Bees, Native Plants and Crop Pollination

Diadasia, the sunflower bee, on Helianthus annuus. Photograph by D.L. Briggs. NATIVE BEES, NATIVE PLANTS, AND CROP POLLINATION IN CALIFORNIA

by Claire Kremen, Robert L. Bugg, Nikki Nicola, Sarah A. Smith, Robbin W. Thorp, and Neal M. Williams

alifornia is recognized were credited with contributing $4.2 Cglobally as an area of ex- billion to crop productivity in Cali- ceptional plant diversity fornia (E. Mussen, pers. comm.). containing a host of plants found Here we focus on the under-appre- nowhere else in the world. It is also ciated role that native bees play in the most important agricultural area California’s agricultural productiv- in North America, producing half ity, and how California’s native of the US supply of fruits, nuts, and plants support these native bee vegetables at an annual value of populations. $16.45 billion, and exporting $6.5 A large number of flowering billion of food and agricultural com- plants (Angiosperms) rely on an ani- modities abroad. mal for pollination, successful seed Insect pollinators are critically set, and fruit growth. Even self-fer- important both for the maintenance tile plants (e.g., tomatoes) or plants of California’s diverse natural eco- systems and for its agricultural pro- Osmia lignaria, the blue orchard bee, on ductivity. In 1997, honey bees alone almond. Photograph by D.L. Briggs.

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 41 The Cache Creek Valley, showing large areas of chaparral-oak woodland adjacent to farm fields. Photograph by C. Kremen. that are typically wind-pollinated Bees (superfamily Apoidea) are len as they visit flowers in search of (e.g., grapes) can benefit from ani- thought to be the most important nectar or mates. mal “vectors”—animals that help to group of pollinators for both crop Over 4,000 species of bees oc- transport pollen. Their help makes and non-crop plants. Female bees cur in North America, and 1,500 possible cross-pollination, which can are one of the few insect groups are currently found in California produce larger, better-tasting fruits that specialize in pollen collection (Thorp, observations). The vast with more viable seeds, and en- to feed their larvae. Over time, they majority of these bees are “solitary” hanced genetic diversity in seedlings. have developed physical traits de- species rather than the familiar so- In the United States, over 100 signed for collecting pollen. These cial honey bees and bumble bees. crops are bee-pollinated, and 15– include numerous “hairs” on their Females of solitary species collect 30% of the average American diet is bodies to which pollens adhere, and pollen, mold it into a pollen “loaf,” comprised of bee-pollinated foods. specialized structures known as and seal it along with a single egg Thus, bee-pollinated crops make up scopae or corbiculae for storing and into a nest cavity. an important component of human transporting pollen on their legs or Within this nest the larvae then dietary stability and diversity. Some abdomens. hatch, complete development, and of the fruits and vegetables requir- Bees also tend to forage consis- pupate, finally emerging as adults. ing bee pollination include: alfalfa, tently on one plant species before All of this occurs with no further almond, apple, avocado, cantaloupe, returning to the nest to deposit their maternal care. Each bee species is cucumber, kiwi, plum, squash, sun- pollen loads. This behavioral fidel- specific in its choice of nesting sub- flower, watermelon, and selected ity enhances the chance that pollen strate: these range from simple to cultivars of apricot, citrus, peach, will be transported from flower to elaborate tunnels dug into the and strawberry. In addition, a far flower of the same species, ensur- ground, to cavities in twigs or dead larger set of fruits and vegetables ing reproduction. Although male wood. require insect pollinators for seed bees do not collect pollen, they too Many farmers import colonies or hybrid seed production. are often hairy and can transfer pol- of the European honey bee, Apis

42 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 mellifera, to ensure adequate polli- therefore set out to understand the do not collect pollen themselves, or nation of crops requiring bee visits role of unmanaged native bees in are bees that carry pollen internally. for fruit set. Unfortunately, declines crop pollination, and how the ser- Further investigation of spring in the availability of colonies due to vices they provide change as envi- crops (mostly orchards) will un- diseases, loss of bee-keeping subsi- ronmental conditions are altered. doubtedly increase the number of dies, and pesticides, have led to Since 1999 we have carried out this species involved. For crops that we shortages of pollination services at work in California in Yolo, Solano, have investigated in detail, we found times. Overall, there are now less and Napa counties; on farm sites that native bees often make up a than half the number of bee colo- situated in the Central Valley; and high proportion of the total bee nies that existed back in the 1950s, in the Cache and Putah Creek wa- visits (i.e., visits that include honey although the demand for bees in tersheds on the eastern edge of the bees), suggesting that native bees some areas continues to increase. Inner Coast Range. can be as or more important than California uses over a third of managed honey bees for these crops the available 2.6 million commer- (Table 1). cial hives each year for almond pol- ROLE OF NATIVE In watermelon, a crop that re- lination alone, importing many BEES IN CROP quires multiple bee visits and depo- hives from other states as distant as POLLINATION sition of 500–1,000 pollen grains the Dakotas, Texas, and Florida (E. for production of a marketable fruit, Mussen, pers. comm.). To date, we have identified 65 we found that the native bee com- Native bee pollinators may be native bee species that visit and po- munity alone could provide suffi- taking up some of the slack caused tentially pollinate a variety of prin- cient pollination for the crop. This by honey bee shortages, but the cipally summer California crops, ability, however, depended on the quantitative importance of most and 14 additional bee species that diversity and abundance of bees in native bee species in crop pollina- visit crops but probably do not con- the community, which in turn was tion remains largely undocumented. tribute to pollination (see Table 1 dependent on the abundance of na- In a few cases, native bees are known on page 44). The latter species are tive habitat in the area. to be more effective pollinators than either parasitic “cuckoo bees” that As agricultural operations have honey bees. Examples include the alkali bee (Nomia melanderi) on al- A typical conventional farm field in the Sacramento Valley. No floral resources, other falfa; bumble bee species on water- than those provided by the crop (in this case watermelon) are available. Photograph by melon and blueberry; and various C. Kremen. native bees on sunflower. Native bees may be at risk, how- ever, from environmental change. Pesticides have taken their toll on native bee populations as they have on honey bees, and have been re- sponsible for the failure of the blue- berry crop in Canada. Habitat loss, fragmentation, and degradation are suspected agents in the decline of native bee populations and diver- sity. Native bees require natural habitat to provide blooming plants throughout their flight period, and nesting sites for rearing young. As natural habitats are converted to in- dustrial or agricultural uses, avail- able areas that can support bees are declining. Thus while natural ecosystems may be providing pollinators—and hence pollination services—for free, non-sustainable land use is poten- tially eroding these benefits. We

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 43 expanded and intensified in areas of bee visitation. Tomato flowers pro- WILD HABITAT AND California, native habitat declined duce no nectar, and their pollen can CROP POLLINATION and could no longer support a size- only be accessed from poricidal an- able native bee community. Conse- thers by high frequency vibration. Many native bee species require quently, native bees could no longer Honey bees are unable to vibrate a diversity of floral resources to pro- provide the needed pollination ser- the flowers, and thus obtain few vide nectar and pollen throughout vices without the addition of honey rewards from tomato flowers (hence their flight season. In addition, they bee colonies. the low proportion of honey bee require protected areas for nesting, The majority of organically- visits, as shown in Table 1). How- including twigs, dead wood, bare managed farms located near native ever, bumble bees and other bees soil, and abandoned rodent nests. It habitat obtained sufficient pollina- (e.g., Anthophora urbana) can obtain therefore seemed that native bee tion solely from the native bee com- the pollen through vibration, and crop pollinators would more likely munity. For those located far from can often be found exploiting this be found on farms close to natural native habitat, a much smaller per- honey bee-free niche. habitat. centage of organically-managed By excluding bees from certain In order to test this hypothesis, farms and no conventionally-man- flowers, cross- and self-pollinating we conducted two types of studies. aged farms received sufficient pol- other flowers by hand, and then First we measured the diversity and lination from native bees. These lat- comparing these against flowers ac- abundance of crop visitors to water- ter farms relied on honey bees for cessible to bees, Smith and Kremen melons and tomatoes on farms that pollination. (in prep.) found that native bees varied in nearby natural habitat from We also found that crops typi- significantly increase the fruit set 0-80% cover within a 1 kilometer cally thought of as “self-pollinated” and size of Sungold cherry toma- radius. For watermelon crop visi- benefited substantially from native toes by promoting cross-pollination. tors, nearby natural habitat strongly affected both native bee diversity and total abundance. For tomato, which TABLE 1. NUMBERS OF NATIVE BEE has only two types of frequent visi- tors, bumble bees (Bombus spp.) and SPECIES AND PROPORTIONS OF TOTAL Anthophora urbana, we found that NATIVE BEE VISITORS (out of all bee visits including the amount of natural habitat posi- honey bees) to selected crops in Yolo and Solano counties, California tively affected visitation by bumble bees but not by A. urbana. Crop Native bee Additional Average Range Bumble bees nest in abandoned visitors non- proportion across rodent nests and have long flight (number pollinating of total bee farms seasons, extending from early spring of species) visitors visits from (proportions) to late summer. In addition, bumble (number of native bees bee colonies produce only one re- species) productive generation per year, and thus only one nest is established per Watermelon 30 9 0.27 0.0 – 0.88 colony per season. Solitary A. ur- bana females excavate nests in the Sunflower 25 2 0.37 0.01 – 0.99 ground; this species has a shorter Strawberry 16 2 0.96 0.87 – 1.00 flight season from late spring to late summer. It is multivoltine (multiple Muskmelon 11 0 0.08 0.0 – 0.42 reproductive generations per year), and nest sites could therefore shift Tomato 6 0 0.98 0.89 – 1.00 over time to track the available flo- Almond 5 1 – – ral resources from place to place. Perhaps bumble bee queens seek Eggplant 5 0 0.74 0.33 – 1.00 out nest sites close to abundant floral resources in the early spring, Cucumber 3 0 – – which are largely concentrated in Squash 2 0 – – wild habitat. Later in the summer when most California wildland spe- Total 65 14 cies have finished blooming, bumble bee workers forage at floral resources

44 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Riparian habitat including Cercis occidentalis (western redbud), an important spring resource for bumble bees and other bees. Photograph by C. Kremen. on farms, but are constrained to for- riparian or mixed chaparral and oak perennials, shrubs, and trees. We aging within a certain distance of woodland. In fact, we found all of now have detailed records of which their nest sites in the wildlands. them there—54% in both habitat native bee species utilize which plant In contrast, both farm and wild types, 17% in riparian alone, and species in this area. We are cur- resources are abundant when A. ur- 29% in chaparral/oak woodland rently complementing the work pre- bana begins nesting, so females can alone. sented here with a more compre- choose either area for nesting. In hensive study that also includes na- addition, subsequent generations of tive annuals, weeds, and crops moni- A. urbana may shift nest sites to CALIFORNIA NATIVE tored at biweekly intervals at 22 track resource availability and PLANTS AND BEES farms and natural area sites. gradually move nest sites into agri- The results for the 2001 study cultural areas. Finally, we explored the habitat are summarized in Table 2 (on pages We also surveyed bees in wild relationships and resource needs of 46 and 47). Table 2 shows which habitats in the Cache and Putah bee species by sampling bees on California perennials provide re- Creek watersheds in order to deter- California native plants in six chap- sources for the greatest number of mine which of our crop pollinators arral/oak woodland and riparian important crop pollinator species. also occur in the wild areas. These sites from January through Octo- Importance of crop pollinator spe- sites were characterized as either ber of 2001. Our main focus was on cies was defined as those insects

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 45 TABLE 2. CROP AND NON-CROP VISITORS TO CALIFORNIA NATIVE PERENNIALS. Organized by the maximum number of important crop visitors (see text) visiting a plant. Species currently used in hedgerow or tail water plantings in Yolo and Solano counties are indicated by “Y”; other species available in nurseries are indicated by a *. A ✛ indicates that European honey bees (Apis mellifera) were also observed foraging on these plants.

NUMBER OF BEE SPECIES

Plant species Currently Important Other Parasitic Non- All used in crop crop bee crop crop bees hedgerow or visitors visitors visitors visiting tailwater bees plantings

Heteromeles arbutifolia✛ Y10812039 Eriogonum fasciculatum Y 8 8 4 11 31 Baccharis salicifolia✛ Y 5 8 0 19 32 Mentzelia laevicaulis✛ – 52018 Eriodictyon californicum✛ – 4 4 1 26 35 Cercis occidentalis✛ Y 4 9 1 10 21 Rosa californica✛ Y 41106 Lotus scoparius✛ – 3 3 0 15 21 Adenostoma fasciculatum✛ * 371314 Lupinus succulentus✛ – 31036 Cornus sericea✛ * 33016 Eremocarpus setigerus – 31116 Eriophyllum lanatum – 220812 Baccharis pilularis✛ Y 240612 Hemizonia congesta – 20013 Lupinus microcarpus – 20012 Ceanothus cuneatus✛ Y 1 8 0 11 20 Lepechinia calycina✛ – 1 4 1 10 16 Epilobium canum✛ * 14049 Stephanomeria virgata – 11046 Salix laevigata✛ Y 14027 Mimulus aurantiacus✛ Y 12126 Rhamnus californica Y 13026

46 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 TABLE 2 (cont.)

NUMBER OF BEE SPECIES

Plant species Currently Important Other Parasitic Non- All used in crop crop bee crop crop bees hedgerow or visitors visitors visitors visiting tailwater bees plantings

Sambucus mexicanus✛ Y 12025 Madia elegans – 10012 Arctostaphylos manzanita✛ Y 12013 Rupertia physodes – 00077 Ceanothus oliganthus✛ – 02068 Salix sessilifolia – 01034 Wyethia helenioides✛ – 01034 Calystegia purpurata – 03025 Lupinus albifrons✛ * 01023 Fraxinus dipetala – 00022 Clarkia sp. – 0 0 0 1 1 Phacelia imbricata – 00011 Toxicodendron diversilobum✛ – 00011 Triteleia laxa – 00011 Aesculus californica✛ Y 01001 Clematis lasiantha * 01001 Eriogonum nudum – 01001 Eschscholzia californica Y 01001 Total bee species in category 16 49 14 113 192

visiting three or more of the crops cies. Six of the 10 plant species with californica, Adenostoma fasciculatum, listed in Table 1. In total, we docu- the greatest number of records for and Cornus sericea, and for non-crop ment records of 192 native bee important crop pollinators were also visitors were Ceanothus cuneatus, species on 41 native plant species. critical for other bee species (Eriod- Lepechinia calycina, Eriophyllum Table 2 also lists the number of ictyon californicum, Heteromeles lanatum, and Rupertia physodes. other crop visitors and of non-crop- arbutifolia, Baccharis salicifolia, Lotus Since the honey bee, Apis melli- visiting native bee species. scoparius, Eriogonum fasciculatum, and fera, is also an important, although Many of the plant species im- Cercis occidentalis). The remaining non-native, crop pollinator, Table portant for the crop pollinators also top 10 plants for crop pollinators 2 lists the native plants at which we provide resources for other bee spe- included Mentzelia laevicaulis, Rosa observed A. mellifera foraging. This

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 47 species makes use of a wide variety wild habitats and show some de- crop pollination services that bees of the California flora, and beekeep- gree of dependence on the native provide. In Yolo, Solano, and Napa ers clearly benefit during off-crop California flora. counties, certain areas are already seasons by using wild areas for bee Finally, the destruction of na- protected to some degree, includ- forage. tive habitat in the Central Valley ing, for example, the Cache Creek appears to be related to a decline in Nature Preserve, Jepson Prairie, the diversity and abundance of na- Yolo Basin Wildlife Area, Putah CONCLUSIONS tive bees found there, along with a Creek UC Davis Campus Reserve, concomitant reduction in the crop Quail Ridge Reserve, Cold Creek Our work during the past four pollination services they provide. A Canyon Reserve, Cache Creek years has documented that hopeful sign, however, is that even Canyon Regional Park, Nichols California’s native bees make an small fragments of wild or semi- County Park, and the Bureau of important contribution to crop pol- wild habitat still sport diverse and Land Management lands along Blue lination. This contribution could abundant bee faunas, such as at the Ridge. All but the first four sites, become even more valuable as an Cache Creek Nature Preserve, a however, are located in the hilly “insurance policy” if honey bees 130-acre riparian and upland area areas of the Inner Coast Range, become more scarce or fail alto- that is currently being restored. and very few natural or semi-natu- gether. We have also shown that all It is important to conserve bee ral lands remain within the Sacra- of these native bee species occur in habitat to maintain the valuable mento Valley itself.

Eriodictyon californicum (yerba santa) and Mimulus aurantiacus (sticky monkeyflower) of chaparral. E. californicum is visited by a wide number of bee species, whereas M. aurantiacus is rarely visited, and only by a few species. Photograph by C. Kremen.

48 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Bringing bees back to the Sac- new plants to add to existing re- Commerce Agency. www.commerce. ramento Valley would require an serve and farm restoration efforts ca.gov/state/ttca/ttca_homepage.jsp extensive restoration effort. None- for the benefit of the pollinator Frankie, G.W., S.B. Vinson, M.A. theless, the dream of restoring community. And “bringing back the Rizzardi, T.L. Griswold, S. O’Keefe, healthy communities of pollinators bees” will ensure a much rosier fu- and R.R. Snelling. 1998. Diversity and abundance of bees visiting a by restoring their plant communi- ture for California’s native flora. mass flowering tree species in dis- ties is not outside the realm of pos- turbed seasonal dry forest, Costa sibility. On-going restoration efforts ACKNOWLEDGMENTS Rica. Journal of the Kansas Entomo- along Cache Creek and Putah Creek logical Society 70:281–296. can ultimately provide archipelagoes Kevan, P.G., E.A. Clark, and V.G. and corridors of bee-friendly habi- This work was supported by the Thomas. 1990. Insect pollinators tat. Over the next 30 years, 1,000 Mead Foundation, the National and sustainable agriculture. Ameri- acres of restoration efforts are Fish and Wildlife Foundation, the can Journal of Alternative Agriculture planned along Cache Creek alone Organic Farming Research Foun- 5:12–22. (J. Lowrey, pers. comm.). dation, the McDonnell Foundation, Kevan, P.G., and W.E. LaBerge. 1979. Farmers can assist the restora- Stanford University, Princeton Demise and recovery of native pollina- tor populations through pesticide use and tion process and benefit their own University, University of Califor- some economic implications. IVth nia Sustainable Agriculture Re- crops through the planting of International Symposium on Polli- “insectary plants” that provide habi- search and Education Program, nation, 489–508. Maryland Agricul- tat and resources for beneficial Wildlife Conservation Society, and ture Experiment Station, College insects ranging from predators to Harry H. Laidlaw, Jr., Honey Bee Park, MD. pollinators. The Community Alli- Research Facility at the University Matheson, A., S.L. Buchmann, C. ance of Family Farmers and the Yolo of California at Davis. O’Toole, P. Westrich, and I.H. Wil- County Resources Conservation N.M. Williams was supported liams 1996. The conservation of bees. District actively encourage the plant- by a Nature Conservancy Smith Academic Press, San Diego, CA. ing of hedgerows and tailwater ponds Postdoctoral Fellowship and S.A. McGregor, S.E. 1976. Insect pollination using native plants (including some Smith was supported by National of cultivated crop plants. USDA-ARS, Washington, D.C. of the plants listed in Table 2). Science Foundation and Environ- Moldenke, A.R., and J.L. Neff. 1974. mental Protection Agency doctoral Many of the plants that farmers The bees of California: A catalogue with are already using were selected be- fellowships. This work could not special reference to pollination and eco- cause they provide pollen or nectar have been completed without the logical research. International Bio- to other beneficial insect species, assistance of the many farmers and logical Program, Santa Cruz, CA. primarily predators and parasitoids ranchers in Yolo and Solano coun- Nabhan, G.P., and S. Buchmann. of crop pests. Our data show that ties who permitted us access to their 1997. Services provided by pollina- many of these plants also benefit properties and provided us with tors. In Nature’s services: Societal de- some of the most important crop invaluable information. We are also pendence on natural ecosystems, ed. pollinators, as well as other bee grateful to the University of Cali- G.C. Daily, 133–150. Island Press, species. fornia Reserve System for permit- Washington, DC. O’Toole, C., and A. Raw. 1992. Bees of Some potentially important ting us access to UC Davis reserves, the world. Facts on File, New York, and to the Cache Creek Nature plants for pollinators, however, are NY. either difficult to include in hedge- Preserve. Proctor, M., P. Yeo, and A. Lack. 1996. row plantings because they cannot The natural history of pollination. be brought into cultivation, such as Timber Press, Portland, Oregon. Eriodictyon californicum (J. Gerland, REFERENCES Tepedino, V.J., S.D. Sipes, J.L. Barnes, pers. comm.) or have not yet been and L.L. Hickerson. 1997. The tested (e.g., Lotus scoparius). Some Bugg, R.L., J.H. Anderson, C.D. need for “extended care” in conser- of these plants may prove critical— Thomsen, and J. Chandler. 1998. vation: Examples from studies of providing resources for a partic- Farmscaping in California: Hedge- rare plants in the western United rows, roadside plantings and wild ularly important bee species, or States. In Proceedings of the Interna- plants for biointensive pest manage- tional Symposium on Pollination, ed. filling in a “phenological window” ment. In Enhancing biological control: K.W. Richards, 245–48. ISHS. during which no bee-attractive Habitat management to promote natu- plants from the current hedgerow ral enemies of agricultural pests, ed. Claire Kremen, Department of Ecology list are blooming. R.L. Bugg. University of California and Evolutionary Biology, Guyot Hall, Our current research will pro- Press, Berkeley, CA. Princeton University, Princeton, NJ vide a rich dataset for identifying California Technology, Trade and 08544. [email protected]

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