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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.
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.
Standard methods for Apis mellifera propolis research
(Taylor and Francis, 2016) Bankova, Vassya; Bertelli, Davide; Borba, Renata; Conti, Bruno José; Barbosa da Silva Cunha, Ildenize; Danert, Carolina; Eberlin, Marcos Nogueira; Falcão, Soraia I; Isla, María Inés; Nieva Moreno, María Inés; Papotti, Giulia; Popova, Milena; Santiago, Karina Basso; Salas, Ana; Sawaya, Alexandra Christine Helena Frankland; Schwab, Nicolas Vilczaki; Sforcin, José Maurício; Simone-Finstrom, Michael; Spivak, Marla; Trusheva, Boryana; Vilas-Boas, Miguel; Wilson, Michael; Zampini, Catiana
Propolis is one of the most fascinating honey bee (Apis mellifera L.) products. It is a plant derived product that bees produce from resins that they collect from different plant organs and with which they mix beeswax. Propolis is a building material and a protective agent in the bee hive. It also plays an important role in honey bee social immunity, and is widely used by humans as an ingredient of nutraceuticals, over-the-counter preparations and cosmetics. Its chemical composition varies by geographic location, climatic zone and local flora. The understanding of the chemical diversity of propolis is very important in propolis research. In this manuscript, we give an overview of the available methods for studying propolis in different aspects: propolis in the bee colony; chemical composition and plant sources of propolis; biological activity of propolis with respect to bees and humans; and approaches for standardization and quality control for the purposes of industrial application.
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.
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.
Propolis envelope in Apis mellifera colonies supports honey bees against the pathogen, Paenibacillus larvae
(Nature Publishing Group, 2017) Borba, Renata S.; Spivak, Marla
Honey bees have immune defenses both as individuals and as a colony (e.g., individual and social immunity). One form of honey bee social immunity is the collection of antimicrobial plant resins and the deposition of the resins as a propolis envelope within the nest. In this study, we tested the efects of the propolis envelope as a natural defense against Paenibacillus larvae, the causative agent of American foulbrood (AFB) disease. Using colonies with and without a propolis envelope, we quantifed: 1) the antimicrobial activity of larval food fed to 1–2day old larvae; and 2) clinical signs of AFB. Our results show that the antimicrobial activity of larval food was signifcantly higher when challenged colonies had a propolis envelope compared to colonies without the envelope. In addition, colonies with a propolis envelope had signifcantly reduced levels of AFB clinical signs two months following challenge. Our results indicate that the propolis envelope serves as an antimicrobial layer around the colony that helps protect the brood from bacterial pathogen infection, resulting in a lower colony-level infection load.
Why does bee health matter? The science surrounding honey bee health concerns and what we can do about it
(CAST Council for Agricultural Science and Technology, 2017) Spivak, Marla; Browning, Zac; Goblirsch, Mike; Lee, Katie; Otto, Clint; Smart, Matthew; Wu-Smart, Judy
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.
Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development
(2016) Wu-Smart, Judy; Spivak, Marla
Many factors can negatively affect honey bee (Apis mellifera L.) health including the pervasive use of systemic neonicotinoid insecticides. Through direct consumption of contaminated nectar and pollen from treated plants, neonicotinoids can affect foraging, learning, and memory in worker bees. Less well studied are the potential effects of neonicotinoids on queen bees, which may be exposed indirectly through trophallaxis, or food-sharing. To assess effects on queen productivity, small colonies of different sizes (1500, 3000, and 7000 bees) were fed imidacloprid (0, 10, 20, 50, and 100 ppb) in syrup for three weeks. We found adverse effects of imidacloprid on queens (egg-laying and locomotor activity), worker bees (foraging and hygienic activities), and colony development (brood production and pollen stores) in all treated colonies. Some effects were less evident as colony size increased, suggesting that larger colony populations may act as a buffer to pesticide exposure. This study is the first to show adverse effects of imidacloprid on queen bee fecundity and behavior and improves our understanding of how neonicotinoids may impair short-term colony functioning. These data indicate that risk-mitigation efforts should focus on reducing neonicotinoid exposure in the early spring when colonies are smallest and queens are most vulnerable to exposure.
Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.)
(2001) Masterman, R.; Ross, R.; Mesce, K.; Spivak, M.
Through the use of proboscis-extension reflex conditioning, we demonstrate that honey bees ( Apis mellifera L.) bred for hygienic behavior (a behavioral mechanism of disease resistance) are able to discriminate between odors of healthy and diseased brood at a lower stimulus level than bees from a non-hygienic line. Electroantennogram recordings confirmed that hygienic bees exhibit increased olfactory sensitivity to low concentrations of the odor of chalkbrood infected pupae (a fungal disease caused by Ascosphaera apis ). Three-week-old hygienic bees were able to discriminate between the brood odors significantly better than three-week old non-hygienic bees. However, the differential performance in brood odor discrimination was primarily genetically based, not a direct result of age, experience, or the temporary behavioral state of the bee. Lower stimulus thresholds for both the olfactory and behavioral responses of hygienic bees may facilitate their ability to detect, uncap and remove diseased brood rapidly from the nest. In contrast, non-hygienic bees, possessing higher response thresholds, may not be able to detect diseased brood as easily. Our results provide an example of how physiological and behavioral differences between the hygienic and non-hygienic honey bee lines, operating at the level of the individual, could produce colony-specific behavioral phenotypes.
The relationship between hygienic behavior and suppression of mite reproduction as honey bee (Apis mellifera) mechanisms of resistance to Varroa destructor
(2006) Ibrahim, Abdullah; Spivak, Marla
We compared the mechanisms of resistance to Varroa destructor displayed by bees bred for Suppression of Mite Reproduction (SMR) and hygienic behavior (HYG). Mites from SMR and HYG source colonies were introduced into recently sealed SMR and HYG worker brood, and the infested pupae were placed either into recipient colonies or into an incubator. SMR colonies removed significantly more miteinfested pupae than the HYG colonies. The reproductive success (fertility and number of viable female offspring) of mites from both sources on pupae not removed by bees was significantly lower in SMR colonies. Within the incubator, the reproductive success of mites was also lower on SMR worker pupae, and lowest when mites from SMR colonies were introduced on SMR brood. Our findings indicated that bees bred for SMR express hygienic behavior; adult bees selectively remove pupae infested with mites. In addition, there is an effect of SMR pupae that reduces mite reproductive success that requires further investigation.
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.
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.
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.
A national survey of managed honey bee 2013–2014 annual colony losses in the USA
(2015) Lee, Kathleen V.; Steinhauer, Nathalie; Rennich, Karen; Wilson, Michael E.; Tarpy, David R.; Caron, Dewey M.; Rose, Robyn; Delaplane, Keith S.; Baylis, Kathy; Lengerich, Eugene J.; Pettis, Jeff; Skinner, John A.; Wilkes, James T.; Sagili, Ramesh; vanEngelsdorp, Dennis
Honey bee colony losses are a major concern in the USA and across the globe. Long-term data on losses are critical for putting yearly losses in context. US colony loss surveys have been conducted yearly since the winter of 2006–2007. Here, we report the results from the eighth annual survey on winter losses and the second annual survey of summer and annual losses. There were 7425 valid respondents (7123 backyard, 190 sideline, and 112 commercial beekeepers) managing 497,855 colonies, 19 % of the total US colonies. Total losses reported were 19.8 % [95 % CI 19.3–20.3 %] over the summer, 23.7 % [95 % CI 23.3–24.1 %] over the winter, and 34.1 % [95 % CI 33.6–34.6 %] for the whole year. Average losses were 15.1 % [95 % CI 14.5–15.7 %] over the summer, 44.8 % [95 % CI 43.9–45.7 %] over the winter, and 51.1 % [95 % CI 50.2–51.6 %] for the whole year. While total winter loss was one of the lowest reported in 8 years, 66 % of all beekeepers had higher losses than they deemed acceptable.
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.
Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior
(2001) Spivak, Marla; Reuter, Gary S.
Honey bee colonies, selected for hygienic behavior on the basis of a freeze-killed brood assay, demonstrated resistance to American foulbrood disease. Over two summers in 1998 and 1999, 18 hygienic and 18 non-hygienic colonies containing instrumentally inseminated queens were challenged with comb sections containing spores of the bacterium Paenibacillus larvae subsp. larvae that causes the disease. The strain of bacterium was demonstrated to be resistant to oxytetracycline antibiotic. Seven (39%) hygienic colonies developed clinical symptoms of the disease but five of these recovered (had no visible symptoms) leaving two colonies (11%) with clinical symptoms. In contrast, 100% of the non-hygienic colonies that were challenged developed clinical symptoms, and only one recovered. All non-hygienic colonies had symptoms of naturally occurring chalkbrood disease (Ascosphaera apis) throughout both summers. In contrast 33% of the hygienic colonies developed clinical symptoms of chalkbrood after they were challenged with American foulbrood, but all recovered. The diseased non-hygienic colonies produced significantly less honey than the hygienic colonies.
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.
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.
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.