Honeybees are celebrated as effective plant pollinators, but just how effective are they? 

Newly published UC Davis research in the American Journal of Botany yields some surprising results.

Honeybees are effective pollinators, but when compared to other pollinators, including wild bees, they are rarely the most effective plant pollinators, according to a meta-analysis project led by doctoral candidate Maureen Page and postdoctoral researcher Charlie Casey Nicholson of the Neal Williams laboratory, UC Davis Department of Entomology and Nematology.   

Page and Nicholson are the co-leading authors of "A Meta-Analysis of Single Visit Pollination Effectiveness Comparing Honeybees and other Floral Visitors," the cover story of the current edition of the journal, published Nov. 30.  

“Although high visitation frequencies make honeybees important pollinators, they were rarely the most effective pollinators of plants and were less effective than the average bee,” said Page.  “This suggests that honeybees may be imperfect substitutes for the loss of wild pollinators and ensuring pollination will benefit from conservation of non-honeybee taxa. In the future, we hope other researchers will use the data we have collected to further investigate the factors that influence pollination effectiveness.” 

Page and Nicholson originated the idea for the project during a graduate seminar led by UC Davis professor and community ecologist Louie Yang in the winter of 2020. While the COVID-19 pandemic shut down or postponed many other research projects, Page and Nicholson forged ahead and organized fellow graduate students and postdoctoral students to collectively read and extract single visit-effectiveness data from more than 468 papers. The two then analyzed the data from a subset of these papers (168) to ask whether honeybees and other floral visitors differed in their single visit pollination effectiveness. 

Page and Nicholson began with the premise: “Many animals provide ecosystem services in the form of pollination including honeybees, which have become globally dominant floral visitors. A rich literature documents considerable variation in single visit pollination effectiveness, but this literature has yet to be extensively synthesized to address whether honeybees are effective pollinators,”

The researchers conducted a hierarchical meta-analysis of 168 studies and extracted 1564 single visit effectiveness (SVE) measures for 240 plant species. “We paired SVE data with visitation frequency data for 69 of these studies,” they wrote. “We used these data to ask three questions: (1) Do honeybees (Apis mellifera) and other floral visitors differ in their SVE? (2) To what extent do plant and pollinator attributes predict differences in SVE between honeybees and other visitors? (3) Is there a correlation between visitation frequency and SVE?”

They compared honeybees to multiple pollinator groups, including ants, bees, beetles, birds, butterflies, flies, moths, and wasps. 

"Surprisingly, honeybees were less effective than other bees as pollinators of crop plants, suggesting that the importance of honeybees as crop pollinators derives largely from their numerical abundance rather than the quality of their floral visits," Page said. 

Results. “Honeybees were significantly less effective than the most effective non-honeybee pollinators but were as effective as the average pollinator," they wrote in their results section of the paper. "The type of pollinator moderated these effects. Honeybees were less effective compared to the most effective and average bird and bee pollinators but were as effective as other taxa. Visitation frequency and SVE were positively correlated, but this trend was largely driven by data from communities where honeybees were absent.”

The researchers concluded that “Although high visitation frequencies make honeybees important pollinators, they were less effective than the average bee and rarely the most effective pollinator of the plants they visit. As such, honeybees may be imperfect substitutes for the loss of wild pollinators, and safeguarding pollination will benefit from conservation of non-honeybee taxa.”

Also contributing to the project were Ross Brennan, Anna Britzman, Jessica Greer, Jeremy Hemberger, Hanna Kahl, Uta Müller, Youhong Peng, Nick Rosenberger, Clara Stuligross, Li Wang, and Professors Louie Yang and Neal Williams.

Cover Photo. The cover photo, by Kathy Keatley Garvey, communications specialist, UC Davis Department of Entomology and Nematology, shows several species of bees on a sunflower, Helianthus sp. They include a honeybee  (Apis mellifera), sunflower bee (Svastra obliqua), and two sweat bees (Halictus tripartitus and Halictus ligatus), as identified by Professor Williams, a pollinator ecologist.

"Honeybees are as effective as the average pollinator, but rarely the most effective pollinators of plants," according to the caption. "Surprisingly, honeybees are less effective than other bees as pollinators of cultivated plants, suggesting the importance of honeybees as agricultural pollinators derives largely from their numerical abundance. Their study confirms a widely held belief that honeybees are not the best pollinators of plants globally and substantiates the growing concern that honeybees may be imperfect substitutes for the loss of wild pollinators."

Charlie Nicholson. Nicholson, a researcher in the UC Davis Department of Entomology and Nematology labs of both Professor Neal Williams, and Extension apiculturist Elina Lastro Niño,  holds a bachelor of arts degree in biology (evolution, ecology and behavior), 2010, cum laude,  from Skidmore College, Saratoga Springs, New York. He received his doctorate in natural resources in 2018 from the University of Vermont, where he was a Gund Institute for Environment graduate fellow. In his dissertation, he examined how landscape and farm management affect the multiple benefits provided by wild bees. 

Nicholson joined UC Davis as a postdoctoral scholar in the spring of 2019, and receives funding support from the USDA Invasive Species and Pollinator Health Unit. He recently co-authored a paper, “Natural Hazard Threats to Pollinators and Pollination,” published in the journal Global Change Biology, that analyzed 117 published research papers on natural hazards that threaten pollinators and pollination.

Maureen Page. Page received her bachelor's degree in biology, cum laude, from Scripps College, Claremont, Calif., in 2016, and then enrolled in the UC Davis entomology graduate program, with a career goal of becoming a professor and principal investigator. In 2018, she received prestigious three-year fellowship, a National Defense Science and Engineering Graduate Fellowship, for her research proposal, “Promoting Food Security by Optimizing Wildflower Plantings to Support Wild and Managed Bees." Long interested in bee research, Page received a 2013 Scripps Environmental Research Grant to establish a solitary bee monitoring program at the Bernard Field Station in Claremont. She created a reference collection and species list of bee diversity at the field station, gaining experience collecting, pinning and identifying bee specimens. She presented her findings at the Scripps Undergraduate Research Symposium. Page later worked on a project categorizing pollen deposition by the yellow-faced bumble bee, Bombus vosnesenkii to California figwort, Scrophularia california.

A newly published, two-year UC Davis study reveals that normal exposure to the insecticide imidacloprid generates a multi-generational effect on the blue orchard bee, Osmia lignaria, reducing both reproduction and population growth.

The research, "Past Insecticide Exposure Reduces Bee Reproduction and Population Growth," by doctoral ecology candidate Clara Stuligross and her co-author, major professor Neal Williams of the UC Davis Department of Entomology and Nematology, is published in the current edition of the Proceedings of the National Academy of Sciences.

The blue orchard bee, sometimes nicknamed BOB, is a native bee active in the early spring. Metallic blue in color and smaller than a honey bee, it is a solitary mason bee often managed commercially to pollinate almond orchards. The bees are also considered excellent pollinators of apple, pear and cherry trees and efficient pollinators of blueberries.  

“We reveal that pesticide exposure, both directly to foraging bees and via carryover effects from past exposure, dramatically reduced bee reproduction, which reduced population growth,” they wrote. “Carryover effects reduced bee reproduction by 20% beyond current impacts on foraging bees, exacerbating the negative impact on population growth rates. This indicates that bees may require multiple generations to recover from a single pesticide exposure; thus, carryover effects must be considered in risk assessment and conservation management.” 

Stuligross and Williams pointed out that “Pesticides are linked to global insect declines, with impacts on biodiversity and essential ecosystem services. In addition to well-documented direct impacts of pesticides at the current stage or time, potential delayed ‘carryover' effects from past exposure at a different life stage may augment impacts on individuals and populations.” 

The scientists investigated the effects of current exposure and the carryover effects of past insecticide exposure on the individual vital rates and population growth of the bee.  “Bees in flight cages freely foraged on wildflowers, some treated with the common insecticide, imidacloprid, in a fully crossed design over two years, with insecticide exposure or no exposure in each year,” they wrote. 

They found that “insecticide exposure directly to foraging adults and via carryover effects from past exposure reduced reproduction. Repeated exposure across two years  additively impaired individual performance, leading to a nearly fourfold reduction in bee population growth.” 

“Exposure to even a single insecticide application can have persistent effects on vital rates and can reduce population growth for multiple generations,” they wrote. “Carryover effects had profound implications for population persistence and must be considered in risk assessment, conservation, and management decisions for pollinators to mitigate the effects of insecticide exposure. 

The 2018-2019 study took place on the grounds of the Harry H. Laidlaw Jr. Honey Bee Research Facility, located west of the central UC Davis campus.

The researchers tested only imidacloprid, a commonly used pesticide related to nicotine, and in exposures that bees would normally encounter in an agricultural field or orchard. The bees visited three species of wildflowers: lacy phacelia (Phacelia tanacetifolia), great valley phacelia (Phacelia ciliata), and purple Chinese houses (Collinsia heterophylla).

Any other adverse effects of the pesticide exposure?  “We also saw effects of current pesticide exposure on offspring sex ratio, probability of nest initiation, and nest construction rate,” Stuligross said.  

The study drew financial support from Stuligross' National Science Foundation Graduate Research Fellowship; her UC Davis Henry A. Jastro Graduate Research Award, and her UC Davis Ecology Graduate Research Fellowship, as well as from the UC Davis Department of Entomology and Nematology through the Harry H. Laidlaw Jr. Bee Research Facility and the Laidlaw Endowment.

The next step? “We are interested in studying how this type of pesticide exposure affects bees in a full field setting, where bees are exposed to multiple stressors simultaneously," she said. 

Unlike honey bees, the reproductive rate of the blue orchard bee is low. A queen honey bee can lay about 2000 eggs a day in peak season, while the female blue orchard bee lays about 15 eggs a year.

Stuligross, who began her doctoral studies at UC Davis in 2016, holds a bachelor's degree in environmental studies (2014) from Earlham College, Richmond, Ind.  “I am broadly interested in bee biology, population ecology, and understanding how bees interact with their environments in natural and managed ecosystems,” she says. “I use a combination of landscape, field cage, and lab experiments to study these interactions at different scales.”

Stuligross previously worked as a science educator at Carnegie Museum of Natural History, a research technician with Rufus Isaacs at Michigan State University studying bee communities in blueberry fields. I was also an undergraduate researcher with T'ai Roulston, Rosemary Malfi, and Wendy Tori studying bumble bee foraging, parasitism, and ecological niche modeling.

Stuligross and Williams assisted with the production of the KQED Deep Look video, "Watch This Bee Build her Bee-Jeweled Nest," posted Aug. 7, 2018.  The video notes that most of the 4000 bees in North America are solitary. Mason bees, or "builder bees," build their nests with mud, and provision their nests with nectar and pollen for their offspring.

In nature, the blue orchard bees use hollow tubes, such as reeds. The UC Davis lab uses wood blocks or "bee condos" drilled with specially sized holes, each filled with a removable six-inch-long paper straw. Almond growers who manage blue orchard bees provide drilled wood blocks in their orchards.  The bee condos are also popular among backyard gardeners.

More Information:

• Pesticides Can Affect Multiple Generations of Bees (UC Davis story by Amy Quinton)
  
  
• The Blue Orchard Mason Bee (U.S. Forest Service website, article by Beatriz Moisset and Vicki Wojcik, Pollinator Partnership)

Pollination ecologist Alexandra Harmon-Threatt, an associate professor at the University of Illinois, Urbana-Champaign, will speak on "Beyond Flowers; Examining the Role of Soils in Bee Conservation Efforts" at the next UC Davis Department of Entomology and Nematology seminar.

The online seminar, the last of the spring quarter, is set for 4:10 p.m., Wednesday, June 2. Host is pollination ecologist and professor Neal Williams. Access the Zoom link here.

More than 80 percent of bees nest below ground and most univoltine species spend more than 90 percent of their life cycle in contact with soils, Harmon-Threatt points out. "Yet most conservation efforts ignore soils and few research studies consider these critical life stages and possible exposures that occur during them. In a series of studies, our lab has begun to explore how much soils matter and whether ignoring them is to the detriment of conservation."

In her research, Harmon-Threatt zeroes in on understanding the patterns and processes that govern plant-pollinator interactions for conservation. "Pollinators play a vital role in plant reproduction, food production and ecosystem stability but are believed to be declining globally," she says. Her work focuses on identifying and understanding patterns in natural environments to help conserve and restore pollinator diversity. With a particular focus on bees, she investigates how a number of factors at both the local and landscape scale, including plant diversity, isolation and bee characteristics, effect bee diversity in local communities.

Harmon-Threatt received her doctorate from UC Berkeley, where she worked on bumble bee preferences and phylogenetic patterns. She completed a National Science Foundation postdoctoral fellowship in biology at Washington University in St. Louis. 

She was recently featured on the podcast, People Behind the Science. Any change in pollinator populations, she told her audience, can have significant effects on natural and agricultural communities. Recent declines in bee populations, in particular, indicate how "little we know about these important insects in their natural environments, she told her audience."

Cooperative Extension specialist Ian Grettenberger, coordinator of the spring seminars, e may be reached at imgrettenberger@ucdavis.edu for any technical issues. 

Community ecologist Romina Rader of the University of New England's School of Environmental and Rural Science, will speak on "The Journey to Effective Pollination" at the UC Davis Department of Entomology and Nematology's virtual seminar on Wednesday, March 10.

The seminar, hosted by Professor Neal Williams begins at 4:10. Click here to register to attend.

Rader, an associate professor, says she is broadly interested in pollination ecology, landscape ecology and plant–animal interactions in natural and human-modified landscapes. She is currently working on projects that investigate the ways in which plant and animal biodiversity respond to global change and the performance of wild and managed insect pollinators in horticultural crops.

She writes on her website: "I am a community ecologist and my research focuses on plant–animal interactions in natural and human-modified landscapes.  I am interested generally in the ecology of plants and animals in different types of habitats and landscapes and how they respond to differing management practices and global change.  My current projects relate to wild and managed insect pollinators, their efficiency at pollinating horticultural crops and finding ways to improve fruit yield and quality by understanding their life history needs."

Rader holds a  bachelor of environmental science (1998) from the University of New South Wales, Sydney, Australia. She obtained both her master's degree (2005) and doctorate (2011) from James Cook University, Cairns, Australia. Her master's thesis:   "Vertical Distribution, Resource and Space Use in a Tropical Rainforest Small Mammal Community."  For her doctorate:  "The Provision of Pollination Ecosystem Services to Agro-Ecosystems by a Diverse Assemblage of Wild, Unmanaged Insect Taxa." She won a 2017- 2020 Australian Research Council Discovery Early Career Researcher Award. 

Among her most recent journal publications:

• S.A.E.C. Wijesinghe, L.J. Evans, L. Kirkland & R. Rader 2020, ‘A global review of watermelon pollination biology and ecology: The increasing importance of seedless cultivars,' Scientia Horticulturae, vol. 271, pp. 109493,
  https://doi.org/10.1016/j.scienta.2020.109493
• Heidi Kolkert, Rhiannon Smith, Romina Rader & Nick Reid 2020, ‘Insectivorous bats foraging in cotton crop interiors is driven by moon illumination and insect abundance, but diversity benefits from woody vegetation cover,' Agriculture, Ecosystems & Environment, vol. 302, pp. 107068,
  https://www.sciencedirect.com/science/article/abs/pii/S0167880920302541
• Jamie R. Stavert, Charlie Bailey, Lindsey Kirkland & Romina Rader 2020, ‘Pollen tube growth from multiple pollinator visits more accurately quantifies pollinator performance and plant reproduction,' Scientific Reports, vol. 10, no. 1,
  https://www.nature.com/articles/s41598-020-73637-5
  
• Liam K. Kendall, Vesna Gagic, Lisa J. Evans, Brian T. Cutting & Jessica Scalzo, Romina Rader. 2020, ‘Self-compatible blueberry cultivars require fewer floral visits to maximize fruit production than a partially self-incompatible cultivar,' Journal of Applied Ecology, 
  https://besjournals.onlinelibrary.wiley.com/doi/abs/10.1111/1365-2664.13751
• Vesna Gagic, Lindsey Kirkland, Liam K. Kendall, Jeremy Jones & Jeffrey Kirkland Romina Rader 2020, ‘Understanding pollinator foraging behaviour and transition rates between flowers is important to maximize seed set in hybrid crops,' Apidologie, 
  https://link.springer.com/article/10.1007/s13592-020-00800-2

Agricultural Extension specialist Ian Grettenberger coordinates the seminars. This is the last of the winter seminars. For technical issues, contact Grettenberger at imgrettenberger@ucdavis.edu.