Marla Spivak

Genetic, Individual, and Group Facilitation of Disease Resistance in Insect Societies

In this review, we provide a current reference on disease resistance in insect societies. We start with the genetics of immunity in the context of behavioral and physiological processes and scale up levels of biological organization until we reach populations. A significant component of this review focuses on Apis mellifera and its role as a model system for studies on social immunity. We additionally review the models that have been applied to disease transmission in social insects and elucidate areas for future study in the field of social immunity.

Socialized medicine: Individual and communal disease barriers in honey bees

Honey bees are attacked by numerous parasites and pathogens toward which they present a variety of individual and group-level defenses. In this review, we briefly introduce the many pathogens and parasites afflicting honey bees, highlighting the biology of specific taxonomic groups mainly as they relate to virulence and possible defenses. Second, we describe physiological, immunological, and behavioral responses of individual bees toward pathogens and parasites. Third, bees also show behavioral mechanisms for reducing the disease risk of their nestmates. Accordingly, we discuss the dynamics of hygienic behavior and other group-level behaviors that can limit disease. Finally, we conclude with several avenues of research that seem especially promising for understanding host-parasite relationships in bees and for developing breeding or management strategies for enhancing honey bee health. We discuss how human efforts to maintain healthy colonies intersect with similar efforts by the bees, and how bee management and breeding protocols can affect disease traits in the short and long term.

Propolis and bee health: the natural history and significance of resin use by honey bees*

Social immunity, which describes how individual behaviors of group members effectively reduce disease and parasite transmission at the colony level, is an emerging field in social insect biology. An understudied, but significant behavioral disease resistance mechanism in honey bees is their collection and use of plant resins. Honey bees harvest resins with antimicrobial properties from various plant species and bring them back to the colony where they are then mixed with varying amounts of wax and utilized as propolis. Propolis is an apicultural term for the resins when used by bees within a hive. While numerous studies have investigated the chemical components of propolis that could be used to treat human diseases, there is a lack of information on the importance of propolis in regards to bee health. This review serves to provide a compilation of recent research concerning the behavior of bees in relation to resins and propolis, focusing more on the bees themselves and the potential evolutionary benefits of resin collection. Future research goals are also established in order to create a new focus within the literature on the natural history of resin use among the social insects and role that propolis plays in disease resistance.ZusammenfassungDie „soziale Immunität“ als neues Forschungsfeld bei sozialen Insekten beschreibt, wie das individuelle Verhalten von Mitgliedern einer Gruppe wirkungsvoll die Verbreitung von Krankheiten und Parasiten auf der Ebene des Sozialstaates verhindern kann. Ein bisher zwar wenig untersuchtes aber wichtiges Verhaltensmerkmal zur Krankheitsabwehr bei Honigbienen ist die Verwendung von Pflanzenharzen. Honigbienen sammeln Harze mit antimikrobiellen Eigenschaften von verschiedenen Pflanzen, mischen diese dann im Bienenvolk mit unterschiedlichen Mengen von Wachs und benutzen dies als Propolis (Abb. 1–4). Propolis ist demnach der bienenkundliche Begriff für Harze, die im Bienenstock verwendet werden. Während es zahlreiche Untersuchungen zur Verwendung bestimmter Bestandteile des Propolis zur Krankheitsbekämpfung beim Menschen gibt, sind kaum Informationen über die Bedeutung von Propolis für die Bienengesundheit vorhanden.Dieses Review ist eine Zusammenstellung neuerer Forschungsergebnisse zum Verhalten der Bienen in Bezug auf Harze und Propolis mit dem Schwerpunkt auf die möglichen evolutiven Vorteile des Harzsammelns für die Honigbienen. Die Verwendung von Harzen durch Bienenvölker (Apis mellifera) ist weit verbreitet. Während es erhebliche Unterschiede zwischen einzelnen Völkern bzgl. der Menge an gesammelten Harzen und Propolis gibt, scheinen alle — und dabei insbesondere die wildlebenden — Bienenvölker das Propolis zur Auskleidung des gesamten Stockinneren zu benutzen. Es wird angenommen, dass Propolis dazu beiträgt, die Homöostase innerhalb des Bienenstockes aufrecht zu erhalten. Konkret könnte das Propolis dabei das mikrobielle Wachstum an den Beutenwänden reduzieren, unkontrollierten Luftzug ins Beuteninnere verhindern und zusätzlich mechanische Barrieren gegenüber Eindringlingen bilden. Einige Forschungsprojekte zeigen eindeutig, dass Propolis im Bienenstock direkt gegenüber Krankheitserregern (z.B. Amerikanische Faulbrut) und Parasiten (z.B. Kleiner Beutenkäfer, Varroa destructor) wirkt. Daneben scheint es aber auch eine subtilere Wirkung über die Unterstützung des individuellen Immunsystems zu geben. Die weiteren Forschungen sollten sich auf das bessere Verständnis der Verwendung von Harzen durch Honigbienen und andere soziale Insekten konzentrieren. Dafür gibt es eine Vielzahl an Forschungsfeldern, von den pharmazeutischen Möglichkeiten des Propolis für die menschliche Gesundheit über die Mechanismen der Sammelstrategie von Propolis auf den Ebenen der Einzelbienen und des Bienenvolkes bis hin zu einer möglichen Anwendung von Propolis als Bekämpfung von Bienenkrankheiten. Schließlich ermöglichen Informationen zur Verwendung von Harzen und deren Aufnahme in den Bienenstock spannende Forschungsansätze zum Einfluss der Umwelt auf Krankheitsresistenz und soziale Immunität.

Hygienic behaviour of honey bees and its application for control of brood diseases and varroa: Part II. Studies on hygienic behaviour since the Rothenbuhler era

Part I of this review summarized the initial research on hygienic behaviour of honey bees, Apis mellifera. This early work that concerned hygienic behaviour as a mechanism of resistance to American foulbrood (AFB) has been the foundation for all subsequent research on hygienic behaviour. In Part II, research on hygienic behaviour in relation to other bee diseases and to Varroa jacobsoni and in Apis species and subspecies is reviewed. In addition, techniques to screen bee colonies for the behaviour are detailed, and practical applications of breeding bees for hygienic behaviour are given. A section on neuroethology demonstrates how modern neurobiological techniques are being used to detect the reasons for differences in responses of hygienic and non-hygienic bees to abnormal brood.

Varroa destructor Infestation in Untreated Honey Bee (Hymenoptera: Apidae) Colonies Selected for Hygienic Behavior

Abstract Honey bee (Apis mellifera L.) colonies bred for hygienic behavior were tested in a large field trial to determine if they were able to resist the parasitic mite Varroa destructor better than unselected colonies of “Starline” stock. Colonies bred for hygienic behavior are able to detect, uncap, and remove experimentally infested brood from the nest, although the extent to which the behavior actually reduces the overall mite-load in untreated, naturally infested colonies needed further verification. The results indicate that hygienic colonies with queens mated naturally to unselected drones had significantly fewer mites on adult bees and within worker brood cells than Starline colonies for up to 1 yr without treatment in a commercial, migratory beekeeping operation. Hygienic colonies actively defended themselves against the mites when mite levels were relatively low. At high mite infestations (>15% of worker brood and of adult bees), the majority of hygienic colonies required treatment to prevent collapse. Overall, the hygienic colonies had similar adult populations and brood areas, produced as much honey, and had less brood disease than the Starline colonies. Thus, honey bees bred for hygienic behavior performed as well if not better than other commercial lines of bees and maintained lower mite loads for up to one year without treatment.

Physiological and Behavioral Changes in Honey Bees (Apis mellifera) Induced by Nosema ceranae Infection

Persistent exposure to mite pests, poor nutrition, pesticides, and pathogens threaten honey bee survival. In healthy colonies, the interaction of the yolk precursor protein, vitellogenin (Vg), and endocrine factor, juvenile hormone (JH), functions as a pacemaker driving the sequence of behaviors that workers perform throughout their lives. Young bees perform nursing duties within the hive and have high Vg and low JH; as older bees transition to foraging, this trend reverses. Pathogens and parasites can alter this regulatory network. For example, infection with the microsporidian, Nosema apis, has been shown to advance behavioral maturation in workers. We investigated the effects of infection with a recent honey bee pathogen on physiological factors underlying the division of labor in workers. Bees infected with N. ceranae were nearly twice as likely to engage in precocious foraging and lived 9 days less, on average, compared to controls. We also show that Vg transcript was low, while JH titer spiked, in infected nurse-aged bees in cages. This pattern of expression is atypical and the reverse of what would be expected for healthy, non-infected bees. Disruption of the basic underpinnings of temporal polyethism due to infection may be a contributing factor to recent high colony mortality, as workers may lose flexibility in their response to colony demands.

Hygienic behaviour of honey bees and its application for control of brood diseases and varroa: Part I. Hygienic behaviour and resistance to American foulbrood

There have been very few studies on hygienic behaviour as a mechanism of resistance to American foulbrood since Park, Woodrow, Rothenbuhler, and Rothenbuhlers students published their seminal work...

Seven suggestive quantitative trait loci influence hygienic behavior of honey bees

Abstract. In 1964, Walter Rothenbuhler proposed a two-gene model to explain phenotypic variance in the remarkable behavior in which honey bee workers remove dead brood from their colonies. Rothenbuhlers model proposed that one locus controls the uncapping of brood cells containing dead pupae, while a second controls the removal of the cell contents. We show here, through molecular techniques and quantitative trait loci (QTL) linkage mapping, that the genetic basis of hygienic behavior is more complex, and that many genes are likely to contribute to the behavior. In our cross, we detected seven suggestive QTLs associated with hygienic behavior. Each detected QTL controlled only 9–15% of the observed phenotypic variance in the character.

Effects of Fluvalinate and Coumaphos on Queen Honey Bees (Hymenoptera: Apidae) in Two Commercial Queen Rearing Operations

Abstract We conducted research on the potential impacts of fluvalinate and coumaphos on honey bee, Apis mellifera L., queen viability and health. Queens were reared in colonies that had been treated with differing amounts of both fluvalinate and coumaphos. Pre- and posttreatment samples of both wax and bees were collected from all of the colonies and analyzed for total concentrations of fluvalinate and coumaphos. All queens were measured for queen weight, ovarial weight, and number of sperm in the spermathecae. The queens treated with high doses of fluvalinate weighed significantly less than low-dose or control queens, but otherwise appeared to develop normally. The highest fluvalinate concentrations were observed in the wax and queen cells of the high-dose group. The developing queens in colonies treated with as little as one coumaphos-impregnated strip for more than 24 h suffered a high mortality rate. Several of the queens showed sublethal effects from the coumaphos, including physical abnormalities and atypical behavior. The queens exposed to coumaphos weighed significantly less and had lower ovary weights than the control group queens. The highest coumaphos concentrations were observed in the queen cells and wax of the high-dose groups.

Facultative expression of hygienic behaviour of honey bees in relation to disease resistance

SUMMARYFour experiments were conducted to examine factors that influence the expression of hygienic and non-hygienic behaviour in honey bees, Apis mellifera, and to examine the correlation between this behaviour and resistance to chalkbrood, Ascosphaera apis. Colonies were headed by instrumentally inseminated queens selected on the basis of uncapping and removal behaviour expressed by their progeny. In the first experiment, colony strength was altered by transferring hygienic and non- hygienic colonies from 10-frame field hives to 2-frame observation hives. This treatment significantly reduced the hygienic response of the hygienic bees but did not affect the response of the non-hygienic bees. In the second experiment, hygienic and non-hygienic bees displayed different responses to freeze-killed and live brood which had been partially or entirely uncapped. Both lines of bees recapped both partially and entirely uncapped live brood, but non-hygienic bees also recapped partially uncapped freeze-killed brood,...