The JapaneseSocietyJapanese Society for Plant Systematics September, 1987 Acta Phytotax. Geobot. 133 Pollination Biology of Circaea (Onagraceae) David E. BouFFoRD' - -n D, E. 7" 7 1 F : J< s ? y v ma (T de i"tN) cD9ts} !Ii im Gk Introduction Circaea L, (Onagraceae) is a genus ofseven species and an additiQnal seven subspecies of rhizomatous herbs that form small to large colonies in moist temperate deciduous ancl boreal forests threughout the northern hemisphere. The genus is notable in the Onagraceae for the hooked hairs on the indehiscent fruits that serve as an aid in dispersal and for the 2-merous flowers, The majority of taxa are fbund in eastern Asia, with 11 in China, six each in Japan, Korea and the Soviet Far East, and tbur in Taiwan. A few species extend southward into northern Vietnam, Laos, Thailand and Burma, India, and C. aipina L. subsp, imaiceta (AscH. & MAG.) KiTAMuRA occurs in southern diajunct from the main portion of its range in the Hima!ayas and China, Two taxa occur in Europe and three are found in North America. Hybrids in the genus are frequent and often abundant, particularly in eastern North America, Europe and Japan (CoopERRmER, 1962; RAvEN, 1963; HABER, 1967, 1977; BouFFoRD, 1982a, l982b). Characterization of the species of Circaea Ci.rcaea can be divided into two groups based on morphological (BouFFoRD, 1982a) and chemical (AvERETT and BouFFoRD, 1985) features that are more or less correlated with the mode of reproduction. The first group inc]udes species with bilocular ovaries, and perhaps also C. ropetzs WALLicH ex AscH. & MAG., which is unilocular and single seeded, but bears a trace of' a $econd locule (BouFFoRD, 1982a). In other words, this group includes all species with the exception ef C. aipina. These taxa are predominantly outcrossing, but facultatively selfLpollinating. The flowers open after the inflorescence axis elengates and are borne on pedicels held perpendicular to the raceme axis (Figure 1-c, d). Flowers ofall species in this group, except those of C, cortlata RoyLE, are distantly spaced and require an insect visiting more than a single flower in one raceme to fly from one to another. In C, cordata the flowers are more closely spaced making it possible ibr small insects to visit all flowers of an inHoresccnce by walking directly from fiower to flower. With the exception of C. cordata, C. glabrescens PAMpANiNi and C. ropens, all members 'Oni"e'rsi{y'"-H''e' * Harvar'd' Ibaria, 22 Divinity Avenue, Cambridge, MA 02IS8, U,S,A. NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlant Plant Systematics ' 134 Acta Phytotax. Geobot. Vol. XXXVllI .-.-.t .. ..........-..... ..... ... ... ' of this group have a fieshy, clearly visible, ring-shaped nectar"y that prejeets beyond the opening of the floral tube (Figure !-e). The secend group comprises the six subspecies of Circaea aipina. These all have unilocular evaries and the flowers ofall but C. aipina subsp. caulescens (KoMARov) TATE- wAm and some populations of C. aipina subsp. qugustijbtia (HAND.-MAzz.) BovFFoRD are borne on erect to ascending pedicels in a coryrnbiform cluster at the apex of the infio- rescence in much the same way as flowers are borne in most Brassicaceae (Figure !-a). As in the Brassicaceae, the fiowers open be{bre the raceme axis elongates. At"ter flowering the raceme axis elongates and the maturing ovaries become more widely spaced on spreading to reflexed pedicels. Insects visiting members of this group can easily visit all flowers in an infiorescence by walking from one to another. In C, aipina subsp, caulescens and some of subsp. augustijbtia the infiorescence begins to elongate before populations ' the flowers open and the flowers arg borne on more or less distantly spaced, spreading to ascending pedicels, as in the first group. The nectary in all subspecies of C. aipina (as in C. cordnta, C. gtabrescems and C, ropens) is located out ofsight at tlie base of the floral tube. Floral biology ' In the first group of species the style is generally longer than the spreading stamens and the anthers are held far from the stigma during anthesis so that automatic self polli- nation does not take place (Figure 1-e). The flowers open early in the morning and the stigma is papillose and receptive at or shortly after anthesis. One anther dehisces at about the same time the flower opens, or slightly later, while the other dehisces still ' later, sometimes as late as mid-afternoon. In Circaea aipina, however, the stamens and style are equal in length (Figurc 1-b) and the anthers are appressed to, and Qften shed pollcn directly on, the receptive stigma betbre the flowers open, This has been observed in dirctzea aipina subsp. aipina in Ontario (HABER, 1967, l977) and in the British Isles (RAvEN, 1963) and I made similar observations in C. aipina subsp. imaicola in the mountains of Taiwan and Hubei provinces, China, in C. aipina subsp, caulescens in Hokkaido, Japan, and in C. aipina subsp, aipina in Japan and in the northeastern United States. Self pollination in the C. aipina group occurs particularly during unfavorable weather conditions or when the ambient tempera- ture remains belgw about 15"C. During periods ofinclement weather or low temperature the buds may never open at all and eventually drop from the maturing ovaries. The 15eC temperature at which the buds be.crin to Qpen is also approximately the temperature ttt tt t Figure 1. Infiorescences and fiowers ofdircaea. cvncaea'211bina L. subsp, micrantha (sKveRTsov) BouFFoRD. a. Inflorescence showing clustered flowers typical ofC.'ttipina. b. Flower with petal removed; note length ofstamens and style. From Ludiew et al 5106 (E). Cincaea lutetiana L, subsp. eanadensis (L.) AscH. & MAG. c. Habit. d. Inflorescencc shewing widely spaced flowers. Frem Botofbrd 18828 (CM, KYO, MHA, MO, PE). Circaea lutetiana subsp, euathsutcata <MAxiM.> AsaH. & MAG. e. Flower with peta1 removed; note length of stamcns and style, and nectary at base of style. From Botofbrd &9 Wbod 19765 (KYO, MO, PE), NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlantSystematics Plant Systematics September,1987 Acta Phytotax,Geobot, 135 ･y', f･Jl･ C ll'l, 12cm V .r T ;... 5MM[ x . il . .1. 1 .. t,L>..-i,.. " .t iY t:. ` lttg z,...J"tl2, Figure l. NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics 136 Acta Phytotax. Geobot. Vol. XXXVII[I at which the chiefinsect visitors to the flowers of Circaea become active. At increasingly higher temperatures thc flowers may open before the pollen is shed and a degree of outcrossing is possible. The frequent hybrids derived from crosses of C. aipina with other species provide c]ear evidcnce for outcrossing. Although the po]len producing parent in these crosses might be considered to be C. aipina, experiments have shown that the styles of the pre- dominantly outcrossing taxa are too long for the pollen tubes of C. aipina to penetrate. Hybrids, using polien from the outcrossing C. Iutetiana L. subsp. Itttetiana to fertilize C. aipina subsp. a4Pina, are easily produced (BENoiT, 1966) indicating that selffertilization of the single evule in C. aipina is not an automatic occurrence. The adaptation to self pollination in the absence of insects, but with the retention of a means for outcrossing under favorable conditions is almost certainly an important reason thr the remarkable success of C. aipina subsp, aipina in cool boreal forests, where it is so widespread. Plants of the bilocular species grewn under controlled conditions do not set fruit unless pQllen is applied to the stigma, but there appears to be no difference in fruit set in selfed and outcrossed plants. In cDntrast, all taxa of C, aipi･na in cultivatiQn have nearly full fruit set without artlficial pollination. The fiowers of Circaea are borne in simple or branched racemes at the apex of the stem and sometimes also at the tips ef short aJcillary branches. The 2-merous flowers are rather small, ranging from about 2 mm across in some plants of C, aipina L. subsp. mierantha (SKvoRTsov) BouFFoRD to about 8mm across in C. Iutetiana subsp. Iutetiana. At anthesis the apically notched white or pink petals spread widely to form a flat surface, and with the generally refiexed, alternating sepals, which are usually completely green or tinged with pink or purple, fbrm a convenient target for insect visitors. As the flowers fade, however, the pedicel becomes reflexed and the flat surfaces of the petals close toward each other and eventually touch (see KNuTH, 1908, fi.cr. 153, and MttLLER, 1883, fig. 88). The stamens then project from the openings at the sides and the style protrudes through the notch at the apex of the appressed petals. Senescence of the fiower causes insects of a size suitable to eflt:ct pollination to be excluded, but it is most likely that aging of the flower is brought on by fertilization and visits by insects after that are of no significance. The floral tube eventually abscises from the summit of the ovary and the fiower fa11s. One or two flowers open on a raceme each day and persist for two or three days, or occasionally longer. Although three to six open fiowers per raceme is usual, I have seen as many as 11 open flowers on a single raceme of C. tutetia.na subsp. canadensis AscH, & MAG. in the northeastern United States. All species in both (L.) ' groups produce nectar, which is most obvious early in the mQrning as a small droplet at the base of the style. Later in the day, if not removed by insects, the nectar becomes concentrated through evaporation. NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics September, 1987 Acta Phytotax.