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Vol. 30, Nos. 3-4 July/October 2002 FREMONTIA

A JOURNAL OF THE NATIVE SOCIETY

IN THIS ISSUE:

INTRODUCTION by G.W. Frankie / 3 • LEPIDOPTERAN FEEDING ON CALIFORNIA NATIVE by J.A. Powell / 5 • CYNIPID-INDUCED AND CALIFORNIA by K.N. Schick / 15 • BARK INFESTING CALIFORNIA’S CONIFERS by D.L. Wood and A.J. Storer / 19 • BUMBLE : BOISTEROUS OF NATIVE CALIFORNIA by R.W. Thorp, P.C. Schroeder, and C.S. Ferguson / 26 • A PINNACLE OF BEES by O. Messinger and T. Griswold / 32 • NATIVE BEES, NATIVE PLANTS, AND CROP IN CALIFORNIA by C. Kremen, R.L. Bugg, N. Nicola, S.A. Smith, R.W. Thorp, and N.M. Williams / 41 • BEES IN BERKELEY? by G.W. Frankie, R.W. Thorp, M.H. Schindler, B. Ertter, and M. Przybylski / 50 • FARMSCAPE ECOLOGY OF A

VOLUMENATIVE 30:3–4, STINK BUG JULY/OCTOBER IN THE SACRAMENTO 2002 VALLEY by L.E. Ehler, C.G. Pease, FREMONTIA and R.F. Long /1 59 • ENDANGERED PLANTS AS GUIDES FOR SAVING ENDEMIC IN CALIFORNIA by D. Rubinoff / 62 • NOTES AND COMMENTS / 67 • BOOKS RECEIVED / 70 • BOOK REVIEW / 70 CALIFORNIA NATIVE PLANT SOCIETY FREMONTIA www.cnps.org MEMBERSHIP VOL. 30, NOS. 3–4, JULY/OCT 2002 Dues include subscriptions to Fremontia and the Bulletin. Distributed May 2003 Life ...... $1,000 Supporting ...... $75 Copyright © 2003 Benefactor ...... $500 , Group, International . . . $45 California Native Plant Society Patron ...... $250 Individual or Library ...... $35 Linda Ann Vorobik, Editor Plant Lover ...... $100 Student/Retired/Limited Income $20 Gordon W. Frankie, Convening Editor CONTACTS CHAPTER COUNCIL Bob Hass, Copy Editor CNPS Alta Peak (Tulare) . . . . Joan Stewart Beth Hansen-Winter, Designer 1722 J Street, Suite 17 Bristlecone (Inyo-Mono) ...... CALIFORNIA NATIVE Sacramento, CA 95814 Stephen Ingram PLANT SOCIETY (916) 447-CNPS (2677) Channel Islands ...... Lynne Kada Fax: (916) 447-2727 Dorothy King Young (the Mendo- Dedicated to the Preservation of [email protected] cino/Sonoma Coast) . Lori Hubbart the California Native Flora ...... Tony Morosco Sacramento Office Staff: El Dorado ...... Amy Hoffman The California Native Plant Society Executive Director . . . . . Pamela C. Kern County . . . . . Laura Stockton (CNPS) is an organization of lay- persons and professionals united by an Muick, PhD /Santa Monica Mountains interest in the native plants of Cali- Membership Coordinator . . Marion Halli Mason fornia, open to all. Its principal aims Millin Marin County ...... Bob Soost are to preserve the native flora and to Chapters & Publications . Paul Maas Milo Baker (Sonoma County) . . . . . add to the knowledge of members and Bookkeeper . . . . . John Caicchiolo Lynn Houser the public at large by monitoring rare ...... Tim Thomas and endangered plants throughout the Monterey Bay . . . Donlon Fremontia Editor . . . . . Linda Ann state; by acting to save endangered Mount Lassen ...... Jim Bishop areas through publicity, persuasion, Vorobik, PhD Napa Valley ...... Marcie Danner and on occasion, legal action; by pro- Sr. Policy Analyst ...... Emily viding expert testimony to government ...... Larry Levine Roberson bodies; and by supporting financially Orange County . . . Daniel Songster and otherwise the establishment of So. California Regional Botanist . . . Redbud (Grass Valley/Auburn) . . . . native plant preserves. Much of this Ileene Anderson Richard Hanes work is done by volunteers through Rare Plant Botanist . . . Dave Tibor Riverside/San Bernardino counties . . CNPS Chapters throughout the state. Vegetation Ecologist . . Julie Evens Katie Barrows The Society’s educational work in- Vegetation Ecologist . . Anne Klein . . Jennifer Hogan cludes: publication of a quarterly jour- ...... Carrie Schneider San Bruno Mtn. Project Coordinator nal, Fremontia, and a quarterly Bulletin San Gabriel Mountains . Lyn McAfee which gives news and announcements Mary Petrilli San Luis Obispo . . . . Dirk Walters of Society events and conservation Legislative Advocate .Vern Goehring Sanhedrin (Ukiah) . Chuck Williams issues. Chapters hold meetings, field Earth Share Liaison . . Halli Mason trips, and plant and poster sales. Non- . . Mary Simpson members are welcome to attend. Legal Advisor . . . . Sandy McCoy Santa Cruz County . Janell Hillman Money is provided through member Website Coordinator . Carol Witham Sequoia (Fresno) . . . . Jeanne Larson dues and funds raised by chapter plant Bulletin Editor . . . . . Steve Tyron Shasta ...... Dave DuBose and poster sales. Additional donations, Sierra Foothills (Tuolumne, Cala- bequests, and memorial gifts from BOARD OF DIRECTORS veras, Mariposa) . . . . Patrick Stone friends of the Society can assist greatly (Palos Verdes) ...... in carrying forward the work of the Directors: Ellen Brubaker Society. Dues and donations are tax- Carol Baird, Sue Britting, Steve deductible. Hartman, Lori Hubbart, Lynne Kada, Tahoe ...... Michael Hogan Betsey Landis, David L. Magney, Willis L. Jepson (Solano) ...... Fremontia logo (by L.A. Vorobik) reprinted Mary Shaw from The Jepson Manual, J. Hickman, Sandy McCoy, Patt McDaniel, J. Ed., 1993, with permission from the Spence McIntyre, Carol Witham Yerba Buena () . . . . . Jepson Herbarium, UC. © Regents of the Randy Zebell University of California. MATERIALS FOR PUBLICATION Members and others are invited to submit material for publication in Fremontia. THE COVER: Showy milkweed (Asclepias speciosa) with a male bumble (probably Instructions for contributors can be found on the CNPS website, www.cnps.org, Bombus vosnesenski) gathering , common or can be requested from Fremontia Editor, Linda Ann Vorobik, vorobik@rock checkered (probably Tri-chodes ornatus) island.com, or c/o University and Jepson Herbaria, 1001 Valley Life Sciences Bldg. resting on , and monarch larvae (Danaus plexippus) foraging on #2465, University of California, Berkeley, CA 94720-2465. . Photograph by S. Sharnoff. Prepress by ScanArt / Printed by Craftsman Trade Press

2 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 INTRODUCTION by Gordon Frankie

t is well known that insects and to the development of the coevolu- hatching, larvae feed on plant tissue Iplants display a wide variety of tion concept in the 1960s. and simultaneously secrete chemi- highly predictable relationships, Insects of several orders are ca- cals that interact with plant com- such as lepidopteran caterpillars and pable of inducing formation in pounds to produce galls that are other larval types that feed on dif- many California native plants. In characteristic of the and plant. ferent parts of plants, or the many the second article, Schick examines These complex relationships have a kinds of insects that gather nectar one group of gall inducers, the cyni- long evolutionary history dating from flowers and pollinate them. pid , which commonly form back millions of years. Researchers have invested consid- galls on California oaks. Depend- Some California native insects erable time in field and laboratory ing on the wasp , females have the reputation of killing large study to elucidate the fundamental carefully lay their eggs in specific numbers of native plants, such as biological and ecological bases of plant tissue such as buds, stems, bark beetles, which cause occasional these relationships. Presented in this flower buds, or even roots. Upon die-offs of some forest tree popula- special Fremontia issue are nine ar- ticles that reflect diverse California Pale swallowtail (Papilio eurymedon) drinking nectar from flowers of western thistle native -plant interactions and (Cirsium occidentale). Photograph by L. Vorobik. some of the interesting history be- hind them. The volume can be divided into three sections. The first contains three articles concerned with com- mon herbivorous insects and their plant hosts. The second presents four articles on bees, which are known to be the most important insect group in Califor- nia and in many other regions of the world. The final section, which contains a strong sociobiological message, includes two articles which demonstrate the complexity of insect-plant relationships. The order , con- taining and , is one of the largest orders of insects. In California there are about 4,500 species and 260 butterfly spe- cies. In the first article, Powell char- acterizes the general life cycle of lepidopterans and the many patterns of use that their larvae have with native host plants. Common uses include leaf feeding, boring in and seeds, and flower feeding. Most of these relationships are beneficial when viewed in the context of an ecosystem, such as the close rela- tionship between pierid butterfly species and their mustard and le- gume host plants, which gave rise

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 3 tions. Wood and Storer provide an Tropical regions, in contrast to mental species are preferred over information-packed article based on temperate areas, are well-known for exotic ornamentals by a factor of years of research that has greatly their rich flora and fauna. It is be- four. They also offer reasons why helped to characterize bark beetles coming increasingly clear, however, urbanites might want to encourage and their relationships with host that some temperate zones have bees and their host flowers in their plants in California. Although there diverse biota that are comparable yards. are 170 species of these small beetles to the tropics. Mediterranean cli- Many California environments in California, only a few of them, mates, for example, often contain have been invaded by exotic plants, restricted to a few genera, are tree bee-rich areas. Messinger and which have become well-established killers. All species provide ecosys- Griswold provide a case history and have led to new ecological rela- tem services through feeding ac- study of native bees and their host tionships with native insects and tivities that lead to nutrient cycling plants in a community at native plants. A few of these may in forest succession. Results from Pinnacles National Monument, be viewed as beneficial, but many the handful of economic species that near Hollister, where more than 500 have created new problems. In ar- have been intensively studied re- flowering host plants provide floral ticle eight, Ehler et al. describe the veal many complex relationships resources for about 400 bee species. ecological relationships between a with their hosts, each other, and The authors focus on the diverse native pestiferous stink bug on to- other insects such as predators and flora and various (in- matoes, the exotic weed species on parasites, fungi, and humans. cluding climatic, seasonal, annual, which the bugs develop, and native Bees are known to be the most and responses to fire) that this group perennial grasses in the Sacramento important pollinators in many, if of bees displays. Valley. Their ongoing work indi- not most, temperate and tropical Recent declines in honeybee cates that by replacing exotic weeds regions of the world. In recent years, populations in the US, which are with native grasses along roadsides, the increasing evidence of global largely attributable to mortality stink bugs can be reduced to levels pollinator decline has motivated re- from parasitic mites, pathogenic that will lead to reductions in insec- searchers to learn more about bees diseases, and pesticides, have raised ticides aimed at the bugs infesting and how to conserve and protect concerns about shortages of hive crops. these valuable pollinators. Articles bees to pollinate crop plants. This In the final article, Rubinoff uses four through seven are concerned is of special concern to agricultur- three case history examples to illus- with bees and the California plants ally diverse states such as Califor- trate that there are numerous unique they visit in a variety of wildland nia. Kremen et al. have been work- relationships between California and human-altered systems. ing in three endemic insects, endemic plants, The article by Thorp et al. be- counties since 1999 to evaluate the and the communities in which they gins the series on bees by providing potential of unmanaged native bees are found. He urges more study of a biological and ecological overview in crop pollination. They have also these relationships, and at the same of the 26 species of native Califor- recorded 192 native bee species on time suggests that conser- nia bumble bees. They occur in 41 native plant species in wild habi- vation planning in ecosystems may many different , but reach tats that are in close proximity to be the only way to conserve many their greatest diversity in the north- agricultural crops. These research- of California’s unique plants and western part of the state. Bumble ers offer abundant evidence of im- endemic insects. bees are considered generalists be- portant ecological relationships that cause of the wide variety of plant exist between native bees, honey- species they visit and also because bees, California native plants, and REFERENCES of several behavioral and morpho- crop pollination. logical adaptations that allow them Wild areas are not the only habi- Buchmann, S.L. and G.P. Nabhan. to pollinate diverse flower types. tats where bee pollinators are found. 1996. The forgotten pollinators. Island Thorp et al. call attention to moni- Frankie et al. report on a recent Press, Covelo, CA. toring studies on two California study of native bee diversity and Shapiro, A.M. 2002. The California bumble bees that are on the decline ecology in residential neighbor- urban butterfly fauna is dependent in the western . One hoods of Albany and Berkeley in on alien plants. Diversity and Distri- is a candidate for federal listing. the . In ad- bution 8:31–40. International trafficking of foreign dition to the relatively high diver- bumble bees for pollination of hot- sity of native species discovered (72 Gordon W. Frankie, 201 Wellman Hall house tomatoes may exacerbate the plus two exotic bee species), they #3112, UC, Berkeley, CA 94720-3112. decline trend in native species. report that native California orna- [email protected]

4 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Aposematic butterfly caterpillars rendered distasteful to vertebrate predators by the chemistry of their host plants. Pipevine swallowtail (Battus philenor, Papilionidae), on Aristolochia (pipevine). See discussion on pages 13 and 14. All photographs except Figure 9 by J.A. Powell. LEPIDOPTERAN CATERPILLARS FEEDING ON CALIFORNIA NATIVE PLANTS by Jerry A. Powell

oths and butterflies and plants. Only a few are serious pests, timate of the number of species of Mtheir caterpillars (Order as defoliators of forest trees, caus- Lepidoptera in California, but there Lepidoptera) are among ing damage to agricultural and are more than 3,500 named and de- the most familiar insects in both vegetable crops, and invading stored scribed, and many smaller species urban and rural habitats. In terms products. Contrary to common be- have yet to be classified. Butterflies of species richness, this is the sec- lief, most Lepidoptera are benefi- are among the most beautiful and ond or third largest order of in- cial and fulfill a wide range of ser- admired insects, but in diversity they sects, with more than 150,000 de- vices in ecosystems. These include are vastly outnumbered by moths. scribed species, about one-tenth of acting as pollinators, providing im- There are about 260 species of but- which live in . portant food sources for birds, bats, terflies and probably at least 4,500 The caterpillars (larvae) of the rodents, and lizards, and assisting species of moths in California. vast majority of species feed on liv- in nutrient recycling by feeding on Our knowledge of larvae and life ing plants and are the most diverse dead leaves, rotting wood, and fungi. histories is very incomplete. There group of that depend on We do not have an accurate es- is some information on host plants

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 5 for perhaps 60–70% of the described At any of these stages—egg, species, but often it is limited to one larva (often first or last instar), pupa, larval collection or a single popula- or adult—there may be a period of tion. As is true of all insects with lengthy delay, called diapause, in complete (those go- ing through egg, larva, pupa, and Figures 1-5: Leaf mines of micro- adult stages), all growth occurs dur- lepidopteran larvae. 1, Stigmella variella ing larval feeding, with successive () (top left) on Quercus agri- folia (coast live ). • 2, Tischeria splen- stages (instars) molting to shed the dida (Tischeriidae) (second from top left) outgrown skin (exoskeleton) and on Rubus ursinus (blackberry). • 3, Cop- head capsule, usually four or five todisca arbutiella () (second times. Adults of most species feed from bottom left) on on nutritive sources such as nectar (manzanita). • : 4, Camer- aria nemoris (bottom left) on Vaccinium from flowers, rotting fruit, and bird ovatum (California huckleberry). • 5, droppings, but they do not grow. opuntiella on Opuntia (cactus) Thus caterpillars are the culprits re- (bottom). • 6, reticulata (F) adult sponsible for damaging plants. (below), a on Q. agrifolia in early instars.

LIFE CYCLE

In a typical life cycle of moth or butterfly, adults mate soon after emergence of the female from the pupa (which is termed the chrysalis in butterflies). She selects plants on which larvae will feed and deposits eggs, singly or in masses, depend- ing upon the species. First instar larvae hatch after seven to ten days incubation and begin to eat the plant or other food material. Sometimes larvae begin feeding after migra- tion to appropriate sites, such as the new leaves at the growing termi- nals. Larval feeding and growth re- quires 35–50 days in most species. At maturity the pre- pares a pupation site in the host plant material or in leaf litter or soil. butterfly caterpillars and those of most moths construct a cocoon made of silk that they pro- duce from glands under the head. Most other butterfly and some moth larvae pupate without a cocoon, ei- ther exposed directly to the air or in cells in the ground. Transforma- tion into an adult occurs in as little as 10–14 days, and the moth or but- terfly then breaks the pupal shell to hatch. Emergence often occurs via a special track or aperture prepared by the larva, which enables the adult to escape from the substrate.

6 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 which metabolic development is has been recorded after 20, 25, and postponed. This allows the insect even 30 years in one species of yucca to avoid seasons when necessary re- moth in experimental conditions. sources are not available. Diapause This suggests the potential of some has been the key to the enormous species to survive many years of evolutionary success of Lepidoptera drought, analogous to seed banks and other plant-feeding insects in of annual plants. temperate zones characterized by harsh winters, and in arid regions and tropical areas of seasonal PATTERNS OF HOST drought. PLANT USE The challenge to California in- sects of surviving both the dry sea- Almost all native plant species son and winter is met by a variety of are fed upon by caterpillars, at least life cycle strategies. Larval feeding occasionally, and host selection is by most species takes place during not random. There are guilds of spring foliation. Development in species that specialize on grasses, many proceeds to the emergence of sedges, and other monocots, or on adults in late spring. Some then pro- conifers. However, perennial an- duce eggs that enter diapause. In- giosperms serve as hosts for the over- stead, larvae may also diapause as whelming majority of moths and first instars, or adults may enter a butterflies. Few species specialize on reproductive diapause and hiber- annual plants. In general, trees host nate. Doing so delays mating and the greatest diversity of caterpillars, egg-laying until late winter or early followed by woody of high spring just before foliation begins. architecture, then low shrubs, pe- Some species continue to de- rennial herbaceous plants, mono- velop and produce a second gen- cots, and annual dicots. eration, with adults flying again in Patterns of host acceptance and the fall. Alternatively, many spring- specificity vary widely among Lepi- feeding species enter diapause as doptera, and inherited instincts dic- last instar larvae or pupae. They tate host plant recognition by egg- wait until late winter to resume de- laying females and acceptance of velopment, timing their emergence foods by caterpillars. Commonly a with the budding of the host plants. given species is restricted to a few Other species pass the summer as hosts within one plant family or prepupal larvae or pupae, metamor- , and chemical similarities phose, and fly in the fall. Then they among plants presumably underlie produce eggs that diapause, or the such specialization. Thus, specialist adults hibernate. larvae reject any but the “right” host, Figures 7-9: Case-bearing larvae. 7, Adela Initiation of diapause and onset sometimes even closely-related septentrionella () (top), which feeds of development when diapause ends plant species, and in the lab will not on fallen leaves under Holodiscus usually is controlled by day-length accept a synthetic diet that is nutri- (oceanspray). • 8, Thyridopteryx meadii (Psychidae) (middle) on Larrea (creosote and temperature changes with the tionally sufficient for development bush). • 9, Coleophora species (Coleo- seasons. Remarkably, many species of many other species. phoridae) (bottom) on Baccharis pilularis can hold over for one or more years “” is not a for- ( brush). Photograph by R. Coville. as an to inconsistent lar- mal taxon; it is a nickname applied val food sources. Examples are seed to the more ancestral lineages and struct shelters with silk in the foli- feeders associated with conifers that superfamilies in which most of age. produce cone crops erratically or in the species are tiny moths, 2–10 Although a few are generalists, alternate years, and desert species millimeters in length. Microlepi- the great majority are relatively host- whose host plants appear sporadi- doptera larvae are mostly concealed specific—confined to a single plant cally in response to rainfall. Dia- feeders. They may be leaf miners, species in some instances (such as pause may last 5 or 6 years in such borers in stems, roots, and seed, or leaf miners), or several within one species, and successful development they may feed externally but con- genus. By contrast, larger moths,

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 7 the so-called “macrolepidoptera” or sometimes causing the plant to cre- With few exceptions, mines in “macro moths,” are nearly all exter- ate galls of a particular form in woody plants in California are lepi- nal feeders, and many—perhaps half which the larva resides. Still others dopterous, whereas those in herbs the species in North America—feed make portable cases from which are caused by members of the order on several or many unrelated plants. they feed, using silk and plant frag- Diptera (two-winged flies). Other Butterfly species in general tend to ments or other debris. regions, such as the southeastern be host plant specialists, in contrast External feeders also usually re- US and the tropics, have rich faunas to macro moths. strict their feeding to particular parts of leaf-mining beetles (Coleoptera) Superimposed on the mosaic of of the plant: new terminals, old and (), but differing host plant preferences, the leaves, , fruit, and so those specialized groups are poorly resources of any given plant com- on. As result, a local flora consisting represented in California. munity are partitioned through the of 350 plant species will have more Typical leaf miners include use of specialized niches within each than twice that number of Lepi- Stigmella (Nepticulidae) (Figure 1, plant species. This is accomplished doptera species dependent on it. page 6), our tiniest moths, with a by behavioral and often morpho- forewing length of 2–3 millimeters. logical adaptations. Some caterpil- Their larvae create serpentine mines lars feed as miners in leaves. Others LEAF AND STEM in the upper part of the leaf of many bore into roots, stems, or seeds, MINERS shrubs, such as Rhamnus (coffee- berry), Heteromeles (toyon), and Figures 10-14: Root and stem borers, Several families of Lepidoptera Toxicodendron (poison oak), and trees including plant gall feeders (below and are characterized by leaf mining hab- including Quercus (oak), Salix (wil- opposite page). 10, Wasp moth, Carmenta its, in which larvae spend early in- low), and Alnus (). At maturity species () adult and its pupal shell (below) protruding from root of Solanum stars or their entire life feeding the larva cuts a slit at the enlarged (nightshade) from Puebla, Mexico. • 11, within a leaf. Usually the species of end of the mine and drops to the Pitch nodule produced around stem- each genus form mines of a particu- ground for cocoon formation. Most boring larva of Petrova metallica (Tor- lar depth, often in either the upper Stigmella species are unnamed, and tricidae) (bottom) on Pinus contorta or lower half of the leaf, or just un- some are known only from the aban- (lodgepole pine). der the epidermis. Mines are exca- doned mines. vated in linear and serpentine forms, Tischeria (Tischeriidae) make or blotch-like and full-depth in the short, trumpet-shaped mines (Fig- new and not yet hardened leaves. ure 2, page 6) that are densely lined Experienced lepidopterists can with silk, causing a whitish appear- identify the mine to the genus level, ance even when still occupied. Al- and most are host specific, so the though fewer than nepticulids, they presence of leaf mining species can occur in many shrubs and trees, as be ascertained throughout the sea- diverse as (alkali son, long after the insect is gone. mallow), Rubus (blackberry), Cea- Some species are subcuticular sap nothus, and Quercus. feeders as stem miners or can move Members of the superfamily from one leaf to another via a stem Incurvarioidea insert their eggs by mine. piercing plant tissues with a saw- like ovipositor. Most oviposit into young seed, but species of the fam- ily Heliozelidae are leaf miners. Lar- vae of Coptodisca leave characteristic oval holes by cutting out disks from the upper and lower epidermis after completion of the mine (Figure 3, page 6) and use them to construct a portable case in which they pupate. Sometimes they are conspicuous by their numbers, with many mines per leaf on Salix (), Arbutus (mad- rone), Arctostaphylos (manzanita), and Quercus (oak).

8 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 The family Gracillariidae con- Umbellularia (California bay). An tains the greatest diversity of lepi- introduced European species lives dopterous leaf miners. There are on garden azaleas. about 150 species known in Califor- Elachistid moths specialize as nia, with some remarkable differ- monocot miners. Nearly all Elachista ences in larval biologies. All are min- form linear mines in grass blades, ers, and larvae of most species change while a few species in other genera to a different form in one or more make blotch mines in plants of the late instars. For instance, Caprifoliaceae (Lonicera and Symph- begin as flattened larvae that form oricarpos), or Hydrophyllaceae (Eri- blotch mines beneath the upper side odictyon and ). About 40 epidermis. In the last instar they be- species are recorded in California, come cylindrical caterpillars, and use of which 26 have been named in the silk to buckle the mine roof, creat- past several years, so it is likely that ing a tent-like space in which they many more remain to be discov- pupate (Figure 4, page 6). Species of ered. They are poorly known be- a sister genus, Phyllornorycter, often cause the mines are inconspicuous, using the same host plant, make simi- and because the adults fly at sun- lar mines—usually inside the lower down and dawn (they are not often epidermis—and do not change their attracted to lights), thus avoiding body form. Species of both genera most collectors. occur on a wide variety of shrubs and trees, including oaks, willow, Caprifoliaceae (honeysuckle and CASE-BEARERS snowberry), madrone, Gaultheria shallon (salal) and other Ericaceae, Some caterpillars make portable and various . Members of cases from which they feed. This the similar genus behavior evidently has originated make bloated blotches in the leaves several times, since it occurs both of Baccharis pilularis (coyote brush), in primitive moths (superfamily Artemisia douglasiana (mugwort), Incurvarioidea) and in - Isocoma and Hazardia (goldenbush), arily more recent groups ( and related plants. and ). Early instar lar- Marmara larvae are extremely vae of Adelidae (long-horned fairy modified, with flattened head and moths) leave the developing seed mandibles and are sap-feeders just where the eggs were inserted, form under the cuticle, creating very long, portable cases of silk covered with convoluted mine tracks that gradu- debris (Figure 7, page 7), and feed ally enlarge (Figure 5, page 6). They on fallen leaves. California species occur on broad-leafed plants such include specialists on Linanthus, as Arbutus, in stems of Opuntia cac- Castilleja or Orthocarpus (’s clo- tus, Rubus (blackberry), , ver), Platystemon (cream cups), Gilia and other plants. capitata, and Holodiscus (oceanspray). Species of Caloptilia (Figure 6, Psychidae are called “bag- page 6) mine in early instars, then worms” because most species con- change form, emerge, and form an struct sack-like cases covered with external shelter by folding a leaf tip in a characteristic manner, within 12, Woody stem gall induced by Gnori- which they graze. After completing moschema baccharisella () on growth, the larva leaves to pupate Baccharis pilularis (coyote brush) (top). • in a silken hammock constructed 13, Soft-stem galls caused by G. grinde- liae on hirsutula (gumplant) nearby. Caloptilia are host specific (middle). • 14, Adult of Epiblema rudei and occur on many kinds of trees () and its pupal shell protrud- and shrubs, including Acer (), ing from stem gall on Gutierrezia (match- Quercus, Salix, Toxicodendron, and weed) (bottom).

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 9 Figures 15 and 16: -feeders. 15, Stem-boring caterpillar of Grapholita edwardsiana (Tortricidae) (above) on Lupinus arboreus (bush lupine). • 16, maculata () -carrying female (left) depositing an egg in flower of Yucca whipplei (our lords candle).

bundled stacks of leaf or flower bits, ened by bacterial cankers or other and so on. The larva mines from the damage. attached case as far as it can reach, Sesiid moths (Figure 10, page then moves to a new site, leaving a 8) are day-flying and colorful, re- series of characteristic circular mines sembling wasps and bees with fragments of the host plant, such as with a round hole off-center. mostly transparent wings. There are grass, sticks, or leaves. The family They are host-specific on a va- about 30 species in California, all of is diverse in the southeastern US, riety of angiosperms, including them specific feeders on particular but only a few species are known in Alnus, Aster, Baccharis, and other plants. The larvae bore in root California. Hyaloscotes fumosa in the , and in the inflorescences crowns of Asteraceae, Eriogonum Sierra has been recorded of Lotus, Grindelia, sedges, and other (buckwheats), bark of conifers, feeding on Purshia (antelope brush) plants. Typically the case is enlarged stems of blackberries, and many and Arctostaphylos. Most psychids are basally as the larva grows, in the other hosts. general feeders, but Thyridopteryx manner of mollusk shells. However, Many Tortricidae, especially meadii in the Mojave Desert is host- Coleophora glaucella mines leaves of Eucosma and Phaneta with more than specific on Larrea (creosote bush) Arctostaphylos and makes its cases by 120 species in California, are root (Figure 8, page 7). An introduced cutting out linear pieces of upper and root crown borers, mostly in European species, Atperona helix, and lower epidermis, replacing them woody Asteraceae (Chrysothamnus, which appeared in El Dorado with successively larger ones dur- Gutierrezia, Isocoma, etc.). Some County in 1950, has spread widely ing growth. Phaneta bore into buds or terminal through the and east- twigs of herbaceous perennials (Ar- ward, feeding on numerous low- temisia, , Gnaphalium), growing plants such as ROOT AND STEM as do Rhyacionia in pines. Larvae of (mules ears), in cases that resemble BORERS Petrova feed in terminal branches miniature snail shells covered with of pines and other conifers, creat- mud. Its spread is remarkable be- Many moth larvae live entirely ing a nodule of pitch and frass (in- cause the population is entirely par- inside roots or stems. The primi- sect excrement) around themselves thenogenic (reproduces without tive ghost moths () are (Figure 11, page 8). males) and flightless; the larviform large but broadcast tiny spherical females oviposit in their larval cases, eggs in appropriate habitats. Lar- and dispersal occurs by wind-blown vae enter the ground and feed on PLANT GALL first instar larvae on silken strands. roots externally, or burrow into FEEDERS make up the larg- them and continue up into the larger est group of case-bearers; 1,000 branches of coastal bush lu- Galls are a specialized kind of species are estimated for North pines and other plants. Goat moths reaction by plants to wounding America, 85% of them unnamed, () are similarly robust, and caused by the presence of insect and there are probably 200–300 in their larvae bore into root crowns larvae, which results in a species- California. The cases are highly vari- of woody shrubs such as Suaeda (al- specific form of enlargement of a able in form, cigar-shaped (Figure kali blite) in the Central Valley, or leaf or stem. Larvae of gall-induc- 9, page 7), slender and curved, feed in larger limbs in trees weak- ing species live in the galls, feeding

10 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 on the continually growing tissue. In California gall induction by Onagraceae. Stagmatophora (Cos- Most galls are caused by “gall Lepidoptera is most prevalent in mopterigidae) induce gall-like midges” (Diptera, Cecidomyiidae), Gelechioidea, in the families Cos- swellings in stems or roots of on herbaceous and woody plants, mopterigidae, , and (bluecurls and turpen- such as the amorphous tip galls of Gelechiidae. Species of Mompha tine weed). Baccharis pilularis. Next most nu- cause several different forms of tip Some members of Gnorimo- merous are galls caused by cynipid and stem galls on Epilobium canum schema (Gelechiidae) cause tip or wasps (Hymenoptera), primarily on (California fuchsia), while other stem galls in Asteraceae (Aster, Quercus and Rosaceae. Gall induc- Mompha bore into growing tips or Baccharis, Ericameria, Grindelia, tion by lepidopterans is less com- stems without gall induction in Isocoma) (Figures 12, 13, page 9), mon but has evolved several times Epilobium (fireweed), Oenothera whereas other Gnorimoschema feed in unrelated superfamilies. (evening primrose), and other as leaf miners or externally on bur- ied leaves of Ambrosia and other Figures 17 and 18: External feeding caterpillars of macro moths. Camouflage colora- plants in active sand dunes. Several tion in Juniperus-feeding caterpillars. 17, an unidentified inchworm (Geometridae) tortricid moths in the genus Epi- (below). 18, Abagrotis mirabilis () (bottom); there are similarly patterned blema also cause stem galls in caterpillars of several other families, characteristic of Cupressaceae-feeders. Asteraceae (e.g., in rhizomatous stems of Ambrosia, or woody stems of Gutierrezia) (Figure 14, page 9). A few species are regular intrud- ers (called ) in galls caused by other insects. Thus Cydia lati- ferreana (Tortricidae) feeds in “” galls, such as on Quercus lobata (valley oak), which are caused by cynipid wasps, while larvae of Batrachedra (Coleophoridae) eat the contents of the red willow leaf galls induced by a (Hymenoptera, ), moving from gall to gall as they are depleted.

INFLORESCENCE- FEEDERS

Many lepidopteran caterpillars eat flowers preferentially when available, such as generalist “woolly ,” which are the caterpillars of tiger moths (Arctiidae) that feed on low-growing annuals. Others are specialist feeders in inflorescences. Examples include a suite of Ethmia species (Ethmiidae) that fly in early spring and depend upon flowers and young seed of annual borages (Am- sinckia, Cryptantha) and a scroph, Collinsia heterophylla (Chinese houses). This food source is more reliable than foliage during poor rainfall years. Related ethmiid spe- cies feed on leaves of hydrophylls (Eriodictyon, Phacelia) later in spring or summer.

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 11 of legumes are a rich resource for by the misshapen foliage. Large insect larvae, and Astragalus (loco- numbers of species in several fami- weed) is particularly favored, with lies (e.g., sensu lato, at least three common species of Gelechiidae, , Tortri- pyralid moths (Etiella, Pima), a cidae) feed in this manner, usually butterfly (, Everes), and as host plant specialists, on an enor- Grapholita vitrana all boarding mous array of conifers, dicots, and there. monocots, including virtually every The most celebrated instances . of obligate seed-feeding and plant- Larger moths and butterfly cat- insect mutualism are species of erpillars, by contrast, mostly feed Tegeticula (Prodoxidae), females of exposed. They depend on an amaz- which have specialized mouthparts ing array of cryptic forms, colors, used to gather pollen of Yucca, which and behavior to elude predators. they purposefully transfer to the Often the highly cryptic caterpil- after they oviposit into the lars remain exposed when at rest, flower’s ovary. exactly matching foliage colors (Fig- Tegeticula females (Figure 16, ures 17 and 18, page 11). Some are page 10) deposit only a few eggs covered with brown patches that per flower, probably regulated by a resemble necrotic spots of leaves. pheromone signal to sisters, and The “trash-carrying” species are the resulting larvae eat only a por- covered with flower fragments at- tion of the seeds. Caterpillars of tached by hooked setae on their the related genera Prodoxus, Aga- backs (Figure 19, left). Others stand venema, and Mesepiola burrow in erect mimicking a twig (Figure 20, sterile tissues of capsules and stalks page 13). of Yucca, Agave, and Nolina respec- Many less cryptic caterpillars tively, with three Prodoxus species feed only at night, thus avoiding partitioning the niche in Y. whipplei heat, desiccation, and daytime Figures 19-22: External feeding in California. predators. Still others are protected caterpillars of macro moths (this page and by modified hairs or spines that dis- facing). 19, Trash-carrying inchworm, charge urticating chemicals that can Synchlora species (Geometridae) (top), EXTERNAL FEEDING cause respiratory inflammation or adorned with fragments of its host flower, CATERPILLARS skin rash in humans, for example, Helenium (sneezeweed) from Virginia. • 21, Larva with urticating spines, Hemi- caterpillars of Californian buck leuca eglanterina () (bottom), a Leaf miners, case-bearers, root moths (Saturniidae, ) (Fig- generalist feeder. and stem borers, including gall in- ure 21, left). Species in several moth ducers, are estimated to comprise families protect themselves by con- Larvae of one species of about 15% of described North structing communal shelters of Grapholita (Tortricidae) specialize American Lepidoptera, a propor- dense silk, e.g., tent moth cater- in flowers of perennial Lupinus, tion that will rise appreciably when pillars, (Figure 22, while other Grapholita feed on the microlepidoptera are better classi- page 13), from which they forage seed of Lupinus and other legumes, fied and cataloged. Larvae of the and derive protection from climatic or burrow in the inflorescence scape remainder feed externally. About variables. Finally, caterpillars of (Figure 15, page 10). Larvae of 40% of these are microlepidoptera some species do not hide but are the related genus Cydia mostly are that live concealed, usually in shel- protected by toxic chemicals they seed feeders, including the notori- ters constructed by tying leaves or sequester from the plants they eat. ous codling moth, the “worm” in other plant parts together with silk. apples, and the Mexican “jumping Typically, concealed feeding bean,” which is a carpel of a Croton caterpillars are small, green or GENERALISTS OR (Euphorbiaceae) that hops about brownish, with little or no integu- SPECIALISTS? when warmed, caused by quick mental pattern other than a dark movements of the larva inside it. head. They feed within or forage Leaf miners and root or stem Several species of Cydia infest pine outward from the shelter, often at borers, especially those that cause cones in California. Seed capsules night, and are most easily detected galls, usually are highly specific, of-

12 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 ten restricted to one or a few closely- populations, but in others it selects to the evolution of complex “model- related species. Concealed feeders willow or even Douglas-fir. mimic” associations among insects, often feed on several plant species Many different plant families especially in tropical regions. The or genera, and there is no precise have evolved natural plant chemi- pipevine family, Aristolochiaceae, definition of host plant specialist cals that typically are repellent to provides a classic example. Swal- versus generalist. Students of plant- vertebrates and to non-adapted in- lowtail butterflies of several genera insect relations sometimes refer to sects. As a result, even the broadest have adapted to its chemicals, all species that feed on unrelated spectrum generalists do not feed on represented in California by the plants as polyphagous (eating all kinds of plants. For example, beautiful blue and orange-spotted many), but in reality the situation is Brassicaceae (mustards) harbor pipevine swallowtail, Battus phile- more complex. specialist guilds of Lepidoptera nor. Caterpillars and adults of this Some species feed on an array (plutellid moths and pierid butter- of angiosperms, or conifers, some flies), but rarely are used by polypha- even on both, but rarely does their gous species. (legumes) diet include monocots, which serve as hosts for many Lepidoptera, mainly serve specialists with modi- especially the seeds, but general fied mandibles. The Argyrotaenia feeders are deterred. franciscana complex (Tortricidae) in Many macro moth and butter- is a good example; fly specialists feed on plants charac- larvae have been found on a vast terized by toxic chemicals that array of angiosperms, both woody render them distasteful or eremetic and herbaceous, native and exotic, to vertebrate predators, which learn and occasionally on conifers. Even to recognize the bright (aposematic) within populations, A. franciscana is colors of these insects. This has led polyphagous, recorded on 24 spe- cies of plants in 15 families at the UC Big Creek Reserve in Monterey County. These include Sequoia (coast redwood), Cupressus macro- carpa (Monterey cypress), and the succulents, Sedum (stonecrop) and Dudleya, feeding in the inflores- cences. On San Miguel Island, A. franciscana insulana larvae have been found on 22 species, which is 10% of the flora, but not on monocots. A common pattern for tree- and -feeding macro moth cater- pillars (Geometridae, Noctuidae, etc.) is use by individual species of unrelated families, including Betulaceae, Fagaceae, Rosaceae, and Salicaceae, but not non-toxic her- baceous plants. Alternatively, poly- phagy may vary spatially or tempo- rally. Some species, such as certain silk moths (Saturniidae) and sphinx moths (), are generalists over their broad ranges but special- ists at any one locality or in a par- ticular season. For example, the giant silk moth euryalus, in California, sometimes called the 22, Tent moth larvae of Malacosoma californicum (Lasiocampidae) (top) on Quercus agrifolia “ceanothus silk moth,” shows strong (coast live oak). • 20, Stick-like larva of Synaxis truxaliata (Geometridae) (bottom) on preference for Rhamnaceae in many Baccharis pilularis (coyote brush).

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 13 species are distasteful to birds and sure before feeding. One example in plants helped lead Paul Erhlich and advertise their presence by their dis- California is Apocynum (dogbane), Peter Raven in the 1960s to pro- tinctive aposematic color pattern eaten by a pyraloid moth (Saucrobotys pose the concept of . (photograph, page 5). Several non- futilalis). Another is Asclepias (milk- The butterfly acting as parasite toxic nymphalid butterfly species weed) eaten by specialized arctiid induces changes in plant chemis- have evolved resemblance to the moths (Euchaetes) and danaid but- try, leading to reciprocal adapta- color pattern of Battus, including terflies (monarchs and queens) (Fig- tions in a step-wise fashion. The species of Limenitis that feed on wil- ure 23, below), which have willow- term, however, over time has been lows, females of Speyeria diana feeding mimics (Limenitis, Nympha- applied to a much broader array of (Diana fritillary), a Viola feeder, as lidae). Some members of the plant relationships, diminishing its use- well as some females of yellow swal- families Convolvulaceae, Euphor- fulness. lowtail butterflies. biaceae, and Asteraceae similarly In any event, the study of inter- Numerous chemically dissimilar produce repellent milky toxins that relations between plants and their plants have evolved secretory canals serve as the basis for specialization caterpillars is a fascinating and fer- containing latex or resin, and dis- and speciation in Lepidoptera, while tile field for investigation. We are charge viscous, often toxic, “milky” remaining free of generalist cater- still a long way from answering most fluids when cut by herbivores. Cat- pillars. of the questions raised by our cur- erpillars in several families overcome Indeed, the close association rent store of knowledge. this by severing the canal basally on between pierid butterfly species and the leaf, thus lowering the fluid pres- their mustard and legume host ACKNOWLEDGMENTS Figure 23. Aposematic butterfly caterpillars rendered distasteful to vertebrate predators by the chemistry of their host plants. Danaus plexippus (monarch butterfly) is shown here I thank Gordon Frankie, Paul on Asclepias fascicularis (narrow-leaf milkweed). Opler, and Dan Rubinoff for com- ments on the manuscript.

REFERENCES

Ehrlich, P.R, and P. Raven. 1964. But- terflies and plants: a study in coevo- lution. Evolution 18: 586–608. Jermy, T. and A. Szenti, eds. 1991. Insects and plants. S.P. Bakker Aca- demic Publications, The Hague, The Netherlands. Powell, J.A. 1992. Interrelationships of yuccas and yucca moths. Trends in Ecology and Evolution 7:10–15. Powell, J.A., C. Mitter, and B. Farrell. 1999. Evolution of larval feeding preferences in Lepidoptera. In Lepi- doptera, Moths and Butterflies, ed. N.P. Kristensen, 403–422. Vol. 1 of Evolution, Systematics, and Biogeogra- phy. Handbook of Zoology, Vol. 4 of Arthropoda: Insecta, Part 35. W. de Gruyter, Berlin and . Stamp, N.E. and T. Casey, eds. 1993. Ecological and evolutionary constraints on caterpillars. Chapman and Hall, New York.

Jerry A. Powell, Essig Museum of Ento- mology, 201 Wellman Hall, University of California, Berkeley, CA 94720. powellj@ nature.berkeley.edu

14 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Oak apple gall ( quercuscalifornicus) on valley oak (Quercus lobata). Photograph by K. Schick.

CYNIPID-INDUCED GALLS AND CALIFORNIA OAKS by Katherine N. Schick

atching a tiny female Suddenly, a gust of wind sweeps ing plant growths called galls, filled WAndricus fullawayi wasp the tiny wasp into the branches of a with nutritive tissues. The galls through a magnifying nearby valley oak (Quercus lobata) provide food and shelter for the glass, I am amazed at the amount of and she is lost to sight. I wonder developing larvae of the wasps. time she spends carefully grooming where this tiny creature is going, Oak gall wasps are members of her wings and antennae with the and whether her offspring will de- the insect order Hymenoptera, fam- special combs on her front legs. As velop within a gall on the stem, leaf, ily Cynipidae, and tribe . I wait anxiously to see where she flower, or root of an oak tree. Unlike bees, , and stinging will fly to lay her eggs, she crawls Like many other cynipid wasps, wasps, in which the ovipositor has awkwardly, brushing her antennae this tiny, ungainly female is smaller evolved into a stinger, cynipid wasps against the twig to test its odors. than this typeset number “1,” yet have retained ovipositors with which She takes her time. More than 20 she and other gall wasps have man- they can carefully position their eggs minutes elapse after I release her aged to colonize every native oak inside plant tissues without harm- from the rearing container before tree species in California. They trick ing any plant cells. she finally becomes airborne. their host trees into forming strik- The most primitive living

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 15 relatives of modern cynipid wasps tionary history, ancestors of cynipid gets as big as a baseball and may use their long ovipositors to lay eggs wasps began to skip the insect host contain as many as 16 developing into the larvae of wood-boring and consume plant tissue directly larvae. The galls generally start wasps and beetles, much as their through gall induction. The oldest forming in early spring and grow earliest ancestors probably did. known cynipid galls, approxi- into round green spheres that re- From such primitive ancestors two mately 115 million years old, are semble juicy green apples, even to modern families of wasps evolved: found in deposits. the point of developing a reddish , which parasitize the lar- Regular readers of Fremontia will blush when they mature. The color vae of flies, lacewings, and other be familiar with some of the exotic quickly fades and the drying galls wasps; and Cynipidae. and bizarre shapes of modern turn beige during the summer. The Apparently early in their evolu- cynipid galls on blue oak (Quercus wasps within finish pupation and douglasii) from the excellent photo- emerge as adults in autumn, leav- Wasp of Andricus quercuscalifornicus graphs in an article over a decade ing the gall behind on the tree. (top) on gall. • Spindle gall (bottom), ago by Russo (1990). Each species After the first year, old galls turn unisexual generation of Heteroecus paci-ficus, of cynipid wasp induces its oak host black, covered in sooty mold. on Quercus vaccinifolia (huckleberry oak). Photographs by K. Schick. to form a unique shape of gall. While many other gall-inducing insects, such as tenthridinid wasps, ALTERNATION OF inject chemicals into plant tissue GENERATIONS along with their eggs so that gall formation begins before larvae Distinctly different galls—often emerge, gall induction in Cynipidae on different parts of the host tree— begins in response to chemicals se- are produced not only by different creted by growing wasp larvae. wasp species, but also by different Cynipid galls are more complex generations of the same cynipid spe- than galls of many other insects. cies. Most cynipid species in the They contain several tissue layers oak-galling tribe Cynipini have two and a separate central chamber for alternate generations each year: a the developing larva. Cynipid lar- bisexual generation with both males vae complete their development by and females developing in spring becoming pupae and then adults galls, and a unisexual generation of before they emerge from their galls only females in autumn galls. This to lay eggs for the next generation. phenomenon of alternating genera- Galls may contain a single larva, tions is called heterogony and results as do those of the jumping gall in females so different from those Neuroteras saltatorius, a tiny spheri- of their alternate generations that cal structure about the size of this many were originally described as “o” which forms on the underside separate species, sometimes even in of oak leaves. These tan-colored separate genera. galls hop up and down under Quercus The unisexual generation of the lobata oaks from June through Au- wasp Antron douglasii produces strik- gust in the Central Valley of Cali- ing pink star-like spiny turbans in fornia. The dropping galls jump summer on the leaves of Quercus around for a while after they fall lobata, Q. dumosa (Nutall’s scrub from the leaves, eventually maneu- oak), and Q. douglasii. The bisexual vering themselves into crevices in generation of this wasp produces the ground where they will endure twig galls that look like large white the winter, and from which the adult semi-translucent mistletoe berries females will emerge in early spring. in early spring, later fading and Other cynipid galls may con- hardening to woody knobs. Wasps tain more than one larva such as emerging from these spring galls the large “oak apple” gall induced were first placed in the genus on Quercus lobata by the wasp Dryophanta because they looked so Andricus quercuscalifornicus (see pho- strikingly different from their al- tograph, page 15). This stem gall ternate generation.

16 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 for the remaining cynipid species lay their eggs. When lar- in California will require a lifetime vae emerge they may consume all of study. the nutritive cells, starving the gall- inducer. Some species may even deliberately kill the gall-inducing A COMMUNITY OF larva in order to consume its food WASPS IN AN OAK resource. GALL A very few cynipid inquilines actually induce changes in the shape At first glance, an oak gall might of the gall, indicating that they have seem an ideal refuge from preda- not entirely lost the ability to se- tors and other dangers to young crete appropriate chemicals. One larval insects. Oak galls are espe- such inquiline species in the genus cially rich in tannins, much more so Synergus causes unisexual galls of than normal plant organs, so the Heteroecus pacificus forming on ei- gall tissue should not be especially ther Quercus chrysolepis (canyon oak) attractive to plant-eaters. However, or Q. vaccinifolia (huckleberry oak) these galls cannot move so they are to change from a narrow spindle Jumping gall, the unisexual generation predictable food resources, attract- shape to a rounded globular shape. of saltatorius, under Quercus lobata ing herbivores as well as insect-eat- I have dissected these galls and leaf. Photograph by K. Schick. ers. Also abundant in oak galls are found as many as five larval cham- two other groups of wasps: herbivo- bers for the smaller inquiline wasps Surprisingly, even though their rous inquiline (“guest”) cynipid around a single central chamber for homes are so distinctive and thus wasps and very specialized parasi- the larger gall-inducer, all of which the insects should be easy to locate, toids in the superfamily Chalci- scientific knowledge of the doidea. fauna in California is far from com- The inquiline wasps all belong plete. Many oak galling species have to the tribe within the yet to be described, and alternate family Cynipidae and appear to have generations are currently known for lost the ability to secrete gall-in- fewer than a fourth of the 122 de- ducing chemicals. Instead, they lo- scribed California species. cate developing galls into which they In the British cynipid fauna, which is well known, some cynipids Oak apple gall (Andricus quercuscali-fornicus) species are known to have alternate (right), on valley oak (Quercus lobata). • generations on separate oak tree Three galls on leaf of Quercus lobata (below): clockwise from tip, Antron species, as well as strikingly differ- douglasii, Xanthoteras clavuloides, and Besbicus ent morphologies and colors with conspicuus. Photographs by G. Frankie. size ranges differing more than five- fold. After many years of caging Andricus quercuscalifornicus wasps on young oak trees, which then pro- duced new oak apple galls within these cages during the second year, I suspect this species has lost its alternate generation. If an alternate generation does exist, the adults must be significantly smaller than the unisexual generation and must induce inconspicuous galls on stems or leaves. Only after several more years of study will we truly under- stand heterogony for this single spe- cies. Finding alternate generations

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 17 apparently matured and emerged munity of wasps. However, prob- instead of gall-inducers. When my as adults. lems can arise when individual trees Canadian colleagues have made are similar to preda- are diseased or stressed. similar collections on Vancouver Is- tors in that they kill their host ani- quecussuttoni, a com- land, they find far lower rates of mal, and they are also similar to mon gall wasp on Quercus agrifolia parasitism in galls, which they be- parasites in having a single host ani- (coast live oak) and Q. wislizeni (in- lieve is a result of their cooler, wet- mal for their entire lifetime. The terior live oak) forms a large spheri- ter weather. Death of these Cana- majority of chalcid parasitoids found cal stem gall slightly smaller than a dian trees may also be related to the in oak galls lay their eggs in cynipid tennis ball in the center of a twig. recent introduction of two species larvae. The growing larvae of the This gall appears to block vascular of oak phylloxera to western Canada. parasitoids slowly consume devel- tissues, and frequently all of the The Vancouver Island oak- oping cynipid larvae or pupae. branch extending past the gall dies. cynipid interaction is an extreme These wasps come in an amazing At any given time many Quercus exception to the norm of gall wasp array of forms and colors, and I am agrifolia trees along the coast in and host tree interactions. Califor- constantly amazed at the number of Monterey County will be growing nia cynipid galls provide colorful different species found several of these galls and appear and spectacular decoration to our on each cynipid species. rather ragged. But the majority of oak woodlands, costing trees only a One of my favorite oak gall para- cynipid galls are not nearly so stress- tiny fraction of the energy they gain sitoids, Torymus californicus, belongs ful to the host tree as is this species. through photosynthesis and provid- to the calcid wasp family A very unusual situation has re- ing homes for a diverse and inter- and can be reared from Andricus cently developed in Canada. Since esting wasp community. quercuscalifornicus oak apple galls. 1986, people on Vancouver Island The female of this species is a me- have observed a tragic interaction tallic coppery red with a long, pin- between their Garry oaks (Quercus REFERENCES like ovipositor extending twice the garryana) and the jumping gall wasp, length of her body. The long ovi- Neuroterus saltatorius. The jumping Csóka, G. et al. 1998. The biology of gall- positor allows the female parasitoid gall wasp had moved north into this inducing . Forest Service, to lay her egg directly into the area only a few years earlier and for US Department of Agriculture, St. cynipid larva deep in the gall. The reasons still not clearly understood, Paul, MN. male of this species is metallic green it induces many galls to form close Duncan, R.W. 1997. Forest pest leaflet and much smaller than the female. together on Garry oak leaves. No. 80: Jumping gall wasp. Pacific Forestry Centre, Victoria, BC. These parasitoids emerge from old The brown spots of necrosis Meyer, J. 1987. Plant galls and gall oak galls in late spring after the around each growing gall are not a inducers. Gebrüder, Borntraeger, season’s galls are nearly half their problem in California, where these Stuttgart, Germany. mature size. same wasps induce only a few galls Redfern, M, and R.R. Askew. 1992. on each leaf, but they cause entire Naturalists’ handbooks 17: Plant galls. leaves to die when galls grow too Richmond Publishing Company, EFFECTS ON THE densely in Canada. Some of the Slough, England. OAKS Vancouver Island Garry oaks actu- Russo, R. 1990. Blue oak: A gall wasp ally lose all their leaves mid-sum- nursery. Fremontia 18:68–71. A quick glance at any California mer as a result of this abundance of ——. 1979. Plant galls of the California woodland will reveal some oak trees galls, and even a formerly healthy region. Boxwood Press, Pacific with numerous galls while neigh- tree will die after two or three years Grove, CA. Shorthouse, J.D., and O. Rohfritsch. boring oak trees remain virtually of mid-summer leaf loss. Many heri- 1992. Biology of insect-induced galls. gall-free. Scientists are only begin- tage trees have died as a result. Oxford University Press, New York, ning to understand the mechanisms There seems little danger that NY. gall wasps use to turn on certain the Canadian problem with Weld, L.H. 1957. Cynipid galls of the plant genes with auxin-like chemi- Neuroterus saltatorius will ever occur Pacific Slope. Privately printed, Ann cals, and the corresponding immune in California. One major difference Arbor, MI. response of the trees. While there between Californian and Canadian is an energy cost to the oak tree that populations of this wasp is the per- Katherine N. Schick, Essig Museum of grows galls, most healthy oak trees centage of galls that are parasitized. Entomology, 201 Wellman Hall #3112, have more than enough energy left When I have collected and reared University of California, Berkeley, CA, over from photosynthesis to spare these galls in California, 80 to 90 94720-3112. [email protected]. tissue and sugar to shelter a com- percent of the galls yield parasitoids edu

18 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 BARK BEETLES INFESTING CALIFORNIA’S CONIFERS by David L. Wood and Andrew J. Storer

ark beetles (Order Coleoptera; be found colonizing cones, branches, Dendroctonus jeffreyi, only colonizes BFamily Scolytidae) colonize limbs, trunks, and roots (Furniss and Jeffrey pine (Pinus jeffreyi) while the most trees and other woody Carolin 1977). red turpentine beetle (D. valens) plants throughout the world. There For example, on ponderosa pine colonizes most pine species in Cali- are in excess of 6,000 named spe- (Pinus ponderosa), the ponderosa pine fornia. Some species typically colo- cies with about 477 species occur- cone beetle (Conophthorus ponderosae) nize trees in certain size classes. ring in the United States (S.L. colonizes the cones (see photograph, Thus, the California five-spined ips Wood 1982). More than 170 spe- page 22); the twig beetle (Pityoph- infests young, pole-sized trees, while cies in 44 genera are found in thorus confertus) colonizes small the western pine beetle infests large California’s forests and woodlands branches; the western pine beetle mature and overmature trees. (Bright and Stark 1973). (Dendroctonus brevicomis), and the Bark beetles play an important California five-spined ips (Ips para- role in forest succession (natural confusus) feed on the phloem of the HISTORY changes that occur in the forest plant larger branches and trunk; the am- community over time) and in the brosia beetle (Gnathotrichus sulca- In the spring and early summer decomposition of woody plant ma- tus) tunnels into the xylem and feeds of 1899, Dr. A.D. Hopkins, then terial. While some bark beetle spe- on fungi growing in the maternal vice-director and entomologist of cies may reach epidemic levels and gallery; and another bark beetle the West Virginia Agricultural Ex- cause tree mortality over thousands (Hylastes macer) infests the roots. periment Station, conducted a re- of hectares, most species escape no- Bark beetles vary greatly in the connaissance trip to investigate tice because of their cryptic habits. number of tree species infested. For insects injurious to forests of Cali- They are one of only a few insect example, the Jeffrey pine beetle, fornia, , , and families that, as adults, penetrate their hosts in order to feed, mate, Extensive white fir (Abies concolor) mortality caused by the fir engraver beetle, Lake and reproduce. In so doing they Tahoe Basin, 1991. Photograph by D.C. Perkins. introduce fungi (either directly or indirectly) that are capable of de- grading plant cell walls and thus help recycle nutrients from trees. Only a few species in the genera Conophthorus, Dendroctonus, Ips, Scolytus, and Trypodendron are con- sidered pests (see photograph at right). Most research over the past three-quarters of a century has been directed at these destructive pests. There is very little information on the biology of the remaining species other than , geographic and host range, and gallery patterns (Bright and Stark 1973). Some conifer-feeding bark beetles confine their feeding activi- ties to xylem (sapwood), phloem (nu- trient-transporting tissue in inner bark), or outer bark, and produce distinctive gallery patterns (see pho- tographs, page 21). Bark beetles may

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 19 . On the day after his arrival mologist for the US Bureau of En- trees, or a directed process in which in San Francisco (April 17, 1899), tomology, estimated losses of the they land preferentially on host ver- he visited the University of Califor- “. . . longest and finest western yel- sus nonhost trees and on weakened nia at Berkeley. low pines . . .” due to D. brevicomis versus healthy host trees. Hopkins notes: “I called on Pro- at 300 million board feet per year Concentration begins with the re- fessor Woodworth, entomologist, in California. He stated that “. . . in sponse to attractive pheromones and Prof. J.B. Davy, botanist of the some localities particularly favor- (chemicals secreted by individuals Agricultural Experiment Station, able to the beetles . . . loss for the of one species that stimulate be- who offered every facility and gave year may represent as much as ten havior or development of individu- valuable assistance in my study of percent of the pine stand” (Keen als of the same species) that are the native forest trees represented 1928). produced by beetles feeding or in the university arboretum. Here I tunneling in the host. Depending collected numerous species of on species, individuals of either sex Scolytids from the pines and other CHEMICAL ECOLOGY or both sexes may produce phero- conifers.” mones, tunneling may occur in the In his first reference to the west- Bark beetles usually infest trees phloem or xylem, and host com- ern pine beetle, he writes: “One that are dead, or that are under some pounds released during attack may species which I have provisionally form of stress. However, apparently enhance or reduce the effect of the identified as Dendroctonus brevicomis healthy trees may be killed by some pheromones. This concentration Lec. was found to be a most de- species. Bark beetles use a complex phase continues beyond the begin- structive enemy of the yellow pine chemical communication system to ning of the establishment phase (Pinus ponderosa) in northern Cali- locate a new host, upon which they because of continued pheromone fornia, southern and eastern Or- can feed, mate, and reproduce (D.L. production and release. Termina- egon, northeastern Washington, Wood 1982). tion of this phase occurs when and western Idaho. A large amount They have evolved a pheromone antiattractants are released or no of the finest timber in all of these that elicits behavior resulting in ag- more aggregation pheromones are localities had died within the past gregation of the population on the produced. seven or eight years, evidently as a new host. This population aggre- direct result of attacks by this bark gation must be both timely and, Establishment (for tree-killing spe- beetle.” with tree-killing species, of a suffi- cies) begins when sufficient fungal Although first described by cient magnitude to exploit the new inoculum has been introduced into LeConte in 1876, this species was resource. As a result of their capac- the xylem to assure death of the not considered distinct from the ity to kill living trees, often over tree, so that beetle mating, gallery southern pine beetle, D. frontalis, very large areas, bark beetles influ- excavation, and oviposition can oc- until Hopkins observed it on this ence age, size, and species distribu- cur. The number of beetle attacks trip: “Just as D. frontalis has proven tions, and thus are a significant fac- and when and where they occur de- to be the most destructive enemy of tor in forest succession. termine the effectiveness of the fun- Eastern conifers, the Western rep- The process of host coloniza- gal inoculum in overcoming tree resentative of this species will doubt- tion has been divided into four resistance. With species that do not lessly prove to be, under similarly phases: dispersal, selection, concen- kill trees, this phase begins with the favorable conditions, equally as de- tration, and establishment (D.L. first pairing of sexes in the new host structive to the Western forests in Wood 1982). These phases are de- or when inseminated females begin which the conifers permeate.” fined as follows: tunneling into the host. This phase Thus, Hopkins was the first to ends when elongation of egg gal- Dispersal begins with emergence record the habits and hosts of the leries and oviposition cease. from the brood tree and ends with a western pine beetle. He observed response to host stimuli and/or at- further, “. . . It [western yellow pine] tractive pheromones. has in Dendroctonus brevicomis a most INTERACTIONS WITH pernicious enemy, which penetrates, Selection begins with the response THEIR HOSTS and excavates winding galleries to host stimuli prior to (or after) through the living bark of the finest landing on the tree, and ends with Healthy trees have mechanisms trees, thus speedily causing their sustained feeding in the phloem. to defend themselves from attack death.” Host selection is either a random by bark beetles. Resin pressure, Hopkins’s words were pro- process in which beetles land indis- flow, composition, and crystalliza- phetic. In 1928, F.P. Keen, ento- criminately on host and nonhost tion rates may each be involved in

20 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 the determination of whether an of tree-killing bark beetles. For ex- story of these species, as well as a attack is successful or not. Other ample, at the Blodgett Forest Re- few scattered ponderosa pines, sugar mechanisms, including those that search Station (University of Cali- pines (Pinus lambertiana), and Dou- are a result of the introduction of fornia at Berkeley) on the western glas-firs (Pseudotsuga menziesii). fungi by the bark beetles, are all slope of the central Sierra Nevada, important in the host-bark beetle logging activities and a fire in the interaction. early 1900s resulted in a pure stand INTERACTIONS WITH Various patterns of forest suc- of ponderosa pine. In the 1960s, OTHER INSECTS cession are related to the activities blackstain root disease became prevalent in this forest and the west- The complex interactions ern pine beetle population increased, among bark beetles and other in- causing extensive tree mortality. sects include those with other bark The bark beetle, Hylastes macer, beetles, with other insects feeding is a vector of the blackstain root on trees, and with predatory and disease pathogen, Leptographium parasitic insects. Bark beetles often wageneri. This beetle apparently se- lects healthy trees which become weakened as disease develops. This pathogen also infects adjacent trees through their fine roots. Western pine beetle aggregates on healthy and diseased trees, resulting in many inoculation sites for bluestain fungi (Ophiostoma minus), and eventually leads to the death of the pines. At the Blodgett Forest Research Sta- tion site, white fir (Abies concolor) and incense cedar (Calocedrus decurrens), both shade-tolerant spe- cies that were growing as small trees in the understory, showed increased productivity after beetle infestation, due to reduced competition from the pines. This resulted in an over-

Examples of gallery patterns produced by bark beetles. • Western pine beetle (Dendroctonus brevicomis) (above). Each winding egg gallery is excavated by one female. The male joins the female soon after she enters the phloem. Eggs are laid in niches in the phloem of the gallery wall. Larvae feed on phloem for the first larval stage, packing frass in their galleries, and then turn out to feed in the outer bark. Photograph by R.W. Stark. • Twig beetle (Pityophthorus spp.) (top right). Maternal galleries radiate from a central nuptial chamber. Larval tunnels radiate from these maternal galleries and are packed with frass. Photograph by P.L. Dallara. • California 5-spined ips (Ips paraconfusus) (middle row, left). Three egg galleries are each excavated by one female. Eggs are laid in niches in the phloem of the gallery wall. The nuptial chamber at the intersection of the three egg galleries is excavated by the male. Larvae feed on phloem until pupation, excavating galleries that are packed with frass. Photograph by T.W. Koerber. • Pine engraver (Ips pini) (middle row, right). Four egg galleries are each excavated by one female. Eggs are laid in niches in the phloem of the gallery wall. The nuptial chamber at the intersection of the four egg galleries is excavated by the male. Larvae feed on phloem until pupation, excavating galleries that are packed with frass. Photograph by A.J. Storer. • Monterey pine ips (Ips mexicanus) (bottom row, left). After leaving the nuptial chamber, the female beetle excavates a “C”-shaped maternal gallery in the phloem laying eggs in groups of 3-4 on the outside of the “C.” Larvae tunnel individually in the phloem, excavating galleries that are packed with frass. Photograph by A.J. Storer. • Fir engraver (Scolytus ventralis). One female excavates two egg galleries which radiate horizontally from a central nuptial chamber (bottom row, right). The male joins the female soon after she excavates the entrance tunnel. Larval tunnels run vertically from the maternal gallery and are packed with frass. Photograph by T.W. Koerber.

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 21 nochila chlorodia (Coleoptera: Tro- gositidae). These predators arrive on the tree with the tree-infesting bark beetles. They consume arriv- ing bark beetles, then mate, lay eggs, and their larvae enter the bark beetle galleries to feed on imma- ture bark beetles and other insects and invertebrates that occur be- neath the bark. Both sexes of the parasitic wasp Tomicobia tibialis (Hymenoptera: ) are attracted by com- pounds that are produced by male Wood 1982; Raffa et al. 1993). The California five-spined ips while compound verbenone is produced attacking ponderosa pines. This by both male and female western wasp inserts eggs into the attacking pine beetles and interrupts response beetles and the wasp larva develops of the California five-spined ips to entirely inside the bark beetle. Again its pheromone. Such chemical in- the compound is detrimental to the teractions confer an advantage to sender of the compound, and is an- the first-arriving species because its other example of a “kairomone.” pheromone will interrupt the at- Other wasps that are parasitic on tractant pheromone of the late-ar- bark beetles, such as Roptrocerus Ponderosa pine cone beetle (Conoph-thorus riving species. Thus competition for xylophagorum (Hymenoptera: Tory- ponderosae) (top). The female beetle tunnels food and space is reduced. This midae) and Dinotiscus burkei (Hy- in at the base of the cone, and then compound benefits the sender and menoptera: Pteromalidae), arrive excavates an egg gallery along the axis of is termed an “allomone.” during the establishment phase, the cone. Larvae feed in the seeds and Bark beetles have a wide range some four to six weeks after initial scales inside the cone. Photograph by T.W. Koerber. • Adult twig beetle of insect enemies that cause mor- attacks have occurred. Parasitoids (Pityophthorus sp.) (bottom) on pine foliage. tality beneath the bark of infested attack their bark beetle hosts, usu- Photograph by A.J. Storer. trees, in addition to other natural ally during the late larval stage. The enemies such as woodpeckers (Stark chemicals to which these parasites exploit trees weakened by other in- and Dahlsten 1970). Several spe- are attracted may result from fun- sects, especially defoliators (Furniss cies of bark beetle predators and gal colonization of the host during and Carolin 1977). In northeastern parasites are attracted to bark beetle the establishment phase. California, for example, white firs pheromones (D.L Wood 1982; defoliated by the Douglas-fir tus- Raffa et al. 1993). Where the chemi- sock moth (Orygia pseudotsugata) are cal signal benefits the receiver, such INTERACTIONS WITH infested by the fir engraver beetle as a predator or parasite, and is det- FUNGI (Scolytus ventralis). Outbreaks of the rimental to the sender (the bark mountain pine beetle (Dendroctonus beetle in this case) in a multi-spe- Bark beetles interact with patho- ponderosae) have been recorded in cies interaction, the compound is genic fungi in a number of impor- lodgepole pines defoliated by the referred to as a “kairomone.” tant ways, including when they act lodgepole needleminer (Coleotech- The red-bellied clerid, Enoclerus as vectors of pathogenic fungi to nites milleri) in Yosemite National lecontei (Coleoptera: Cleridae) is a healthy trees, and when they pref- Park. In these examples, white firs general predator of bark beetles. It erentially colonize diseased trees and lodgepole pines utilize the space is attracted to ipsenol and ipsdie- (Schowalter and Filip 1993). Tree- and light following mortality of the nol, pheromone components pro- killing species in the genera Den- overstory trees to develop into the duced by the California five-spined droctonus, Ips, and Scolytus have a next overstory generation. ips. The compound exo-brevicomin close association with pathogenic Competition for space and re- which is produced by the female fungi. Fungal propagules in the gen- sources may be reduced by inter- western pine beetle, is highly at- era Leptographium, Ophiostoma, and rupting the response of other bark tractive to another predatory beetle, Trichosporium are carried by adults beetles to their pheromones (D.L the blue-green trogositid, Tem- and occur in their galleries in re-

22 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 cently killed trees (summarized in Trees weakened by diseases can shown to be associated with dis- Harrington 1993). be detected by bark beetles (sum- eased trees, and are known to visit Many of these fungi are co- marized in Goheen and Hansen and infest non-diseased trees. Indi- evolved mutualistic fungi that are 1993). In the central Sierra Ne- viduals of these species carry Fusa- only found in association with cer- vada, ponderosa pines infected by rium circinatum propagules, and tain bark beetle species. Their role the fungus that causes blackstain transmission of the pathogen has in the colonization of the host by root disease are predisposed to in- been demonstrated in controlled the bark beetle is not fully under- festation by the western pine beetle. studies. Hence, all of these species stood, but may include helping to Ponderosa pines growing in pure are regarded as vectors of the pitch overwhelm the defenses of the tree stands are killed by the western pine canker fungus in California. by causing a vascular wilt disease, as beetle. Then these stands are re- Other species in the same gen- well as providing nutritional ben- placed by shade-tolerant incense era feeding on Monterey pine are efits to the larvae. These coevolved cedar and white fir, both of which also considered to be likely vectors fungi are often carried inside spe- are apparently immune to this root as they associate with healthy and cialized structures on the bark beetle pathogen. diseased trees, and carry propagules called “mycangia.” The blackstain fungus causes a of the pathogen. Analysis of the Owen et al. (1987) wound- similar root disease in Douglas-fir, native host ranges of the proven inoculated two-year-old ponderosa which predisposes trees to attack vectors and their congenerics (spe- pine seedlings with fungi isolated by the stem-infesting bark beetles, cies of the same genus), and the from three species of Dendrocto- Pseudohylesinus nebulosus and Scolytus geographic distribution of their nus that colonize ponderosa pine: unispinosus, as well as several other hosts, indicate many possible av- Leptographium terebrantis from the species. Root-infesting bark beetles, enues of spread for pitch canker to red turpentine beetle, Ophiostoma Hylastes nigrinus, and H. macer, as the North Coast and Sierra Nevada (=Ceratocystis) minus from the west- well as the weevils, Pissodes fasciatus (Gordon et al. 2001). ern pine beetle, and O. clavigerum and Steremnius carinatus (Coleoptera: from the mountain pine beetle. Curculionidae), are vectors of this Each killed a high proportion of root pathogen to Douglas-fir. While INTERACTIONS WITH the seedlings. Seedling mortality the origins of blackstain root disease ENVIRONMENTAL caused by L. terebrantis was greater are unclear, it is likely that the vec- AGENTS than that caused by the other two tor and predisposition relationships fungi. described above have evolved to- Environmental factors such as This was a surprising result in gether over time. air pollution, drought, windthrow light of the well-known tree-kill- Some bark beetles carry fungi (uprooting of trees by the wind), ing habit of the mountain pine with which they have not coevolved. flooding, and snow breakage can beetle and western pine beetle, and Perhaps the best-known example cause an increase in bark beetle the non-tree-killing behavior of the comes from hardwood forests where population levels, resulting in in- red turpentine beetle. Ophiostoma the exotic Dutch elm disease fun- creased tree mortality. In particu- ips from the red turpentine beetle gus is carried from host to host by lar, the effects of drought have and mountain pine beetle reduced both native (Hylurgopinus rufipes) dramatic impacts on forest dynam- seedling mortality caused by L. and exotic (Scolytus multistriatus) ics. The extended drought between terebrantis and O. clavigerum, re- bark beetles. 1986 and 1992 resulted in greatly spectively. Ophiostoma nigrocarpum In California, the exotic fungus increased levels of tree mortality from the western pine beetle pro- that causes pitch canker, Fusarium caused by bark beetles throughout duced the same result when inocu- circinatum, has developed associa- California. Thousands of bleached lated together with the pathogenic tions with a number of native bark white fir stems are visible today O. minus. beetle species that infest Monterey throughout the Basin, Thus, each of these three bark and other pines in central coast of a result of an epidemic of the fir beetle species carries one patho- California. In many cases, these bark engraver beetle during the ex- genic fungus and one fungus that beetles have been shown to vector tended drought (see photograph, inhibits the effects of the patho- the pathogen to healthy trees (sum- page 19). genic fungus in seedling inocula- marized in Storer et al. 1999). Damage caused by the air pol- tion studies. The same phenomena The California five-spined ips, lutant, ozone, may also predispose were observed when these fungi a twig beetle (Pityophthorus setosus), trees to attack by bark beetles. were inoculated into pole-sized trees and the Monterey pine cone beetle Ozone damage was initially referred (Parmeter et al. 1989). (Conophthorus radiatae), have been to as “X-disease” because the causes

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 23 of chlorotic mottling on pine tion between native bark beetles and tacked is decreased. At the same needles and reduced needle size and this pathogenic fungus results in the time, smaller incense cedar and retention were unknown. These death of cones, twigs, branches, tree white fir growing in the understory symptoms had been observed since tops and ultimately the death of the grow to occupy the space left from the early 1950s in the San Bernar- entire tree. the thinning operation. This in- dino Mountains of southern Cali- creases the diversity of the stand fornia. A relationship between which further reduces the impact of needle symptoms and photochemi- TREATMENT bark beetles. cal air pollutants was subsequently TACTICS AND Treatments aimed at reducing made, and it was found that, as the STRATEGIES bark beetle densities so as to prevent severity of oxidant injury increased, infestations on living trees have uti- the incidence of bark beetle infes- Once bark beetles reach epi- lized techniques including the use of tation by the western pine beetle demic levels and cause extensive insecticides; the use of behavioral and the mountain pine beetle in- tree mortality, treatments aimed at chemicals, such as anti-aggregation creased. Specifically, ozone dam- reducing densities of the beetles pheromones; destroying infested age resulted in reduced resin flow, are futile (D.L. Wood et al. 1985). material by cutting and burning; or which thus facilitated bark beetle Felling and burning infested trees debarking and removal from the gallery excavation in the phloem. or treating them with insecticides forest. These “direct control” or “re- This favored the successful estab- have been attempted, but with little medial” methods have not been lishment of western pine beetle and effect on the course of the epi- proven effective in forest-wide ap- mountain pine beetle in ponderosa demic. plications because treatment effects pines that had been damaged by The symptoms of tree death ap- could not be separated from other photochemical atmospheric pollu- pear quite suddenly as the foliage naturally-occurring mortality agents. tion (Lorio 1993). turns yellow. Valuable lumber can Therefore, these techniques are be recovered from infested trees if rarely used in managing bark beetles they are cut in the same year or the in forests and large plantations. INTERACTIONS WITH year after they were killed. How- However, insecticides are avail- HUMAN ACTIVITIES ever, in spite of early removal of able for treating high-value trees in infested trees, lumber will likely be the urban forest and in camp- Logging activity has undoubt- devalued by bluestrain fungi intro- grounds in forested areas. These edly increased the breeding mate- duced into the tree by the bark compounds are applied to the trunk rial available for root-infesting bark beetles and by tunnels of wood bor- of the tree to prevent tunneling by beetles. This activity may have cre- ing beetles (Cerambycidae, Bupresti- beetles. ated a larger vector population for dae, Scolytidae) and woodwasps A promising and more environ- Leptographium wageneri, with a con- (Siricidae) that colonize trees killed mentally acceptable method utilizes comitant increase in the incidence by bark beetles. Dense, single-spe- “behavioral” chemicals. For ex- of black-stain root disease. Logging cies stands of conifers are especially ample, the Douglas-fir beetle anti- also has probably increased the susceptible to bark beetle infesta- aggregation pheromone has been incidence of annosum root disease tion because growth of these trees registered by the Environmental caused by the root pathogen, Hetero- is reduced by competition for wa- Protection Agency to prevent at- basidion annosum. Freshly-cut stumps ter, nutrients, light, and space. tacks by the Douglas-fir beetle on are colonized by spores of this root Plantations of a single species, individual trees (Ross 2001). It can pathogen. such as ponderosa pine or Douglas- also be used in forest-wide applica- Similarly, human activity is fir, are especially susceptible to bark tions to prevent the infestation of probably responsible for the recent beetle infestation. Manipulation of trees that have blown down. Popu- introduction and spread of the pitch density and species composition is lations of this beetle build up in canker fungus in California. The one of the most valuable strategies fallen trees and then emerge and increasing incidence of this disease available to forest managers to re- infest nearby living trees. is likely a result of increased abun- duce the impact of bark beetles. For Other antiaggregation phero- dance of many potential bark beetle example, by thinning a pure stand mones such as ipsdienol produced vectors (i.e., Conophthorus spp., Ips of ponderosa pine in the mixed co- by male western pine beetles and spp., Pityophthorus spp.) which can nifer forest of the west side of the male California five-spined ips, and be moved around by humans, as Sierra Nevada, the growth rate of verbenone produced by male and well as carry the pathogen from tree the remaining pines is increased, female western pine beetles, are to tree in nature. The new associa- and susceptibility to bark beetle at- promising candidates to protect

24 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 ponderosa pine from infestation by where they have or can become Raffa, K.F., T.W. Phillips, and S.M. these species. The natural role of damaging pests. Salom. 1993. Strategies and mecha- these chemicals is to prevent too nisms of host colonization by bark many beetles from attacking the beetles. In Beetle-pathogen interac- tree, which would result in a low REFERENCES tions in conifer forests, ed. T.D. survival of offspring due to compe- Schowalter and G.M. Filip, 103– 128. Academic Press, NY. tition among them. Further re- Bright, D.E. and R.W. Stark. 1973. Ross, D.W., K.E. Gibson, and G.E. The bark and ambrosia beetles of Cali- search is needed to develop a treat- Daterman. 2001. Using MCH to fornia, Coleoptera: Scolytidae and ment to prevent attacks on indi- protect trees and stands from Dou- Platypodidae. Bulletin No. 16 of the vidual trees, especially Monterey glas-fir beetle infestation. USDA California Insect Survey. pines, which are widely planted in Forest Service, Forest Health Tech- Furniss, R.L. and V.M. Carolin. 1977. urban environments in California. nology Enterprise Team, FHTET- Western forest insects. USDA Forest Forest management practices Service, Miscellaneous Publication 2001–09. may also help to reduce the im- No. 1339, Washington, D.C. Schowalter, T.D. and G.M. Filip, eds. pacts of bark beetle populations. Goheen, D.J. and E.M. Hansen. 1993. 1993. Beetle-pathogen interactions in Strategies available to foresters in- Effects of pathogens and bark conifer forests. Academic Press, NY. clude the removal of susceptible beetles on forests. In Beetle-patho- Stark, R.W. and D.L. Dahlsten, eds. trees, thinning of stands to increase gen interactions in conifer forests, ed. 1970. Studies in the population dy- namics of the western pine beetle, tree vigor, prescribed burning to T.D. Schowalter and G.M. Filip, 175–196. Academic Press, NY. Dendroctonus brevicomis LeConte eliminate susceptible host material, (Coleoptera: Scolytidae). Division of and enhancement of natural enemy Gordon, T.R., A.J. Storer, and D.L. Wood. 2001. The pitch canker epi- Agricultural Science, University of populations. For instance, thinning California, Berkeley. lodgepole pine stands reduces tree demic in California. Plant Disease 85:1128–1139. Storer, A.J., D.L. Wood, and T.R. mortality caused by the mountain Hopkins, A.D. 1899. Preliminary re- Gordon. 1999. Insect vectors of pine beetle. Also, setting prescribed port on the insect enemies of forests in Fusarium circinatum in California, fires following harvesting opera- the Northwest. USDA, Division of and their potential for the spread tions in ponderosa pine forests re- Entomology, Bulletin No. 21, of pitch canker disease. In Current duces populations of the California Washington, D.C. and potential impacts of pitch canker five-spined ips that breed in log- Harrington, T.C. 1993. Biology and in radiata pine, eds. Devey, M.E., ging debris. This practice lowers taxonomy of fungi associated with A.C. Matheson, and T.R. Gordon, 45–48. Proceedings of the IMPACT the probability of these populations bark beetles. In Beetle-pathogen in- teractions in conifer forests, ed. T.D. Monterey Workshop, 30 November emerging and killing living trees in to 3 December, 1998, Monterey, the area. Schowalter and G.M. Filip, 37–58. Academic Press, NY. CA. 1998. CSIRO Australia. Keen, F.P. 1928. Insect enemies of Cali- Wood, D.L. 1982. The role of phero- mones, kairomones, and allomones SUMMARY fornia pines and their control. State of California, Department of Natural in the host selection and coloniza- Resources, Division of Forestry, tion behavior of bark beetles. Annual Bark beetles are a natural com- Bulletin No. 7. Review of Entomology 27:411– 46. ponent of coniferous forest ecosys- Lorio, P.L. 1993. Host response to Wood, D.L., R.W. Stark, W.E. Wa- tems in California. They provide bark beetle and pathogen coloniza- ters, W.D. Bedard, and F.W. Cobb an essential role in the cycling of tion. Beetle-pathogen interactions in Jr. 1985. Treatment tactics and strat- nutrients and in the process of for- conifer forests, ed. T.D. Schowalter egies. In Integrated pest management est succession. They are involved in and G.M. Filip, pp. 81–101. Aca- in pine-bark beetle ecosystems, eds. W.E. Waters, R.W. Stark, and D.L. a myriad of interactions with other demic Press, NY. Owen, D.R, K.Q. Lindahl Jr., D.L. Wood, 121–139. John Wiley & entities in their environment, in- Sons, New York, NY. cluding their hosts, each other, Wood, and J.R. Parmeter. Jr. 1987. Pathogenicity of fungi isolated from Wood S.L. 1982. The bark and am- other insects, fungi, and humans. brosia beetles of North and Central Research has focused on the few Dendroctonus valens, D. brevicomis, and D. ponderosae to ponderosa pine seed- America (Coleoptera: Scolytidae), a species that cause economic dam- lings. Phytopathology 77:631–636. taxonomic monograph. age and has uncovered many of the Parmeter, J.R. Jr., G.W. Slaughter, Naturalist Memoirs, No. 6. mechanisms by which these inter- Mo-Mei Chen, D.L. Wood, and actions occur. In turn, this infor- H.A. Stubbs. 1989. Single and mixed David L. Wood, Division of Insect Biology, mation has provided insights into inoculations of ponderosa pine with University of California, Berkeley, CA ways of managing bark beetles to fungal associates of Dendroctonus spp. 94720-3112. [email protected]. reduce economic losses in situations Phytopathology 79:768-772. edu

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 25 Worker of Bombus fraternus buzz pollinating senna (Cassia fasciculata). The wings are blurred due to thoracic muscle vibration. All photographs by R. Thorp. BUMBLE BEES: BOISTEROUS POLLINATORS OF NATIVE CALIFORNIA FLOWERS by Robbin W. Thorp, Peter C. Schroeder, and Carol S. Ferguson

umble bees (Bombus spp.) are Bumble bees depend on pollen We hope the following informa- Blarge, fuzzy insects with eye- and nectar for satisfying their en- tion will lead you to appreciate catching colors and noisy ergy needs and for rearing their bumble bees and inspire you to help flight. Their boisterous behavior young. In turn, by altering the avail- protect and conserve these native around flowers easily captures the ability of nectar or pollen, flower- pollinators in your community. attention of nearly everyone. These ing plants shape the life history, salient traits overshadow the bumble community structure, and foraging bee’s less apparent features, such as habits of bumble bees. This bind- BUMBLE BEE LIFE specialized structures for collecting ing partnership between bees and HISTORY and transporting pollen, unusually flowers makes bumble bees a vital long tongues for gathering nectar, component of natural communities. Worldwide there are about 240 and a unique ability to shiver for Habitat fragmentation from urban- species of Bombus (including the warmth. Each of these characteris- ization and agriculture and the cuckoo bumble bees, , tics help join the food-gathering introduction of non-native bees which is now considered a subge- needs of bumble bees with the re- threaten the livelihood of bumble nus of Bombus). Most bumble bees productive needs of flowering plants. bees and other native pollinators. are confined to the Holarctic re-

26 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 gions of the earth, although some When she returns to the nest- larvae are better fed by the larger extend into the Oriental and Neo- ing site, the queen regurgitates nec- worker force and, when they emerge tropical regions as well. None are tar into the honey pot, forms the as adults, are larger than their sis- native to south of the Sahara pollen into a single loaf, lays eggs ters who emerged before them. or within the Australasian region. on the mass, and sometimes covers Eventually, as workers continue to There are 26 species of bumble it with wax. She then extends her increase in size, the colony produces bees native to California, where on top of the mass and new queens. they inhabit plant communities incubates her developing brood At about the same time the new from the Pacific Coast to above with heat generated by rapidly shiv- queens emerge, males develop from timberline. Bumble bee populations ering her wing muscles. To gain unfertilized eggs laid either by the in California are most diverse in energy while incubating her brood, original queen or by her unmated the northwestern part of the state she drinks from the nearby honey daughters. Adult males selfishly for- and within the Sierran-Cascade pot. The queen feeds her young age during the day and rarely re- ranges. In general, bumble bees pre- mixtures of honey and pollen. turn to the nest, usually resting on fer moist, cool habitats and show When mature, larvae spin co- vegetation at night. Young queens life cycles well-adapted to habitats coons and transform into sterile mate with males away form the nest, ranging from cool temperate to arc- adult females (workers). The first then actively forage to store energy tic climates. Few are found in semi- workers to emerge in the colony necessary for hibernation. All other arid to arid or dense coniferous for- are much smaller than the founding members of the colony (the old est habitats. queen and cooperate in construct- queen, workers, and males) die as Bumble bees are social and form ing cells, regulating nest tempera- the season ends. Newly mated annual colonies more similar to so- ture and humidity, and rearing their queens overwinter in shallow bur- cial wasps (yellowjackets and paper sisters. As workers in the colony rows and emerge the following wasps) than to honey bees, whose become more numerous, they as- spring to start the cycle again. Over- societies are perennial. Only fertile sume the foraging duties of the wintering queens emerge the fol- females (queens) overwinter, emerg- queen who eventually confines her lowing spring to start the cycle ing the following spring from their activity solely to egg-laying. Worker again. All other remaining mem- shallow underground chambers (hibernaculae). Robust newly- Worker of stealing nectar from larkspur (Delphinium). emerged queens search for suitable nesting sites by flying low and er- ratically over the ground in rela- tively open areas. Abandoned small rodent shelters or burrows often serve as nesting sites. Other shel- tered areas that contain fibrous ma- terials such as abandoned bird nests, upholstery, or insulation can pro- vide a suitable nesting site as well. Once she finds a nesting site, the founding queen constructs a wax cell or “honey pot” for nectar stor- age. She then visits flowers for nec- tar to give her energy, and pollen to serve as food for her prospective young. While foraging, the queen holds gathered nectar in her crop (a specialized region of her digestive tract) and grooms pollen from her body. She then mixes the groomed pollen with a small amount of nec- tar and forms it into moist lumps, which she carries in special pollen baskets (called corbiculae) on the outside surface of her hind legs.

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 27 bers of the colony, the old queen, of the bumble bee species compris- colonies of a given species. Conse- workers, and males, die as the sea- ing the community. In most locali- quently, the relationship between son ends. ties, bumble bee communities con- tongue lengths and community tain a variety of species possessing structure is closest (and possibly different tongue lengths. only applicable) early in the season THE STRUCTURE OF Bumble bee tongue length is re- when queens are most predominant BUMBLE BEE lated to the depth of nectaries of in the community. COMMUNITIES available host flowers and, within a This relationship is further species, is correlated with body size confounded by phenological dif- Bumble bee communities in the (larger bees have longer tongues) ferences in emergence patterns, and Klamath Ranges (including the and head shape (bees with triangu- subsequently tongue lengths Siskiyou Mountains) of northern lar heads have longer tongues than among bumble bee queens. For California and southern Oregon bees with rounded heads). Tongue example, queens that emerge early commonly contain six to a dozen lengths are usually uniform among in the season (typically B. bifarius, species that often coexist in areas as queens of the same species. How- B. melanopygus, and B. vosnesenskii) small as 100 square meters. Struc- ever, tongue lengths among worker have moderate tongue lengths, ture (diversity of members) of a bumble bees (who show a wide va- whereas queens that emerge later bumble bee community is largely riety of body sizes) vary greatly (typically B. appositus, B. flavifrons, determined by the tongue lengths among individuals and between and B. nevadensis) have longer tongues. A mixture of long-tongued Worker of foraging for pollen on lupine (Lupinus). (B. californicus) and short-tongued (B. franklini and B. occidentalis) bumble bees emerge even later in the season.

FORAGING HABITS OF BUMBLE BEES

Bumble bees visit flowers to gather nectar or pollen. They are typically considered “generalists” and visit a broad array of species. Many species of plants restrict the types of visitors that seek their flowers by limiting the acces- sibility of pollen or nectar. For ex- ample, snapdragon (Antirrhinum) and scotch broom (Cytisus) conceal their pollen or nectar within flower parts that must be pushed aside by large-bodied, strong visitors like bumble bees. The flowers of nightshade (Sola- num), tomato (Lycopersicon), and senna (Cassia) contain apically- pored (salt shaker-like) anthers that release pollen in response to vibra- tion (see photograph, page 26). While visiting these flowers, bumble bees and a few other bees are ca- pable of vibrating their bodies by rapidly oscillating their wing muscles without engaging the wings (honey bees lack this ability). Con-

28 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 sequently, bumble bees are among FLORAL the most efficient pollinators of ASSOCIATIONS OF these flowers. The ability to “buzz BUMBLE BEES pollinate” is one reason that bumble bees are used commercially to pol- The Klamath Ranges of the linate hothouse tomatoes. Northwest Region of the Califor- When foraging for nectar, nia Floristic Province contains a di- bumble bees preferentially seek flow- verse natural geography and hosts a ers with high nectar rewards acces- wide assemblage of flora frequently sible to their tongues. Some plants visited by bumble bees (over 7,400 store their nectar within deeply re- flower records in California revealed cessed parts of the flower, such as 61 families and 226 genera of plants the floral spurs of larkspur (Del- Queen of Franklin’s , Bombus visited by bumble bees). In Cali- phinium) or the long corolla tubes franklini, foraging on California poppy fornia, the most frequently visited of beardtongue (Penstemon). Long- (Eschscholzia californica). native plant genera by bumble bees tongued bumble bees like B. appositus, are listed in Table 1 (page 30). B. flavifrons, and B. nevadensis can they receive no immediate energy Recent studies in the United successfully and legitimately acquire from pollen, bumble bees must in- Kingdom as well as the Califor- nectar from these flowers. termittently visit nectar-bearing nia Floristic Province suggest that To obtain the same nectar, plants while foraging for pollen. bumble bees prefer long-lived bien- shorter-tongued bumble bees like We have often observed these nial and perennial flowering plants B. franklini and B. occidentalis must “flower-switching” bees carrying rather than annuals. Early spring resort to “nectar-robbing” by biting reddish orange pollen while visit- queens visit manzanita (Arctostaphy- the tip of the spur or base of the tube ing nectar-rich flowers of mints or los), gooseberry (), and willow that conceals the nectar and imbib- thistles that produce light-colored (Salix) while fall queens commonly ing the nectar through the resulting pollen. When plants with nectar- visit thistles (Cirsium). Males, who hole (see photograph, page 27). Bees producing flowers are rare or widely typically appear near the end of the that rob nectar this way avoid con- spaced among plants with pollen- nesting season, primarily visit thistles tact with the anthers or stigma of only flowers, bumble bees may and rabbit brush (Chrysothamnus). the flower and consequently do not imbibe nectar stored in the nest However, because bumble bee pollinate the flower. Nectar robbing before they leave to forage for colonies persist beyond the indi- may also reduce seed set by reduc- pollen—an advantage enjoyed by vidual blooming period of most ing the amount of nectar available bumble bees over non-social bees. plant species, bumble bees depend to legitimate pollinators. At cool temperatures, bumble on a succession of nectar and pollen Nectar-rich flowers of horse bees are capable of warming their sources during the course of a sea- mint (Agastache), coyote-mint bodies by shivering their wing son. Besides those from native (), and black sage (Salvia) muscles (muscular thermogenesis) plants, bumble bees also benefit ensure pollination by depositing prior to foraging. The ability of from pollen and nectar resources their pollen on the foraging bee’s bumble bees to alter their body tem- provided by many introduced plants, back (a process called nototriby). perature through muscular thermo- including agricultural crops such as Thus deposited, the pollen cannot genesis allows bumble bees to for- alfalfa (Medicago sativa), horticultural be groomed and packed into loads age at temperatures otherwise too introductions such as rhododendron destined as brood food back at the cold for most other foraging insects (Rhododendron spp.), and even inva- nest. The pollen is eventually trans- and therefore gain first access to sive weeds such as yellow star-thistle ferred to the stigma of another early spring or high elevation flow- (Centaurea solsititalis). flower as the bee continues to for- ers such as fireweed (Epilobium). age for nectar. However, bumble bees use a rela- CONSERVATION OF Some flowers offer no nectar tively large amount of energy to and rely solely on pollen to attract generate heat by muscular thermo- BUMBLE BEES AND potential pollinators. Examples of genesis. And, as Bernd Heinrich re- OTHER plants with nectarless flowers at- vealed in his work on bumble bee POLLINATORS tractive to bumble bees include lu- energetics (Heinrich 1979), they pine (Lupinus), California poppy must carefully balance their energy Most flowering plants are pol- (Eschscholzia), and wild (Rosa) needs or expenditures with the nec- linated by insects (including but- (see photograph, page 28). Because tar rewards of flowers. terflies, moths, flies, and beetles),

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 29 TABLE 1. NATIVE CALIFORNIA PLANTS MOST FREQUENTLY VISITED BY

Plants are listed by relative rank of visitation frequency (1 = most frequent), genus, common name, life cycle (annual or perennial, listed in order of importance), and resource (nectar or pollen) offered to bumble bees. From Thorp et al. 1983.

RANK GENUS COMMON NAME LIFE CYCLE RESOURCE

1 Cirsium Thistle Ann. Per. Both 2 Chrysothamnus Rabbit brush Per. Both 3 Sunflower Ann. Per. Both 4 Lupinus Lupine Per. Ann. Pollen 5 Trifolium Clover Ann. Per. Both 6 Melilotus Sweetclover Ann. Bien. Both 7 Eriogonum Wild buckwheat Per. Ann. Both 8 Isocoma Goldenbush Per. Both 9 Ceanothus California lilac Per. Both 10 Aster Aster Ann. Per. Both 11 Solidago Goldenrod Per. Both 12 Solanum Nightshade Per. Ann. Pollen 13 Phacelia Phacelia Ann. Per. Both 14 Penstemon Beardtongue Per. Both 15 Monardella Monardella Per. Ann. Nectar 16 Rhododendron Rhododendron Per. Nectar/Both 17 Ribes Gooseberry Per. Both 18 Arctostaphylos Manzanita Per. Nectar/Both 19 Vicia Vetch Ann. Per. Both 20 Astragalus Locoweed Per. Ann. Both 21 Salvia Sage Per. Ann. Nectar 22 Rubus Blackberry Per. Both 23 Senecio Groundsel Ann. Per. Both 24 Lotus Trefoil Per. Ann. Both 25 Asclepias Milkweed Per. Ann. Nectar

though some are pollinated by birds bee, on which we rely heavily as especially in the once common and and bats. Bees are most important the principal pollinator of our widespread western bumble bee (B. among these pollinators because crops. occidentalis) and the narrowly en- they collect both pollen and nectar Recent declines in bumble bee demic Franklin’s bumble bee (B. as food. Buchmann and Nabhan populations have been documented franklini). Franklin’s bumble bee (see (1996) recognized that many in the European community, and photograph, page 29) has the small- groups of pollinators are declin- we have been tracking similar de- est range of any North American ing, including the European honey clines in the western United States, bumble bee. Its entire distribution

30 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 extends only 144 miles north to bumble bees into the areas where cient nectar and pollen gathering. south and 75 miles east to west in they can compete or possibly inter- Bumble bees are undoubtedly wor- south-central Oregon and north- breed with native bumble bee spe- thy of any effort to conserve them. . cies. Such has been the case with To protect them, however, we need Because of its narrow endemism, the European to know more about their habitat B. franklinii is listed as a candidate which has been introduced to many requirements so that we can effec- species for protection by the US areas of the world including Japan, tively manage and protect their Fish and Wildlife Service. Data re- where native bumble bees suitable natural foraging and nesting areas. garding the habitat requirements of for commercial rearing could have To encourage others to assist in Franklin’s bumble bee are currently been used instead. this effort, field guides that assist in being gathered by Robbin Thorp The potential introduction of the identification of bumble bee spe- to try and determine its suitability foreign pathogens to bumble bees cies are needed. for listing, an effort we feel is par- raises further concerns about the ticularly important considering re- ecological risks of trafficking bumble cently observed declines in the bees for commercial use. Recently REFERENCES populations of this species. an internal parasitic mite of a ge- We are collecting similar data netic strain different from local Buchmann, S.L., and G.P. Nabhan. on the western bumble bee, which Japanese mites has been found in 1996. The forgotten pollinators. Island is closely related to and whose range bumble bees imported to Japan from Press, Covelo, CA. encompasses that of Franklin’s Europe. Heinrich, B. 1979. Bumblebee econom- bumble bee. The western bumble Preservation of plant-pollinator ics. Harvard University Press, Cam- bridge, MA. bee is a widespread polymorphic systems will require a better under- Kearns, C.A. and J.D. Thomson. 2001. species that occurs from Monterey standing of bumble bee ecology, The natural history of bumblebees. A and Tuolumne counties of Califor- particularly the floral associations sourcebook for investigations. Univer- nia north to and south of bumble bees. Current studies sity Press of , Boulder, through the Rocky Mountains to typically rely on observations made CO. northern and . in the field, often in cooperation O’Toole, C., and A. Raw. 1999. Bees of Colonies of the western bumble bee with naturalists, botanists, and other the world. Sterling Publishing Com- have been commercially reared for field personnel. However, accurate pany, New York, NY. pollinating greenhouse tomatoes identification of bumble bees in the Schmidt, M.G. 1980. Growing Califor- since 1992. field is often difficult. nia native plants. California Natural From 1998 to date, natural Populations of native bumble History Guides: 45. University of California Press, Berkeley, CA. populations of this species have bees may benefit most by the pres- Sladen, F.W.L. 1912. The humble-bee. steadily and precipitously declined ervation of appropriate habitat. Its life-history and how to domesticate in the area between California and Landowners and gardeners can help it. Macmillan & Company, Ltd. southern British Columbia. These preserve bumble bee populations by London, U.K. Reprinted in 1989 by declines may be caused by a proto- establishing landscapes that provide Logaston Press, Woonton, U.K. zoan (Nosema) disease which ap- suitable habitat for bumble bee nest- Thorp, R.W. 2003. Bumble bees (Hy- peared in commercial rearing stocks ing and by planting flower gardens menoptera: ): Commercial of the western bumble bee in 1998. that offer a season-long supply of use and environmental concerns. In Current studies hope to determine nectar and pollen. Details on meth- For non-native crops, whence pollina- if the protozoan disease is respon- ods for preparing and maintaining tors of the future?, ed. K. Strickler and sible for declines in natural popula- bumble bee gardens can be found J. Cane, Thomas Say Publications tions of the western bumble bee, in various gardening publications. in Entomology: Symposium Pro- ceedings of the Entomological So- and possibly Franklin’s bumble bee With over two dozen species, ciety of America. In press. as well. bumble bees represent a diverse and Thorp, R.W., D.S. Horning, Jr., and Urban development and agri- important group of insects in Cali- L.L. Dunning. 1983. Bumble bees culture alters habitats otherwise fornia and southern Oregon. Their and cuckoo bumble bees of Califor- suitable for bumble bee nesting and foraging habits and life history se- nia. Bulletin of the California Insect reduces the variety of flora used by cure them as important pollinators Survey 23:1–79. bumble bees as forage resources. of a wide variety of flowering plants. Commercial trafficking of bumble Their close and binding relation- Robbin W. Thorp, Department of Ento- bees for pollination of hothouse to- ship to flowering plants is revealed mology, One Shields Ave., University of matoes further threatens native by their specially adapted bodies and California, Davis, CA 95616. rwthorp@ bumble bees by introducing alien unique behaviors that ensure effi- ucdavis.edu

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 31 View of Pinnacles National Monument showing the nearly continuous blanket of chaparral over much of the uplands. All photographs by O. Messinger. A PINNACLE OF BEES by Olivia Messinger and Terry Griswold

To make a prairie it takes a clover of poppies are vying for prospective der some related issues: Do abun- and one bee, pollinators. dant flowers relate to bee diversity? One clover, and a bee. Bees are notable pollinators in What is the role of bees in plant And revery. California (Moldenke 1976a), ef- success? And what happens when The revery alone will do, fectively bussing pollen grains from one of these two actors (flower or If bees are few. one effulgent floret to consecutive bee) fails to appear? What does hap- —Emily Dickinson mates. But from the bee’s perspec- pen, as Ms. Dickinson mused, if tive, pollination is a secondary role; bees are few? hile floral displays are each trip to a floret is a purposeful Such questions are easier to pose Wattractive to the eye, the attempt to harvest loads of pollen than to answer. Bees are highly bright and luminescent with which to provision nests. Such mobile and generally short-lived comprising these often fra- interdependence between bees and creatures. A complete understand- grant bouquets play a role far more their flowers raises several commu- ing of bee community dynamics re- important than just aesthetics. Eco- nity-level questions. Central among quires not only extensive surveying logically, fields of flowers are com- these is to what extent these two time, but also unaltered landscapes peting ad campaigns; yellow groups of organisms are dependent with little unnatural influence. Pin- spangles of asters and orange washes upon each other. But we also pon- nacles National Monument is one

32 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 such natural laboratory. Comprised bloom commences in February with robust chamise plants sparked just of several distinctive habitats and a the flowering of manzanita (Arcto- the opposite response from our bee myriad of flowering plants, this ref- staphylos spp.). While flowering con- researchers. Such burns provided uge has been virtually untouched tinues to some extent at least through us with the opportunity to seek an- by agricultural practices. the middle of October, most of the swers to some additional questions: It was with high expectations species at Pinnacles bloom in the How does the presence of transients that we accepted an offer from Amy spring (March to mid-June). like fire-following plants influence Fesnock, wildlife biologist in Pin- Pinnacles National Monument bee composition? Since fire and the nacles National Monument, to em- was ideal for a bee study not only subsequent bloom are unpredict- bark on a multiyear, systematic for its pristine nature, but for other able, can concrete relationships ex- study of such a critical faunal com- reasons as well. We had high expec- ist between fire-following plants and ponent on this 25-square-mile pre- tations for a rich bee fauna, a pre- bee species? serve. Here was a rare opportunity sumption that arose from several Minor catastrophes seemed to to go beyond basic inventory—to sources. While most genera achieve be a recurring theme during the study bee spatial and temporal pat- their highest diversity in tropical cli- course of our research, and enabled terns across years and to investigate mates, bees flourish in more tem- us to investigate rarely studied pro- their complex relationship with perate zones. Drier soils have been cesses in bee communities. One plants. By systematically collecting hypothesized as the likely explana- such opportunity came in the sec- bees from portions of the monu- tion for this trend, as they decrease ond year of our study during the ment across an entire flowering sea- the chance of nest failure due to torrential rains and cold spring tem- son, the intricacies of a bee com- fungal infection (Linsley 1958). peratures of the 1998 El Niño event. munity could be explored. In the Previous studies in Mediterra- In the wake of the storms, we were face of changing environments, such nean (Michener 1979) and chapar- able to observe just how resilient knowledge is essential to monitor- ral regions have produced im- bees are to a climatic change of this ing pollinator health. pressive laundry lists for bees in magnitude. Pinnacles National Monument both North and South America is part of the rugged landscape that (Moldenke 1976b), leading us to lies along the in believe the same could be expected METHODS the inner South Coast Range. The in Pinnacles. As anticipated, an ex- diversity of plants in Pinnacles is ploratory visit to Pinnacles in 1996 In order to characterize the bee notably high. While nearly 600 spe- yielded 87 species in just four days. fauna and its floral relationships, cies of flowering plants occur here, Further incentives for studying we attempted to collect foraging chaparral dominates this landscape bees in Pinnacles included the pres- bees on all flowering plants that (see photograph, page 32). Stands ence of several recently burned habi- occur within Pinnacles across rep- of buck brush () tats. The largest of these is a burn resentative areas of the monument. intermingle with manzanita (Arcto- from August 1993 that charred Systematic sampling by net was con- staphylos spp.). Holly-leafed cherry many acres of chaparral, clearing ducted along trail segments and in (Prunus ilicifolia), woolly bluecurls the way for rare, fire-following other open areas within the typi- (Trichostema lanatum), and black plants, as well as providing ample cally dense habitats of the monu- sage (Salvia mellifera) prevail amidst open ground for plants otherwise ment. Collected bees were first the rocky crags of the High Peaks. constrained to rather small sunlit pinned and then labeled with plant Chamise (Adenostoma fascicula- patches. Two additional burns oc- association, date of capture, and tum) fills in any remaining gaps, curred during our study: one was a habitat descriptors (i.e., chaparral coating rolling hillsides, clothing the prescribed burn in the fall of 1997, or riparian habitat). Finally, our highest point (Chalone Peak at 3,304 while the other was a large burn specimens were identified. feet), and often forming pure, im- that occurred in August 1998. Our first concerted collecting penetrable stands. At the lowest Fire is thought to play a vital effort began in late March 1997. A points (minimum elevation, 824 feet) role in chaparral ecology, as evi- strict regimen of weekly collections river bottoms support more open denced by the many chaparral was maintained along a set of se- communities of blue oak (Quercus shrubs adapted to intense heat. lected trails. We returned for two douglasii) and valley oak (Q. lobata). Many fire-following plants appear days in late June and once in Sep- The park receives an average of only in areas that have recently tember to capture what we expected only 16 inches of rain each year, burned. What one might perceive to be a limited summer and fall primarily in winter precipitation as relatively catastrophic when look- fauna. (January to March). The resulting ing at the remaining crowns of once Observations from our first year

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 33 of fieldwork indicated the need for an earlier start in the flowering sea- TABLE 1. THE BEE FAUNA OF PINNACLES son, so plans were made to begin NATIONAL MONUMENT the 1998 field season in late Febru- ary (nearly a month earlier). Analy- Two asterisks indicates all members of the genus in Pinnacles are sis of 1997 data also indicated that specialists, one asterisk indicates some members of the genus in seasonality in bees could still be as- Pinnacles are specialists. sessed if sites were collected on a 10-day cycle instead of weekly. This Family Genus Number Clepto- Oligolectic would allow us to expand into more of Species parasites areas of the monument within each round of collecting. Colletes 5* Our carefully laid out plans for Hylaeus 18 1998 did not anticipate dramatic Ancylandrena 1** weather. The spring field season in 60 * 1997 was marked by only one rainy Calliopsis 7** day. In contrast, spring 1998, influ- enced by El Niño, was defined by Panurginus 5* cold rain and frequent clouds. Perdita 13 ** Creeks that typically were ankle Conanthalictus 1** deep became, at times, torrents Dufourea 6** forceful enough to destroy bridges, Micralictoides 2** closing the monument for nearly a Augochlorella 1 month. In the wake of the down- 1 pours, quicksand replaced gravelly Dialictus 12 beaches, fallen trees and limbs lit- tered last year’s groves, and fields Evylaeus 15 of flowers inundated the grasslands 3 of past years. Lasioglossum 3* Restless bee collectors spent Sphecodes 10 • many days watching for sunny skies 2** (good “beeing” weather). Indeed, Ashmeadiella 14 * one unbearably long period of Atoposmia 3** sunless skies lasted for 11 days! Chelostoma 7** While the subsequent bloom was Heriades 1 incredible, bees that survived the deluge had to cope with a new envi- Hoplitis 17 ** ronment characterized by unseason- Osmia 37 * ably chilly days, repeated rains, and markedly delayed blooming even among the most hardy of chaparral Our focus was on the most thor- matched by an amazing array of plants. The wet, cool spring de- oughly collected areas of previous bees. Nearly 400 bee species are layed and then extended the flow- years. We also sampled the burn now known to reside in the monu- ering season beyond our planned that occurred during the late sum- ment, representing 52 genera and end to the field season. To supple- mer of 1998. all six North American bee families ment our thorough spring collec- (see Table 1, pages 34 and 35). The tions and to catch latecomers de- bees at Pinnacles range in size from tained by the weather, we made spo- RESULTS miniscule (mosquito-sized) to gar- radic collections in June, July, Au- gantuan (the size of one’s thumb), gust, and October. Despite rainy days, unexpect- and come in colors as varied as the Our final field season was an edly delayed blooming, and plenty plants they visit—from coppery attempt to assess the effects of the of “strikes” when swinging nets and greens, to steely blues, or glossy El Niño event. We sampled only missing bees, our efforts were richly black. during the last three weeks of May rewarded. They demonstrated that At least two of these bees ap- 1999—the height of bee activity. the diverse flora of Pinnacles is pear to be endemic to the monu-

34 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 to the Western Hemisphere, was TABLE 1 (cont.) found almost exclusively on flowers of the non-native, meadow-invad- Family Genus Number Clepto- Oligolectic ing star thistle (Centaurea solstitialis). of Species parasites The vast majority of bees at Pinnacles are solitary. Each female Protosmia 1 is responsible for her own nests, the Anthidiellum 1 cells of which she carefully provi- Anthidium 6*sions with collected masses of Dianthidium 4*pollen and nectar. In addition to Protostelis 2• being solitary, most female bees Stelis 11 • in Pinnacles nest independently, Trachusa 2 choosing nesting sites at fair dis- tances from any neighbors. How- Dioxys 4• ever, some gregarious nesters build Coelioxys 5• aggregations more akin to apart- Megachile 17 * ment complexes. Apidae Xylocopa 1 A few sites in Pinnacles seemed 11 * particularly popular with certain 21 • species, and looking down on such 3• sites is reminiscent of a gopher town 3• with holes by the hundreds pepper- 2• ing the ground. Bees at Pinnacles also include some social species, Townsendiella 1• identified by the fact that all mem- 2 bers live together in one nest. These 5**include the well-known , 10 * bumble bees (Bombus), and sweat Synhalonia 10 * bees (Halictini). 11 Even within the relatively small 3 area of Pinnacles, bees appear to 1 prefer certain habitats. Burned ar- Apidae 3• eas harbored a diverse bee fauna. 2• Well over half of the species in the monument were caught within these Bombus 6 areas, yet only a handful of species Apis 1 appear to be restricted to this short- Total 393 lived habitat. Centris californica and Megachile davidsoni, previously un- recorded from the Coast Ranges, ment and surrounding areas. pear to reach their northern limit were present only in the burned Andrena annectans has been collected in Pinnacles. Included are the most areas. In addition, we found that only in Pinnacles and the nearby northerly records for the genera unburned upland areas were home town of Bitterwater; Ceratina hurdi Ancylandrena and Centris. Four non- to over half of the total bee fauna. is known only from Pinnacles and a native bees are present in the monu- The greatest diversity in Pinnacles, single site to the west at the north ment. Honey bees (Apis mellifera), however, exists in and near riparian end of the Santa Lucia Mountains. originally brought over from Eu- areas. For example, over 260 spe- Additional endemics are probable rope nearly 300 years ago, are the cies were encountered along the among the 15 new species found in most prevalent of these. Feral 2.3-mile Old Pinnacles Trail. Pinnacles. (meaning they have escaped from The rich bee fauna in Pinnacles Pinnacles also supports a num- domestication and become wild) National Monument is certainly ber of species not previously known honey bee populations can be found related to the diverse flora harbored to occur in the South Coast Range. in many hollow stumps throughout within its boundaries. Bees were Several of these are inhabitants of the monument. Megachile apicalis, a found on half of the roughly 600 xeric areas to the south, which ap- more recent accidental introduction flowering plants in Pinnacles, visit-

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 35 Polygonaceae in larval dietary restrictions. In con- 17% trast, the flexibility of generalists 28 Plant Families may make them less susceptible to 27% the vagaries of flowering times and abundance. Since the flight season of social bees is relatively long com- pared to the short flowering period Hydrophyllaceae of many plants, only solitary spe- 13% cies are specialists. Within Pinnacles, approxi- mately 25% of all pollen-collecting 5% bees are specialists. For example, Fabaceae Papaveraceae Chelostoma cockerelli and C. phaceliae 10% 5% females visit almost exclusively Rosaceae woolly yerba santa (Eriodictyon Scrophulariaceae 6% tomentosa) and species of Phacelia, 9% Asteraceae respectively. Megachile davidsoni 8% consistently visits golden eardrops Figure 1. Floral utilization by bees in Pinnacles National Monument. Proportion of (Dicentra chrysantha), though it is females from all years visiting plant families (28 families with less than 4% of bees were interesting to note that despite combined). consistent bloom and reasonable sampling across all three years of ing nearly two-thirds of the 70 or We noticed that plants which the study, we detected M. davidsoni so plant families in the monument are heavily visited by bees do not only in 1997. This relationship is (see Figure 1 above). necessarily support the highest spe- made even more interesting by the While bees visit a large pro- cies diversity; some plants are domi- fact that Dicentra chrysantha is a portion of the flora in the monu- nated by only a few species. Nor fire-following plant, typically found ment, a few plants together sup- is plant abundance necessarily in- only in areas that have recently port the greatest diversity of bees dicative of the quality of food burned, and its populations dwindle (see Table 2 on page 37), attract- resources (pollen and nectar) avail- as post-fire changes in vegetation ing 53% of all bee species collected able to bees. Willow, while sparsely occurs. One wonders how this spe- in the monument (but represent- present in the 5% of the monument cialist bee manages to detect plant ing only 13% of all bee specimens). that is riparian, supports as diverse populations as patchy and unpre- Buckwheat () a bee fauna as does chamise, which dictable as those of golden eardrops. alone was found to support over dominates in over 90% of the A variety of structural and be- 100 species of bees. The sight of a monument. havioral traits are associated with buckwheat bush obscured by a While bees visit flowers for both pollen specialization (Thorp 1979, blurry cloud of miniscule bees is nectar and pollen, it is pollen for 2000). Most solitary bees have an truly amazing, and presents a vivid nest provisions that drives floral visi- area of stiff hairs, called a pollen reminder of the importance of tation patterns for most bees. Some brush or scopa, into which pollen floral resources to bees. bees (generalists or “polylectic”) grains are pushed. In Pinnacles, the There are several early season collect from a wide array of plants, bee Hoplitis (Proteriades) has mouth- plants that were not sampled equally providing their offspring with a parts with hooked hairs for pollen across years. For example, some smorgasbord of . Other extraction from the narrow throats flowering species that were highly mothers are more discriminating. of Cryptantha flowers. The special- attractive in 1998 were not sampled These bees (specialists or “oligo- ist bee Diadasia accommodates the in 1997, or were sampled only at lectic”) consistently gather pollen large pollen grains of Clarkia and the very end of their flowering; they from a single genus of plants or a morning glory (Calystegia) with might well belong in this table. closely-related group of plants. widely-spaced hairs in its scopa. These plants include: buck brush The evolutionary advantage of Mouthpart lengths in the bumble (Ceanothus cuneatus: 18 species), Cali- such specialization is unclear. Pos- bees Atoposmia and Hoplitis are dif- fornia goldfields (Lasthenia califor- sibilities include more efficient use ferentially proportional to corolla nica: 39 species), popcorn plant of time when collecting pollen, less depth in flowers, and may allow (Plagiobothrys nothofulvus: 50 species), competition with other bees for these bees to collect nectar while and willow (Salix spp.: 28 species). pollen and nectar, and differences harvesting pollen.

36 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Behavioral traits include sea- stigma with useless foreign pollen. reap the rewards of the anthers thus sonal emergence from nest cells syn- In contrast, a specialist bee that only exposed. (The majority of bees have chronous with the first bloom of forages on Lasthenia flowers can be pollen-collecting hairs on their legs.) their preferred flowers, foraging expected to deposit only conspe- Most plants in Pinnacles play coincident with when pollen is avail- cific pollen. In this way, the poten- host to diverse suites of both gener- able (e.g., early morning foraging tial for successful fertilization of this alist and specialist bees. This is most by Synhalonia venusta, when Clarkia plant species is greatly increased. easily demonstrated for Clarkia be- pollen is present), and manipula- The form and structure of many cause of the comprehensive study tion of flowers with hidden pollen. plants in Pinnacles demonstrates by MacSwain et al. (1973) on bee For example, Megachile davidsoni was how plants encourage specialization, relationships with this plant genus observed to stand on its head to thereby narrowing the pool of pos- throughout cismontane (in this case, access the nectar and pollen in flow- sible contaminating vectors. The west of the Sierra crest) California. ers of golden eardrops. tubes of Penstemon flowers are nar- (Such studies are rare for the Cali- Though they are not as com- row enough that only “skinny” bees fornia flora.) mon, plant species visited by spe- can crawl inside where the anthers In Pinnacles, 85 pollen-collect- cialist insects enjoy advantages as are located. Many pea flowers re- ing species visited Clarkia at one or well. A generalist flying from a Cali- quire very specific bees. Not only more of the 12 sampling sites where fornia goldfield (Lasthenia califor- must the bee be able to open the it was present. Though the major- nica) to an owl’s clover (Castilleja lower keel petal by spreading it with ity of these species were generalists exserta) is not likely to leave behind her hind legs; she must also have (76), the handful of specialists rep- the right kind of pollen. Indeed, pollen-collecting hairs on the un- resented over half of the visits to such bees are likely to clog the derside of her abdomen in order to Clarkia. This high dependence

TABLE 2. DIVERSITY OF BEES ON MAGNET PLANTS IN PINNACLES

Diversity is based on females only. As sole collectors of pollen, their visitation patterns are more indicative of the importance of floral components.

1997 1998 NUMBER OF NUMBER OF COMMON NAME LATIN NAME SPECIMENS SPECIES SPECIMENS SPECIES

California buckwheat Eriogonum 1196 104 1139 78 fasciculatum

California broom Lotus scoparius 490 67 210 49

Yerba santa Eriodictyon 337 53 31 19 tomentosa

California poppy Eschscholzia 248 44 68 20 californica

Clarkia Clarkia 243 48 99 26 unguiculata

Chinese houses Collinsia 181 39 107 34 heterophylla

Summer mustard Hirschfeldia 133 53 27 15 incana

Chamise Adenostoma 90 19 225 30 fasciculatum

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 37 Collinsia heterophylla

sitic bee species in Pinnacles (62%) nest in the soil. Most excavate their own nests, and some show prefer- ence for specific sediments. A significant number of bees nest in stems or wood (28%), including all of the exotic bees. Most of these are “renters,” bees that occupy al- ready existing holes, but a few drill into pithy stems or soft wood. Many Lupinus albifrons of the renters also require specific nest-building materials for construc- tion of nest cells, such as mud, gravel, resin, or leaf material. Certain Osmia, for example, were found in large numbers along the moist banks of waterways in Pinnacles, likely be- cause this was an excellent place to mine mud for their nests. By comparison, Trachusa popu- lations were found in two dry loca- tions with friable soils higher up in the monument. These soils were in Pholistoma auritum proximity to manzanita, whose leaves Trachusa cut into narrow strips to line their nests. This shrub, then, may be a determinant in de- fining this bee’s distribution. Other bees (for example, Dianthidium) take advantage of the prevalent rocky surfaces throughout the monument, building their nests like miniature masons on the craggy cliffs. Not all the bees of Pinnacles are Figure 2. Phenological shift of bee activity in Pinnacles between successive years for pollen collectors. Some surrepti- three flowering plants. X-axis = day of year; Y-axis = relative number of flower visits. tiously deposit their eggs in the nests of other bees (cleptoparasites). Fully makes Clarkia specialists more pre- known, though Diadasia may be lim- 17% of the bees at Pinnacles dis- dictable. All nine Clarkia specialists ited to fine-grained, hard-packed play such behavior (see Table 1, known to occur in the South Coast level ground for nesting. Diadasia, pages 34 and 35). Upon hatching, Range (MacSwain et al. 1973) are with its particular food and nesting the parasite larva destroys the host present in Pinnacles. Indeed, spe- habits, is a nice example of the vari- egg or larva and then consumes the cialist bees could be accurately pre- ety of factors that play a strong role pollen provisions. Since these bees dicted in the 12 Clarkia sites 44% in bee patterns of abundance. parasitize specific pollen-collecting of the time, versus 22% of the time The restrictions on bee ranges bee genera, their distributions are for generalists. One such bee, are additive. A species can only ex- defined by that of their hosts. Hesperapis illicifoliae, was present ist where all the environmental com- Most bees in Pinnacles only live wherever Clarkia was found. ponents necessary for survival oc- for a short time. Exceptions include On the other hand, and despite cur; for example, where appropri- many of the social species, like the the fairly broad distribution of Clar- ate nesting conditions and adequate honey bee. Seasonal patterns ob- kia in Pinnacles, Diadasia angusticeps flowers overlap. While nesting pref- served in Pinnacles suggest that the (another specialist) was consistently erences were not the focus of this average duration of adult activity present in only one lowland Clarkia study, we did observe a diversity of for a solitary species is roughly a patch across all three spring seasons. nest site preferences for bees in Pin- month to six weeks, with individual The reason for this restriction is un- nacles. The majority of nonpara- life spans likely less. Since the sea-

38 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 son of bee activity spans nine pends on a seed bank and is deter- months, the bee population is there- mined by resource availability im- fore constantly renewing itself. The mediately prior to germination. bee species flying in the spring are As an example, consider two suc- not the same species flying in the cessive years. In the first one, little fall. In fact, of the bees flying at any rain falls, and few flowers germi- given time in the spring, 50% finish nate. Bee mothers have a limited provisioning nests and die over the pollen supply with which to provi- next two weeks. Perhaps this high sion nest cells, and they lay few rate of turnover is related to the eggs. The following year may be incredible number of species present relatively wet with abundant flow- in such a relatively small area. ers. However, bees are scant be- A comparison of the seasonal cause of the drought the previous abundance of bees between 1997 year, and so open blossoms go un- The crags of Pinnacles. and 1998 demonstrates the effect visited. Perennials, while less influ- El Niño had on both bee and plant enced by variations in rainfall, still Weather in 1998 severely im- activity (see Figure 2, page 38). Like flower in response to the precipita- pacted other bees. All species of a baseball game perpetually post- tion from the current year. small carpenter bees (Ceratina) ex- poned, nearly all budding flowers Relationships may be further perienced radical reductions in in 1998 waited at least a month complicated by variation in the populations despite the fact that longer than they did in 1997 to availability of nest sites. Bumble they are generalists and active bloom—presumably as a result of bees, which often utilize rodent bur- throughout the blooming season. the extremely cold, wet spring rows for nests, may be affected by Ceratina nest in pithy stems, and months of the El Niño year. A look fluctuations in rodent populations. the relative fragility of this nesting at the bee patterns of emergence Nesting queens in the cold, wet material may have made them par- (indicated by first collections) shows spring of 1998 may have experi- ticularly susceptible to the severe a similar seasonal shift. More inter- enced high mortality due to the in- weather. Hylaeus, which frequently estingly, such delayed emergence ability to forage or may have been nest in stems, also appear to have coincides very closely with times of drowned out of their nests. suffered population crashes. plant bloom. Though bees appear to track their floral resources, bee popula- TABLE 3. GENERIC AND SPECIES tions may experience rapid declines DIVERSITY AMONG BEE FAUNA IN THE independent of the availability of floral resources, leaving blooms UNITED STATES largely unattended. In 1997 we ob- LOCATION GENERA SPECIES APPROX. served a flurry of activity as an en- TOTAL tire hillside in the 1993 burn buzzed AREA with a single species of bumble bee (sq. mi.) (Bombus crotchii) that was taking ad- vantage of snapdragon (Antirrhi- Clark County, Nevada 67 598 7,910 num) flowers. By our estimation, several thousand bumble bees were Mojave Natl. Preserve, California 58 305 2,500 foraging on that hillside at any one Pinnacles Natl. Mon., California 52 398 25 time. San Rafael Desert, 49 333 2,000 Snapdragon continued to bloom Curlew Valley, Idaho 43 340 1,930 substantially in subsequent years, yet bumble bees were few. Perhaps, Albany County, 40 194 4,273 like their flowered partners, bees Channel Islands, California 36 154 349 can be capricious too. The rela- Sand Mt. & Blow Sand Mt., Nevada 28 59 4.8 tionship is a complex one—bee population size is determined by New England 43 365 63,851 resource availability in the year prior to their emergence. Conversely, the Modified from Griswold et al. 1998. population size of annual plants de-

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 39 SUMMARY erence information for a wide array helped with the data management. of bees, some of whom have ranges Finally, thanks to Pat Lincoln and Our study suggests that this re- that extend far beyond the monu- Tom Stohlgren for editorial com- gion may be one of the hotspots of ment, but the consequences of their ments. bee diversity in the world. Com- fickle natures is ponderous. parisons with other well-studied bee These observations warrant ad- faunas in the United States (see ditional studies on many fronts: REFERENCES Table 3 on page 39) support this How do bees time their emergence contention, particularly when one with flowers? What, if any, safe- Barthell, J.F., T.L. Griswold, G.W. considers the much greater size and guards might bees (particularly spe- Frankie, and R.W. Thorp. 1997. habitat diversity of most of the other cialists) possess to ward off extinc- Osmia diversity at a site in central studies. Pinnacles, with significantly tion when flowers fail to flourish? coastal California. Pan-Pacific Ento- less than 1% (more like 0.001%) of And alternatively, what measures mologist 73:141–151. the total landmass of the contigu- might a plant incorporate for their Griswold, T., F.D. Parker, and V.J. Tepedino. 1998. The bees of the ous United States, is home to over own preservation in the face of in- San Rafael Desert: Implications for 10% of all US bee species, and 43% consistent bees? Further, such fluc- the bee fauna of the Grand Stair- of the genera. The diversity of bees tuations emphasize the importance case—Escalante National Monu- in Pinnacles compares favorably not of multi-year studies to document ment. In Learning from the land: only within the US but with other the full fauna of a pollinating com- Grand Staircase—Escalante National regions around the world. munity—the significant find of Monument Science Symposium Pro- A five-year study of a Mediter- Megachile davidsonii, for example, a ceedings, ed. L.M. Hill, pp. 23-34. ranean site in Greece amassed only bee collected in only one of the Cedar City, UT. 262 bee species (Petanidou and three years. Linsley, E.G. 1958. The ecology of Ellis 1993). Studies in a chaparral As stewards in Pinnacles Na- solitary bees. Hilgardia 27:543–599. community in yielded just tional Monument, managers must MacSwain, J.W., P.H. Raven, and R.W. 183 species (Moldenke 1976b). efficiently monitor long-term trends Thorp. 1973. Comparative behav- Even within the South Coast in inherently variable pollinator ior of bees and Onagraceae. IV. Clar- Range, Pinnacles may be unusu- populations. Such an in-depth un- kia bees of the western United States. University of California Publi- ally diverse. A four-year study of derstanding of pollinator faunas is cation in Entomology 70:1–80. Osmia in the UC Hastings Reserve, the first step to ensuring healthy Michener, C.D. 1979. Biogeography located less than 25 miles west of pollinator services in what increas- of the bees. Annals of the Missouri Pinnacles, resulted in 30 species ingly threatens to become an island Botanical Gardens 66:277–347. (Barthell et al. 1997) compared to in a sea of development. Conserv- Moldenke, A.R. 1976a. California pol- 37 within the monument (35% of ing such pollinator functions and lination ecology and vegetation all Osmia in California, 24% of the wealth of bee diversity it re- types. Phytologia 34:305–361. those in the US). Though com- quires is pivotal in maintaining the Moldenke, A.R. 1976b. Evolutionary parisons for other genera are not flowering fields of spring. history and diversity of the bee fau- available, such high numbers for nas of Chile and Pacific North Osmia are indicative of a rich di- America. Wasmann Journal of Biol- versity for other components of the ACKNOWLEDGMENTS ogy 34:147–178. bee fauna of Pinnacles. Petanidou, T. and W.N. Ellis. 1993. Three years of fieldwork have Our work in Pinnacles National Pollinating fauna of a phryganic ecosystem: composition and diver- demonstrated that the bees of Pin- Monument would not have been sity. Letters 1:9–22. nacles are diverse and ubiquitous. successful without the assistance and Thorp, R.W. 1979. Structural, behav- While the sheer numbers of bees encouragement of the monument ioral, and physiological adaptations encountered leave no doubt as to staff. We particularly want to thank of bees () for collecting pol- the importance of this often over- members of the resource division, len. Annals of the Missouri Botanical looked element, field observations Amy Fesnock, Larry Whalon, Tom Gardens 66:788–812. indicate that relationships between Leatherman, and Chad Moore. Thorp, R.W. 2000. The collection of pollinators and host plant popula- Thanks also to Melissa Andres and pollen by bees. Plant Systematics and tions are fluid across seasons and Carol Shultz, who assisted with the Evolution 222:211–223. sites. There remains little doubt that summer fieldwork; to Susanna bees and flowers are mutually de- Messinger, Wensdae Miller, and Olivia Messinger, USDA Bee Biology and pendent on each other. Indeed, for Gina Garvin for processing speci- Systematics Laboratory, Logan, UT, Pinnacles we now have floral pref- mens; and to Linda Kervin, who 84322-5310. [email protected]

40 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Diadasia, the sunflower bee, on . 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 . 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 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, , 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., ) 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 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 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 physodes – 00077 Ceanothus oliganthus✛ – 02068 Salix sessilifolia – 01034 ✛ – 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- , Eriophyllum Table 2 also lists the number of ictyon californicum, Heteromeles lanatum, and . 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]

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 49 Eschscholzia californica (California poppy) and other native plants in flower beds of the Peralta Garden, Berkeley. Photograph by G.W. Frankie. BEES IN BERKELEY? by Gordon W. Frankie, Robbin W. Thorp, Mary H. Schindler, Barbara Ertter, and Margaret Przybylski

he bee honey bees and bumble bees. In In our study, we have used ba- Thas received considerable California wildlands, bees are re- sic information on wildland bees study over the years by nu- garded as the most important group to ask new questions about bees in merous researchers who focused of pollinators. the urbanized environments of much of their attention on the sys- Much still remains to be learned northern California. More specifi- tematics, distribution, and biology about California bees, especially cally, we wanted to know if urban of bees in mostly wildland environ- about their dynamic relationships areas supported a low or high di- ments. Based on these studies, it is in the ever-changing landscape of versity of bee species. We also estimated that the highly diverse the state. Recent and ongoing stud- wanted to know how urban bees habitats of California probably ies are now focusing more on long- used floral resources of native and house about 1,500 species (Thorp, term bee population trends at spe- exotic plant species. pers. obs.); about 4,000 are thought cific sites, direct human impacts on To answer these two questions, to occur in the continental US. bees (e.g., destruction of habitat), we initiated a survey of urban bees The vast majority of these bees and interactions between exotic and and their host flowers in two cities are solitary in their life history habit, native bee species on exotic and na- in the San Francisco Bay Area in in contrast with the social habit of tive plant species. 1999. A progress report of this on-

50 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 going study is presented here; it is surable attraction were established: scheduled to continue through “Common” for averages of 5 or more 2003. It is noteworthy that with the bees per three minutes; “Occasional” exception of a few limited studies, for averages of 1 to <5 bees per little is known about bees in urban three minutes; and “Rare” if aver- California. ages were consistently low, ranging between 0.5 to <1 bees per three minutes. Extremely rare bee visits METHODS to flowers were noted but not tabu- lated for the purposes of this study. Bee surveys were conducted on The exotic honey bees (all Eu- ornamental plants in residential ropean) were separated from native neighborhoods of Albany and north bees in these counts. In some cases Berkeley in the San Francisco Bay there was not enough flowering veg- Megachilid bee (Megachile fidelis) drinking Area of northern California. Casual etation to make a standardized bee from disk flowers of the head of a member surveys of plants in flower and their count. In these situations, we esti- of the sunflower family. Photo-graph by bee visitors were made at least twice mated relative bee attraction (see R.E. Coville. each week from 1999 to 2002 by footnote 5 of Table 1 on page 52). walking through different streets At times it was difficult to iden- flower. The vast majority of these of both cities. Once bee-attractive tify certain plants, as some urban were exotic to the two East Bay plants were located, follow-up visits plants have numerous subspecies, cities and to northern California. were made to collect bees and quali- varieties, and cultivars. In most cases During the course of our intensive tatively assess relative attraction of it was possible to identify a plant to research period from 2001 to 2002, plants to their bee visitors. Voucher species or subspecies by using The we estimated that we had observed collections of host flowers were also Jepson Manual (1993) or the Sunset 600–700 plant species, subspecies, taken for later identification. Western Garden Book (2001). In other varieties, and cultivars in flower Bee visitation or frequency cases, we were only able to take the from March through October. counts were experimentally initi- plant to the genus level (e.g., Calen- Despite the great available di- ated in 2001 and were standardized dula, Lavandula, and Nepeta). Finally, versity of flowers at any given pe- in 2002 in the following manner. with the help of local nurseries and riod, only a small percentage of Flowering vegetation plots measur- their knowledge of local plant us- plants showed measurable attrac- ing 1.5m2 (or the equivalent in the age, we were also able to identify tion to honey bees or native bees. case of linear plantings) were ob- some plants to . Based on our visitation counts, only served for three minutes in order to Native and exotic ornamental about 5–10% of the flowering plants record the number of bees that en- plants were designated, and weedy examined in any given month had tered this space and made contact species were also noted. In the case measurable bee numbers. Plants with the reproductive parts of the of natives, we regarded a plant as that attracted bees for pollen or nec- flowers. The number of flower vis- native if it was known to occur natu- tar are listed alphabetically by ge- its by a given bee was not recorded. rally in northern California. Plants nus in Table 1 (see pages 52–54). Replications of bee counts were native to and About 75% of these plants are exot- made on the same plants (usually elsewhere outside the state were re- ics, whereas 25% are natives to different sides) and on other plants garded as exotics to the Berkeley northern California. In addition, of the same species whenever pos- and Albany areas. there was also a mixture of families sible. Counts were made on warm, and plant life forms (ranging from sunny days when temperatures were herbs to trees) among both exotic about 65˚ F or higher during a pe- SURVEY RESULTS and native plants that attracted bees. riod of high atmospheric pressure. In general, honey bee and na- Plants with dense flowering in sun- The residential environments of tive bee populations appear to be exposed sites were selected for Albany and Berkeley contain ex- low in Albany and Berkeley, as evi- counts whenever possible. The ba- tremely diverse offerings of exotic denced by the relative counts of sic guideline was to record bee vis- and native plant elements. For ex- both bee groups (see “Attraction” its under the most optimal plant ample, in a given two-hour walk column of Table 1). Most of the 72 and climatic conditions. through either city during spring “bee plants” listed in Table 1 at- Based on average count data, the or summer, it was common to ob- tracted honey bees (44 plant spe- following three categories of mea- serve about 200 plant types in cies or 61%) and native bees (62

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 51 5 5

5

5 5

4

R

R-O

5

5

PERIOD HB NB

5 bees per 3 min.

>

3

ve.

REWARD

2

Ex N Sum. – R-O

Ex N Sum. O O Ex N Sum. O R

PLANT FLORAL FLOWERING ATTRACTION

ORIGIN

1

5 bees per 3 min.; C = common, A

<

ve. 1-

ound cover; V = vine

r, Sh)r, Ex N Spr. R R

California buckeye (Tr) NC N Sum. R R Lily of the nile (H) Ex N Spr.-Sum. R

Honeywart (H) Ex N Spr. – R-O

Lilac (Sh) NC N Spr. O-C O-C Lilac (Sh) NC N Spr. O O-C

Rock rose (Sh) Ex N Spr.-Sum. R

e, Ave. <0.5-1 bee per 3 min.; O = occasional, A e, Ave.

(Asteraceae) Marguerite, Paris daisy (Sh)

Y) COMMON NAME (PLANT FORM)

(Amaranthaceae)

(Asteraceae) Dusty miller (W/H) Ex N, P Sum. O O

(Asteraceae) Cape weed (Gc) Ex P Spr.-Sum. – R

‘Sunset’ (Cistaceae)

(Onagraceae) Elegant clarkia (H) NC N Spr. R-O R-O

(Rosaceae) Hawthorn (Tr) Ex N P, Spr. C –

(Rhamaceae) Lilac (Sh) NC N Spr. ? O

(Hippocastanaceae)

(Liliaceae) Lily (H) Ex? N Sum. O R

(Rosaceae) Cotoneaster (Sh)

(Asteraceae) Cosmos (H) Ex P Sum. – C

(Boraginaceae) Borage (H) Ex N Spr. C R-O

(Rosaceae) thorn (Tr) Washington Ex N Sum. C O

‘Purpurascens’ (Boraginaceae)

(Asteraceae) Shasta Daisy (W/H) Ex P Spr.-Sum. – R-O

(Rosaceae) Cotoneaster (Sh)

‘Julia Phelps’ (Rhamaceae) ‘Ray Hartman’ (Rhamaceae)

spp. (Asteraceae) Marigold (H) Ex P Spr. – R-O

pulverulentus

spp. (Rutaceae) Orange, Lemon (T

TABLE 1. PLANTS AND BEES IN BERKELEY TABLE 1. PLANTS AND BEES IN BERKELEY

1. Plant form: Tr = tree; Sh = shrub; W/H = woody and herbaceous; H = herbaceous; Gc = gr 1. Plant form: Tr 2. NC = native to northern California; Ex = exotic to northern California 3. P = pollen; N = nectar 4. HB = Honey bee; NB = Native bee; R = rar

5. Estimated visitation frequency

TABLE 1. PLANTS AND BEES IN BERKELEY

Flowering plant species and their relative attraction to honeybees and native California bees in Albany and Berkeley.

PLANT SPECIES (FAMIL

Aesculus californica Agapanthus orientalis

Alstroemeria aurea Borago officinalis Calendula Ceanothus cuneatus

Ceanothus

Cerinthe major

Chrysanthemum frutescens Ceanothus C. maximum Centaurea cineraria Centaurea Cistus

Citrus

C. phaenopyrum Clarkia unguiculata Cosmos bipinnatus Cotoneaster lacteus C. franchetii Crataegus laevigata

TABLE 1. PLANTS AND BEES IN BERKELEY TABLE 1. PLANTS AND BEES IN BERKELEY

52 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 5

4

O

5

PERIOD HB NB

3

REWARD

2

Ex N Sum. C R

Ex P Spr.-Sum. – R-O

Ex N Sum. O O

NC N Sum. ? C

NC P Spr. – R-O

NC N Spr.-Sum. – R

Ex N Sum.Ex C N O Spr R O

NC N Sum.Ex O N C Spr.-Sum. – O

Ex N Sum. C –

PLANT FLORAL FLOWERING ATTRACTION

ORIGIN

1

Frades escallonia (Sh)

Wax-leaf privet (Sh) Wax-leaf

(Rosaceae) Fernleaf Catalina ironwood (Tr) Ex N Sum. C O

asplenifolius

ssp.

(Polemoniaceae) Globe gilia (H) NC N Spr. O O

Y) COMMON NAME (PLANT FORM)

(Polygonaceae) San Miguel Island buckwheat (H)

(Asteraceae) Daisy fleabane (H, Gc) Mexican daisy,

(Rosaceae) Sh) (Tr, Toyon NC N Sum. C O

(Papaveraceae) California poppy (H)

(Polygonaceae) Buckwheat (Sh) Ex N Sum. R R

‘Texanum’ (Oleaceae) ‘Texanum’

(Scrophulariaceae) Sticky monkeyflower (Sh)

‘Fradesii’ (Escallaceae)

() Horehound (W/H)

(Rosaceae) Pt. Reyes (H, Gc)

‘Bicolor’ () Shrub mallow (Sh) Ex N Spr.-Sum. R ?

(Brassicaceae) Sweet alyssum (H)

(Geraniaceae) bill (H, Gc) Crane’s Ex N Spr. – R

capitata

nica

() Blazing star (H) NC P Spr. – O

(Rosaceae) Ocean spray (Sh)

(Boraginaceae) Echium (Sh) Ex N P, Spr. C O

(Scrophulariaceae) (W/H) Toadflax Ex N Sum. – O

(Rosaceae) Crab apple (Tr) Ex N Spr. O O

rubescens

ssp.

(Oleaceae) California privet (Sh)

japonicum

sp. (Geraniaceae) Geranium (H) Ex N Spr.-Sum. R O

spp. (Lamiaceae) Lavender (W/H) Ex N Spr.-Sum. O R-O

sp. (prostr.) (Asteraceae)sp. (prostr.) Gumplant (H) NC N P, Sum. R

var. var.

spp. (Fabaceae) Lupine (W/H) NC N Spr. – R

floribunda

‘Blue Elf’ (Scrophulariaceae) (Sh) Veronica Ex N Sum. R R-O

Echium candicans Erigeron karvinskianus Eriogonum arborescens E. grande Escallonia exoniensis Eschscholzia califor

Hebe Heteromeles arbutifolia Geranium incanum Holodiscus discolor Geranium Gilia capitata Grindelia Malus Marrubium vulgare Mentzelia lindleyi Horkelia marinensis Lobularia maritima Mimulus aurantiacus Lupinus Lyonothamnus floribundus Ligustrum L. ovalifolium purpurea

Lavandula Lavatera maritima

Key to 1–5: see page 52

PLANT SPECIES (FAMIL

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 53 5

5

5

5

4

R

R

R

5

5

5

PERIOD HB NB

3

REWARD

2

Ex N Sum. R O

Ex N Spr.-Sum. O O

NC N Sum. O O NC N P, Spr. O C

Ex N Spr. R R

Ex N Sum. R-O R-O Ex ?N P, Spr.-Sum. O

Ex N P, Spr. O O Ex N Sum. O O

Ex N Sum.Ex R N R Spr.-Sum. R-O O

PLANT FLORAL FLOWERING ATTRACTION

ORIGIN

1

) )

)

) )

cont. cont.

cont.

cont. cont.

( (

(

( (

Tansy leaf phacelia (H) Tansy

Coffeeberry (Sh) NC N Sum. C –

Cleveland sage, California blue sage (W/H)

Indigo spires salvia Ex N Sum. R R

Y) COMMON NAME (PLANT FORM)

(Geraniaceae) Scented geranium (Sh)

‘Midnight’ (Scrophulariaceae) Midnight penstemon (W/H)

(Lamiaceae) Rosemary (Sh) Ex N Spr. O R

(Lamiaceae) blue curls (Sh) Woolly Ex N Sum. O R

(Hydrophyllaceae)

‘Mound San Bruno’ (Rhamnaceae)

(Dipsacaceae) Pincushion flower (H)

(Polygonaceae) Knotweed Ex N Spr.-Sum. R R

(Lamiaceae) Purple sage (Sh) Ex N Spr. O O

(Pittosporaceae) Japanese mock orange (Sh)

vel. aff. (Lamiaceae) Coyote mint (W/H)

(Papavaraceae) Oriental poppy (H)

(Lamiaceae)

(Fabaceae) White clover (H)

(Rosaceae) (Tr) Hollyleaf cherry NC P Spr..-Sum. C R

(Rutaceae) (W/H) Ex N Spr.-Sum. R

(Verbenaceae) Lippia (H, Gc) Ex N Sum. R –

(Lamiaceae) Mint (H) NC N Spr. O O

(Rosaceae) Himalayan blackberry (V)

(Lamiaceae) Catmint, catnip (H)

(Rosaceae) Sh) Portugal laurel (Tr, Ex P Spr.-Sum. – O

(Fabaceae) (H) Vetch Ex N Spr. R

sp. (Rosaceae) Sh) (Tr, Firethorn Ex N Spr. R-C –

tanacetifolia

spp.

‘Indigo Spires’ (Lamiaceae)

‘Nozomi’ (Rosaceae) Nozomi rose (Gc) Ex P Sum. – R

Monardella villosa Monardella Phacelia

Pelargonium graveolens Penstemon gloxinioides

Nepeta Phyla nodiflora Pittosporum tobira Persicaria capitata Prunus ilicifolia P. lusitanica P. Pyracantha Rhamnus californica Papaver orientale Rosa

Rosmarinus officinalis Rubus discolor Ruta graveolens

Salvia clevelandii Salvia villosa Vicia Salvia ?leucophylla Scabiosa columbaria Stachys bullata Trichostema lanatum Trichostema Trifolium repens Trifolium

Key to 1–5: see page 52

TABLE 1. PLANTS AND BEES IN BERKELEY TABLE 1. PLANTS AND BEES IN BERKELEY

TABLE 1. PLANTS AND BEES IN BERKELEY

PLANT SPECIES (FAMIL

TABLE 1. PLANTS AND BEES IN BERKELEY TABLE 1. PLANTS AND BEES IN BERKELEY

54 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 plant species or 86%) at the Rare or Occasional levels. Relatively few plants attracted either honey bees (13 plant species or 18%) or native bees (7 plant species or 10%) at the Common level. About 65% of the plants in Table 1 mutually attracted honey bees and native bees. When they occurred together on the same flowers, there was no evidence that either bee attempted to prevent the other from gathering pollen or nec- tar, a phenomenon known as “in- terference competition.” For many plant types, bee visi- tation frequency varied from one flower patch to the next, which is reflected in the attraction ranges shown in the last column of Table 1. The low end of the ranges usually occurred where host flowers were relatively isolated from other attrac- Horkelia marinensis (Pt. Reyes horkelia) being visited by a bumble bee (). tive flowering plants in an urban Photograph by B. Ertter. landscape. The high end generally occurred when a host plant was spp. received frequent visits from extent, in several residential gar- grouped together with several other diverse native bees. In surrounding dens containing eight or more at- bee-attractive plants in a garden. urban areas, these plants usually re- tractive plant species flowering at Increased attraction to host ceived only rare or no measurable the same time. These gardens also flowers was especially noticeable visits. It is noteworthy that honey had a relatively diverse group of when large numbers of attractive bee abundance in both gardens was native bees (7–10 species) as well as flowering plants were planted in about the same as in surrounding higher visitation frequencies. close proximity to each other. Two areas of Albany and Berkeley. Overall bee diversity was sur- excellent examples are the Peralta Not only were native bees more prisingly high in the two East Bay Community Garden in the Berke- abundant overall, but there was also cities. Five families, 20 genera, and ley flatlands and the UC Berkeley a greater diversity of native bees 74 species were recorded from net- Oxford Tract in the student com- visiting flowers. The Peralta Gar- ted bee collections on flowers over munity garden of the College of den had approximately 20 native a three-year period from 1999 to Natural Resources. bee species visiting a wide variety of 2002 (see Table 2, page 56). Three Native bees, in particular, were exotic and native plant species (15– groups of bees were most conspicu- more abundant on flowers in these 20 in any given month). The Ox- ously observed on any given collec- two gardens, and this was reflected ford Tract, which is only one-third tion day: the European honey bee in higher visitation counts on sev- the size of the Peralta Garden and (Apis mellifera), bumble bees (Bombus eral plants. For example, Califor- contains one-third its plant diver- spp.), and leafcutter or mason bees nia poppies in both gardens at- sity, also had approximately 20 na- (usually Megachile and Osmia of the tracted two to three bee species at tive bee species visiting a wide vari- Megachilidae). the Common level, whereas pop- ety of exotic and native plants. Only the European honey bee pies in all surrounding areas of Al- Given their small size, Peralta and one megachilid, Megachile bany and Berkeley only rarely at- at 0.25 hectare (one hectare is 100 rotundata (the alfalfa leafcutting tracted native bees, and then usu- m2) and Oxford at 0.1 hectare, each bee), are exotic to California and ally bumble bees. garden had an unusually high di- the New World. Although bee col- In the Peralta Garden, plants versity of bee species present. This lection records are still considered such as major ‘purpur- may, in part, be due to the fact that incomplete for many plant species, ascens’, Cistus pulverulentus ‘Sunset’, both gardens were managed with- preliminary data suggest that many Clarkia unguiculata, Calendula spp., out the use of pesticides. This pat- bee species have a wide range of Erigeron karvinskianus, and Lupinus tern was evident, although to a lesser host plants.

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 55 otic plants (approximately 600 types) TABLE 2. MAJOR BEE TAXA FOUND IN and native plants (approximately 50 ALBANY AND BERKELEY types) that have been surveyed to date. Bee Families Genera Nos. of Species Despite small patch size, low numbers of attractive plants, and of- ANDRENIDAE Andrena 15 ten wide spacing among plants of APIDAE Anthophora 4 the same species, we recorded a Apis mellifera1 1 much higher overall diversity of na- Bombus 3 tive bee species than expected. Many Ceratina 2 bees seem to be able to locate their Habrapoda 1 preferred plants, as indicated by bee Melissodes 1 type(s) on given plant species being Nomada 4 generally consistent through time. Synhalonia 1 For example, California poppies Xylocopa 1 commonly attracted bumble bees COLLETIDAE Hylaeus 5 and a few small bees of the family Halictidae. Himalayan blackberries HALICTIDAE Agapostemon 1 consistently attracted a wide variety Halictus 1 of leafcutter bees, bumble bees, and Lasioglossum 12 honey bees. Cosmos regularly at- Sphecodes 1 tracted large anthophorid bees of MEGACHILIDAE Anthidium 1 the family Apidae. Dusty Miller, Coelioxys 2 Centaurea cineraria, regularly at- Hoplitis 1 tracted males and females of large Megachile2 8 megachilids. It should be stressed Osmia 9 again that some native bee collec- tions were taken from plants that Totals: 5 Families 20 Genera 74 Species received only extremely rare visits, 1. Apis mellifera is the exotic European honey bee from the Old World. and these records were not listed in 2. Megachile rotundata is an exotic species from the Old World. Table 1. Indirect evidence suggests that honey bees were much more com- DISCUSSION two reasons. First, many horticul- mon on ornamental plants of Al- tural selections have reduced re- bany and Berkeley several years ago. In comparison to the relatively wards (pollen and nectar) for bees During our study, many home gar- large-sized patches of native plants as a result of commercial attempts deners observed that honey bee that were once part of the San Fran- to produce larger or more showy numbers have gone down notice- cisco East Bay natural landscape flowers. One example is the selec- ably during the past 10 years or so. (and still are in many places), the tion of for multiple petals at This downturn in numbers seems urban landscape consists of very the expense of pollen-bearing sta- to correspond well with the intro- small patches of both native and mens. Second, native bees have no duction of parasitic tracheal and exotic plants. Moreover, although historical (evolutionary) relation- varroa mites into California honey diversity of flowers in urban areas ship with exotic plants. bee populations. is high—600 to 700 plant species, A good indicator of the histori- Furthermore, some plant spe- subspecies, varieties, and cultivars cal connection between bees and cies that characteristically attracted have been seen to date in Albany floral hosts is the fact that northern high honey bee numbers in the past and Berkeley—only a small per- California native plants were at least had relatively modest visitations by centage have shown a measurable four times more likely to attract this bee, including Trifolium repens attraction to bees. measurable numbers of native bees and Phyla nodiflora. We believe that The vast majority of these plants than exotic plants. This emerging if this study had been conducted 10 are exotics to northern California. pattern is based on a comparison of to 15 years ago, we would have re- The relatively low attraction of bees, absolute numbers of exotic (53) and corded higher numbers on many of especially native bees, to exotic native (19) “bee plants” in Table 1 the plants that were attractive to plants is to be expected for at least with the estimated number of ex- honey bees.

56 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Although estimates of bee at- traction frequencies (as shown in the last column of Table 1) were developed entirely within the cities of Albany and Berkeley, these fre- quencies and associated bee types should generally be expected in adjacent and nearby San Francisco East Bay cities on the same plant species. For example, during the summer of 2002 we evaluated about a dozen ornamental plant species in Martinez (about 12 miles or 19 km north of Berkeley), which also occur commonly in Berkeley. Most of the same bee species were at- tracted to these plants and at the same frequencies. Differences were observed, however, in the cases of catmint (Nepeta sp.), Shasta daisy garden (which can range widely in (Chrysanthemum maximum), flea- size), this grouping tends to attract bane (Erigeron karvinskianus), and a greater number and diversity of marigold species (Calendula), all of bee species. In these situations, it which had more frequent bee visits appears that flowering patches con- in Martinez. taining the bee-attractive plants As our study continues, we will need to be equivalent to at least be introducing various California one meter in diameter in order to native plant species into urban draw in a diverse population of gardens in Albany and Berkeley in bees. order to evaluate the relative at- So far we have identified urban traction of resident bee populations plants that are attractive to native to these plants. Candidate plants bees, and have also suggested ways scheduled for testing include Helian- to increase the number of bees in thus annuus (California sunflower), urban yards. But why would one California natives visited by native bees in urban gardens: Horkelia marinensis (Pt. (gumplant), Rosa want to increase bee numbers? Reyes horkelia) (top) and Rosa californica californica (California wild rose), Don’t bees sting, and aren’t bee (California rose) (bottom). Photographs Salvia mellifera (black sage), and stings dangerous to humans? These by B. Ertter. Lythrum californicum (California are questions asked frequently by loosestrife). home gardeners. and protect bees as human devel- We will also be testing a few There are several reasons why it opment continues to destroy wild relatively noninvasive plants such is desirable to have bees in your habitats. as Lotus corniculatus and Trichostema yard. On a global level, scientific On a more personal level, it is lanceolatum, which are known to be evidence is mounting that pollina- fascinating to observe bees taking high-quality nectar resources for tors are declining. Not only are bees, pollen and nectar from flowers. In native bees. All of the above plants like other wild animals, a critical this regard, bumble bees, which are flower for long time periods, a con- part of our natural environment, large and easy to see, can be ap- dition favorable for bees. but they also provide a valuable en- proached relatively closely to make One unique urban bee pattern vironmental service when they pol- these observations. Other interest- did emerge from our study, sug- linate our fruit and vegetable crop ing behaviors include male territo- gesting that grouping bee-attrac- plants. rial patrolling (looking for females) tive plants together in the future Urban areas may provide im- around several flowers by some will increase bee visitations, espe- portant habitats for greater num- large leafcutter bees and large apid cially of native bee species. When bers of bee species than previously bees (Melissodes). Sleeping aggrega- many (eight or more) attractive bee suspected. If so, this might help in tions of large male apid bees in plants are planted together in one ongoing global efforts to conserve cosmos flowers are common and

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 57 lected valuable bee and floral host records for the project. Volunteer high school students from Oak- land, working through a student environmental education program at the Oakland Zoo, also assisted in collecting bees and host flower information.

REFERENCES

Barthell, J.F. and H.V. Daly. 1995. Male size variation and mating site fidelity in a population of Habropoda depressa (Hymenoptera: Antho- phoridae). Pan-Pacific Entomologist 71:137–141. Barthell, J.F., D.M. Bromberger, H.V. Daly, and R.W. Thorp. 1999. Nest- ing biology of the solitary digger bee Habropoda depressa (Hymenoptera: Anthophoridae) in urban and island environments. Journal of the Kansas Entomological Society 71(2):116–136. Buchmann, S.L. and G.P. Nabhan. 1996. The Forgotten Pollinators. Is- land Press, Covelo, CA. Chemsak, J.A. and R.W. Thorp. 1962. Note on the sleeping habits of males of Melissodes robustior Cockerell (Hy- menoptera: Apoidea). Pan-Pacific Entomologist 38(1):53–55. Grissell, E. 2001. Insects and Gardens. Timber Press, Portland, Oregon. Frankie, G.W., R.W. Thorp, et al. Mixed plantings of native and non-native species in Peralta Garden, Berkeley. 1998. Monitoring solitary bees in Photograph by G.W. Frankie. modified wildland habitats: Impli- cations for bee ecology and conser- easily observed in late summer and yards, give us a sense of pleasure vation. Environmental Entomology early fall. knowing that wild organisms can 27:1137–1148. You need not fear being stung make productive use of artificial ur- Linsley, E.G. and J.W. MacSwain. since bees only use their stinger ban environments. In the case of 1959. Ethology of some Ranunculus defensively when inadvertently bees, all but two species (see Table insects with emphasis on competi- grabbed or stepped on with bare 2) are native Californians. tion for pollen. University of Cali- fornia Publications in Entomology feet—something more likely to oc- For more information and up- 16:1–46. cur in a lawn that contains white dates on our study, visit the City Moldenke, A.R. 1976. California pol- clover or some other desirable low- Bugs website: www.cnr.berkeley.edu/ lination ecology and vegetation growing flower. Care should also citybugs. types. Phytologia 34:305–361. be taken around nests of bumble Schmidt, M.G. 1980. Growing Califor- bees, as some species can be quite nia native plants. California Natural defensive against would-be intrud- ACKNOWLEDGMENTS History Guides: 45. University of ers. It should be emphasized that California Press, Berkeley. only female bees sting; males of all The California Agricultural Ex- bee species lack this capacity. periment Station provided major Gordon W. Frankie, 201 Wellman Hall Bees, like birds and butterflies support for this research. Jerry #3112, UC, Berkeley, CA 94720-3112. and many other animals in our Powell and Jaclyn Kohleriter col- [email protected]

58 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 FARMSCAPE ECOLOGY OF A NATIVE STINK BUG IN THE SACRAMENTO VALLEY by Les E. Ehler, Corin G. Pease, and Rachael F. Long

tink bugs are pests of crops tight clusters on the undersides of is the consperse stink bug, Euschistus Sthroughout tropical and tem- leaves. There are five nymphal conspersus. Adults overwinter in leaf perate regions of the world. stages or instars; the first instar nor- litter, then break diapause and Adults are generally long-lived and mally does not feed, whereas the emerge in mid to late March. This typically deposit clutches of eggs in remaining ones (and the adults) feed species produces two generations primarily on developing seed and per year. The first develops on ex- fruit. Such feeding can reduce both otic, spring-time weeds such as com- yield and quality of the harvested mon mustard (Brassica kaber), black product. mustard (B. nigra), wild radish Crucifer and legume pods are (Raphanus sativus), and cheeseweed major foods for both nymphs and (Malva parviflora). By early June, adults. However, these foods tend the spring generation is complete. to be ephemeral, so a sequence of Adults from this generation seek host plants is usually necessary for new hosts such as tomato, because development of successive genera- weedy hosts from the spring have tions during the growing season. In dried up and are no longer suitable temperate climates, adults from the for the development of offspring. last generation enter a reproductive The second generation devel- diapause (an arrest in development) ops primarily on tomato, a major and spend the winter months in pro- crop in the Sacramento Valley. This tected places, such as beneath leaf is not necessarily because of a pref- litter or under the bark of trees. erence for this crop, but because In the spring, the surviving tomato is about the only suitable adults mate and seek out suitable host available for much of the sum- host plants for feeding and repro- mer. Feeding by adults and nymphs duction. Hosts for the first genera- on developing fruit results in white, tion of stink bugs are typically corky lesions that become apparent non-crop plants, especially weeds. as the fruit ripens, reducing fruit Subsequent generations develop on yield and quality. By the end of crops such as soybean, cotton, rice, summer, adults from the second pepper, bean, or tomato. generation enter a reproductive In this article, we outline the diapause and disperse to over- seasonal life history of a native stink wintering sites that are well drained bug and describe how replacing and have a sufficient layer of leaf exotic weeds with native perennial litter. One of the most common grasses can be employed in stink- over-wintering habitats is black- bug management. We also note the berry (Rubus spp.) leaf litter, par- importance of economic benefits ticularly in riparian zones. linked to the restoration of native The consperse stink bug has a vegetation in agricultural landscapes. complex of natural enemies, includ- ing both native and exotic species. Native scelionid wasps, such as CONSPERSE Gryon obesum, Telenomus podisi, and STINK BUG Trissolcus euschisti, parasitize the eggs, typically exploiting the entire Egg mass, nymph, and adult of consperse In the Sacramento Valley, there egg mass. Eggs also are eaten by stink bug. Photographs by J.K. Clark, UC are several species of native stink predators, especially by exotic spe- Statewide IPM Program. bugs. However, the major crop pest cies such as the Argentine

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 59 (Linepithema humile) and common important refuge for native plants pillbug (Armadillidium vulgare). and wildlife. In such cases, weed These two predators can be espe- management is a more promising cially important during the spring. approach. Also, a number of native predators The weeds in question are typi- feed on the smaller nymphs. cally part of roadside vegetation that However, these natural enemies is dominated by exotic species. In can be slow to colonize tomato the spring, wild radish, black mus- crops, allowing stink-bug popula- tard, and cheeseweed are common tions to reach damaging levels. As along roadsides, often within a few a result, growers frequently apply feet of a developing tomato crop. chemical insecticides such as meth- The most obvious solution is to re- amidophos, a highly toxic organo- move these weedy hosts, either phosphate material, for stink-bug chemically or mechanically. This is control. being practiced by a number of to- mato growers in the area. Unfortu- nately, much of this weedy vegeta- FARMSCAPE tion is on highway rights-of-way, ECOLOGY and thus is not under the grower’s control. For a tomato grower in the Sac- An alternative approach to weed ramento Valley, managing the management is restoration of na- consperse stink bug should take into tive vegetation, especially native account the whole farm or “farm- perennial grasses, along roadsides scape,” not just the tomato crop. A adjacent to riparian vegetation and typical farmscape in the region tomato fields. This should also be consists of a mixture of habitat of interest to governmental agen- patches, such as bare ground, non- cies that are responsible for manag- crop vegetation (e.g., weeds), ripar- ing roadside vegetation. ian areas, and cultivated crops. The term farmscape describes this within-farm configuration of habi- FARMSCAPING WITH tat patches. Farmscaping deals with NATIVE GRASSES the modification of agricultural settings, such as planting hedge- Some farmers in Yolo County rows of trees, shrubs, and perennial are currently engaged in farm- grasses on the farm. There are three scaping with native perennial grasses essential components to the farm- as part of a roadside restoration scape ecology of the consperse stink project with the Yolo County Re- bug in the Sacramento Valley: habi- source Conservation District. Sev- tat for overwintering, exotic weeds eral native grasses are being grown, for development of the first gen- usually a mix of the following: eration, and tomatoes for develop- purple needlegrass (Nassella pulchra), ment of the second generation. nodding needlegrass (Nassella cer- Tomato growers who report nua), California onion grass (Melica stink-bug damage often have all californica), one-sided bluegrass (Poa three components on their farm, secunda var. secunda), and blue wild Farmscape ecology of the consperse stink bug in the Sacramento Valley: Adult stink typically in close proximity. In such rye (Elymus glaucus). bugs overwinter in riparian areas (top). cases, the key to managing con- Native grasses are seeded in the First stink bug generation develops on sperse stink bug is prevention—i.e., fall into prepared seed beds. Weeds cheeseweed, mustard, and wild radish by removing overwintering sites or are controlled during the first three (middle). Second stink bug generation managing weedy vegetation in the years of establishment by mowing, develops on tomato (bottom). Photo- graphs by Yolo County Resource spring. Unfortunately, the con- burning, hoeing, or applying herbi- Conservation District (upper) and J.K. sperse stink bug often overwinters cides. Once established, native Clark (middle, lower). in riparian vegetation, which is an grasses can provide nearly 100%

60 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 up of the consperse stink bug. In- stead, the main goal was restoration and conservation of native grasses. The impetus for a grower or land owner to adopt such a practice de- pended on his or her environmen- tal ethic and philosophy of land stewardship. This is perhaps why the practice has not been widely adopted in Yolo County. What has been missing in this equation is a practical or economic benefit to roadside restoration. Now there is such a benefit in the form of pest reduction. We believe that, in highly agricultural regions, such eco- nomic benefits to growers and land owners will be essential in imple- menting and sustaining ecological restoration of native vegetation. In summary, we believe that Roadside restoration of native perennial grasses next to a tomato field in Yolo County. widespread adoption of roadside Photograph by L.E. Ehler. restoration with native perennial grasses would have a major impact cover. This is apparently sufficient However, not all native peren- on populations of the consperse to outcompete cheeseweed, mus- nial grasses are suitable for use in stink bug in the Sacramento Val- tards, and wild radish, thus preclud- roadside restoration projects adja- ley. This would presumably reduce ing development of the first gen- cent to tomato fields. A good ex- the need for chemical insecticides eration of consperse stink bug at ample is deergrass (Muhlenbergia in tomato crops; because such in- that site. rigens), a relatively large bunchgrass secticides are costly and tomato These native perennial grasses that has well drained, protected prices are relatively low, increas- are poor hosts for consperse stink spaces near the base of the plant ing profits is of great concern to bug. Our research has shown that that are suitable overwintering sites farmers. We are currently working these bugs generally do not occur in for a variety of insects, including with interested tomato growers and these roadside grasses during the the consperse stink bug. However, processors to bring this vision to spring, except in those cases where deergrass also is a suitable over- fruition. poor management has allowed weedy wintering site for beneficial insects, hosts of the bugs to invade. Also, such as ladybird beetles and preda- consperse stink bug does not appear ceous bugs. In some cases, we REFERENCES to overwinter in these grasses. have observed 100 or more conver- While we have not detected sig- gent ladybeetles per plant. Thus Bugg, R.L., C.S. Brown, and J.H. nificant numbers of other crop pests deergrass could be used to con- Anderson. 1997. Restoring native in the roadside grasses, we do find serve beneficial species in situations perennial grasses to rural roadsides beneficial insects such as hover flies, where the consperse stink bug or in the Sacramento Valley of Cali- green lacewings, ladybird beetles, and other potential pests it might har- fornia: Establishment and evalua- tion. Restoration Ecology 5:214–228. damsel bugs on the grasses during bor are of little or no concern to Ehler, L.E. 2000. Farmscape ecology of the spring, and have observed hover the farmer. stink bugs in northern California. flies and green lacewings feeding Memoirs, Thomas Say Publications on grass pollen. Thus, such roadside in Entomology, Entomological So- HIDDEN BENEFITS OF restoration may help sustain popula- HIDDEN BENEFITS OF ciety of America, Lanham, MD. tions of beneficial insects by provid- RESTORATION ing key resources (e.g., pollen, aphid L.E. Ehler, Department of Entomology, honeydew) during the spring, prior Roadside restoration of native University of California, One Shields to the development of pests on adja- grasses in Yolo County was not Avenue, Davis, CA 95616-8584. leehler cent crops such as tomato. originally designed to prevent build- @ucdavis.edu

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 61 ENDANGERED PLANTS AS GUIDES FOR SAVING ENDEMIC INSECTS IN CALIFORNIA by Daniel Rubinoff

alifornia has more species the most famous plants of Califor- In coastal sage scrub, the pres- Cfound only within its bor- nia: coast redwood (Sequoia semper- ence or absence of an endangered ders (endemics) than any virens) and Monterey pine (Pinus bird, the California gnatcatcher other state, including over 1,000 radiata). At first glance, plans to (Polioptila californica, Muscicapidae), kinds of plants by the latest esti- save the endemic plants might seem is being used to identify the size mates. Of these, 179 are endemic certain to save the insects depen- and configuration of habitat frag- plants that are among the 292 spe- dent on them, but upon closer ex- ments that will be saved. Additional cies of plants and animals listed as amination, the shortcomings of a small plots with populations of en- endangered in California by the US species-based approach become dangered plants are also being pre- Fish and Wildlife Service. evident. served with the assumption that, in Current theories about the co- combination, these plant- and bird- evolution of plants and insects sug- based preserves will maintain a large SOUTHERN gest that many herbivorous insect measure of the region’s incredible groups may have achieved their tre- CALIFORNIA biodiversity. I decided to test the mendous richness by diversifying COASTAL SAGE wisdom of this practice using a few along with their flowering hosts. It SCRUB coastal sage scrub insects (see pho- might stand to reason then, that the tographs on pages 62 and 63). abundance of endemic plant spe- Coastal southern California Some of my recent research both cies in California would carry with hosts nearly 100 species that are in the field and using DNA in the it an intrinsically matched diversity designated or are being considered of insects, with particular insect spe- for protection under the Endan- This electra buckmoth (Hemileuca electra cies dependent on specific species gered Species Act. Many reside electra) female ovipositing near Eriogo-num of plants. wholly or partially in southern Cali- fasciculatum (flat top buckwheat) and the butterflies on opposite page (top) were Therefore, from a conservation fornia coastal sage scrub, which is significantly more sensitive to southern perspective, logic tells us that if we arguably one of the most endan- California coastal sage scrub just save some populations of each gered habitats in North America. It fragmentation than either the endemic of these endemic plants, we will also has been reduced to less than bird or plant species around which the save the unique insects dependent 162,000 hectares (one hectare is conservation plans were designed. Photo- graph by D. Rubinoff. on them. In general this has been 100m2), mostly in parts of River- the pattern for conservation plans side, Orange, and San Diego coun- to date. Conservation has been ties. Southern California coastal geared toward specific species (with sage scrub is home to 13 endan- the Endangered Species Act func- gered plant species that are found tioning as a cornerstone of envi- nowhere else, and represents a ronmental protection policies) hotspot of diversity. rather than toward endangered Conservation planning has been “ecosystems” or “habitat.” Unfor- intense and contentious in this re- tunately, when we take a closer look gion of rampant development. A at some of the areas where endemic dominant paradigm emerging from plants occur and then look for the the battles between conservation associated endemic insects in those organizations and developers has areas, the story is not nearly so been the use of “umbrella” species simple. to guide preservation of habitat. The In this paper, I present com- tacit assumption is: “Simply focus parative examples involving moths on a few areas where the umbrella and butterflies from California species occurs, and the rest of the coastal sage scrub, coastal sand sage scrub community will be shel- dunes, and associated with two of tered in those same fragments.”

62 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Virgulti metalmark (Apodemia virgulti) (left). • Bernardino blue (Euphilotes bernardino) (middle and right) female. All perched on Eriogonum fasciculatum (flat top buckwheat) host plant. Photographs by D. Rubinoff. laboratory revealed a subspecies of dependent on the same habitat, even gusts to travel across loose sand dur- the electra buckmoth (Hemileuca when the insects’ hostplants occur ing their daytime activity period. At electra, Saturniidae) apparently in the fragments. If we rely on night, or during high winds, the found only in southern California umbrella species like the gnat- moths exhibit another amazing (and coastal sage scrub. It was originally catcher, or the presence of typical novel) trait—they burrow down into thought to be genetically related to coastal sage scrub plants to indicate the sand and disappear, sheltered much larger populations to the east habitat fragments to be saved, we from predators and the elements. in the deserts of San Diego and will likely lose many of the coastal A burrowing, flightless moth Riverside counties, but DNA analy- sage scrub insect species. that runs around during the day on sis reveals the relationship to be far open sand?—Is it any surprise, then, more distant. that the genus and its one species CENTRAL One of the typical plants of the remained unknown to science until sage scrub community, California CALIFORNIA 1975, despite their occurrence in flat top buckwheat (Eriogonum fasci- COASTAL SAND a relatively accessible part of cen- culatum), is the only food plant of DUNES tral California? Unfortunately, the the coastal electra buckmoth. While moths have only been found at the flat top buckwheat is not endemic The Santa Maria dunes of San Santa Maria sand dune system and to coastal sage scrub, it and three Luis Obispo County harbor one of the habitat has been in decline since other plants—California sagebrush the most unusual moths known to before the moths were discovered. (Artemisia californica) and two sages science. The caterpillars are so Coastal sand dunes represent a (Salvia mellifera and S. apiana)—are adaptively modified to live beneath very restricted and unique mosaic usually dominant members of the the sand dunes that the UC Berke- of habitats. There are foredunes of southern California coastal sage ley entomologists who first collected unstabilized sand right against the scrub plant community. them did not recognize them as cat- ocean, adjacent to more vegetated, One might think it would be erpillars! stabilized dunes. Active dunes pre- easy to save the buckmoth—just set Similarly, the adults of Powell’s sent a unique challenge to plants, aside land for the gnatcatcher that flightless jumping sand dune moth also has the buckwheat host plant. (Areniscythris brachypteris, Scythri- Powell’s flightless jumping sand dune However, saving sage scrub insects didae) are hardly reminiscent of moth (Areniscythris brachypteris). Illus- like the electra buckmoth is more your average Lepidopteran (see im- tration by C. Green. • Powell’s flightless jumping sand dune moth in its sand dune complicated than setting aside habi- ages below). They are the only con- habitat. Photograph by J.A. Powell. tat with the host plant, even if the tinental moths in the world in which threatened gnatcatcher occurs in the adults of both sexes are flightless. habitat in good numbers. The moth, Although they can’t fly, they do and at least a few butterflies, re- scurry and jump, catching wind quire relatively larger plots of sage scrub than the bird or endangered sage scrub plants do to maintain populations. In southern Califor- nia coastal sage scrub, conservation planning for plant and bird species is not going to save endemic insects

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 63 of different plants as the advancing sand dunes bury them. Plants used include Phacelia distans (phacelia), Monardella crispa (coyote mint), Lu- pinus chamissonis (bush lupine), and Senecio blochmaniae (groundsel). So it is these specialized conditions, not a particular plant, that allow the moth to hang on. Sand dune habitat is threatened by sand mining, off-road vehicles, and other human activities that rip up and destroy vegetation, and by alien plants like iceplant or sea fig (Carpobrotus edulis) that stabilize the dunes, eliminating the active dune habitat. Efforts to save endemic dune plants may not necessarily save the dune insects, since it is the existence of moving sand in a very narrow strip next to vegetated areas that allows Powell’s flightless jumping sand dune moth to exist. If the sand stops moving, or the vegetation near it disappears, so will this entire ge- nus of moth, known only by this one charming and unusual species.

COAST REDWOOD

For a tree endemic to the Cali- Habitat for Powell’s flightless jumping sand dune moth. Note the presence of both fornia floristic province, the coast active sand and dune vegetation. Photograph by J.A. Powell. redwood (Sequoia sempervirens) is remarkable in how few insect spe- but those that have adapted to the endemic coastal strand plants. In cies it supports. Only five insects shifting landscape are rewarded with addition to Powell’s flightless jump- feed solely on its foliage. The red- a habitat relatively free of competi- ing sand dune moth, there are en- wood is a common sight in coastal tion. Once a dune becomes thor- demic species of grasshopper and northern California. While it oc- oughly vegetated, these active dune robber fly, the life histories of which curs in large swaths of contiguous specialists are quickly outcompeted are virtually unknown, and a possi- forest in the northern part of its and disappear. bly extinct species of long-horned range, redwood declines to a few Most of California’s sand dunes beetle which is known only from isolated riparian strips in steep can- originally harbored rare and spe- the first collected specimens. yons at its southern extreme in cialized plants and animals. For ex- While it is tempting to suspect Monterey County of central Cali- ample, San Francisco’s now van- that the flightless moth is restricted fornia. quished dune system had many en- because of a dependence on one of Although coast redwood is one demic species including the extinct the endemic sand dune plants, this of the most famous of the world’s Xerxes blue butterfly (Glaucopsyche turns out not to be the case. The natural wonders—it is renowned as xerxes Lycaenidae), whose name moths exist in a narrow strip at the the tallest living organism in the is now used by an organization edge of advancing sand dunes (see world—it still harbors a few secrets. (Xerxes Society) devoted to insect the above photograph). While the One such mystery is a newly dis- conservation. The Santa Maria adults steer clear of living vegeta- covered species of moth found near dune system is the largest remain- tion, the caterpillars form silk tubes the southern extent of the natural ing in California, and harbors 10 under the sand and feed on a variety range of redwood in Monterey and

64 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 Santa Cruz counties. The small moth is in the Tortricid genus Syn- demis and the caterpillar feeds only on redwood (see photographs be- low). Part of the reason this species remained unknown is because it is very rare to find one in moth light traps set out to survey nocturnal lepidopteran faunas. Jerry Powell at UC Berkeley and I recently stumbled upon a possible reason for this supposed rarity, al- most by accident. Because the moths were found so rarely in the light traps, we put out traps baited with the scent, or pheromone, of female syndemis moths, which are attrac- tive to males, and placed them in a redwood canyon at the University of California Big Creek reserve in Monterey County. These pheromone traps, to- gether with the typical light traps, were left out all night, but by early morning only one moth had come. Because of some daytime field work, we didn’t retrieve the pheromone traps until noon, but by then more than 50 moths had arrived and by late afternoon more than 100 males had been caught (see photograph on page 66). For a number of years we had University of California Big Creek Reserve, showing strip of redwood trees along been looking for these moths at creek bottom, flanked by Artemisia californica (California sagebrush) dominated chaparral night, but as we learned, they are on south-facing slopes. Photograph by J.A. Powell. active during the day—an unre- corded habit in the genus. The only because scientists had been vested, or if global warming elimi- redwood syndemis had escaped looking in the right place at the nates the trees from the southern notice and was thought to be rare wrong time. Perhaps this denizen outposts of its range, one of the of the chilly central coast switched very few insects that evolved with Redwood syndemis (Syndemis sp.) cater- activity periods to avoid the cold this famous symbol of California pillar on redwood foliage. Photographs and foggy summer nights. may disappear even while its more by D. Rubinoff. Those interested in saving this famous host plant survives. unusual insect might think the best place to find or conserve a redwood- feeding moth would be in the large MONTEREY PINE areas of forest in the northern part of the state. However, the red- Monterey pine (Pinus radiata) wood syndemis has only been found is possibly the most important in- in the narrow, isolated, redwood- troduced timber tree in the south- bottomed canyons of Monterey ern hemisphere, grown extensively County, with one specimen re- within Australia and especially New corded from the nearby Santa Cruz Zealand. Despite this abundance in Mountains. Should the southern the southern hemisphere and else- redwood groves end up being har- where in the world, Monterey pine

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 65 Botanists are still unsure why health is harder to evaluate and is the Monterey pine was restricted to certainly more nebulous than pro- three small groves, since it grows so tecting a particular species of con- easily when introduced elsewhere. cern, but it is clear that species- It is possible that the pine syndemis based conservation plans can leave moth, which remains restricted to gaps large enough to cause the loss the endemic groves, may be able to of endemic insects. Adult male redwood syndemis (Syndemis sp.), perched after flying to pheromone give us some insight into this ques- Continued research and careful lure at midday. Photograph by D. tion. Monterey pine as a species is planning to preserve not just the Rubinoff. now planted throughout the globe, plant species, but also particular eco- but unless the original groves along logical features of unique floral was originally one of the most California’s central coast are saved communities, is the only way we’ll restricted trees in North America. from development and threats like preserve not only California’s Prior to human intervention, it the deadly pitch canker, the rela- unique plants, but also the endemic was endemic to just three groves tionship between this endemic tree insects in whose company they along the central California coast: and its moth will become a part of evolved. Cambria Pines, San Luis Obispo history. County, the southern extreme of its range; Carmel area of Monterey ACKNOWLEDGMENTS County in the middle of its range; WHERE DO WE GO and Año Nuevo, San Mateo FROM HERE? I thank G. Frankie, J. Powell, County, in the northern portion of and J. Sabet-Peyman for comments its range. California’s large number of on the manuscript, the staff of While the pine has now been endemic plants and animals present and Año Nuevo State widely planted, the original groves a special challenge and responsibil- parks for research permits, J. Smiley are in sharp decline due to an intro- ity to those interested in preserving for access to UC Big Creek Re- duced pitch canker pathogen and natural history. Although endemic serve, and C. Niwa for pheromone are considered endangered. A rela- plants and insects may share the lures. Research was supported by tive of the aforementioned redwood same habitat, their conservation a National Science Foundation syndemis moth is endemic to these needs are not identical. Even con- PEET grant and the Monterey three original Monterey pine groves servation planning that assures the Pine Forest Ecology Cooperative. and is also new to science (see pho- survival of the plants upon which tograph below). Even though the rare insects feed does not guarantee pine has been planted just over the that the invertebrates will persist. REFERENCES coastal mountains in the San Fran- Reduced and fragmented habitat, cisco Bay Area, the Monterey pine specific microhabitat requirements, Hickman, J.C., ed. 1993. The Jepson syndemis has not spread from the and an array of unknown factors manual: Higher plants of Califor- nia. University of California Press, original groves. DNA analysis sug- may contribute to the disappear- Berkeley, CA. gests that the pine syndemis popu- ance of endemic insects, even while Powell, J.A. 1976. A remarkable new lations in the three original groves their host plants thrive. genus of brachypterous moth from are isolated from each other, indi- The preceding examples illus- coastal sand dunes in California cating that these moths may not be trate how little is known about our (Lepidoptera: Gelechioidea, Scyth- able to travel between the isolated endemic insect fauna. Many taxa rididae). Annals of the Entomological groves. are newly discovered or have re- Society of America 69:325–339. quirements that are poorly known. Powell, J.A. 1981. Endangered habi- tats for insects: California coastal Syndemis in California. Top row: redwood Microhabitats with subtly different sand dunes. Atala 6:41–55. syndemis; Middle row: Monterey pine conditions must be identified and Rubinoff, D. 2001. Evaluating the syndemis; Bottom row: “typical”-looking explored, even where plant com- Syndemis found from Sierra Nevada and California gnatcatcher as an um- Cascade mountains through to the munities are apparently identical. brella species for conservation of Eastern US. Photograph by D. Rubinoff. But this task can be prohibitively coastal sage scrub. Conservation time-consuming. Biology 15:1374–1383. Perhaps the only tenable solu- tion to this conservation conundrum Daniel Rubinoff, Department of Ento- lies in regional or habitat-based con- mology, University of Hawai’i, Honolulu, servation planning. Ecosystem Hawai’i 96822. [email protected]

66 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 NOTES AND COMMENTS

PLANT PROTECTION and other current laws and regula- though admittedly inadequate and NOT A GIVEN tions. CNPS and the Native Plant uncertain, of federal funding to im- Conservation Campaign (NPCC) are prove management, conserve habitat, Don’t take plant protection for working to raise awareness of this in- or even increase population sizes. granted: environmental protections appropriate imbalance between pro- Moreover, though the Sodaville are being assaulted by the current ad- tection afforded to imperiled plants milk-vetch is state-listed in both Cali- ministration on a number of levels. and animals. Consult the NPCC web fornia and Nevada, state listing pro- Emily Roberson, CNPS Senior Pol- site for additional information (www. vides questionable protection. State icy Analist, has compiled an excellent cnps.org/NPCC). governments, laws, priorities, and list entitled “Federal Environmental Though we agree that the on-the- budgets constantly change. For ex- Proposals Affecting Native Plants, ground benefit of each listing decision ample, California is currently facing a Public Lands, Waters, and Biologi- should be considered, listing determi- budget shortfall in excess of $30 bil- cal Diversity.” nations under the ESA should be lion. Such an enormous deficit can based solely on biological data and threaten conservation programs for This list can be viewed on the CNPS threat information. Congress specifi- California-listed plants and animals. In website, www.cnps.org/NPCC, and pro- cally mandated that the listing process the current climate, it is imperative posed rules open for comment can be be based on species status only, exclud- that we employ all possible avenues accessed by searching by agency at ing economic impacts or other factors. available to achieve long-term conser- www.regulations.gov. If listing determinations are based on vation, even if they seem redundant A particularly helpful website on concern about “lack of awareness” of in the short term. the Bush environmental record and private landowners or other extrane- As an aside, the final listing deter- agenda is at www.nrdc.org—click “Bush ous issues, would this not erode the mination (in this case, to withdraw) Record.” intent of the ESA and integrity of the was made over five years beyond the federal list? one-year timeline for such decisions For selected issues, see the Native If landowner misunderstanding of as mandated by the ESA, and only Plant Conservation Campaign web- the consequences of federal listing is then in response to a CNPS lawsuit. site, www.cnps.org/NPCC—click a problem, we suggest that an appro- In summary, we agree with More- “Make A Difference.” priate role for the US Fish and Wild- field that the ESA does not always If you would like to receive “NPCC life Service (FWS) would be to edu- provide consistent conservation of News” (e-mail news on native plant sci- cate landowners in order to dispel such imperiled plants, and that many land- ence and conservation) send a request unwarranted concerns, rather than to owners and other members of the to [email protected]. retreat from controversy and fail to list public have serious misconceptions a biologically-deserving taxon. CNPS about the benefits and restrictions of Send letters to agencies and public offi- has long worked to educate the public the law. However, we do not believe cials, and to Preident G.W. Bush (The about the ESA, and its provisions for these are sufficient reasons to decline White House, 1600 Pennsylvania Ave. flexibility and opportunities to mini- to list species which meet the legal and NW, Washington DC, 20500). mize adverse economic impacts that biological listing criteria, particularly may be associated with listings. We in this era of unprecedented habitat would welcome the opportunity to and species loss. LETTERS TO THE work with the FWS to spread this Emily B. Roberson EDITOR message more widely. Importantly, it is the opinion of CNPS Senior Policy Analyst CNPS that federal listing would have Sodaville milk-vetch David P. Tibor afforded additional conservation ben- CNPS Rare Plant Botanist Dear Editor, efit to this taxon. Federal listing pro- We read with interest the Letter to vides an additional set of management San Diego Covservation Plan the Editor from James D. Morefield requirements and conservation stan- [Volume 30, No. 2] regarding the “in- dards. Listing would also result in the Dear Editor, explicable” withdrawal of the Sodaville development of a federal recovery plan This letter is written in response milk-vetch (Astragalus lentiginosus var. to help coordinate conservation action to the article “Understanding the sesquimetralis) from the federal listing among landowners and state and fed- Political Realities of Regional Con- process. The letter raises some excel- eral governments. Recovery plans can servation Planning” by Allison Rolfe lent points. lead to new research which may be in the July/October 2001 Fremontia. We concur that plants receive “sec- critical to successful conservation of That article contained a general ond class” treatment under the Fed- highly restricted and imperiled taxa. discussion of habitat conservation eral Endangered Species Act (ESA) Listing can also provide a source, planning, but it specifically focused

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 67 on one plan in the incorporated City the plan. In fact, it is likely to occur at The increased growth rate in popu- of San Diego. a faster rate. The areas being set aside lation, coupled with the large number As you may recall, the Natural as part of the preserve systems must of unusual and rare species in San Di- Communities Conservation Planning be preserved “in perpetuity.”) ego County, were leading this region (NCCP) Act was enacted as a State This is a major accomplishment toward what former Secretary of In- program to conform to the Federal that has had a positive effect on land terior Bruce Babbitt described as a Endangered Species Act. A group of use planning in the region. The suc- “train wreck.” Furthermore, as the jurisdictions in San Diego County cess of the County of San Diego number of individual species listed as generated a local plan, referred to as MSCP has raised its visibility as a bal- rare and endangered by the State or the Multiple Species Conservation anced approach to planning. Due to Federal Government began to grow, Program (MSCP) Plan, and this plan coordinated support from govern- the County, wildlife agencies, and conforms to the NCCP process. It mental, environmental, and building property owners scrambled to deter- should be clarified that within the industry groups, the County has ob- mine the most appropriate way these overall MSCP, each jurisdiction must tained consistent funding from local, species could be protected. This of- independently approve a subarea plan state, federal, and private sources for ten resulted in decisions that were to obtain a permit from the Califor- the acquisition of open space from both confusing and in conflict with nia Department of Fish and Game and willing sellers for permanent preser- economic growth issues. US Fish and Wildlife Service (Wild- vation. That is, when species are listed on a life Agencies). The MSCP serves as a In addition, several thousand acres case by case basis in a non-coordinated framework plan. Subarea plans are have been set aside as part of the fashion, as species were listed, it was limited to a particular area or jurisdic- MSCP for mitigation of development necessary to scramble to determine the tion and must conform to the frame- projects. The County of San Diego most appropriate way that the species work plan. (In the case of the County recently celebrated its Fifth Anniver- should be protected while at the same of San Diego, there will ultimately be sary since the adoption of the MSCP. time deal with economic growth is- three separate subareas, the existing A major positive spillover effect that sues. It was a situation resulting in one covering the southwestern part of has emerged from this program is that conflicts from inefficiency, lack of co- the County, a North County subarea, biologically diverse lands located ordination, and continually having to and an East County subarea to deal within future MSCP subareas in deal with additional new species and with the size and diversity of habitats northern and eastern San Diego their mitigation. The overall effect of and ownerships.) County have received increased inter- the MSCP is that it has provided for a The San Diego County subarea est from conservationists, and are be- large, connected preserve area that plan, adopted by the Board of Super- ing acquired as permanent open space addresses a number of species at the visors in 1997, is for the unincorpo- from a growing number of willing sell- habitat level, rather than species-by- rated area only and is separate and dis- ers. The County has worked with pri- species and area-by-area. tinct from the City of San Diego sub- vate groups including the Nature area plan or plans for other cities Conservancy and the Trust for Public Practical Progress within the MSCP. Ms. Rolfe is appar- Lands, as well as the Anza Borrego ently most familiar with the City of Desert Foundation, to complete these Under the heading “Practical Prob- San Diego subarea plan. Therefore, I transactions. It is interesting to note lems,” Ms. Rolfe states that there are would like to present the positive as- that since the adoption of the MSCP, inherent incongruities between the pects of the County of San Diego The Nature Conservancy and Na- “reactive safety net of the CESA and MSCP subarea plan and the NCCP tional Wildlife Federation have FESA (California and Federal Endan- in general. opened local offices in San Diego. gered Species Acts) and the proactive Without the MSCP, a continual mission of the NCCP program.” On process of piecemeal development the other hand, a program that ad- Benefits of the Plan with postage stamp preserves existed dresses biological issues on a regional Of primary importance, the NCCP in the San Diego region. Though the scale by protecting large blocks of and MSCP programs acknowledge California Environmental Quality Act habitat for rare and endangered spe- that large blocks of habitat are impor- required reduction and mitigation of cies should not be considered in con- tant in the San Diego region due to impacts from development projects, as flict with the ESA response to species the diversity of species and habitats development occurred it usually cre- in jeopardy of extinction. that exist here. The implementation ated small areas of open space that The NCCP program enhances the of the MSCP, a 50-year program, has were often disconnected from other ESA by providing a means to deal with had the effect of providing a strong habitat areas, and sometimes too small a number of species at the same time. scientific basis for creating large, con- to support any significant populations San Diego County and other loca- tiguous, and viable preserve areas. of wildlife. While County planning tions in California are considered “hot (Note: The Federal and State Permits staff made an effort to connect these spots” for containing unique and un- are effective for 50 years. The assump- areas, the end result was a series of iso- usual species. The only means to tion was that it might take 50 years to lated and potentially ineffective miti- accommodate the protective needs of assemble the entire preserve system in gation sites. a large number of rare and endangered

68 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 California Plant Life PESTS OF THE NATIVE CALIFORNIA INTRODUCTION TO TREES OF THE CONIFERS SAN FRANCISCO BAY REGION David L. Wood, Thomas W. Koerber, Glenn Keator Robert F. Scharpf, and Andrew J. Storer This guidebook, with its easy-to-use keys, inform- “An important compilation of information on ative species accounts, and copious illustrations, major pathogens, insects, and other pests of is the perfect guide to California’s native and nat- conifers. Because conifers are of tremendous uralized trees for those who want a handy, ecological and economic importance in authoritative manual to carry into the field. California, this book will fill a unique niche.” California Natural History Guides, $29.95 cloth, $14.95 paper —Dave M. Rizzo, University of California, Davis California Natural History Guides, $48.00 cloth, $19.95 paper PLANTS OF THE SAN FRANCISCO BAY REGION INTRODUCTION TO CALIFORNIA Mendocino to Monterey PLANT LIFE Linda H. Beidleman and Eugene N. Kozloff Robert Ornduff, Phyllis M. Faber, and REVISED EDITION Todd Keeler- “A good guide for students and beginning nature REVISED EDITION lovers, though even sophisticated plant enthusi- “Packed with new information, this revised guide asts will consult it for its easy style and useful will delight both the well informed and the novice.” photos.” —Peter Raven, —Frank Almeda, California Academy of Sciences Director of the Missouri Botanical Garden $60.00 cloth, $29.95 paper California Natural History Guides, $39.95 cloth, $16.95 paper INTRODUCTION TO SHORE INTRODUCTION TO CALIFORNIA WILDFLOWERS OF CALIFORNIA, MOUNTAIN WILDFLOWERS OREGON, AND WASHINGTON Philip A. Munz Philip A. Munz Edited by Dianne Lake and Phyllis Faber Edited by Dianne Lake and Phyllis Faber New Introduction by Robert Ornduff New Introduction by Robert Ornduff REVISED EDITION REVISED EDITION First published in 1963, this convenient guide is This new edition describes more plants, includes now available in a fully updated and revised edi- helpful hints for identifying species, and incorpo- tion that reflects the many advances in botany rates new taxonomic and distribution informa- that have occurred in the past forty years. tion of the diverse coastal habitats of the spec- $39.95 cloth, $16.95 paper California Natural History Guides, tacular Pacific Coast. California Natural History Guides, $39.95 cloth, $16.95 paper NATURAL HISTORY OF THE ISLANDS OF CALIFORNIA Allan A. Schoenherr, C. Robert Feldmeth, and Michael J. Emerson Illustrations by David Mooney and Michael J. Emerson At bookstores or order New in Paperback—“This wonderfully illustrated (800) 822-6657 • www.ucpress.edu book is an extraordinary guide for visitors to these islands and a fascinating work of natural UNIVERSITY OF history for those limited to an armchair view.” CALIFORNIA PRESS —Audubon Magazine California Natural History Guides, $24.95 paper

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 69 species is to address them together in By building upon an established ship efforts, habitat conservation plans a multiple-species type of habitat plan. cooperative relationship with the wild- will continue to save significant sen- life agencies and other partners, the sitive lands. County has been able to embark on Measuring Success Thomas A. Oberbauer subarea plan development for the Environmental Resource Manager, It is obvious that the multiple spe- northern and eastern portions of the Dept. of Planning and Land Use, cies planning process is not also able MSCP. These additional subarea plans County of San Diego to address the other regional issues of will enlarge the County’s open space water quality, transportation, and af- preserve for the enjoyment of genera- fordable housing. It was never de- tions of Californians. ERRATA signed to do that, and the process of While the program and process dealing with endangered species is may not always be implemented in a Volume 30, No. 2, page 9. At the complicated enough. However, manner desired by all parties, it is the bottom of Table 2 in the article by through the MSCP—and its ability to only major program that has demon- Ellen Dean, the footnote, “Angro- work in a collaborative effort with lo- strated any success in the conserva- sperm Phylogeny Group,” should cal, state, and federal government tion of entire habitat areas. While Ms. be “Angiosperm Phylogeny Group.” agencies, landowners, conservancies, Rolfe points out what she considers For more information about this and other stakeholders—the County deficiencies in some specific plans, it group and links to synonyms for mod- has been able to conserve long-term is important to remember that the ern interpretations of plant classifica- viable populations of the federal- and overall effect of this planning process tion, see www.systbot.uu.se/classification/ state-listed species and their habitats. is highly positive. Through partner- APG.html.

BOOKS RECEIVED

Xeriscape Plant Guide: 100 Water-Wise Plants for Gardens and the design process soil; compost, Water-Wise Plants for Gardens and Landscapes, D. Winger, Ed. 1998. mulch, and fertilizer; planting and de- Landscapes, by Denver Water Con- Fulcrum Publishing, Golden CO. 62 velopment, health and maintenance; servation Office, with Introduction by pages. A companion to Xeriscape Plant and applying water. Price $24.95, R. Proctor. 1996. Fulcrum Publishing, Guide described above, with same size softcover. Golden CO. 184 pages. Although writ- and format, but information summa- Mediterranean Gardening: A ten as a general guide for many states rized and re-arranged according to Water-Wise Approach, by H. with arid environments, this beauti- plant form or flower color. Price Gildemeister. 1995. 2002, First Cali- fully designed volume includes many $15.95, softcover. fornia Edition. UC Press, Berkeley, California natives. Each entry includes Xeriscape Handbook: A How-To CA. 208 pages. This beautifully de- photograph(s), color illustration(s), Guide to Natural, Resource-Wise signed book with attractive photo- and comments on landscape use, form, Gardening, by G. Weinstein. 1999. graphs was originally written for the native range, characteristics, culture, Fulcrum Publishing, Golden CO. 142 Mediterranean region, but will be use- best features, companion plants, and pages. A companion to Xeriscape Plant ful in California because of its climate, disadvantages. Price $27.95, softcover. Guide described above, with same size and does include some California na- Xeriscape Color Guide: 100 and format. Chapters include: climate; tive species. $24.95, softcover.

BOOK REVIEW

Flowering Plants and Ferns of Local floras provide a floristic clar- (which Ertter herself identifies, then , California, by B. ity analogous to the increasing mag- rationalizes). However awkward this Ertter and M.L. Bowerman. 2002. nification of a microscope. If The method might seem to some readers, CNPS Press, Sacramento, CA. 424 Jepson Manual is the naked-eye view it makes historical comparison easier. pages. Hardcover, $34.95; softcover, of the California flora, then the revised The interweaving of new material and $19.95. flora of Mt. Diablo is a 40-fold mag- the original occurs throughout the This new edition of Bowerman’s nification. Nearly six decades elapsed book in prefaces, introductory essays original flora has been fully revised (1944 to 2002) before this sorely (soils, geology, paleobotany, vegeta- and updated by UC Jepson Herbarium needed revision finally appeared. tion, floristics), and under the discus- botanist, Barbara Ertter. It includes The Mt. Diablo flora interweaves sion of each plant. over 700 species, with the addition text from the first edition with exten- The catalog of plants is organized of over 200 native and naturalized sive new material. Some might quibble in the Englerian sequence, which, al- species. about this as an awkward juxtaposition though it offers the advantage of plac-

70 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002 ing similar families together, can be a CONTRIBUTORS (cont’d) Mary H. Schindler, BA, is a labora- bit of a challenge for me at times; tory and research assistant in the Di- when under the influence of a fine- Nikki Nicola is a research technician vision of Insect Biology, College of scented April day, I am less likely to based in Davis, CA who has worked Natural Resources, University of Cali- forget alphabetical arrangement. An on the native bee project since 1999. fornia, Berkeley. index only partially solves this di- Corin G. Pease is a graduate student Peter C. Schroeder, PhD, is an ad- lemma. Fortunately a list of page in Plant Protection and Pest Manage- junct professor and instructor of biol- numbers for families is available as a ment at the University of California, ogy at Southern Oregon University in supplemental sheet. Davis. Ashland. Nearly 900 taxa are illuminated in Jerry A. Powell, PhD, is a professor Sarah A. Smith is a doctoral candi- this small, convenient field guide (the date in Ecology and Evolutionary paperback edition weighs only about of the Graduate School, Division of Insect Biology, College of Natural Biology at Princeton University and 1.5 pounds). A failure of many recent an EPA-STAR fellow. Her disserta- county floras is the lack of voucher Resources, University of California, Berkeley. tion research is on pollination services citations. Ertter inspected and anno- in northern California. tated thousands of specimens, build- Margaret Przybylski was a labora- Andrew J. Storer, D.Phil., is an as- ing upon the vouchers cited originally tory assistant in the Division of Insect sistant professor of Forest Insect Ecol- by Bowerman. Sometimes names are Biology, College of Natural Re- ogy, School of Forest Resources and changed, but the reasons for changed sources, University of California, Ber- keley. Environmental Science, Michgian determinations are fully discussed. Technological University, Houghton. About one-quarter of the book fo- Daniel Rubinoff, PhD, is an assistant cuses on the vegetation, while the professor of Entomology in the De- Robbin W. Thorp, PhD, is an emeri- remainder treats the flora consisting partment of Plant and Environmen- tus professor of entomology at the University of California, Davis. of 841 taxa, an increase of 26% over tal Protection Sciences at the Univer- the 1944 edition. The value of the Mt. sity of Hawai’i, Honolulu. Neal Williams, PhD, is a Smith Na- Diablo flora rests not just in its list of Katherine N. Schick, PhD, is a cu- ture Conservancy Postdoctoral Fellow. documented taxa—Ertter provides ratorial assistant at the Essig Museum David L. Wood, PhD, is a professor explicit rationale for a list of rejected of Entomology at the University of emeritus and professor of the Gradu- records. Of most direct value are lists California at Berkeley. She specializes ate School, Division of Insect Biology, of potential disappearances and de- in the : gall wasps, in- College of Natural Resources, Univer- clines (5% of the flora), naturalized quilines, and their parasitoid relatives. sity of California, Berkeley. aliens (14% of the flora in 1944 in- creasing to 22%), waifs, and horticul- tural relics (aliens that have not yet become established). The change in CLASSIFIED ADS the composition of Mt. Diablo’s flora is striking, which makes the original material by Bowerman on vegetation Classified ad rate: $1.00 per word, shipping in USA. P.O. Box 4978, Arcata, minimum $15; payment in advance. CA 95518. www.telosrarebulbs.com. and specific sites (springs, ponds, and Address advertising inquiries and copy to: unusual habitats) nearly as valuable as CNPS, 1722 J Street, Suite 17, Sacra- ECOLOGICAL RESTORATION mento, CA 95814. (916) 447-2677 or fax permanent plot analysis. Native California grassland and desert (916) 447-2727. This volume should serve as the ecological restoration standards and model for other local flora revisions. PUBLICATIONS costs, plus pictures showing results. Several floras on the CNPS bookshelf www.ecoseeds. com/standards.html. Flora & Fauna Books, 121 First Avenue warrant immediate attention using South, Seattle WA 98104, Tel. (206) ART the Ertter model, particularly those of 623-4727, Fax (206) 623-2001, ffbooks California wildflower prints & free the Mount Hamilton Range (Kern @blarg.net, Specializing in Botany, wildflower screensavers. Visit www. Gardening, Birding, and Ecology, both County) and of Marin County. The wildflowergreetings.com or call Alice new and out-of-print. We carry a large (877) 432-2999 toll-free. 1944 first edition of the Flora of Mt. inventory of floras, keys, and field guides Diablo is now rare and valuable (I could for the west coast and worldwide. A Notecards, Prints, and Originals. not find a used copy for sale on the large selection of our inventory is now Visit www.VorobikBotanicArt.com. internet). Those of us fortunate available on the web: www.abebooks.com/ PO Box 866, Lopez Island, WA 98261 enough to have a copy—likely dog- home/FFBOOK/. SERVICES eared from repeated stuffing in and NURSERIES AND SEEDS Nature landscape design. Landscape out of a knapsack—can now stow it Telos Rare Bulbs. Bulbs for your gar- safely away on the bookshelf, while we Design that celebrates the rich heritage den, restoration projects, landscaping. of California’s native flora. Duber Land- shift to using this fine new revision. Many Calif. native species, including scape Design, CA license #4316. (510) Calochortus, Fritillaria, Brodiaea rela- 524-8665. Dean Taylor, tives, Erythronium. Catalog $3.00. Free Santa Cruz Chapter

VOLUME 30:3–4, JULY/OCTOBER 2002 FREMONTIA 71 FROM THE EDITOR

e are very fortunate in this larvae of “micro moths” to the spe- pollinators. The implication of the last Wspecial issue of Fremontia cialist or generalist foraging behavior two facts is that more native plant to have several excellent of bees. habitats in cities and adjacent to crop- articles portraying relationships be- For example, did you know that lands will support native bee popula- tween native plants and their insect as- scientists can identify the pattern of a tions, which would in turn be an asset sociates. Gordon Frankie, Convening leaf mine scar to the genus of micro to farmers. In addition, plantings of Editor, and other expert contributors moth that makes it? Or that the some- purple needle grass, Nassella pulchra, have written articles that expand our times apple-sized oak galls are made adjacent to tomato crops could signi- attention from the plant alone to how by wasps smaller in size than an ant? ficantly reduce the populations of native plants fit into their world, what Or that there are more species of bark stink bug pests, and thus reduce the they provide for other organisms, and beetles alone in the world than there use of insecticides. I hope that you are how human-made changes affect not are species in Califor- as inspired and edified by this selec- only plant populations but their asso- nia? I have learned that sometimes up tion of articles as I am, so that we can ciated insect species. The authors de- to a dozen species of bumble bees can continue to educate others about the scribe the great variety of insects oc- coexist in an area as small as 100 values of native plants and their natu- curring in various habitats and offer square meters, that native bees are ral environments. amazing facts about their behaviors abundant in urban areas, and that and life cycles, from the leaf mining native bees can be important crop- Linda Ann Vorobik, Editor

CONTRIBUTORS

Robert Bugg, PhD, is with the Sustainable Agriculture Research and Education Program at University of Califor- nia at Davis.

Les E. Ehler, PhD, is a professor in the Department of

Address Service Requested Service Address

1722 J St., Suite 17 Suite St., J 1722 Sacramento, CA 95814 CA Sacramento, Entomology, University of California, Davis. Society Plant Native California Barbara Ertter, PhD, is curator of vascular plants of west- ern North America at the Jepson and University Herbaria, University of California, Berkeley. Carol S. Ferguson, PhD, is an associate professor of biol- ogy at Southern Oregon University. Gordon Frankie, PhD, is a professor in the Division of Insect Biology, College of Natural Resources, University of California, Berkeley. Terry Griswold, PhD, is a researcher at the USDA Bee Biology and Systematics Laboratory, Logan, UT. Claire Kremen, PhD, is an assistant professor of Conser- vation Biology in the Department of Ecology and Evolu- tionary Biology at Princeton University. Rachael F. Long is a farm advisor, Yolo County Coopera- tive Extension, Woodland, CA. Olivia Messinger is a graduate student at Utah State Uni- versity and technician with the USDA Bee Biology and Sys-

tematics Laboratory, Logan. Postage U.S.

Nonprofit Org. Nonprofit Permit # 3729 # Permit

(continued on page 71) CA Oakland, PAID

FREMONTIA EDITORIAL ADVISORY BOARD Ann Bradley; Travis Columbus; Susan D’Alcamo-Potter; Ellen Dean; Kathleen Dickey; Phyllis M. Faber; Bart O’Brien; John Sawyer; Jim Shevock; Teresa Sholars; Nevin Smith; Dieter Wilken; John Willoughby; Darrell Wright 72 FREMONTIA VOLUME 30:3–4, JULY/OCTOBER 2002