Selbyana 29(1): 87-91. 2008. POLLINATION OF THE ORNAMENTAL ORCHID ONCIDIUM SPHACELATUM By THE NATURALIZED OIL-COLLECTING BEE (CENTRIS NITIDA) IN FLORIDA ROBERT W. PEMBERTON Fairchild Tropical Garden, Coral Gables, FL Correspondence address: Invasive Plant Research Laboratory, USDA-Agricultural Research Service, 3225 College Ave., Ft. Lauderdale, FL 33314 Email: [email protected] ABSTRACT. The recently naturalized oil-collecting bee Centris nitida pollinates the cultivated Oncidium sphacelatum in southern Florida. Female C. nitida bees seeking food are the pollinators of this food deceit orchid, which appears to mimic species of Malpighiaceae, which have oil rewards collected by the bee. The fruit set rate ranged from 0.54% to 3.0% and averaged 1.49%, which is many times higher than the 0.0% and 0.25% reported for this orchid in its native Mexico. The many capsules produced (66 fruits in the three large exposed plants in this study) contain many millions of seed. The large number of seeds produced could promote the naturalization of O. sphacelatum in Florida if suitable mycorrhizae are present. Centris nitida and o. sphacelatum are broadly sympatric in tropical America and may interact in their native area. Centris nitida and Euglossa viridissima (an orchid bee which has also recently naturalized in southern Florida) are participants in pollination webs involving many plants including native, ornamental, naturalized, and invasive plants. Key words: bee, deception orchid, naturalized, pollination, rewardless flowers Oncidium sphacelatum LindL is a popular or bee, and then removed pollinia from several namental orchid that is frequently cultivated out flowers from the O. sphaceLatum plants for com of-doors in southern Florida. Known as one of parison, and found the pollinia from the flowers the dancing doll orchids, it is native to Mexico, to be identical in size and shape to the pollinar to Costa Rica, and Venezuela (Pridgeon 1994). ium borne by the bee (FIGURE i). In addition, all Its bright yellow flowers, barred with brown three O. sphacelatum plants bore mature fruits markings, are nectarless and have little fragrance from the previous year's flowering, suggesting to the human nose. Solitary oil-collecting bees that pollination was occurring in the plants. in the genera Centris and Tetrapedia, and sting The presence of the pollinarium on the face less bees Trigona (Apidae) are reported to be of C. nitida strongly suggested that the bee is a pollinators of Oncidium species (van der Cingel pollinator of the piant. A small study was un 2001, Alcantara et aL 2006). Oncidium sphace dertaken to examine the interactions of C. nitida latum was recently reported to be pollinated by and 0. sphacelatum, which broadly co-occur in Centris bees in Mexico (Damon & Cruz-Lopez tropical America. I manipulated flowers to learn 2006). about the breeding system of the plant in order On March 8, 2007 at about 12:30 pm, I cap to better interpret the bee-flower interaction. I also determined which of the several previously tured a Centris nitida Smith in a Ft. Lauderdale, described Centris-Oncidium pollination syn Florida garden with an orchid pollinarium on its dromes (van der Cingel 2001) was involved with face. The captured bee was a female gathering the C. nitida-O. sphacelatum interaction. the edible oil reward from the flowers of the native Florida shrub Brysonima Lucida (MilL) DC. (Malpighiaceae), which was planted in the METHODS residential garden. The bee with the pollinarium was captured as part of an effort to obtain spec Brief timed watches were made of two plants imens of C. nitida, which I had discovered to be in an attempt to observe C. nitida visitation of a recently naturalized bee in southern Florida O. sphacelatum flowers on the two large bloom and native to the Neotropics (Pemberton & Liu ing plants in large baskets in the Ft. Lauderdale 2008). The pollinarium appeared to be from an residential yard. Observations of exposed pollin Oncidium species; three large baskets of flow ia and pollinia falling onto or near the stigmas ering O. sphacelatum plants were in the same of some flowers suggested that self pollination garden, about 15 meters from the shrub where may occur. Potential apomixis and self pollina the bee was captured. I made a specimen of the tion were examined in these plants by bagging 87 88 SELBYANA Volume 29(1) 2008 flower to flower briefly touching the lips, and landing On only a few. No pollinia removal was observed. Precise observation was difficult be cause of the bees' rapid movement and many large inflorescences with abundant flowers on two plants. A single honey bee also visited dur ing the April I watch, but did not remove the pollinia. On April 5 at 12:54 pm, one female C. nitida was observed to visit five flowers on two plants and removed a pollinarium from a flower before being captured. The pollinarium was placed in the middle of her face in the same manner as the O. sphacelatum pollinarium on the other bee captured on B. ludida flowers on March 8. FIGURE 1. Female of the naturalized oil-collecting Of 10 tagged flowers with intact anther caps, bee (Centris nitida) bearing a pollinarium of the or six lost their caps after two days and two self namental orchi d (Oncidium sphacelatum) on her face. pollinia were found on or near the stigmas of the flowers that produced them. Two anther caps from these flowers were found on the stigmas. Of the 10 tagged flowers with missing anther eight inflorescences and three additional inflo caps but with erect pollinaria, four of the falling rescence tips prior to flower opening and main pollinia were missing and another leaning down taining the bags until the flowering finished. I ward near the stigma two days later. None of also tagged 10 flowers with intact anther caps these flowers set fruit. The assessment of flow and 10 flowers without anther caps to detect ering inflorescences for male success found 32 changes in anther caps and the exposed pollinia. of 213 (15%) anther caps missing from flowers Supplementing these treatments was the main on the two inflorescences evaluated on April 22. tenance of a single plant with seven inflores The June 2 evaluation found that neither of the cences in an insect proof screen house during its two older inflorescences (which had no buds and entire bloom. some aging flowers) had any anther caps re Male reproductive function was assessed by maining in the 37 flowers, while the five youn counting the number of flowers without anther caps (missing anther caps implying pollinaria re ger inflorescences, (which had some unopened moval by pollinators) in two inflorescences, one flower buds), had 10 of 40 (25%) of flowers with from each plant on April 22, and seven inflores missing anther caps. Because the anther cap and cences (two old, and five young) on second pollinia loss due to flower aging could not be flowering pulse on one of the plants on June 2. distinguished from removal by C. nitida, male Female reproductive success was assessed on reproduction (pollinia removal rates) could not May 26 and 31 at the end of the flowering period be confidently assessed. for two of the plants and near the end for the No fruit formation was seen in any of the 11 third plant, when all old inflorescences were cut bagged inflorescences, nor on any of the seven from the plants. The persistent bracts that sub inflorescences on the plant held inside the screen tend individual flowers were counted to obtain enclosure, indicating that the plants were not the total number of flowers borne on each inflo apomictic or self pollinating. rescence, along with the number of fruit form The end of the bloom reproductive assessment ing, so that the percent of pollination success of the three large plants indicated that they had could be calculated per inflorescence and plant. produced 13, 26 and 57 inflorescences and a to tal of 876, 1241, and 5160 flowers, respectively, and a mean of 2425 flowers per plant. The three RESULTS plants produced 12, 26 and 28 capsules and a Flowers on two large plants were watched at mean of 22 per plant, and a mean of almost one mid-day on March 12 (1:35-3:00 pm), April 1 capsule per inflorescence (0.927, SD = 0.438). (1:30-2:30 pm), and April 5 (12:34-1:21 pm A total of 66 capsules were produced overall by and 2:24-2:34 pm) for a total of 205 minutes. the 7,277 flowers, yielding effective pollination On March 12 the only visitors to appear were rates ranging from one half of a percent (0.54%) two Euglossa viridissima which hovered briefly to a high of almost three percent (2.97%), and a before flowers. During the April 1 watch, six C. mean fruit set for the three plants of almost one nitida visited at least 23 flowers, mostly moving and half percent (1.49%, SD = 0.0129). PEMBERTON: POLLINATION OF ONCIDIUM SPHACELATUM 89 DISCUSSION have true reward flowers, offering oil rewards (Whitten et al. 2000), but the majority employ The anther caps appear to be routinely shed oil deceit flowers in which the lip calli suggest as the flowers age, resulting in their absence in the presence of oil. These Oncidium are thought most old flowers. Fallen pollinia were frequently to mimic the oil reward flowers of the many spe found on or near stigmas and also appear to be cies of Malpighiaceae, which can have similar part of the aging process in the flowers. The ultraviolet light patterns on their flowers (Nie complete absence of fruit in the bagged inflo renberg 1972). A recent study (Reis et al. 2007) rescences and in the plant held in the screen has shown that the oil chemistry of the oil re house demonstrated that neither self pollination wards of Oncidium species is similar to those of nor apomixis was occurring. If either had oc Brysonima spp. (Malpighiaceae) and that bees curred, some fruit should have been produced not only collect oils from both plants, but chem by the enclosed inflorescences because the fruit ically modify the oils for use in their brood pro production rate (almost one per inflorescence in visions. the exposed plants) should have been detectible. Oncidium sphacelatum appears to be a re Self pollination is known in some Oncidium spe wardless mimic of Malpighiaceae oil reward cies and occurs because the stipe of the pollinia models which exploits C. nitida's oil collecting which is standing erect initially grows outward behavior. Byrsonima lucida is a novel model en and then downward until the pollinia contact the countered by C. nitida in its invasive range. This stigmatic surface (van der Pijl & Dodson 1969). native Florida shrub is the principal oil resource Oncidium sphacelatum has been reported to be whose flowers are continually foraged during self incompatible (East 1940), which makes self their entire blooming period by female C. nitida. pollination impossible. The flowering periods of both plants overlap en The only observed visitors other than C. ni abling the association to be reinforced on a daily tida was a single honey bee which did not re basis. It is interesting to note that no fruit were move a pollinarium from the single flower it vis observed on the O. sphacelatum plants prior to ited, and two Euglossa viridissima which ex 2006 after a single flowering B. lucida was amined but did not enter flowers. Euglossine planted in the yard. As soon as this B. lucida bees are not known to be associated with On shrub flowered, C. nitida appeared and began to cidium orchids, and the rewardless flowers regularly collect oil from the flowers. Fruit set would be of little interest to honey bees. South in mimetic orchids can increase when its model ern Florida's native C. errans Smith is a poten is more abundant (Anderson et al. 2005). Centris tial visitor of O. sphacelatum. A single female nitida also collects oils from ornamental species C. errans was observed collecting oil from B. of Malpighiaceae in southern Florida including lucida at the Ft. Lauderdale study site, north of Malphighia spp. and Galphimia gracilis Bartl., where it has been previously recorded (Pember as well as Angelonia angustifolia Benth. (Scro ton & Liu 2008). Trigona and Tetrapedia spe phulariaceae) . cies, the other known pollinators of Oncidium The degree of visitation and fruit set observed species, are tropical American bees not known to in the pollination of the ornamental O. sphace occur in Florida (http://www.discoverlife.org). latum plants by the naturalized C. nitida in Flor Direct observation of C. nitida removing a pol ida is higher than seen in the recently reported linarium from an O. sphacelatum flower, and the pollination study of O. sphacelatum at two Chia capture of a C. nitida carrying an O. sphacela pas, Mexico sites by different Centris species tum pollinarium indicate that this naturalized bee (Damon & Cruz-Lopez 2007). Three candidate is pollinating this ornamental orchid in Florida. bee pollinators of this orchid in the Mexican An insect carrying a pollinarium is very likely study were observed. Centris trigonoides Lepe to be a pollinator of the species that produced lier was seen to visit and continually hover be the pollinarium (Dressler 1976). The large num fore and occasionally "lunge" at the flowers at bers of fruit being produced on the observed one site, exhibiting what was probably male ter plants and the apparent absence of other polli ritorial behavior. An unidentified bee was also nators also support this finding. observed to attack the flowers at both sites. Nei Among the Centris-Oncidium visitation syn ther bee was observed to remove or deposit pol dromes reported are male bees that attack and linia, but there was a modest level of fruit set pollinate flowers as part of its territorial defense (0.25%) in the 14 inflorescences at the other site, (van der Cingel 2001), and female bees search but none at the other site which had eight inflo ing for food. Both of the observed o. sphace rescences. Another Centris, C. mexicana Smith, latum pollinia-carrying C. nitida bees in this was observed to make brief, once-a-day visits to study were females that were seeking food when a few flowers at the site with eight inflorescenc they visited the flowers. A few Oncidium species es. This bee flew directly to the center of flowers 90 SELBYANA Volume 29(1) 2008 much as C. nitida can do in Florida. No polli Chase, all of which are rare (Wunderlin & Han naria removal or deposition was observed, but sen 2003). The bee could pollinate and increase C. mexicana was collected from an orchid gar fruit production in these plants and aid their res den in another Chiapas location with an O. spha toration. Centris nitida could also interact with celatwn pollinarium attached to its face, dem southern Florida's native C. errans Fox and in onstrating that it can be a pollinator of this or fluence its performance as a pollinator (Pember chid. It appears that O. sphacelatum attracts a ton & Liu 2008). range of Centris species, which are either fe Centris nitida is the second solitary bee to males seeking food or males defending their ter recently naturalize in southern Florida. Another ritories. Because both C. nitida and O. sphace Mesoamerican bee, Euglossa viridissima Friese, latum are native to Mexico and Central America, was detected in 2003 and has become locally this bee, along with other Centris species, could abundant (Skov & Wiley 2005, Pemberton & be part of the same pollination web with O. Wheeler 2006). Florida has none of the male sphacelatum and perhaps other Oncidium spe orchid bee's perfume orchid mutualists, but fe cies. males of this orchid bee are pollinating the or Other studies of Oncidium species have also namental orchid Guarianthe skinneri (Bateman) reported low fruit set. Fruits are rarely observed Dressler and W.E. Higgins (Pemberton 2007b). in the field for O. hookeri Rolfe and other Bra Euglossa viridissima also has the potential to in zilian Oncidium species (Alcantara et al. 2006). teract with other orchids (Pemberton 2007a). Tremblay et al. (2005) summarized the fruit set The orchid bee is pollinating the newly natural rates for three other Oncidium species as 1.8%, ized resin-reward flower, Dalechampia scandens 2.0% and 4.9%, many times higher than that re L. (Euphorbiaceae) (Pemberton & Liu in press corded in O. sphacelatum in Mexico (0.0% and [aJ), as well as other selected native, ornamental 0.25%), but not so different from the 1.49% and naturalized plants (Pemberton & Wheeler mean fruit set I recorded in Florida. Deception 2006). Centris nitida is interacting with Cyrto orchids can have quite low visitation rates (Nei podium orchids in southern Florida (Liu & Pem land & Wilcock 1998, Tremblay et al. 2005). berton in press [bD. Both of these bee species Dodson reported sitting for days in Ecuador ob and most of these plants are from tropical Amer serving a flowering Oncidium planilabre Lind!. ica. Subtropical Florida has had many tropical and saw little except for a single brief visit by American plants as pre-Colombian colonizers, a single Centris bee which pollinated many more recent invaders, and ornamentals. Now flowers (Dodson 1962). highly specialized solitary bees have arrived The number of capsules produced on the three from tropical America to establish, or probably Florida O. sphacelatum plants was large (66). re-establish pollination mutualisms with these The number of seed produced in the capsules of plants. Although these interactions make our O. sphacelatum is unknown, but probably num gardens and parks much more interesting and bers more than a million per capsule. Such a could promote fruit production of some rare na large amount of seed production in an ornamen tive plants, they threaten to increase the number tal plant increases the chances of its naturaliza of plant naturalizations and invasions, as well as tion. One third of Florida's flora is comprised of the complexity and severity of invasive species non-native species (calculated from Wunderlin problems. & Hansen 2003), but few orchids have natural ized. The need for mycorrhizae and specialist ACKNOWLEDGEMENTS pollinators probably limits their naturalization (Daehler 1998). Whether or not appropriate my I thank Hong Liu for statistical assistance and corrhizae are present for O. sphacelatum will de a helpful review the manuscript. Paul Skelley termine whether or not the species naturalizes in kindly took the photograph of Centris nitida southern Florida, because it now has a specialist with the Florida Division of Plant Industry'S pollinator and appears well-suited to the normal photomontage system. weather conditions. However, this epiphytic spe cies may not be able to survive the periodic hard LITERATURE CITED freezes, although some native epiphytic orchids, such as Encyclia tamp ense (Lindl.) Small, ap Alcantara, S., J. Semir, and Y.N. Solferini. 2006. Low parently do. genetic structure in an epiphytic Orchidaceae (On cidium hookeri) in the Atlantic rainforest of south Centris nitida might interact with other On eastern Brazil. 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