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The Department of Entomology
The Robert H. Smith Faculty of Agriculture, Food and Environment
The Hebrew University of Jerusalem
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Skaliter, O. ; Kitsberg, Y. ; Sharon, E. ; Shklarman, E. ; Shor, E. ; Masci, T. ; Yue, Y. ; Arien, Y. ; Tabach, Y. ; Shafir, S. ; et al. Spatial patterning of scent in petunia corolla is discriminated by bees and involves the ABCG1 transporter. PLANT JOURNAL 2021, 106, 1746-1758.Abstract
Floral guides are patterned cues that direct the pollinator to the plant reproductive organs. The spatial distribution of showy visual and olfactory traits allows efficient plant-pollinator interactions. Data on the mechanisms underlying floral volatile patterns or their interactions with pollinators are lacking. Here we characterize the spatial emission patterns of volatiles from the corolla of the model plant Petunia x hybrida and reveal the ability of honeybees to distinguish these patterns. Along the adaxial epidermis, in correlation with cell density, the petal base adjacent to reproductive organs emitted significantly higher levels of volatiles than the distal petal rim. Volatile emission could also be differentiated between the two epidermal surfaces: emission from the adaxial side was significantly higher than that from the abaxial side. Similar emission patterns were also observed in other petunias, Dianthus caryophyllus (carnation) and Argyranthemum frutescens (Marguerite daisy). Analyses of transcripts involved in volatile production/emission revealed lower levels of the plasma-membrane transporter ABCG1 in the abaxial versus adaxial epidermis. Transient overexpression of ABCG1 enhanced emission from the abaxial epidermis to the level of the adaxial epidermis, suggesting its involvement in spatial emission patterns in the epidermal layers. Proboscis extension response experiments showed that differences in emission levels along the adaxial epidermis, that is, petal base versus rim, detected by GC-MS are also discernible by honeybees.
Arien, Y. ; Dag, A. ; Yona, S. ; Tietel, Z. ; Lapidot Cohen, T. ; Shafir, S. Effect of diet lipids and omega-6:3 ratio on honey bee brood development, adult survival and body composition. JOURNAL OF INSECT PHYSIOLOGY 2020, 124.Abstract
Lipids have a key role in a variety of physiological functions in insects including energy, reproduction, growth and development. Whereas most of the required fatty acids can be synthesized endogenously, omega-3 and omega-6 polyunsaturated fatty acids (PUFA) are essential fatty acids that must be acquired through nutrition. Honey bees (Apis mellifera) obtain lipids from pollen, but different pollens vary in nutritional composition, including of PUFAs. Low floral diversity and abundance may expose bees to nutritional stress. We tested the effect of total lipids concentration and their omega-6:3 ratio on aspects of honey bee physiology: brood development, adult longevity and body fatty acids composition. All three parameters were affected by dietary lipid concentration and omega-6:3 ratio. Higher lipid concentration in diet increased brood production, and high omega-6:3 ratio increased mortality rate and decreased brood rearing. Fatty acid analysis of the bees showed that the amount of lipids and the omega-6:3 ratio in their body generally reflected the composition of the diet on which they fed. Consistent with previous findings of the importance of a balanced omega-6:3 ratio diet for learning performance, we found that such a balanced PUFA diet, with above threshold total lipid composition, is also necessary for maintaining proper colony development.
Barazani, O. ; Erez, T. ; Ogran, A. ; Hanin, N. ; Barzilai, M. ; Dag, A. ; Shafir, S. Natural Variation in Flower Color and Scent in Populations of Eruca sativa (Brassicaceae) Affects Pollination Behavior of Honey Bees. Journal of Insect Science 2019, 19. Publisher's VersionAbstract
Plants of Eruca sativa Mill. (Brassicaceae) from desert and Mediterranean populations in Israel differ in flower color and size. In the desert habitat, the population has higher abundance of flowers with cream color and longer petals, whereas in the Mediterranean habitat, the population has higher abundance of flowers with yellow and shorter petals. Choice experiments with honey bee foragers (Apis mellifera Linn., Apidae, Hymenoptera), the main pollinator in the natural habitat in Israel, confirmed that they are more attracted to the yellow flower morph than to the cream one. A proboscis extension response test indicated that honey bees are able to discriminate between flower scents of the desert and Mediterranean populations. Considering the advantage of plants of the yellow morph in attracting pollinators, we further tested in a common garden experiment whether these possess higher fitness than plants of the desert population. Indeed, a significant association was found between flower color and fruit set, and seed mass. In general, our results provide evidence for ecotypic differentiation between populations imposed by pollinators. The advantage of the yellow color morph in attracting pollinators may explain its dominance among plants of the Mediterranean population. We discuss why the cream color morph may be dominant in the desert habitat, considering the possibility of different pollinators, tradeoffs between traits, or pleiotropy. © 2019 The Author(s).
Hendriksma, H. P. ; Toth, A. L. ; Shafir, S. Individual and Colony Level Foraging Decisions of Bumble Bees and Honey Bees in Relation to Balancing of Nutrient Needs. Frontiers in Ecology and Evolution 2019, 7 177. Publisher's VersionAbstract
Foraging decisions of social animals occur in the context of social groups, and thus may be subject to considerations of not only an individual's nutritional state and nutrient input, but those of the social group in which they live. In eusocial insects, which live in colonies containing workers that forage for food that is mostly consumed by others, foraging decisions that reflect colony needs may also be considered at both the colony and individual level. If colony energy balance is perturbed, is the counteracting response occurring on the group level (a change in division of labor) or on the individual level (a change in individual foraging choices)? To address this, colony and individual level foraging behaviors were observed in two species of eusocial bees: the highly social honey bee Apis mellifera and the primitively eusocial bumble bee Bombus terrestris. After manipulations of protein (P) and carbohydrate (C) stores in colonies of both species, there were changes in multiple different behavioral responses including colony level (number of foragers, allocation to nectar and pollen foraging, nutrient mass foraged) and individual level (P and C concentration preference and loading during foraging). These results suggest both honey bee and bumble bee colonies balance nutrient needs through a combination of both colony level shifts in foraging allocation, as well as slight modulation of individual nutrient preferences. This study also uncovered colony level differences between the two bee species; honey bees balanced P intake while bumble bees balanced C intake. These patterns may reflect differences in life history traits such as perenniality and hoarding, traits that are developed in more highly social species. Overall, this study highlights the importance of considering both group and individual level behavioral responses in foraging decisions in social animals.
Maori, E. ; Garbian, Y. ; Kunik, V. ; Mozes-Koch, R. ; Malka, O. ; Kalev, H. ; Sabath, N. ; Sela, I. ; Shafir, S. A Transmissible RNA Pathway in Honey Bees. Cell Rep 2019, 27, 1949-1959.e6.Abstract
Systemic RNAi, initiated by double-stranded RNA (dsRNA) ingestion, has been reported in diverse invertebrates, including honey bees, demonstrating environmental RNA uptake that undermines homologous gene expression. However, the question why any organism would take up RNA from the environment has remained largely unanswered. Here, we report on horizontal RNA flow among honey bees mediated by secretion and ingestion of worker and royal jelly diets. We demonstrate that transmission of jelly-secreted dsRNA to larvae is biologically active and triggers gene knockdown that lasts into adulthood. Worker and royal jellies harbor differential naturally occurring RNA populations. Jelly RNAs corresponded to honey bee protein-coding genes, transposable elements, and non-coding RNA, as well as bacteria, fungi, and viruses. These results reveal an inherent property of honey bees to share RNA among individuals and generations. Our findings suggest a transmissible RNA pathway, playing a role in social immunity and signaling between members of the hive.
Wright, G. A. ; Nicolson, S. W. ; Shafir, S. Nutritional Physiology and Ecology of Honey Bees. Annu Rev Entomol 2018, 63, 327-344.Abstract
Honey bees feed on floral nectar and pollen that they store in their colonies as honey and bee bread. Social division of labor enables the collection of stores of food that are consumed by within-hive bees that convert stored pollen and honey into royal jelly. Royal jelly and other glandular secretions are the primary food of growing larvae and of the queen but are also fed to other colony members. Research clearly shows that bees regulate their intake, like other animals, around specific proportions of macronutrients. This form of regulation is done as individuals and at the colony level by foragers.
Arien, Y. ; Dag, A. ; Shafir, S. Omega-6:3 Ratio More Than Absolute Lipid Level in Diet Affects Associative Learning in Honey Bees. Frontiers in Psychology 2018, 9 1001. Publisher's VersionAbstract
Floral pollen is a major source of honey bee nutrition that provides them with micro- and macro-nutrients, including proteins, fatty acids, vitamins, and minerals. Different pollens vary in composition, including in the essential fatty acids, alpha-linolenic acid (omega-3) and linoleic acid (omega-6). Monocultures, prevalent in modern agriculture, may expose honey bee colonies to unbalanced omega-6:3 diets. The importance of omega-3 in the diet for adequate learning and cognitive function, with a focus on suitable omega-6:3 ratio, is well documented in mammals. We have recently shown, for the first time in invertebrates, the importance of omega-3 in diets for associative learning ability in honey bees. In the current work, we examine the effect of the absolute amount of omega-3 in diet compared to the omega-6:3 ratio on honey bee associative learning. We fed newly emerged bees for 1 week on different artificial diets, which had lipid concentration of 1, 2, 4, or 8%, with omega-6:3 ratios of 0.3, 1, or 5, respectively. We then tested the bees in a proboscis-extension response olfactory conditioning assay. We found that both omega-6:3 ratio and total lipid concentration affected learning. The most detrimental diet for learning was that with a high omega-6:3 ratio of 5, regardless of the absolute amount of omega-3 in the diet. Bees fed an omega-6:3 ratio of 1, with 4% total lipid concentration achieved the best performance. Our results with honey bees are consistent with those found in mammals. Best cognitive performance is achieved by a diet that is sufficiently rich in essential fatty acids, but as long as the omega-6:3 ratio is not high.
Topman, S. ; Tamir-Ariel, D. ; Bochnic-Tamir, H. ; Stern Bauer, T. ; Shafir, S. ; Burdman, S. ; Hayouka, Z. Random peptide mixtures as new crop protection agents. Microbial Biotechnology 2018, 11, 1027-1036. Publisher's VersionAbstract
Summary Many types of crops are severely affected by at least one important bacterial disease. Chemical control of bacterial plant diseases in the field vastly relies on copper-based bactericides, yet with limited efficacy. In this study, we explored the potential of two random peptide mixture (RPM) models as novel crop protection agents. These unique peptide mixtures consist of random combination of l-phenylalanine and l- or d-lysine (FK-20 and FdK-20, respectively) along the 20 mer chain length of the peptides. Both RPMs displayed powerful bacteriostatic and bactericidal activities towards strains belonging to several plant pathogenic bacterial genera, for example, Xanthomonas, Clavibacter and Pseudomonas. In planta studies in the glasshouse revealed that RPMs significantly reduced disease severity of tomato and kohlrabi plants infected with Xanthomonas perforans and Xanthomonas campestris pv. campestris respectively. Moreover, RPM effects on reduction in disease severity were similar to those exerted by the commercial copper-based bactericide Kocide 2000 that was applied at a 12-fold higher concentration of the active compound relative to the RPM treatments. Importantly, the two tested RPM compounds had no toxic effect on survival of bees and Caco-2 mammalian cells. This study demonstrates the potential of these innovative RPMs to serve as crop protection agents against crop diseases caused by phytopathogenic bacteria.
Zarchin, S. ; Dag, A. ; Salomon, M. ; Hendriksma, H. P. ; Shafir, S. Honey bees dance faster for pollen that complements colony essential fatty acid deficiency. Behavioral Ecology and Sociobiology 2017, 71, 172. Publisher's VersionAbstract
Honey bee colonies require adequate pollen for maintenance and growth. Pollens vary in nutritional value, and a balanced diet is achieved by mixing pollens with complementary essential nutrients. We tested subjective evaluation of pollens by foragers in colonies deprived of one of two essential fatty acids (eFAs), alpha-linolenic acid (omega-3) or linoleic acid (omega-6). We used four pollens, two rich in omega-3 and two rich in omega-6. A colony in an observation hive was allowed to forage for 2–5 days on a single pollen source. The following day, we repeatedly presented one of three pollens: the same pollen that the bees had been collecting the previous days, a novel pollen that was similarly deficient in omega-3 or omega-6, and a novel pollen that complemented their eFA deficiency. We measured the rate of waggle dances, which reflects on the strength of recruitment effort, of foragers returning to the observation hive from each of the pollens. Dance rates did not differ between the four pollens, but they were the highest to the ``complementary'' pollen and the lowest to the ``same'' pollen. Furthermore, this effect was greater for pollen combinations with greater eFA disparity between the same and the complementary pollens. Our findings support the ability of bees to balance colony eFA intake. Conditioning of the proboscis extension response (PER) tests showed that pollen foragers discriminated well between the four pollen odors, but the mechanisms by which bees assess pollen eFA composition remain to be elucidated. Differential dancing would recruit foragers to pollens that balance colony nutritional needs.
Sapir, G. ; Baras, Z. ; Azmon, G. ; Goldway, M. ; Shafir, S. ; Allouche, A. ; STERN, E. ; Stern, R. A. Synergistic effects between bumblebees and honey bees in apple orchards increase cross pollination, seed number and fruit size. Scientia Horticulturae 2017, 219, 107 - 117. Publisher's VersionAbstract
Most apple cultivars are self-sterile and completely dependent on cross-pollination from a different cultivar in order to set fruit. Various insects may be pollinators, but the main one is the honey bee [HB] (Apis mellifera). However, despite the advantages of the honey bee as pollinator of many plants, it is a relatively inefficient pollinator of apple flowers. The main reason for this is the tendency of HBs to visit the apple flower from the side (sideworker), thus “stealing” nectar without touching the flower’s reproductive organs – stamens and stigma. In contrast, a bee that visits the flower from the top (topworker) contacts the flower’s reproductive organs, which results in better pollination. Due to the low pollination efficiency, few seeds are formed, and often the resulting fruit is too small to be of commercial value. Experiments conducted in Israel over the last few years have shown for the first time that adding bumblebees [BB] (Bombus terrestris) into pear orchards improved cross-pollination, thus increasing the number of seeds and subsequently fruit size. The goal of the present work was to test the hypothesis that adding BBs to apple orchards may improve cross-pollination. We found that adding BBs to the HBs in the apple orchard improved pollination in all tested cultivars, especially in ‘Gala’, which naturally suffers from relatively few seeds in the fruit. It appears that the addition of BBs did not only increase the number of pollinating insects in the orchard that could perform cross-pollination, including in the cool mornings and in adverse weather conditions, but that it also changed HB foraging behavior, which resulted in improved cross-pollination and increased efficiency, and subsequently more seeds and larger fruit. The improved pollination was due to the greater mobility of HBs between rows of pollinated cultivar and pollenizer, and to the greater proportion of topworkers, which are more efficient pollinators.
Hendriksma, H. P. ; Shafir, S. Honey bee foragers balance colony nutritional deficiencies. 2016, 70, 509 - 517. Publisher's VersionAbstract
Honey bee colonies, foraging predominantly on a single pollen source, may encounter nutritional deficits. In the present study, we examined the nutritional resilience of honey bee colonies, testing whether foragers shift their foraging effort towards resources that complement a nutritional deficit. Eight honey bee colonies were kept in screened enclosures and fed for 1 week a pollen substitute diet deficient in a particular essential amino acid. Foragers were subsequently tested for a preference between the same diet previously fed, a different diet that was similarly deficient, or a diet that complemented the deficiency. Foragers preferred the complementary diet over the same or similar diets. Appetitive conditioning tests showed that bees were able to discriminate also between the same and similar diets. Overall, our results support the hypothesis that honey bees prefer dietary diversity, and that they do not just include novel sources but specifically target nutritionally complementary ones. Whereas we specifically focused on deficiencies in essential amino acids, we cannot rule out that bees were also complementing correlated imbalances in other nutrients, most notably essential fatty acids. The ability of honey bees to counter deficient nutrition contributes to the mechanisms which social insects use to sustain homeostasis at the colony level.