Phenology, Sexual Expression, and Reproductive Success of the Rare Neotropical Palm Geonoma Epetiolata1

BlOTROPlCA 33(4): 596-605 2001

Phenology, Sexual Expression, and Reproductive Success of the Rare Neotropical Palm Geonoma epetiolata’

Silvana Marten2 Escuela de Biologia, Universidad de Costa Rica, San Jose, Costa Rica and Mauricio Quesada3 Departamentode Ecologia de 10s Recursos Naturales, lnstituto de Ecologia, Universidad Aut6noma de Mexico, Apartado Postal 27-3 (Xangari), Morelia, Michoacan 58089, Mexico

ABSTRACT We studied the phenology and reproductive biology of the stained glass palm Geonoma epetiolata in a premontane rain forest of Costa Rica. This understory species is endemic to Costa Rica and Panama. We followed 102 plants for two years and found that G. epetiolata is monoecious and protandrous. Flowering duration at the inflorescence level is three to six months for the male phase and two to three weeks for the female phase; this is one the most extended flowering periods reported for palms. Flowering in this palm is continuous throughout the year, both at the individual and population level. This long and continuous flowering pattern may represent an adaptation to increase the chances of reproduction in a environment of high and unpredictable rainfall. The species is self-compatible, hut self-pollination is possible only when there is overlap of male and female inflorescences (38% of the cases). Only 28 percent of the stigmas of 1020 flowers received pollen grains and 20 percent developed pollen tubes in the styles. Of all the flowers produced by an inflorescence, I4 percent initiated fruit development but only 3 percent develop into mature fruits. Seventy-six percent of the initiated fruits were aborted.

RESUMEN Estudiamos la fenologia y la biologia reproductiva de la palma Geonoma epetiolata en un bosque hlimedo del pre- montano en Costa Rica. Esta palma de sotobosque es endtmica de Costa Rica y Panami. Durante dos arios observamos 102 plantas marcadas y encontramos que G. epetiolata es monoica y protindrica. La duraci6n de floraci6n a nivel de inflorescencia es de tres a seis meses para la fase masculina y de dos a tres semanas para la fase femenina, este es el periodo de floraci6n mis prolongado que se ha reportado para cualquier especie de palma. La floracibn de esta palma es continua a travts del afio, tanto a nivel individual como poblacional. Esre patr6n de floraci6n largo y continuo parece representar una adaptacibn para aumentar las posibilidades de reproducci6n en un ambiente de precipitacion aka e impredecible. La especie es auto-compatible pero la autopolinizaci6n solo es posible cuando existe traslape de flores femeninas y masculinas dentro de un mismo individuo (38% de 10s casos). Unicamente el 28 por cienro de 10s esrigmas de 1020 Bores analizadas recibieron granos de polen y 20 por ciento desarrollaron tubos polinicos en 10s estilos. De codas las flores producidas por una inflorescencia, en promedio 14 por ciento inician el desarrollo de frutos pero solo el 3 por ciento de las flores llega a producir frutos maduros. El 76 por ciento de 10s frutos iniciados se abortan.

Kq, word: bet-hedging dichogamy; fiuit abortion; Geonoma epetiolata; monoecy; palm phenology; polLen limitation.

PALMS ARE ONE OF THE MOST ABUNDANT AND DIVERSE mans as materials for construction, ornamental groups of plants in Neotropical rain forests and plants, and food products (Balick 1984, Rich represent important food resources for many spe- 1987, Bernal 1992, Lescure etal. 1992, May 1992, cies of animals (De Steven et al. 1987, Foster 1990, Pedersen & Balslev 1992, Joyal 1994, Durin Foster & Hubbell 1990, Hammel 1990, Prance 1995). Despite the ecological and economic im- 1990, Kahn & de Granville 1992, Clark et a/. portance of palms, the population biology of most 1995, Scariot 1999). Palms are also used by hu- species is still unknown (Scariot et al. 1995). The least studied palms are the habitat special- ists and the species with restricted geographic rang- ’ Received 15 August 2000; revision accepted 30 April es. These species are the most vulnerable to extinc- 2001. E-mail: [email protected]. tion due to the rapid deforestation obliterating Corresponding author. E-mail: mquesada@ibiologia. Neotropical rain forests (Bawa & Ashton 1991, unammx Duran 1995, Whitmore 1997). Therefore, to pre-

596 Reproductive Biology of Palms 597 serve and manage these rare species of palms, it is leaves are reddish and have conspicuous purple essential to understand the factors that influence spots. This feature makes this palm potentially the reproduction and viability of their populations valuable as an ornamental. Seeds have been har- (Bawa & Krugman 1991, Ratsirarson & Silander vested on a small scale to develop commercial nurs- 1996). eries. Aspects related to the timing, frequency, and Geonoma epetiolata is monoecious and protan- synchrony of flowering are directly related to the drous with interfoliar, spicate inflorescences (50 crn breeding success of plant populations (Rathcke & in length) that produce staminate and pistillate Lacey 1985, Clark & Clark 1987, Marquis 1988). flowers in separate sexual phases. Pistillate flowers Flowering synchrony and intensity have been are dark red and they have a tubular corolla that shown to affect visitation by pollinators, which in measures 4-6 mm in length. Staminate flowers turn determines fruit set (Augspurger 1981, 1983). have a 2 mm corolla and 6 protruding stamens, These aspects of flowering phenology are particu- which have red filaments that are 5-6 mm long, larly important in monoecious plants because tem- and white anthers. Both flower types lack nectar poral differentiation in the expression of unisexual (Marten 1998). Mature fruits are purplish black flowers determines the mating patterns within and and single-seeded. among populations (Bullock 1981). Many Neotropical palms are monoecious, but STUDYsire.-The study was conducted at Rara little is known about the relationship between sex- Avis Private Reserve in Sarapiqui, province of He- ual expression patterns and the reproductive success redia, Costa Rica (10"15'N, 84"05'W) . This re- of rare palms (Henderson 1986, Ratsirarson & Sil- serve is located at 560 to 800 m in elevation and ander 1996). In this study, we examined the rela- borders the Braulio Carrillo National Park. Mean tionships among phenology, sexual expression, and annual rainfall is between 7000 and 8000 mm and reproductive success in Geonoma epetiolata H. E. there is no regular seasonality. The vegetation is Moore, a monoecious palm, found only in a few premontane rain forest (Holdridge 1967). localities of Costa Rica and Panama. To our knowl- edge, this is the first study on the reproductive bi- INFLORESCENCEDEVELOPMENT.-we determined the ology of this rare palm species. The main objectives development of 100 inflorescences on 78 individ- of our study were to: (1) characterize the repro- uals from December 1995 to October 1997. For ductive phenology of G. epetiolata at the inflores- each inflorescence we recorded the longevity of the cence, individual and population level; (2) evaluate following phases: (a) elongation phase: time elapsed the spatial and temporal variation in gender ex- between the emergence of the inflorescence from pression; (3) determine the relationship between the bract to the beginning of flowering; (b, c) sta- pollination success and reproductive output with minate and pistillate phases: times of male and fe- flowering phenology; and (4) ascertain the breeding male flower production, respectively; and (d) fruit system of G. epetiolata. production phase: time elapsed between the end of the pistillate phase and fruit maturation. Fruit de- MATERIALS AND METHODS velopment was further divided into three stages: young, green, and ripe. STUDYswclm.-Geonoma epetiohta is an understo- We also recorded mean daily staminate flower ry palm that is restricted to mature forests on the production per inflorescence and flower longevity Caribbean slopes of Costa Rica and Panama (Hen- for each of 50 individuals that were observed twice derson et al. 1995). In Costa Rica, it is currently a day for four weeks. We estimated the mean num- found on a strip of land located between lowland ber of pistillate flowers produced per day by divid- and premontane rain forest (ca 50 km2) of the ing the total number of flowers in an inflorescence Central Mountain Range (Chazdon 1987); no oth- by the total number of days of the pistillate phase. er populations have been located between this area Receptivity of pistillate flowers was determined by and northern Panama. Much of the habitat where applying 3 percent H202 on stigmas of various G. epetiolata occurred has been lost or fragmented ages (1-20 d; Kearns & Inouye 1993). due to deforestation and the only large protected To determine the floral sex ratio per inflores- area where this species is found is the Braulio Car- cence, we counted the total number of staminate rillo National Park in Costa Rica (Fig. l). and pistillate flowers on 20 inflorescences of dif- Geonoma epetiolata has solitary stems and at- ferent plants. Each inflorescence was covered with tains a maxiinurn height of 2.5 m. The young a mesh net bag and the fallen staminate flowers 598 Marten and Quesada

FIGURE 1. Geographic distribution of Geonomu epetiolatu in Costa Rica. Top right: map of Costa Rica with Braulio Carrillo National Park in the center. Left: Area of Braulio Carrillo National Park where G. epetiolatu is found.

were counted every two weeks throughout the The frequency of flowering, measured as the flowering period. Pistillate flowers were counted di- number of inflorescences produced per year per in- rectly on the inflorescence because they do not fall dividual, was correlated with plant age and size us- until the fruits begin to develop. ing Spearman’s correlation tests. The degree of overlap (measured as the number of times pistillate REPRODUCTIVEPHENOLOGY.-TO study the flower- and staminate inflorescences overlapped within a ing and fruiting phenology of G. epetiolata, we used plant divided by the number of pistillate inflores- 102 reproductive plants and recorded the following cences produced) was also correlated with plant age reproductive parameters in each individual every and size. Plant size was measured as stem length, two weeks from November 1995 through October number of nodes, and number of leaves, which 1997: (1) number of inflorescences in elongation, were measured every six months on each individ- staminate, and pistillate phase; (2) number of sta- ual. The youngest leaf was tagged to determine leaf minate and pistillate flowers per inflorescence; and production rate. Age was estimated by using the (3) number of infructescences and fruits per plant. number of stem nodes, leaf production rate, and The flowering phenology was examined at the pop- seedling growth rate (from a sample of 50 seeds ulation and individual level according to the cri- planted in a greenhouse; Corner 1966). teria of frequency and synchrony described in To examine the effect of flowering time on fruit Newstrom et a/. (1994). production, we tagged each inflorescence initiating Reproductive Biology of Palms 599

TABLE 1 . Characteristics of inflorescence development in Geonoma epetiolata. N = the number of individuals sarnpled.

Inflorescence characteristic 2? SD Range N Duration of elongation stage (d) 140 2 22.4 90-210 78 Duration of staminate phase (d) 121 2 19.8 75-180 78 Duration of the pistillate phase (d) 17 2 2.94 13-28 78 Time from flower production to fruit maturation (mo) 7 t 0.8 5-9 41 Number of staminate flowers produced per day per inflorescence 3 2 0.8 0-20 50 Number of pistillate flowers produced per day per inflorescence 12 5 2.3 1-25 78 the pistillate phase to follow the date of flowering. and cross-pollinations on 94 flowers of 12 individ- We recorded the number of pistillate flowers and uals to test for self-compatibility. We bagged pis- fruit set per inflorescence in 32 1 inflorescences. To- tillate inflorescences prior to anthesis and pollinat- tal and mean monthly rainfall for 1996 and 1997 ed the flowers the following day by rubbing de- were also correlated with the blooming time of fe- hisced anthers onto the stigmas. For cross-pollina- male inflorescences and to their fruit set. tions we used pollen from at least two donors. Pollinated flowers were bagged again to prevent NAIIJRALIiOL.i.INA I ioN.-observations for pollina- contamination. Styles were collected 24 hours after tors were conducted on 11 plants (6 staminate- pollination and treated with the same staining tech- phased and 5 pistillate-phased) on six different days nique described previously. Pollen tubes at the base in January, February, and June 1996. Observations of the styles were counted using a UV microscope. were done between 0730 and 1000 h. Each plant To control fruit production using artificial crosses, was monitored for 1 hour for a total of 11 hours we hand-pollinated an additional sample of flowers of observations. Staminate-phased inflorescences from 6 plants and recorded the number of fruits had 3 or more flowers and pistillate-phased inflo- produced after 30 days. rescences had at least 50 percent of the flowers open. SrA-riAL DISTRIRUTION.-TOdetermine the spatial To determine the pollination success of G. epe- distribution of G. epetiolata, we recorded the num- tiolata under natural conditions, we counted the ber, height, and reproductive status of all individ- number of pollen grains deposited onto stigmas uals found in 20 randomly distributed 50 m tran- and the number of pollen tubes present at the base sects, 3 m at each side of the transect (300 m2/ of the styles of 1020 flowers. We collected 10 flow- transect). The distance of each individual along a ers from 102 plants during 1996, at least two days transect line was recorded and the spatial distri- after flower senescence. Pistils were fixed in 70 per- bution of adult and young individuals estimated cent alcohol, softened in 8 N NaOH for eight (Zar 1996). hours, and stained with a solution of 0.01 percent aniline blue decolorized with 0.01 M K3P04 (Mar- RESULTS tin 1959). Pistils were mounted and observed under a UV microscope. In addition, any visitor to a INFLORESCENCE DEVELOPMENT.-The inflorescence flower of G. epetiolata was collected and checked of G. epetiolata is a single spike that is folded in a for pollen. zigzag pattern and enclosed by one peduncular bract. This bract opens apically and the spike be- FRUITPmDucrioN.-we recorded the total num- gins to elongate. Afier three to seven months, the ber of initiated and ripened fruits on 321 inflores- inflorescence is Fully extended and the staminate cences produced over the course of the study and phase begins. For a period of two to six months, calculated fruit initiation rate and fruit set. These the staminate flowers are produced daily within the were estimated as the number of fruits initiated or same inflorescence (Table 1). Anthesis occurs be- ripened divided by the total number of pistillate tween 0600 and 0800 h and flower abscission oc- flowers produced per inflorescence. We also count- curs at dusk (after 1700 h). There is an interval of ed the number of preyed upon, parasitized, and 1 to 5 days between the staminate and pistillate aborted fruits per inflorescence and the develop- phase when inflorescences do not produce flowers. mental stage at which abortions occurred. Pistillate flowers are produced basipetally, from the tip to the base of the inflorescence. The duration BREEDING susrEM.-We performed a series of self- of the pistillate phase is 17 days on average (Table 600 Marten and Quesada

OSmimcOPhnilLleABdr TABLE 2. Mean number of individuals and flowers of im , Geononia epetiolata in staminate phase (f), phtillate phase (E), and ouerlapping phases (TE), and mean number offlowers of each sex per sampling date. Standard deviations (SO), ranges, and the coe$cient of variation (CV) are included.

Level of cv analvsis 2 t SD Ranee (%) L Planrs r 78 2 4.4 67-87 6 7 ? 2.7 2-13 40 tt+--4 tt+--4 E NO I F MAMJ 1 AS OND 1 f MAMI I AS 0 TE 3 % 1.6 1-8 47 Flowers r 247 t 140 164-340 I6 FIGURE 2. Flowering phenology of Geonoma epetiolata E 422 f 177 170-811 41 from November 1995 to October 1997 in Rara Avis. Tri- angles represent individuals with inflorescences in elon- garion phase (buds); open diamonds indicare individuals in staminate phase; and black circles denore individuals in pistillate phase. On average, only one-third of the inflorescences produced by individual plants developed mature fruits. At the population level, flowering was contin- 1). Flower stigmas are receptive for ca 8 days and uous throughout the year (Fig. 2). Synchrony of turn dark after senescence. Flowers do not abscise flowering, measured as the percentage of individ- until fruits initiate development. The morpholog- uals flowering simultaneously at any time, was be- ical floral sex ratio of individual inflorescences is 2: tween 70 and 95 percent. The number of individ- 1 staminate/pistillate, equivalent to the basic triad uals in the staminate phase throughout the sam- cluster of all geonomoid palms (Uhl & Dransfield pling period (70-92%) significantly exceeded the 1987). number of individuals in the pistillate phase (3- Staminate flower production is asynchronous at 16%; G-test of heterogeneity G = 994.5, P < the inflorescence level. Staminate inflorescences 0.0001; df 36). The floral sex ratio per sampling produce an average of 3 flowers per day and only day was significantly different than the expected five percent of the flowers in an inflorescence are morphological ratio (2r:l E; G = 10269, P < open in one day. In contrast, pistillate inflores- 0.0001, df = 36; Table 2). On most sampling days, cences produce an average of 12 flowers per day. pistillate flowers outnumbered staminate flowers Seventy to 90 percent of the pistillate flowers are (Fig. 3). synchronously open within each inflorescence. The fruiting phenology was continuous at the Fruits initiate development three to five weeks after flowering of the pistillate phase. During the first two months, fruits change from yellow to green. Fruits remain green for three to seven months and turn dark purple at maturity (Table 1).

PRODUCTIVE PHF.Not.OGY.-The flowering phenology of G. epetiolata was continuous at the individual level; 98 percent of the plants produced inflorescences throughout the year for two consec- utive years. Plants produced one to three inflorescences per year. Thirty eight percent of the pistillate inflorescences overlapped with the staminate inflo- Montb rescences within the same plant. Neither plant size FIGURE 3. Number of staminate and pisrillate flowers nor age was related to the degree of sexual overlap. opened each sampling day in a population of Geonoma the individual level, fruit production was epetiokztu in Rara Avis. Dares are December 1995 to ocrober 1997. not continuous in spite of continuous flowering. Reproductive Biology of Palms 601

TABLE 3. Flower and juit production per inj’oresrence of Geonoma epetiolata. A total of 320 infro- rescences jom 102 plants were sampled.

2 t SD Range Number of pistillate flowers 190 5 39.3 75-282 Number of initiared fruits 24 t 17.4 1.3-109 Number of matured fruits 5 t 5.7 0-35 Fruit initiation rate 13 5 6.7 049 Fruit set (Yo) 3 % 4.9 0-29 Abortion rate (%) 76 t 28.5 0-100 DIFHAMIlASONDlFMAMJJAS~ Month FIGURE 4. Fruiring phenology of Geonoma epetiohta (Table 3). Although most abortions (67%) oc- for individuals with young, green, and ripe fruits from curred during the first stages of fruit development, December 1995 to Ocrober 1997 in Rara Avis. the probability of abortion was not different for young or green fruits. A weevil larva attacked the seeds and was responsible for 6 percent of the seeds population level (Fig. 4). Approximately 57 to 80 loss. It is not known if early attacks by weevils were percent of the plants were in fruit throughout the the cause of some of the abortions, year but only 36 percent of the individuals bore Mature fruits remained attached to infructesc- mature fruit. A peak of fruit maturation occurred ences for an average of 54 days (SD = 37.2, N = from May to July 1996 (Fig. 4). 112 infructescences). We did not observe any ani- Flowering time was not correlated with the mals removing the fruits during this study. Instead, number of initiated fruits or to fruit set (Spear- many of the fruits simply fell near the maternal man’s r = -0.11, P = 0.89, N = 247; r = 0.08, plant. P = 0.21, N = 247). Inflorescences that bloomed during peaks of flowering did not bear more fruits BREEDINGsusrEM.-Neither the number of out than other inflorescences. Total monthly rainfall crossed (77%) and self-pollinated (82%) flowers was not correlated with the flowering phenology (r containing pollen tubes 24 hours after hand-polli- = 0.28, P = 0.1, N = 36) or to the time of fruit nation (x2 = 1.32, P > 0.25) nor the number of maturation (r = -0.22; P = 0.2 ; N = 36). out crossed (76%) and selfed (61%) flowers that initiated fruit was different (x2 = 0.44, P > 0.50). NATURALPOl.I.INATION AND FRUIT PRODUCTION.- These results demonstrated that the studied pop- During 11 hours of observations, only one visitor ulation was self-compatible at the pre-zygotic level. (a weevil) was recorded on a pistillate inflorescence. A few other insect species were observed visiting SPATIAI. DlSTRlBUTlON.-The spatial distribution Of the inflorescences of G. epetiolata during our field- the overall population (coefficient of dispersion I work: one stingless bee ( Trigona filviventris) on a = 3.36, x2 = 171.4, gl = 50) and young individ- staminate inflorescence, weevils (Curculionidae) uals (I= 3.05, x2 = 122, gl = 10) was aggregated. observed on pistillate inflorescences, drosophilid The spatial distribution of the adult individuals flies on staminate inflorescences, and ants on pis- considered alone was random (I = 0.86, x2 = 8.6, tillate inflorescences. Visitors to flowers were rare gl = 40). and the insects mentioned may be only a partial list of the possible pollinators of this palm. No nec- DISCUSSION tar production was recorded although the pistillate flowers produced an exudate that ants collected. Monoecism has been considered as a reproductive Of the 1020 flowers observed to determine pol- system that evolved to reduce self-fertilization be- lination success, only 28 percent had pollen grains cause it enhances the spatial separation of male and on the stigmas and 20 percent had pollen tubes at female functions (Bawa et al. 1982). In the palm the base of styles. On average, 13 percent of the subfamily Arecoideae, most species are monoecious flowers produced by an inflorescence initiated fruit and dichogamous (pistillate and staminate phases and only 3 percent developed to maturity. Fruit within inflorescences are temporally separated). abortion occurred at any time during development Overlap of staminate and pistillate phases in inflo- and accounted for 75 percent of the initiated fruits rescences within plants is rare or nonexistent 602 Marten and Quesada

(Schmid 1970; Olesen & Balslev 1990; Listabarth palms. This unusual reproductive strategy may in- 1993, 1994; Cunningham 1995; Ratsirarson & Sil- crease the probability of pollination in an environ- ander 1996; Borchsenius 1997; Ervik & Feil 1997), ment of high and unpredictable rainfall in which and many species of this subfamily have been con- the weather may limit the activity of flower visitors sidered obligate outcrossers. As described for other and make pollinator service unreliable. Moreover, members of the subfamily, G. epetiokzta is mon- strong and frequent rains may result in pollen loss- oecious and protandrous; however, inflorescences es as rainwater washes off the pollen of the anthers. in staminate and pistillate phase ofcen co-occur Hence, extended low-intensity flowering may have within the same plant (38% of the cases). The re- been selected to spread the risk of misspending result is a mixed mating system; self-fertilization via productive effort during adverse weather conditions geitonogamy is likely to occur when two inflores- (Bawa 1983, Rathcke & Lacey 1985). cences in different sexual phases overlap because G. The phenological pattern displayed by G. epe- epetiokzta is self-compatible. tiokzta in which individuals have low-intensity This mixed reproductive strategy is a result of flowering spread out over a long period of time, the particular flowering phenology of G. epetiokzta, has been referred to as “steady-state flowering” which has continuous production of inflorescences (Frankie et al. 1974, Gentry 1974, Augspurger and extended flowering at the individual level. This 1983). This term has been used to describe the phenological pattern is uncommon in palms, which flowering of certain hermaphroditic plants that are are in most cases seasonal in their production of associated with pollination by large bees and tra- flowers and fruits (De Steven etal. 1987, Sist 1989; pliner hummingbirds. In G. epetiolata, however, the .f: Borschenius 1997, Henderson et al. 2000). small unisexual flowers are not likely to be polli- Continuous flowering occurs in some species of nated by large trapliner insects or birds. The rare palms, but only at the population level and seldom visitors to the flowers included small bees, weevils, within individuals (Anderson et al. 1988, Voeks and flies; but whether or not they play a role in 1988, Ratsirarson & Silander 1996, Henderson et the pollination of G. epetiokzta is still unknown. al. 2000). For example, Henderson et al. (2000) Rainy weather and low-frequency flower visi- conducted a phenological study of a palm com- tation by insects make synchronous flowering an munity in Manaus, Brazil, and found that four spe- important element in the reproduction of G. epe- cies of Geonoma had flowering periods that ranged tiolata. Flowering synchrony at the population level between 6 and 12 months at the population level; is determined by the proportion of individuals in however, none of those palm species exceeded 4 the staminate phase that flower simultaneously (not months of flowering at the individual level. Several by the starting time of flowering). Individuals in tropical understory plants show extended or con- the pistillate phase are found in small numbers tinuous flowering in nonseasonal wet environments throughout the year, whereas plants in the stami- (Frankie et al. 1974, Croat 1975). Blooming over nate phase always exceeded 60 percent of individ- an extended period of time may be associated with uals in the population (due to the staggered flow- a lack of seasonal differences in the availability of ering of inflorescences). As a result, there were on pollinators or resources (Ackerman 1989). It could average eight potential pollen donors for every in- also be a strategy to accumulate resources for fruit dividual in the pistillate phase. This flowering pat- maturation in places where these are temporally tern should be advantageous for the female func- variable or sparse (Rathcke & Lacey 1985). Geon- tion of individuals because it increases the diversity oma epetiokzta occurs in a region with high and of matings (Newstrom et al. 1994). constant rain throughout the year; this could pro- In contrast to the proportion of pistillate- and mote continuous and extended flowering in this staminate-phased individuals in the population, the species. floral sex ratio showed a different trend. The av- Environmental conditions may also influence erage number of pistillate flowers at anthesis on flowering intensity and duration at the inflores- most sampling days exceeded the number of sta- cence level in G. epetiokzta. Individual inflorescenc- minate flowers by a factor of two to six. Since pis- es produce flowers for up to 200 days, which is tillate flowers remained viable for 8 days and the more than twice the longest flowering periods re- opening of these flowers occurred within 17 days, ported for any other palm species (Borchsenius pistillate inflorescences had many flowers in anthe- 1993, 1997; Ratsirarson & Silander 1996). Fur- sis at the same time. In addition, staminate-phased thermore, daily staminate flower production in G. inflorescences showed low-intensity flowering but epetiokzta is one of the lowest ever recorded for it was staggered over several months (Table 1). Reproductive Biology of Palms 603

Thus, at any given time, there were relatively high at the base of the styles. Because ovaries of G. epe- numbers of staminate inflorescences with few flow- tiolata have one ovule per ovary, only the pistils ers and a few pistillate-phased inflorescences with with two or more pollen tubes at the base of style many flowers. The distribution of few staminate were likely to produce a mature fruit. Evidence flowers scattered in numerous plants forced polli- from the literature indicates that the number of nators to visit many individuals in order to gain microgametophytes in the pistil usually has to ex- reward. We assume that pollen is the main reward, ceed the number of ovules for fruit set to occur because staminate and pistillate flowers apparently (Bertin 1982, 1988; Casper 1983; Lee 1988; Que- lack nectar. Pollination of pistillate flowers could sada et al. 1993, in press; Niesenbaum & Casper occur by mistake as the insects are searching for 1994; Stephenson et al. 1995). pollen. Pollination by mistake has been document- Fruit abortion also decreased fruit set in G. epe- ed in several monoecious, dioecious, and dichoga- tiolata, more than 70 percent of the initiated fruits mous species in which pistillate or female flowers aborted during development. Environmental con- resemble staminate or male-phase flowers in mor- ditions such as low light availability in the under- phology (Baker 1976, Bawa 1980, Montalvo & story have been related to fruit abortion (Stephen- Ackerman 1986, Dukas 1987, kren & Schemske son 1981, Lee 1988, Cunningham 1995); however, 1991) or in odor (Armstrong 1997). In G. epetiol- the causes of fruit abortion in G. epetiolata still ata, pistillate- and staminate-phased spikes are the need to be determined. same color but pistillate and staminate flowers dif- In addition to limited pollination and high fer in color and morphology. Pollination by mis- fruit abortion rates, fruit removal was rare. Fruits take has rarely been described in palms (Olesen & of G. epetiokzta remained attached to the maternal Balslev 1990) and further research is needed to de- plants for several months and most of them termine if this type of pollination occurs in G. epe- dropped easily near maternal plants. Thus, this pat- tiolata. tern of fruit dispersal explains the aggregate spatial Geonoma epetiolata presented low pollination distribution of young plants. and fruit-set rates; more than 70 percent of the In conclusion, our study showed that G. epe- flowers did not receive pollen. The average fruit tiolata is a species with an unusual reproductive initiation rate per inflorescence was 13 percent and behavior. An extended and slow inflorescence de- only 3 percent of the flowers developed into mature velopment combined with a low intensity flowering fruit. This value is below the mean fruit set re- led to infrequent pollinator visitation and low fruit ported for other monoecious species (Sutherland & production. This pattern of flowering can be con- Delf 1984, Cunningham 1996, Ratsirarson & Sil- sidered an example of a “bet-hedging’’ strategy that ander 1996). The low reproductive output of G. increases the probabilities of mating in unpredict- epetiokzta is a critical issue for the conservation of able environments (Stearns 1976, Bawa 1983). the species, especially when considering that this palm has solitary stems. Unlike other species of Geonoma which have clustered stems (Henderson ACKNOWLEDGMENTS et al. 1995), G. epetiolata is not capable of any We want to express our gratitude to Geovanny Camacho other form of asexual reproduction. for field assistance: Frank Joyce, Christian Listabarth, and Our results indicated that low amounts of mi- an anonymous reviewer for valuable comments on this crogametophytes per pistil and high fruit abortion manuscript; Eduardo Rodriguez for designing the loca- tion map; and Amos Bien and Rara Avis S. A. for pro- rates were important limiting factors that influ- viding lodging and logistical support at the field site. Lab- enced fruit production in G. epetiolata. Only 11 oratory facilities were provided by the La Selva Biological percent of the pistils had two or more pollen tubes Station.

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