Bee Lab

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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.
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.
A cell line resource derived from honey bee (Apis mellifera) embryonic tissues
(Public Library of Science, 2013) Goblirsch, Michael J.; Spivak, Marla S.; Kurtti, Timothy J.
A major hindrance to the study of honey bee pathogens or the effects of pesticides and nutritional deficiencies is the lack of controlled in vitro culture systems comprised of honey bee cells. Such systems are important to determine the impact of these stress factors on the developmental and cell biology of honey bees. We have developed a method incorporating established insect cell culture techniques that supports sustained growth of honey bee cells in vitro. We used honey bee eggs mid to late in their embryogenesis to establish primary cultures, as these eggs contain cells that are progressively dividing. Primary cultures were initiated in modified Leibovitz’s L15 medium and incubated at 32°C. Serial transfer of material from several primary cultures was maintained and has led to the isolation of young cell lines. A cell line (AmE-711) has been established that is composed mainly of fibroblast-type cells that form an adherent monolayer. Most cells in the line are diploid (2n = 32) and have the Apis mellifera karyotype as revealed by Giemsa stain. The partial sequence for the mitochondrial-encoded cytochrome c oxidase subunit I (Cox 1) gene in the cell line is identical to those from honey bee tissues and a consensus sequence for A. mellifera. The population doubling time is approximately 4 days. Importantly, the cell line is continuously subcultured every 10–14 days when split at a 1:3 ratio and is cryopreserved in liquid nitrogen. The cell culture system we have developed has potential application for studies aimed at honey bee development, genetics, pathogenesis, transgenesis, and toxicology.
Climatic limits of tropical African honeybees in the Americas
(International Bee Research Association, 1984) Orley, Taylor R., Jr.; Spivak, Marla
A comparison of honey bee-collected pollen from working agricultural lands using light microscopy and ITS metabarcoding
(Oxford, 2017) Smart, M. D.; Cornman, R. S.; Iwanowicz, D. D.; McDermott-Kubeczko, M.; Pettis, J. S.; Spivak, M. S.; Otto, C.R.V.
Taxonomic identification of pollen has historically been accomplished via light microscopy but requires specialized knowledge and reference collections, particularly when identification to lower taxonomic levels is necessary. Recently, next-generation sequencing technology has been used as a cost-effective alternative for identifying beecollected pollen; however, this novel approach has not been tested on a spatially or temporally robust number of pollen samples. Here, we compare pollen identification results derived from light microscopy and DNA sequencing techniques with samples collected from honey bee colonies embedded within a gradient of intensive agricultural landscapes in the Northern Great Plains throughout the 2010–2011 growing seasons. We demonstrate that at all taxonomic levels, DNA sequencing was able to discern a greater number of taxa, and was particularly useful for the identification of infrequently detected species. Importantly, substantial phenological overlap did occur for commonly detected taxa using either technique, suggesting that DNA sequencing is an appropriate, and enhancing, substitutive technique for accurately capturing the breadth of bee-collected species of pollen present across agricultural landscapes. We also show that honey bees located in high and low intensity agricultural settings forage on dissimilar plants, though with overlap of the most abundantly collected pollen taxa. We highlight practical applications of utilizing sequencing technology, including addressing ecological issues surrounding land use, climate change, importance of taxa relative to abundance, and evaluating the impact of conservation program habitat enhancement efforts.
Do measurements of worker cell size reliably distinguish Africanized from European honey bees (Apis mellifera L.)?
(American Bee Journal, 1992) Spivak, M.; Erickson, E. Jr.
Two experiments were conducted to determine whether the size of the cells in which bees develop affects the size of the cells they subsequently construct. The results indicate that when the size of bees has been modified through the use of foundation with larger or smaller cell bases, bees will construct natural cells of a size consistent with their genetic origin. When 22 Africanized colonies were hived on commercial European foundation, they subsequently constructed · natural cells which were not significantly different in size from those of 66 Africanized colonies hived on all natural comb. Also, eight European colonies reared on noncommercial foundation with small cell bases subsequently constructed natural cells which were significantly larger than the cells from which they emerged. Therefore, averaging the width of 10 linear cells in three diagonal rows on naturally built comb is a relatively reliable and accurate method to distinguish between Africanized and European bees in the field. However, colonies with intermediate cell sizes, which may include some feral European colonies and "hybrids" between Africanized and European colonies, may not be evaluated with certainty.
Effects of neonicotinoid imidacloprid exposure on bumble bee (Hymenoptera: Apidae) queen survival and nest initiation
(Oxford, 2017) Wu-Smart, Judy ; Spivak, Marla
Neonicotinoids are highly toxic to insects and may systemically translocate to nectar and pollen of plants where foraging bees may become exposed. Exposure to neonicotinoids can induce detrimental sublethal effects on individual and colonies of bees and may have long-term impacts, such as impaired foraging, reduced longevity, and reduced brood care or production. Less well-studied are the potential effects on queen bumble bees that may become exposed while foraging in the spring during colony initiation. This study assessed queen survival and nest founding in caged bumble bees [Bombus impatiens (Cresson) (Hymenoptera: Apidae)] after chronic (18-d) dietary exposure of imidacloprid in syrup (1, 5, 10, and 25 ppb) and pollen (0.3, 1.7, 3.3, and 8.3 ppb), paired respectively. Here we show some mortality in queens exposed at all doses even as low as 1 ppb, and, compared with untreated queens, significantly reduced survival of treated queens at the two highest doses. Queens that survived initial imidacloprid exposure commenced nest initiation; however, they exhibited dose-dependent delay in egg-laying and emergence of worker brood. Furthermore, imidacloprid treatment affected other parameters such as nest and queen weight. This study is the first to show direct impacts of imidacloprid at field-relevant levels on individual B. impatiens queen survival and nest founding, indicating that bumble bee queens are particularly sensitive to neonicotinoids when directly exposed. This study also helps focus pesticide risk mitigation efforts and highlights the importance of reducing exposure rates in the early spring when bumble bee queens, and other wild bees are foraging and initiating nests.
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.
Honey production by Africanized and European honey bees in Costa Rica
(Springer, 1989) Spivak, M.; Batra, S.; Segreda, F.; Castro, A.L.; Ramirez, W.
Seventeen colonies of bees were used in a test of honey production in a coffee plantation in Costa Rica. The identities of the colonies were not known at the beginning of the experiment. Behavioral identifications were made in the field as to whether a colony was ’strongly Africanized’, ’strongly European’ or ’intermediate’. The distance spanned by 10 linear worker cells was also measured in the field. Morphometric analyses, conducted independenUy, identified colonies as probably Africanized or probably European. Although the ’intermediate’ category tended to produce more honey, there was no significant difference in honey production between bee types, whether sorted by behavior or morphometrics. There was no significant correlation between initial colony weight or brood area and total amount of honey produced. Appropriate uses of behavioral and morphometric identifications are discussed.
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.
The influence of temperature on cuticular color of honeybee (Apis mellifera L) queens
(Springer, 1993) DeGrandi-Hoffman, G.; Spivak, M.; Martin, J.
Temperatures were monitored around emergency queen cells in queenless honeybee hives to determine the effect of temperature on queen color. Concurrently, sister queens of those reared in the queenless colony were placed in incubators set at 31.1, 32.8, or 34.4 °C for the postcapping interval. Queens from the 34.4 °C incubator were significantly lighter in color than those in the 31.1 °C in all but one trial. Queens that developed in the colony were not significantly different in color rank from those that emerged in the 34.4 °C incubators in any trial, and from the 32.8 or 31.1 °C incubators in most trials. The median color ranks of queens emerging in the colony did not differ throughout the year.
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.
Land use in the Northern Great Plains region of the U.S. influences the survival and productivity of honey bee colonies
(2016) Smart, Matthew D.; Pettis, Jeff S.; Euliss, Ned; Spivak, Marla S.
The Northern Great Plains region of the US annually hosts a large portion of commercially managed U.S. honey bee colonies each summer. Changing land use patterns over the last several decades have contributed to declines in the availability of bee forage across the region, and the future sustainability of the region to support honey bee colonies is unclear. We examined the influence of varying land use on the survivorship and productivity of honey bee colonies located in six apiaries within the Northern Great Plains state of North Dakota, an area of intensive agriculture and high density of beekeeping operations. Land use surrounding the apiaries was quantified over three years, 2010–2012, and survival and productivity of honey bee colonies were determined in response to the amount of bee forage land within a 3.2-km radius of each apiary. The area of uncultivated forage land (including pasture, USDA conservation program fields, fallow land, flowering woody plants, grassland, hay land, and roadside ditches) exerted a positive impact on annual apiary survival and honey production. Taxonomic diversity of bee-collected pollen and pesticide residues contained therein varied seasonally among apiaries, but overall were not correlated to large-scale land use patterns or survival and honey production. The predominant flowering plants utilized by honey bee colonies for pollen were volunteer species present in unmanaged (for honey bees), and often ephemeral, lands; thus placing honey bee colonies in a precarious situation for acquiring forage and nutrients over the entire growing season. We discuss the implications for land management, conservation, and beekeeper site selection in the Northern Great Plains to adequately support honey bee colonies and insure long term security for pollinator-dependent crops across the entire country.
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.

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