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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.
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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
the infiorescence begins to elongate and some populations of subsp. augustijbtia ' before 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
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･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.
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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
(L.) AscH, & MAG. in the northeastern United States. All species 'in both 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.
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Insect visitors of Circaea
My studies to determine the major pollinators of Circaea were carried out on popu-
lations ofindividual or mixed taxa in the field in Canada, the northeastern United States and Japan (Table 1). Additional observations were made, but no insects collected, in xrarious parts of China. The chiefinsect visitors to the flowers of Circaea, unlike in most other Onagraceae (RAvEN, 1979), are Syrphidae, with small bees ofthe family Halictidae fiies being of slightly lcss importance (KuaLER, 1938; BouFFoRD, 1982a). Syrphid seek nectar primarily, especially early in the day when it is most conspicuous, but occasion-
ally also lick the anthers and stigma in search of pollen, Halictid bees seek pollen almost exclusive!y, but occasionally also gather nectar. Other insect visitors (Lepido- ptera, largc Hymenoptera (bumble bees), ants and rnembers ofother families ofDiptera) arc infrequent and sporadic and of no significance in pollinating the flowers oC Circaea. All fiies collected on Circaea are deposited in the co]lections of the Insect Identification
and Beneficial Insect Introduction Institute, Beltsville, Maryland, and the Systematic
Entomology Laboratory, USDA, Smithsonian Institution, Washington, DC. The
bees and other Hymenoptera are deposited in the collections of the Department of
Entomology, University of Kansas, Lawrence, Kansas, the Department of EntQmology,
Cornell University, Ithaca, New York, and the Entomological Laboratory, Kyushu
University, Fukuoka, Lepidoptera are in the Section of Entomology, Carnegie Museum
of Natural History, Pittsburgh, Pennsylvania. The behavior of insects varies between species of insects and the structure of the inflorescence of (]Vrcaea, but in general syrphid flics are less constant and systematic than
halictid bees and will indiscriminantly switch to flowers of conveniently located neighbor-
ing plants of diflbrent species. Halictid bees are mor'e deliberate and systematic in their
visits. They tend to be fast fiiers with a rapid, darting flight, but are slow and deliberate oncc they begin taking pollen, They also tend to visit all flowers of a raceme, and systematically fly from one raceme to another wlthin a population. Halicted bces are most often found around populations ofS Circaea growing in sunny or open sites and less often in more heavily shaded woodland sites. Syrphid flies visit plants in all habitats, but become more important in the pollination of shaded plants. The fo11owing are briefdiscussions of observations of insect behavior on the flowers of Circaea at the localities
given in Table 1.
Observations in North America
Circaea aipina subsp. aipina. A single colony about 10m by 2.7m was the only
population of C. aipina subsp. aipina where insects were collected. Intermixed within
this colony were 14plants, bearing 21 infiorescences, of C. tutetiana subsp. canadensis.
Because of the far greater number and density of plants of C, aipina, their inflorescences
dominated at this site and were more conspicuous.
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Table. 1. Taxa of Circaea and localities where observations of insect visitors were carried out. Acronyms of herbaria where voucher specimens of CVreaea arc deposited in parentheses.
Circaea alpina L. subsp. alpina. Unitcd States. Connecticut, I.itchfield County, 1.4 miles
N of U.S. Toute 44 on road to Mt, Riga from town of Salisbury, Tbttga canadensis (L.) Carr. forest opseepyslepe above stream, 27 July 1977, Botdibrd &r H, E, Ahles 18833 (KYO, MO) (mixed
population with C, lutetiana subsp, cattadensts, BotEfibrd Cij' Ahles 18824).
Circaea cordata RoyLE,Japan. Hokkaido Prefecture, Hidaka-shicho, Samani-gun, Sarnani- cho, Okada, mixed deciduous forest, 20 August 1977, Bot!i7brd &7 E, PV. PVbod 19699 (BM, aM, E, G, K, KYO, LD, MHA, MO, NCU, P, PE, SHIN) (mixed population with C. erabescens,
Botet7brd Cif PVbod I9690).
Circaea erubescens FRANaH. & SAv. Japan, Hokkaido Prefecture. Kushiro-shicho,
Kawakami-gun, Shibecha Experimental Forest of Kyeto University, mixcd deciduous forest, 24
August 1977, BezEfibrd er E. thl, PVbod 19764 (CM, E, K, KYO, MHA, MO, PE, UC) (mixed population with C, lutetiana subsp. euadeisutcata, BozEZ7brd (lj' "ibDd 19765 ); Hidaka-shicho, Samani- gun, Samani-cho, Okada, mixed deciduous forest, 20 August 1977, Botefibrd &e E. PV. Mfoed 19690 (BM, CM, G, GH, K, KYO, MHA, MO, NCU, PE, TUS) (mixed population with C. cordata, BotEfibrd er Plibod I9699). Hyego Prefecture, Yabu-gun, Sekinomiya-cho, NE base of Mt, Hyeno-
sen, along stream in mixed deciduous forest, 26 July 1977, BotgM}rd (l? E. VV. VVbod 19513 (BM,
CM, DS, G, GH, K, KYO, LE, LD, MASS, MHA, MO, NCU, NY, P, PE, S, SHIN, UC).
Circaealutetiana L. subsp. canadensis {L,) AscH. & MAG. Canada. Ontario, Grey County,
Owens Sound,Jones Falls; moist, forested slope at base oflimestone lcdges, 15-16July 1976, BoteffZ}rd
ISel4 (BM, qM, G, K, KYO, MHA, MO, ?, S). United States. Connecticut, Litchfield aounty, 1.4 milesNofU.S. route44 on road to Mt. Riga from town of Salisbury, 27 July 1976, Bowfbrd (}P HL E.' Ahles 188S4 (MHA, MO) (rnixed population with C. aipina subsp. aipina, Bodibrd &P Ahles
1883B). New Hampshire, Cheshire County. towrl of AIstead, O.5mile N of the Surry-Alstead
town line on N.H. route 12-A, moist, mixed deciduous fbrest, 25-26 July 1976, BozEffbrd IB858 (CM, KYO, MO), Ohio, ?ortage County, O.3 miles S ofthe Geauga CountylineonOhio route mixed deciduous forest floocl S06, gn plain ofsmallstream, 17-18 July 1976, BotEZ7brd IB8I9 (BM, CM, DS, E, G, K, KYO, LD, MHA, MO, NCU, ?E, SHIN),
Circaea lutetiana I., subsp, quadrisulcata (MAxiM.) AsaH. & MAG. Japan.Hokkaide
Prefecture, Kushiro-shieho, Kawakami-gun, Shibecha Experimental Forest ofKyoto University,
Mixed deciduous forest, 24 August 1977, BozEt7i)rd es E. VV. VVZ,od 1976b' (BM, CM, E, G, K, KYO, MHA, MO, NCU, NY, P, PE, S, SHIN, TUS, UC) (mixed population with C. erubescens, Bota7brd
er WbodI9764); Tekachi-shicho, Urahoro-eho, 10.2 km W of Tokachikobetsu on highway 38,
mixed deciduous streamside forgst, 22 August 1977, Bota7brd &9 E. VV. uaod 19723) BM, aM, E,
G, K, KYO, rmA, MO, NCU, PE, UC).
Circaea mollis SmB. & Zvac. Japan. Hyogo Prefecture, Yabu-gun, Sekinomiya-cho, NE foot of Mt. Hyono-sen, mixed deciduous forcst, 28July 1977, Botsffbrd er E, Pti. maod 19553 (BM,
CAS, CM, E, G, GH, K, KYO, MHA, MO, NCU, NY, P, PE, S, SHIN, UC). Kyoto ?refecture,
Kyoto city, Sakyo-ku, tributaryof Kitashiro-kawa River, SWsideofMt.Hiei-zan,2 August 1977,
Botefibrd 19604 (MO). Hokkaido Prefecture, Kushiro-shiche, NW edge ef Lake Toro-ko, deciduous
forest at base of slope and upper edge of marsh, 23 August 1977, Bot!fibrd es E, W. Vtlbod 19744
(CM, G, K, KYO, MHA, MO, NaU, PE).
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Insects visiting the flowers of Circaea exhibit two difllerent modes ofL behavior. In
C. aipina the corymbifbrm clusters of flowers are usually approached from above, with
the cntire inflorescence being treated as a unit. Flies visiting C. aipina alight on the
infiorescence and probe with their tongue around the opening of the floral tube of each
ol' the open flowers in search of the minute amount of nectar offered by each flower. Bees predominantly seek pollen, In going from fiower to flower both groups of insects walk across the infiorescence. In doing so their legs and the undersurface of their bodies
come in contact with the anthers and stigmas. In visits to C. tutetiana subsp. canadensis
syrphids first approach the lowest part of the inflorescence, even if the lowermost fiowers
have already dropped. As they fly upward, syrphids usually hover in front of each
ovary or flower until eventually alighting on flowers with nectar or pollen. After re- moving the nectar or pollen from one flower, they then fly upward to the next open
flower. Syrphids switching from one species of Circaea to the other require one to three
visits to reorient themselves to the diflerence in the way the fiowers are bome. When
switching from aipina to tutetiana the fly first approaches from the top of the inflorescence
befope eventually finding the open fiowers lower down on the raceme. Flies switching
from lutetiana to aipina approach the lower part of the elongated portion of the inflores-
cence, where the flowers have already fa11en, before rising to find the open flowers
clustered at the apex of the raceme.
Of the 47 insects observed visiting flowers of Circnea at this site, 32 were on C. aipina.
Table 2, Insects collected at flowers ofCircaea in mixed colony ofC. aipina subsp. aipina and C. Iutetiana subsp. canadensis, U.S.A,, Connecticut, Litchfield County, Mt. Riga. Temp- erature range during observation period 22.20-24,5aC, 11:30-14:10, 14:40-15:15 sunny; 14:10-14:40, 15:15-16:OO shaded, All visitors solely on C, aipina subsp. aipina unless indicated. aone individual visiting both C, aipina and C. Iutetiana subsp. eanadensis; bone individual solely en C. Iutetiana subsp. canadensis,
Time periods Insectspccles Total 11:30-I2:OO12:OO-13:OO13:OO-14:eo14:OO- 15:OO- 15:OO 16:OO -----//-,
Qptadimtlaria laetCticai 1
Baccha elengata2 11 1
A(felanostoma metlinum2 2a 1 4
Slericon!yia chnysotoxeides2 1' I SPhagiua keeniana2 la 1 Eipheginapetiolata2 1 1 2
Elyrphus rectas2 12117 1
7loxomeris gemiuatus2 4a 2 23a,b 2 12 Dialictus abanci3 4
thlicttLs coi!fiisus3 1 Total visitors 4 5 8 4 28
iMuscidae, 2Syrphidae 3Halictidac (Diptera); (Hyrnenoptera).
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Tbxomeris geminatzcs (SAy), Metanostoma mellinum (LiNNAEus), S)bhegina keeniana WiLLisToN (all Syrphidae) and Diatictus abanci (aRAwFoRD) (Halictidae) visited fiowers of both C. aipina and C. tutetiana in succession. The insects collected are Iisted in Table 2.
Despite the obvious cross pollination taking place within this mixed population, there were po hybrids between the two species of Circaea in the vicinity, probably because of
the absence ofdisturbance, which appears to be necessary for hybrids of Circaea to become
established (BouFFoRD, 1982a, 1982b). Circaea lutetiana subsp. eanadensis, Insect visitors to the flowers of C. Iutetiana subsp.
canadensis were observed and collected in three widely separated areas: Grey County,
Ontario, Canada; and Portage County, OhiQ, and aheshire County, New Hampshire, U.S.A. In addition to the insects collected at the three sites (Tables 3, 4, 5), eight
daylight hours over two days were spent observing the behavior of insects at the Naw
Hampshire site to determine the extent of visits to individual flowers within a population.
To do this, 50 adjacent racemes in a colony approximately 1 m by 2 m were selected
and numbered from 1 to 50. The epen flowers on each raceme were then numbered
from lowest (numbered 1) to highest. There were 207 open flowers on the 50 racemes, an average of4.14 fiowers per raceme. The most flowers open on a singlc raceme was
11; three racemes on the first day of observations and two on the second day bore only a single open flower. During the periods of observation the temperature ranges were
13.9e-21.10C and 16,90-19.40C. All visits to the flowers were recorded by inflorescence
Table 3. Insects collected at flowers of Circaea lutetiana subsp. canadensis,U,SA., Ohio, ?ortage County, Aurora. Temperature range during observation period 14D--230C; filtered sun,
Time periods . ------Insectspecies . Total 8- 9- 10- 11- 127 137 147 15. 167 17- 187 9 10 1112 l3 I4 15161718 18:15
QPhionEyia sp.1 11 1 2 ･1 Baccha elongata2 I7
lhlanostoma mellinum2 4 1 1
Platycheirzas obscurus2 1 112132266
Rhingin nasica2 1 ophagina keeniana2 2 syrphas vitifrons2 12 Tl)xomeris geminatas2 2 4 4722321 6 6 l
Dialictus abanci3
Dialictzas atlantieusB 12 1 Dialidtzas taevisst'mus3
Diatictzts lineatulus3 11l2 1
Diaticttts rohweri3 163
Totals visitors 4 3 7 14 7 9 5 1 1
IAgrQmyzidae, 2Syrphidae 3Halicticlae (Diptera); CHymenoptera).
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Table 4. Insects collected at fiowers of Circaea iuteiiana subsp. canadensis, U.S.A., New Ham- pshire, Cheshire County, Alstead. Temperature range during observation period 13.80- 210a; broken sun-slightly overcast.
Time periods - -- ''-- -- Insect species Tetal 9"1010-1111-1212-13 13-1414-15l5-1616-17
ParanEyia nitensi 4 1 1131 6114118211111148
Cheilosi (pallipes complex)2
Mlrliscaeva cincteila2 1 5 4 1
A{felanostoma mellinum2
Platvcheirus ebscurus2 12
Rhingia tzasica2 1 l1 4 SPheginaj7avimana2 113 SPhegina keeniana2 7-bxomerusgemiuatus2 5 2 1
Siphona (geniculata complex)3 1 Diaticttes abanci4 1
Diaiictas atlanticus4 12
Total visitors 6 I 11 13 105
IMilichiidae, 2Syrphidae, 3Tachinidae (Diptera); 4Halictidae (Hymenoptera),
Table 5. Insects collected at fiowers of Circaea lutetiana subsp. canadensis. Canada, Ontarie, Grey County, Owen Sound. Temperature range during observation period I70-22,5eC; Sunny, occasienal large cloud$,
Time periods
Insect species Totals 8- 9- 107 11- 12- 137 16- 17- 9 IO 11 12 13 !414-1515-1611 17 IB
Mletasyrphus latijinsciatusi 13111142i15
Plae,cheirus obscurusi 2
Rhingia nasioai l
Sericongyia chu,sotoxoidesl 1 1 ophegina campanuiatai SJ,rphzts knabil 1 7bxomerusgeminatzas･i 2
Dialictus auanci2 215 1
Lasioglossum (Chleralict"s> sp.2 13 Total visitors 12 2 2
iSyrphidae 2Halictidae (Diptera); (Hyrnenoptera).
and flower number (Table 6) and the behavior of the insects noted. The uppermost flowers on a raceme consistently received the mest visits from insects. The uppermost fiower on 42 (84%) of the 50 racemes was visited at least once over the
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Tabie6. Insect visits to numbered inflorescences and flowers of Circaea Jutetiana subsp. canadensis. U.S.A,, New Hampshire, aheshire County, Alstead. Infierescences numbered i to 50; flowers numberedfrom lowest (number 1) to highest en eachinflorescence. Totai number ef flowers 207; average number of flowers per inflorescence 4.1'4; total numbcr ef visits 269; visits to uppermost fiowers=89 (33.09%); visits to 2nd uppermost fiowers==58 (21.56%>; visits to 2nd lowest flowers=49 (13.38%); visits to Iowermost flowers=t:58 (20.81%); visits to uppermost and 2nd uppermest fiowers"147 (54.65%) ; numbers in parentheses are numbers of fiowers open in same infiorescence on 2nd day ifdifferent.
inflor-escence flowersl flowers infior- fiowers1 flowersvisitecl inflorescence visited escence inflorescence
123 3(4)3(4)53,2,3,2,4,3,2,1,3 2627282930314(5)4(6)2(3)4(6)2(4)64, 2, 4, 3, 2, 4 1,1,3,1,2,3,3,3,3,2,4,2 4,4
4, 5, 5, 2, 2, 3, 4, 5, 5, 5, 3, 3, 5,2,3,4,3,5,3,5 4,42,1,3,2,1 45 44 3,1,3,2,1,3,2,2,4
2, 1, 3, 3, 1, 4, 4, 1, 1, 4, 2, 4, 2, 1, 4, 1, 1.6, 5, 6, 4, 4, 5, 3. 3, 2, 3,2 43,I,3,3,1,2,1,2,2,3 6789 4(2)355(6)17(8)53, 3, l, 2,2 3233 35 l,34, 5, 2, 1, 2, 4, 5, 3, 5, 2, 2, 1, 2, 1, 3, 2, 5, 3, 1, 1, 4, 4 5, 4, 3, 4, 1, 5 5, 1, 2, 4, 4, 2, 5, 2, 3, 5, 1, 3, 34353637 525(3)4(3)2,5,4,4,5,4,2,5 5,3,414, l,2,2,22, IO11 4, 4, 4, 2, 5, 3, 1, 3 6, 7, 1, 7, 6, 5, 7, 4, 7, 5, 8, 1, 4, 3, 2, 4, 4, 3, l, 1, 2, 1, 1, 8, 8, 2, 5, 3 4, 1,4, l,3 12 4,5,5,5,5,4,3,3,5,2,5,3, 383940416(5)553 5, 5, 4, 1, 2, 2, 3 5,2,5,3,5,3,5,3,2,3,4 131415161718192e2122234(6)4(1)632i(3)13(4)54(5)56,5,6,5,6,3,6 4, 3, 5, 1, 2, 3. 2, 5, 4, S 1,16,6,6,2,5,5,2,5,2 5, 1, 5, 3, 5, 5 2, 1,2,3,1,2,1,3,2,1,3, ;, 3,1;1,3,3,2 42 4 4, 3, 4, 4, 1, 4, 3, 4, 4, 4, 1, 2. 39.
1,2,313,1,3,3,4,1 4344454647ng4950ll(10)5(6)9(8)3(4)534(6)2 85,5,4,1,2,3
7, 1, 4, 7, 8, 7 5,4,2,4,4,3,4,3,4,4 2,i,21,
4, 3, 3, l, 3, 2, 3, 2, 4, 3 3, 2, 4, 1, l, 1, 1, 5, 3, 5 5,k;,3,1,1,3,5,1,1,2,s, 1,2,3,2,3
,5,2,3,4 4, 1,22, 2425 5(4)4(3) 1, 2,2
eight hours of obser"vation, and the next uppermost flower was visited on 38 (7.6%) racernes. Taken together, either the uppermost or second uppermost flower was visited
on 46 (929/6) of the 50 racemes. The high number of visits to the uppermost fiowers would be expected since these are the youngest and provide the greatest reward of nectar and pellen, but it also indicates that there are probably suMcient visits to insure effbctivc cross pollination of essentially all flowers in a population.
NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics
September, 1987 Acta Phytotax. Geobot. 143
The major visitors collected onflowersof Circaea inNorth America areIisted in
Table 7.
Table 7, Insects collected at flowers of crrcaea at four Iocalities (Table 1) in North Amcrica (1, Grey County, OntaTio, Canada; 2, Portage County, Ohlo, U.S.A.; 3, Cheshire County, NewHampshire, U,S.A.; 4, Litchfield County, Connecticut, U.S.A. Cl-3, C. Iutetiana subsp. canadensis; 4, C. aipina subsp. aipina and C, lutetiana subsp. canadensis).
Taxon number of lecality number individuals 1 2S4
Agromyzidae (D{ptera) QPhio,,!yia sp,i 2 ÷
Milichiidae (Diptera) 1'arampia nitens (LoEw)i 6 +
Muscidae (Diptera) C2ptadrularia laetijifa (R.-D) 1 +
Syrphidae (Diptera) Baccha etbngata (FABRrcius) 21141215102l2.4211159+ -- eneilosia pallipes complex +--+ lhtiscaeva cinctella (ZETTIIRsTEDT) ndelanestema mellinum :14btasyiphus iatij}zsciattts MAcgvART 'f++++ PIat.ycheirzas (C2ipsocalis) obscurtts (SAy) ++ ++ Rhiugia nasica (SAy) Sericon!yia chnysotoxoides S.vrphus vittcofi'ons SHArlNoN ++ 7bxomerus geminatus (SAy) + + + Tachinidae (Diptera) Siphona sp. (geniculata complex) l + Halictidae (Hymenoptera) Dialictus abanci (CRAwFoRD) 97611l1 + +++++ ++ + Dialictus atlanticzas MiTcHELij Dialictzts taevissimus (SMiTH) DialicttLs "neatulus (CRAwFoRx) Dialictzas rohtveri (ELus) Hdlictus cerijitstts SMITII + Lasioglessum (C)Eloraltctus) sp. + ipresent around base ofpetals and around nectary, too small to efflrct pollination. NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlant Plant Systematics !44 Acta Phytotax. Geobot. Vol. XXXVI[I ' tt Observations in Japan. The behavior of insects on the flowers of Circaea in Japan is essentially the same as in North America. At the seven sites in Japan where collections were made halictid bees represented a larger percentage of the pellinators than at the North American sites (see Tables 7 and 15). Whether'their relatively greater importance was due to these' particular sites being especially favorable foY halictids, or because halictids play a greater role in the pollination of small flewers in Japan, will require additional observations. ' Of the seven sites in Japan where insects were collected three were in west central Honshu and four on Hokkaido. None of the insects was collected at all seven sites, and only one, 1ipisyt:phus balteattts DeGEER (Syrphidae) was collected at as many as four sites. Baccha WALKER Five species of insects (bystropus ((:lePhenius) sp. (Bombyliidae), maculata and Paragus haemorrhus MEiGEN (Syrphidae) and Lasioglossum (Eqylaeus) taenioleUus complex and Lasioglossum (Eaylaeus) sp. (sp. II-12) (Halictidiae)) were coilected at three sites (Table 15), but only a single individual of Elvstropus sp. was collected at each site. Circaea erubescens. Plants of'Circaea erubescens were at three sites (one en Honshu and two on Hokkaido) where observations and collections were made. They were a conspicuQus part of the vegetation, however, at only one site ([[iable 8) ; at the second site they were part of a mixed populption with C. cordata, and at the third site they were essentially past flowering and intermixed with C, gutetiana subsp. guadrisutcata, which was at its peak ef fiowering. The correlatiQn between weather conditions and insect activity was clearly evident at the Hyogo site where the greatest insect activity Table 8. Insects collectod at flowers ofCircnea erubescens. Japan, Hyogo Prefecture, NE foet of Mt. Hyono-sen, Tempcrature range during observation period 24.50-350C, 10:OO- 10:50 shade; 10:5e-12:45-partlysunny; 12:45-14:l5 evf.r-cast; 14:l5- .rain.. Time periods ''- ' ' Totals Insect species 10- 11- 12- 13- l4- 11 !2 13 14 15 Systropus (Cigphenias) sp.i 11311 125111331l8 Eipisyrphus balteatus2 1 Paragns haemorrhtks2 1 1 Siphena sp.2 EPhaerophoriaphilanthus2 Botnbus fiotzshuensis honshuensis (worker)3 112 Lasioglossum (Eaylaeas) paliidulum 24 1 11110 Lasiegtossttm (Eop:laeus) sp. (sp. II-12) \4 Lasioglossum (Eaylaeus) sp. (sp. II-8) 94 Total visitors 2 5 l 'ZHall'Gtidae iBembyliiciae, 2Syrphidae (Diptera) ;3Apidae, (Hymenoptera). NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlant Plant Systematics September, 1987 Acta Phytotax,Geobot. 145 occurred during sunny periods, decreased as the coleny of Cireaea became shaded, and dropped off dramatically as the sky became overcast. Circaea mollis. Of the three sites where insects were collected on Circaea moltis, two were on Honshu (Tablcs 9 and 10) and one was on Hokkaido (Table l1). The Hokkaido site was in a mestly open area at the upper edge of a marsh-lower edge of a forested slope. The Honshu sites were in mesic, forested situations, Ofinterest is the fact that ants were so conspicuous on the fiowers of C. mollis at the sitc in Hyogo Prefecture. Table9. Insect visitors collccted at llewersof Circaea mollis. Japan, Hyogo Prefecture, Fukusada near NE foot of Mt, Hyono-sen, Temperature range during observation period 27.9e-3e.70C. 9:45--11:OO mostly sunny; 11:OO-14:30 partially shaded; 14:30-16:OO overcast. Time periods Insect species Totals 8:45- 9- 10- 13- 14- 15- 9:ee 10 1111-12 1312- l{F 15 16 Mkla)iagrompla sp.i 1 1 op,siropus (Cephenius) sp.2 1 1 (]bndylostylus sp.3 11i 1 Limnophora,fiztiax4 1 Allobaoaha apisalis5 1 AUograpta J'avana5 1 1 2 Chalcosyiphus sp.5 1 1 Qisyiphus balteatus5 1 1 1 1 4 Eumerusj'aponicus5 149 1 Paragus haemorrhzas5 391 141 1 927 tSPhaeroj)heria macrogaster5 1l 2 2 5Phaerophoriaphildnthus5 3 fQblon!Jia conjinisfi I 1 Siphena sp,6 l I 2 Bombus honshztensis henshttensis (worker)7 111 1 8 Clrmtina ((:leratinidia) J'dipenica ? 1 2 Lasioglossum (Lasiagtassunz> occidens gS 1 S Lasioglossum (Eaylaetts) Pallidulu,n 9 1 1 Lasiogtessum (Eaytaeus) taeniolellus9S 2 l 1 4 Lasioglo.gsum (Euvlaeus) taenioletl"s9S 1 1 Lasioglessum (EaylaezLs) sp. (sp. II-1) ?8 1 2 3 Lasio.cgossum (Ezlputaeus) sp. (sp. Il-3a) 9S l t IVbmada sp. nearufittvaS 15 142 Fbrmisaj'aponica9 11 15 6 4 1 Clerceris 7nontivaga olO 1 1 Crossocerus sp. 9 10 1 1113 Total visitors 1 33 35 17 8 8 9 iAgromyzidae, 2Bombyliidae 3Dolichopodidae, 4Muscidae, SSyr[phidae, GTachinidae NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlantSystematics Plant Systematics 146 Acta Phytotax. Geobet. Vol. XXXVIII Table 10. Insects collected at flowers ofCircaea mollis. Japan, Kyoto Prefecturc, Kyoto city, Sakyo-ku, SW side of Mt, Hiei-zan. Temperature range during observation period ' 24"-28ea. 8:45-10:40 clear, but plants shaded; 10:40-1:30 sunny to partly cloudy; 1:30- 3:15 full shade. Time periods Insect species 8:945-9L1010-1111-1212-1313-1414uI515-15:15Totals El;,stropus (C4phenius) sp,i 1 1 Asphonofvlia sp.Z 16122 1 Dro`alPhilapuncticeps3 21431 8 Drosophila sp.3 2 Baccha maculata4 14 111 812･3 Eipisyiphus balteateLs4 11 1 Paragus haemerrhtas4 ParzrgtLs n, sp.4 2l11 2 EPhegina sp.4 1 nig4)phus n. sp,4 1 Siphona sp.5 1 toPemtcrogastersp,6 131 1 Lasiaglossum (Eqylaetes) taeniotellus ?6 1 3 3 1 ll Laslvglossum taeniolellas S6 1 Ochlodes ochmcea7 l 1 Pieris meleteS 113 155 Tota1 visitors 1 13 13 8 5 2 iBombyliidae, 2Cecidomyiidae, 3Drosophilidae, 4Syrphidae, 5Tachini 6Braconidae, (Diptera); 7Halictidae 7Hesperiideae, gPieridae (Hymenoptera); (Lepidoptera).dae Table 11. Insects collected at fiowers of Circaea mollis. Japan, Hokkaido Prefecture, Kushiro- shicho, NW edge of Lake Toro-ko. Temperature range during observation period 220- 240C, 10:OCFI4:l5 sunny, but plants sporadically shaded. Time perieds ･･-- Insect speeies Totals 10-ll 11-12 12-･13 13-14 14L14: 15 Baccha maculatai 1 1112115113 Ebemerusjapenicusi 1 Hblophiius bybridits! 1 SPhegiua sp. 2 Lasieglessttm iSyrphidae(Diptera);2Halictidae(Hymenoptera); 3Pieridae (Lepidoptera). NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics September, 1987 Acta Phytotax. Geobot. 147 tt --ttttttt tt tt ttt tt tt tt tttt Plants of Circaea at this location were grewing intermixed with a number oi' other coarse herbs and shrubs and it was relatively convenient tbr ants to walk acrQss other vegetation ･walked to reach adjacent inflorescences of (]Vrcaea. Although the ants over all parts of the flower in their search for nectar they rarely made contact with the anthers and stigma ancl it is very unlikely that they ever efllected pollination. Some syrphids at the Hyogo site, in addition to collecting nectar, occasionally licked the anthers or stigma in search of pollen. Syrphids were also rather indiscriminate in their visits and would frequently shift to {lowers ol'other nearby species. Circaea cordata. Circaea cordata was observed at only a single station (Table 12), where it was growing adjacent to and intermixed with C. erubescens. Unfortunately, the weather during the period of observation was poor and insect activity was minimal. Visits to the fiowers o[' Circaea were further reduced because of the greater attraction of the more numerous flowers on the corymbose infiorescences of nearby plants of Patrinia. The insects that did visit C. cordata tended to visit all of the closely spaced flowers on an inflorescence by walking, rather than fiying. In C. cordata the nectary is located at the base of the floral tube where it is presumably less convenient for insects than the prq]'ecting nectary in other species, Having the flowers closely spaced, however, insures an adequate reward or fbod from scvcral flowcrs without the large expenditure of energy needed for flying. For the plant it insures that a!1 fiowers in a raceme are visited, although consider- able self pollination must take place. But since only a I'ew llowers are open on each raceme, an insect must eventual!y fiy to other plants and thereby eflbcts a certain degree ofoutcrossing. The only insect that was seen on the flowers of C. erubescens, Baccha maculata (Syrphidae), visited both C. cordota and C. e-rabescens. Hybrids between C, cordata and C. Table i2. Insect visitors to flowers of Circaea corduta (mixed population with C. erubeJ'cens), Japan, Hokkaido Prcfecture, Samani-cho, Okada. Temperature range during ebservation period 17"--2leC. 9:OO-10:OO mostly cloudy-partly sunny at times; 10:OO-14:15 overcast, rarely sunny, occasional lightrain. aOne individualon both C. corduta ang.S erubesoens. . Timc periods Insect species Totals 910IO- 11- 12T il 12 1313-1414-14:15 Baccha maculatal 1 2a1 311211110 Adet･iscaeva cincteUttsi Paragus n, sp.i 1 Xbnthogramma sqnporoensel 2 Andrena (Oreometissa) rnitakensis2 1 Bombus ftzPocritdea sclnPoroensis (worker)3 1 4 Lasioglossum (Eop,laeus) trispinis cornplex ? 14 Total visitors I 5 iSyrphidae (Diptera) ; 2Andrenidae, 3Apidae and 4Halictidae (Hymenoptera). NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlant Plant Systematics l48 Acta Phytotax. Geobot. Vol. XXXVIII erubescens (C. × dubia HARA) are common in Japan and are particularly abundant at this site. The variation in morphology of the almost totally sterile hybrids indicates that crossing has occurred on a number ofoccasions and is no doubt a frequent event. Circaea tutetiana subsp. quadrisulcata. Insects were collected at the flowers of two populations of Circaea lutetiana subsp. guadrisutcata. The population in the Shibecha Experimental Forest was in fu11 fiower and was growing intermixed with plants of C. erubescens, which were essentially past flowering and were not visited by insects Table 13. Insects collccted at flowers of Circuea lutetiana subsp, guadeisttlcata, Japan, Hokkaide Prefecture, Kushiro-shiche, Urahore-cho. Temperature not recercled, 12:15-2 :15 broken shade. Timc periods - Insectspecies Totals 12:15- 13:OO- 14:OO. I3:OO I4:OO 14:15 '' ' '-"--"- '"'''-2---- IIPisyrphzas batteatus' 2 Mkliscaevap inctetlusi 2 1 3 Rhingia taevigatai 2 2 Actia j'ocularis2 1 1 Total visitors 6 2 8 ISyrphidae, 2Tachinidae (Diptera). Tablc 14. Insccts collected at flowcrs of Circaea lutetiana subsp. auadeisutcata. Japan, Hokkaido Pre fecture, Kushiro-shicho, Kawakarni-gun, Shibecha Experiment Forest ef Kyote University. Tcrnperature range during observation peried 200-230C. 9:45-11:45 fuII sun; 11;45-14:OO broken shade. Time periods ------Insectspecies Totals 9-10 10-11 11-!2 12-13 13r14 7)Uecophora sp,i I 1212144315125 oprittaPipiens2 2l EbtqPhasia sinensis3 Cblletes sp. near junkowslp,i o4 2 Hdlicttts (Sleladonia) near tumulorum o4 121113 Lasiaglossum Pieris napi3 11 TotaI visitors 2 4 10 8 iConopidae, 2Syrphidae,3Tachinidae 4Halictidae (Diptera); (Hymenoptera); 5Pieridae (Lepidoptera). NII-Electronic LibraryMbrary Service The JapaneseSocietyJapanese Society forforPlant Plant Systematics September,1987 Acta Phytotax.Geobot. 149 during the period of observation, Although only a I'ew visitors were collected on the plants at Urahoro-cho (Table 18), all bitt one were syrphids, and all were Diptera. The habitat of this colony was a vcry shaded, moist, streamside situatien, In contrast, the colony of C. Iutetiana subsp, guach'isutcata at the Shibecha site was aleng a semi-open roadside in a dry, upland mixed deciduous forest, and here the majority of visitors were halictid bees (Table l4). This pattern is a general one, first observed in Europe by KuGLER (1938), where syrphids are mQrc important, or the only visitors, on Circaea in Table IS. Insects collectcd at i'lowers of Circaea at seven localities (Table 1> in Japan (1, Hyogo Prefecture (C. erubescems); 2, Hyoge Prcfecture (C. moUis); 3, Kyoto Prefecture (C. mollis); 4, Hokkaido, Toro-ko (C. motlds); 5, Hokkaido, Okada (C. cordeta); 6, Hokkaido, Urahore-cho (C. Iutetiana subsp. guadiisulcata); 7, Hokkaido, Shibecba (C. Iutetiana subsp. auadeiszalcata)), Taxonandnumberofindivicluals l 2IOCa31itY4nUMsber6 7 Diptera Mlalana.orompua sp. (Agromyzidae) 1311182112121202141722 +++ opstrqsbus (Cophenius) sp. tltlobaccha opicalis (LoEw) (Syrphidae) Allogroptajuvana (WiEDEMANN) (Syrphidae) Baccha maculata WAuKER (Syrphidae) ++ C7Latcosyrphus sp. (Syrphidae) ++++ + 1ipisyrphus balteatus al32 ,S?)haerophoria Philanthus MEiGEN (Syrphidae) SPhegina sp, (Syrphidae) ++ S}'rittaPiPicns (LiNNAEus) Siphona sp. (Tachinidae) 3 ++ NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlant Plant Systematics 150 Acta Phytotax.Geobot. Vol. XXXVfi1 Hymenoptera Andeena (Oreomelissa) mitakensds HIRAsHiMA (Andrenidae) 11+1l4222 + Bombus henshtsensis honshuensis Lepidoptcra Ochtedes echracea BREMER (Hesperiidac) 112 ++ Pieris melete imNETRms' Pisris napi LiNNAEus (Pieridae) + + moist habitats and halictid bees predominate en drier sites. The insect visitors collected on the flowers on Circaea in Japan are listed in Table 15. In addition to the observations and collections noted above, I have also observed small flies and bees on Qrcaea aipina subsp. augmstijblia near Kunming, Yunnan, on C. glabrescens in the Shennongjia Forest District, Hubei, aod on C. motlis near Guiyang, Guizhou, China. Discussion Flies of the family Syrphidae and small bees ot' the t'amily Halictidac are the chief pollinators oi' the flowers of Circaea. Other insect visitors are infrequent and usually of a size that prevents eflective pollination. In mesic, shaded habitats syrphids are rnuch more important than halictid bees, but as light intensity increases and on drier sites halictids play a greater role in pollination. Of the 398 insects collected on the fiowers of (:ircaea in North America and Japan, 77.6% were either syrphid flies or halictid bees. In North America these two groups of insects made up 93% of all visitors. Their lower percentage (59%) ef the total nurnber of visitors in Japan can be explained by the greater NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics September, l987 Acta Phytotax. Geobot. 151 number of individuals of other groups of insects found on the flowers of Circaea there, Ifvisits by nonpollinating members of these other groups (Lepideptera, ants and small flies) are excluded, syrphid fiies and halictid bees make up 83.39{, of the visitors that are of a size to efll]ct pollination. In North America halictid bees made up 16.9% of the total visitors, whereas in Japan they represented 259t'., Of the total nurnber of eflbctive pollinators in Japan, halictid bees made up 30.8%. When only syrphid flies and halictid bees are considered in thc calculations, the percentage fbr ha!ictids in North America changes only slightly to 180/,, but inJapan it rises to 40%. The diflbrence in the number of syrphid {lies as a perccntage of total visitors was much greater in the two areas with this group representing 76.6% of the total visitors in North America and 42.6% of the total in Japan. When incfTective fiower visitors in Japan are excluded, the percentage of syrphid flies rises to only 52.5%. I noticed no diflbrences in the habitats or light eonditions in the two areas that could account for the difierent percentages. Despite their comparatively lessened role in pollination of CVrcaea in Japan, syrphids still comprise the most ivnportant class of visitors to the flowers of this genus. The activity and behavior of syrphid fiies on the flowers of Circaea is basically the same in Japan and North America. Syrphid fiies are sluggish at low temperatures (below about 16.50C), but increase activity as ambient temperature rises. During the warmest parts of the day fiies becomc territorial, often resting on foliage in the midst of a population of Circaea and occasionally flying up to inspect or make brief visits to only the best fiowers (the youngest, or more exactly, those with the greatest amount of nectar and pollen) within the territory or to drive off other fiies of the same species that intrude on their space. F]ies of difTerent species are ignored. Generally, the territory has a radius of about 10 to 15 cm. Aftcr driving off an intruder, a fiy will hovcr in front of and appear to inspect sevet'al inflorescences and flowers within the territory. During these inspections no nectar or peilen is gatherecl and eventually the fly returns to a leaf to groom or to rest in the sun. Flieg show no territoriality or aggressiveness when the plants are heavily shaded or when the temperature faIls below about l80C. At lower temperatures fiies tend to visit mere flowers on each inflorescence, tend to remain on each flower longer, appear to become more deliberate in their visits and do not rest on leaves to clean themselves as they do at higher temperatures, Late in the afternoon and early in the morning the majerity ofvisits to the flowers in a population are by only a few flies, but the number of visitors increases with rising temperature and brighter light conditions. Both halictid bees and syrphid fiies tend to shift to diflZ rent parts of a population as the light shifts, and sorne areas are almost totally neglected if they become too hcavily shaded, Early in the day syrphid flies gather nectar almost exclusively, but later they also lick the anthers and stigma, apparently in search of pollen. In the afternoon syrphids NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics ' 152 Acta Phytotax. Geobot Vol. XXXVllI ttt-ttt-t t-ttttttt t t can frequently be seen licking what appears to be a perfectly dry nectary, no doubt to gather the concentrated sugars left behind after evaporation of the conspicuous drop of nectar produced each morning, There is no particular pattern in the way flies alight on a flower and they generally grasp any convenient part to get a fbothold. Very rarely do flies approach directly from the front of the fiower ahd grasp the stamens and style in the manner described by MtiLLER (l883), KrruTH (1908) and HABER (1977). Once on the fiower a fiy maneuvers into position to lick the nectary or to probe the opening of the fiorai tube and in doing so comes into frequent contact with the anthers and stigma. Halictid bees are most active in the middle of the day when the sun is almost directly overhead and the temperature is highest. Halictids are deliberate in their visits, fiying directly to a raceme and then systematically visiting all open flowers. KuGLER (l938) noted the same behavior in halictids in Germany on Circaea lutetiana subsp. tutetiana. In fu11 sun the leaves of Circaea wi!t and the infiorescences frequently nod so that flowers are held upside down. Syrphids appear to best utilize flowers held in the normal upright position, but halictid bees have no difllculty with flowers held in any position and even seem to prefer those that nod. They alight by grasping any convenient part of the flower and then maneuver into position to feed on pollen. The insect's body frequently makes contact with both the anthers and stigma while maneuvering, but once in position halictids grasp a filament and remove the pollen from the anther. Halictids occasionally take pQllen deposited on the stigma, and sometimes also gather nectar. All ofthe halictids collected on Circaea in North America wcre females, but in Japan both sexes of some species were collected. Syrphid flies and halictid bees visiting Circaea frequently visit difierent flowers and infiorescences within a population, but these insects, particularly flies, are not constant to Circaea and will also visit fiowers of neighboring plants in widely unrelated families. The halictid bees collected on CVrcaea in North fimerica are broadly polylectic (George C. EicKwoRT,･pers. comm.) and most likely the Japanese species are also. It seems thirly clear that visits by short tongued flies have provided the selection pressures in Circnea resulting in the enlargement ef the nectary so that it completely fills and prejects beyond the opening of the fioral tube in a number of species, making it more convenient for visitors to gather nectar. The nectary is still located at the base of the floral tube in other Onagraceae and in ta)ca considered primitive within CVrcnea, and in the more advanced C. aipina (BouFFoRD, l982). In the inbrceding C. aipinasuch selection pressures have not aflected the position of the nectary, but several flowers are generally clustered at the apex of the raceme so that insects can obtain the minute amount of nectar from each without having to expend the energy to fly from flower to flower. The extent of outcrossing in Circaea ' Despite the obvious role of insects in the pollination of flowers of CVrenea, it is quite NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics September, 1987 Acta Phytotax. Geobet. I53 tttttttttt tt tt tttt ttttt ttttt tttt - t probable that the majority of fruit set is due te self pollination. This is because all speeies of Circaea are strongly rhizomatous and form small to large colonies by vegetative means. The success ol' vegetative reproduction can be seen especially well in hybrids, which are nearly or totally sterile yet frequently form colonies ofseveral square meters or more. All plants within a population of Circaea tend to be remarkably similar morpho- logically, but plants from widely separated populations show considerable variation. Furthermore, seeds of Cireaea, which are borne either singly or in pairs in the indehiscent, corky fruits, do not germinate well in cultivation, even after various scarification treat- ments, and may also gerrninate with clifficulty in nature. It seems quite likely that most colonies in Circaea consist of only a single genotype. Small halictid bces remain fairly constant on the flowers of Circaea, at least within a colony, but it is not known il' they preferentially seek other distant colonies of Circaea over more convenient locally available fiowers of other species, Syrphid fiies, on the other hand, I'requently shift their visits to flowers ofother species of plants and probably carry little polten between widely separated colonies of Circaea. Thus, the result of "outcrossing" these plant-insect interactions in the species of Ciraaea appears to be another rather complex {'orm of sell' pollination, but with the retention at the same time of a mechanism that allows a certain degree of outcrossing to take place. Acknowledgments Professor Peter H. RAvEN first suggested CVrcaea as an interesting research prospect and I would lilce to thank him for his continued interest, advice and encouragement during the course of this study. I am grateful to Professor K. IwATsuKi fbr his kindness in making the facilities of the Department of Botany, Kyoto University, available to rne during my stay inJapan and for his help in many other ways. I also wish to thank Drs. H. KoyAMA, T. SHmnzu, G. MuRATA, M. KATo and H. NisHiMuRA lbr taking me to impor- tant localities in central and northern Japan, and Emily W. WooD for her assistance in the field and with the specimens and for her help with the manuscript. I would also like to thank P. F, STEvENs for his comments on the manuscript. Drs. A. SAKAi, M. ONo, K. SoHMA, H. KANAi, E, MiKi, S. MiTsuTA, H. NisHrDA, M. TERABAyAsHi, K. UEDA, MJ WAKABAyAsHr and T. YAHARA helped in numerous ways. The Syrphidae, which constituted the bulk of the insect collections, were identified by Dr. F. Christian THoMpsoN; Drs, George C. EicKwoRT, C. D. MicHENER and Y. HiRAsHiMA determined the bees; other insects collected on the flowers of Circaea were identified by Drs. William BRowN, R.J. GAGNE, Lloyd KNuTsoN, P. H. MARsH, W, N. MATHIs, C. W. SABRowsKy and G. STEysKAL. I am especially gratefu1 for their help. Support {'rom the U,S. National Science Foundation through individuat grants to P.H. RAvEN and D,E. BouFFoRD are gratefu11y acknowledged. NII-Electronic Library Service The Japanese SocietySooiety for Plant SystematicsSystematios 154 Acta Phytotax， Geobot． Vo1 ． XXXVIIl 要 約 ミ ズ タ マ ソ ウ 属 は 北 半球 に 広 く分布 し ，落 葉樹林 の 湿 っ た 林 床 に 生 育 す る匐 枝 を持 つ 多 年草 で あ る 。 一 本 属 は 2 つ の 群 に 分 け られ る。 第 群 の 花 は 総 状 花序 の 軸 か ら開 出 し た小 花柄 に つ き （Fig． − が し た に 。 が い よ 長 い た め ， は 直接 柱 頭 に 花粉 を落 せ な 1 d ）， 花 序 伸 長 後 開 く 柱 頭 雄 ず り 葯 い の 一 い 一 一 〜 。 ま た ， 葯 裂 開 も 斉 で は な 。 般 に ， 毎 日 花 序 あ た り 1 2 個 の 花 が 開 く。 こ の 群 の の つ い る ．1−C に が あ 多 くは 蜜腺 が 花筒 開 口 部 か ら き 出 し て （Fig ）。 開 花 は 気 候 と温 度 関係 り ， 蕾 が 開 き は じ め る 15℃ は 本 属 の 訪 花 昆 虫 が 活 発 に な る温 度 で あ る 。花 が 互 に 離 れ て い る の で ， へ の 訪 花 昆 虫 は 花 か ら花 飛 び 移 る必 要 が あ る 。 こ の 群 は 本来 他 家受 粉 で あ る が ， 自 家 受粉 可 能 性 もあ る 。 二 こ 第 群 の 花 は 総状 花序 が 伸 長 す る前 に 数個 同 時 に 開 く。 の 時 に小 花柄 が直 立 し て い る の で ， Fig．1−a こ の ア ブ ラ ナ 科 に 見 られ る よ う に ， 開 い た 花 は 互 に 接 し て い る （ ）。 群 の 花 を 訪 れ る 昆 へ 虫 は 開花 して い る花 を花 か ら花 と歩 き ま わ っ て 訪 れ る こ とが で き ， 飛 ぶ 必 要 が な い 。 柱 頭 と こ の こ 雄 ず い の 長 さ は等 し く， 受 粉 は しば しば蕾 の 中 で 行 な わ れ て い る こ と が あ る 。 と は 天 候 こ の 不 順 時 に 普 通 に 見 られ る が ， 良 い 天 気 の 時 に は 葯 が裂 開 す る直前 に 花 が 開 く と もあ る で ， 他 家 受粉 も可 能 で あ る。 Syrphidae ハ Halctidae コ ハ 訪 花 昆 虫 の 主 な も の は （双翅 目 ， ナ ア ブ科 ） と （膜 翅 目， ナ ア 一 ハ コ ハ バ ブ 科 ） で あ る 。 般 に ， ナ ア ブ 類 は 湿 っ た ， 日 影 に 生 え る 植物 を訪 れ る が ， ナ チ 類 は の の つ い っ 乾 い た ， 日 当 り 良 い 所 を 好 む 。 こ れ ら 昆 虫 は 花 を 動 き ま わ て る間 に ，受 粉 を 行 て い ハ エ ハ る 。 舌 の 短 い や チ の 訪 花 は 植物 群 に選 択性 を与 え て きた よ うで あ る 。 そ の 結 果 ， 外 交配 一 一 一 の っ い を す る第 群 多 くは 蜜腺 を持 て る 。 方 ， 部 の 外 交配機構を 残 しな が ら ， 自家受粉機 二 マ ニ 能 を 発達 させ た 第 群 は ， 冷温 帯 の 林 床 に 生 育 す る ミ ヤ タ タ デ に 顕 著 な 分 化 を もた ら し た 。 References AvERETT ． E ． and D ． E ． BouFFoRD 1985． The flavonoids and Havonoid syste 皿 atics of Circaea Gircaeeae ， J ， （ ， − Onagraceae ）。 Syst． Bot ．10 ： 363 373 ． BENGIT P M 1966 Synthesized α γoα θα 泌 X lutetiana Bot Soc Brit Islcs Proc 6 ： 271 ， ． ． ． ψ ， ． ． ． ． ． BouFFoRD D E l982a The systematics and evolution of Circa砌 Onagraceae Ann Missouri Bot ， ． ． （ ）． ． ． − Gard ，69 ： 804 994 ． − 一＿ ，1982b ． The genus Circa砌 （Onagraceae in Japan． Acta Phytotax ． Geobot ．33 ： 28 40 ． ） ’ CoopERRIDER ， T ． S ．1962． The occurrerlce and hybrid nature of an Enchantcr s Nightshade in Ohio ． Rhodora 64 ： 63＿67． HABER ， E ．1967． Systβmatic studies in the genus Circaea in Ontarie ． M ．S． thesis， University of Ontario． 一 ，1977， Circaea X intermedia in eastern North America with particular reference to Ontario ． − canad ． J． BQt ．55 ： 2919 2935 ． KNuTH P ．1908 ． Handbook of Flower Pollination 2 ： 45 〔｝−452 ， Translation from Ge an by ． R ． ， J Ainsworth DAvls Clarendon Prcss Oxford ． ， ． citamaedr s und ？ KuGLER ， H ，1938． Sind Veronica ］ L ． CircaeatutetianaL ．Schwebfliegenblumen Bot ，Arch ． 39 ： 147−165 ． MOLLER H ，1883， The FertiliSatiQn of FIQwers 265−267 ． Translation from German by D ． W ． TIloMpsoN ． ， MacMi11an and Company London ， ． RAvEN P E 1963 Circaea in the British Isles 、Vatsonia 5 ： 262−272 ， ， ． ． ． 1979． Asurvey of reproductive biology in Onagraceae ． New Zealand ． Bot ．17 ： 575 − 593 一一．．一一一．一， J ． 一 NII-ElectronicN 工 工 Eleotronio Library Service