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Biotic resource needs of specialist orchid pollinators.


Pollinator networks are much more generalized than previously thought (Waser et al., 1996) and extreme pollination specialization is relatively rare (Waser et al., 1996; Olesen & Jordano, 2002). Orchids are the rare exceptions having large numbers of species employing extreme pollination specialization. It is estimated that approx. 60% of all orchid species have only one pollinator species or a discrete lineage of pollinators (Tremblay, 1992). The evolution of pollinia, which occurs in the majority of orchids, functions best with specialist pollinators. Pollinators are manipulated by orchids that glue the pollinia to a specific location on their bodies so it can be subsequently removed and placed on the stigma when the pollinators visit another orchid of the same species. Even orchids without pollinia can be extremely specialized as has been found in some Paphiopedilum species (Shi et al., 2007). The evolution and widespread occurrence of pollination through pseudocopulation in orchids depends of specialist pollinators, as does brood site pollination in Paphiopedilum, both of which employ single species of a single gender as a pollinator. Chemical mimicry is best known in pseudocopulatory pollination of orchids but it occurs in other types of orchid pollination as recently discovered in Dendrobium sinense Tang & F.T.Wang. The fragrance of this orchid mimics the alarm pheromone of honey bees to attract the honey bee predator Vespa bicolor Fabricius as its pollinator (Brodmann et al., 2009).

Overall, orchids with specialist pollinators are more vulnerable than orchids with generalist pollinators. Biotic resource needs of all orchid pollinators are important but those of specialist orchid pollinators are relatively more important. Even a single essential resource can determine both the presence and abundance of an essential specialist orchid pollinator and the reproductive success of the orchid.

In this review, I seek to examine the biotic resources needed by some specialist orchid pollinators. My objectives in addition to describing these examples are as follows.

--To provide insights into the highly complex relationships involved.

--To identify potential vulnerabilities of orchids because of their highly specialized pollinator resource needs.

--To imply the difficulties likely to be encountered in attempts to restore pollination services to orchid species and communities where they have been lost.

Facilitation Plants

The most apparent resource needs for orchid pollinators are nectar and pollen which are used widely as foods for adults and also as the brood provision for most bee pollinators. Because most orchids bear pollinia, pollen in most orchids is not a collectable adult food or brood provision. The large number of orchid pollinators that need pollen, which include not only bees, but syrphid flies, heliconine butterflies, and many others, must also obtain pollen from other plants.

Nectar is an even more widely needed food for adult pollinators as well as for a brood provision in bees. Bird pollinators of orchids are nectar seekers (van der Cingel, 2001), as are the majority of orchid insect pollinators. Because about one third of the orchids, or about 10,000 species, have no floral nectar (Neiland & Wilcock, 1998; Vereecken, 2009; Jersaikova et al., 2006; Jersakova et al., 2009), the numerous pollinators of these plants must acquire the needed nectar from other plants. Orchid pollinator needs for nectar can increase the pollination of rewardless orchids through pollinator visitation to facilitation plants.

Magnet Plants

One mechanism for facilitation of pollination is the magnet species effect (Thomson, 1978), whereby a rewarding species increases the pollination success of neighboring plants with inferior rewards. The rewardless orchid Anacamptis morio (L.) was found to have higher visitation of its queen bumble bee pollinators when growing with magnet flowers with nectar rewards (Johnson et al., 2003). Experimental work, however, indicates that co-occurring nectar bearing plants can compete for pollinators to the detriment of the rewardless orchid (Lammi & Kuitunen, 1995).

Model Plants

A more explored type of facilitation plants are those that are rewarding model plants of rewardless orchid mimics (Dafni, 1984). Studies examining these relationships include: Dafni and Ivri (1981) in which Orchis israelitica Baumann and Dafni mimics the Bellevalia flexuosa Boiss. (Liliaceae) in Israel; Johnson (1994) where the specialist satyrid butterfly Aeropetes (Meneris) tulbaghia (L.) pollinates Disa uniflora which mimics a red flowered Kniphofia (Asphodelaceae) in South Africa; Johnson and Johnson (1995) and Johnson and Steiner (1997) where long tongued horse and tangle winged flies pollinate Disa draconis (L.f.) Sw. which mimics an assortment of coexisting long-spurred flowers in different families in South Africa; Gigord et al. (2002) in a glasshouse experiment, bumble bee queens pollinated Dactylorhiza sambucina Soo that mimics Mimulus guttata Fisher ex DC (Scrophulariaceae); Peter and Johnson (2008) where a specialist bee pollinated Eulophia zeyheriana Sonder that mimics the bellflower Wahlenbergia cuspidata Brehmer (Campanulaceae) in South Africa. The importance of both magnet and model plants demonstrates the need to conserve the plant communities in which orchids live.

Bees-Pollen Specialists

In contrast with the lack of pollinator specialization on nectar, there is considerable specialization for pollen and it occurs in bees. Host specificity for pollen is the most common form of specialization in bees. Many bee species restrict pollen foraging throughout their geographic range to a single plant genus, tribe, subfamily or family (Linsley & MacSwain, 1958; Wcislo & Cane, 1996). Pollen specialists or oligophages range from 60% of all pollen collecting bee species in the warm deserts of California, to 30% in central and northern Europe and subtropical Brazil, and 15-20% in Finland and Sweden (references cited in Minckley & Roulston, 2006). One might suspect that being a pollen specialist may make oligolectic bees more vulnerable but this does not appear to be true for a number of reasons. Pollen specialization for particular taxa of plants (the extreme being monolecty, the use of a single plant species for pollen) is exceedingly rare among bees (Minckley & Roulston, 2006). The pollen plants visited by most oligolectic bees are usually among the most abundant and predictable pollen resources in the environment, and these plants have simple flowers and are shared by many generalist bees. These include Larrea tridentata (DC.) Coville (Zygophyllacceae) and Helianthus species in North America (Minckley & Roulston, 2006).

Oligolectic bee pollinators of orchids may not be common except in Orphys species in the Mediterranean region (See Vereecken, 2009; Dafni et al., 2010 this volume and references therein). The Eurasian red helleborine orchid, Cephalanthera rubra (L.) L.C. Rich., is pollinated by a few species of Chelostoma bees (Megachilidae) which collect pollen for their brood almost exclusively from bellflowers (Campanula) (Nilsson, 1983). Yellow and brown donkey orchids (Diuris maculata R.Br. and other similarly colored Diuris) in Australia are pollinated by colletid bees in the genera Leioproctus and Trichocolletes (Beardsell, 1986). These bees are thought to be pollen specialists on the so-called bacon and egg peas in the genera Daviesia and Pultenaea (Beardsell, 1986). The inability to precisely identify the Leioproctus and Trichocolletes bee species involved limits our understanding of the degree of their pollen specialization (Peter Bernhardt, personal communication). The loss or reduction in the pollen host plants of oligolectic bee pollinators of orchids will likely mean a corresponding reduction in the pollinators. In the case of the highly specific pseudocopulatory pollinators of Orphys species, this could result in the loss of the orchids.

Oil-Collecting Bees

Oil-collecting bees gather the oil rewards from particular flowers to provision their brood cells and are thus closely tied to oil bearing flowers (Buchmann, 1987; Steiner & Whitehead, 1991). Oil-collecting bees belong to two bee families and are important specialist pollinators of orchids. Melittid bees in the genus Rediviva are pollinators of South African orchid species in the genera Diascia and Bowkeria (Steiner & Whitehead, 1991; Pauw, 2006), Pterygodium and Corycium (Pauw, 2006). These South African orchids have oil-reward flowers so are able to provide oil for their oil-collecting bee pollinators. The Athophorine of the Apidae are Neotropical and subtropical Neartic bees with a number of genera of which Centris is the most widespread and speciose (Michener, 2000). Centris species are pollinators of rewardless orchids in the genus Oncidium sensu-lato (Dodson, 1962; Ackerman & Montero-Oliver, 1985; Damon & Cruz-Lopez, 2006; Pemberton, 2008) and Cyrtopodium (Pemberton & Liu, 2008a, Pansarin et al., 2009). These Centris pollinators depend primarily on oil of the many reward flowers of plants that belong to the Malpighiaceae. Pemberton and Liu (2008a) found that fruit set in Cyrtopodium punctatum (L.) Lindley is much higher in plants growing near oil-reward species of Malpighiaceae than in plants growing where Malpighiaceae were sparse. Brysonima lucida (Sw.) DC., the only native malpighiaceous plant in southern Florida, is a pine rockland habitat specialist which has been reduced with loss of this habitat due to urban development (Pemberton & Liu, 2008a). This reduction of the only oil-reward plant for Centris errans Fox in natural areas, probably has resulted in a reduction in the bee's abundance and its pollination services for Cyrtopodium punctatum. Carmona-Diaz and Garcia-Franco (2009) have found similar facilitation of a pink flowered Oncidium by Malpighia glabra L. in Mexico.

Both Oncidium sensu lato and Cyrtopodium orchids appear to mimic oil-reward species belonging to the Malpighiaceae (Pemberton, 2008; Pemberton & Liu, 2008a; Pansarin et al., 2009), although this has not yet been demonstrated. The pollination of few of these orchids have been studied. The appearance of Oncidium and Cyrtopodium orchid flowers suggests that many if not most are pollinated by oilcollecting bees and are Batesian mimics of oil-reward flowers in the Malpighiaceae. Oil-reward flowers, however, also occur in several South American Oncidium, and in species of Lockhartia, Ornithocepalus, Stigmatostalix and Trichocentrum (Whitten et al., 2000; Silvera, 2002; Stpiczynska & Davies, 2008). Mullerian mimicry is probably involved in these orchids and the Malpighiaceous species they resemble (Silvera, 2002), an idea supported by similarity in chemical components in the floral oils of Byrsonima intermedia Ad. Jussieu and some oil-reward Oncidium species (Reis et al., 2007). These neotropical orchid-oil-reward flower systems could involve large numbers of orchids because there are ca. 600 Ochidium sensu-lato species and 44 Cyrtopodium species (Alrich et al., 2008).

Fragrance Oil Collecting Bees

Almost 200 species of orchid bees are the exclusive pollinators of nearly 700 specialized orchids in the neotropics (Dressler, 1982). This well-known mutualism involves orchids, called perfume orchids, which produce species-specific blends of floral fragrances, and male orchid bees, which collect and use these fragrance compounds during their courtship (Dodson et al., 1969; Cameron, 2004; Roubik & Hanson, 2004; Eltz et al., 2005). All of the orchids in the tribes Catasetinae, Stanhopeinae, Lycastinae and Zygopetalinae are participants in this pollination mutualism with male orchid bees (Dressler, 1993). The naturalization of a Mesoamerican orchid bee, Euglossa viridissima Friese, in Florida, where no perfume orchids occur except for uncommon ornamentals, led to the understanding that orchid bees don't need their orchid mutualists (Pemberton & Wheeler, 2006). The males of this orchid bee collect sufficient amounts of the required chemicals for their courtship from aromatic leaves and other sources and are as abundant in Florida as in their native range (Pemberton & Wheeler, 2006). The orchid bee-perfume orchid mutualism is therefore facultative for the bees but obligatory for the orchids. The fact that orchid bee abundance is not determined by their perfume orchid mutualists suggests that if perfume orchids become rare their pollinators will not be affected and can maintain a presence as essential pollinators. The bees should maintain a presence even if their perfume orchids are lost in an area and would be available if their perfume orchid mutualist(s) are restored.

Non-perfume orchids such as, Sobralia, Vanilla and Guarianthe (formerly Cattleya) and other orchids are often pollinated by female and sometimes male orchid bees (Dressler, 1993; Pemberton, 2007) seeking nectar. This type of euglossine pollination probably benefits from the independence of the bees from perfume orchids. Otherwise their pollination success of non perfume orchids would be dependent on the presence and abundance of particular perfume orchids.

Floral Resin Collecting Bees

Female orchid bees collect the resin rewards from the flowers of species of Dalechampia (Euphorbiaceae) and Clusia (Clusiaceae) to construct their brood cells (Roubik & Hanson, 2004). When Euglossa viridissima encounters the flowers of these resin reward flowers in Florida, it intensively collects resin from the flowers, pollinating them in the process (Pcmberton & Liu, 2008b). Floral resins, however, do not appear to be an essential resource for the bees because Dalechampia and Clusia species are relatively uncommon in Florida yet the bees are abundant, indicating that they are probably obtaining the needed resin from other sources such as trees. An apparent resin-reward pollination system also occurs in some tropical American orchids. Maxillaria cerifera Barb. and M. friedrichsthalii Rchb.f. have resin secretions on the callus and lips of their flowers (Flach et al., 2004), which are presumed to be rewards for female bees that collect the material for nest building. Although the pollinators of these orchids are unknown, Maxillaria species are often pollinated by stingless bees (Melipona and Trigona species) (Roubik, 2000), and Meloipinine bees are well known to use resin in their nest construction (Michener, 2000). It is unknown how important these resins might be to the bees but the orchids may have too limited a presence to make their resin important. Maxillaria picta Lindl. and M. madida Hook. have glossy, dark lips and calli that appears wet with oil or resin, but produce no obvious secretion, in what may be a case of deceit of resin or oil-collecting bees but pollination data and chemical analyses are lacking (Mark Whitten, personal communication).

Predator Pollinators

Many predaceous insects are highly specialized to particular prey types. Some orchids have evolved specialized pollination systems in which they mimic specific prey to attract predators for pollination. Hoverflies (Syrphidae) are the specialist pollinators of some Paphiopedilum slipper orchids in tropical Asia (Atwood, 1985; Banziger, 1996; Shi et al., 2007), in brood site pollination, in which female flies are attracted to aphid-like markings or honey dew-like shining areas on the flowers. While investigating suitable oviposition sites on the orchid, the flies fall into the lip traps of the orchids, and pollinate the flowers by contacting the stigma and an anther prior to escaping from small openings at the top rear of the lip. Examples include" P. villosum (Lindl.) Stein, which is pollinated by six hoverflies in Thailand (Banziger, 1996); and others that depend on single species of hoverfly such as P. rothschildianum (Rchb. f.) Stein on Dideopsis aegrota (Fabricius) (Atwood, 1985) in Borneo, and P. dianthum (T. Tang and F.T. Wang) on Episyrphus balteatus (De Geer) in China (Shi et al., 2007). These hoverflies lay their eggs in or near aphid colonies or aphid honey dew secretions because their larvae only consume aphids. The reproductive fates of these and probably other Paphiopedilum orchids depend on the presence and abundance of the aphid prey for their hoverfly pollinators. The reduction of wildflower, weed and hedgerow habitats can reduce both aphid prey and pollen needed for female hoverflies to mature their eggs (Landis et al., 2000). Barriers such as dense tree plantings have been found to inhibit the movement of hoverflies, including Episyrphus balteatus (Wratten et al., 2003), the pollinator of P. dianthum.

Wasps belonging to several families of Hymenoptera are specialized predator pollinators of orchids. These wasps also have specific prey types which adult females hunt, sting to paralyze, and place in their nests for use as their larval food provision. Disa sankeyi Rolfe was found to be pollinated almost exclusively by Hemipepsis spider hunting wasps (Pompilidae) m South Africa (Johnson, 2005). Wasps in the family Pompilidae only hunt and provision spiders. A Chinese hornet (Vespa bicolor) was recently been found to be the only pollinator of Dendrobium sinense on Hainan Island (Brodmann et al., 2009). The floral scent of D. sinense mimics the alarm pheromone of the Chinese honey bee Apis cerana Fabricius. Vespa bicolor is an important pest of A. cerana colonies (Ranabhat & Tamrakar, 2008). Predation of A. cerana may increase V. bicolor populations and reinforce the attracting quality of the A. cerna alarm pheromone and the attractiveness and reproductive success of the orchid. Vespa species are commonly eaten in China (personal observation) and used in traditional medicine (Ding et al., 1997). If such uses of Vespa species also occur in Hainan, it could lead to the reduced availability of V. bicolor as a D. sinense pollinator.

Parasitoid Pollinators

Insect parasitoids comprise a diverse assemblage of unrelated insects involving primarily the wasps and true flies (Hymenoptera and Diptera). Parasitoid larvae develop on or inside the developmental stages of their insect prey, which die after the parasitoid larvae are fully grown and/or exit from the bodies of their prey hosts. Female adult parasitoids locate and lay their eggs in or on the prey (typically prey larvae, but also the eggs and pupae of their prey). The majority of parasitoids are specialized with regard to prey types (Clausen, 1940), and can have single host species. Some parasitoids are highly specialized pollinators of nectarless orchids through pseudocopulation. In pseudocopulation, the orchid floral fragrances mimic the sex pheromones of the females, attracting the males of the same species which pollinate the flowers while attempting to mate with them (Kullenberg, 1961; Stoutamire, 1979; Borg-Karlson, 1990; Schiestl et al., 1999; van der Cingel, 2001). The deception can be so precise that some male wasps even ejaculate on the orchid flowers (Coleman, 1928; Gaskett et al., 2008). Extreme specificity appears to be the rule in deceptive orchids that mimic the species-specific sexual traits of female insects (Nilsson, 1992).

Pseudocopulatory pollination by wasp parasitoids has evolved in many groups of terrestrial orchids in Australia (Dafni & Bemhardt, 1990; Stoutamire, 1979). Orchids in the genus Chiloglottis are pollinated through the sexual deception of male wasps mainly from the genus Neozeleboria (Tiphiidae: Thynninae). The orchids mimic both the appearance and sex pheromones of wingless female thynnines (Mant et al., 2002). Male thynnine wasps of various genera also pollinate species of all or most species of Caleana (flying duck orchids-7 species), Caladenia (spider orchids and others-250 species), Chiloglottis (27 species), and Drakaea (hammer orchids-9 species), (Peakall, 1990; Adams & Lawson, 1993; van der Cingel, 2001; Alrich et al., 2008). Thynnine wasps are parasitoids of "subterranean scarab larvae (Riek, 1970), and adult males have been recorded to feed pollen, often from plants in the Myrtaceae, to the wingless females (Maelzer, 1962). Some of the scarab hosts of thryinnine wasps are pests of improved pastures (Maelzer, 1962), and thus subject to management that tan limit their numbers or that of the parasitoids.

Perhaps the most famous wasp enticed by pseudocopulatory orchids is the so called orchid dupe, Lissopimpla excelsa (Costa), the sole pollinator of all five Cyrptostylis species in Australia (van der Cingel, 2001). This ichneumonid wasp parasitizes the larvae tobacco budword, Helicoverpa virescens (Fabricius), and armyworms (Queensland Government, 2009), all noctutid moths that are serious crop pests in Australia and elsewhere. The orchid dupe's hosts are probably not limiting, although L. excelsa is subject to insecticides and the disturbance of row crop agriculture which may limit its abundance and availability as a pollinator. Calochilus (beard orchids-11 species) are pollinated through pseudocopulation by Campsomeris species of scoliid wasps, which like thrynnine wasps, parasitize scarab larvae (Riek, 1970).

A South American scoliid wasp also in the genus Campsomeris pollinates the subtropical terrestrial orchid Geoblasta penicillata (Rchb.f.) Hoehne ex M.N.Correa (Chloraeinae) (Cioteka et al., 2006). This parasitic wasp probably also uses scarab larvae as hosts. The importance of scarab larvae as an essential biotic resource for many specialist orchid pollinators is hot generally recognized, but few specific pollinator resources are known or recognized.

Tachinid fly parasitoids may be pseuocopulatory pollinators of some, perhaps many, of the species of telipogninine orchids in the South American tropics (van der Pijl & Dodson, 1969). This subtribe includes ca. 176 species in Trichoceros, Stellilabium, Telipogon (Alrich et al., 2008). Dodson (1962) observed copulation attempts of male flies to the flowers of Trichoceros antennifera [H.B.K.] Kunth but did not document pollen removal or deposition. Many of these orchids have bristly tachinid fly-like appearances and colors. All of the numerous species of tachiniid flies are parasitoids, and they have a range of host specificities, from species in multiple insect orders to single species (Arnaud, 1978). Even if more was known about the species of tachinid flies involved as probable pollinators of telipogoninine orchids, it is unlikely that much will be known about what their host insects may be.

Long-tongued tanglewing files (Diptera: Nemestrinidae) belonging to two genera pollinate rewardless Disa species, Disa draconis (L. f.) Sw., and two other Disa species in South Africa (Johnson & Steiner, 1997). The files pollinate these deceptive Disa species hot via pseudocopupulation but while seeking nectar. Tanglewing flies belonging to two genera also pollinate two Browleea orchid species which have foral nectar. No details of the life cycles of the South American tanglewing flies are known, but the few studied tanglewings are parasitoids on locusts (Orthoptera Acrididae) (Goldblatt & Manning, 2000).

Blood Feeding Fly Pollinators

Long-tongued robberflies (Diptera: Tabanidae) seeking nectar also pollinate Disa draconis and D. harveiana Lindl. in South Africa (Johnson & Steiner, 1997). Female robber flies require a blood meal from suitable mammal hosts before they tan lay eggs, while their aquatic larvae are carnivorous (Goldblatt & Manning, 2000). Mosquitos (Aedes communis DeGreer and A. canadensis Theobold) pollinate Habenaria obtusata (Banks ex Pursh) Richards in North America (Thien, 1969). Aedes canadensis rarely feeds on people but feeds abundantly on turtles (DeFoliart, 1967), which means that this Habenaria is indirectly dependent at least to some degree on reptiles. Conservation effort to preserve blood feeders of vertebrates would be challenging, especially with the South African tabanid pollinators of Disa species about which so little is known (Goldblatt & Manning, 2000). Such potential conservation efforts could well be resisted by their human vertebrate hosts.

Fungus Gnat Pollinators

Bradysia floribunda Mohrig, a dark-winged fungus gnat (Diptera: Sciaridae), is the pseudocopulatory pollinator of Lepanthes glicensteinii Luer (Pleurothallidinae) in Costa Rica (Blanco & Barboza, 2005). Other species of dark-wing fungus gnats were observed visiting three other species of Lepanthes in Costa Rica (Blanco & Barboza, 2005), suggesting that sciarid species may be pseudocopulatory pollinators of Lepanthes in tropical America, where more than 900 species occur (Alrich et al., 2008). Sciarid larvae are usually round in rotting vegetation or highly organic soils, but one Bradysia is reputed to attack plants of glasshouse plants (Colless & McAlpine, 1970).

Greenhood orchids (Pterostylis) native to Australia and New Zealand are pollinated by fungus gnats in a family (Mycetophilidae), closely related to the Sciaridae. These flies also appear to be pseudocopulatory pollinators of the orchids (Bernhardt, 1995a,b; Jones & Clements, 2002; Lehnebach et al., 2005). Pollination by pseudocopulation in this group is supported by observations of male fungus gnats flying directly towards the labellum with their genitalia exerted (Jones & Clements, 2002). Listera ovata (L.) R. Br. (Listerinae) growing in northern California is another orchid pollinated by mycetophilids and other small insects apparently attracted by the flower's nectar and fragrance (Ackerman & Mesler, 1979). Mycetophilid larvae are usually round associated with fungi, but some are predaceous (Colless & McAlpine, 1970), and few have been studied. Some fungus feeding species tend toward monophagy (Hackman & Meiander, 1979). The highest species richness and individual species abundance of mycetophilids has been round to be associated with old growth forests (Okland, 1996). Forest management practices (e.g. clear cut, and selective harvest) reduce their abundance (Okland, 1994), so protection of natural forests is considered the best conservation measure for the mycetophilids (Okland, 1996).

Carrion Fly Pollinators

Many of the ca. 1,800 Bulbophyllum species have flowers with putrid odors and brown-purple colors which attract carrion flies (Diptera: Calliphoridae) as pollinators in a syndrome called sapromyophily (van der Cingel, 2001; Alrich et al., 2008). Differences in the odors among foul smelling Bulbophyllum species, some smelling of rotten fish and others of dead mammals, suggest that different species are attracting a somewhat different range of flies. The carrion flies themselves can be somewhat specialized with regard to carrion types used, such as small mammals or invertebrates, and may differ by season (Kneidel, 1984). Disturbance or simplification of habitats may reduce or shift carrion types and in mm influence the availability of carrion fly pollinators for their dependent orchids.

Alkaloids Seeking Butterflies

Neotropical orchids, Epidendrum paniculatum Ruiz and Pavon species complex, are pollinated by butterflies, especially clear wing ithomine butterflies, which seek pyrrolizidine alkaloids that the flowers produce or mimic (DeVries & Stiles, 1990). Ithomiine butterflies, distasteful models in neotropical mimicry complexes, show warning coloration and are usually rejected by both vertebrate and invertebrate predators (Brower & Brower, 1964; Brown, 1984). The butterflies are toxic because they collect and sequester pyrrolizidine alkaloids as adults from flowers (mostly Eupatorieae in the Asteraceae) and decomposing foliage (mostly Boraginaceae) (Brown, 1984). Pyrrolizidine alkaloids are also important in the reproduction of the Ithomiinae (Brown, 1984). The Monarch butterfly (Danaus plexippus L.), another toxic model in a mimcry complex, is a frequent pollinator of the neotropical Epidendrum ibagense and E. radicans (Boyden, 1980). It also collects and sequesters pyrrolizidine alkaloids (Kelley et al., 1987), as well as cardenolide-based chemicals that the larvae obtain during their consumption of Asclepias species (Brower et al., 1988). The need for orchid pollinating butterflies (and euglossine bees--see the section above) to collect specific chemicals from sources unrelated to their sources of nutrition illustrates how subtle and complex resource needs can be.

Herbivorous Pollinators

Most herbivorous pollinators of orchids are Lepidoptera-butterflies and moths. Butterflies and most orchid pollinating moths consume the foliage of plants during their larval period. The host plant specificities of Lepidoptera vary from highly generalized feeders that consume plants from many different orders and families to specialists that are limited to plants from a single family, a few related plants, or in some cases a single plant species (Bernays & Chapman, 1994).


The ithomine butterfly pollinators of Neotropical Epidendrum paniculatum complex orchids are limited to the Solanaceae for their larval hosts, except for some primitive species which use a few Apocynacae (Trigo & Brown, 1990). The monarch butterfly pollinators of Epidendrum species use milkweeds (Asclepias species, Asplepidaceae) as larval hosts (Malcom & Brower, 1989). Heliconius erato phyllis (L.) is reported to pollinate Habenaria pleiophylla Hoehne & Schlechter in Brazil (van der Cingels, 2001). Heliconius species, often called passionvine butterflies, feed only on Passiflora species. Heliconius erato phyllis larvae are able to feed on a number of Passiflora species but prefer Passiflora misera Kunth on which they produce larger more fecund females (Rodrigues & Moreira, 2002), that can increase population sizes and their availability as orchid pollinators. The sole pollinator (Aeropetes tulbaghia) of South Africa's Disa uniflora uses only two species of indigenous grasses, Hyparrhenia hirta (L.) Stapf. and Ehrharta erecta Lam., as larval hosts (Migdoll, 1997). Hyparrhenia hirta is probably the most popular thatching grass used in South Africa. (

The swallowtail butterfly Papilio palamedes Drury is the main pollinator of Platanthera ciliaris (L.) Lindley in the coastal plain of the southeastern United States (Robertson & Wyatt, 1985). This butterfly's caterpillars feed on Persea species and a few other members of Lauraceae (Scott, 1986). Recently, a Chinese ambrosia beetle, Xleborus glabratus Eichhoff, and the fungus, Raffaelea sp., it transmits have naturalized in the southeastern United States (Mayfield & Thomas, 2006). The fungal infection called laurel wilt, is causing high levels of death of Persea species and other Lauraceae (Mayfield & Thomas, 2006). The reduction or potential loss of these host plants will probably result in concurrent reduction of P. palamedes and its pollination of the yellow-fringed orchid.


Moths are probably more important and specialized orchid pollinators of orchids than are butterflies. Angraecoid orchids in Madagascar and Africa and their hawkmoth pollinators (Sphingidae) are the best known. The star orchid of Madagascar, Angraecum sesquipedale Thou., is pollinated by a single hawkmoth, Xanthopan morganii predicta Walker (Wasserthal, 1997; Nilsson, 1988) whose existence was famously predicted by Darwin (1862). Angraecum arachnites Schltr. is also pollinated by and adapted to a single species of hawkmoth, Panogena lingens (Butler) in Madagascar (Nilsson et al., 1985), which also pollinates Aergangis and Jumellea angraecoid orchids on the island (Nilsson et al., 1987). Most of the 300 plus species of angraecoid orchids in Madagascar and Africa (Alrich et al., 2008) exhibit sphingophilous flowers with white colors, nectar spurs with nectar and nocturnal fragrances, and appear to be hawkmoth pollinated. The extraordinary number and diversity of long-spurred Orchidaceae in Madagascar appears to be a direct coevolutionary consequence of an Old-World-unique diversity of long-tongued archaic Sphingidae that has persisted in this isolated land (Nilsson et al., 1985).

The famous ghost orchid, the angraecoid Dendrophylax lindenii (Lindley) Bentham ex Rolfe [Polyrrhiza lindenii (Lindl.) Cogn.] of Florida and Cuba, has the same floral syndrome as angraecoid orchids of Madagascar, and appears to be pollinated in Florida by the hawkmoth Cocytius antaeus (Drury), as suggested by Luer (1972). What appears to be the moth has been videotaped visiting the orchid by Chris Aggie, but a scientific study on its pollination has yet to be conducted. Cocytius and Xanthopan are closely related (Kawahara et al., 2009) as are their larval host plants. Xanthopan morganii develops on Annona and Uvaria species (Annonaceae) in East Africa, while C. anataeus is limited to a single species, Annona glabra L., in Florida (Robinson et al., 2009). Sphinx moths can have broad or narrow larval host plant specificities. In contrast to X. morganii and C. anataeus, sphinx pollinators with narrow host plant ranges that can depend on one or a few plants, Agrius convolvuli (L.), that pollinates many African angraecoid orchids (Martins & Johnson, 2007), is a broad generalist (Kroon, 1999). The larval host plant(s) of the important angraecoid orchid pollinator Panogena lingens are unknown (Ian Kitching, personal communication).

Bonatea speciosa L. (Habenariinae) is unrelated to angraecoid orchids but shares the sphingophilous syndrome flowers and is pollinated by two hawkmoths, Theretra capensis (L.) and to a lesser degree Hyles lineata (Fabricius) in South Africa (Johnson & Liltved, 1997). Hyles lineata has a broad host range spanning many plant families, while Thereta capensis is limited to several species in the Vitaceae including grape (Vari & Kroon, 1986).

Even though the host plant (Annona glabra) of the putative pollinator of Florida's ghost orchid (Cocytius antaeus) is very common, the moth is still rare (Orchid Specialist Group, 2009). Obviously there are many factors that determine the presence and abundance orchid pollinators. This review has only dealt with biotic factors in the environment and ignored abiotic factors which are also critical (New, 2009). Not covered as well are nest sites and resources, some of which are biotic (Dafni et al., 2010 this volume). Examples of nectar and pollen needs, insect prey of predators and parasitoids, chemical needs related to reproduction, and developmental host plants of orchid pollinators were given. Typically this encompassed three levels of relationships--the orchid, its pollinator and the pollinator's essential biotic resource. Absent are other trophic levels involving the predators, parasitoids, parasites, and diseases of orchid pollinating insects. Most insects have specialist parasitoids that limit their abundance and hyperparasitoids (tiny wasps) which usually limit the abundance of parasitoids. Even if the inclusion of these other tropic levels were not beyond the scope of this review, knowledge limitations would have prevented it for most insect pollinators discussed.

Conservation and Restoration of Orchid Pollinators

Specialist pollinators are members of pollination webs through their visitation of facilitation plants and other plants to obtain nectar and pollen not provided by the orchids they pollinate. Memmott (2002) recognized that pollination webs are, with regard to bees collecting pollen to provision their young, also food webs. Food web or food chain components that are specific resources of specialist orchid pollinators such as prey, parasitoid hosts, and host plants, which are essential for their developmental stages, are usually unknown or unconsidered. It is important to develop this knowledge to enable the building of food webs or food chains and then link them to pollination webs to have a more realistic picture of the players involved in orchid pollination. Identifying these participants may be key to the conservation of some orchid pollination systems.

Evidence is accruing that pollinator loss can lead to extinction of plant species (Bond, 1995). By contrast, loss of floral resources is a key threat facing pollinating insects (Kearns et al., 1998). Increased risk of pollination failure is associated with pollinators that are too few or too inconsistent, and with plants that are too specialized or too selective (Wilcock & Neiland, 2002), characteristics that occur in many orchids. Specialist pollinators are often the first casualties when ecosystems degrade (Dixon, 2009).

Climate change is a major threat to pollination services and networks (Memmott et al., 2007, Dixon, 2009), but this threat to pollinator resources is unstudied except for the implied potential losses of pollen and nectar due to plant pollinator asynchronies projected by Memmott et al., 2007. Few studies have addressed the climate change threat to orchids. The only study that I am aware of that examines the threat of climate change to an orchid community is that by Liu and Luo (2010, this volume)

Even though insects are the most diverse and abundant animals in out world, the number of restoration efforts devoted to specific insect species are modest compared to better understood groups such as mammals, birds (New, 2009) and plants. The lack of human cultural interest has limited insect restoration to a few charismatic species such as butterflies and large beetles (New, 2009). Major problems with the conservation and potential restoration of orchid insect pollinators are that most orchid pollinators are unknown and, as indicated in this review, little is known of the complex resource needs of the pollinators that are known. It is obviously better to conserve the habitats of orchids than attempt restoration which can easily fail to adequately restore the orchids and their pollinators. Because pollinators are mobile, we need to consider not only of the local scale where their services are delivered, but also the distribution of resources at the landscape scale (Kremen et al., 2007). Oil-reward orchids in Cape South African nature preserves smaller than 500 ha have lost their specialist oil-collecting bee pollinator (Rediviva peringueyi Friese), for unknown reasons, and are no longer setting fruit (Pauw, 2007). Protecting the natural habitats of orchids, especially large plant rich and pesticide-free habitats, is probably the best hope of maintaining the diverse biological resources and the complex ecological interactions to enable the continuation and viability of orchid pollinator populations.

DOI 10.1007/s 12229-010-9047-7

Acknowledgements Yi-bo Luo and Hong Liu invited me to present a talk on resource needs of orchid pollinators at the 1st Guangxi International Orchid Conservation Symposium in Guangxi Province, China in May 2009, which was the genesis of this paper. Phillip Seaton provided valuable discussion. Amots Dafni, Mark Whitten, and Hong Liu provided helpful reviews of the manuscript. Rachel Taylor provided technical editorial assistance.

Published online: 31 March 2010

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Robert W. Pemberton (1,2,3)

(1) Center for Tropical Plant Conservation, Fairchild Tropical Botanic Garden, c/o 2121 SW 28th Terrace, Fort Lauderdale, FL 33312, USA

(2) Florida Museum of National History, c/o 2121 SW 28th Terrace, Fort Lauderdale, FL 33312, USA

(3) Author for Correspondence; e-mail:
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Author:Pemberton, Robert W.
Publication:The Botanical Review
Article Type:Report
Geographic Code:1USA
Date:Jun 1, 2010
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