Selbyana 29(1): 6-19. 2008. THE USE OF ORCHID POLLINIA OR POLLINARIA FOR TAXONOMIC IDENTIFICATION RODRIGO B. SINGER* Depto Botanica, Instituto de Biociencias, Universidade Federal do Rio Grande do SuI, Av. Bento Gon\ialves 9500, RS 91501-970, Porto Alegre, Brasil. Email: [email protected] BARBARA GRAVENDEEL Nationaal Herbarium Nederland, Universiteit Leiden, P.O. Box 9514 Leiden, The Netherlands HUGH CROSS Nationaal Herbarium Nederland, Universiteit Leiden, P.O. Box 9514 Leiden, The Netherlands SANTIAGO R. RAMIREZ Museum of Comparative Zoology, Harvard University, 26 Oxford St., Cambridge, MA 02138, USA ABSTRACT: The structural variation of pollinia and pollinaria in Orchidaceae is discussed. Pollinia and polJinaria are restricted to two (of the five) orchid subfamilies: Orchidoideae and Epidendroideae. The attributes of pollinia and pollinaria of these subfamilies are commented on and discussed. Pollinia and pollinaria also occur in the plant family Apocynaceae, in the subfamilies Asclepiadoideae and Periplocoi­ deae, but these are structurally different from those found in the family Orchidaceae. A number of mor­ phological features of orchid pollinaria are informative taxonomically and ecologically. These features are briefly discussed and examples are given. The recent description of the first unequivocal fossil orchid (Meliorchis caribea; Orchidoideae: Goodyerinae) from a pollinarium attached to an insect pollinator is briefly discussed. This example is used to illustrate the use of informative morphological and palynological characters. A fascinating new perspective, the possibility of species identification using DNA sequencing from pollinia or pollinaria attached to pollinators, is also discussed. Suggestions and future avenues of research focusing on orchid pollination are given. Key words: DNA barcoding, ecology, morphology, Orchidaceae, pollen, pollinia, pollinaria, pollination, taxonomy INTRODUCTION 1993; Judd et al. 2008). Although a significant part of the median stigmatic lobe normally be­ A Brief Overview of Orchid comes non-receptive (sterile), it produces secre­ Floral Features tions or tissues that are involved in the pollina­ In its current delimitation (Cameron et al. tion process (see below). This modified median 1999; Chase et al. 2003) the orchid family en­ stigmatic lobe is widely known as rostellum compasses about 24,190 spp. distributed among (Dressler 1981, 1993; Judd et aI, 2008). five subfamilies. The phylogenetic relationships Most orchids characteristically package pollen between these subfamilies are becoming fairly into discrete units that are removed as a single well understood, and are summarized in FIGURE unit from the flower during the pollination pro­ 1. Orchids are remarkable for a number of rea­ cess (FIGURE 2). In functional terms, this means sons. Being monocots, they present a 3-merous that the whole pollen content of a flower is re­ perianth made up by three sepals and three pet­ moved during a single pollinator visit. These als. The median petal is normally bigger, more pollen packages are called pollinia (singular: colored, dotted and/or ornamented. This floral pollinium). We have to make a short digression part is widely known as lip or labellum. The here: pollinia plus any secretions and/or tissues ovary is inferior and the androecium (of 1-3 fer­ that aid in the removal of the structure from the tile anthers) and gynoecium are fused into a sin­ flower are collectively known as pollinarium gle structure called gynostemium or column. (plural: pollinaria) (Dressler 1981, 1993; En­ There are three stigmatic lobes (Dressler 1981, dress 1994). The terms pollinia and pollinaria (singular: pollinarium) are often used inter­ * Corresponding author. changeably, but this is incorrect from a morpho- 6 SINGER ET AL.: ORCHID POLLINIA 7 _- Epidendroideae (pollinia entire) D 1 Orchidoideae (pollinia friable) 2 Cypri ped ioideae (pollen agglutinated) 1 ..-- Vanilloideae ~ (pollen agglutinated) ..- Apostasioideae (pollen loose) I = number of fertile anthers FIGURE 1. Cladogram of Orchidaceae, depicting phylogenetic relationships between subfamilies (modified from Chase et al. 2003) and patterns of pollen aggregation. A. Cleistes libonii (Vanilloideae), B. Paphiopediulum insigne (Cypripedioideae), C. Pelexia orobanchoides (Orchidoideae), D. Cattleya loddigesii (Epidendroideae). 8 SELBYANA Volume 29(1) 2008 in the neotropical species of the genus Bulbo­ phyllum (notice, however, that more morpholog­ ically complex situations may also be found in this genus) as well as within the Asian genus Dendrobium and close relatives (Dressler 1981, 1993). Pollinia devoid of any additional stalks A constitute the so-called "naked pollinia" (Dress­ We r ler 1981, 1993) and are, as explained above, re­ moved with the aid of rostellar secretions. 2mm '0 Most orchids, however, develop a number of additional stalks that are functional during the ~~ H pollination process. Tail-like, elastic pollinium I projections made of viscin and abortive pollen are widespread features. These projections are J known as caudicles or caudiculae, which can be very reduced and inconspicuous to the naked eye. Pollinia provided with caudicles and no ad­ ditional stalks are widespread, for instance, ii~ within several genera of the subtribe Pleuroth­ 1 allidinae (e.g., Dryadella, Specklinia, Acianth­ . L era, etc.) and Laeliinae (e.g., Cattleya, Isabelia, ' Leptotes, Pseudolaelia, most Sophronitis spp. FIGURE 2. Pollinia and pollinaria of twelve sym­ and others) (Dressler 1981, 1993) (FIGURE 2E­ patric Orchidaceae, occurring in Araucaria forests in G). In these orchids the caudiculae are moist­ Southern Brazil. (A-D) belong to the subfamily Or­ ened with rostellar secretions that glue onto the chidoideae and display friable (divisible) pollinia. (E­ pollinator's body surface (Dressler 1981, 1993). L) belong to the subfamily Epidendroideae and display In many Orchidaceae a further step of mor­ entire pollinia. A. Microchilus austrobrasiliensis phological complexity is achieved when part of (Goodyerinae). B. Veyretia simplex (Spiranthinae). C. the rostellum becomes not only adhesive, but Cyclopogon diversijolius (Spiranthinae). D. Habenaria parviflora (Orchidiinae). E. Isabelia pulchella (Laeli­ also detachable. This part is often a pad-like inae). F. Leptotes unicolor (Laeliinae). G. Acianthera structure commonly known as viscidium (plural luteola (Pleurothallidinae). H. Campylocentrum aro­ viscidia) (Dressler 1981, 1993). In these orchids, maticum (Angraeciinae). I. Zygostates dasyrrhiza (On­ the viscidium is responsible for gluing the pol­ cidiinae). J. Brasiliorchis picta (Maxillariinae). K. On­ linarium to the pollinator's body surface. In the cidium loefgrenii (Oncidiinae). L. Oncidium paran­ simplest case, the pollinaria consist of pollinia aense (Oncidiinae). connected by caudicles to a viscidium (FIGURE 2A-D, H-L). There are, however, several vari­ ations. In many Orchidaceae, an additional stalk logical perspective. The term pollinia should be may appear between the pollinia (and caudicles) restricted to the very pollen-bearing structures of and the viscidium. These stalks are often elon­ the pollinarium (Dressler 1981, 1993; Endress gate and are collectively known as stipes (Greek 1994), and pollinarium to the entire translatory for "column") (FIGURE 2H, I, K, L). The con­ unit or complex involving both fertile (pollinia cept of stipes, however, involves at least three and pollen content) and sterile (various pollini­ different structures. In many cases stipes consist um stalks) tissues (Dressler 1981, 1993; Endress of an epidermal layer of column sterile tissue 1994). that becomes detachable (Dressler 1993). This is The basic pollinia number for the orchid fam­ the commonest kind of stipes, and the name te­ ily as a whole is four, in agreement with the four gula (Greek for "roof") has been proposed for pollen-sacs usually found in the rest of angio­ such structures (Dressler 1981, 1993). The name sperms (Dressler 1981, 1993). Within Orchida­ hamulus (plural: hamuli) has been proposed for ceae, however, secondary reductions or increas­ stalks derived from a projection of the rostellum es are common and widespread (Dressler 1981, (Dressler 1981, 1993). This kind of stalk is quite 1993) (FIGURE 2). It should be noted that pollinia restricted and has been reported for a very few alone carmot be removed from the anther. In the taxa (Dressler 1993). Finally, a third kind of simplest case, pollinia are removed along with stalk (with no formal name so far) was recently rostellar secretions that stick to the pollinator's described from Christensonella uncata (Maxil­ body surface. During the pollination process, the lariinae) (as Maxillaria uncata) and related spp. rostellum is disturbed and a glue-like secretion In these orchids, the stalk between the pollinia is released. This floral mechanism is widespread and the viscidium consists of a long, straight, SINGER ET AL.: ORCHID POLLINIA 9 TABLE 1. Pollinia from museum accessions from which nrITS and tmL-tmF sequences could be obtained. Collection Species Voucher year Preservation NCBI accession Catasetum fimbriatum FLAS 181451 (pollinia from herbarium) 1986 Air dried EU441210 Catasetum saccatum Gerlach 1771 (pollinia on insect) 1999 Unknown EU441204, EU441214* Coelogyne fimbriata Leiden cult. 923836 (fresh pollinia) 2004 Air dried EU441205 Leiden cult. 30759 (fresh leaves) 1997 Air dried AF302745 Coelogyne swaniana Leiden cult. 27645 (fresh pollinia) 2004 Air dried EU441206