ORCHID ECOLOGY Orchid Pollination Exploring a Fascinating World by ron mchatton

[1] the first example of sexual deception in Australian orchids involved the . These orchids are pollinated by male parasitic wasps of the genus Lissopimpla. Here four male Lissopimpla excelsa wasps compete for the favors of

a Cryptostylis erecta flower. mark clements [2] silver-spotted skipper (Epargyreus clarus) pollinating a small purple fringed orchid ( psycodes) at Mt. Mitchell, North Carolina. The long spurs of the orchid have nectar at their ends and the skipper must push its proboscis deep into the spur to get to the nectar. Note the pollinia attached to the base of

james petranka james the skipper’s proboscis. bumblebee . In this case, pollinia of Den. infundibulum are placed on the head of the bee while that from the , with much longer , becomes at- tached to the bee’s central thorax. Because the column of the former species is much shorter, only pollinia placed near the front of the bee will be in a position to contact the stigmatic surface of the column as the bee exits the flower (Du Puy and Cribb 2007). Orchids with large gullet flowers such as Cymbidium are typically pollinated by large carpenter bees and bumblebees are known to pollinate Spiranthes and are implicated in the pollination of northern and some high-elevation species where other large bees are less common or active. 3 4 eric h u nt eric h u nt Some bees gather oils from flowers rather than nectar or and many orchids [3–4] Sobralia [3] and [4], two gen- No one is really sure how long have evolved to attract these . A ago orchids evolved but recent fossil evi- era from very different parts of the orchid couple of examples include Ornithocepha- dence suggests that the development of pol- family, share parallel evolution of the lus and some species of that linia was well established at least 75 million gullet-flower structure characteristic of bee have elaiophores (open, nectar-producing years ago and perhaps earlier (Ramierez pollination. In these genera, the chamber glands) on the lateral lobes of the lip (Buch- 2007). The development of fused reproduc- is formed from the lip and column alone; mann 1987). Orchids pollinated by bees and tive structures, the so-called column, and the remainder of the flower serves as wasps also share a suite of characteristics pollinia are rare outside the advertisement. Here they are illustrated in addition to the presence of some form of and set the stage for the development of gulletlike or bowl-shaped floral structure. an extremely varied and fascinating re- by Sobralia veitchii and . Growers: [3] Bruce Rogers, [4] Fred Shull. Bee- and wasp-pollinated orchids exhibit a productive ecology. Pollinia, more-or-less wide color range with the exception of true fused, relatively large masses of compact red because bees and wasps cannot see red. pollen grains, because of their mass are Fragrance, if present, will be sweet or spicy not effectively distributed by water or and column alone and the remainder of the flower functions only as advertisement. and noticeable during the daylight hours wind and require the active intervention when these pollinators are active. Bees and of an animal, typically an , to effect While perhaps harder to see, the flowers of species can be interpreted wasps land to gather pollen or nectar so the pollination. In addition to the dependence orchids they pollinate have well-developed on a pollen vector, or , orchids as gullet flowers since it’s the “chamber” formed by the complex lip and column landing platforms, nectar guides, either have also evolved myriad pollination syn- structural or visual and sturdy connection dromes or mechanisms that run the gamut that controls pollination in these orchids. The remainder of the flower has evolved to to the column to allow the bees to grasp from advertisement and reward to sexual the flowers. Rewards, offered nectar or mimicry (Dressler 1981). Humans tend tissue-thin texture and reflexes completely to effectively “get out of the way” of the food, may be real or perceived and may or to think of the world in anthropomorphic may not be concealed in a nectary (what terms and forget that orchid flowers have action. Because the pollinating bee must first enter this chamber the bee does not we orchidists typically think of as a spur); the shapes and fragrances they do not for the latter is a common feature of orchids us, but to ensure one thing and one thing receive or deposit pollen when it enters the flower but only as it , thereby making pollinated by nectar-feeding bees and the only — successful reproduction. length of the nectary is directly related to THE POLLINATORS self-pollination highly unlikely. In addition, It has been es- proboscis (tongue) length in the pollinating timated that about 60 percent of the orchid many orchids prevent self-pollination by their pollinating vector by requiring a re- species (Dressler 1987). family is pollinated by wasps and bees In addition to wasps and bees, orchids (essentially pollen-collecting wasps) (van orientation of the deposited pollinaria; such are pollinated by a whole range of creatures der Pijl and Dodson 1966). The form and reorganization only occurring over some including, but not limited to euglossine bees symmetry of orchid flowers suggests that minutes as the soft tissues of the dry (also called orchid bees), flies, butterflies one of the first steps that separated orchids and curl. Specificity of pollinator and pol- and moths, as well as many species of from their close relatives may have been linated species is achieved through adapta- birds; each pollinator group is attracted by the adaptation to pollination by this group tion of chamber size and column placement of pollinators. Bee-pollinated flowers are to insect size. Compaction of orchid pollen a specific combination of attractants and often gullet flowers or modifications of this into pollinia with sticky structures makes forms. Euglossine bees, closely allied to type of flower. In so-called gullet flowers pollen placement much more precise than bumblebees, are limited to tropical Amer- the floral segments create a sort of cham- that of most other flowers and a single bee ica. They range in size from about the size ber in which the pollinating insect must species may serve as the pollinator of mul- of a typical housefly to some large species. enter in the process of gathering pollen. In tiple orchid species without interference. As This group of bees is so closely involved orchids, especially Sobralia and Cattleya, an example, and in the pollination of many orchids that they this chamber is often formed from the lip Cymbidium insigne appear to use the same are often called orchid bees. However, they

340 Orchids jUNE 2011 www.AOS.org 5 david d u p y david

are also involved in the pollination of many tropical American families. Females of some species pollinate nectar-producing orchids such as Sobralia and in that mode resemble other bee pollinators. However, it’s the males of the species that are much 6 more important in orchid pollination. Male f o g den michael and patricia euglossine bees collect fragrance oils from the surface of the flowers they visit and store them in specialized hollow pockets in their hind legs. These oils are then used to attract mates. Because fragrance is the key to attracting these bees, orchids pollinated by male euglossine bees have powerful, of- ten resinous fragrances and will be fragrant during daylight hours. In addition, because nectar is unnecessary, these species do not produce nectar nor are nectar guides pres- ent in the floral structures. But wait you say, what about species. These are pollinated by male euglossine bees and they have unique liquid-producing glands that fill the characteristic bucket with fluid. These glands aren’t nectar producing. Their sole presence appears to be to create a liquid reservoir that, once the pollinating bee enters by accident, leaves the bee un- able to fly and the only escape route is out a narrow, dry passage past the column with its anther and stigmatic cavity. While male euglossine bees land to 7 collect fragrance oils, their mode of flight pemberton robert allows them to maneuver like helicopters [5] pollinia of Dendrobium infundibulum on and even land on vertical surfaces. As a pollinia with the opening of the stigmatic result, orchids pollinated by such bees cavity. The specificity of chamber size to the head of a bee (left) while that from may or may not have well-developed pollinating bee is so strong in the genus Cymbidium insigne, with much longer landing platforms. Examples of euglossine Stanhopea that two examples of the same column, is attached to the bee’s central bee pollinated orchids include all of the species may have overall flower size that thorax (right). and as well as differ by as much as 50 percent while the [6] male euglossine bees collecting chemi- most members of the and column and lip cavity opening will be iden- cals from rotting wood. Note the enlarged some . Pollinator specificity is tical. Remember that the and hind legs used to store these chemicals in this genus serve only to provide a protec- maintained by either a specific euglossine and the orchid pollinia attached to the tive covering during flower development bee–orchid interaction based on fragrance backs of two of the bees. composition or, in the case of promiscuous and advertisement during anthesis. [7] male Euglossa viridissima visiting Gon- bees, a specific size relationship. Such is The complex relationship between gora powellii in cultivation. These bees the case with many species of Stanhopea male and female euglossine bees and the which may be visited by many euglossine plants they pollinate can be illustrated by are known to visit other species bee species. One species will fit correctly the Brazil nut tree (Bertholletia excelsa). in the wild. within the cavity formed by the lip epichile, Plantation farming of this nut tree has mesochile horns and the ventral surface of proven difficult to do with reasonable yield the column, thereby properly aligning the because of this complex interplay. The tree

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10 11 12 eric h u nt lynn o’sha lynn dennis m. hansen dennis m.

[8–9] orchids adapted to butterfly and is pollinated by female long-tongued eu- created from the fusion of the lip to the un- moth pollination have noticeable spurs. glossine bees of the genus Eulaema (Mota derside of the column and the only feature The length of the spur is tightly tied to the Maues 2002). These bees are strong enough that may be visible is the keyhole formed proboscis length of the pollinating moth to lift the coiled hood on the nut tree flowers between the underside of the column and or butterfly.L ong-tongued hawk moths and possess a tongue long enough to snake the nectar guides or lip crests. Butterflies pollinate species such as its way through the complex, coiled flower and moths are normally associated with to reach the nectar reserve. The presence of pollination of flowers that have few ovules. dollii [8] characterized by a very long spur the female bees is dependent on the flower- This is because, in nonorchids, pollen is while citrata [9] is pollinated by a ing of an orchid species that does not grow usually transported adhering to the ’ moth with a much shorter tongue. on the nut tree. The orchid flowering causes tongues and their long narrow tongues are [10] a sarcophagid (carrion) fly carrying pol- a swarming of the males of this bee species not suited for carrying large quantities of linia from Satyrium pumilum, an African who are attracted to the orchid’s resinous pollen. Orchids avoid this problem because species that attracts its pollinator by fragrance, collecting it to be used in at- the pollinia become affixed to the insects mimicking the smell of carrion. tracting female bees. The swarming of the head, or in the case of discolor, to [11–12] Fly pollinated orchids often are male bees causes the swarming of female the eye of the pollinating miller (Whigham outfitted with hairs and other moveable bees that feed on, and pollinate the nut tree. and McWhety 1980). Butterflies and some parts that attract the attention of the Think of it as sort of the insect equivalent moths (mostly those that are day-active), pollinating fly.T he tassellike ornamenta- of a singles bar. unlike bees, see red and many butterfly pol- tion on [11] Butterflies and moths are nectar feeders linated orchids are bright pink, red, yellow and villosa1 [12] appear to mimic and are almost as common pollinators as or even vivid violet. bees. Because of their long, coiled tongues, Because visual clues appear to be the maggots feeding on the flower. In the orchids adapted to butterfly and moth pol- most important attractant for butterfly pol- case of Bulb. phalaenopsis this ruse is lination have a narrow spur or nectary and linated orchids, fragrance is usually lack- further strengthened by the fragrance of belong to a floral classification called key- ing. Moths on the other hand, especially the flower — carrion. Growers: [11] Bill hole flowers. In many species, such as those those that are nocturnal, can really only Weaver, [12] Lynn O’Shaughnessy. of Angraecum and Aerangis, the spur may distinguish light from dark and a common be pronounced. In many others, such as characteristic of moth pollinated orchids is 1Formerly schiedei. many species of , the nectary is that they are white, cream-colored or green

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and are typically fragrant, the aroma acting pleurothallids and many Bulbophyllinae. [13] a green violetear (Colibri thalassinus) as an additional attractant in the darkness. The floral features involved in attracting feeding at the flowers of anElleanthus Since nature wastes nothing, moth pol- flies depend on the group of flies involved. species in the Monteverde Cloud Forest linated orchids will exhibit fragrance only In the case of mosquitoes, the insects func- of Costa Rica. during the period of day or night in which tion essentially as tiny moths and may take the particular pollinator is active. As ex- the place of moths at high latitudes. At least of Bulbophyllum phalaenopsis and Stelis amples, is pollinated by one orchid, Platanthera obtusata is known villosa or the buzzing activity of other flies a small Miller active only just before and to be pollinated by mosquitoes (Thien and around host material. Orchids pollinated by after sunset and as a result this orchid spe- Utech 1976). A second group of prominent carrion flies have odors that mimic rotten cies is fragrant for only a period of a couple orchid pollinating flies are those that collect flesh and often are dark red, dark brown of hours beginning about one hour before oils. Orchids pollinated by oil-gathering or red-purple. A great many species of sunset. By contrast, Angraecum sesquipe- flies are characterized by open-or shal- Bulbophyllum and appear to dale reaches its peak fragrance only during lowly-cupped flowers with disagreeable be pollinated by carrion flies. the wee hours of the night. Examples of odors during the daylight hours. Orchids Even termites and crickets may get orchids pollinated by butterflies and moths with fecal odors are pollinated by oil-col- into the act. The majority of Angraecum include and many Epidendrum lecting flies. In addition, because the fly is species endemic to the Mauritius and species as well as most of the attracted to the appearance of excrement or Reunion islands are clearly pollinated by and . There are examples of something decomposing, most oil gathering something other than long-tongued Hawk specificity similar to those between male fly-pollinated orchids are either brown or moths as evidenced by their development euglossine bee and orchid as well. For red-purple. Nectar, in the form of the oil of short-spurred, mostly green flowers. We instance, is visited the flies collect, will always be present and now know that at least Angraecum cadetii by males of a single species of Ctenuchid many orchids so pollinated will have shiny is pollinated by a species of raspy cricket moth and the species which comprise the wet structures visible on the flower as is (Micheneau et al. 2010). The cricket, also Epidendrum paniculatum complex attract the case with many Bulbophyllum species. new to science, represents the first clearly sup- male Ithomiid butterflies (Adams and Goss Many flies, especially carrion flies, are ported evidence of pollination by herbivorous 1976). Flies, including mosquitoes, repre- attracted to fringes and it is thought that orthopterans (grasshoppers, crickets and ka- sent a diverse group of insects and pollinate the movement associated with the fringes tydids) in the orchid family and in flowering a wide range of orchids, including most is sensed as either maggots as in the case plants in general. Rhizanthella gardneri, one

www.AOS.org jUNE 2011 orchids 343 a variety of Zosterops borbonicus also endemic to Reunion Island and represents a great example of the evolutionary inter- dependence of orchid and pollinator. In bird pollination, the pollinia are usually attached to the beak and, at least in hum- mingbird pollinated orchids, a significant percentage of species have dark pollinia suggesting that natural selection has fa- vored those with more difficult to see dark pollinia over those with typically more visible yellow pollinia. Structural changes brought on by adaptation to pollinators can have such dramatic effect on flower form that closely related species may appear to belong to different genera and conversely, orchids not really closely related may produce very 14 15 james osen james parsons ron similar flowers — the result of convergent evolution. Such seems to be the case in of ’s curious underground orchids, the Oncidium alliance where a wide range appears to be regularly pollinated by termites, of pollinators is operative. Historically, the only known example of termite pollina- the generic limitations in this group of tion in the Orchidaceae (van der Cingel 2001). orchids have often been dominated by flo- This rare and unusual orchid spends its entire ral structural differences and we are now life underground in association with the roots finding, based on DNA sequences, that of a member of the genus Melaleuca. At flow- this may not necessarily be correct. One ering time, a head of small, spirally arranged interpretation of the data places a large flowers emerges from the ground but remains number of closely related species from concealed under the -litter. While pollina- multiple genera into the genus Oncidium tion by a gnat has been demonstrated, and conversely moves a group of species termites have also been observed to regularly with otherwise Oncidium-like flowers into and systematically visit newly opened flowers (Chase et al. 2009). Basically and to transport pollen masses making them flat, bright yellow-and-brown likely pollinators. 16 appear to mimic the flowers of a group of eric h u nt While birds may not seem like likely plants in the Malpighiaceae. The flowers orchid pollinators they are however, fairly [14–15] bird-pollinated orchids often share of these flowering trees and shrubs are regularly encountered. The syndrome similar urn- or tubular-shaped flowers. bright yellow and one is modified for bird pollination is similar to that of into a structure called the banner petal. [14] is known butterfly pollination, with tubular, viv- to be pollinated by birds. Although the On the banner petal are specialized glands idly colored red, yellow, violet or white that produce thick brown oil. Pollination in pollinator of sanguineus keyhole-flowers except that the flowers this group of flowering plants is effected [15] is unknown, the urn-shape, bright are typically much stiffer and fragrance is by oil-collecting bees of the genus Centris. red flowers and arrangement on the usually absent. Bird pollination becomes These bees land on the banner petal and, more and more important with increas- all strongly suggest the while grasping this petal tightly, scrape ing altitude and may represent a natural pollinator to be a bird species. the oil-producing glands. Oncidiums pol- progression as insects become less and Growers: [14] Smithsonian Institution, linated by Centris bees are bright yellow less active at colder, higher elevations. In [15] Marni Turkel. and often have brown markings that mimic the Old World tropics, Sunbirds (Nectari- [16] not all bird-pollinated orchids are niidae) are efficient pollinators and many oil-producing glands (in some oncidiums, tubular or urn-shaped. This Cattleya2 species of Dendrobium are probably pol- actual oil glands are present on the side coccinea is dramatically reduced in linated by these birds. In the New World lobes or crest of the lip). When the polli- size from its larger, bee-pollinated tropics the role is filled by hummingbirds nating bee lands to harvest the oil deposit, relatives. The bright red color and (Trochilidae). Examples of humming- it firmly grasps the oncidium’s lip with its mandibles while attempting to harvest narrow constricted lip are also both bird-pollinated orchids include species of oil from the flower. Such a pollination characteristic of the changes that re- , Cochlioda, and strategy requires a solid, strong connection sult from adaptation to bird pollination. and Epidendrum pseudepidendrum (van der Cingel 2001). Lastly, not all bird- between the orchid lip and the column or Grower: Anna S. Chai. pollinated orchids are vividly colored. oil-harvesting runs the risk of destroy- Angraecum bracteosum and Angraecum ing the flower. As such, the lip of these striatum, both endemic to the Island of Oncidium species is fused to the column Reunion off the coast of Madagascar, across the entire lip base. In contrast, bees are pollinated by birds (Micheneau et al. of the genus Bombus (bumblebees), like 2Formerly Sophronitis. 2008). The latter species is pollinated by honey bees, feed on nectar and collect

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pollen to feed their larvae. These bees are forms on their lips. The pollinating in- attracted to floral structures that resemble sects, usually bees, eat this pseudopollen, or suggest the presence of nectar and pol- thereby assuring that the bees will return len and in orchids this can take the form to additional flowers (Dressler 1981). Al- of yellow crests and yellow dusting of ternatively, some species form color against light flower color resembling waxes on their lip calluses that are collected spilt pollen and shallow cavities formed by the pollinators for some purposes not by the narrow attachment of the lip to clearly understood. The labellum of freshly column in some species. Nectar-feeding opened flowers is cov- bees do not grasp the flower in the same ered with fine trichome hairs that produce way as oil-collecting bees while harvesting starch or sugar. These hairs are connected and in these cases the orchid lip may be to the lip surface by a section of specialized attached to the column by just a narrow cells that decompose as the flower ages. claw. Finally, adaptation to bird pollination When the flowers are too old to be good w hitten results in the most dramatic changes. The candidates for pollination or are actually 19B current DNA data suggests that Cochlioda pollinated, these cells die and are sloughed mark and Symphyglossum, whose bright red, off leaving a lip surface devoid of reward [17–19] nowhere are the changes induced pink and orange flowers look nothing like (Kjellson and Rasmussen 1987, Davies and by pollinator more dramatic than those those of an Oncidium, are in fact just that Turner 2004). In some species, the promise in the genus Oncidium sensu latu. — oncidiums pollinated by hummingbirds of reward is hollow. The yellow crest of and even Sigmatostalix, a genus that at hairs in Calypso, Arethusa and Historically the of this group of first glance seems distinctive, is nothing evidently resemble a cluster of pollen- orchids has largely been based on floral more than a scaled-down version that has bearing anthers and pollination depends on morphology and modern DNA sequenc- specialized in the small end of the oil-col- deceiving inexperienced bees. ing suggests that a number of genera, lecting bee spectrum. Often the promise of rewards is also including Oncidium, and FLORAL ATTRACTIONS any dis- coupled with the presence of moveable Cochlioda, may indeed all be oncidiums. cussion of orchid pollination wouldn’t parts. Such moving parts can be passive as The yellow-and-brown be complete without a discussion of the in the fringes present on many Bulbophyl- stipitatum [17] represents the group of mechanisms by which the pollinators lum flowers to those that spring shut (with Malpighiaceae-mimics pollinated by are attracted to the flower. We’ve briefly or without the creation of a trap) when Centris bees that collect oil. Odontoglos- touched on orchids that use fragrance to triggered by a pollinating insect. Fringes, sum crispum [18] represents the changes mimic rotting flesh but that’s just the tip of hairs, tassels and other appendages may do that occur when the pollinators are pollen the iceberg. No other plant family exhibits nothing more than give the appearance of and nectar-feeding Bombus species and the range found in orchids: from real or constant motion around the flower or they Odontoglossum sanguineum [19] is hum- perceived rewards (food or sex) to those may provide more interest. In the case of mingbird pollinated. As in many epiden- with moveable parts or floral traps to those Bulbophyllum phalaenopsis, the white drums, the nectary in Odm. sanguineum that attract pollinators based on mimicry of structures on the flower resemble maggots is formed by fusion of the lip to the other flowers or insects. Food rewards, real and help to strengthen the impression of underside of the column. The entrance to or perceived, may represent the simplest of something dead. It has been suggested these attraction mechanisms. While orchid that the tassels present on the flowers of this short chamber is visible in the face-on pollen isn’t consumed by the insects that Stelis villosa are actually perceived by view [19A]. The up-turned aspect of the pollinate orchids, most and the pollinating insect as larval maggots on flower, common in bird-pollinated orchids, some Maxillaria and species have which their own larvae feed. Fringes and is seen in the side-on view [19B]. Grower evolved mealy, pollenlike substitute that appendages may be coupled with moveable [17]: Hawk Hill Nursery.

www.AOS.org jUNE 2011 orchids 345 pollinators to territorial insect species to sexual mimicry involving flowers that re- semble females of the pollinating species. Some species of are believed to be mimics of Malpighiacae. Female oil- gathering bees collect oil from the glands of the flowers of these vines and the same bees have been seen to seize Tolumnia spe- cies and then attempt to fly away (Nieren- berg 1972). Such mimicry may be a fairly common occurrence. Phragmipedium kovachii is believed to mimic a species of Tibochina, Phrag. besseae appears to mimic a similarly-colored gesneriad and appears to mimic both lantana and a milkweed species with n vieira n Á orange-and-yellow flowers (Dressler 1981). In the last case, the mimicry may 20 sebasti actually accomplish two things. Inexperi- enced insects may be fooled into visiting [20] sebastián Vieira observed this wasp parts. A good example of this combination the Epidendrum flowers at a frequency is the yellow fringe on the hinged label- inspecting every flower on the inflores- sufficient to ensure reproductive success lum of Calopogon species that appears to cence of this Pleurothallis species in and herbivores may mistake them for the the pollinating insect as edible pollen on a forest in the mountains of Colombia. unpalatable species they resemble. In fact, a non-orchid flower. When the pollinat- Evidently one of the “honest” species there is an entire group of Epidendrum ing bee lands on the lip, the weight of the in this genus, the wasp was observed species that superficially resemble Epi. bee causes the lip to fall forward onto the to lick the nectar from each flower for ibaguense, varying in color and details of column, transferring pollen. some seconds before proceeding to the the lip. Each of these species appears to Trap flowers run the gamut from pas- mimic a different related shrub based on sive traps such as Cypripedium acaule next flower. In the process, the orchid’s pollinaria were attached to the wasp’s flower color. Recently, Du Puy and Cribb and Phragmipedium besseae to those (2007) have suggested that Cymbidium head. with active traps such as Pterostylis and insigne subsp. seidenfadenii is a floral . Passive traps function by mimic of Rhododendron lyi, a species with creating a single point of entry and a single that the pollinia be upright or pointed which it grows and flowers sympatrically. escape route that brings the pollinating forward toward the bee’s head. The orchid This subspecies is found in two forms, one insect out past the flower’s anther. The avoids this complication by the fact that with the characteristic red-marked white escape route can be created by a lining the bee is wet when it leaves the escape lip and a form devoid of red markings in of aligned hairs that allow only one way route and cannot fly. As the bee dries, the the lip. The Rhododendron bears a white out, surface texture that allows the pol- pollinarium stipe dries as well and curls flower with a touch of yellow in the throat linating insect to establish footing only forward aligning the pollinia. and freshly opening flowers of the three along the appropriate route or stair like In several orchid species, the hinged species appear remarkably similar. This structures that force the insect past the lip movement is not passive in nature. The Cymbidium, Rhododendron and Dendro- anther. The elliptical “windows” around genus Porroglossum is a good example. In bium infundibulum (a species which is the rim of the pouch of Phrag. besseae also common in the same habitat) were are actually windows composed of color- these orchids, the hinged lip is connected observed to be visited by the same spe- less, transparent cells that are designed to to the column by a long column foot and cies of bumblebee, Bombus eximius, and allow sufficient light to enter the pouch the lip is sensitive to touch at the callus pollinia from both orchid species was ob- to keep the trapped, diurnal insect active near the base of the lip. When touched, the long enough to emerge from the pouch. sensitive lip quickly snaps shut, creating served on the visiting bees. They suggest Without them, the trapped insect would a cavity between the lip and the ventral that the presence of the red-free color form simply go to sleep and perhaps even die surface of the column trapping the visit- in large numbers might be an excellent in the pouch. The most incredible example ing insect. The only exit is up along the example of natural selection in process. of passive traps in orchids is Coryanthes lip surface past the stigma and rostellum. This color form more closely resembles where the visiting euglossine bee, attracted Insects too small to effect pollination ei- the Rhododendron flower when freshly by the powerful resinous fragrance, is ma- ther do not trigger the lip or simply leave opening and may be being selected for in neuvered into a liquid-filled bucket from through what for them is a wide open path- the competition for pollinating bees. which the only escape for the now wet bee way. Insects that are too large may force Floral mimicry that depends on resem- is out through a narrow channel at the back their way out the side of the trap. A similar blance of an orchid’s flowers to invading of the bucket. Bees too small simply leave mechanism occurs in Acostaea, Pterostylis insects has been characterized by van der the bucket without contacting the anther and some species of Drakaea. Pijl and Dodson as pseudoantagonism but and bees too large cannot get out. When FLORAL MIMICRY orchids are it might be better called pseudotrespass- the bee exits the passageway, the pollinia masters of mimicry in the plant world. ing. This mimicry is observed in several attach pointed toward the back of the bee. Floral mimicry in orchids ranges from species of Oncidium as well as possibly Contact with the stigmatic cavity requires mimicking other flowers to compete for Tolumnia henekenii. The pollinator of

346 Orchids jUNE 2011 www.AOS.org Oncidium species, such as and , appears to be the male of a species of oil-collecting bee. The females collect oil from clusters of plants and the males tend to pick these clusters as bases to defend their territories against any flying insects that are not females of their species. The inflores- cences of these orchid species wafting in the breeze appear sufficiently like invading swarms of insects that the male bees attack the flowers and carry pollen away on their faces with the “border skirmish” to be re- peated on other within the territory. Tolumnia henekenii, endemic to the island of Hispaniola, was long thought to be pollinated by pseudocopulation because the flowers are visited by male bumblebees (Dod 1976). However, it now appears that the mechanism may be more likely pseudoantagonism. Bumblebees are terrestrial, territorial bees and typically occupy fiercely defended territories. The bumblebeelike flowers of this orchid are thought to resemble male bumblebees and pollination may result from attack on the flowers by the defending male bee. The epitome of floral mimicry involves those cases where orchid flowers resemble females of the pollinating insect and pol- lination occurs as the result of pseudocopu- lation. Pseudocopulation in orchids has evolved multiple times in different parts of the world and with different groups of orchids and insects, and it’s remarkable that it appears to be found only in orchids. In some cases, the specificity is so well de- veloped that natural hybrids are prevented while in other cases natural hybridization is relatively common. For instance, in Euro- 21 pean Ophrys, the resemblance is essentially u se backho g ary visual and fairly unspecific. Recent genetic seeking insects from bees and wasps analyses suggest that of the 216 distinctly different taxa in this genus, 118 of them to beetles and flies. Here Lissopimpla are of hybrid origin (World Checklist of excelsa, known in Australia by the com- Selected Plant Families 2011). This is in mon name orchid dupe wasp, pollinates stark contrast to the situation observed for Prasophyllum vitetrum. The wasp is Australian terrestrial orchids, such as Chi- known as the orchid dupe because this loglottis and Drakeae. In these cases, the species is duped into pollinating a Cryp- attraction of the male insect is pheromonal tostylis species by sexual mimicry. Like and reinforced visually. Natural hybrids in all members of its genus, Lissopimpla these genera are essentially nonexistent. In excelsa is parasitic. the Western Hemisphere, pseudocopulation [22] some orchids combine pollinator has evolved in at least two orchid tribes, the gu e syndromes. The pronounced crest on Maxillarieae and the . It is 22 the lip of this Calopogon flower looks the main pollination syndrome in Tricho- bob spra strikingly like a cluster of pollen-bearing ceros and (both in the Maxillar- [21] Prasophyllum is one of the few genera ieae tribe). Both are apparently pollinated anthers. In addition, the lip is hinged by flies, the former by males of the genus in the known to attract its near its base so that when a feeding Paragymnomma (van der Cingel 2001). It pollinators with the reward of nectar, bee lands on the crest, the weight of has recently been observed in the other genera invoking deceit or the bee will cause the lip to collapse for- (Blanco and Barboza 2005). In Lepan- sexual mimicry. Pollinators, depending ward dropping the bee onto the column thes, the pollinator is a male fungus gnat on species, are all manner of nectar- in the flower’s center.

www.AOS.org jUNE 2011 orchids 347 and we now know that at least in one group of Australian terrestrials, Cryptostylis, the encounters lead to ejaculation by the male insect (Gaskett et al. 2008). The cost of sperm wastage is fascinating and begs the question as to why these insects continue to visit these flowers. The pollinators of these Australian sexually-deceptive orchids are almost always solitary and haplodip- loid species. Therefore, female insects deprived of matings by orchid deception can still produce male offspring, and as a result increase the percentage of males in the population and concurrently enhance orchid pollination. In addition to these simple examples of mimicry in which an orchid species produc- es a fragrance suggestive of the female of the pollinating species or evolves a flower that looks like another species in order to compete for pollinators, some orchids express what might be called second-order mimicry. Mimicry of the second order is especially intriguing. In these second-order situations, the flower produces chemical or visual signals that suggest another insect, the presence of which attracts the pollinator to the flowers. As an example, veratrifolia has dark structures on the la- bellum that superficially resemble a colony of black aphids. When aphid colonies are under attack by predatory insects, the aphids emit a chemical pheromone that alerts the remainder of the colony to the attack. This pheromone however, also attracts other predatory insects to the fray. In the case of this Epipactis species, the flower’s fragrance is a chemical copy of the aphid-under-attack pheromone. The pollinating wasp sees the

23 u l piko dark lumps on the labellum and smells aphid pa colony in distress and lands on the flower to [23–24] sexual mimicry may take more feed on the aphid colony. As a result, orchid pollinia are transferred from flower to flower than one route. Australian terrestrials (Stökl et al. 2010). such as this Chiloglottis species [23] The more we study the world of or- mimic both sight and smell, producing chid pollination, the more intricate and fragrance compounds that mimic the convoluted it becomes. Eventually, we sexual pheromones of the pollinat- may figure out the answer to that age old ing insect species. In these cases the question, “Which came first, the chicken combination of sight and smell make or the egg?” but in the meantime one thing attraction exceptionally specific and is clear: form and function are intimately natural hybrids in these systems are linked when it comes to orchid pollination. effectively unknown. On the other If you can imagine a pollination mechanism hand, in European terrestrials such as we will probably someday find an orchid that utilizes it. this Ophrys species [24] the mimicry appears to be strictly visual, the orchid References appearing to the insect to be a female Adams, R.M. and G.J. Goss. 1976. The Reproductive of its species. The deceit is not nearly Biology of the Epiphytic Orchids of Florida III. — Epidendrum anceps Jacquin. Amer. Orchid Soc. perfect and as a result natural hybrids Bull. 45(6):488–492. abound in European terrestrials. Blanco, M. and G. Barboza. 2005. Pseudocopulatory Pol- lination in Lepanthes (Orchidaceae: ) w hitten by Fungus Gnats. Ann. Bot. 95(5):763–772. 24 Buchmann, S.L. 1987. The Ecology of Oil Flowers and mark

348 Orchids jUNE 2011 www.AOS.org 25 alex smart

Their Bees? Annual Review of Ecology and Systemat- ics. Annual Reviews, Palo Alto. 18:343–96. Chase, M. and A. Pridgeon. 2009. Subtribe Oncidiinae, pp. 211–394. In Genera Orchidacearum Vol. 5 Epiden- droideae (Part Two), A.M. Pridgeon, P.J. Cribb, M.W. Chase and F.N. Rasmussen (eds.). Oxford University Press, Oxford. Coleman, E. 1928. Pollination of an Australian Orchid by the Male Ichneumonid Lissopimpla semipunctata Kirby. Transactions of the Entomological Society of London 76:533–539. __. 1932. Pollination of pedunculata R.Br.? Vic- torian Naturalist 49:179–186. Davies, K.L. and M.P. Turner. 2004. Pseudopollen in Dendrobium unicum Seidenf. (Orchidaceae): Reward or Deception? Ann. Bot. 94:129–132. Dod, D.D. 1976. Oncidium henekenii — Bee Or- chid Pollinated by Bee. Amer. Orchid Soc. Bull. 45(9):792–794. Dressler, R.L. 1981. The Orchids, Natural History and Classification. Harvard University Press, Cambridge and London. Du Puy, D. and P. Cribb. 2007. The Genus Cymbidium, 2nd Edition. Kew Publishing, Royal Botanic Gardens, Kew. Gaskett, A.C., C.G. Winnick and M.E. Herberstein. 2008. Orchid Sexual Deceit Provokes Ejaculation. The 26 American Naturalist 171:E206–E212. mattinson nathan Kjellson, G. and F.N. Rasmussen. 1987. Does the Aphid Alarm Pheromones to Attract Hoverflies for Pollination of Dendrobium unicum Seidenf. Involve [25] pollination of Diuris behrii is not well Pollination. Proceedings of the Royal Society B, Online, Pseudopollen? Die Orchidee 38:183–187. understood. Visitation by only males of DOI: 10.1098/rspb.2010.1770. Micheneau, C., J. Fournel, L. Humeau and T. Pailler. Thien, L.B. and F. Utech. 1970. Thien, L.B., and F. Utech. one bee species while other similarly 2008. Orchid–Bird Interactions: A Case Study from The Mode of Pollination in Habenaria obtusata (Orchi- Angraecum (, Angraecinae) and Zosterops colored species are ignored are aspects daceae). Amer. J. Bot. 57:1031–1035. (White-Eyes, Zosteropidae) on Reunion Island. Botany of sexual mimicry while the flower’s van der Cingel, N.A. 2001. An Atlas of Orchid Pollination, 86:1143–1151. America Africa and Australia. A.A. Balkerma, bright yellow color and floral structures Micheneau, C., J. Fournel, B.H. Warren, S. Hugel, A. Rotterdam. Gauvin-Bialecki, T. Pailler, D. Strasberg and M.W. are indicative of nectar mimicry (Cole- van der Pijl, L. and Dodson, C.H. 1966. Orchid Flowers: Chase. 2010. Orthoptera, A New Order of Pollinator. Their Pollination and Evolution. University of Miami man 1932, Nash 1979). Ann. Bot. 105(3):355–364 doi: 10.1093/aob/mcp299. Press, Coral Gables. [26] Cryptostylis leptochila, the small- Mota Maues, M. 1998. Reproductive Phenology and Whigham, D.F. and McWhety, M. 1980. Studies on the Pollination of the Brazil Nut Tree (Bertholettia excelsa tongued orchid, is pollinated by male Pollination Ecology of Tipularia discolor (Orchidaceae). Humb. & Bompl. Lecythidaceae) in Eastern Amazonia, Amer. J. Bot. 67(4):550–555. Lissopimpla semipunctata wasps. The p. 208. In Pollinating Bees — The Conservation Link World Checklist of Selected Plant Families. 2011. The Between Agriculture and Nature, eds. P.G. Kevan and wasps are common throughout Aus- Board of Trustees of the Royal Botanic Gardens, Kew. V.L. Imperatriz-Fonseca. Ministério do Meio Ambi- tralia but the orchid is endemic to New Published on the Internet; http://apps.kew.org/wcsp/ac- ente, Brasília. cessed 2011. South Wales and Victoria States. If the Nash, R.C. 1979. Observation of Native Bees on Diuris pedunculata. Journal of the Native Orchid Society of orchid is introduced to an area where it South Australia 3:7–9. Ron McHatton, PhD, has been growing or- is new the male wasps detect the flow- Nierenberg, L. 1972. The Mechanism for the Maintenance chids for more than 47 years. A chemist by ers almost immediately and are drawn of Species Integrity in Sympatrically Occurring Equi- training, he is the Society’s chief operating tant Oncidiums in the Caribbean. Amer. Orchid Soc. to them (Coleman 1928). Bull. 41(10):873–881. officer, director of education and editor of Stökl, J., J. Brodmann, A. Dafni, M. Ayasse and B. Hans- its monthly e-newsletter. (e-mail rmchat- son. 2010. Smells Like Aphids: Orchid Flowers Mimic [email protected]).

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