HAND-POLLINATION OF californica IMPROVES SEED SET

Kazuki Ariyoshi Emily Magnaghi, and Mark Frey

ABSTRACT

Hand-pollinating milkmaids (Cardamine californica

85%. In the Presidio of San Francisco, a district of the Golden Gate National Recreation Area in , our restoration efforts using milkmaids were hampered by low seed set of our locally adapted . Plants in 2 populations were successfully cross-pollinated by hand

are not available, we noted that germination of hand- pollinated seeds was at least 40% in the nursery. This

discuss the role of natural pollinators and the physical

maturation. Ariyoshi K, Magnaghi E, Frey M. 2006. Hand-potlination of Cardamine californica improves seed set. Native Plants Journal 7(3):249-252.

KEY WORDS milkmaids, seed production, propagule, pollinator, reproduction,

NOMENCLATURE USDA NRCS (2006)

Figure 7. Milkmaids (Cardamine californica (Nutt.) Greene var. p integrifolia (Nutt.) Rollins [Brassicaceae]) hoto by Mark Frey

NATIVEPLANTs r FALL 2006

M ilkmaids (Cardamine californ i c a nursery records indicate low seed more than 5% of annual seed set (Nutt.) Greene var. set. In 2002 we collected only 25 from each population of any native integrifolia (Nutt.) Rollins seeds. In an attempt to increase seed species. [ B r a s sicaceae]) are a common native yields, a hand-pollination experiment All Presidio populations of species in California and Oregon. This was conducted in the field. We milkmaids are isolated from one peren- nial herb grows below 500 m hypothesized that hand-pollination another. Two populations were (1640 ft) in habitats such as open might: 1) reveal if milkmaids lack studied, located in areas of the meadows, hill slopes, and canyons the capability to effectively park called Log Cabin/Doyle (Hickman 1993). Plants can reproduce produce seeds; and 2) increase Drive South Corridor (Log from tuber-like rhizomes (Hickman the amount of seeds produced. Cabin) and Inspiration Point 1993) and generally grow in Natural Areas (Inspiration Point). clusters. At our location The Log Cabin population is (described below), we have noted that SITE DESCRIPTION located along a gravel road that milkmaids are one of the earliest spring extends from a parking lot and wildflowers, blooming January through Seven populations of milkmaids May. The closes its petals in late follows the edge of a seasonal grow on the 603 ha (1490 ac) Presidio afternoon as the sun goes down and wetland. This population is of San Francisco (Presidio), nods its pedicel before a rain, protect- divided and partially surrounded California. The Presidio is located ing the pollen (Fauver and others by California blackberry (Rubus within the Golden Gate National 1998). Synonyms include Dentaria ursinus Cham. & Schlecht. Recreation Area, at the northern integrifolia, D. califoruica var. [Rosaceae]) and Himalayan edge of San Francisco, on the integrifolia, Cardamine paucisecta, blackberry (R. armeniacus Focke C. integrifolia, and C. californica prol. south side of the Golden Gate [Rosaceae] ), both shrubs are up to 2 integrifolia. Bridge. The area's mediterranean-like m (8 ft) tall. Other associated Milkmaids can grow to a height of climate is moderated by the Pacific plants include various nonnative 20 to 70 cm (8 to 27 in) and develop Ocean, creating average species, such as common sheep sorrel both rhizomal and cauline leaves. temperatures of 14 °C (56 °F). An ( Rumex acetosella L. [Polygonacea] ), Rhizomal leaves number 1 to 3 per eastward onshore wind is predomi- poison hemlock (Conium maculatum L. (occasionally more), are always nant. The Presidio has many remnant [Apiaceae] ), common velvetgrass larger, make up the majority of the and restored habitats, such as (Holcus lanatus L. [Poaceae]), photosynthetic surface, and are usually serpentine grassland, coastal English plantain (Plantago lanceolata L. more fleshy (Deitling t936). Leaves on scrub, live oak woodland, coastal [Plantaginacea]), and shortpod mustard the rhizome generally have 3 leaflets, salt marsh, coastal foredune, and (Hirschfeldia incana L. Lagreze-Fossat which are simple, entire, and elliptic to riparian forest. Dominant vegetation [Brassicaceae]) and native species, round, tapering at the base. Cauline assemblages also include such as western blue-eyed grass leaves have 3 lobes or leaflets and are plantation forests of trees not native (Sisyrinclinun bellum S. Wats. short-petioled, linear to oblong in to the Presidio. These plantations [Iridaceae]), fringed willowherb shape, and generally entire. There are are populated by Monterey cypress (Epilobium ciliatum Raf. [Ona- also upper cauline leaves, which are lin- (Cupressus macrocarpa Hartw. ex graceae]), and slough sedge ear to oblong, entire, and sessile. The Gord. [Cupressaceae] ), Monterey (Carex obnupta Bailey [Cyperacea]). inflorescence is a raceme of white to pine (Pinus radiata D. Don [Pina- The Inspiration Point population light pink with 9 to 14 mm (0.3 ceae]), and blue gum eucalyptus is located in a serpentine grassland to 0.5 in) long petals. In fruit, the (Eucalyptus globulas Labill. near the top of a dry, north-facing pedicels are ascending 10 to 30 mm (0.4 [Myrtaceae]). slope. The grassland contains to 1.2 in) and the dehiscent siliques are The Presidio was an active Holcus lanatus L. [Poaceae], erect, 20 to 50 mm (0.8 to 2 in) long military base from 1776 to 1989. In Rumex acetosella [Poly- and 1.5 to 2 mm (.05 to .08 in) wide 1994, with its tr a n s fe r f r om t he gonaceae], and many native (Hickman 1993). US Army to the National Park species including stemless Although common in California, Service, the Presidio was designated morning-glory (Calystegia subacaulis milkmaids are uncommon in the for public use and habitat Hook. & Am. [Convolvulaceae]), and Presidio of San Francisco. Only 1 of the restoration commenced. The 7 known Presidio populations has more Presidio Native Plant Nursery is than 50 individuals. This species has run by the nonprofit Golden Gate been collected for propagation and

KAZUKI ARIYOSHI, EMILY MACNAGHI, AND MARK FREY NATIVEPLANTS I FALL 2006 METHODS contrast with the plant parts) for RESULTS immediate transport to another The log Cabin population was pollinated population. When a receptive stigma The number of fruit-producing flowers with pollen collected from a population was found, forceps were used to pick up for the Log Cabin and Inspiration Point on the serpentine coastal bluffs. The the filament from the container and to hand-pollinated, weeded populations Inspiration Point population was polli- rub the stamen and stigma together averaged 85% (Table 1), much higher nated with pollen from the Log Cabin lightly until the stigma turned yellow. than those weeded but not hand-polli- population. Subsamples of the Log Cabin The style was left intact to allow for nated (8%). Personal observations of and Inspiration Point populations were natural pollination. To facilitate non-weeded, not hand-pollinated not hand-pollinated. Both hand-polli- monitoring, a label with a unique plants on the coastal bluffs indicate that nated and non-hand-pollinated popula- number was attached to each pedicel, the natural pollination success rate was tions at Log Cabin and Inspiration Point and flagging tape with a unique much lower (15%; data not shown). were weeded to increase visibility of tags number was tied around the bottom For hand-pollinated flowers, the aver- and flowers, to make monitoring easier, of each stem. age ripening duration was 50 d, and the and to facilitate harvest of fruits. After successful pollination, the highest number of pollinated fruits For pollen collection, anthers were ovary lengthens, transforming into a became ripe and dispersed seeds monitored every 3 d for maturity start- dehiscent silique in 2 to 3 d. The fruit is around the third week of May. Using ing in early March. This species is initially reddish purple. Within a the average ripening duration, naturally protandrous. Stamens mature in 3 to 5 month, approximately 10 seeds become pollinated flowers were likely pollinated d of the flower opening and stigmas visible through the capsule wall as the between late March and early April, mature several days later. An immature fruit color changes to light green. The coincident with our hand-pollination anther is swollen, glossy yellow, with no fruit is finally ripe and ready to dehisce of treated plants. We collected 18 seed- visible pollen grains. The anther is thin when it turns yellow. pods, representing 56% of the success- and dull yellow once it has opened to The 2 locules of the silique are sepa- fully hand-pollinated fruits. release pollen. The stigma is receptive rated by a septum. In each locule, 6 to 12 Although accurate records arc when it is a glossy whitish-green. When seeds are attached in a line along the unavailable, germination in the nursery pollinated, the stigma turns yellow. We septum, on alternating sides. The silique was at least 40%. used forceps to cut the base of the fila- is flattened in the same plane as the sep- ment on a mature anther. Anthers were tum. The valves are elastic and open placed in a sealed, black container (to suddenly, ejecting the seeds some dis- tance (Deitling 1936).

TABLE 1

Results of hand-pollinating milkmaids.

251

DISCUSSION sizes of existing populations, and the presence of many landmarks between Milkmaids can reproduce well in the those populations may also hamper pol- Presidio if hand-pollinated, but hand- lination. Expanding existing popula- pollination is time and labor intensive. tions to improve connectivity may As blooming is not simultaneous, fre- enhance the ability of native pollinators. quent visits are necessary. Hand-polli- nation, however, may be useful for species such as milkmaids that have low ACKNOWLEDGMENTS propagule demands and that exhibit limited natural reproduction. The authors thank the Golden Gate We found it helpful to weed around National Parks Conservancy and the the target population immediately fol- Presidio Trust for providing staff time lowing hand-pollination to successfully for the authors to work on this project. monitor fruit development and harvest Thank you to the editor and two review- seedpods. Weeding probably reduced ers for extensive and helpful comments competition as well and may have stim- on an early draft. ulated vegetative sprouting and repro- ductive success. It is unclear what factors are causing REFERENCES low seed set in milkmaids at the Bugbios. 2003. Bee flies. URL http://vwvw.insects.org Presidio. In the future, a simple cross- (accessed 21 Mar 2003). pollination experiment focusing on Deitling LE. 1936. A taxonomic and distribu- plants within only one of the Presidio's tional study of the Pacific Coast species of populations may help answer this ques- Cardamine and Dentaria [PhD dissertation]. tion. If pollen transfer within a popula- Palo Alto (CA): Stanford University. 122 p. tion is successful, low seed set is likely Fauver T, Kemp M, Breck H. 1998. Wildflower the result of a missing pollinator or walks and roads of the Sierra Gold competition with annual grasses that County. Grassvalley (CA): Comstock often overtop the plants. If pollen trans- Bonanza Press. 122 p. fer within a population is unsuccessful, Hickman JC, editor. 1993. The Jepson manual: there may he genetic constraints and cross- higher plants of California. Berkeley pollinating between populations is (CA): University of California Press. p recommended. This may he accom- 407-409. Proctor M. 1973. The pollination of flowers. plished by either transplanting individ- London: Collins. p 77-80. uals or direct seeding and would need to [USDA NRCS] USDA Natural Resources he monitored carefully. Conservation Service. 2006. The PLANTS If pollinators are identified as the database, version 3.5. URL: http://plants. limiting factor, it is critical to identify usda.gov (accessed 2 Aug 2006). Baton milkmaids' native pollinators outside Rouge (LA): National Plant Data Center. the Presidio. In late March, we observed bee flies (Bombyliidae; Proctor 1973; Bugbius 2003) hovering above and probing the center of milkmaids' flowers at the Log Cabin site. We do not know if this species is a pollinator or if other pollinators are necessary. If appropriate pollinators are present, further research is needed into why they are not able to pollinate milkmaids within the Presidio. Significant fragmentation of milkmaid 252 populations in the Presidio, the small

KAZUKI ARIYOSHI, EMILY MACNAGHI, AND MARK FREY NATIVEPLANTS I FALL 2006