Browsing by Author "Spivak, Marla"

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3-Acyl dihydroflavonols from poplar resins collected by honey bees are active against the bee pathogens Paenibacillus larvae and Ascosphaera apis
(Elsevier, 2017) Wilson, Michael B.; Pawlus, Alison D.; Brinkman, Doug; Gardner, Gary; Hegeman, Adrian D.; Spivak, Marla; Cohen, Jerry D.
Honey bees, Apis mellifera, collect antimicrobial plant resins from the environment and deposit them in their nests as propolis. This behavior is of practical concern to beekeepers since the presence of propolis in the hive has a variety of benefits, including the suppression of disease symptoms. To connect the benefits that bees derive from propolis with particular resinous plants, we determined the identity and botanical origin of propolis compounds active against bee pathogens using bioassay-guided fractionation against the bacterium Paenibacillus larvae, the causative agent of American foulbrood. Eleven dihydro-flavonols were isolated from propolis collected in Fallon, NV, including pinobanksin-3-octanoate. This hitherto unknown derivative and five other 3-acyl-dihydroflavonols showed inhibitory activity against both P. larvae (IC50 ¼ 17e68 mM) and Ascosphaera apis (IC50 ¼ 8e23 mM), the fungal agent of chalkbrood. A structure-activity relationship between acyl group size and antimicrobial activity was found, with longer acyl groups increasing activity against P. larvae and shorter acyl groups increasing activity against A. apis. Finally, it was determined that the isolated 3-acyl-dihydroflavonols originated from Populus fremontii, and further analysis showed these compounds can also be found in other North American Populus spp.
Befriending Bumble Bees: A Practical Guide to Raising Local Bumble Bees
(St. Paul, MN: University of Minnesota Extension Service, 2007) Evans, Elaine; Burns, Ian; Spivak, Marla
Methods for rearing native bumblebee, Bombus impatiens, in confinement. The methods can be used to rear bumblebee colonies for backyard garden pollination, for commercial hot-house pollination of tomatoes, for cranberry and blueberry growers, and to help with native prairie restoration projects.
Behavioral defenses of honey bees against Varroa jacobsoni Oud.
(1999) Boecking, Otto; Spivak, Marla
Two behaviors of honey bees, hygienic behavior and grooming, are mechanisms of defense against brood diseases and parasitic mites. Studies have shown that Apis mellifera colonies remove worker brood infested with Varroa jacobsoni mites from the nest (hygienic behavior), and groom the mites off other adult bees, but to a limited extent compared to the original host of V. jacobsoni, A. cerana. Research is reviewed on hygienic and grooming behaviors with respect to their potential as mechanisms of resistance to V. jacobsoni. Studies related to hygienic behavior include the removal of experimentally infested and naturally infested brood, measurements of heritability, the uncapping and recapping of cells containing infested pupae, and the detection of infested brood. Studies on grooming include the process by which a groomer detects and damages a mite found on itself or on another adult bee, how the behavior is quantified, and problems with these methods of quantification. Finally, unresolved questions concerning grooming and the effects of hygienic and non-hygienic behaviors on limiting the population growth of V. jacobsoni are discussed.
Climatic limits of tropical African honeybees in the Americas
(International Bee Research Association, 1984) Orley, Taylor R., Jr.; Spivak, Marla
Facultative expression of hygienic behaviour of honey bees in relation to disease resistance
(Taylor and Francis, 1993) Spivak, Marla; Gilliam, Martha
Four experiments were conducted to examine factors that influence the expression of hygienic and non-hygienic behaviour in honey bees, Apis mel/itera, 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 nonhygienic colonies from 1O-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, suggesting that non-hygienic bees either could not detect dead or diseased brood or avoided it by sealing it within a comb cell. The third experiment tested whether the degree of hygienic behaviour could be increased by adding hygienic bees to non-hygienic colonies. Adding 20-30% young hygienic bees to nonhygienic colonies did not increase the degree of hygienic behaviour, but adding young nonhygienic bees to hygienic colonies suppressed the behaviour. The results suggest that although hygienic behavior is genetically determined, its expression depends on colony strength and composition of workers within the colony. In the fourth experiment, the hygienic and non-hygienic colonies were fed with pollen patties containing A. apis spores. The weak correspondence that was observed between removal behaviour and physiological resistance to chalkbrood suggested that few colonies are both highly hygienic and physiologically resistant to chalkbrood. Selection against uncapping and removing diseased brood might occur if this behaviour also promotes the spread of disease through the colony. This possibility is discussed in relation to avoidance behaviour of other social insects toward pathogens.
Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor
(2007) Ibrahim, Abdullah; Reuter, Gary S.; Spivak, Marla
We compared colonies selectively bred for both hygienic behavior and Suppression of Mite Reproduction (HYG/SMR) with colonies bred solely for hygienic behavior (HYG) and unselected control colonies. Colonies were evaluated for strength, brood viability, removal of freeze-killed brood, honey production, mite loads on adult bees and within worker brood, and mite reproductive success on worker brood for two years in two locations. By autumn in both years, the HYG/SMR colonies had significantly fewer mites on adult bees and in worker brood compared to the control colonies, and the HYG colonies had intermediate mite populations. Contrary to expectation, there were no differences among the lines in mite reproductive success. Further studies are required to determine if the genes and neural mechanisms that regulate the SMR trait are the same or different from those regulating hygienic behavior.
Honey bee hygienic behavior and defense against Varroa jacobsoni
(Springer, 1996) Spivak, Marla
Hygienic and non-hygienic colonies from ’Starline’ stock of Apis mellifera were tested for their ability to remove pupae infested with Varroa mites. The hygienic and non-hygienic lines were selected and bred on the basis of their removal response to freeze-killed brood. A Jenter Box® was used to test whether they would remove experimentally infested pupae following methods of Boecking and Drescher (1992). In 1994, the hygienic colonies removed significantly more pupae infested with one mite per cell than the non-hygienic colonies. In 1995, there was no significant difference between the hygienic and non-hygienic colonies when one or two mites were introduced per pupa due to variation in response among hygienic colonies. There was no significant difference between the rate of removal of infested pupae from the Jenter Box and from natural wax comb by the hygienic colonies. The number of mites damaged by grooming ranged from 6.0 to 42.3% among all colonies. The reproductive success of the mites not removed from the cells by the bees was low in both hygienic and non-hygienic colonies.
Hygienic behaviors of honey bees in response to brood experimentally pin-killed or infected with Ascosphaera apis
(2010) Palacio, María Alejandra; Rodriguez, Edgardo; Goncalves, Lionel; Bedascarrasbure, Enrique; Spivak, Marla
Hygienic behavior of honeybees involves inspection, uncapping and removal of diseased and dead brood from the colony. The objective of this work was to study the activities involved in hygienic behavior of individually tagged bees from selected hygienic (H) and non-hygienic (NH) colonies in the presence of chalkbrood infected brood (Ascosphaera apis) or pin-killed brood. No significant difference was detected in the age of bees inspecting, uncapping or removing brood in H and NH colonies; the median age was 15 days for all activities. The percentage of bees that performed these activities was significantly higher in H colonies. In NH colonies the bees that performed this behavior were more persistent but bees in H colonies were more efficient in the removal of the chalkbrood mummies. H colonies began uncapping more rapidly in response to the stimulus of dead brood independent of the method used to kill it. H and NH bees took the same amount of time to remove the mummies once they initiated the uncapping process but NH colonies took longer to remove pin-killed brood. These findings confirm previous behavioral studies on the activities of hygienic and non-hygienic bees toward freeze-killed brood, but this is the first time the entire process from inspection to removal was focused on individual cells containing actual diseased brood.
Hygienic behaviour of honey bees and its application for control of brood diseases and varroa: Part I. Hygienic behaviour and resistance to American foulbrood
(International Bee Research Association, 1998) Spivak, Marla; Gilliam, Martha
There have been very few studies on hygienic behaviour as a mechanism of resistance to American foulbrood since Park, Woodrow, Rothenbuhler, and Rothenbuhler’s students published their seminal work.The studies outlined in this part of the review form the core of information from which all later studies on hygienic behaviour have been based.
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
(International Bee Research Association, 1998) Spivak, Marla; Gilliam, Martha
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.
Increased resin collection after parasite challenge: a case of self-medication in honey bees?
(Public Library of Science, 2012) Simone-Finstrom, Michael D.; Spivak, Marla
The constant pressure posed by parasites has caused species throughout the animal kingdom to evolve suites of mechanisms to resist infection. Individual barriers and physiological defenses are considered the main barriers against parasites in invertebrate species. However, behavioral traits and other non-immunological defenses can also effectively reduce parasite transmission and infection intensity. In social insects, behaviors that reduce colony-level parasite loads are termed “social immunity.” One example of a behavioral defense is resin collection. Honey bees forage for plant-produced resins and incorporate them into their nest architecture. This use of resins can reduce chronic elevation of an individual bee's immune response. Since high activation of individual immunity can impose colony-level fitness costs, collection of resins may benefit both the individual and colony fitness. However the use of resins as a more direct defense against pathogens is unclear. Here we present evidence that honey bee colonies may self-medicate with plant resins in response to a fungal infection. Self-medication is generally defined as an individual responding to infection by ingesting or harvesting non-nutritive compounds or plant materials. Our results show that colonies increase resin foraging rates after a challenge with a fungal parasite ( Ascophaera apis : chalkbrood or CB). Additionally, colonies experimentally enriched with resin had decreased infection intensities of this fungal parasite. If considered self-medication, this is a particularly unique example because it operates at the colony level. Most instances of self-medication involve pharmacophagy, whereby individuals change their diet in response to direct infection with a parasite. In this case with honey bees, resins are not ingested but used within the hive by adult bees exposed to fungal spores. Thus the colony, as the unit of selection, may be responding to infection through self-medication by increasing the number of individuals that forage for resin.
Individual precocity, temporal persistence, and task-specialisation of hygienic bees from selected colonies of Apis mellifera.
(De Gruyter Open, 2016) Scannapieco, Alejandra C.; Lanzavecchia, Silvia B.; Parreño, María A.; Liendo, María C.; Cladera, Jorge L.; Spivak, Marla; Palacio, María A.
Hygienic behaviour is a complex trait that gives Apis mellifera L. resistance against brood diseases. Variability in the expression of hygienic behaviour is evidenced at the colonylevel and is explained by the proportion and propensity of individual worker bees that engage in hygienic activities. We investigated the temporal performance and the dynamics of task-specialisation of individual bees over time, both in selected hygienic (H) and non-hygienic (NH) colonies. Then we evaluated the impact of these behavioural aspects on the colony performance. Bees that perform hygienic behaviour (hygienic bees) in our H colonies were more persistent in the hygienic activities throughout the days of the investigation. Such bees were more efficient in the removal of pin-killed brood than hygienic bees in the NH colonies. Hygienic bees in the H colonies were also specialist in the sub-tasks involved in the detection of odour stimulus from dead brood and continued to perform these activities throughout the days of the investigation (temporal persistence). Age-distribution of hygienic bees in the H colonies was asymmetrical, with a larger proportion of these bees performing hygienic activities early in life. At a colony-level, H showed higher efficiency compared to the NH colonies. The present results highlight the fact that individual behaviour may influence the collective dynamics of the hygienic behaviour in honeybee colonies. The results also note that the selection for highly hygienic colonies would result in changes in individual bees that improve the performance of the behaviour at the colony level. The relevance of task-partitioning and age-specialisation of hygienic bees on social immunity is discussed.
Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health
(Public Library of Science, 2014) Chen, Yan Ping; Pettis, Jeffery S; Corona, Miguel; Chen, Wei Ping; Li, Cong Jun; Spivak, Marla; Visscher, P. Kirk; DeGrandi-Hoffman, Gloria; Boncristiani, Humberto; Zhao, Yan; vanEngelsdorp, Dennis; Delaplane, Keith; Solter, Leellen; Drummond, Francis; Kramer, Matthew; Lipkin, W. Ian; Palacios, Gustavo; Hamilton, Michele C; Smith, Barton; Huang, Shao Kang; Zheng, Huo Qing; Li, Ji Lian; Zhang, Xuan; Zhou, Ai Fen; Wu, Li You; Zhou, Ji Zhong; Lee, Myeong-L; Teixeira, Erica W; Li, Zhi Guo; Evans, Jay D; Schneider, David S
Israeli acute paralysis virus (IAPV) is a widespread RNA virus of honey bees that has been linked with colony losses. Here we describe the transmission, prevalence, and genetic traits of this virus, along with host transcriptional responses to infections. Further, we present RNAi-based strategies for limiting an important mechanism used by IAPV to subvert host defenses. Our study shows that IAPV is established as a persistent infection in honey bee populations, likely enabled by both horizontal and vertical transmission pathways. The phenotypic differences in pathology among different strains of IAPV found globally may be due to high levels of standing genetic variation. Microarray profiles of host responses to IAPV infection revealed that mitochondrial function is the most significantly affected biological process, suggesting that viral infection causes significant disturbance in energy-related host processes. The expression of genes involved in immune pathways in adult bees indicates that IAPV infection triggers active immune responses. The evidence that silencing an IAPV-encoded putative suppressor of RNAi reduces IAPV replication suggests a functional assignment for a particular genomic region of IAPV and closely related viruses from the Family Dicistroviridae, and indicates a novel therapeutic strategy for limiting multiple honey bee viruses simultaneously and reducing colony losses due to viral diseases. We believe that the knowledge and insights gained from this study will provide a new platform for continuing studies of the IAPV–host interactions and have positive implications for disease management that will lead to mitigation of escalating honey bee colony losses worldwide.
Linking measures of colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use
(Public Library of Science, 2016) Smart, Matthew; Pettis, Jeff; Rice, Nathan; Browning, Zac; Spivak, Marla
We previously characterized and quantified the influence of land use on survival and productivity of colonies positioned in six apiaries and found that colonies in apiaries surrounded by more land in uncultivated forage experienced greater annual survival, and generally more honey production. Here, detailed metrics of honey bee health were assessed over three years in colonies positioned in the same six apiaries. The colonies were located in North Dakota during the summer months and were transported to California for almond pollination every winter. Our aim was to identify relationships among measures of colony and individual bee health that impacted and predicted overwintering survival of colonies. We tested the hypothesis that colonies in apiaries surrounded by more favorable land use conditions would experience improved health. We modeled colony and individual bee health indices at a critical time point (autumn, prior to overwintering) and related them to eventual spring survival for California almond pollination. Colony measures that predicted overwintering apiary survival included the amount of pollen collected, brood production, and Varroa destructor mite levels. At the individual bee level, expression of vitellogenin, defensin1, and lysozyme2 were important markers of overwinter survival. This study is a novel first step toward identifying pertinent physiological responses in honey bees that result from their positioning near varying landscape features in intensive agricultural environments.
Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees
(Public Library of Science, 2013) Wilson, Michael B.; Spivak, Marla; Hegeman, Adrian D.; Rendahl, Aaron; Cohen, Jerry D.
The deposition of antimicrobial plant resins in honey bee, Apis mellifera, nests has important physiological benefits. Resin foraging is difficult to approach experimentally because resin composition is highly variable among and between plant families, the environmental and plant-genotypic effects on resins are unknown, and resin foragers are relatively rare and often forage in unobservable tree canopies. Subsequently, little is known about the botanical origins of resins in many regions or the benefits of specific resins to bees. We used metabolomic methods as a type of environmental forensics to track individual resin forager behavior through comparisons of global resin metabolite patterns. The resin from the corbiculae of a single bee was sufficient to identify that resin’s botanical source without prior knowledge of resin composition. Bees from our apiary discriminately foraged for resin from eastern cottonwood (Populus deltoides), and balsam poplar (P. balsamifera) among many available, even closely related, resinous plants. Cottonwood and balsam poplar resin composition did not show significant seasonal or regional changes in composition. Metabolomic analysis of resin from 6 North American Populus spp. and 5 hybrids revealed peaks characteristic to taxonomic nodes within Populus, while antimicrobial analysis revealed that resin from different species varied in inhibition of the bee bacterial pathogen, Paenibacillus larvae. We conclude that honey bees make discrete choices among many resinous plant species, even among closely related species. Bees also maintained fidelity to a single source during a foraging trip. Furthermore, the differential inhibition of P. larvae by Populus spp., thought to be preferential for resin collection in temperate regions, suggests that resins from closely related plant species many have different benefits to bees.
A multifactorial study of the resistance of honeybees Apis mellifera to the mite Varroa destructor over one year in Mexico
(2005) Mondragon, Luis; Spivak, Marla; Vandame, Remy
A one year study was conducted to evaluate the population growth of three kinds of honey bee colonies and Varroa destructor mites in Mexico, and to estimate the relative contributions of three resistance mechanisms of the bees: hygienic behavior, grooming behavior, and reproductive ability of the parasite. Very significant changes over the year were observed in the number of mated female offspring produced per mother mite (Wr), mite fertility and mutilation of V. destructor. These changes were correlated to the total number of mites per colony. A factorial analysis showed that two mechanisms explained the variation in the amount of mites per colony: Wr (r2 = 0.73) and proportion of mutilated mites (r2 = 0.51). A multi-factorial model including these two mechanisms was significant (r2 = 0.97). The mite fecundity and the hygienic behavior could not explain the population changes of the mite, and the different kinds of bees showed no differences in the expression of the resistance mechanisms.
Performance of hygienic honey bee colonies in a commercial apiary
(1998) Spivak, Marla; Reuter, Gary S.
Colonies with naturally mated queens from a hygienic line of Italian honey bees (Apis mellifera ligustica) were compared to colonies from a commercial line of Italian bees not selected for hygienic behavior. The following characteristics were compared: rate of removal of freeze-killed brood; amount of chalkbrood; incidence of American foulbrood; honey production; and the number of mites, Varroa jacobsoni, on adult bees. The hygienic colonies removed significantly more freeze-killed brood than the commercial colonies, had significantly less chalkbrood, had no American foulbrood, and produced significantly more honey than the commercial colonies. Estimates of the number of Varroa mites on adult bees indicated that the hygienic colonies had fewer mites than the commercial colonies in three of four apiaries. In previous studies on the relation between hygienic behavior and resistance to diseases and mites, the test colonies contained instrumentally inseminated queens. This is the first study to evaluate hygienic stock in large field colonies with naturally mated queens.
Physiological and behavioral changes in honey bees (Apis mellifera) induced by Nosema ceranae infection
(Public Library of Science, 2013) Goblirsch, Mike; Huang, Zachary Y.; Spivak, Marla
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.
Propolis and bee health: the natural history and significance of resin use by honey bees
(2010) Simone-Finstrom, Michael; Spivak, Marla
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.
Propolis counteracts some threats to honey bee health
(MDPI, 2017) Simone-Finstrom, Michael; Borba, Renata S.; Wilson, Michael; Spivak, Marla
Honey bees (Apis mellifera) are constantly dealing with threats from pathogens, pests, pesticides and poor nutrition. It is critically important to understand how honey bees’ natural immune responses (individual immunity) and collective behavioral defenses (social immunity) can improve bee health and productivity. One form of social immunity in honey bee colonies is the collection of antimicrobial plant resins and their use in the nest architecture as propolis. We review research on the constitutive benefits of propolis on the honey bee immune system, and its known therapeutic, colony-level effects against the pathogens Paenibacillus larvae and Ascosphaera apis. We also review the limited research on the effects of propolis against other pathogens, parasites and pests (Nosema, viruses, Varroa destructor, and hive beetles) and how propolis may enhance bee products such as royal jelly and honey. Although propolis may be a source of pesticide contamination, it also has the potential to be a detoxifying agent or primer of detoxification pathways, as well as increasing bee longevity via antioxidant-related pathways. Throughout this paper, we discuss opportunities for future research goals and present ways in which the beekeeping community can promote propolis use in standard colonies, as one way to improve and maintain colony health and resiliency.

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