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Breeding Biologies, Seed Production and Species-Rich Bee Guilds of Cleome Lutea and Cleome Serrulata (Cleomaceae)

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Breeding Biologies, Seed Production and Species-Rich Bee Guilds of Cleome Lutea and Cleome Serrulata (Cleomaceae) Plant Species Biology (2008) 23, 152–158 doi: 10.1111/j.1442-1984.2008.00224.x Breeding biologies, seed production and species-rich bee guilds of Cleome lutea and Cleome serrulata (Cleomaceae) JAMES H. CANE US Department of Agriculture–Agricultural Research Service, Bee Biology and Systematics Laboratory, Utah State University, Logan 84322–5310, United States of America Abstract The summer-blooming annual forbs Cleome lutea and Cleome serrulata (Cleomaceae) are native across the US Intermountain West and Rocky Mountains, respectively. Their farmed seed is sought to help rehabilitate western rangelands in those regions. This study of the reproductive biologies and pollinator faunas of C. lutea and C. serrulata is the first for this cosmopolitan family, the sister family to the Brassicaceae. Unlike the S-allele self-incompatibility systems of some Brassicaceae, both species of Cleome were found to be self-fertile and capable of some autogamy. Compared with selfing, outcrossing did not enhance seed set, seed viability or seedling vigor for either species (in fact, selfed progeny were more robust). Large, openly visited plants yielded >20 000 seeds each. Like several species of the sister family Capparaceae, flowers of both species first shed their pollen, secreted nectar and became receptive nocturnally. Although no nocturnal visitors were found, both Cleome species attracted a diverse array of diurnal native bees, wasps and butterflies. Among the many floral generalist bees that work Cleome flowers for pollen and nectar are two managed agricultural pollinators, Apis mellifera and Megachile rotun- data. These observations bode well for pollinating C. lutea and C. serrulata in small commercial seed fields. It appears that diverse wild bees would benefit from the addition of native Cleome to restoration seed mixes, with the objective of sustaining native polli- nator faunas during the first few years of postfire plant community rehabilitation. Keywords: Apiformes, Brassicaceae, Capparaceae, pollination, seedling fitness, self-compatibility. Received 3 January 2008; accepted 24 July 2008 Introduction the evolution of self-incompatibility systems in the Bras- sicaceae, and is certainly needed to successfully farm The small cosmopolitan eudicot family Cleomaceae (300 Cleome seed for large-scale rangeland restoration projects. species) is the sister family to the more diverse Brassi- Native species of Cleome might have a unique role to caceae; it also shares characters with the Capparaceae play in plant community restoration in xeric valleys and (= Capparidaceae), with which it has been formerly clas- plains of the US Intermountain West. Rehabilitating sified (Hall et al. 2002). Dominating the family Cleomaceae western USA rangeland plant communities has long are the 180–200 species of the type genus Cleome (called included reseeding, but primarily with grasses and ‘spider-flowers’ or ‘bee-plants’) that occur in many shrubs. Seed of several native forbs are now being grown warmer regions of the world (Iltis 1957; Sanchez-Acebo commercially for this purpose, with more to follow (Cane 2005). Some are annual forbs common in disturbed habi- 2008), but these are all herbaceous perennials that typi- tats; others are woody, but short-lived. Knowledge of the cally do not flower in the year after seeding. In contrast, breeding biologies of Cleome species might be relevant to Cleome are annuals that can provide bloom quickly and, if used by a diverse array of wild bees, might help sustain Correspondence: James H. Cane pollinator communities the year after an autumn restora- Email: [email protected] tion seeding. Larger quantities of affordable seed from Journal compilation © 2008 The Society for the Study of Species Biology No claim to original US government works POLLINATION NEEDS OF CLEOME 153 native Cleome species, if available from seed farmers, could be added to seed mixes that are used to rehabilitate vast burned rangelands of the Great Basin and neighboring biomes of western USA (Cane 2008). Farming seed crops generally requires pollinator supplementation to realize potential seed yields (Free 1993), but how much can depend on a plant species’ breeding biology. The Brassicaceae, sister group to the Cleomaceae, has a distinctive sporophytic incompatibility (SI) system (Charlesworth et al. 2005) and only pollen flow between plants sets seed. However, species of Cleome are early successional species at disturbed sites; such attributes in other species are often associated with self- fertility and autogamy (Baker & Stebbins 1965). Thus, eco- logical versus phylogenetic inferences give contrasting predictions for the pollination needs of Cleome. Fig. 1 Flower, fruits and seeds of Cleome lutea. Shown are the To evaluate the pollination needs of a plant, the breed- pistil atop its gynophore and the dehiscing anthers of this her- maphroditic flower, an immature and mature fruit (silique), and ing biology of the plant must be understood. The objec- its dehiscent valves removed to reveal the loop-like replum and tives of the present study were to characterize the floral the content of mature dark seeds. Inset: X-ray positive of C. lutea and breeding biologies of two of the six species in Cleome seeds showing viable (X-ray dense) and non-viable (gray) section Peritoma (Iltis 1957), Cleome lutea (yellow or embryos. Nevada bee-plant) and Cleome serrulata (Rocky Mountain bee-plant). The necessity or benefit of pollinators and cross-pollination was evaluated for producing fruits, magenta for C. serrulata). Hermaphroditic flowers have six fertile seeds and vigorous progeny. Flowering phenology stamens and a large pistil atop a stalked gynophore and the timing of stigma receptivity and anther dehis- (Fig. 1). Staminate flowers have rudimentary pistils that cence were characterized. Data from museum specimens never set pods (Stout 1923). However, Cleome are not and limited field collections of flower visitors to these andromonoecious. A staminate flower begins as a her- plants were also compiled to document pollinator species maphroditic bud; its pistil thereafter fails to develop fully. richness and the attributes of the pollinator guilds. When a raceme is shunting resources to many maturing fruits, most of its flowers become staminate. Over the long Materials and methods flowering season, racemes alternate between the produc- tion of staminate and hermaphroditic flowers (Murneek Traits of Cleome lutea and Cleome serrulata 1937); thus, maturing siliques and shedding seed while Both species are robust, tap-rooted annuals native to the continuing to bloom. xeric valleys and plains of western North America. They Daily blooming phenologies were observed on plants are typically found at disturbed sites, such as waste grown in two common gardens in Logan, Utah, USA ′ ′ places, margins of washes or barren sandy desert plains (41°45 N, 111°48 W). To judge stigma receptivity, excised (Iltis 1957). Owing to its beauty, C. serrulata has been cul- pistils were individually inserted into a Pasteur pipette tip tivated in gardens in and beyond its native range in filled with hydrogen peroxide (J. Thomson, pers. comm., western USA. Plants of both species are erect (3–25 dm 1999). Receptivity was indicated by the visible generation tall), glabrous and malodorous. They invariably produce of oxygen bubbles on the bare stigma, the result of per- one or more compact, bracteolate terminal racemes. Indi- oxidase activity (Zeisler 1938). vidual racemes are indeterminate, continually producing new flowers for weeks during the summer. The round Breeding biology seeds (2–4 mm in diameter) are borne in siliques. The seeds lack an endosperm (Sanchez-Acebo 2005) and Seeds were commercially collected and pooled from wild require moist cold stratification for embryo development populations in Utah. The seeds were shallowly planted and germination. outdoors in autumn 2003 at the common garden of the Bee Biology and Systematics Laboratory in Logan, Utah, USA. The following summer, the clay loam soils were infre- Flowering quently irrigated as needed to maintain plant vigor. For Individual plants of both Cleome species produce two each of the four pollination treatments, six well-separated types of like-sized showy flowers (yellow for C. lutea and individuals per species of similar size, vigor and bud Plant Species Biology 23, 152–158 Journal compilation © 2008 The Society for the Study of Species Biology No claim to original US government works 154 J. H. CANE development were chosen, randomly assigned their medium grain industrial film) (Fig. 1) from lots of 20 treatment, and tagged. These plants were enclosed in seeds per species and color, representing all pollination 7m¥ 7m¥ 2 m walk-in field cages made of Lumite treatments. Persistently pale seeds and pale seeds that had screening (Synthetic Industries, Chicopee, GA, USA) to darkened 1 week after harvest were X-rayed again and exclude flower visitors. Individual pollinator exclusion their germination evaluated. Two lots of 10 dark seeds bags were not used because, in earlier trials, we found that each per species were weighed. flowers on the crowded tall racemes of Cleome transfered Three large, mature, intact plants of C. lutea were taken pollen by passively rubbing or jostling against the at the end of flower production. The life-time silique pro- bag netting. Once the flowers began to shed pollen, each duction per uncaged plant was determined by counting new flower on every tagged raceme was marked and their complements of siliques and replums (a loop of pollinated.
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