Ohad Afik’s research while affiliated with University of Georgia and other places

1. The concept of pollinator niche complementarity maintains that species-rich pollinator communities can provide higher and more stable pollination services than species-poor communities, due to contrasting spatial and/or temporal pollination activity among groups of pollinators. Complementarity has usually been examined in pollinators' patterns of flower visitation or abundance, while largely neglecting the possibility of complementarity in patterns of single-visit contribution to fruit/seed set (pollination efficiency). However, variability in pollination efficiency can greatly affect pollinators' overall pollination services and may therefore contribute an additional, important aspect of complementarity. 2. In the current study, we investigated the existence of pollinator complementarity in both visitation rates and pollination efficiencies. The study was conducted in 43 watermelon fields cultivated for seed consumption in a Mediterranean agro-natural landscape in central Israel. We studied spatiotemporal variation in pollinators' visitation activity, measured by repeated observations and netting, and single-visit pollination efficiency, measured by the fruit and seed set rates of hermaphrodite flowers exposed to a single bee visit. Visitation and pollination efficiency were measured throughout the day and season, within and between fields with contrasting availability of nearby wild plants, and among flowers of different sizes. 3. Pollinator species' visitation rates as well as single-visit fruit set efficiencies, but not seed set efficiencies, exhibited significant spatiotemporal variation that contributed to their complementarity. Pollinators' visit frequencies were affected by surrounding land use, location within field, time throughout the season, and time of day. Pollinators' fruit set efficiencies were affected by ovary size and time of day. 4. Synthesis and applications. Crop pollinators may exhibit complementarity in both their visitation rates and pollination efficiencies, which can promote the overall level and stability of their pollination services. Complementarity in pollination efficiencies suggests further diversity effects on crop yield, and calls for taking into account the variability in pollination efficiency along spatiotemporal scales rather than considering it a constant, species-specific trait. However, some modes of niche complementarity may not necessarily translate into increased pollination services and crop yield; the relevance and limitations of such mechanisms should be considered in light of the specific crop and management system studied.

Background/Question/Methods The concept of pollinator niche complementarity maintains that species-rich pollinator communities can provide higher and more stable pollination services as compared to species-poor communities, due to contrasting spatial and/or temporal pollination activity between groups of pollinators. Complementarity has usually been examined in pollinators' patterns of flower visitation or abundance, while largely neglecting the possibility of complementarity in patterns of single-visit contribution to fruit/seed set (pollination efficiency). However, variability in pollination efficiencies can greatly affect pollinators' overall pollination services and thus their complementarity. In the current study, we investigated the existence of pollinator complementarity in both visitation rates and pollination efficiencies. The study was conducted in a Mediterranean agro-natural landscape in central Israel in 43 watermelon fields cultivated for seed consumption. We studied spatio-temporal variation in pollinators' visitation activity, measured by repeated observations and netting, and pollination efficiency, measured by the fruit and seed set rates of hermaphrodite flowers exposed to a single bee visit. Visitation and pollination efficiency were measured along the day and season, and within and between fields with contrasting availability of nearby wild plants. Results/Conclusions Pollinator species' visitation rates as well as single-visit fruit set efficiencies, but not seed set efficiencies, differed spatiotemporally and exhibited complementary patterns. Pollinators' visit frequencies responded differently to surrounding land use, location within field, time along the season, and time of day. Pollinators' fruit set efficiencies responded differently to time of day and ovary size. Our study generally supports the view that diverse pollinator communities can deliver higher and more stable pollination services through spatiotemporal complementarity in both flower visitation rates and pollination efficiency. Complementarity in pollination efficiencies suggests further potential for diversity effects on crop yield, and calls for taking into account the variability in pollination efficiency along the spatiotemporal scales of the study rather than considering it as a species-specific constant trait. Noteworthy, the existence of niche complementarity does not necessarily translate into increased pollination services and crop yield; rather, the relevance and limitations of such mechanisms should be considered in light of the specific crop and management system.

Various nectar components have a repellent effect on flower visitors, and their adaptive advantages for the plant are not well understood. Persea americana (avocado) is an example of a plant that secretes nectar with repellent components. It was demonstrated that the mineral constituents of this nectar, mainly potassium and phosphate, are concentrated enough to repel honey bees, Apis mellifera, a pollinator often used for commercial avocado pollination. Honey bees, however, are not the natural pollinator of P. americana, a plant native to Central America. In order to understand the role of nectar minerals in plant-pollinator relationships, it is important to focus on the plant's interactions with its natural pollinators. Two species of stingless bees and one species of social wasp, all native to the Yucatan Peninsula, Mexico, part of the natural range of P. americana, were tested for their sensitivity to sugar solutions enriched with potassium and phosphate, and compared with the sensitivity of honey bees. In choice tests between control and mineral-enriched solutions, all three native species were indifferent for mineral concentrations lower than those naturally occurring in P. americana nectar. Repellence was expressed at concentrations near or exceeding natural concentrations. The threshold point at which native pollinators showed repellence to increasing levels of minerals was higher than that detected for honey bees. The results do not support the hypothesis that high mineral content is attractive for native Hymenopteran pollinators; nevertheless, nectar mineral composition may still have a role in regulating flower visitors through different levels of repellency.

In the Report “Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance,” it is possible that some pollinator species were misidentified in lowland coffee, Uganda, one of the 41 studies included in the synthesis. This potential misidentification does not invalidate the analyses, conclusions, or the wider implications of the study. The results are not sensitive to which of the 41 studies are included, because the authors performed several analyses with different subsets of studies, and they all showed similar results. Furthermore, the mixed-effect models allow for individual variation in trends for each study. The results of these analyses depend on the consistency of patterns across all of the 41 studies sampled in 600 fields, and are not influenced to any large extent by a particular pattern occurring in just one study. The main analysis compared the flower visitation rate of honey bees versus all wild insect species combined. This analysis should be largely insensitive to identification concerns because honey bees were readily separable from other species in all studies. Indeed, the analyses performed in the synthesis do not make use of the species names of the wild insects (see database S1).

In most terrestrial ecosystems, nitrogen (N) is the most limiting nutrient for plant growth. Honey bees may help alleviate this limitation because their feces (frass) have high concentration of organic nitrogen that may decompose in soil and provide inorganic N to plants. However, information on soil N processes associated with bee frass is not available. The objectives of this work were to 1) estimate the amount of bee frass produced by a honey bee colony and 2) evaluate nitrogen mineralization and ammonia volatilization from bee frass when surface applied or incorporated into soil. Two cage studies were conducted to estimate the amount of frass produced by a 5000-bee colony, and three laboratory studies were carried out in which bee frass, surface-applied or incorporated into soil, was incubated at 25(o)C for 15 to 45 days. The average rate of bee frass production by a 5,000-bee colony was estimated at 2.27 to 2.69 g N month(-1). Nitrogen mineralization from bee frass during 30 days released 20% of the organic N when bee frass was surface applied and 34% when frass was incorporated into the soil. Volatilized NH3 corresponded to 1% or less of total N. The potential amount of inorganic N released to the soil by a typical colony of 20,000 bees foraging in an area similar to that of the experimental cages (3.24 m(2)) was estimated at 0.62 to 0.74 g N m(-2) month(-1) which may be significant at a community scale in terms of soil microbial activity and plant growth. Thus, the deposition of available N by foraging bees could have adaptive benefits for the plants they visit, a collateral benefit deriving from the primary activity of pollination.

Honeybees Can't Do It Alone The majority of food crops require pollination to set fruit with the honeybee providing a pollination workhorse, with both feral and managed populations an integral component of crop management (see the Perspective by Tylianakis , published online 28 February). Garibaldi et al. (p. 1608 , published online 28 February) now show that wild pollinators are also a vital part of our crop systems. In more than 40 important crops grown worldwide, wild pollinators improved pollination efficiency, increasing fruit set by twice that facilitated by honeybees. Burkle et al. (p. 1611 , published online 28 February) took advantage of one of the most thorough and oldest data sets available on plant-pollinator interaction networks and recollected data on plant-pollinator interactions after more than 120 years of climate change and landscape alteration. The historical data set consists of observations collected by Charles Robertson near Carlinville, Illinois (USA), in the late 1800s on the phenology of plants and their pollinating insects, as well as information about which plants and pollinators interacted with one another. Many sites were revisited in the early 1970s and in 2009 and 2010 to collect similar plant-pollinator data. Pollinator function has declined through time, with bees showing lower visitation rates and lower fidelity to individual plant species.

In modern agriculture, most pollination is done by honeybees, despite the significant potential of wild bees. Reliance on honeybee pollination is problematic due to recent declines, and because of potential harm to surrounding ecosystems. We conducted a two-year survey in central Israel, that included active and passive bee collecting and flower observations, to measure visit frequencies and identify main species of wild bees visiting almond, sunflower and watermelon. We used single-visit fruit set experiments to quantify pollination efficiencies of key visitors and their overall contribution to pollination in comparison with honeybees. Our findings show that honeybees are the main visitor and pollinator of all crops examined. Wild bees contributed 0.7, 7, and 15% of bee visits in almond, sunflower and watermelon, respectively. Lasioglossum malachurum and L. politum were the two main wild bee visitors of sunflower and watermelon. In single-visit experiments, both species successfully pollinated watermelon, but not sunflower. Overall, wild bees´ contribution to pollination was negligible in almond and sunflower, and around 5-15% of the total bee contribution in watermelon. Our results show that the potential for pollination services in diversity-rich areas is not easy to predict; more studies are needed to evaluate such services in different ecosystems.

Intensive activity of honey bees, Apis mellifera L., is essential for high fruit set in avocado, Persea americana Mill., orchards, but even when hives are located inside the orchard, many bees still search for alternative blooms. We tested for a possible genetic component for a preference of avocado bloom relative to competing bloom. The honey from each hive was extracted at the end of the avocado bloom and the concentration of perseitol, a carbohydrate that is unique to avocado, was analyzed as a measure for avocado foraging. During the first year, five bee strains were compared in three different sites in Israel. Significant differences were found between strains in honey perseitol concentrations, suggesting differences in their efficiency as avocado pollinators, although these differences were site dependent. At two sites, colonies with the highest and lowest perseitol concentrations were selected as parental "high" and "low" lines. Queens were raised from the selected colonies and were instrumentally inseminated by drones from other colonies of this line. During the second and third years, colonies with inseminated queens were introduced to the avocado orchards, together with the selected colonies still surviving from the previous year. Colonies of the high line had greater perseitol concentrations than those of the low line. Selected colonies that survived from the previous year performed consistently vis-à-vis perseitol concentration, in the second year of testing. Heritability value of 0.22 was estimated based on regression of offspring on midparent. The results reveal a heritable component for willingness of honey bees to collect avocado nectar.

The effects of nicotine on honey bees were tested as a model system to understand possible roles of secondary compounds in floral nectar. Eight honey bee colonies were tested for their preference among six feeders containing all the combinations between two sugar concentrations (20% or 50%) and three nicotine concentrations (0, 5 or 50 ppm). Individual bees from these colonies were tested for the effect of nicotine on learning performance using the proboscis extension response paradigm. Afterwards, half of the tested colonies were fed for three weeks with pure sucrose solution and the rest were fed with sucrose solution enriched with nicotine. Then the bees were tested again for preference and learning. In addition, harnessed bees were tested for their daily food consumption and survival while being fed with sucrose solution with various nicotine concentrations. We found that nicotine repelled bees, but repellency was partially overcome by increased sugar concentration and that early exposure to nicotine may decrease its repellency. Nicotine added to reward did not affect learning performance and survival, but at high concentration it decreased food consumption. We concluded that nicotine concentration in the range that naturally occurs in nectar repels bees. Higher concentrations are more repellent and reduce consumption. Interestingly, prolonged exposure to nicotine resulted in habituation to nicotine. Thus, nicotine in floral nectar may serve as a repellent for occasional visitors, but less so to regular visitors, which would be more efficient pollinators.