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Fruit set, nectar reward, and rarity in the Orchidaceae ¹

¹ Department of Plant and Soil Science, University of Aberdeen, Cruickshank Building, St. Machar Drive,Aberdeen AB24 3UU, Scotland, UK

Received for publication September 17, 1996. Accepted for publication March 10, 1998.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
A review of comparative levels of reproductive success among nectariferous and nectarless orchids worldwide was compiled from a comprehensive survey of fruit set from 117 orchid species in the literature and from our own field studies. It confirms the hypothesis that nectariferous orchids are more successful in setting fruit than are nectarless species. Overall fruit set figures for nectarless and nectariferous orchids were 19.5 and 49.3% for North America, 27.7 and 63.1% for Europe, 41.4 and 74.4% for the temperate southern hemisphere, and 11.5 and 24.9% for the tropics, demonstrating that the dichotomy is consistent across all geographical areas. On average, the provision of nectar doubles the probability of fruit set in both temperate and tropical areas, but tropical orchids are remarkable in that all (whether nectarless or nectariferous, or terrestrial or epiphytic) display low fruit productivity (<50%). Fruiting failure in the tropics may be balanced by higher productivity per capsule, since tropical orchid fruits contain on average 150 times more seeds than temperate ones. Hybridization occurs more frequently among nectarless orchids in Britain and Europe than among nectariferous ones, and there is a significant positive association between orchid rarity and lack of nectar reward in the British Isles. Sexual reproduction in the Orchidaceae is predominantly pollinator dependent, but this can sometimes be successfully circumvented by asexual seed production (agamospermy) or, more frequently, by automatic self-pollination (autogamy). The proportion of highly successful nectarless orchids from all geographic areas is very low and comparable with that of orchids offering rewards other than nectar (~14% of species in each case) emphasizing that high reproductive success is only associated with nectar reward (53% of species). It is suggested that the evolution of nectar production within the family has been the most frequent means of escaping the reproductive limitations of low pollinator visitation frequencies.

Key Words: deceit pollination • hybridization • nectar • Orchidaceae • rarity • reproductive success • temperate orchids • tropical orchids

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The orchid fruit is a capsule containing abundant dust-like seeds. Since agamospermy (asexual seed production) is rare in the family (Nygren, 1967 ; Catling and Catling, 1991 ), the presence of a fruit is almost always an indication of successful pollination (Neiland and Wilcock, 1995 ). Following pollination, embryogenesis and capsule ripening may take from several weeks to many months depending on the species involved (Veyret, 1974 ; Arditti, 1992 ). Consequently, the opportunity for recording the fruit productivity of orchids is often quite prolonged. Levels of fruit production are frequently noted in ecological studies of orchid species and fruit set is the most widely used measure of reproductive success (Proctor and Harder, 1994 ). Given the large size of the orchid family (estimated as 18 000 species by Dressler [1990] ) with taxa occupying a wide range of temperate and tropical environments and displaying a diversity of epiphytic and terrestrial habits, we might expect reproductive success to also be variable. However, low fruit set is often thought to be characteristic of the family (e.g., Ackerman and Zimmerman, 1994 ; Sabat and Ackerman, 1996 ) perhaps because of the number of reported observations of low fruit productivity among nonautogamous species (e.g., Thien and Marcks, 1972 ; Ackerman, 1981 , 1986 ) and the investigations of reproductive limitation in orchids usually involving species with high levels of fruiting failure (e.g., Zimmerman and Aide, 1989 ; Ackerman and Montalvo, 1990 ).

Reproductive failure in plant species can often be attributed to either pollination limitation where there is insufficient movement of viable pollen between flowers (e.g., because of an absence of pollinators) or to resource limitation where insufficient resources (such as water or nutrients) are available to allow maximum fruit set to take place (Bierzychudek, 1981 ; Stephenson, 1981 ), or to both. Among the Orchidaceae some recent studies have suggested that fruit production in one season may incur a cost to reproduction such that reproductive output and/or vegetative growth is lower in future seasons (Montalvo and Ackerman, 1987 ; Ackerman, 1989 ; Zimmerman and Aide, 1989 ; Snow and Whigham, 1989 ; Ackerman and Montalvo, 1990 ; Primack and Hall, 1990 ). However, an individual orchid can still be pollination limited over its lifetime depending on the level of pollination relative to the cost of reproduction and degree of resource limitation. Demographic modeling has shown that pollination limitation may have an overriding influence on the lifetime reproductive success of individuals when pollination levels are very low (e.g., 10%; Calvo and Horvitz, 1990 ). If these models are correct, lifetime reproductive success in many orchids can be attributed to low pollinator frequencies (e.g., Calvo, 1990a ).

The insect and bird pollinators that visit orchids can obtain a variety of rewards from them including oil (as in Disperis spp.; Steiner, 1989 , 1991 ), floral fragrances (e.g., in Catasetum spp.; Dodson et al., 1969 ; Williams, 1982 ; Kaiser, 1993 ) and, occasionally, pollen (in Cleistes spp.; Gregg, 1991a, b ). But the most common reward collected by orchid pollinators is floral nectar (van der Pijl and Dodson, 1966 ; Arditti, 1992 ; Dressler, 1993 ). It may be completely exposed on the labellum as in Listera spp., collected in a cup-like hypochile, e.g., in Epipactis spp., or, more commonly, hidden in a floral spur, as in Platanthera spp. It has been estimated, however, that one-third of the family are deceptive and that their pollinators receive no rewards at all (van der Pijl and Dodson, 1966 ; Ackerman, 1984 ). Most of these species exploit the food-foraging behaviors of their pollinators through their visual/olfactory resemblance to nectariferous plants (Ackerman, 1986 ; Nilsson, 1992 ). The potential impacts that nectar rewarding or rewardless-based pollination systems may have on fruiting success have been discussed by a few authors. Davis (1986) , for example, has suggested that low fruit set in the American terrestrial species Cypripedium acaule is related to the absence of a floral reward for pollinating bumble bees, while Ackerman, Rodríguez-Robles, and Meléndez (1994) have shown that even a small nectar reward in the Puerto Rican species Comparettia falcata enhances pollinator attraction and fruit set. Following his own long-term study of C. acaule and a brief review of some other published studies, Gill (1989) has suggested that there is a dichotomous pattern in the visitation frequencies of pollinators between nectariferous and nectarless orchids. He stated that while the pollination percentage of nectariferous orchids "is high, often 100%, orchids that produce no nectar and other rewards have very low (often less than 10%) frequencies of capsule formation." This hypothesis was based on the results of 15 species and remains the best attempt to date to quantify the relationship among reward, pollinator visitation, and fruit production in the Orchidaceae.

In recent years some workers have attempted to place the fruit production data from their study species into a broader context by citing the results from a few other published works (e.g., Calvo, 1990a ; Whigham and O'Neill, 1991 ). But these comparisons have always been based on a limited number of geographically restricted species and usually make little mention of the pollination systems involved. Even though there is a substantial available data set on fruit productivity in orchids in the scientific literature, no complete survey of fruit set levels has ever been compiled. In this paper we present a comprehensive survey of fruit set levels in the Orchidaceae, including the results of our recent European studies (Neiland and Wilcock, 1993 , 1994 ; Neiland, 1994 ), to provide a benchmark for future studies. We compare the relative reproductive success of nectariferous and nectarless orchids on a worldwide basis to test the extent and accuracy of Gill's hypothesis and consider the implications that different fruit set levels may have on orchid evolution, rarity, and conservation.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Worldwide literature survey and European field studies
To assess whether levels of reproductive success vary between nectariferous and nectarless orchids in different environments, lists of all of the reported capsule set figures for orchid species were compiled from the literature by scanning appropriately titled papers obtained through literature databases (Biosis and Science Citation Index), orchid books, and paper reference lists. More than 200 referenced sources were checked, resulting in the most comprehensive review of capsule production in the Orchidaceae to date. In all cases only capsule set figures that were, or could be, derived as a percentage of the total number of flowers available were used in our analysis, and those few papers that expressed fruit set as a proportion of plants in a population bearing one or more fruits were omitted since it was not possible to derive figures for fruit:flower ratios from them. Most fruit set data for individual species represent the results from one season of study for a single population, but in some cases they are the mean of the results obtained by the researcher over successive years or from a range of different sites. Where a species had been reported in more than one study, the average fruit set was calculated for that species from all of the cited results. In this way, a single figure of fruit production was derived for each individual species. In addition, we included our data on natural levels of capsule set among 17 European orchids from field sites in the Mediterranean region (Italy and Portugal) and the British Isles (England and Scotland) made between 1991 and 1995.

The fruit set data derived from the literature and field surveys were compared by categorizing orchids as either nectariferous, when they were said to produce nectar on any floral part (following Caspary, 1848 : in Bentley and Elias, 1983 , p. 174), or nectarless when they were not, and, for geography, as either North American, European, from the temperate southern hemisphere, or as tropical. Three nectariferous species from Japan were placed in a separate category of north temperate Asia. For each geographic area, an overall average was calculated simply by averaging all of the percentage figures from each citation within each of the groups. The total number of plants and flowers examined of each species was listed in the results tables when these were available and types of pollinator systems, as described in the original studies, were also noted. For nectarless species we distinguished between mimics, where a specific model had been identified, and deceivers, where orchids resembled general search images. Different growth habits were described for tropical orchids, with epiphytic or terrestrial species being indicated in the tables. We combined the figures from all temperate areas to compare temperate fruit levels of nectarless and nectariferous orchids with those of their tropical counterparts. All species listed in Tables 1 and 2 were either known or assumed to be self-compatible and require pollen vectors for successful fruit production. For completeness, two further lists were compiled of capsule set data from orchids with nonpollinator-dependent breeding systems (autogamous or agamospermic orchids) and from the self-incompatible species.

Orchid rarity
Within the British Isles, some orchids are widespread and/or occur in large numbers and are therefore considered to be common. The distribution of others is more restricted, with fewer plants growing in smaller populations. In his flora of the British Isles, Stace (1991) has assigned these rare species to three groups according to their degree of rarity. Using his categories we referred to those species found in more than 100 different 10 x 10 km Ordnance Survey Grid squares (Perring and Walters, 1962 ) as "widespread," those found in between 15 and 100 different 10 x 10 km squares as "restricted," and those in less than 15 km squares as "rare." We determined the proportions of nectariferous and nectarless species within each group from the literature or personal observations to test the null hypothesis of no association between the provision of nectar and distribution using the chi-squared test of association. We omitted two species from our analyses. For one species, Himantoglossum hircinum, there is conflicting evidence of nectar production (Summerhayes, 1985 ; van der Cingel, 1995 ), which, to date, we have not been able to resolve. The recently discovered species of Epipactis (E. youngiana) was also excluded because its status as a distinct species is still in doubt (Stace [1991] states that it is of uncertain origin and may be a hybrid derivative of E. helleborine and E. phyllanthes).

Hybridization and nectar reward
We compared the observed occurrence of naturally occurring hybrids in the orchid floras of Britain and Europe cited by Stace (1991) and Davies, Davies, and Huxley (1988) , respectively, with their expected frequencies obtained using the binomial distribution to a null hypothesis of no association between hybrid formation and nectar reward and the relative proportions of nectariferous and nectarless orchid species in each flora. Because some nectarless orchid genera include many species and might have been more likely to hybridize within them, such as Ophrys (29), Dactylorhiza (19), and Orchis (27), we repeated the analysis for Europe at the generic level. We omitted from the analyses two monospecific genera (Neottianthe and Comperia) and the four species of Himantoglossum for which we were unable to establish whether or not they were rewarding.

	RESULTS

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Capsule production data
The survey of the literature, starting with Darwin's classic work on orchids (1888) , provided a total of 98 reference sources from which data could be obtained. We found that there had been a marked increase in the number of records of fruit set data in the widely available literature in the last 25 yr (Fig. 1), indicating an increasing interest in the subject. Most of the work had been carried out in North America, Europe, and the tropics. Far fewer studies had been undertaken in the temperate southern hemisphere (only seven from Australia, New Zealand and South Africa combined) and studies (six) from Asia were noticeably absent, despite its species richness. Some species had been repeatedly studied by several investigators (e.g., Orchis mascula in Europe and Platanthera ciliaris in North America), but most were cited only once. Altogether, capsule production data were available in the literature for 104 orchid species, the majority of these being nectarless (73). A further 13 previously unstudied species were included from our field survey of orchid reproduction in Europe. Thus we found fruit set data for a total of 117 orchid species worldwide.

View larger version (17K): [in this window] [in a new window]   Fig. 1. Publication frequency of orchid studies providing data on fruit production from 1951 to 1995.

Fruit production in nectariferous orchids
Compared with nectarless species, capsule production in nectariferous orchids in North America, Europe, and the temperate southern hemisphere was generally high at >50% (Table 2). Floral nectar was provided as a reward, either superficially on the labellum or hidden in spurs, and attracted a wide range of generalist insect pollinators (as with Listera ovata) or a restricted range of specialists such as Lepidoptera (in Platanthera spp.) or hummingbirds (as in Comparettia falcata). The nectar-rewarding species from the tropics were distinctive in having much lower capsule set levels in comparison with nectariferous orchids from temperate areas.

Comparative fruit production in nectariferous and nectarless orchids
Average capsule production figures were higher for nectariferous species than for nectarless ones in all geographic areas (Table 3). The biggest differences found between them were in North America and Europe where nectariferous orchids were on average over two times as successful. The difference between them in the temperate southern hemisphere was not so marked because the nectarless figure was based on a few, apparently successfully pollinated, sexual and nectar mimics from South Africa with operators and models present (Table 2). Among the tropical group, while nectariferous orchids were twice as successful as the nectarless ones, the relative productivity of both types was lower than in temperate regions. The most successful nectarless tropical orchids were the fragrant Coryanthes spp., which had been studied by Dodson (1965) . The average fruit set from the combined data set for all nectariferous species from all areas is 50.8% and for all the nectarless species is 22.2%.

View larger version (47K): [in this window] [in a new window]   Fig. 2. The percentage of high and low fruit set in nectariferous and nectarless orchids from North America (20 spp.), Europe (37 spp.), temperate southern hemisphere (11 spp.), and the tropics (32 spp.). Data are derived from Tables 1 and 2 .

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Analysis of all of the published data we have reviewed on capsule production has confirmed Gill's hypothesis that nectariferous orchids are generally much more successful in terms of fruit production than are nectarless species, and this dichotomy holds true for orchids in each of the temperate zones (North America, Europe, and temperate Southern Hemisphere), as well as in the tropics. In addition, the data have shown, for the first time, that reproductive success of both nectarless and nectariferous orchids in the tropics is consistently lower than in comparable groups in temperate areas. Tropical species are, on average, only one-third as successful as their temperate counterparts (13.6 vs. 38.2%; Table 3). Furthermore, it is a remarkable fact that of more than 67 000 individual orchid flowers that have so far been examined in the tropics, less than 6% have set any fruit. Perhaps, then, it is not surprising that fruit set in the Orchidaceae is often considered to be low. Why should a flower from the tropics be so much less successful in pollination than its counterparts in the temperate areas? One possible explanation is that tropical orchids display a different population structure than do those of temperate areas. Tropical populations are generally small and widely dispersed (Ackerman, 1986 ) and may be unable to sustain pollinator interest even with rewards. Other possibilities could be a lack of suitable pollinators in the tropics or increased competition for fewer pollinators. Alternatively, because the data set is predominantly based on epiphytic species from Central America, this reproductive failure may be a regional or growth habit phenomenon, but the few data collected from other tropical areas also have low reproductive success, suggesting that it is not restricted to central America. Unfortunately, there are insufficient data published on terrestrial species in the tropics to establish whether the epiphytic habit is associated with increased reproductive failure in the tropics. In a preliminary attempt to resolve this question we have compared comments on fruit set levels of terrestrial and epiphytic orchids listed in a single tropical orchid flora (Ackerman's Orchid Flora of Puerto Rico [1995] ). Of the total 145 orchids on the island, some indication of fruit set level was given for 61 species. For these, we classed orchids with fruit set referred to as "uncommon," "infrequent," or "rare" or with a figure of <50% as low (N = 30), and those with "common," "frequent," or "excellent" fruit sets as high (N = 31). Among these orchids, there is no significant association between reproductive success and epiphytic or terrestrial habit (² = 0.096, P > 0.05, df = 1). This suggests that, in one of the best studied orchid floras, the epiphytic habit is not the explanation for the generally low levels of reproductive success that are recorded in the tropics.

Among tropical orchids, even though their success is relatively low compared to temperate species, the dichotomy in success between nectariferous and nectarless species is still distinct and suggests visitation frequencies are twice as common in nectar-rewarding orchids as nectarless ones. This difference holds true, even though the nectarless group includes the floral-fragrance-rewarding Coryanthes species from Central and South America, which are successful in attracting male euglossine bees. The rest of the species in this group are deceptively pollinated and given that Ackerman (1984) has found that a larger proportion of orchids in the tropical floras he examined were rewardless compared with temperate areas and that we have shown that, of all groups, tropical orchids are the least reproductively successful, what maintains this pollination system in the tropics? Possible explanations include (1) increased seed number per ovary, (2) increased survival probability of offspring, (3) increased longevity of the plants, or (4) as suggested by Calvo (1993) increased fruit set is not translated into increased seedling recruitment. There is some evidence that supports the first hypothesis. Arditti (1992 , p. 303) has compiled from the literature the number of seeds produced per capsule for 17 orchids. When we separated these according to tropical and temperate habitats, we found that the nine tropical species produced ~150 times more seeds per fruit than the eight temperate species (the average figure for tropical species was 1 512 516 [±980 082] and for the temperate was 10 056 [± 12 463]). This preliminary result should be further investigated. We are not aware of any supporting evidence for the second or third hypotheses, but European orchids can have very short lifespans, e.g., Ophrys sphegodes which has a half-life of 2 yr (Hutchings, 1989 ), or survive for longer periods, e.g., Dactylorhiza sambucina, which has a maximum recorded age of 30 yr (Tamm, 1972 ), and some current studies of temperate orchids may soon provide data on seed and protocorm survival under natural conditions (Rasmussen and Whigham, 1993 ). For the fourth possibility, Ackerman, Sabat, and Zimmerman (1996) have shown that this is not the case, at least for epiphytic orchids. They showed that if an increase in pollinator attraction occurs, the increase in seed output should result in population growth as seedling recruitment was not microsite limited.

Nectar reward, pollen flow, and hybridization in orchids
While nectariferous orchids in all temperate regions are the most successfully pollinated, in Europe they form interspecific and intergeneric hybrids less frequently than do nectarless species. This finding is in marked contrast to the expectation that nectariferous orchids should form hybrids more often because of their higher pollinator visitation frequencies (Dafni, 1987 ), but is consistent with reported differences in pollinator behavior at nectariferous and nectarless orchid flowers (Dafni and Ivri, 1979 ). Pollinators of nectariferous species spend more time at each flower and visit several flowers on the same inflorescences, whereas visitors to nectarless species stay for a shorter duration and visit few flowers before departing the plant (Dafni, 1987 ). For example, in the nectariferous Spiranthes romanzoffiana of North America, visits by bees lasted 5–35 sec, as they probed for nectar, and there was a high revisitation rate (Larson and Larson, 1990 ), while with the nectarless Orchis morio in England Bombus queens were observed to visit only one flower per plant during their much shorter visits of 2–6 sec duration (Dafni, 1987 ). Because of this high level of constancy and revisitation of pollinators to nectariferous inflorescences, hybrids between nectariferous species are less likely to occur than is the case with nectarless orchids. Here, visitation patterns are likely to be highly randomized between plants of different species due to the inability of the insects to distinguish between flowers with a generalized foraging image or between specific models and mimics. Alternatively visitation patterns may reflect the ability of naive insects to learn to avoid nectarless flowers (as described for bees on Calypso bulbosa in California by Ackerman [1981] , and for Orchis morio in Sweden by Nilsson [1984] ). In either case, pollinators are likely to abandon a nectarless inflorescence for another plant more quickly than is the case with nectariferous species, thereby promoting xenogamy (outcrossing with a conspecific plant) or pollen wastage (with an incompatible species) or interspecific hybridization (with a cross-compatible coflowering orchid). A similar pattern of insect movement may also be found among the nonrewarding Ophrys orchids (Dressler, 1990 ), which are pollinated through pseudocopulation rather than nectar deceit, since a large number of intrageneric hybrids have been recorded (N = 45). Some ethological isolation of the orchids probably takes place, however, as only one intergeneric hybrid involving Ophrys has been found (O. sphegodes ssp. mammosa x Serapias sp., [Davies, Davies and Huxley, 1988] ).

Nectar reward and orchid rarity
From his observation that Orchis purpurea had a fruit set level of only 3% in Kent, England, Darwin (1888) commented that "the suspicion naturally arises that Ophrys fusca [= Orchis purpurea] is so rare a species in Britain from not being sufficiently attractive to insects, and to its not producing a sufficiency of seed." In the same volume he refers to Sprengel's similar observations in Germany on Orchis militaris, which he contrasted with that of Gymnadenia conopsea "in which almost every flower produces a capsule." We now know that this represented the first demonstration of Gill's dichotomy, as O. purpurea and O. militaris are nectarless and G. conopsea is nectariferous. At the same time, Darwin pointed to the absence of fruit set as a potential explanation for orchid rarity. In our investigation of all British orchids we confirmed the association between lack of nectar production and rarity. Although the causes of rarity and extinction are potentially diverse, this characteristic of rare orchids in Britain may enhance their vulnerability to extinction. As the dichotomy between fruit set levels of nectariferous and nectarless orchids occurs worldwide, the association between rarity and nectarlessness may also appear elsewhere. Further studies are necessary on other local floras to establish the extent of this association within the family, especially as this feature may have implications for the successful long-term conservation of rare orchids.

Evolution of nectariferous orchids
Dafni (1987) postulated from a consideration of the systematic affinities of several European genera that their ancestral taxa were nectariferous. He recognized two main evolutionary lines from nectar reward to pollination by deceit, sexual deception and food mimicry/shelter imitation. However, it is difficult to envisage how these deceptive mechanisms, with such low levels of fruit formation, could have evolved from a group of orchids that is the more successful today. It seems more likely that the absence of nectar is the ancestral condition in the orchid family as a whole since (1) the majority of extant primitive orchids are nectarless (Dressler, 1993 ) and (2) the most closely related outgroup to the Orchidaceae are the Hypoxidaceae (which also lack nectaries) as recent studies of chloroplast DNA have confirmed (Chase et al., 1994 ). In addition, the DNA data suggest that the Orchidaceae are a much older family than previously realized with a suggested origin before the end of the Cretaceous period, 65 million years ago. During the Cretaceous, most angiosperm flowers would have been visited by unspecialized insects like beetles and flies, which pollinated them while feeding on both floral and vegetative parts (Endress, 1990 ). A possible hypothesis that could explain the origin of highly adapted deceptive mechanisms among nectarless orchids is that they arose from primitive orchids, which had even lower levels of fruit set than seen today because of their existence in this unspecialized and largely unrewarding anthecological environment. Any mutant having a small adaptation that improved pollinator attraction, even one based on deceit, would have had a reproductive adaptive advantage and would have increased in frequency. Increasing pollination success in these mimetic systems is constrained by potential evolutionary feedback from the operators effecting pollination. It is perhaps for this reason that these orchids have, as we have shown elsewhere (Neiland and Wilcock, 1995 ), evolved nonpollinator-selected mechanisms that promote pollination success in conditions of infrequent pollination (e.g., extreme prepollination floral longevity, prolonged excised pollen viability, and extended postpollination female receptivity). Nevertheless, it is clear from the present survey that the level of fruit set in deceitful orchids is still comparatively low today.

To break away from the ecological and evolutionary limitations imposed by consistent sexual reproductive failure, the only potential means of escape are adoption of pollinator-independent fruit production or the provision of pollinator rewards. However, agamospermy is infrequent in orchids and may be inhibited because embryo-sac formation in the family is unusual in requiring the presence of pollen on the stigma as a stimulus (Neiland and Wilcock, 1995 ) and, although automatic self-pollination has been reported to be more widespread (Catling, 1990 ) and can be successful in circumventing dependence on pollinators (Neiland and Wilcock, 1994 ), it is probably morphologically prevented in most orchids by the structure of the flower (in particular the rostellum; Summerhayes, 1985 ). Of the provision of nectar rewards, when we compared the fruit-set levels of orchids offering rewards other than nectar with those of nectar-rewarding orchids (Fig. 3) we found that rewards other than nectar failed to significantly improve reproductive success above that of nonrewarding orchids. Therefore, the adoption of nectar production, while imposing an additional energy cost that may have to be balanced by a reduction in seed set (Ackerman and Montalvo, 1990 ; Pyke, 1991 ), may prove to have been the most effective and frequent means of escaping low pollination success in the Orchidaceae.

View larger version (47K): [in this window] [in a new window]   Fig. 3. Comparison of the percentage of high and low fruit set in orchids with differing floral rewards. Data are derived from Tables 1 and 2 .

	FOOTNOTES

 
¹ This work was carried out under the auspices of the Harvais Orchid Research Studentship held by one of the authors (M.R.M.N.) at the University of Aberdeen, with additional financial support for fieldwork generously provided by the A. S. Watt and Harvey of Ardo Funds (Aberdeen) and the Percy Sladen Memorial Fund (The Linnean Society, London). The authors thank the many botanists who advised on orchid sites in Britain, particularly Scottish Natural Heritage staff, and our colleagues at the Universita di Napoli (Istituto di Botanica, Portici), and the A Rocha Centre, Algarve, for their hospitality while in Italy and Portugal, respectively. We are also grateful to the reviewers, Joseph Arditti and Arlee Montalvo, and to the Editor-in-Chief, Karl Niklas, for their highly constructive comments and improvements to the final manuscript.

² Author for correspondence.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Ackerman, J. D. 1975 Reproductive biology of Goodyera oblongifolia (Orchidaceae). Madroño 23: 191–198.

———. 1981 Pollination biology of Calypso bulbosa var. occidentalis (Orchidaceae): a food-deceptive system. Madroño 28: 101–110.

———. 1983 Euglossine bee pollination of the orchid, Cochleanthes lipscombiae: a food source mimic. American Journal of Botany 70: 830–834. [CrossRef][ISI]

———. 1984 Pollination of tropical and temperate orchids. In K. W. Tan [ed.], Proceedings of the 11th World Orchid Conference, 98–101. American Orchid Society, Miami, FL.

———. 1986 Mechanisms and evolution of food-deceptive pollination systems in orchids. Lindleyana 1: 108–113.

———. 1989 Limitations to sexual reproduction in Encyclia krugii (Orchidaceae). Systematic Botany 14: 101–109.

———. 1995 An orchid flora of Puerto Rico and the Virgin Islands. Memoirs of the New York Botanical Garden 73.

———, E. J. Meléndez-Ackerman, and J. Salguero-Faria. 1997 Variation in pollinator abundance and selection on fragrance phenotypes in an epiphytic orchid. American Journal of Botany 84: 1383–1390. [Abstract]

———, and M. R. Mesler. 1979 Pollination of Listera cordata (Orchidaceae). American Journal of Botany 66: 820–824. [CrossRef][ISI]

———, and A. M. Montalvo. 1990 Short- and long-term limitations to fruit production in a tropical orchid. Ecology 71: 263–272. [CrossRef][ISI]

———, and J. C. Montero-Oliver. 1985 Reproductive biology of Oncidium variegatum: moon phases, pollination and fruit set. American Orchid Society Bulletin 54: 326–329.

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