SciELO - Scientific Electronic Library Online

 
vol.33 issue4Sustainable production of bioactive alkaloids in Psychotria L. of southern Brazil: propagation and elicitation strategiesUpdates on extratropical region climbing plant flora: news regarding a still-neglected diversity author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

Share


Acta Botanica Brasilica

Print version ISSN 0102-3306On-line version ISSN 1677-941X

Acta Bot. Bras. vol.33 no.4 Belo Horizonte Oct./Dec. 2019  Epub Nov 25, 2019

https://doi.org/10.1590/0102-33062019abb0111 

Review

A literature review of the pollination strategies and breeding systems in Oncidiinae orchids

1 Instituto de Biociências, Universidade Federal do Rio Grande do Sul, 91509-900, Porto Alegre, RS, Brazil


ABSTRACT

Oncidiinae is an exclusively Neotropical orchid subtribe with about 1600 described species and an impressive array of vegetative and floral morphological adaptations. We present the results of a literature survey on the pollination strategies and breeding systems of this orchid subtribe. The flowers are pollinated by a wide range of insects (mostly bees) and, sometimes, hummingbirds. Several genera reward their pollinators with floral resources such as oils, nectar or perfumes. Whereas pollination by oil-gathering bees likely evolved several times within Oncidiinae, exclusive pollination by perfume-gathering male Euglossine bees is likely restricted to a set of closely-related genera. Pollination by food or sexual deception is also present within the subtribe. Up to date, the pollen-vectors of the 92 species of Oncidiinae studied so far are as follows: 84.7 % are pollinated by bees, 6.5 % by wasps, 4.3 % by hummingbirds, 3.2 % by butterflies and 3.2 % by flies. Oncidiinae orchids are preferentially self-incompatible (69.4 % of the species studied so far), some may also present protandry as a mechanism to promote cross-pollination. Fruiting success is generally low. The rate of visitation with subsequent pollination is low, in general, which contributes to the low reproductive success of this plant group.

Keywords: breeding systems; deception; elaiophores; fruiting success; nectaries; Oncidiinae; orchids; osmophores; pollination strategies

Introduction

Orchid flowers and their structures have long been studied in detail by researchers from all around the world, lured by their high potential as ornamental plants (Dressler 1961; 1974; Pijl & Dodson 1966; Cingel 2001). One of the most representative orchid subtribes is Oncidiinae (Epidendroideae: Cymbidieae), which shares with Pleurothallidinae the largest numbers of species within the Neotropics (Chase et al. 2009; 2015). In its current circumscription, the subtribe holds 65 genera and about 1600 species (Chase 2009; Neubig et al. 2012; Chase et al. 2015). Givnish et al. (2015) dated the divergence time of the Oncidiinae to approximately 20 my. The geographical distribution of the subtribe ranges from southern United States and northern Mexico to southern Brazil and northern Argentina. They comprise terrestrial or epiphytic herbs, inhabiting a wide variety of environments, from well-drained hill slopes to wetlands. They normally bear sympodial growth, uninodal pseudobulbs and distichous and bifacial leaves (Chase 2009) (Fig. 1). The flowers of Oncidiinae orchids generally feature lips much bigger than the rest of the perianth, often presenting ornamentations - the so-called “callus” or “calli” (Fig. 1) - or secretions, which serve as attractors to pollinators or floral visitors. They also may present a thickened structure on the base of the column, the tabula infrastigmatica (Fig. 1). This structure is supposed to assist in the stabilization of floral visitors, which grab the tabula while foraging for floral rewards (Dressler 1981; 1993). Lastly, it is important to highlight the presence of a complex pollinarium bearing 2 or 4 indivisible pollinia. In the practice, such pollinia prompt the transfer of all the pollinic contents during a single or very few pollination events (Dressler 1993; Singer et al. 2006; Judd et al. 2009), facilitating the monitoring of pollen-flow during pollination studies.

Figure 1  Habits, growth types and morphological features of the Oncidiinae. A. The terrestrial Gomesa hydrophila, adapted to wetlands; B. Monopodial growth and distichous leaves in an unidentified species of Fernandezia; C. Detail of pollinia (white arrow), tabula infrastigmatica (red arrow) and the callus (light blue arrow) in flower of Gomesa imperatoris-maximiliani; D. Epiphytism, uninodal pseudobulbs and sympodial growth in the “oncidioid” orchid Gomesa concolor

Convergent evolution in response to functionally similar pollinators may be responsible for similar floral traits (Fig. 2) evolving within independent clades in Oncidiinae, in particular the development of oil-bee pollination in many non closely-related taxa (Papadopulos et al. 2013). These convergences were misinterpreted by early taxonomists, a fact that created considerable taxonomic problems in the subtribe. Until the end of the last decade, the taxonomic and phylogenetic relationships among Oncidiinae genera were not clear, because several genera were usually described based upon few morphological features that were proven not to reflect the actual parental relations between the taxa (Faria 2004). In Genera Orchidacearum (Chase 2009) is presented a phylogenetic framework based on DNA analyses, with a robust generic sampling, clarifying some issues and proposing recircumscriptions in several genera. Neubig et al. (2012) produced a phylogeny based on plastid and nuclear loci of 590 species of Oncidiinae, largely corroborating the results of the previous work (Chase 2009). Oncidium, the type genus of the subtribe, has always been on debate due to the inconsistent traditional boundaries assumed over the years. In its broader delimitation, it covers more than 400 species popularly known as “dancing ladies” or “golden shower orchids”, defined by the characteristic callosity observed in the lip, resembling tumors (from the greek word “onkos” = swelling or tumor). It was not a surprise when studies involving molecular characters, such as this of Chase & Palmer (1992) using plastid DNA and this of Williams et al. (2001a; b) using plastid and nuclear DNA sequences, proved that Oncidium in a broader sense is a polyphyletic grouping. With the advent of cladistic methods allied to analyses of molecular characters, Oncidium sensu lato was recircumscribed and several species were transferred to different genera (Chase et al. 2009; Chase & Whitten 2011; Neubig et al. 2012).

Figure 2  Diversity of flowers within Oncidiinae. Note the representativeness of yellow/brown flowers (A-F), corresponding to the “oncidioid” orchids. A. Oncidium ornithorrhynchum; B. Grandiphyllum divaricatum; C. Lockhartia lunifera; D. Gomesa longipes; E. Cyrtochilum tetracopis; F. Cyrtochilum auropurpureum; G. Gomesa crispa; H. Gomesa radicans; I. Caucaea sp.; J. Miltonia regnellii; K. Rodriguezia decora; L. Fernandezia sp.  

To our knowledge, the first studies of Oncidiinae regarding aspects of reproductive biology are the preliminary observations of Darwin (1885) that paid attention on column/pollinarium structure and eventually mentions fragmentary information from his correspondent (especially Johann Friedrich Fritz Muller, that was based on Santa Catarina - Southern Brazil - and made some preliminary observations on a species of Gomesa). Much later, Pijl & Dodson (1966) compiled numerous reports. However, as already noticed for other authors (Caballero-Villalobos et al. 2017) most of these observations are limited to the mere observation of bees/hummingbirs onto flowers, without really proving that these animals acted as pollen-vectors. Indeed, some of the suggestions made by Pijl & Dodson (1966), such as the existence of pollination through pseudoantagonism need to be reappraised under a new light, owing to new evidences (see below). Many years later, Cingel (2001) published a comprehensive treatise on orchid pollination, but kept many of the preliminary (and sometimes, erroneous) inferences found in Pijl & Dodson (1966). More recently, Chase (2009) compiled all the known information up to the date and discussed some of the issues of the previously mentioned works, being a more reliable and updated source of information on pollination within Oncidiinae.

In spite of the increasing interest on the pollination biology of orchids during the last decades, an overview of the Oncidiinae orchids is still lacking. The study of the pollination biology of these plants frequently poses important problems that prevent a quick increase of the available information. Many times, these plants are rare or do not form large or accessible populations. Even when the number of individuals is large enough within a small area, plants may not flourish satisfactorily in quantitative terms (not all individuals flower) or flower irregularly, therefore not drawing sufficient attention from potential pollinators.

Methods

This compilation focuses mainly on pollination strategies, but also provides information on breeding systems and fruiting successes among the species of this subtribe. We followed the circumscription of Oncidiinae as proposed by Chase (2009) and Neubig et al. (2012). In our bibliographic revision, we considered pollinators all the visitors that were seen or captured carrying pollinaria of a given orchid species, since an insect carrying a pollinarium is very likely to be a pollinator of the species that produced the pollinarium, according to Dressler (1976). The names of plants followed The International Plant Names Index (IPNI 2019) and The Plant List (2019) and names of animals were checked at Global Biodiversity Information Facility (GBIF 2019) and Integrated Taxonomic Information System (ITIS 2019) databases. Our aims are to elucidate (1) the pollination strategies based upon the presence or absence of a given floral reward and the group of animals involved in each case; (2) the breeding systems; and (3) the fruiting success represented by the natural observed fruit set of the orchids. Results are organized based on the floral resource (or absence of it) offered by each group of orchids. At each section (strategy), we address important works regarding the subject matter; the type of resource and main chemical compounds (if applicable); the secretory structures and their locations (if applicable); the pollinators and their behaviors; studies of cases; and the group of orchids that present each strategy.

Pollination strategies

Floral oils

Elaiophores (oil-secreting glands) are present in a number of Angiosperm families (reviewed in Renner & Schaefer 2010 and Possobom & Machado 2017), mainly from the Americas, but also from Southern Africa. So far, this pollination strategy is known to occur within the families Calceolariaceae, Cucurbitaceae, Iridaceae, Krameriaceae, Malpighiaceae, Orchidaceae, Plantaginaceae, Primulaceae, Scrophulariaceae, Solanaceae and Stillbaceae (Renner & Schaefer 2010; Possobom & Machado 2017). Solitary bees of different Apidae tribes (Renner & Schaefer 2010; Possobom & Machado 2017) gather these oils and mix them with pollen, in order to nurture their larvae. From a chemical point of view, these oils are mainly acyl-glicerols and hydrocarbons (Reis et al. 2000; 2006; 2007; Reis 2005; Singer et al. 2006). Vogel (1969; 1974) was the first researcher to demonstrate the existence of elaiophores in Orchidaceae and other families of plants. The locations and features of these glands have been elucidated in anatomical (Singer & Cocucci 1999a; Alcántara et al. 2006; Pacek & Stpiczyńska 2007; Stpiczyńska et al. 2007; 2013; Stpiczyńska & Davies 2008; Davies & Stpiczyńska 2009; Aliscioni et al. 2009; Pacek et al. 2012; Blanco et al. 2013; Gomiz et al. 2013; 2014; 2017; Davies et al. 2014) and chemical (Reis et al. 2000; 2007; Silvera 2002) studies. These works described the morphological structure of the elaiophores and characterized their secretions, supporting the possibility that oil-collecting bees perform their pollination, as a result of deliberate gathering behavior (Singer et al. 2006; Torretta et al. 2011). In fact, some species produce sufficient quantity of floral oils (mainly acyl-glycerols) and offer them as a reward to pollinators (Tab. 1).

Table 1  Pollinators, floral resources and pollination strategies in Oncidiinae orchids. Reward uncertain/Stategy uncertain = We make this assumption for the studies that do not clearly indicate the gathering of a floral reward by the pollinators, and we may make inferences on the possible pollination strategy based upon floral features and closely related taxa. * = Misidentification.  

Oncidiinae species and synonyms in literature Pollination features (1) Pollinator group; (2) Floral resource aimed; (3) Pollination strategy Pollinator species References for pollinators and floral resources
Aspasia principissa Rchb.f. (1) Euglossini bees (2) Nectar, absent (3) Deception of nectar Eulaema bombiformis (Packard, 1869); Eulaema cingulata (Fabricius, 1804); Eulaema meriana (Olivier, 1789); Eulaema nigrita Lepeletier, 1841; Exaerete frontalis (Guérin-Méneville, 1845); Exaerete smaradigna (Guérin-Méneville, 1845) Williams (1974; 1982); Ackerman (1983); Roubik & Ackerman (1987); Zimmerman & Aide (1989)
Aspasia psittacina (Rchb.f.) Rchb.f. * Aspasia epidendroides Lindl. (1) Euglossini bees (2) Nectar, absent (3) Deception of nectar Eulaema cingulata (Fabricius, 1804); Eulaema polychroma (Mocsáry, 1899) - mistakenly identified as Eulaema tropica L. Dodson & Frymire (1961b); Pijl & Dodson (1966); Williams (1974; 1982)
Brassia antherotes Rchb.f. (1) Wasps (2) Nectar, absent (3) Deception of nectar Unidentified Vespidae Ospina-Calderón et al. (2007)
Brassia aff. arcuigera Rchb.f. * Brassia aff. antherotes Rchb.f. (1) Wasps (2) Reward uncertain (3) Strategy uncertain, pseudoantagonism (misinterpretation) Campsomeris columba (Saussure, 1858) Pijl & Dodson (1966); Dodson (1990)
Brassia ochroleuca Barb.Rodr. (1) Wasps (2) Reward uncertain (3) Strategy uncertain, pseudoantagonism (misinterpretation) Pepsis sp. (Pepsis gloriosa?) Pijl & Dodson (1966); Dodson (1990)
Capanemia thereziae Barb.Rodr. (1) Wasps (2) Nectar (3) Supply of nectar Polybia fastidiosuscula de Saussure, 1854 Singer & Cocucci (1999a); Buzatto et al. (2012)
Cischweinfia dasyandra (Rchb.f.) Dressler & N.H.Williams (1) Euglossini bees (2) Nectar, absent (3) Deception of nectar Unidentified Euglossini bees Williams (1982); Chase (2009)
Comparettia coccinea Lindl. (1) Butterflies (2) Nectar (3) Supply of nectar Heliconius erato phyllis Fabricius, 1775; Heliconius ethilla narcaea Godart, 1819 Pansarin et al. (2015)
Comparettia falcata Poepp. & Endl. (1) Hummingbirds (2) Nectar (3) Supply of nectar Amazilia tzacatl (De la Llave, 1833); Chlorostilbon maugaeus (Audebert & Vieillot, 1801) Dodson (1965); Pijl & Dodson (1966); Vogel (1969); Rodríguez-Robles et al. (1992); Ackerman et al. (1994); Meléndez-Ackerman et al. (1997)
Cyrtochiloides ochmatochila (Rchb.f.) N.H.Williams & M.W.Chase = Oncidium ochmatochilum Rchb.f. (1) Oil-collecting bees (2) Reward uncertain (3) Strategy uncertain Centris sp. Dodson (1965); Pijl & Dodson (1966)
Cyrtochilum macranthum (Lindl.) Kraenzl. = Oncidium macranthum Lindl. (1) Oil-collecting bees and Bombini bees (2) Reward uncertain (3) Strategy uncertain Bombus hortulanus Smith, 1904; Centris sp. Dodson (1962; 1965); Pijl & Dodson (1966)
cf. Gomesa sp, = Oncidium sp. (1) Oil-collecting bees (2) Reward uncertain (3) Probably supply of floral oils Tetrapedia rugulosa Friese, 1899 Schlindwein (1995; 1998)
Gomesa bifolia (Sims) M.W.Chase & N.H.Williams (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Centris trigonoides Lepeletier, 1841 Aliscioni et al. (2009); Torretta et al. (2011)
Gomesa cf. blanchetii (Rchb.f.) M.W.Chase & N.H.Williams * Gomesa montana (Barb.Rodr.) M.W.Chase & N.H.Williams (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Centris analis (Fabricius, 1804) Pansarin et al. (2016)
Gomesa cornigera (Lindl.) M.W.Chase & N.H.Williams = Baptistonia cornigera (Lindl.) Chiron & V.P.Castro = Baptistonia fimbriata (Lindl.) Chiron & V.P.Castro = Oncidium cornigerum Lindl. = Oncidium fimbriatum Lindl. (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Paratetrapedia fervida (Smith, 1879); Tetrapedia diversipes Klug, 1810 Singer (2003); Reis et al. (2003; 2007); Faria (2004); Reis (2005); Singer et al. (2006); Chiron (2008; 2010); Chiron et al. (2009); Pansarin & Pansarin (2010; 2011); Gomiz et al. (2017)
Gomesa paranensoides M.W.Chase & N.H.Williams = Oncidium paranense Kraenzl. (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Tetrapedia diversipes Klug, 1810 Singer & Cocucci (1999a); Singer (2004); Singer et al. (2006)
Gomesa pubes (Lindl.) M.W.Chase & N.H.Williams = Baptistonia pubes (Lindl.) Chiron & V.P.Castro = Oncidium pubes Lindl. (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Tetrapedia sp.; Tetrapedia diversipes Klug, 1810 Reis et al. (2000; 2003); Singer (2003; 2004); Faria (2004); Reis (2005); Singer et al. (2006); Reis et al. (2007); Chiron (2008; 2010); Chiron et al. (2009); Pansarin & Pansarin (2010)
Gomesa varicosa (Lindl.) M.W.Chase & N.H.Williams = Oncidium varicosum Lindl. (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Centris sp.; Epicharis flava (Friese, 1900) Reis (2005); Gomiz et al. (2013); Pansarin et al. (2016)
Ionopsis sp. (1) Meliponini bees (2) Nectar, absent (3) Deception of nectar Trigona fulviventris Guérin-Méneville, 1845 Roubik (2000)
Ionopsis utricularioides (Sw.) Lindl. (1) Oil-collecting bees, Ceratinini bees, Meliponini bees and Halictidae bees (2) Nectar, absent (3) Deception of nectar Augochlora sp.; Ceratina sp.; Nannotrigona testaceicornis (Lepeletier, 1836); Paratetrapedia flaveola Aguiar & Melo, 2011; Paratrigona lineata (Lepeletier, 1836) Montalvo & Ackerman (1987); Pansarin & Pansarin (2010); Aguiar (2014); Aguiar & Pansarin (2019)
Leochilus sp. (1) Wasps (2) Reward uncertain (3) Probably supply of nectar Pachodynerus nassidens (Latreille, 1812) Pijl & Dodson (1966)
Leochilus labiatus (Sw.) Kuntze (1) Halictidae bees (2) Nectar (3) Supply of nectar Lasioglossum (Dialictus) sp. Chase (1986)
Leochilus scriptus (Scheidw.) Rchb.f. (1) Wasps (2) Nectar (3) Supply of nectar Stelopolybia areata (Say); Stelopolybia hamiltoni Richards, 1978 Chase (1986)
Macradenia brassavolae Rchb.f. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa hemichlora Cockerell, 1917; Euglossa villosiventris Moure, 1968 Williams (1982); Singer et al. (2006)
Macradenia paraensis Barb.Rodr. * Macradenia multiflora (Kraenzl.) Cogn. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Eufriesea violacea (Blanchard, 1840); Euglossa sp. Essinger (2005); Koch (2016)
Macroclinium lineare (Ames & C.Schweinf) Dodson = Notylia linearis Ames & C.Schweinf. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa cybelia Moure, 1968; Euglossa deceptrix Moure, 1968; Euglossa dodsoni Moure, 1965; Euglossa dressleri Moure, 1968 Roubik & Ackerman (1987)
Macroclinium wullschlaegelianum (H.Focke) Dodson = Notylia wullschlaegeliana H.Focke (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Eufriesea surinamensis (Linnaeus, 1758) = Euplusia surinamensis (Linnaeus, 1758); Pijl & Dodson (1966); Dodson, 1967); Williams (1982);
Macroclinium xiphophorus (Rchb.f.) Dodson = Notylia xiphophorus Rchb.f. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Eufriesea surinamensis (Linnaeus, 1758) = Euplusia surinamensis (Linnaeus, 1758); Dodson & Frymire (1961b); Pijl & Dodson (1966); Dodson (1967); Williams (1982)
Miltoniopsis warszewiczii (Rchb.f.) Garay & Dunst. = Miltonia endresii G.Nicholson (1) Colletidae bees (2) Reward uncertain (3) Strategy uncertain Ptiloglossa ducalis Smith, 1853 Dodson (1965); Pijl & Dodson (1966)
Notylia sp. 1 (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa dodsoni Moure, 1965; Euglossa tridentata Moure, 1970 Dressler (1968)
Notylia sp. 2 (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa championi Cheesman, 1929; Euglossa mixta Friese 1899; Euglossa tridentata Moure, 1970 Roubik & Ackerman (1987)
Notylia sp. 3 (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa chalybeata iopoecila Dressler; Euglossa sapphirina Moure, 1968 Singer et al. (2006)
Notylia albida Klotzsch (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa hemichlora Cockerell, 1917 Ackerman (1983); Roubik & Ackerman (1987)
Notylia barkeri Lindl. (1) Euglossini bees (2) Perfumes (3) Supply of perfumes Euglossa dissimula Dressler, 1978; Euglossa tridentata Moure, 1970; Euglossa variabilis Friese, 1899; Euglossa viridissima Friese, 1899 Ackerman (1983); Roubik & Ackerman (1987); Gerlach & Schill (1991); Warford (1992); Damon & Salas-Roblero (2007);
Notylia aff. barkeri Lindl. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa sp.; Euglossa hansoni Moure, 1965; Euglossa ignita Smith, 1874; Euglossa tridentata Moure, 1970 Pijl & Dodson (1966); Dodson, 1967); Dressler (1968); Williams (1982)
Notylia cf. barkeri Lindl. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa sp.; Euglossa erythrochlora Moure, 1968; Pijl & Dodson (1966); Dodson, 1967); Dressler (1968); Williams (1982)
Notylia buchtienii Schltr. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa augaspisDressler, 1982 Dodson (1965; 1967); Pijl & Dodson (1966); Williams (1982); Gerlach & Schill (1991)
Notylia cf. buchtienii Schltr. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa ignita Smith, 1874 Dodson (1965; 1967); Pijl & Dodson (1966); Williams (1982)
Notylia cf. durandiana Cogn. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa sp.; Eulaema nigrita Lepeletier, 1841 Singer & Koehler (2003)
Notylia cf. longispicata Hoehne & Schltr. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa chalybeata iopoecilaDressler; Euglossa sapphirina Moure, 1968 Singer & Koehler (2003)
Notylia nemorosa Barb.Rodr. (1) Euglossini bees (2) Perfumes (3) Supply of perfumes Eulaema nigrita Lepeletier, 1841; Euglossa melanotricha Moure, 1967 Singer & Koehler (2003); Singer (2004); Singer et al. (2006)
Notylia orbicularis A.Rich & Galeotti = Notylia tridachne Lindl. & Paxton (1) Euglossini bees (2) Perfumes (3) Supply of perfumes Euglossa viridissima Friese, 1899 Warford (1992)
Notylia panamensis Ames (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa hemichlora Cockerell, 1917 Pijl & Dodson (1966); Dodson (1967); Dressler (1968); Williams (1982)
Notylia pentachne Rchb.f. (1) Euglossini bees (2) Perfumes (3) Supply of perfumes Euglossa cognata Moure, 1970; Eulaema bombiformis (Packard, 1869); Eulaema cingulata (Fabricius, 1804); Eulaema meriana (Olivier, 1789); Exaerete frontalis (Guérin-Méneville, 1845) Pijl & Dodson (1966); Dodson (1967); Dressler (1968); Williams (1982); Ackerman (1983); Roubik & Ackerman (1987)
Notylia trisepala Lindl. & Paxton (1) Euglossini bees (2) Perfumes (3) Supply of perfumes Euglossa viridissima Friese, 1899 Warford (1992)
Notylia cf. trisepala Lindl. & Paxton = Notylia cf. turialbae Schltr. (1) Euglossini bees (2) Perfumes (3) Supply of perfumes Euglossa hansoni Moure, 1965; Euglossa tridentata Moure, 1970 Dressler (1968)
Oncidium hyphaematicum Rchb.f. (1) Oil-collecting bees (2) Reward uncertain (3) Strategy uncertain, pseudoantagonism (misinterpretation) Centris buchwaldi Friese, 1901 Dodson & Frymire (1961a); Pijl & Dodson (1966)
Oncidium kegeljani (E.Morren) M.W.Chase & N.H.Williams = Odontoglossum kegeljani E.Morren (1) Bombini bees (2) Nectar, absent (3) Deception of nectar Bombus hortulanus Smith, 1904 Dodson (1962); Pijl & Dodson (1966)
Oncidium planilabre Lindl. (1) Oil-collecting bees (2) Reward uncertain (3) Strategy uncertain, pseudoantagonism (misinterpretation) Centris geminata Cockerell, 1914 Dodson & Frymire (1961a); Pijl & Dodson (1966)
Oncidium roseum (Lindl.) Beer = Cochlioda rosea (Lindl.) Benth. (1) Hummingbirds (2) Nectar (3) Supply of nectar Unknown hummingbirds Dodson (1965); Pijl & Dodson (1966)
Oncidium sphacelatum Lindl. (1) Oil-collecting bees (2) Floral oils, absent (3) Deception of floral oils Centris mexicana Smith, 1854; Centris nitida Smith, 1874 Damon & Cruz-López (2006); Damon & Salas-Roblero (2007); Pemberton (2008)
Oncidium vulcanicum (Rchb.f.) M.W.Chase & N.H.Williams = Cochlioda vulcanica (Rchb.f.) Benth. & Hook.f. ex Rolfe (1) Hummingbirds (2) Nectar (3) Supply of nectar Unknown hummingbirds Dodson (1965); Pijl & Dodson (1966)
Ornithocephalus sp. (1) Euglossini bees (2) Reward uncertain, possibly seeking for nectar (3) Strategy uncertain Euglossa cybelia Moure, 1968 Cingel (2001)
Ornithocephalus bicornis Lindl. (1) Oil-collecting bees (2) Reward uncertain (3) Probably supply of floral oils Paratetrapedia calcarata (Cresson, 1878) Pijl & Dodson (1966); Brito (2001); Silvera (2002)
Ornithocephalus ciliatus Lindl. = Ornithocephalus avicula Rchb.f. = Ornithocephalus kruegeri Rchb.f. (1) Oil-collecting bees (2) Reward uncertain (3) Probably supply of floral oils Paratetrapedia testacea (Smith, 1854) Dodson (1965); Pijl & Dodson (1966); Brito (2001); Pacek & Stpiczyńska (2007)
Ornithocephalus cochleariformis C.Schweinf. (1) Oil-collecting bees (2) Reward uncertain (3) Probably supply of floral oils Paratetrapedia sp. Brito (2001); Silvera (2002)
Ornithocephalus cf. patentilobus C.Schweinf. (1) Oil-collecting bees (2) Reward uncertain (3) Probably supply of floral oils Paratetrapedia testacea (Smith, 1854) Dodson (1965); Pijl & Dodson (1966); Brito (2001)
Ornithocephalus powellii Schltr. (1) Oil-collecting bees (2) Reward uncertain (3) Probably supply of floral oils Paratetrapedia calcarata (Cresson, 1878) Pijl & Dodson (1966); Brito (2001)
Phymatidium delicatulum Lindl. (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Tetrapedia amplitarsis Friese 1989; Trigonopedia sp. Brito (2001); Reis et al. (2006); Singer et al. (2006); Pacek et al. (2012); Cabral (2014)
Rodriguezia bahiensis Rchb.f. (1) Xylocopini bees and flies (2) Nectar (3) Supply of nectar Philopota sp.; Xylocopa suspecta Moure & Camargo, 1988 Carvalho & Machado (2006)
Rodriguezia decora (Lem.) Rchb.f. (1) Butterflies (2) Nectar (3) Supply of nectar Ascia monuste (Linnaeus, 1764); Astraptes fulgerator Walch, 1775; Dryas iulia Fabricius, 1775; Urbanus dorantes Stoll, 1790 Pansarin et al. (2018)
Rodriguezia granadensis (Lindl.) Rchb.f. (1) Euglossini bees (2) Nectar (3) Supply of nectar Eulaema cingulata (Fabricius, 1804); Eulaema meriana (Olivier, 1789); Exaerete smaragdina (Guérin-Méneville, 1845) Ospina-Calderón et al. (2015)
Rodriguezia lanceolata Ruiz & Pav. = Rodriguezia secunda Kunth (1) Hummingbirds and butterflies (2) Nectar (3) Supply of nectar Amazilia fimbriata (Gmelin, 1788); Amazilia versicolor (Vieillot, 1818); Heliconius hermathena Hewitson, 1854 Dodson (1965); Braga (1977); Pansarin et al. (2018)
Rodriguezia leeana Rchb.f. (1) Euglossini bees (2) Reward uncertain, (3) Probably supply of nectar Euglossa nigropilosa Moure, 1965 Dodson (1965); Pijl & Dodson (1966); Williams (1982)
Rosioglossum grande (Lindl.) Garay & G.C.Kenn = Odontoglossum grande Lindl. (1) Oil-collecting bees (2) Reward uncertain (3) Strategy uncertain Centris sp. Dodson (1965); Pijl & Dodson (1966)
Telipogon peruvianus T.Hashim (1) Tachinid flies (2) Mates (3) Pseudocopulation Eudejeania aff. browni Curran, 1941 Martel et al. (2016)
Tolumnia bahamense (Nash) Braem = Oncidium bahamense Nash (1) Oil-collecting bees (2) Reward uncertain (3) Strategy uncertain, pseudoantagonism (misinterpretation) Centris versicolor Fabricius, 1775 Nierenberg (1972)
Tolumnia guibertiana (A.Rich.) Braem (1) Oil-collecting bees (2) Floral oils, absent (3) Deception of floral oils Centris poecila Lepeletier, 1841 Vale et al. (2011)
Tolumnia henekenii (M.R.Schomb. ex Lindl.) Nir = Oncidium henekenii M.R.Schomb. ex Lindl. (1) Oil-collecting bees (2) Mates (3) Pseudocopulation Centris aff. versicolor Fabricius, 1775 - Probably male of Centris insularis Smith, 1874 Dod (1976); Cingel (2001)
Tolumnia lucayana (Nash) Braem = Oncidium lucayanum Nash (1) Oil-collecting bees (2) Floral oils, absent (3) Deception of floral oils Centris versicolor Fabricius, 1775 Nierenberg (1972); Dodson (1975); Ackerman (1986)
Tolumnia quadriloba (C.Schweinf.) Braem = Oncidium quadrilobum C.Schweinf (1) Oil-collecting bees (2) Reward uncertain (3) Probably deception of floral oils Centris sp. Nierenberg (1972)
Tolumnia variegata (Sw.) Braem = Oncidium variegatum (Sw.) Sw. (1) Oil-collecting bees (2) Floral oils, absent (3) Deception of floral oils Centris versicolor Fabricius, 1775 Nierenberg (1972); Ackerman & Montero-Oliver (1985); Ackerman (1986); Ackerman et al. (1997)
Trichocentrum andrewsiae (R.Jiménez & Carnevali) R.Jiménez & Carnevali = Lophiaris andrewsiae R.Jiménez & Carnevali (1) Oil-collecting bees (2) Reward uncertain (3) Probably deception of floral oils Centris sp. Cen (2016)
Trichocentrum ascendens (Lindl.) M.W.Chase & N.H.Williams = Oncidium ascendens Lindl. (1) Meliponini bees (2) Resin (3) Supply of resin Frieseomelitta nigra (Cresson, 1878) = Trigona nigra Cresson Parra-Tabla & Magaña-Rueda (2000); Parra-Tabla et al. (2000); Silvera (2002)
Trichocentrum capistratum Linden & Rchb.f. = Trichocentrum panamense Rolfe (1) Euglossini bees (2) Reward uncertain, (3) Probably deception of nectar Euglossa allosticta Moure, 1969; Euglossa bursigera Moure, 1970; Euglossa cordata (Linnaeus, 1758); Euglossa crassipunctata Moure, 1968; Euglossa deceptrix Moure, 1968, Euglossa gorgonensis Cheesman, 1929; Euglossa tridentata Moure, 1970; Euglossa variabilis Friese, 1899 Pijl & Dodson (1966); Williams (1982); Ackerman (1983); Roubik & Ackerman (1987)
Trichocentrum carthagenense (Jacq.) M.W.Chase & N.H.Williams = Trichocentrum oerstedii (Rchb.f.) R.Jiménez & Carnevali (1) Oil-collecting bees (2) Reward uncertain, possibly seeking for floral oils (3) Strategy uncertain Centris sp. Cen (2016)
Trichocentrum jonesianum (Rchb.f.) M.W.Chase & N.H.Williams = Oncidium jonesianum Rchb.f. (1) Oil-collecting bees (2) Reward uncertain, possibly seeking for floral oils (3) Strategy uncertain Epicharis sp. Singer (2004); Gomiz et al. (2017)
Trichocentrum lanceanum (Lindl.) M.W.Chase & N.H.Williams = Oncidium lanceanum Lindl. (1) Oil-collecting bees (2) Reward uncertain, possibly seeking for floral oils (3) Strategy uncertain Centris sp. Dodson (1965); Pijl & Dodson (1966)
Trichocentrum luridum (Lindl.) M.W.Chase & N.H.Williams = Oncidium cosymbephorum C.Morren (1) Oil-collecting bees (2) Floral oils, absent (3) Deception of floral oils Centris ruthannae Snelling, 1966 Carmona-Díaz & García-Franco (2009)
Trichocentrum pumilum (Lindl.) M.W.Chase & N.H.Williams (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Lophopedia nigrispinis (Vachal, 1909); Tetrapedia diversipes Klug, 1810 Pansarin & Pansarin (2011)
Trichocentrum stipitatum (Lindl.) M.W.Chase & N.H.Williams = Oncidium stipitatum Lindl. (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils, pseudoantagonism (misinterpretation) Centris sp.; Possibly Centris inermis Friese, 1899 Dodson (1965); Pijl & Dodson (1966); Silvera (2002)
Trichocentrum tigrinum Linden & Rchb.f. (1) Euglossini bees (2) Reward uncertain, possibly seeking for nectar (3) Probably deception of nectar Eulaema cingulata (Fabricius, 1804) Dodson (1962); Pijl & Dodson (1966); Williams (1982);
Trichoceros antennifer (Humb. & Bonpl.) Kunth = Trichoceros parviflorus Kunth (1) Tachinid flies (2) Mates (3) Pseudocopulation Paragymnomma sp. Dodson (1962); Pijl & Dodson (1966)
Trichopilia sp. (1) Euglossini bees (2) Reward uncertain, possibly seeking for nectar (3) Strategy uncertain Euglossa cybelia Moure, 1968 Roubik & Ackerman (1987)
Trichopilia cf. leucoxantha L.O.Williams (1) Euglossini bees (2) Reward uncertain, possibly seeking for nectar (3) Strategy uncertain Euglossa heterosticta Moure, 1968 Williams (1982)
Trichopilia maculata Rchb.f. (1) Euglossini bees (2) Reward uncertain, possibly seeking for nectar (3) Strategy uncertain Euglossa bursigera Moure, 1970; Euglossa dissimula Dressler, 1978; Euglossa imperialis Cockerell, 1922; Euglossa tridentata Moure, 1970 Ackerman (1983); Roubik & Ackerman (1987)
Trichopilia rostrata Rchb.f. (1) Euglossini bees (2) Reward uncertain, possibly seeking for nectar (3) Strategy uncertain Euglossa hemichlora Cockerell, 1917 Dodson (1962); Pijl & Dodson (1966); Williams (1982)
Trichopilia subulata (Sw.) Rchb.f. (1) Euglossini bees (2) Reward uncertain, possibly seeking for nectar (3) Strategy uncertain Eufriesea mussitans (Fabricius, 1787); Euglossa dressleri Moure, 1968; Unidentified Euglossa spp. Williams (1982); Ackerman (1983); Roubik & Ackerman (1987)
Trizeuxis falcata Lindl. (1) Meliponini bees (2) Reward uncertain (3) Strategy uncertain Unknown Meliponini bees Dodson & Dodson (1980)
Warmingia eugenii Rchb.f. (1) Euglossini bees (2) Reward uncertain (3) Probably supply of perfumes Euglossa iophyrraDressler, 1982 Singer & Gerlach (2002); Singer (2004); Singer et al. (2006)
Zelenkoa onusta (Lindl.) M.W.Chase & N.H.Williams = Oncidium onustum Lindl. (1) Xylocopini bees (2) Reward uncertain (3) Strategy uncertain Xylocopa cf. transitoria Pérez, 1901 Dodson & Frymire (1961a); Pijl & Dodson (1966)
Zygostates alleniana Kraenzl. (1) Oil-collecting bees (2) Floral oils (3) Supply of floral oils Lophopedia nigrispinis (Vachal, 1909) Gomiz et al. (2014)

Vogel (1974) classified the elaiophores in two distinct types: epithelial, when the oils are secreted by layers of the epidermal tissue (Fig. 3A), and trichomal, when the secretory tissue is composed by uni- or multicellular trichomes (Fig. 3B). In the Oncidiinae, the genera Lockhartia, Ornithocephalus, Phymatidium and Zygostates have trichomal elaiophores (Reis 2005; Blanco et al. 2013). However, most species of oil-secreting Oncidiinae orchids present epithelial elaiophores (Blanco et al. 2013; Gomiz et al. 2014) and secrete the oils directly onto an epidermis. Then, bees gather the oils through scratching movements over the lip, during which the oils adhere to their legs by capillarity (Stpiczyńska et al. 2007; Stpiczyńska & Davies 2008; Torretta et al. 2011). Conversely, sometimes the oil may accumulate under a thick layer of cuticle, forcing the visitor to “squeeze” and break the cuticle in order to achieve the content (Singer & Cocucci 1999a; Stpiczyńska et al. 2007). Also, some species may produce and retain oils inside their flowers but no apparent structure is involved in its secretion, therefore they are functionally rewardless flowers because the resources are not externalized (Reis 2005; Stpiczyńska et al. 2007). In several Oncidiinae species the elaiophores are most present in the callus and parts of the lateral lobes (Stpiczyńska et al. 2007; Stpiczyńska & Davies 2008). In a few cases, the elaiophores occur solely on the lateral lobes (Singer & Cocucci 1999b; Stpiczyńska et al. 2007; Stpiczyńska & Davies 2008; Pansarin et al. 2016).

Figure 3  Floral structures and supply of resources in Oncidiinae orchids. A. Epithelial elaiophores (arrow) of Gomesa pubes; B. Trichomal elaiophores (arrow) of Grandiphyllum divaricatum; C. Flower with nectaries (arrow) of Capanemia thereziae; D. Fragrant flower of Notylia sp. visited by an euglossine bee. 

The presence of a tabula infrastigmatica in an Oncidiinae orchid flower is an indication that oil-collecting bees may be acting. Dressler (1981; 1993) suggested that those bees hold the tabula infrastigmatica using their mandibles to stabilize themselves in the flowers, making possible the extraction of floral oils. In fact, several oil-collecting bees have been already reported pollinating species of Oncidiinae (Tab. 1), but the use of the tabula infrastigmatica is yet to be demonstrated. Oil-secreting flowers are pollinated by bees belonging to Melittidae, Ctenoplectridae and Apidae, though only the latter has representatives in the Neotropics (Buchmann 1987; Vinson et al. 1996; Singer & Cocucci 1999a; Cingel 2001; Torretta et al. 2011; Neubig et al. 2012). Among these, the pollinators of Oncidiinae species are distributed in the genera Centris (Centridini), Epicharis (Epicharitini), Lophopedia and Paratetrapedia (Tapinotaspidini), and Tetrapedia (Tetrapedini) (Tab. 1). These insects deliberately collect the contents from the elaiophores by grasping them and during this process promote the pollination while carrying pollinaria attached to different parts of their body. A similar grasping behavior is performed by Centris bees while pollinating some Malpighiaceae species, which grasp the constrictions at the base of the petals while using their forelimbs for the gathering (Vogel 1974; 1990).

Some authors believe that the flowers of many Oncidiinae orchids mimic the oil-secreting flowers of several Malpighiaceae (Chase et al. 2009; Neubig et al. 2012). Just as several Oncidiinae orchids, American malpighiaceous plants bear floral oils, and both taxa exhibit similar coloration, morphology and light absorption spectra (Silvera 2002; Chase et al. 2009; Neubig et al. 2012). The resemblance between flowers of some Oncidiinae and Malpighiaceae species may be due to convergence due to the sharing of pollinators (Singer & Cocucci 1999b; Cingel 2001; Singer et al. 2006; Stpiczyńska et al. 2007; Davies & Stpiczyńska 2008; Papadopulos et al. 2013). Stpiczyńska et al. (2007) and Stpiczyńska & Davies (2008) indicate anatomic and structural features shared between the elaiophores of Oncidiinae species investigated thus far and those of Malpighiaceae. The similarities extend to the chemical level, as demonstrated by the presence of both oncidinol and byrsonic acid produced in these two unrelated taxa (Reis et al. 2007). In addition, Powell (2008) and Papadopulos et al. (2013) established that many Oncidiinae with yellow flowers closely match yellow Malpighiaceae species also in terms of spectral reflectance. Then, anatomical and chemical features may be responsible for the successful sharing of pollinators between Oncidiinae and Malpighiaceae, even though these bees may have evolved to pollinate the latter at a first moment (Stpiczyńska & Davies 2008).

In a recent study, Pansarin et al. (2016) described the pollination mechanisms and pollinators of Gomesa varicosa and G. cf. blanchetii - misidentified as G. montana. They mentioned several species of bees attracted by these two orchids, belonging to Bombini (Bombus), Centridini (Centris), Epicharitini (Epicharis), Tapinotaspidini (Lophopedia), Tetrapedini (Tetrapedia) and Xylocopini (Xylocopa). However, only Centris and Epicharis bees were able to pollinate them. The authors indicate that the elaiophores are present only in the lateral lobes of the lip, but the callus deceives the bees due to resemblance to stamens of some Malpighiaceae species, where Centridini bees collect pollen (Sigrist & Sazima 2004; Pansarin et al. 2016).

Elaiophores in Oncidiinae species have arisen at least seven times (Renner & Schaefer 2010), being considered as a parallelism found in different groups of the subtribe. Buchmann (1987) mentions that 50 species out of 350 of the former Oncidium s.l. bear elaiophores, many of these species currently placed within the genus Gomesa. Within Oncidiinae, pollination by oil-collecting bees while gathering floral oils was already reported to species of Gomesa, Ornithocephalus, Phymatidium, Trichocentrum and Zygostates (see Tab. 1 for complete list of species).

Nectar

Nectar is essentially constituted by water and diluted sugars. The production of nectar in a flower increases its visitation frequency, and it constitutes a resource aimed by most groups of pollinators (Pijl & Dodson 1966; Calvo 1990; Neiland & Wilcock 1998). The structures and locations of the nectaries (nectar-secreting glands) in Oncidiinae may differ from one species to another. In Rodriguezia bahiensis, R. venusta and Comparettia coccinea, the lateral sepals are connate to form the nectariferous spur (Carvalho & Machado 2006; Leitão et al. 2014; Pansarin et al. 2015). In Oncidium strictum - as Symphyglossum sanguineum - the nectaries are located at the auricles of the lip (Stpiczyńska & Davies 2006). The secretory tissue may be formed by a single-layered epidermis with the presence of some stomata, followed by a couple of layers of subepidermal cells (Stpiczyńska & Davies 2006; Buzatto et al. 2012). In other cases, a tongue-like, trichomed nectar gland composes the secretory tissue (Leitão et al. 2014; Pansarin et al. 2015). The animals drink the nectar from the nectaries and, while doing so, remove the pollinarium, which adheres to their body (Singer & Cocucci 1999a). Pollinator behavior considerably varies, depending on the specific group of animal pollen-vectors.

Hummingbirds are one of the animal groups that pollinates Oncidiinae orchids while seeking for nectar (Dodson 1965; Pijl & Dodson 1966; Rodríguez-Robles et al. 1992; Meléndez-Ackerman et al. 1997; Siegel 2011). Due to their fast movements, they demand high levels of energy, so they visit orchid flowers looking after food sources. Although these birds also feed on insects and spiders they find in flowers, much of the energy needed comes from feeding on nectar (Pijl & Dodson 1966; Siegel 2011). These birds are very efficient to access the nectaries and remove their liquid content while hovering in front of the flowers (Rodríguez-Robles et al. 1992; Siegel 2011). Bird-pollinated orchids generally show some degree of guidance of the bill, by the shape and form of some parts of the perianth (Dodson 1965; Pijl & Dodson 1966). The curvature of some flowers matches the curvature of the beaks to enhance feeding. To reach a position favoring nectar withdrawal, birds need to force their beaks against the column and thus contact the orchid pollinarium. Ornithophilous orchids usually have a callus that partially closes the floral tube at the level of the anther and stigma (Pijl & Dodson 1966). In Comparettia falcata, for example, the nectary spur is formed by the fusion of the lateral sepals. The position and orientation of the column guarantees that visitors that are able to reach the nectar end up dislodging the pollinarium and/or pollinating the flower (Rodríguez-Robles et al. 1992). Hummingbird-pollinated orchids generally present vivid coloration, as bright red, pink, purple, orange and yellow. According to Buchmann & Nabhan (1996), several insects cannot perceive the red end of the light spectrum and, consequently, do not visit these flowers in search of nectar, which are left alone for the hummingbirds. Furthermore, these birds pollinate orchids that usually lack odors. It is also noteworthy the development of dark (blue, gray or brown) and cryptic pollinia in these orchids, because bright yellow pollinia would contrast with the dark beaks and bring the attention of the birds, which could try to get rid of it (Dressler 1981; Siegel 2011). The genera of hummingbird pollinators identified so far are Amazilia and Chlorostilbon. Pollination by hummingbirds in Oncidiinae was already reported for Comparettia, Oncidium and Rodriguezia (see Tab. 1 for complete list of species).

Butterflies may also be pollinators of some nectariferous Oncidiinae orchid species. Braga (1977) described the process in which individuals of Heliconius hermathena collect nectar in flowers of Rodriguezia lanceolata (as R. secunda) and adhere the pollinaria on the head, close to the proboscis, promoting pollination. Pansarin et al. (2015) reported the pollination of Comparettia coccinea by two species, Heliconius ethilla narcaea and H. erato phyllis. After landing on the flowers, the butterflies inserted their proboscis into the nectariferous spur guided by the horn-shaped lip callus. The pollinaria adhere to one of the eyes of the insects, depending on which nectariferous entrance they choose. Sometimes, these Nymphalidae butterflies were observed carrying pollinaria on both eyes. So far, Ascia, Astraptes, Dryas, Heliconius and Urbanus are the genera of butterflies that have been observed pollinating Oncidiinae orchids. These insects pollinate species of Comparettia and Rodriguezia (see Tab. 1 for complete list of species).

Other insects reported to search for nectar in Oncidiinae orchids are wasps. According to Pijl & Dodson (1966) wasps are not particularly efficient pollinators. In the nectariferous orchid Capanemia thereziae Barb.Rodr., for example, they are much bigger than the flowers and use a substantial part or the whole inflorescence as a landing platform (Singer & Cocucci 1999a). They hover in front of the flowers until locate somewhere to land, or walk on the tree until reach the inflorescence which is pendulous and sometimes lie on the surface of the tree. Then, they search for the nectar stored at the base of the lip (Fig. 3C) and end up removing the pollinarium eventually, which attaches to the clipeum of the insect. Each wasp may transport several pollinaria at the same time, and thus have the potential to pollinate more than one flower. However, many pollinaria may disturb these wasps and make them to try to clean their heads, what may lead to the loss of pollinaria (Singer & Cocucci 1999a). The pollination takes place when one of these pollinia is arrested on the concave stigmatic surface of a flower, which easily retains it. Remarkably, C. thereziae presents different features in relation to the other species of the genus. It bears greenish, scentless, nectar-bearing flowers (vs. white, fragrant, nectarless flowers), which agree with the wasp-pollinated syndrome according to Pijl & Dodson (1966). The wasp genera of pollinators recorded so far for Oncidiinae are Campsomeris, Pachodynerus, Pepsis, Polybia and Stelopolybia. So far, pollination by wasps collecting nectar in Oncidiinae orchids has been reported to Capanemia and Leochilus (see Tab. 1 for complete list of species).

To a lesser extent, studies have shown the gathering of nectar by different groups of bees that forage on Oncidiinae orchids and promote their pollination. We may cite: (1) Xylocopini: bees of Xylocopa suspecta were reported gathering nectar and pollinating flowers of Rodriguezia bahiensis (Carvalho & Machado 2006); (2) Halictid: bees of the genus Lasioglossum present short tongue suited to process nectaries in flowers of Leochilus labiatus, which in turn bear a shallow, open nectar cavity at the base of its lip (Chase 1986); and (3) Euglossini: males of Eulaema meriana, El. cingulata and Exaerete smaradigna pollinate Rodriguezia granadensis while foraging for nectar (Ospina-Calderón et al. 2015).

Lastly, Acroceridae flies had their first record of pollination of an Oncidiinae species performed by Carvalho & Machado (2006), who described the pollination of Rodriguezia bahiensis by these insects (among others such as some aforementioned bees). These flies land on the flowers frontally and spend a substantially high time on the same flower (approximately 3 minutes). They insert their mouth-parts between the lip and the column and force the column with their heads or backs, easily removing the pollinaria. The viscidium glues to the apex of their back and, then, are carried to another flower. The flies of the genus Philopota Wiedemann, 1830 present the apical dorsal portion of the thorax well developed, which facilitates the removal and deposition of pollinaria in an orchid flower (Luz 2004; Carvalho & Machado 2006). These insects usually visit only one flower per inflorescence and, by doing so, they prevent the loss of pollinaria that often occurs involving other groups of pollinators (Carvalho & Machado 2006).

In spite of being the most offered floral resource among orchids, nectar is not easily found in members of Oncidiinae. So far, the known genera that supply this floral resource to their visitors are Capanemia, Comparettia, Leochilus, Oncidium and Rodriguezia (see Tab. 1 for complete list of species).

Perfumes

Odors play an important role in the attraction of some animal species. In some Oncidiinae orchids (Tab. 1), the osmophores (perfume glands) bear combinations of terpenes and aromatics (Vogel 1963a; 1966a; b; Williams 1982; Williams & Whitten 1983; Antón et al. 2012). These structures may be composed by a solely layer of cells or by uni- to multicellular pappillae. More informations about the chemical composition, micromorphology, ultrastructure, morphology and anatomy of some osmophores are discussed and detailed in Stern et al. (1986), Vogel (1990), Gerlach & Schill (1991), Kaiser (1993), Endress (1994), Dudareva & Pichersky (2006), Cseke et al. (2007), Antón et al. (2012) and Uribe-Holguin (2016). The location of these glands in orchids may vary, between the adaxial surface of sepals, petals or parts of the lip (Dressler 1993). Male Euglossine bees are known for actively collecting perfumes from either floral or non-floral sources, that they likely use during courtship (Ramírez et al. 2002) (see below). Among perfume-secreting flowers, Orchidaceae accounts for 84 % of the known pollination interactions, Araceae for 6 % and the remaining 10 % by nine different families (Amaryllidaceae, Apocynaceae, Bignoniaceae, Euphorbiaceae, Gesneriaceae, Haemodoraceae, Iridaceae, Solanaceae and Theaceae) (Ramírez et al. 2002). Within Orchidaceae, this pollination strategy is restricted to subfamily Epidendroideae, within the subtribes Catasetinae, Stanhopeinae and part of Zygopetaliinae and Oncidiinae.

The compounds of some floral scents are gathered specially by males of Euglossini bees (Fig. 3D), an exclusive tribe of the Neotropics (Pijl & Dodson 1966; Dressler 1982; Williams 1982). Cruger (1865) was the first to describe the relationship between orchid flowers and euglossine bees, also described by Darwin (1885), but the true nature of this interaction was not fully understood until recently. At a first moment, researchers believed that several fragrances were collected by the males in order to use them as precursors for sex pheromones to attract females (Ackerman 1983; Williams 1982). Actually, Euglossini males make up a bouquet of fragrances which is indicative of their fitness for females and that can be “sprayed” near the females. Then, is the female who decides which individual to copulate with, by “measuring” its fitness (Bembé 2004; Eltz et al. 2005). The behavior of Euglossini bees at the flowers follows a pattern that has already been described by many authors, as Dressler (1982) and Williams (1982). After being attracted by the odor of the flowers, they hover for a moment in front of them before landing. Then, they stabilize themselves over the flowers by placing their heads between the column and the lip and grasping the flower with their midlegs. The gathering of the scents is performed by brushing the secreting tissues with their forelegs, in a similar manner to what oil-collecting bees do. These insects absorb the substances with their modified forelegs, specifically the foretarsal brushes, and transfer them to expanded, bottle-like (sponge-like inside) cavities in the hind legs (Vogel 1963b; 1966b; Kimsey 1984).

The Euglossini that collect these aromatic compounds in Oncidiinae species are divided in four genera: Euglossa, Eulaema, Eufriesea and Exaerete (Tab. 1). Interactions between Oncidiinae orchids and perfume-collecting male Euglossini bees were reported for Notylia Lindl. and are probably present in Macradenia, Macroclinium and Warmingia (see Tab. 1 for complete list of species), all phylogenetically close genera. Therefore, unlike the floral oils, which would have appeared several times independently within Oncidiinae (Renner & Schaefer 2010), exclusive pollination by perfume-gathering male Euglossine bees is likely restricted to this set of closely-related genera. In addition, both male and female euglossine bees may forage for nectar, as any other Hymenoptera (Williams 1982).

Deceptive strategies

Floral scents are not solely employed to attract male Euglossini bees. These fragrances are equally important on mechanisms based on deception, acting as a fake signal to mislead insects looking for food or sexual partners (Aguiar 2014; Martel et al. 2016). In some cases, these compounds are unnoticeable to the human nose. Ionopsis utricularioides, for example, presents 22 chemical compounds that were not studied until recently (Aguiar 2014). However, deceptive strategies are not only based upon perception of fragrances, sometimes they may also take place through some degree of mimicry. In Oncidiinae, deception mechanisms are divided basically in generalized food-deception (plants known as food-frauds) and sexual deception (by pseudocopulation or pre-copulatory behavior).

Food-frauds (deception of resources)

Some orchids developed mechanisms to mislead their potential pollinators, by presenting features that resemble secretory tissues/structures or imitating the general appearances of rewarding species (Caballero-Villalobos et al. 2017). Generally, flowers of rewardless species are fragrant and their volatiles consist of monoterpenoids and sesquiterpenoids (Flach et al. 2004; Singer et al. 2006; Davies & Stpiczyńska 2012). According to Tremblay et al. (2005), about a third of the known orchids deceive pollinators. For example, Oncidium kegeljani (as Odontoglossum kegeljani), is polinated by male bees of Bombus robustus var. hortulans (Bombini) in Ecuador (Pijl & Dodson 1966). The insects come to the flowers and attempt to reach false nectaries, which are actually empty. The callus impedes the advance of the visitor into the flower and, by forcing the passage, they detach the viscidium of the pollinarium with their heads. The position of the stipe is reset by curving downwards, making the pollinia to assume a position in front of the head of the animal (Pijl & Dodson 1966) (Fig. 4A). This arrangement facilitates pollination when the individual visits subsequent flowers. Williams (1982), in turn, reported both male and female Euglossini bees pollinating Cischweinfia dasyandra, in search for nectar. However, Chase (2009) dissected five species of the genus and no nectar was detected.

Figure 4  Deceptive pollination strategies and aspects of the breeding systems in Oncidiinae orchids. A. Pollinaria of an unidentified species of Oncidium attached to Bombus rubicundus, a putative case of deception of resources; B. Flower of Telipogon ortizii, a putative case of sexually deceptive species; C-D. Protandry in Notylia cf. hemitricha; C. Male function, when the stigmatic cavity is closed (arrow) and unable to receive pollen loads; D. Female function, when the column walls open and expose the stigmatic cavity (arrow), allowing its pollination; E. Development of fruits by self-pollination (green mark) and cross-pollination (red mark) in Gomesa imperatoris-maximiliani. Note its tendency to self-incompatibility, since fruits formed by selfing are aborted; F. Well-developed fruit of Gomesa flexuosa

Silvera (2002) concluded that some Oncidiinae species may present Batesian mimicry, because despite producing no reward, they attract the pollinators of Malpighiaceae species which serve as vectors for their pollination processes. Ackerman & Montero-Oliver (1985) and Montalvo & Ackerman (1987) classified, respectively, Tolumnia variegata - as Oncidium variegatum - and Ionopsis utricularioides as species that use this strategy and deceive the visitors that are searching for rewards. In a recent study, Aguiar & Pansarin (2019) described a deceptive mechanism of pollination to I. utricularioides. They did not identify any kind of secretion in the spur of their flowers, so the species, in fact, does not produce nectar or any other reward to their visitors. These rewardless flowers present similar colors to several of the neighboring plants and make part of a guild mimicry, attracting many generalist bee species. The bees land on the lips of the flowers and try to reach the lip base by following the nectar guides. By inserting their heads between the lip and the column, they remove the pollinarium, which attaches to their proboscis (Aguiar & Pansarin 2019). The pollinators identified were members of oil-collecting bees (Tapinotaspidini), Halictidae, Ceratinini and Meliponini. Roubik (2000) also mentioned a Meliponini bee, Trigona fulviventris, carrying pollinaria of an unidentified species of Ionopsis. The pollinaria were placed on the scuttelum of the stingless bee. Also, Parra-Tabla et al. (2000) indicated the gathering of resins by Meliponini bees (Tab. 1) in flowers of Trichocentrum ascendens (as Oncidium ascendens), which they employ in nest-building practices. Regarding food frauds, besides the already mentioned genera Cischweinfia, Ionopsis, Oncidium, and Tolumnia, deception of floral resources was also reported to Aspasia, Brassia and Trichocentrum (see Tab. 1 for complete list of species).

Pseudocopulation (sexual deception)

Sometimes, rewardless flowers mimic female individuals of some animal species, luring the males that pollinate them while searching for females to mate. The latter phenomenon is known as pollination by sexual deceit or pseudocopulation (Pijl & Dodson 1966; Dressler 1993; Ayasse 2006; Martel et al. 2016). This pollination strategy is known to occur within a few genera of the families Asteraceae, Iridaceae, but it is more important in Orchidaceae (reviewed by Vereecken et al. 2012). Within Orchidaceae, this pollination strategy is restricted to the clade composed by subfamilies Orchidoideae and Epidendroideae. Within Orchidoideae, this pollination strategy is very well-documented in the genera Ophrys and Serapias (Vereecken et al. 2012) as well as in several Australian terrestrial orchids of Diuridae and Pterostylidinae (reviewed by Phillips et al. 2013). Within Epidendroideae orchids, sexual mimicry has been documented in species of Lepanthes (Pleurothallidinae; Blanco & Barboza 2005), Trigonidium (Maxillariinae; Singer 2002), Mormolyca (Maxillariinae; Singer et al. 2004), Telipogon, Tolumnia and Trichoceros (Oncidiinae; Chase 2009; Martel et al. 2016).

A remarkable case involving Oncidiinae orchids is that of Trichoceros antennifer - as T. parviflorus (Dodson 1962; Pijl & Dodson 1966). Their flowers imitate the female tachinid flies of Paragymnomma in a high degree, presenting similar coloration, general morphology of both column and base of the lip and lateral extensions simulating the wings of a sitting fly. The stigma of the flower reflects sunlight much as the female fly genitalia, stimulating the male flies that thereby attempt copulation with it (Dodson 1962; Pijl & Dodson 1966). The viscidium, in contact to the body of the insect, detaches and connects to the basal portion of the abdomen of the fly. The long stipe of the pollinarium reconfigures and bends down, ensuring its positioning into the stigma when the fly visits a succeeding flower (Dodson 1962; Pijl & Dodson 1966). Pseudocopulation was also suggested to occur in Tolumnia henekenii - as Oncidium henekenii - by Dod (1976). Observations involved males of Centris aff. versicolor, although Cingel (2001) suggests these insects may be the unknown male of C. insularis. Whereas the flowers of T. henekenii are very insect-like in appearance, these observations (Dod 1976) are very preliminary.

Martel et al. (2016) recently described a sexually deceptive pollination system in Telipogon peruvianus, although Dressler (1981) was the first to suggest this pollination strategy for this orchid genus. Most species of the genus imitate the appearance of an insect sitting on a flower and their columns present spiny calli and hairs (Fig. 2B). Species of Telipogon are known to produce volatiles but have been recorded as scentless, at least to the human perceptions (Martel et al. 2016). By chemical analyses, Martel et al. (2016) evaluated the presence of scents and the compounds present in the odor bouquet of T. peruvianus, predominantly composed of saturated and unsatured hydrocarbons, which attract the orchid visitors. In spite of four Tachinid species approaching the flowers of T. peruvianus, only male flies of Eudejeania aff. browni (an undescribed Eudejeania species) were seen carrying pollinaria, attached to their legs (Martel et al. 2016). The behavioral responses of the male flies were similar in the presence of both T. peruvianus flowers and female dummies carrying chemical baits. However, in contrast to what has been described for other sexually deceptive orchids, the flies do not demonstrate pseudocopulatory behavior on T. peruvianus flowers. Instead, their behavior match pre-copulatory movements (touching and grasping) observed in a couple other species of Tachinid flies (Reitz & Adler 1991; Martel et al. 2016).

Based upon the three mentioned genera, pollination by pseudocopulation would have evolved twice within Oncidiinae: to the clade formed by Telipogon-Trichoceros and inside Tolumnia (see Tab. 1 for complete list of species).

Pseudoantagonism

Pijl & Dodson (1966) proposed the term pseudoantagonism while observing, in their words, male bees attacking flowers, which were mistaken as enemies. Indeed, the male insects of some bee species are extremely territorial, surveying their areas while resting upon near twigs or leafs, while expecting for coespecific females and attacking any other males or flying insects that enter the territory (Pijl & Dodson 1966). According to Pijl & Dodson (1966), by mistaking flowers as enemies, the bees strike them hard several times. In the process, the viscidium supposedly attaches to the frons of the bee and the stipe bends down, assuming a frontal position in the head of the animal, between the compound eyes. Dodson & Frymire (1961b) and Pijl & Dodson (1966) reported Centris bees attacking the flowers of Oncidium hyphaematicum and O. planilabre in the coastal zone of Ecuador. These authors also attribute pseudoantagonism to the orchid genus Brassia, which is visited and pollinated by females of the wasp genera Pepsis and Campsomeris (Pijl & Dodson 1966) (Tab. 1). These insects hunt spiders and sting them, feeding the paralyzed preys to their larvae. Wasps supposedly mistake Brassia flowers for spiders and sting their lips. In the process, pollinia would be attached to their heads (Pijl & Dodson 1966; Dodson 1990). Pseudoantagonism was also inferred to Tolumnia bahamense (as Oncidium bahamense) and Trichocentrum stipitatum (as Oncidium stipitatum), by Dodson (1965), Nierenberg (1972) and Pijl & Dodson (1966) (Tab. 1).

However, by our observations in the field while working with pollination of Gomesa spp., we agree with Chase (2009) by doubting of the existence of this mechanism. It is extremely unlikely that insects remove pollinaria and even more pollinate any flower by striking them in a rapid movement. The visitors generally need to assume a given positioning over the flowers and manipulate them in a certain way in order to remove the pollinarium and promote pollination. Also, some species proposed to be pseudoantagonists actually present floral oils, as for example Trichocentrum stipitatum (as Oncidium stipitatum; Silvera 2002). So, we believe that these authors may be misinterpreting the real behavior of insects that would be only defending the inflorescences while waiting for females. In sum, we believe that Pijl & Dodson (1966) may have seen both females pollinating the flowers and male bees defending the territory while waiting for the arrival of females, and confused their genders and behaviors.

Spontaneous self-pollination

Some cases of spontaneous self-pollination/autogamy, were reported in Oncidiinae species (Pijl & Dodson 1966; Catling 1990; Brito 2001; Cingel 2001; Chase 2009). In Erycina glossomystax (as Oncidium glossomystax), the stipe may naturally bend and curl downward, forcing the pollinia into the stigma. Brito (2001) reported spontaneous self-pollination to Hofmeisterella eumicroscopica, but he cited another flower in which the stigma was filled with two pollinaria, therefore insect pollination takes place as well. According to Catling (1990), Cingel (2001) and Chase (2009), other species that may also be autogamous are Erycina pumilio (as Psygmorchis gnomus), E. zamorensis (as P. zamorensis), Oncidium iricolor (as Oncidium pollardii), Trichocentrum oestlundianum (as Oncidium oestlundianum) and Trichopilia fragrans.

Breeding systems

Pollinators may dislodge the pollinarium and leave the pollinia on the stigma of the same flower or from another flower from the same individual, promoting self-pollination. Self-pollination causes the loss of genetic diversity in populations and several species developed mechanisms to avoid it (Dressler 1993). There are species of plants that do not develop fruits resulting from their own pollen or abort them at some point of the process. So, we can coarsely classify the orchids into self-compatible or self-incompatible species. Self-compatible species are able to set fruit and viable seed following self-pollination. Self-incompatible plants are the opposite, this is, unable to set fruit and viable seed after self-pollination. Many Oncidiinae fall inside the latter (Tab. 2), although intermediate cases may occur (Dressler 1993; Singer & Koehler 2003; Singer et al. 2004; Tremblay et al. 2005; Singer et al. 2006). Tremblay et al. (2005) provided a list of self-incompatible species of orchids and the references to each study, in which are included species of the Oncidiinae genera Cyrtochilum, Gomesa, Grandiphyllum, Oncidium, Tolumnia and Trichocentrum. Self-incompatibility was demonstrated for most of the Oncidiinae species studied so far (East 1940; Ackerman & Montero-Oliver 1985; Warford 1992; Ackerman 1995; Ackerman et al. 1997; Parra-Tabla et al. 2000; Cingel 2001; Torretta et al. 2011; Singer & Koehler 2003; Carvalho & Machado 2006; Damon & Cruz-López 2006; Pemberton 2008; Vale et al. 2011; Ospina-Calderón et al. 2015; Pansarin et al. 2016; 2018) (Tab. 2).

Table 2  Self-compatibility and natural fruit set in the Oncidiinae. ND = No data. * = Misidentification. 

Oncidiinae species and synonyms in literature Self-compatibility Natural fruit set (%) Reference
Aspasia principissa Rchb.f. Self-compatible 9.5 Zimmerman & Aide (1989); Chase (2009)
Brassia antherotes Rchb.f. ND 3.38 Ospina-Calderón et al. (2007)
Brassia verrucosa Lindl. ND 0 Damon & Salas-Roblero (2007)
Comparettia coccinea Lindl. Self-compatible ND Pansarin et al. (2015)
Comparettia falcata Poepp. & Endl. Self-compatible 16.9 - 19.4 Rodriguez-Robles et al. (1992)
Cyrtochilum cimiciferum (Rchb.f.) Dalström = Oncidium cimiciferum Rchb.f. ex Linden Self-incompatible ND East (1940); Tremblay et al. (2005)
Erycina crista-galli (Rchb.f.) N.H.Williams & M.W.Chase ND 0 Damon & Salas-Roblero (2007)
Erycina glossomystax (Rchb.f.) N.H.Williams & M.W.Chase Self-compatible and self-incompatible populations ND Cingel (2001)
Erycina pusilla (L.) N.H.Williams & M.W.Chase ND 0 Damon & Salas-Roblero (2007)
Gomesa bifolia (Sims) M.W.Chase & N.H.Williams Predominantly self-incompatible ND Torretta et al. (2011)
Gomesa cf. blanchetii (Rchb.f.) M.W.Chase & N.H.Williams = Gomesa montana (Barb.Rodr.) M.W.Chase & N.H.Williams* Self-incompatible ND Pansarin et al. (2016)
Gomesa imperatoris-maximiliani (Rchb.f.) M.W.Chase & N.H.Williams = Oncidium crispum Lodd. ex Lindl. Self-incompatible ND East (1940); Tremblay et al. (2005)
Gomesa longicornu (Mutel) M.W.Chase & N.H.Williams = Oncidium unicorne Lindl. Self-incompatible ND East (1940); Tremblay et al. (2005)
Gomesa varicosa (Lindl.) M.W.Chase & N.H.Williams Self-compatible and self-incompatible populations ND Pansarin et al. (2016)
Grandiphyllum divaricatum (Lindl.) Docha Neto = Oncidium divaricatum Lindl. Self-incompatible ND East (1940); Tremblay et al. (2005)
Ionopsis utricularioides (Sw.) Lindl. Self-compatible (Puerto Rico) and self-incompatible (Brazil) populations 6.1; 0.58-5.35; 5.25-7.20 Montalvo & Ackerman (1987); Pansarin et al. (2016); Aguiar (2014); Aguiar & Pansarin (2019)
Leochilus labiatus (Sw.) Kuntze Self-compatible 0 - 12 Chase (1986); Cingel (2001); Damon & Salas-Roblero (2007)
Leochilus oncidioides Knowles & Westc. ND 0 - 15 Damon & Salas-Roblero (2007)
Leochilus scriptus (Scheidw.) Rchb.f. Self-compatible 60; 0 - 6 Chase (1986); Cingel (2001); Damon & Salas-Roblero (2007)
Lockhartia oerstedii Rchb.f. ND 0 Damon & Salas-Roblero (2007)
Notylia barkeri Lindl. Self-incompatible 0.7; 0-3 Warford (1992); Damon & Salas-Roblero (2007)
Notylia longispicata Hoehne & Schltr. Predominantly self-incompatible ND Singer & Koehler (2003)
Notylia nemorosa Barb.Rodr. Predominantly self-incompatible 12.86 Singer & Koehler (2003)
Notylia orbicularis A.Rich & Galeotti = Notylia tridachne Lindl. & Paxton Self-incompatible ND Warford (1992)
Notylia trisepala Lindl. & Paxton Self-incompatible ND Warford (1992)
Oncidium altissimum (Jacq.) Sw. Self-incompatible 2 Ackerman (1995)
Oncidium laeve (Lindl.) Beer ND 0 Damon & Salas-Roblero (2007)
Oncidium ornithorrhynchum Kunth ND 0 Damon & Salas-Roblero (2007)
Oncidium sphacelatum Lindl. Self-incompatible 0 - 0.25; 0.4; 1.49 East (1940); Tremblay et al. (2005); Damon & Cruz-López (2006); Damon & Salas-Roblero (2007); Pemberton (2008)
Ornithocephalus tripterus Schltr. ND 0 Damon & Salas-Roblero (2007)
Phymatidium delicatulum Lindl. Self-compatible 10.7 Cabral (2014)
Rodriguezia bahiensis Rchb.f. Self-incompatible 6.57 Carvalho & Machado (2006)
Rodriguezia decora (Lem.) Rchb.f. Self-incompatible ND Pansarin et al. (2018)
Rodriguezia granadensis (Lindl.) Rchb.f. Self-incompatible 11.3 Ospina-Calderón et al. (2015)
Rodriguezia lanceolata Ruiz & Pav. Self-incompatible ND Pansarin et al. (2018)
Telipogon peruvianus T.Hashim Self-compatible ND Martel et al. (2016)
Tolumnia guianensis (Aubl.) Braem = Oncidium lemonianum Lindl. Self-incompatible ND East (1940); Tremblay et al. (2005)
Tolumnia guibertiana (A.Rich.) Braem Self-incompatible 15 Vale et al. (2011)
Tolumnia variegata (Sw.) Braem Self-incompatible 1.2 - 2.6; 0.13 - 10.05 Ackerman & Montero-Oliver (1985); Ackerman et al. (1997); Cingel (2001); Tremblay et al. (2005)
Trichocentrum ascendens (Lindl.) M.W.Chase & N.H.Williams = Cohniella ascendens (Lindl.) Christenson = Oncidium ascendens Lindl. Self-incompatible 3.1 - 6.8; 0 - 3 Parra-Tabla et al. (2000); Tremblay et al. (2005); Damon & Salas-Roblero (2007)
Trichocentrum candidum Lindl. ND 0 Damon & Salas-Roblero (2007)
Trichocentrum carthagenense (Jacq.) M.W.Chase & N.H.Williams = Trichocentrum oerstedii (Rchb.f.) R.Jiménez & Carnevali ND 0 Damon & Salas-Roblero (2007)
Trichocentrum cavendishianum (Bateman) M.W.Chase & N.H.Williams = Oncidium cavendishianum Bateman Self-incompatible ND East (1940); Tremblay et al. (2005)
Trichocentrum luridum (Lindl.) M.W.Chase & N.H.Williams = Oncidium cosymbephorum C.Morren Self-incompatible ND Carmona-Díaz & García-Franco (2009); Cen (2016)
Trichocentrum microchilum (Bateman ex Lindl.) M.W.Chase & N.H.Williams = Oncidium microchilum Bateman ex Lindl. Self-incompatible 0 East (1940); Tremblay et al. (2005); Damon & Salas-Roblero (2007)
Trichocentrum pumilum (Lindl.) M.W.Chase & N.H.Williams Self-incompatible 9 Pansarin & Pansarin (2011)
Trichocentrum stipitatum (Lindl.) M.W.Chase & N.H.Williams ND 1.8 Tremblay et al. (2005)
Trichopilia tortilis Lindl. ND 0 - 5 Damon & Salas-Roblero (2007)
Warmingia eugenii Rchb.f. Self-compatible ND Singer et al. (2006)

In self-incompatible orchids, the self-pollinated flowers turn yellow and fall (abort) generally after three to five days (Warford 1992) (Fig. 4E). It is important to emphasize that self-incompatibility affects the whole individual. In self-incompatible species, pollen-flow among flowers of the same individual will promote abortions as well. Rodríguez-Robles et al. (1992) cited Comparettia falcata as self-compatible but not autogamous, although the values of fructification were lower in comparison to cross-pollinated flowers in 1989 and 1990 (53.8 % and 64.3 % against 86.4 % and 86.7 %, respectively). This difference in data, despite not statistically significant, suggests that the species may be partially self-incompatible or suffer from inbreeding depression when self-pollinated (Rodríguez-Robles et al. 1992). Pansarin et al. (2016) classified Gomesa varicosa as partially self-incompatible, because the species presented 54 % and 87 % of fruit set for self-pollination and cross-polination treatments, respectively. Self-compatibility was also reported to Aspasia, Erycina, Ionopsis, Leochilus, Phymatidium, Telipogon and Warmingia (Chase 1986; Montalvo & Ackerman 1987; Zimmerman & Aide 1989; Cingel 2001; Singer et al. 2006; Aguiar 2014; Cabral 2014; Martel et al. 2016; Aguiar & Pansarin 2019) (Tab. 2), but represents a rare condition in Oncidiinae orchids as a whole (Montalvo & Ackerman 1987; Dressler 1993; Pansarin et al. 2016).

Mechanism to promote cross-pollination: protandry

As previously mentioned, several Oncidiinae species are self-incompatible. Yet, there are intrinsic mechanisms that eventually favour cross-pollination. In some cases, the just-removed pollinarium needs to modify its conformation and bends down the stipe before being properly inserted into the stigmatic cavity (Chase 2009). Some species present protandry as a mechanism to increase the chances for cross-pollination to take place. The protandrous plants present two fertile stages. In the first stage, the stigmatic cavity does not work as a receiver of pollen, by physical/chemical/conformation blocking, ensuring that the flowers function only as pollen donors (Fig. 4C). Then, in the second stage, the flowers change their features/configuration and become pollen receivers (Warford 1992; Singer & Koehler 2003; Singer et al. 2006) (Fig. 4D). In Notylia spp., for example, the flowers expand their stigmatic cavity at the female phase (Fig. 4D), without changing the angle between the column and the lip, making possible the placement of the pollinarium in the stigma. (Warford 1992; Singer et al. 2006). Indeed, older flowers at female phase and younger flowers at male phase may still coexist, allowing the occurrence of few geitonogamous pollinations (self-pollinations among flowers of the same individual) (Singer & Koehler 2003). So far, protandry was demonstrated in the Oncidiinae genera Macradenia and Notylia (Warford 1992; Singer & Koehler 2003; Singer et al. 2006).

Fruiting success

The fruits in Orchidaceae consist of capsules with abundant dust-like seeds (Dressler 1993; Neiland & Wilcock 1998) (Fig. 4F). Specialized literature points out that orchids as a whole often have infrequent pollinator visits and, by consequence, low natural fruit set (Darwin 1885; Dressler 1968; Montalvo & Ackerman 1987; Tremblay et al. 2005) (see Tab. 2 for values of fruiting within Oncidiinae). Factors such as phenology, microhabitat, inflorescence size, population size and synchronicity between plants and pollinators have been advocated as affecting fruit set in Orchidaceae (Fritz & Nilsson 1994; Donaldson et al. 2002; Tremblay et al. 2005). It is clear, however, that presence/absence of floral rewards are of importance. Silvera (2002) and Tremblay et al. (2005) found that the presence of floral rewards positively correlates with fruit production (sometimes almost doubling the chances of fruiting).

Alternative explanations for the observed low fruit set may rely in a combination of factors involving pollinator behavior, presence/absence of floral rewards and breeding systems, not necessarily acting all together: (1) low pollinator abundance, so that many flowers are never visited; (2) loss of pollinaria, through deliberate removal by insects, because they may feel disturbed by the structures adhered to their bodies (JB Castro unpubl. res.); (3) rewardless flowers, whose pollinators tend to visit few flowers before leaving the plant (Dafni 1987); (4) passive pollinators that visit several flowers/inflorescences of the same individual/plant; and (5) presence of self-incompatibility (this is, in these plants all self-pollinated flowers will abort) (Singer & Koehler 2003). Rewardless orchids will tend to be unfrequently visited and, consequently, their fruit sets may be low. If pollinators are rare, this phenomenon will be accentuated. On the other hand, plant species with rewarding flowers may also display low fruit set if their pollinators are passive (visiting several flowers of the same plant/individual) and the plants are self-incompatible. Passive pollinators of rewarding flowers may tend to maximize their collecting efforts, promoting some degree of abortions, through self-pollinations (Singer & Koehler 2003).

Final considerations

The present review of the literature supports that, as a whole, Oncidiinae orchids are predominantly pollinator-dependent (unable to set fruit and viable seed in absence of pollinators). Within the so-far studied Oncidiinae orchids, floral oils prevail as the main floral reward. In a general summary of the plant resource-pollinator relationships among Oncidiinae orchids, we may cite: (1) floral oils and females of oil-collecting bees; (2) perfumes - or aromatic compounds - and males of Euglossini bees; and (3) nectar and several animal families (wasps, hummingbirds, butterflies and bees of the Halictidae, Xylocopini and Euglossini). Within Oncidiinae, the percentages of pollinators from a total of 92 orchid species surveyed (Tab. 1) are as follows: bees 84.7 % (found in 78 out of 92 species) - Euglossini 39.1 % (36/92); oil-collecting 36.9 % (34/92); Meliponini 4.3 % (4/92); Halictidae, Xylocopini and Bombini 2.1 % (2/92) each; Colletidae and Ceratinini 1.1 % (1/92) each -, wasps 6.5 % (6/92), hummingbirds 4.3 % (4/92), butterflies 3.2 % (3/92) and flies 3.2 % (3/92). Most of the Oncidiinae orchids studied so far are self-incompatible. Out of 36 research papers involving detailed reproductive biology studies, 69.4 % (25/36) of the species were self-incompatible, 22.2 % (8/36) were self-compatible and 8.3 % (3/36) had both self-incompatible and self-compatible populations (Tab. 2).

Still, there are many gaps in the knowledge of pollination of some important taxa within Oncidiinae. Most studies described the pollination of orchids from southern and southeastern Brazil. However, many species-rich genera occurring in the Andean region are poorly known, as Brassia (35 spp.), Cyrtochilum (120 spp.), Lockhartia (30 spp.), Pachyphyllum (40 spp.) and Telipogon (170 spp.). Even Oncidium sensu stricto presents studies out of date and not representatives of its total diversity (only 6 species out of 520 studied so far). In addition, the study of genera with few species (for example, Seegeriella) may reveal unique pollination strategies. As a long-term perspective, we hope that the topics discussed here - presence or absence of secretory structures, floral resources, pollinator group and behavior, mechanisms favoring cross-pollination, self-compatibility/self-incompatibility, etc. - may be plotted on more complete and dense molecular phylogenies of the clade (such as Chase et al. 2009 and Neubig et al. 2012), helping to elucidate well-supported evolutionary scenarios for the arising of pollination strategies and breeding systems in Oncidiinae orchids.

Acknowledgements

This contribution is part of the first author’s Ph.D. Thesis (in Botany) at the Programa de Pós-graduação em Botânica of the Universidade Federal do Rio Grande do Sul (UFRGS), entitled “Estratégias de polinização e biologia reprodutiva em orquídeas Oncidiinae do sul do Brasil/Pollination strategies and breeding systems in Oncidiinae orchids from Southern Brazil”. This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. J.B.C. gratefully acknowledges his CAPES grant.

References

Ackerman JD. 1983. Specificity and mutual dependency of the orchid-euglossine bee interaction. Biological Journal of the Linnean Society 20: 301-314. [ Links ]

Ackerman JD. 1986. Mechanisms and evolution of food-deceptive pollination systems in orchids. Lindleyana 1: 108-113. [ Links ]

Ackerman JD. 1995. An orchid flora of Puerto Rico and the Virgin Islands. Memoirs of the New York Botanical Garden 73: 1-203. [ Links ]

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

Ackerman JD, Montero Oliver JC. 1985. Reproductive biology of Oncidium variegatum: moon phases, pollination and fruit set. American Orchid Society Bulletin 54: 326-329. [ Links ]

Ackerman JD, Rodríguez-Robles JA, Meléndez EJ. 1994. A meager nectar offering by an epiphytic orchid is better than nothing. Biotropica 26: 44-49. [ Links ]

Aguiar JMRBV. 2014. Biologia reprodutiva das Ionopsis Kunth (Orchidaceae) do Brasil. MSc Thesis, Universidade de São Paulo, São Paulo. [ Links ]

Aguiar JMRBV, Pansarin ER. 2019. Deceptive pollination of Ionopsis utricularioides (Oncidiinae: Orchidaceae). Flora 250: 72-78. [ Links ]

Alcántara S, Semir J, Solferin VN. 2006. Low genetic structure in an epiphytic Orchidaceae (Oncidium hookeri) in the Atlantic rainforest of southeastern Brazil. Annals of Botany 98: 1207-1213. [ Links ]

Aliscioni SS, Torretta JP, Bello ME, Galati GB. 2009. Elaiophores in Gomesa bifolia (Sims) M.W.Chase & N.H.Williams (Oncidiinae: Cymbidieae: Orchidaceae): structure and oil secretion. Annals of Botany 104: 1141-1149. [ Links ]

Antón S, Kamińska M, Stpiczyńska M. 2012. Comparative structure of the osmophores in the flowers of Stanhopea graveolens Lindley and Cycnoches chlorochilon Klotzsch (Orchidaceae). Acta Agrobotanica 65: 11-22. [ Links ]

Ayasse M. 2006. Floral scent and pollinator attraction in sexually deceptive orchids. In: Dudareva N, Pichersky E. (eds.) Biology of floral scent. Boca Raton, CRS Press. p. 219-241. [ Links ]

Bembé B. 2004. Functional morphology in male euglossine bees and their ability to spray fragrances (Hymenoptera, Apidae, Euglossini). Apidologie 35: 283-291. [ Links ]

Blanco MA, Barboza G. 2005. Pseudocopulatory pollination in Lepanthes (Orchidaceae: Pleurothallidinae) by fungus gnats. Annals of Botany 95: 763-772 [ Links ]

Blanco MA, Davies KL, Stpiczyńska M, Carlsward BS, Ionta GM, Gerlach G. 2013. Floral elaiophores in Lockhartia Hook. (Orchidaceae: Oncidiinae): their distribution, diversity and anatomy. Annals of Botany 112: 1775-1791. [ Links ]

Braga PIS. 1977. Aspectos biológicos das Orchidaceae de uma campina da Amazônia Central. Acta Amazônica 7: 1-89. [ Links ]

Brito AVLT de. 2001. Systematic review of the Ornithocephalus group (Oncidiinae: Orchidaceae) with comments on Hofmeisterella. Lindleyana 16: 157-217. [ Links ]

Buchmann SL. 1987. The ecology of oil flowers and their bees. Annual Review of Ecology and Systematics 18: 343-369. [ Links ]

Buchmann SL, Nabhan GP. 1996. The forgotten pollinators. Washington, Island Press/Shearwater Books. [ Links ]

Buzatto CR, Davies KL, Singer RB, Santos RP, Berg C. 2012. A comparative survey of floral characters in Capanemia Barb.Rodr. (Orchidaceae: Oncidiinae). Annals of Botany 109: 135-144. [ Links ]

Caballero-Villalobos L, Silva-Arias GA, Buzatto CR, Nervo MH, Singer RB. 2017. Generalized food-deceptive pollination in four Cattleya (Orchidaceae: Laeliinae) species from Southern Brazil. Flora 234: 195-206. [ Links ]

Cabral PRM. 2014. Biologia reprodutiva e polinização de orquídeas nativas do estado de São Paulo: Encyclia patens Hook.; Phymatidium delicatulum Lindl. e Mesadenella cuspidata (Lindl.) Garay. MSc Thesis, Universidade de São Paulo, Ribeirão Preto. [ Links ]

Calvo RN. 1990. Pollinator limitation, cost of reproduction, and fitness in plants: a demographic approach. PhD Thesis, University of Miami, Miami. [ Links ]

Carmona-Díaz G, García-Franco JG. 2009. Reproductive success in the Mexican rewardless Oncidium cosymbephorum (Orchidaceae) facilitated by the oil-rewarding Malpighia glabra (Malpighiaceae). Plant Ecology 203: 253-261. [ Links ]

Carvalho R, Machado IC. 2006. Rodriguezia bahiensis Rchb.f.: biologia floral, polinizadores e primeiro registro de polinizacão por moscas Acroceridae em Orchidaceae. Brazilian Journal of Botany 29: 461-470. [ Links ]

Catling PM. 1990. Auto-pollination in the Orchidaceae. In: Arditti J. (ed.) Orchid biology: reviews and perspectives. Portland, O. R. Timber Press. p. 121-158. [ Links ]

Cen IT. 2016. Polinización por engaño de Lophiaris andrewsiae (Orchidaceae: Oncidiinae). Desde el Herbario CICY 8: 4-8. [ Links ]

Chase MW. 1986. Pollination ecology of two sympatric synchronously flowering species of Leochilus in Costa Rica. Lindleyana 1: 141-147. [ Links ]

Chase MW. 2009. Subtribe Oncidiinae. In: Pridgeon AM, Cribb PJ, Chase MW, Rasmussen FN. (eds.) Genera Orchidacearum. Vol. 5. Epidendroideae (part two). Oxford, Oxford University Press. p. 211-394. [ Links ]

Chase MW, Cameron KM, Barrett RL, et al. 2015. An updated classification of Orchidaceae. Botanical Journal of the Linnean Society 177: 151-174. [ Links ]

Chase MW, Palmer JD. 1992. Floral morphology and chromosome number in subtribe Oncidiinae (Orchidaceae): evolutionary insights from a phylogenetic analysis of chloroplast DNA restriction site variation. In: Soltis DE, Soltis PS, Doyle JJ. (eds.) Molecular systematics of plants. New York, Chapman and Hall. p. 324-339. [ Links ]

Chase MW, Whitten WM. 2011. Further taxonomic transfers in Oncidiinae (Orchidaceae). Phytotaxa 20: 26-32. [ Links ]

Chase MW, Williams NH, Faria AD, Neubig KM, Amaral MCE, Whitten WM. 2009. Floral convergence in Oncidiinae (Cymbidieae; Orchidaceae): an expanded concept of Gomesa and a new genus Nohawilliamsia. Annals of Botany 104: 387-402. [ Links ]

Chiron GR. 2008. Un exemple d’endémisme dans la forêt atlantique brésilienne: Baptistonia Barbosa Rodrigues (Orchidaceae, Oncidiinae)- taxinomie, phylogénie et biologie de la conservation. PhD Thesis, Université de Lyon, Lyon. [ Links ]

Chiron GR. 2010. Aspects of the pollination syndrome in Baptistonia (Orchidaceae, Oncidiinae) with link to genus evolution. Revista Guatemalensis 13: 15-43. [ Links ]

Chiron GR, Oliveira RP, Santos TM, Bellvert F, Bertrand C, Berg C. 2009. Phylogeny and evolution of Baptistonia (Orchidaceae, Oncidiinae) based on molecular analyses, morphology and floral oil evidences. Plant Systematics and Evolution 281: 35-49. [ Links ]

Cingel NA. 2001. An atlas of orchid pollination; America, Africa, Asia and Australia. Rotterdam, AA. Balkema. [ Links ]

Cruger H. 1865. A few notes on the fecundation of orchids and their morphology. Botanical Journal of the Linnean Society 8: 127-135. [ Links ]

Cseke LJ, Kaufman PB, Kirakosyan A. 2007. The biology of essential oils in the pollination of flowers. Natural Product Communications 2: 1317-1336. [ Links ]

Dafni A. 1987. Pollination in Orchis and related genera: evolution from reward to deception. In: Arditti, J. (ed.) Orchid biology: reviews and perspectives IV. Ithaca, London, Cornell University Press. p. 79-104. [ Links ]

Damon AA, Cruz-López L. 2006. Fragrance in relation to pollination of Oncidium sphacelatum and Trichocentrum oerstedii (Orchidaceae) in the Soconusco region of Chiapas, Mexico. Selbyana 27: 186-194. [ Links ]

Damon AA, Salas-Roblero P. 2007. A survey of pollination in remnant orchid populations in Soconusco, Chiapas, Mexico. Tropical Ecology 48: 1-14. [ Links ]

Darwin C. 1885. The various contrivances by which orchids are fertilized by insects. 2nd. edn. New York, D. Appleton. [ Links ]

Davies KL, Stpiczyńska M. 2008. The anatomical basis of floral, food-reward production in Orchidaceae. In: Silva JAT. (ed.) Floriculture, ornamental and plant biotechnology: advances and topical issues. Vol. 5. London, Global Science Books. p. 392-407. [ Links ]

Davies KL, Stpiczyńska M. 2009. Comparative histology of floral elaiophores in the orchids Rudolfiella picta (Schltr.) Hoehne (Maxillariinae sensu lato) and Oncidium ornithorhynchum H.B.K. (Oncidiinae sensu lato). Annals of Botany 104: 221-234. [ Links ]

Davies KL, Stpiczyńska M. 2012. Comparative labellar anatomy of resin-secreting abd putative resin-mimic species of Maxillaria s.l. (Orchidaceae: Maxillariinae). Botanical Journal of the Linnean Society 170: 405-435. [ Links ]

Davies KL, Stpiczyńska M, Rawski M. 2014. Comparative anatomy of floral elaiophores in Vitekorchis Romowicz & Szlach., Cyrtochilum Kunth and a florally dimorphic species of Oncidium Sw. (Orchidaceae: Oncidiinae). Annals of Botany 113: 1155-1173. [ Links ]

Dod DD. 1976. Oncidium henekenii - Bee orchid pollinated by bee. American Orchid Society Bulletin 45: 792-794. [ Links ]

Dodson CH. 1962. The importance of pollination in the evolution of the orchids of tropical America. American Orchid Society Bulletin 31: 525-735. [ Links ]

Dodson CH. 1965. Agentes de polinización y su influência sobre la evolución en la família Orquidacea. Iquitos, Universidade Nacional de la Amazonía Peruana. [ Links ]

Dodson CH. 1967. Studies in orchid pollination. American Orchid Society Bulletin 36: 209-214. [ Links ]

Dodson CH. 1975. Coevolution of orchids and bees. In: Gilbert LE, Raven PH. (eds.) Coevolution of animals and plants. Austin, University of Texas Press. p. 91-99. [ Links ]

Dodson CH. 1990. Brassia. In: Escobar R. (ed.) Native Colombian orchids. Vol. 1. Medellín, Editorial Colina. p. 52-53. [ Links ]

Dodson CH, Dodson PM. 1980. Icones Plantarum Tropicarum. Vol. 4. Orchids of Ecuador, part. 4. Sarasota, Marie Selby Botanical Gardens. [ Links ]

Dodson CH, Frymire GP. 1961a. Preliminary studies in the genus Stanhopea. Annals of the Missouri Botanical Garden 48: 137-172. [ Links ]

Dodson CH, Frymire GP. 1961b. Natural pollination of orchids. Missouri Botanical Garden Bulletin 49: 133-139. [ Links ]

Donaldson J, Nanni I, Zachariades C, Kemper J. 2002. Effects of habitat fragmentation on pollinator activity and plant reproductive success in renosterveld shrublands of South Africa. Conservation Biology 16: 1267-1276. [ Links ]

Dressler RL. 1961. The structure of the orchid flower. Missouri Botanical Garden Bulletin 49: 60-69. [ Links ]

Dressler RL. 1968. Observations on orchids and euglossine bees in Panama and Costa Rica. Revista de Biología Tropical 15: 143-183. [ Links ]

Dressler RL. 1974. Classification of the orchid family. In: Ospina M. (ed.) Proceedings of the Seventh World Orchid Conference. Medellín, Seventh World Orchid Conference. p. 259-278. [ Links ]

Dressler RL. 1976. How to study orchid pollination without any orchids. In: Senghas K. (ed.) Proceedings of the Eighth World Orchid Conference. Frankfurt, German Orchid Society. P. 534-537. [ Links ]

Dressler RL. 1981. The orchids: Natural history and classification. Cambridge, Harvard University Press. [ Links ]

Dressler RL. 1982. The biology of orchid bees (Euglossini). Annual Review of Ecology and Systematics 13: 373-394. [ Links ]

Dressler RL. 1993. Phylogeny and classification of the orchid family. Portland, Dioscorides Press. [ Links ]

Dudareva N, Pichersky E. 2006. Biology of floral scent . Florida, Taylor and Francis, CRC Press. [ Links ]

East EM. 1940. The distribution of self-sterility in the flowering plants. Proceedings of the American Philosophical Society 82: 449-518. [ Links ]

Eltz T, Sager A, Lunau K. 2005. Juggling with volatiles: exposure of perfumes by displaying male orchid bees. Journal of Comparative Physiology 191: 575-581. [ Links ]

Endress PK. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge, Cambridge University Press. [ Links ]

Essinger LN. 2005. Euglossini (Apidae, Hymenoptera) no sul de Santa Catarina. MSc Thesis, Universidade do Extremo Sul Catarinense, Criciúma. [ Links ]

Faria AD. 2004. Sistemática filogenética e delimitação dos gêneros da subtribo Oncidiinae (Orchidaceae) endêmicos do Brasil: Baptistonia, Gomesa, Ornithophora, Rodrigueziella, Rodrigueziopsis e Oncidium pro parte. PhD Thesis, Universidade Estadual de Campinas, São Paulo. [ Links ]

Flach A, Dondon RC, Singer RB, Koehler S, Amaral MEC, Marsaioli AJ. 2004. The chemistry of pollination in selected Brazilian Maxillariinae orchids: floral rewards and fragrance. Journal of Chemical Ecology 30: 1039-1050. [ Links ]

Fritz AL, Nilsson LA. 1994. How pollinator-mediated mating varies with population size in plants. Oecologia 100: 451-462. [ Links ]

GBIF - Global Biodiversity Information Facility. 2019. GBIF Home Page. https://www.gbif.org . 26 Mar. 2019. [ Links ]

Gerlach G, Schill R. 1991. Composition of orchid scents attracting euglossine bees. Botanica Acta 104: 379-391. [ Links ]

Givnish TJ, Spalink D, Ames M, et al. 2015. Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proceedings of the Royal Society B 282: 20151553. doi: 10.1098/rspb.2015.1553 [ Links ]

Gomiz NE, Torretta JP, Aliscioni SS. 2013. Comparative anatomy of elaiophores and oil secretion in the genus Gomesa (Orchidaceae). Turkish Journal of Botany 37: 859-871. [ Links ]

Gomiz NE, Torretta JP, Aliscioni SS. 2014. Zygostates alleniana (Orchidaceae: Epidendroideae: Cymbidieae: Oncidiinae): estructura floral relacionada a la polinización. Anales del Jardín Botánico de Madrid 71: 1-9. [ Links ]

Gomiz NE, Torretta JP, Aliscioni SS. 2017. New evidence of floral elaiophores and characterization of the oil flowers in the subtribe Oncidiinae (Orchidaceae). Plant Systematics and Evolution 303: 1-17. [ Links ]

IPNI - The International Plant Names Index. 2019. IPNI Home Page. http://www.ipni.org/index.html . 26 Mar. 2019. [ Links ]

ITIS - Integrated Taxonomic Information System. 2019. ITIS Home Page. https://www.itis.gov . 26 Mar. 2019. [ Links ]

Judd WS, Campbell CS, Kellog EA, Stevens PF. 2009. Sistemática vegetal: um enfoque filogenético. Porto Alegre, Editora Artmed. [ Links ]

Kaiser R. 1993. The scent of orchids: olfactory and chemical investigations. Basel, Editiones Roche. [ Links ]

Kimsey LS. 1984. The behavioural aspects of grooming and related activities in euglossine bees (Hymenoptera: Apidae). Journal of Zoology 204: 541-550. [ Links ]

Koch AK. 2016. Revisão taxonômica e filogenia do gênero Macradenia R.Br. (Oncidiinae - Orchidaceae). PhD Thesis, Instituto de Botânica da Secretaria do Meio Ambiente, São Paulo. [ Links ]

Leitão CAE, Dolder MAH, Cortelazzo AL. 2014. Anatomy and histochemistry of the nectaries of Rodriguezia venusta (Lindl.). Rchb.f. (Orchidaceae). Flora 209: 233-243. [ Links ]

Luz JRP. 2004. A associação de Philopota sp. Wiedemann (Diptera, Acroceridae) com flores do Gervão-Azul, Stachytarpheta cayennensis (Verbenaceae) na Ilha de Marambaia, Rio de Janeiro, Brasil. Entomología y Vectores 11: 681-687. [ Links ]

Martel C, Cairampona L, Stauffer FM, Ayasse M. 2016. Telipogon peruvianus (Orchidaceae) flowers elicit pre-mating behavior in Eudejeania (Tachinidae) males for pollination. PLOS ONE 11: e0165896. doi: 10.1371/journal.pone.0165896 [ Links ]

Meléndez-Ackerman EJ, Ackerman JD, Rodríguez JA. 1997. Factores limitantes en la reproducción en una población natural de Comparettia falcata (Orchidaceae). Pinar del Río, Resúmenes IV Taller Internacional de Orquídeas. [ Links ]

Montalvo AM, Ackerman JD. 1987. Limitations to fruit production in Ionopsis utricularioides (Orchidaceae). Biotropica 19: 24-31. [ Links ]

Neiland MRM, Wilcock CC. 1998. Fruit set, nectar reward, and rarity in the Orchidaceae. American Journal of Botany 85: 1657-1671. [ Links ]

Neubig KM, Whitten WM, Williams NH, et al. 2012. Generic recircumscriptions of Oncidiinae (Orchidaceae: Cymbidieae) based on maximum likelihood analysis of combined DNA datasets. Botanical Journal of the Linnean Society 168: 117-146. [ Links ]

Nierenberg L. 1972. The mechanism for the maintenance of species integrity in sympatrically occurring equitant Oncidiums in the Caribbean. American Orchid Society Bulletin 41: 873-882. [ Links ]

Ospina-Calderón N, Diazgranados-Cadelo M, Viveros-Bedoya P. 2007. Observaciones de la polinización y fenología reproductiva de Brassia cf. antherotes Rchb.f. (Orchidaceae) en un relicto de selva subandina en la reserva natural La Montaña del Ocaso en Quimbaya, Quindío (Colombia). Universitas Scientiarum 12: 83-95. [ Links ]

Ospina-Calderón NH, Duque-Buitrago CA, Tremblay RL, Otero JT. 2015. Pollination ecology of Rodriguezia granadensis (Orchidaceae). Lankesteriana 15: 129-139. [ Links ]

Pacek A, Stpiczyńska M. 2007. The structure of elaiophores in Oncidium cheirophorum Rchb.f. and Ornithocephalus kruegeri Rchb.f. (Orchidaceae). Acta Agrobotanica 60: 9-14. [ Links ]

Pacek A, Stpiczyńska M, Davies KL, Szymczak G. 2012. Floral elaiophore structure in four representatives of the Ornithocephalus clade (Orchidaceae: Oncidiinae). Annals of Botany 110: 809-820. [ Links ]

Pansarin ER, Alves-dos-Santos I, Pansarin LM. 2016. Comparative reproductive biology and pollinator specificity among sympatric Gomesa (Orchidaceae: Oncidiinae). Plant Biology 19: 147-155. [ Links ]

Pansarin ER, Bergamo PJ, Ferraz LJC, Pedro SRM, Ferreira AWC. 2018. Comparative reproductive biology reveals two distinct pollination strategies in Neotropical twig-epiphyte orchids. Plant Systematics and Evolution 304: 793-806. [ Links ]

Pansarin ER, Pansarin LM. 2010. The family Orchidaceae in the Serra do Japi, State of São Paulo, Brazil. Wien, Springer. [ Links ]

Pansarin ER, Pansarin LM. 2011. Reproductive biology of Trichocentrum pumilum: an orchid pollinated by oil-collecting bees. Plant Biology 13: 576-581. [ Links ]

Pansarin ER, Pansarin LM, Alves-dos-Santos I. 2015. Floral features, pollination biology, and breeding system of Comparettia coccinea (Orchidaceae: Oncidiinae). Flora 217: 57-63. [ Links ]

Papadopulos AST, Powell MP, Pupulin F, et al. 2013. Convergent evolution of floral signals underlies the success of Neotropical orchids. Proceedings of the Royal Society B 280: 20130960. doi: 10.1098/rspb.2013.0960 [ Links ]

Parra-Tabla V, Magaña-Rueda S. 2000. Effects of deforestation on the reproductive ecology of Oncidium ascendens (Orchidaceae). Tropical bees: management and diversity. In: Munn P. (ed.) Proceedings of the VI International Conference on Tropical Bees. Cardiff/ San José de Costa Rica, IBRA. p. 335-340. [ Links ]

Parra-Tabla V, Vargas CF, Magaña-Rueda S, Navarro J. 2000. Female and male pollination success of Oncidium ascendens (Orchidaceae) in two contrasting habitat patches: forest vs agricultural field. Biological Conservation 94: 335-340. [ Links ]

Pemberton RW. 2008. Pollination of the ornamental orchid Oncidium sphacelatum by the naturalized oil-collecting bee (Centris nitida) in Florida. Selbyana 29: 87-91. [ Links ]

Phillips RD, Scaccabarozzi D, Retter BA et al. 2013. Caught in the act: pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae). Annals of Botany 113: 629-641. [ Links ]

Pijl L, Dodson CH. 1966. Orchid flowers: Their pollination and evolution. Coral Gables, University of Miami Press. [ Links ]

Possobom CCF, Machado SR. 2017. Elaiophores: their taxonomic distribution, morphology and functions. Acta Botanica Brasilica 31: 503-524. [ Links ]

Powell MP. 2008. Evolutionary convergence of Neotropical orchids, with an emphasis on Oncidiinae. PhD Thesis, University of Reading, Reading. [ Links ]

Ramírez S, Dressler RL, Ospina M. 2002. Abejas euglosinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notas sobre su biología. Biota Colombiana 3: 7-118. [ Links ]

Reis MG. 2005. Caracteres químicos em estudos de filogenia e biologia de polinização de espécies de Oncidiinae (Orchidaceae). PhD Thesis, Universidade Estadual de Campinas, São Paulo. [ Links ]

Reis MG, Faria AD, Bittrich V, Amaral MCE, Marsaioli AJ. 2000. The chemistry of floral rewards - Oncidium (Orchidaceae). Journal of the Brazilian Chemical Society 11: 600-608. [ Links ]

Reis MG, Faria AD, Amaral MCE, Marsaioli AJ. 2003. Oncidinol - a novel diacylglycerol from Ornithophora radicans Barb.Rodr. (Orchidaceae) floral oil. Tetrahedron Letters 44: 8519-8523. [ Links ]

Reis MG, Singer RB, Gonçalves R, Marsaioli AJ. 2006. The chemical composition of Phymatidium delicatulum and P. tillandsioides (Orchidaceae) floral oils. Natural Product Communications 1: 757-761. [ Links ]

Reis MG, Faria AD, Santos IA, Amaral MCE, Marsaioli AJ. 2007. Byrsonic acid - the clue to floral mimicry involving oil-producing flowers and oil-collecting bees. Journal of Chemical Ecology 33: 1421-1429. [ Links ]

Reitz SR, Adler PH. 1991. Courtship and mating behavior of Eucelatoria bryani (Diptera: Tachinidae), a larval parasitoid of Heliothis species (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 84: 111-117. [ Links ]

Renner SS, Schaefer H. 2010. The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees. Philosophical Transactions of the Royal Society B 365: 423-435. [ Links ]

Rodríguez-Robles JA, Meléndez EJ, Ackerman JD. 1992. Effects of display size, flowering phenology, and nectar availability on effective visitation frequency in Comparettia falcate (Orchidaceae). American Journal of Botany 79: 1009-1017. [ Links ]

Roubik DW. 2000. Deceptive orchids with Meliponini as pollinators. Plant Systematics and Evolution 222: 271-279. [ Links ]

Roubik DW, Ackerman JD. 1987. Long-term ecology of Euglossine orchid-bees in Panamá. Oecologia 73: 321-333. [ Links ]

Schlindwein C. 1995. Wildbienen und ihre Trachtpflanzen in einer südbrasilianischen Buschlandschaft: Fallstudie Guaritas, Bestäubung bei Kakteen und Loasaceen. PhD Thesis, University of Tübingen, Tübingen. [ Links ]

Schlindwein C. 1998. Frequent oligolecty characterizing a diverse bee-plant community in a xerophytic bushland of subtropical Brazil. Studies on Neotropical Fauna and Environment 33: 46-59. [ Links ]

Siegel C. 2011. Orchids and hummingbirds: sex in the fast lane. Orchid Digest 75: 8-17. [ Links ]

Sigrist MR, Sazima M. 2004. Pollination and reproductive biology of twelve species of Neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Annals of Botany 94: 33-41. [ Links ]

Silvera K. 2002. Adaptive radiation of oil-reward compounds among Neotropical orchid species (Oncidiinae). MSc Thesis, University of Florida, Gainesville, United States. [ Links ]

Singer RB. 2002. The pollination mechanism in Trigonidium obtusum Lindl. (Orchidaceae: Maxillariinae): Sexual mimicry and trap-flowers. Annals of Botany 89: 157-163. [ Links ]

Singer RB. 2003. Orchid pollination: recent developments from Brazil. Lankesteriana 7: 111-114. [ Links ]

Singer RB. 2004. Orquídeas brasileiras e abelhas. São Paulo, WebBee. http://www.webbee.org.br/singer/texto_singer.pdf. 22 Mar. 2019. [ Links ]

Singer RB, Cocucci AA. 1999a. Pollination mechanisms in four sympatric southern Brazilian Epidendroideae orchids. Lindleyana 14: 47-56. [ Links ]

Singer RB, Cocucci AA. 1999b. Pollination mechanism in southern Brazilian orchids which are exclusively or mainly pollinated by halictid bees. Plant Systematics and Evolution 217: 101-117. [ Links ]

Singer RB, Flach A, Koehler S, Marsaioli AJ, Amaral MCE. 2004. Sexual mimicry in Mormolyca ringens (Lindl.) Schltr. (Orchidaceae: Maxillariinae). Annals of Botany 93: 755-762. [ Links ]

Singer RB, Gerlach G. 2002. Prachtbienen und Orchideen. Neue Erkenntnisse und Anmerkungen zu Sudost-Brasilien. Journal fuer den Orchideenfreund 9: 139-149. [ Links ]

Singer RB, Koehler S. 2003. Notes on the pollination of Notylia nemorosa (Orchidaceae: Oncidiinae): Do pollinators necessarily promote cross-pollination? Journal of Plant Research 116: 19-25. [ Links ]

Singer RB, Marsaioli AJ, Flach A, Reis MG. 2006. The ecology and chemistry of pollination in Brazilian orchids: recent advances. Floriculture, Ornamental and Plant Biotechnology 4: 570-583. [ Links ]

Stern WL, Curry KJ, Whitten WM. 1986. Staining fragrance glands in orchid flowers. Bulletin of the Torrey Botanical Club 113: 288-297. [ Links ]

Stpiczyńska M, Davies KL. 2006. Nectary structure in Symphyglossum sanguineum (Rchb.f.) Schltr. (Orchidaceae). Acta Agrobotanica 59: 7-16. [ Links ]

Stpiczyńska M, Davies KL. 2008. Elaiophore structure and oil secretion in flowers of Oncidium trulliferum Lindl. and Ornithophora radicans (Rchb.f.) Garay & Pabst (Oncidiinae: Orchidaceae). Annals of Botany 101: 375-384. [ Links ]

Stpiczyńska M, Davies KL, Gregg A. 2007. Elaiophore diversity in three contrasting members of Oncidiinae (Orchidaceae). Botanical Journal of the Linnean Society 155: 135-148. [ Links ]

Stpiczyńska M, Davies KL, Pacek-Bieniek A, Kamińska M. 2013. Comparative anatomy of the floral elaiophore in representatives of the newly re-circumscribed Gomesa and Oncidium clades (Orchidaceae: Oncidiinae). Annals of Botany 112: 839-854. [ Links ]

The Plant List. 2019. The Plant List Home Page. Kew, The Royal Botanic Gardens, Missouri Botanical Garden. https://www.theplantlist.org . 26 Mar. 2019. [ Links ]

Torretta JP, Gomiz NE, Aliscioni SS, Bello ME. 2011. Biología reproductiva de Gomesa bifolia (Orchidaceae, Cymbidieae, Oncidiinae). Darwiniana 49: 16-24. [ Links ]

Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society 84: 1-54. [ Links ]

Uribe-Holguin C. 2016. Morphology and anatomy of osmophores in Cycnoches Lindl. (Orchidaceae, Catasetinae) and their utility in phylogenetics. MSc Thesis, Ludwig Maximilian University of Munich, Munich. [ Links ]

Vale Á, Navarro L, Rojas D, Álvarez JC. 2011. Breeding system and pollination by mimicry of the orchid Tolumnia guibertiana in Western Cuba. Plant Species Biology 26: 163-173. [ Links ]

Vereecken NJ, Wilson CA, Hötling S, Schulz S, Banketov SA, Mardulyn P. 2012. Pre-adaptations and the evolution of pollination by sexual deception: Cope’s rule of specialization revisited. Proceedings of the Royal Society B 279: 4786-4794. [ Links ]

Vinson SB, Frankie GW, Williams HJ. 1996. Chemical ecology of bees of the genus Centris (Hymenoptera: Apidae). Florida Entomologist 79: 109-129. [ Links ]

Vogel ST. 1963a. Duftdrüsen im Dienste der Bestäubung: Über Bau und Funktion der Osmophoren. Akademie der Wissenschaften und der Literatur, Mainz. Abhandlungen der mathematisch-naturwissenschaftlichen Klasse 10: 1-165 [ Links ]

Vogel ST. 1963b. Das sexuelle Anlockungsprinzip der Catasetinen- und Stanhopeen-Blüten und die wahre Funktion ihres sogenannten Futtergewebes. Oesterreichische botanische Zeitschrift 110: 308-337. [ Links ]

Vogel ST. 1966a. Scent organs of orchid flowers and their relation to insect pollination. In: DeGarmo LR. (ed.) Proceedings of the Fifth World Orchid Conference. California, Long Beach. p. 253-259. [ Links ]

Vogel ST. 1966b. Parfümsammelnde Bienen als Bestäuber von Orchidaceen und Gloxinia. Oesterreichische botanische Zeitschrift 113: 302-361. [ Links ]

Vogel ST. 1969. Über synorganisierte blütensporne bei einigen Orchideen, Oesterreichische botanische Zeitschrift 116: 244-249. [ Links ]

Vogel ST. 1974. Ölblumen und ölsammelnde Bienen. Akademie der Wissenschaften und der Literatur, Mathematisch-Naturwissenschaftliche Klasse. Tropische und Subtropische Pflanzenwelt 7: 285-547. [ Links ]

Vogel ST. 1990. The role of scent glands in pollination: on the structure and function of osmophores. New Delhi, Amerind Publishing Co. [ Links ]

Warford N. 1992. Pollination biology: the reciprocal agreement between Notylia and Euglossa viridissima. American Orchid. Society Bulletin 61: 884-889. [ Links ]

Williams NH. 1974. Taxonomy of the genus Aspasia (Orchidaceae: Oncidieae). Brittonia 26: 333-346. [ Links ]

Williams NH. 1982. The biology of orchids and euglossine bees. In: Arditti J. (ed.) Orchid biology: reviews and perspectives . Vol. 2. New York, Cornell University Press. p. 119-171. [ Links ]

Williams NH, Chase MW, Fulcher T, Whitten WM. 2001a. Molecular systematics of the Oncidiinae based on evidence from four DNA regions: expanded circumscriptions of Cyrtochilum, Erycina, Otoglossum and Trichocentrum and a new genus (Orchidaceae). Lindleyana 16: 113-139. [ Links ]

Williams NH, Chase MW, Whitten WM. 2001b. Phylogenetic positions of Miltoniopsis, Caucaea, a new genus Cyrtochiloides, and Oncidium phymatochilum (Orchidaceae: Oncidiinae) based on nuclear and plastid DNA data. Lindleyana 16: 272-285. [ Links ]

Williams NH, Whitten WM. 1983. Orchid floral fragrances and male euglossine bees: methods and advances in the last sesquidecade. Biological Bulletin 164: 355-395. [ Links ]

Zimmerman JK, Aide TM. 1989. Patterns of fruit production in a Neotropical orchid: pollinator vs. resource limitation. American Journal of Botany 76: 67-73 [ Links ]

Received: March 31, 2019; Accepted: July 10, 2019

* Corresponding author: jonasbc91@gmail.com

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License