Research articles NAT. NAT. HIST. BULL. SIAM Soc. 52 (1): 9-26 ，2004

BREEDING SYSTEM ，POST -POLLINATION GROWTH ，AND SEED DISPERSAL IN EXILIS ()

Henrik A. Pedersen 1， Santi Watthancr ，Somran Sudde ，r， and Saw 妙 'e e Sasirar

ABSTRACT

A Th ai population of Gastrodia exilis was studied 佃 the period 27 Oc tober --6 De cember 2002. 2002. Plowering 飢 d fruit set ，phenology ，morphologic 叫 size relations ， and post -pollination grow 出 were examined in 出e field ， and pedicels and seeds were characterized by SEM. 百le relative relative fruit set was found to be 25% on average ， both under natural conditions and in bagged specimens. specimens. No visiting insects were observed ， but the shape of the Lorenz curve and other features features argue against autogamy. Th e breeding system probably involves pollination by minute insects ，possibly thrips. Contrary to the peduncle and rachis ， the pedicels of pollinated flowers underwent underwent pronounced elongation during 伽 it ripening. 百 lis post-pollination grow 出阻kes place place mainly by cell elongation and describes a more or less sigmoidal c町 ve. Gr owth ceases just just before dehiscence of the capsule. We propose 白at elongation du 巾 g 合uit ripe 凶ng should should be seenωa way of maximizing the expo 制限of the distal part of 出e to the wind ，

出 us facilitating seed dispersal by “miniatuI 官， low-power jactitation".

Key words: orchids ，Gastrodiinae ，phenology ，pollination ，fruit set ， wind dispersal

問 TRODUCTION

THE Gastrodia R. Br. encomp 酪 ses 16- 17 species di 柑 ibuted from In dia and Madagascar in 白e west to e価低m Siberia ， ， the Pacific islands ，and Aus 住alia in 血e eas t. A single species ，G. sesamoides R.Br. ， is naturalized in South A 食ica (L 町 DER & Ku 昭 .WEIL ，1999: 354). Gastrodia Gastrodia belongs to the small subtribe Gastrodiinae ，a pantropical alliance of presumably primitive epidendroid orchids (DRESSLER ，1993; FREUDENS1 宮町&RASMUSSEN ， 1999; 1999; MOLVRAY ET AL. ，2000; FREUDENSTE 町&CHASE ，2001). 百le seven genera assigned to to this subtribe (A 町 opus ，Didymoplexiella ，Didymoplexiopsis ， ，Gastrodia ， Neoclemensia ，Uleiorchis) all consist of achlorophyllous species. In MONTFORT & Kus 百双S' (1940: (1940: 621) classification of the Orchidaceae into five types ，創Tanged in ascending order of dependence upon their mycosymbionts ，血 e genera under Gastrodiinae fit type V (the Corallorhiza Corallorhiza type) - except for the circumstance 白at they are not universally devoid of roots. roots. Th us ，these genera belong to the class of ecophysiologically most reduced orchids andc 組 be considered holomycotrophic (sensu H. N. RASMUSSEN ，1995). For details on

IBotanical IBotanical Museum ，University of Copenllagen ，Gothersgade 130 ，DK ・1123 Copenllagen K ，De mn 紅 K 2Queen 2Queen Sirikit Botanic Garden ， P. O. Box 7，Mae Rim ，Ch iang Mai 50180 ，百 lailand 3Porest 3Porest Herbarium (BK め， National Park ，Wildlife and Plant Conservation De par 回 .ent ，Chatuchak ，B 叩 gkok 10900 ，Th ail 釦 d Received Received 9 A 噌 1St 2;∞ 3; accepted 28 January 2004.

9 10 10 HENRIK A. PEo 眼 S凹， SANTI WATIHANA ，SOM 臥 N SUOOEE ， ANO SAWITREE SASIRAT

the the ecophysiology of Gastrodia 阻 d Didymoplexis ， see KUSANO (191 1)， BURGEFF (1932) ， McLE 州 AN (1959) ，and CAMPBELL (1962 ，1963 ， 1964). KURZ (1866) found the pedicels of Didymoplexis pallen 司 Griff. to be highly interesting: Originally “Originally they are only 2-6 lin. long ， but when the fruit becomes fully ripe ， they elongate and are often twice as long as the whole plant". Subsequently ，pronounced elongation of the the pedicels during fruit ripening tumed out to be widely distributed within the subtribe

Gastrodiinae. Gastrodiinae. Up to now ，this phenomenon has been reported from taxa cu 町 entlyassigned to to Auxopus (RIDLEY ， 1930; SUMMERHAYES ， 1953; HUNT ，1984) ，Didymoplexiella (SMITH ， 1920; 1920; WOOD ET AL. ，1993) ， Didymoplexis (e.g. ，HEMSLEY ， 1883; SM lT H ， 1905; RIDLEY ， 1930; 1930; BURGEFF ， 1932; SUMMERHAYES ，1953 ， 1956; HALL 邑， 1977;S1 芭WART & HENNESSY ， 1980; 1980; LEWIS & CRffiB ， 1991; PEARCE & CRffiB ，2002) ， Gastrodia (e.g. ，SM lT H， 1905; CARR ，1929 ， 1935; BURGEFF ， 1932; GARAY & SWEET ， 1974; JOSEPH ET AL. ，1980) ，and Uleiorchis Uleiorchis (COGNIAUX ， 1893-1896; HOE 削 E， 1945). Pedicel Pedicel elongation during fruit development in representatives of the Gastrodiinae has never never been described in detail ，and its adaptive significance (ぜ any) remains poorly understood. understood. Our general knowledge of the reproductive. biology of these is very limited. limited. To help remedy these deficiencies ，we examined a population of Gastrodia exilis Hook.f. Hook.f. (syn. G. siamensis Rolfe ex Downie ， G. hayatae Tuyama) in 2002.

MATE RlAL AND METHODS

Study Species and Population

G. G. exilis is known only from a few sca 仕ered localities in In dia (Kerala ，Meghalaya) and Th ailand (SEIDENFADEN ， 1978: 181; JOSEPH ET A L.， 1980; SATHISH KUMAR & Su 阻 SH KUMAR ， 2001). According to these ，it grows among moist decaying leaves on the forest f1 00r at 500 ー1300 m altitude and f1 0wers during the monsoon. G. exilis is a 5-30 cm high ，delicate ，lea f1 ess herb (Fig. 1).官 le 0.5-7 cm long rachis carries carries 2-13 fragile whitish f1 owers ， each produced on a c. 5・mm long pedice l. The f1 0wers do not emit any scent that can be perceived by the human nose ，and they appear to offer no reward to potential pollinators. Th e 佃 d are connate for almost their whole length length to form a narrowly um-shaped perianth with slightly erose margins (Fig. 2). 百le labellum labellum is ovate with slightly erose m 訂 gins ，a pair of almost globose ， swollen glands at its its base (see transverse section in F. N. RASMUSSEN ， 1982: Fig. 64F) ，and a pair of short keels keels cI ose to its apex. It is firmly attached to a sub cI avate ，distally winged . Th e 組 ther is incumbent and holds four sectile ， granular pollinia. lt is subtended by a well- developed developed rostellum ending in a minute viscidium.τ 'h e receptive part of the stigma is proximal proximal on the column. For informative sections through the column ， see F. N. RASMUSSEN (1982: (1982: Fig. 64). 百le cI earance between 組 ther and labellum is c. 1(-2?) mm. Unpollinated f1 0wers are soon shed from the nodes on the rachis. A pollinated f1 0wer looses its perianth ， after after which the pedicel elongates markedly (Fig. 3) until the ellipsoidal capsule dehisces by six longitudinal slits (Fig. 4).

Th e study population was si 卸 ated ne 紅 the summit of Doi Pu i in northem Th ailand ， Chiang Mai Pr ovince (1 8 0 49' 36.0" N ，098 0 53' 15.9" E). Th e habitat can be characterized as as a west-exposed ，10 0 slope in hill evergreen forest (cf. Table 1) at c. 1550 m altitude. BRE E DI NG SYS T EM ET C. IN GAS TR OD IA EX IL! S (OR C I-I IDACEAE ) 11

Fi gut 巴お 1--4. Gas {/' odia e.r ili .l'. 1. I-I ab il. 2. Ra chi s w ilh fl owers and bl1 ds. 3 . R ac hi sw ilh ca psl1 l es on 巴longa led P巴dic els. 4. R 巴ce nl ly cl ehi scc d c‘Ip sl1 lc. - Doi P l1 i. No rrh e rn Thail ancl ，O Clober- Nove lllb er 2002 Ph olog rap h by 1-1 . A. Pecl erse n 12 12 HENRIK A. PEDERSEN ，SANTI WATTHANA ，SOMRAN SUDDEE ，AND SAWITREE SASIRAT

Table Table 1. List of vascular plants occurring in the study area on Doi Pui ，November 2002

TREES Archidendron Archidendron clypearia (Fabaceae) Betula Betula alnoides (Betulaceae) Castanopsis Castanopsis acuminatissima (Fagaceae) Castanopsis Castanopsis diversifolia (Fagaceae) Cinnamomum iners (Lauraceae) Engelhardtia Engelhardtia spicata (Juglandaceae) Eurya acuminata var. wallichiana (Th eaceae) Glochidion Glochidion acuminatum (Euphorbiaceae) Helicia Helicia nilagirica (Proteaceae) Li tsea verticillata (Lauraceae) Olea Olea salicifolia (Oleaceae) Phoebe lanceolata (Lauraceae) Pyrenaria Pyrenaria cameliiflora (Th eaceae) Pyrenaria Pyrenaria garrettiana (百leaceae) Quercus Quercus semiserrata (Fagaceae) Rapanea yunnanensis (Myrsinaceae) Symplocos Symplocos cochinchinensis S.str. (Symplocaceae) Turpinia Turpinia pom 俳ra (Staphyleaceae) SHRUBS Ardisia Ardisia virens (Myrsinaceae) Daphne sureil (百lymelaeaceae) Euodia tr 伊hylla (Rutaceae) Maesa montana (Myrsinaceae) Melastoma malabathricum S.str. (Melastomataceae) Sarcandra Sarcandra glabra (Chloranthaceae) SCANDENTS Mussaenda parva (Rubiaceae) Rubus ellipticus (Rosaceae) Smilax Smilax sp. (Smilacaceae) HERBS Alpinia Alpinia sp. (Zingiberaceae) Commelina diffusa (Commelinaceae) Curculigo Curculigo gracilis (Hypoxidaceae) Dendrobium falconeri (Orchidaceae) Dianella Dianella ensifolia (Liliaceae) Gastrodia Gastrodia exilis (Orchidaceae) Ophiopogon intermedius (Liliaceae) Otochilus Otochilus albus (Orchidaceae) P 伊er sp. (Piperaceae) Polygonum sp. (Polygonaceae) Strobilanthes Strobilanthes consors (Acanthaceae) Zeuxine Zeuxine nervosa (Orchidaceae) BREED 町 G SYSTEM ETC. IN GASTRODIA EX. 山 S (ORCHIDACEAE) 13

百le plants were growing in black ， humus-rich soil with a neu 回 1pH and overlayered with c. c. 5 cm of litter.

General General Notes on Sampling and Data Analysis

百le study population was examined on 27 October ，3 ，9 ，21 ， 28 November ， and 6 Dec 四 nber 2002. In組釘 ea of approximately 1000 m 2， 23 specimens of G. exilis were found found and examined during the six days of study. However ， since not all specimens were present present (or discovered?) 合om the beginning ， and since some of them were damaged (experimentally (experimentally or by incidents unknown to us) before the end of 出e study ， not all of them could could be included in all calculations. Statistical Statistical analyses were performed by 血e program Pra ctiStat (ASHCRO Ff & PE 阻 IRA ， 2003). 2003). Pri or to inclusion in statistical tests ，all data sets were checked for normality. In cases cases where normality could not be confrrmed ，a non-par 創 ne 住ic test was chosen.

Flowering Flowering and Fruit Set

For For 20 specimens ， the total number of flowers was established from the number of nodes nodes in the raceme. By the end of flowering ， the natural fruit set w 部 determined as the number of caps 凶es produced ， and the relative fruit set w 拙 calculated. Spearman' s rank correlation correlation coefficient w 出 used to test for correlation between the numbers of flowers and capsules capsules produced. Additionally ，血 e specimens were sorted 泊 ascending order by the number of capsules they produced ， and the cumulative percent of specimens was then plotted plotted against 出at of 白e capsules to form a Lorenz curve (W E町 ER & SOLBRIG ， 1984; CALVO 1990). Thr oughout 血e flowering time ，we attempted to spot any insects visiting the flowers. flowers. On 27 October ，two other specimens ，still in bud ， were bagged (width of meshes: 1. 0 x 1.5 mm). By the end of flowering ，出 .e fruit set was checked in order to test the possibility of of spontaneous autogamy.

Phenology Phenology

Th e mode and sequence of flowering in a raceme was established by repeated observation observation of 20 specimens throughout the study period. In each of 由e 20 racemes ， the numbers numbers of flower buds ， fresh flowers ， and capsules + shed flowers were counted six times. times. For For each of the. 24 capsules that completed development to seed dispersal ， the approximate approximate time of dehiscence was noted.

Morphological Morphological Size Relations

For For each of the 23 specimens ， the total number of flowers w 前 established from the number of nodes in the raceme ， and the maximum lengths of peduncle and rachis were scored. 百le three data sets were tested pairwise for correlations (Spearman's r: 創 lk correlation coefficient) ， and the best-fitting curves were estimated by linear regression. 14 取 NRIK A. PlID ERS 聞， SANTI WA 1THAN A ，SOMRAN SUDDEE ，釧D SAWITREE SASIRAT

F'O r each 'O f the 24 caps 叫 es (distributed am 'O ng 11 racemes) 白 at c'O mpleted development t 'O seed dispersal ， the maximum length 'O f the pedicel was sc 'O red and c 'O rrelated (Spearman's (Spearman's rank c'O rrelati 'O n coefficient) wi 白 the maximum lengths 'O f the coηesp 'O nding peduncles peduncles and rachises. 百le best- 自白血 g curves were estimated by linear regressi 'O n.

Post-pollination Post-pollination Growth

All All meas 町 'ements menti 'O ned in 白 is secti 'O n were taken fr 'O m plants 白紙devel 'O ped at least least 'O ne ripe capsule ，when all fl 'O wers had already withered. Th e gr 'O wth studied 血.u s represented represented p'O st-p 'O ll 加ati 'O n gr 'O w 血 F'O r each 'O f th 'O se 11 specimens 白紙 devel 'O ped at least 'O ne ripe caps 叫.e ，白e leng 白 s 'O f peduncle and rachis were measured repeatedly until 血 e first day 白紙 a caps 叫ew 部 'O bserved t 'O have dehisced. 百lI s day w 出 defmed as “ day 0" ， and the individual series 'O f measurements measurements were arranged acc 'O rdingly. F'O rb 'O血 peduncle and rachis ，this resulted 泊 白 ree series 'O f meas 町 'ements: (i) a series 'O f specimens (n = 2) measured 'O n “ day 0" as well 部 7 days bef 'O re; (ii) a series 'O f specimens (n = 4) measured 'O n “ day 0" as well as 12 ，18 ， 佃 d 25 days bef 'O re; (iii) a series 'O f specimens (n = 5) measured 'O n “ day 0" as well as 8， 15 ，27 ， and 33 days bef 'O re. F'O r each series ，血e mean was calculated f'O r each date and ， whenever whenever applicable ，Pears 'O n's c'O rrelati 'O nc 'O efficient was calc u1 ated 旬 test f'O rc 'O rrelati 'O n between between peduncle 'O r rachis len 訓1， and time bef 'O re dehiscence 'O f 曲 e flrst capsule. F'O r each 'O f 血 e 24 caps u1 es that devel 'O ped t 'O seed dispersal ，血e len 併1 'O f 出e pedicel was measured repeatedly t 'O the day 'O f capsule dehiscence. 百世 s day w 部 defmed 錨“day

0" ， as ab 'O ve ，f 'O r the f'O ll 'O wing 田serie 白s 'Oぱ fme 儲 u悶 :men 蹴ts 配: (町 as 鴎erie 邸s 'O f pedic 印els (刷 n= 3) measured measured 'O n “"da 可yOぴ"邸 well 酎.sa 7d也ay 戸s bef 'O re; (但 II) as 田erie 郎s 'Oぱ f pedicels (刷 n=5 町) mea 拙.s ure 芭e o叩n “"da 町y 0" 酪as well 卸as6 佃 d 13 伽day 戸s bef 'O re; (皿) a series 'O f pedicels (n = 5) measured 'O n “ day 0" as well as 12 ，18 ，加d 25 days bef 'O re; (IV) a series 'O f pedicels (n = 11) measured 'O n “ day 0" 出 well 部 8， 15 ， 27 ，加d 33 days bef 'O re. F'O r each series ， the me 佃 was calculated calculated f'O r each date and ， whenever applicable ，Pears 'O n's c'O rrelati 'O nc 'O efficient was calculated calculated t 'O test f'O rc 'O rrelati 'O n between pedicel length and time bef 'O re dehiscence 'O f the capsule. capsule.

Scanning Scanning Electron Microscopy of Pedicel and Seed

A pedicel fr 'O m ay 'O ung caps 凶e that had just begun t 'O devel 'O p as well as a pedicel 仕om 姐'O ld ， dehisced caps 凶e were c'O llected and flxed in F AA. Fr 'O m each 'O f these pedicels ，a pr 'O ximal ，a median ， and a distal secti 'O n were critical p 'O int drled and examined by scanning elec 住on microsc 'O py (SEM). Additi 'O nally ，tw 'O ripe capsules were c 'O llected and 命ied ，after which seeds were examined by SEM. 百le SEM studies were carried 'O ut by a Je 'O l JSM 5410LV micr 'O sc 'O pe after previ 'O us c 'O ating 'O f the samples with g 'O ld. BREEDING SYSTEM ETC. 町 GASTRODIA EX. ι IS (ORCHIDACEAE) 15

Table Table 2. Phenologic a1 progression in Gastrodia exilis throughout the study period. For flower flower buds ，f 詑sh flowers ， and capsules + shed flowers ， the mean :!: SD is indicated indicated for each date

270c t. 3 Nov. 9. Nov. 21 Nov. 28 Nov. 6 Dec.

帯flower buds 1.∞:1: 1. 59 O. ∞ま O. ∞ O.ω 企O. ∞ O. ∞企 O. ∞ O. ∞主 O. ∞ a∞主 O. ∞ #白官 sh flowers 1. 50 主1. 79 0.20 ま0.52 0.1 0 :1: 0.45 O. ∞:1: 0. ∞ O. ∞ま 0; ∞ O. ∞主 O. ∞ capsules # capsules + shed flowers 3. 30 :1: 3.64 5.60 主2.85 5.7 0 :1: 2.7 7 5.80 企2.59 5.80 :1: 2.59 5.80 :1: 2.59 % cap 田ules dehisced 。 13 33 54 54 l∞

RESULTS

Flowering Flowering and Fruit Set

Th e individu a1 specimens of G. exilis produced 2・13 flowers (μ= 5.95; SD = 2.44) and developed 0ー7 capsules (μ= 1. 50; SD = 1. 79). Th e relative fruit set ranged between 0.00 組 d 0.67 (μ= 0.25; SD = 0.23). No statistic a1 1y significant correlation between the numbers of flowers and capsules produced was found (P > 0.05). 百 le relative con 凶bution of of specimens to the capsule pool of the population c組 be seen from the Lorenz curve (F ig. 5). 5). No insects were observed to visit the flowers. 官le two bagged specimens of G. exilis had a relative fruit set of 0.00 佃 d 0.50 ， respectively. respectively.

Phenology Phenology

Th e flowering univers a1 1y started from the proximal p制 of the raceme and lasted up to to c. 1 week. A survey of the over a1 1 progression in flowering is given in Table 2. At 白e bottom bottom of the table is indicated the progression in fruit ripening ， based entirely on those capsules 白紙 completed their development to dehiscence (see also Fig. 6).

Morphological Morphological Size Relations

Th e maximum length of peduncle varied between 6.0 and 27.7 cm'(μ= 17.05; SD = 5.53) ， the maximum length of rachis r叩 .ged from 0.6 to 7.6 cm (μ= 3.68; SD = 1. 93) ，佃d the the individu a1 specimens carried 2-13 flowers (μ= 5.5 7; SD = 2.50). All pairwise tests revealed revealed significant ，positive correlations (P < 0.05). Th e equations of the regression lines are are given in Table 3. Th e maximum length of pedicel varied between 2.9 and 16.0 cm (μ= 7.4 9; SD = 3.73). 3.73). A significant ，positive correlation (P < 0.05) was found between the maximum pedicel pedicel and peduncle lengths as well as between the maximum pedicel and rachis leng 出s. 百le equations of the regression lines are given in Table 3. 16 HENRlK A. PEDERSEN, SANTI WATTHANA, SOMRAN SUDDEE, AND SAWITREE S AS lRAT

80

(f) ..!!! :::J (f) a. ro ....u 60 0

0~ Q) > :.:; 40 ..!!:! :::J E u:::J 20

0 20 40 60 80 100 Cumulative% of specimens

Figure 5. Lorenz curve for Gastrodia exilis. A diagonal li ne from the lower left to the upper right corner would indicate equal contributions of individuals to the capsule pool, while curves deviating from thi s diagonal line indicate inequality. Equality is usuall y associated with spontaneous autogamy.

27 Oct. 3 Nov. 9 Nov. 21-28 Nov. 6 Dec.

Figure 6. Phenological progression in Gastrodia exilis during the period of observation. Small closed circle: bud. Large closed ci rcle: flower. Closed triangle: undehi sced capsule. Open triangle: dehisced capsule. It shoul d be borne in mind th at this tigure deals with phenology onl y and says nothing about the natural level of fruit set. BREED 悶 G SYSTEM ETC. 別 GASTRODIA EXI Ll S (ORCHIDACEAE) 17

Table Table 3. Equations for linear regression lines - representing positive mo 中hological size correlations correlations in Gastrodia exilis Abscissa Abscissa (x) Ordinate (y) Regression line Max. length of peduncle (cm) Max. length of rachis (cm) y= -0.4 2 + 0.24x Max.leng 出 of peduncle (cm) Total number of flowers y= ー0.4 1 + 0.35x Max. length of rachis (cm) Total number of flowers y= 1.94 + 0.98x Max. length of peduncle (cm) Max. length of pedicel (cm) y= -3.58 + 0.53x Max. length of rachis (cm) Max. length of pedicel (cm) y= 1. 28 + 1. 38x

Post-pollination Post-pollination Growth

Wi 白 regard to. the length of peduncle ， the data sets representing specimen series (i) and and (iii) were unfit for statistical test 均 (normality not confirmed). The test of series (ii) against against the time of sampl 泊g did not reveal a significant correlation between the length of peduncle peduncle and time before dehiscence of the first capsule (P > In 0.05). other words ，it could not not be documented that the peduncle continues to grow after flowering has ended. Conceming the length of rachis ， the data set representing specimen series (i) was unfit for for testing (normality could not be confrrmed). Th e tests of series (ii) and (iii) against the time time of sampling did not reveal a significant correlation between the length of rachis and time time before dehiscence of the first capsule (P > 0.05). Thus ， the rachis appears not to continue continue growth after flowering has ended. With regard to 血e leng 白 of pedicel ， the data sets representing capsule series (1) and (11) (11) did not permit testing (normality not confirmed). 百le tests of series (III) and (IV) against against time of sampling both revealed a significant correlation between the length of pedicel pedicel and time before dehiscence of the capsule (P << 0.05). Hence ， the pedicel of a developing developing capsule does continue growth after flowering has ended. A survey of the overall overall growth of the pedicel after 白e end of flowering is given in Table 4， and Figs. 7 and and 8 illustrate the growth and the relative growth ，respectively ， of the pedicel for series (II1) (II1) and (IV).

Table Table 4. Growth of pedicel in Gastrodia exilis after the end of flowering (capsule series III III and IV ，cf. the Material and methods section). For each series and date ， the length length of pedicel (in cm) is indicated as the mean :!: SD Days before dehiscence Series III Series IV of of capsule (n = 5) (n = 11) 33 33 0.76 :!: 0.34 27 1.00 :!: 0.39 25 25 1. 65 :!: 0.51 18 18 3.38 :!: 1. 09 15 15 2.68 :!: 2.19

12 12 4.86 主 2.44 . 8 . 4.67 :!: 2.5 5 。 6.76 :!: 5.61 6.06:!: 2.23 18 H ENRIK A. PEDERSEN, SANTI W A TTl-lANA, SOMR AN SUDDEE, AND SAWITREE SASIRAT

8

7

6

~ E ~ 5 Qj .!:! 1:l Q) c. 4 ~ 0 .r::..., 0"> 3 c Q) --' 2

•· ····· ·· ·· •

01-----.----.----,---~,----.----,---~ -35 -30 -25 -20 -15 -10 -5 0

Days after dehiscence of capsule

- Series Ill ···•·· Series IV

.r::..., 0"> c 80 .!!! ro c ~ ~ 0 60 cf. c Qj .!:! 40 1:l Q) c.

20 •·· ·· ··· ·· ·•

0~----,-----,-----~----r---~r---~-----; -35 -30 -25 -20 -15 -10 -5 0

Days after dehiscence of capsule

Figures 7-8. Growth and relative growth of pedicel in Gastrodia exilis after the end of flo wering. 7. Length of pedicel (for each series indicated as means for each elate) as function of time. 8. Relative length of pedicel (i.e. in percent of length at the time of capsule dehiscence) as fu nction of time; fo r each seri es, the means plotted in Fig. 7 have been transformed to percent ages. BREED ING SYSTEM ET C. IN GASTROD IA EX ILl S (ORCHJDACEAE ) 19

"里郡司随時箇自開~

Figures Figures 9- 10 . Ep id ermi s fr om pedic els of Gastrodia ex ili .l' depi ct ed by SEM. 9. Young ped ic eJ. 10. O ld pedice J. - Scale bar s = 100μ 111 20 HE N R IK A. P E DER SEN ，SANT I W A TTH ANA ，SOMR AN S U DDEE ，AN D S AW ITR E E SA SIR A T

Figur 巴s 11- 12. Se ed from G 仙 台tr odia ex ili s d巴pi ctedb y SEM. 11. Seed. 12. Med ian part of t巴Slas ho w in g th e

weak r巴ti cu1 ate Lhi cke nin gs of Ih 巴 per iclin a1 ce ll wa1 1s. - Sca 1巴 bars = 100μm BREEDING SYSTEM ETC. IN GASTRODIA EX 山 S (ORCHIDACEAE) 21

Scanning Electron Microscopy of Pedicel and Seed

百le SEMcomp 回 sons of sections 企om a young and an old pedicel revealed the shape of of the epidermal cells. 百 le differences were identical for the youn g/ old pairs of proximal ， median ，and distal sections. In most epidermal cells from 由e young pedicel ，血 e peri c1泊 al wall wall was 1泊e釘・oblong in outline (Fig. 9) ，w hi1 e it was band-shaped 加 most epidem 叫 cells cells from the old one (F ig. 10). 官le light brown seed c. is 1. 5 mm long and consists of a slenderly ellipsoidal embryo ina 血泊， papery testa which is slenderly fusiform and somewhat curved (Fig. 11). 百le testa testa cells are almost similar and rectangul 釘 with weak reticulate secondary thickenings on their periclinal walls (Fig. 12). Th e junctions of their anticlinal walls do not protrude sig 凶白.cantly.

DISCUSSION

Breeding Breeding Sys 総m

Very little is known about the diversity of breeding systems wi 血泊出.e Gas 佐odiinae. CHRISTENSEN (1994: 433) presumed 出at most species of Gastrodia 釘 e pollinated by bees. However ， bee pollination has only been observed 泊 G. sesamoides ，which is pollinated by a small xylocopid bee (Exoneura sp.) ga 出回ng pseudopollen from the labellum (1 0 阻 S 1981 ， 1985). CARR (1 928) observed fly pollination 泊 G.javanica (Blume) L 泊dl. (sub syn. G.mal 句， lana Ridl.). Spontaneous 加 togamy has been described for G. cunninghamii Hook.f. (LEWIS (LEWIS & CRIBB ， 1989: 48) and G. verrucosa Blume (CARR ， 1929: 40 ， sub syn. G. holttumii Carr) Carr) ， while STEWART & HENNESSY (1 980) noticed cleistogamous pollination in Didymoplexis Didymoplexis verrucosa J. Stewart & E. F. Hennessy. KUSANO (1 915) thoroughly examined the the fertilization and embryology of G. elata Blume. He demonstrated 白紙 the flowers are fully fully self-compatible and 血at no parthenogenetic reproduction seems to take place. G. G. exilis does not really fit any of 白e 位aditionally recognized pollination syndromes (e.g. ，VOGEL 1954; VAN DER PUL & DODSON ，1966) ， but it shares the combination of connate connate perian' 血 parts ， a relatively short ，w 泊.ged column ，and granular poll 加ia with a considerable considerable number of other holomycotrophic species. MOL VRA Y ET AL. (2000) suggest 白紙白is combination of features may well be recognized 出 a special “achlorophytic pollination pollination syndrome". 官ley reg 釘 d fungus 伊 ats (Dip 飽ra: Mycetophilidae) as 血.e most likely likely pollinators ， but also consider autogamy a possible altemative. 百le flowers of G. exilis exilis correspond reasonably well with flowers of species 白紙 VOGEL (1 978) reported to be pollinated by fungus gnats. However ，no part of the G. exilis flower obviously mimicks a fungus ，and there appears to be no olfactory mimicry either. Th e brief span of flowering ， the detection of fruit set in one of the bagged specimens ， and 血e fact 白紙 no insect visitors were observed during our study of G. exilis indicate 白紙 由is species might be autogamous. 百lis is supported by the lack of a positive correlation between between the number of flowers and capsules produced by the individual specimens. In species species poll 泊ated by insects ， many-flowered spec 加 ens usually produce relatively more capsules capsules th 佃 few-flowered ones. In G. exilis we even found a positive correlation between plant plant height (expressed by the lengths of pedun c1 e and rachis) and 血e number of flowers 22 出 NRIK A. PEo 盟国N ，SANTI WA 'ITHAN A ，SOMRAN SUOD 凪 AND SAWITREE SAS lRA T

(Table (Table 3)-which must 白川町紺en 併記 n the floral advertisement in many-flowered specimens specimens (though not tow 紅白 geophilous insects such as fungus gnats). On the other hand ，a significant number of open flowers (and ，hence ，a realistic chance toencoun 町 visi 曲19 加sects) w 鎚 only found on 27 October (Table 2; Fig. 6) ， and the well- developed developed ros 飽11 0m as well as 由.eb 槌 al position of the rec 叩 tive stigma p副 (f. 釘 removed

企om 出ean 血er) s関 m to obstruct rather th 叩 facilitate spontanωusau 旬 g創 ny. Additionally ， the the overall fruit set 泊由e two bagged spec 泊lens was only 25% as opposed to 血.e c. 100% expected expected for an autogamous species (e.g. ，CA TI..町 G ， 1990). Finally ， the Lorenz c町 ve for O 町 population of G. exilis (Fig. 5) is much more simil 紅 to the curves 血at CAL vo (1 990) provided provided for allogamous orchid species 白血 for the autogamous Oeceoclades maculata (Li nd l.) L泊dl. Our data do not unequivocally reveal the breeding system of G. exilis ， but they favour a scenario of pollination by insects sufficiently small to force the 1. 0x 1. 5 mm meshes surrounding surrounding the bagged specimens (a possibility 白紙 does not seem unlikely ，cf. the very sma11 sma11 clearance between anther and labellum). Th ese small insects could be fungus gnats ， but but a more qualified guess would be thrips ('百 lys 佃 optera). 百lU S，出 rips 紅 e generally smaller smaller (most species 0.5 -4 mm long) and 紺 eamlined and seem much better suited 旬 sneak sneak through fme mesh. In some species of thrips the males 紅 e known to mediate autogamy 泊 some plants ， while the females conduct allogamy. Th e latter process is usually associated associated with the females depositing eggs in 血.e flower (e.g. ， O. HAGBRUP ，1950 ， 1954; E. E. HAGBRUP AND O. HAGBRUP ， 1953). Consequently ，出 rips and their eggs should be specifically specifically searched for in flowers of G. exilis. Pollination by 白rips might well explain the25% 台uit set in bagged sp 田泊lens and would be consistent with the lack of morphological as as well as olfactory mimicry of fung i.

Pedicel Pedicel Elongation and Fruit Ripening

BURG 日干(1 932: 93 ， 127) mentioned 白at the elongation of the pedicel in D. pallens and G. callosa J.J.Sm. is due to intercalary grow 由， but no information on 血.ena 阻 re of 白is inte 則的growth has been publish 吋 .0 町 SEMsωdies of G. exilis cle 叫 indicate 伽 t strong strong elongation of the individual ce11s plays an important part 泊出e remarkably rapid post-pollination post-pollination growth of the p' edicel (F igs. 9-10 トー at least 回 f釘 as 出e epidermis is concerned. concerned. CARR (1 929: 39) noticed 白紙出e elongate pedicel 泊 G. verrucosa is ho11ow. We found the same condition in G. exilis ， and suggest that it may be due to longiωdinal lacunae lacunae appear 血gin 血e place of 佐ache 紅 yelements 白紙 are destroyed during elongation of of the ground tissue. 百 le post-pollination grow 出 of 白e pedicel in G. exilis seems to fo11ow a more or less sigmoidal sigmoidal curve ， i. e. with the grow 血 rate accellerating by the end of flowering and decellerat 泊g shortly before dehiscence of the capsule (Figs. 7-8).百 le nice fit be 何回n ce 出 e of pedicel elongation and dehiscence of the capsule suggests that 出e post-pollination grow 血 of the pedicel has an adaptive significance in relation to seed dispersal.

Seed Di spersal

百le seed of G. exilis (Figs. 11 ー12) belongs to the so-called Gastrodia type (DRBSSLBR ， 1993: 1993: 53) ， the morphology and anatomy of which coη.espond we11 wi 血血e majority of BREED 町 G SYS 百 METC. 凹 GASTRODIA 脱出'S (ORCHIDACEAE) 23

'O rchid seeds. ARDITTI & GHANI (20 ∞)白 ld 血 at the small size 'O fm 'O st 'O rchid seeds and 出 eir large internal air spaces make them we11 adapted t 'O wind dispersal ， but als 'O rec 'O gnize 白紙血 .e internal air spaces and the difficult-t 'O幽 wet surface 'O f the testa facilitates dispersal thr 'O ugh sma11 run-o 町 rivulets 血 at may f'Ol1'O w rains. Like Like m 'O st 'O ther h'O l'O myc 'O tr 'O phic 'O rchids ， G. exilis usually gr 'O ws in deep layers 'O f decaying decaying leaves ，f 'O r which reas 'O n small run- 'O ff rivulets ass 'O ciated with rain are unlikely t 'O 'O ccur. C 'O nsequently ， we d 'O n'O tc 'O nsider water-assisted dispersal imp 'O rtant f'O r 白 is species. 百世 s leaves us with wind as 出 e presumedly m 'O st imp 'O rtant dispersal agen t. HEMSL 町 (1883) suggested 白紙偽e adaptive significance 'O f the el 'O ngated capsule pedicel 泊 D. pallens is that it “carries up the ripening fruit ab 'O ve the decaying vegetable matter 泊 which the pl 佃 t gr 'O ws". C 組 R (1929: 39) m 'O re explicitly suggested 白紙 the el 'O ngati 'O n 'O f the pedicel in G. verrucosa “ ensures the dispersal 'O f seed t 'O much greater distances 白血 w 'O uld 'O therwise be p'O ssible ， while during fl 'O we 巾 g the plant is rendered inc 'O nspicu 'O us and 白 us less liable t 'O attack". Wh ile it d'O es seem l 'O gical that the ability 'O f the the species t 'O disperse its seeds 'O ver l'O nger distances w i1l increase wi 血 increasing height 'O f the p'O加 t 'O f seed release ， the sぬtements 'O f Hemsley and Carr d 'O n'O t explain why each pedicel pedicel and n'O t just 血 e peduncle el 'O ngates after fl 'O wering. In G. exilis ，p 'O st-p 'Ol1泊 ati 'O n gr 'O w 白ぱ血e peduncle 'O r rachis d'O es n'O t even c 'O ntribute t'O出 eω ta1 height 'O f 白 e plant at at the time 'O f seed dispersal. RIDLEY (1930: 16) described the c'O ncept 'O f jactitati 'O n: “In m 'O st small plants 血 e fruits 紅 'e b'O rne 'O nl 'O ng peduncles ，stand 泊 g we11 ab 'O ve the mass 'O ff 'O liage ，加df 詑quently 出 e pedicels pedicels lengthen 泊合uit and stand stiffly 'O ut S 'O as t 'O exp 'O se 由e 仕凶ts m 'O re th 'O r'O ughly t 'O the wind as it sweeps 'O ver the 'O pen c'O un 町， d'O wns ，mead 'O ws 'O rm 'O untain sides and carries carries the seed s'O me distance. 百le spring 泊 ess 'O f the peduncle a11 'O ws 'O f its being jerked back ，after the blast has passed ，泊 such a manner that the seeds are liable t 'O be thr 'O wn 'O n all all sides 'O f 血 e plan t.官邸 is we11 seen 加 such tall plants as the F 'O xgl 'O ve (Digitalis) ， Evening Evening Primro se (Oeno 幼era biennis) ，組 d theMu11e 加s (Verbascum) ，where the 飽11 racem 邸 bend bef 'O re the wind ，thr 'O wing 血 .e light seed in the directi 'O n 'O f the wind ，and when the breeze breeze dr 'O ps and the raceme rec 'O vers its erect p'O siti 'O n， the seeds 'O n the windward side 紅 e ejected 泊 the 'O pp 'O site directi 'O n". Th e size and s回 ngth 'O f G. exilis is evidently very di 町erent 企om the sturdy herbs ab 'O ve ， but als 'O血 e prevailing wind vel 'O cities in its habitat are are very differen t-一組 d we w i1l argue 伽 t the features characterizing G. exilis and its habitat habitat at the time 'O f seed dispersal 釘 ec 'O nsistent with a hyp 'O thesis 'O f “miniature ，l 'O w- p'O wer jactitati 'O n". G. G. exilis (l ike m 'O st 'O ther Gas 住'O diinae) gr 'O ws under sheltered c'O nditi 'O ns 'O n the f 'O rest fl 'O'O r. C 'O nsequently ，wind is n'O ta prevailing phen 'O men 'O n，and even when a breath 'O f air c'O mes ar 'O und ，its vel 'O city is usually very m 'O des t. Th is must be a problem f'O ra small ， wind-dispersed wind-dispersed herb as G. exilis. H 'O wever ， by markedly el 'O ngating the pedicels after fl 'O wering (Fig. 3) ，血e plant “sets sail" by maximizing the exp 'O sure 'O f its distal p制 t'O the wind. wind. Due t 'O the delicate ，flexible nature 'O f the peduncle and pedicels ， this w i1l， 'O n a m 泊 iaωre and l'O w-p 'O wer scale ， bring ab 'O ut the same “jactitati 'O n" as described by RIDLEY (1 930) f'O r large ， rigid herbs fr 'O m windy habitats (加 e町ect 出 at c'O uld n'O t have been achieved achieved t'O出 e same extent by el 'O ngati 'O n 'O f 血 e peduncle). Naturally ， the limited elasticity 'O f the delicate peduncle and pedicels d'O es n'O t all 'O w the seeds t 'O be thr 'O wn f'O ra l 'O ng distance ， but the pr 'O cess sh 'O uld be seen 泊 c'O herence with the tiny ，ball 'O'O n-like seeds 白紙 (unlike (unlike the the large ， heavy seeds 'O f the herbs ab 'O ve) 訂 'e perfectly adapted t 'O wind- 24 H 凹 RIK A. PEDERSEN ，SANTI WATTHANA ， SOMRAN SUDDEE ， AND SAWITREE SASIRAT

dispersal dispersal once they have been ejected from the capsule. It should als 'O be remembered that the the height 'O f the p'O int 合'O m where the seeds are released is increased by the el 'O ngated pedicels. pedicels. It It is 'O bvi 'O us 由at 'O ur hyp 'O thesis 'O f “miniature ，l'O w-p 'O wer jactitati 'O n" sh 'O uld be tested experimentally. experimentally. At 白e same time it should be checked if the physical in f1 uence 'O f individual rain rain drops fa Ii ing on dehisced capsules 'O r their pedicels can bring ab 'O ut ejecti 'O n 'O f seeds. In deed ，we suspect 血at increased exp 'O sure of the capsules t 'O rain is an additi 'O nal adaptive feature feature 'O f the el 'O ngated pedicels-if they were n'O t pr 'O l'O nged ， the l'O wer capsules would be placed in rain shelter below the upperm 'O st 'O nes (and the elasticity 'O f the sh 'O rt pedicels w 'O uld be negligible).

ACKNOWLEDGMENTS

We 訂 'e indebted t 'O DANIDA f'O r supp 'O rting the field w 'O rk financially and Nar 'O ng

K 'O'O nkhunth 'O d 佃 d Panna Sanguangsak f'O r assistance during the field w 'O rk. In additi 'O n， we w 'O uld like t 'O express 'O ur grateful th 創Ik: st 'O C. Sathish Kumar and Paul Ormerod f'O r help help with literature ，R 'O jana Luangpai f'O r access t 'O the scanning electr 'O n micr 'O sc 'O pe at Mae J 'O University ，Lene K 'O lind Sk 'O ugaard f'O r technical assistance with illustrati 'O ns ，and tw 'O an 'O nym 'O us reviewers f'O r useful c'O mments 'O n 血e manuscrip t.

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