorphisms (SNPs) located genome-wide. (C) Evolutionary relationships among A. mellifera samples constructed with a neighbor-joining tree using SNPs located within protein-coding regions. Asterisks represent node support of 100%. Node support and maximum likelihood. A. cerana was used as an outgroup. Adapted from Dogantzis, K.A., Tiwari, T., Conflitti, I.M., Dey, A., Patch, H.M., Muli, E.M., Garnery, L., Whitfield C.W., Stolle, E., Alqarni, A.S., Allsopp, M.H. Zayed, A., 2021. Thrice out of Asia and the adaptive radiation of the western honey bee. Sci. Adv. 7(49) eabj2151.

Description: This illustration shows a map of the geographic origins of the seven currently recognized lineages of A. mellifera in Europe, Africa, and Asia as described in the text, and two possible phylogenetic arrays obtained using the available samples of genetic material. One array used the entire genome and the other used only protein-coding sequences. The results were identical except for the position of the O lineage within the A group of samples and both had a 100% statistical likelihood for the major nodes.

It is no surprise that many A. mellifera subspecies have multiple names either through separate discoveries or by revision of the names over time. At least 33 subspecies are now recognized and more may be identified as the research proceeds (Kandemir et al., 2011; Coulibaly et al., 2019; Ilyasov et al., 2020; Alabdali et al., 2021). All of them are capable of interbreeding (Ruttner et al., 1978). For the remainder of this book, we use the name honey bee exclusively for A. mellifera, except where specified, and we use the names and spellings from Ilyasov et al. (2020) and the lineages from Dogantzis et al. (2021). The use of the two-word form of the common name follows the recommendation of the Entomological Society of America, although the single word honeybee is widely accepted.

The primary honey bee subspecies used in beekeeping are carniola, caucasia, ligustica, and mellifera, in the M and C lineages of the European honey bee (Tihelka et al., 2020), although there are local exceptions, for example, in Arabia (Alabdali et al., 2021). It is these subspecies that have been most often moved to nonnative habitats around the world. Even in China, where the closely related endemic A. cerana has long been used for pollination and production of honey and wax, A. mellifera is favored for its productivity (Moritz et al., 2005).

Genetic changes in evolution

The mechanisms that brought about the evolutionary transitions (Table 1.1) have in some cases been discovered in genomic and proteomic studies of extant species of different evolutionary ages. Some transitions occur as a result of familiar mutation and recombination processes (Gadagkar, 1997). Many of the changes were supported by duplication of genetic sequences, repurposing or adding functionality to existing genes, or changes in the expression of genes (Amdam et al., 2006; Drapeau et al., 2006; Lin et al., 2021). Often the same genes have multiple roles in different circumstances (pleiotropic). In three examples, it has been shown that an ancestral reproductive gene set was coopted to regulate behavior in honey bees in the reproductive ground plan (RGP) (Amdam et al., 2004; Hunt et al., 2007; Rueppell et al., 2004; Wang et al., 2009; West-Eberhard, 1996): 1) the ovaries of nonreproductive workers influence their behavior (Wang et al., 2010). 2) The egg protein vitellogenin plays a role in protein storage for bees in winter (Amdam and Omholt, 2002). 3) Vitellogenin acts with juvenile hormone to regulate the age of transition to foraging (Amdam and Omholt, 2003). In some cases, multiple genes evolved into a quantitative trait locus (QTL) which governs the development of a trait such as foraging (Hunt et al., 1995, 2007). There is also a QTL responsible for controlling the age of transition to foraging (Rueppell, 2009).

Some genes, even within a QTL, such as the foraging gene PKG and the complementary sex-determining (CSD) locus are highly conserved across diverse species (Beye et al., 2003; Fitzpatrick and Sokolowski, 2004). The mitochondrial DNA used in epigenetic studies is also conserved through the maternal line and can be used in phylogenetic studies (Beye et al., 2003; Zheng et al., 2018).

Since honey bees are polyphenic, the role of gene regulatory mechanisms in determining the path taken in the development of the various phenotypes is very important, and in honey bees the process is to some extent reversible at the level of gene expression (Herb et al., 2012; Sieber et al., 2021). A level of organization even higher than the QTL is the recently reported gene regulatory network (GRN) which governs patterns of ontogeny or behavior through the coordinated influence of large numbers of genes (Jones et al., 2020; Sinha et al., 2020). In honey bees, the regulation and ontogeny of traits in an individual bee are highly complex and involve the interaction of genes at multiple locations (epistatic) with sensory inputs (Rueppell et al., 2006).

Evolution of sociality

The influence of relatedness is considered to be the main impetus for the evolution of sociality in honey bees (Rautiala et al., 2019). Hamilton introduced the concept of inclusive fitness to describe how the genes in the members of a colony have a probability to be inherited in proportion to their relatedness, i.e., how many of them share the same genes. He quantified the bias toward relatedness among members of a colony that results from haplodiploid genetics using a mathematical model (Hamilton, 1964, 1972; Rautiala et al., 2019). Inclusive fitness arises from cooperative behavior and altruism among members of a colony and operates on the genes of reproductive bees (Page et al., 2006; Rautiala et al., 2019). Support for this theory, which is a more general form of kin selection theory has been added from genomics (Boomsma and Franks, 2006; Rautiala et al., 2019) and behavioral studies (Getz et al., 1982; Page, 2011). Essentially, this was a quantification of the colony as a reproductive unit. Hamilton’s inclusive fitness theory explains why most social species are in the Hymenoptera and have female workers (Rautiala et al., 2019).

The involvement of multigene regulatory networks (GRNs) (Chandrasekaran et al., 2011; Sinha et al., 2020) implies that multiple transitions were involved in the evolution of sociality (Hunt, 2012). The evolution of sociality was marked by increasingly complex and responsive genetic pathways beyond the fixed GRNs (Kapheim, 2017; see Chapter 3). Some developmental and regulatory gene expression is determined by the activation status at one or more separate genes, which is called epistasis (Page et al., 2012). The stability of the social lifestyle is established in the genus Apis and genomic studies have helped to elucidate which genes are involved in the social genome (Fouks et al., 2021). There is consensus that the genes that govern sociality are not unique, but were inherited from solitary ancestors (Wenseleers, 2009).

Honey bees, such as Hymenoptera, have haplodiploid genetics of reproduction (Dzierzon, 1845; Whiting, 1945; Page et al., 2002), and this has a major influence on how genes are inherited. Males (drones) arise from unfertilized eggs in the form of parthenogenesis called arrhenotoky and are haploid, while females are born from fertilized eggs and may develop into a diploid queen or worker depending on how the larvae are raised (Cook, 1993). There is no sex chromosome, but A. mellifera has a single CSD locus. In eggs that are heterozygous at this locus, CSD induces the fem gene, which sustains the development of the female sex (Heimpel and de Boer, 2008; Gempe et al.,