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First Reports and Generic Descriptions of the Achlorophyllous Holoparasites Apodanthaceae (Cucurbitales) of Colombia

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First Reports and Generic Descriptions of the Achlorophyllous Holoparasites Apodanthaceae (Cucurbitales) of Colombia González y Pabón-Mora Actual Biol Volumen 36 / Número 101, 2014 First reports and generic descriptions of the achlorophyllous holoparasites Apodanthaceae (Cucurbitales) of Colombia Primeros registros y descripciones genéricas de la familia de holoparásitos aclorófilos Apodanthaceae (Cucurbitales) de Colombia Favio González1, 3, Natalia Pabón-Mora2, 4 Abstract The Apodanthaceae (Cucurbitales) are one of the 12 parasitic clades of flowering plants and the only holoparasitic family with a vegetative phase entirely endophytic, growing primarily on Fabaceae and Salicaceae stems. The two genera of the family, Apodanthes and Pilostyles, are broadly distributed in Colombia, although they remain extremely under-collected and poorly known. Based on field and herbarium work, and a review of the literature, we provide detailed generic-level descriptions of the family. We also update the records of the family in Colombia and discuss the homology and taxonomic implications of floral characters such as perianth scales, pollen sacs, and the central column. Finally, we provide photographic records of Colombian Apodanthaceae, and some guidelines for properly collecting these plants. Key words: Apodanthaceae, Apodanthes, Cucurbitales, Colombian flora, parasitic flowering plants,Pilostyles Resumen Apodanthaceae (Cucurbitales) es uno de los doce clados de angiospermas parasíticas, y la única familia de especies holoparasíticas con la fase vegetativa completamente endofítica en tallos principalmente de especies de Fabaceae y Salicaceae. Los dos géneros de la familia, Apodanthes y Pilostyles están ampliamente distribuidos en Colombia, aunque han sido muy poco recolectados y permanecen poco conocidos. Con base en trabajo de campo y de herbario, y una extensa revisión bibliográfica, se describen en detalle los caracteres genéricos de la familia. A la vez, se actualizan los registros de la familia en Colombia y se discute la homología e implicaciones taxonómicas de caracteres florales tales como piezas del perianto, sacos polínicos y columna central. Finalmente, presentamos fotografías de las Apodanthaceae colombianas, así como algunas recomendaciones para recolectar adecuadamente estas plantas. Palabras clave: Apodanthaceae, Apodanthes, Cucurbitales, flora colombiana, plantas con flor parasíticas, Pilostyles INTRODUCTION consisting of small gregarious flowers that emerge from the parasitized stems of a limited group of hosts (table 1). The The family Apodanthaceae Takhtajan consists of 11 wide distribution of the family on four continents strongly species in the genera Apodanthes Poit. (1 species suggest a long evolutionary history (Filipowics and Renner, from the New World) and Pilostyles Guill. (10 spp. from 2010) and make intercontinental dispersal a less plausible North-, Central- and South America, Iran, Irak, Syria, biogeographic scenario. Asia Minor, subtropical eastern Africa and southwestern Australia) (Bellot and Renner, 2014). All members of the The affinities of Apodanthaceae have long been debated. family are achlorophyllous holoparasites with an intrincate They have been placed as part of Rafflesiales/Rafflesiaceae but histologically simple endophyte and an exophyte primarily based on the parasitic life style, the dioecy Received: February 2014; accepted: May 2014. 1 Instituto de Ciencias Naturales, Universidad Nacional de Colombia. A. A. 7495. Bogotá, Colombia. 2 Docente e investigadora, Instituto de Biología, Universidad de Antioquia. A. A. 1226. Medellín (Antioquia), Colombia. E-mail addresses: 3 <[email protected]>; 4 <[email protected]>. 123 Actual Biol Volumen 36 / Número 101, 2014 González y Pabón-Mora Table 1. Summary of members of Apodanthaceae, their hosts and their geographical range. Herbarium voucher on the right-hand column are written in italics [1 = species recognized by Bellot and Renner (2014); for a complete synonymy see Bellot and Renner (2014); 2 = Dalea taxonomy follows Barneby (1977); 3 = Herbarium specimens in italics; HUA = Herbario Universidad de Antioquia, Medellín (Antioquia), Colombia] Species1, autor Host Country Reference/voucher3 Trema micrantha Blume Bellot and Renner 2013, (Cannabaceae); Casearia Bolivia, Brazil, 2014, Brown 1845, Gómez Apodanthes macrophylla Vahl, C. nitida Colombia, Costa 1983, Harms 1935, Idárraga caseariae Poit. (L.) Jacq., C. silvestris Sw. Rica, Guyana, Peru, 2011, Yatskievych and (Salicaceae); Burseraceae; Suriname, Venezuela Meijer 2004, Callejas et al. Meliaceae 8062 (HUA) Berlinia eminii Taub., B. paniculata Benth., Brachystegia Angola, Malawi, Bellot and Renner 2013, Pilostyles aethiopica spp.; Julbernardia globiflora Tanzania, Zambia, 2014, Blarer et al. 2004, Welw. (Benth.) Troupin (Fabaceae- Zimbabwe Harms 1935, Meijer 1993 Faboideae) Bellot and Renner 2013, Adesmia arborea Bertero, A. 2014, Brown 1845, Filipowics Argentina, Bolivia, P. berteroi Guill. emarginata Clos (Fabaceae- and Renner 2010, Guillemin Chile, Peru Faboideae) 1834, Harms 1935, Jaffuel 1933, Rodríguez et al. 2008 Calliandra spp. (Fabaceae- Mimosoideae); Inga sp.; Mimosa maguirei Barneby, M. foliolosa Amaral 2007, Amaral and Benth., M. maguirei, M. Ceccantini 2011, Bellot setosa Benth., M. setosissima Argentina, Brazil, and Renner 2013, 2014, Taub., Mimosa sp. (Fabaceae- Cayman Islands, Costa P. blanchetii Blassingame 1968, Brown Mimosoideae); Bauhinia sections Rica, Guyana, Jamaica, 1845, Endriss 1902, Gomes (Gardner) R. Br. Caulotretus and Pauletia; B. Panama, Uruguay, and Fernandes 1994, Harms lunarioides A. Gray; Cassia sp. Venezuela 1935, Robinson 1891, Rose (Fabaceae-“Caesalpinioideae”); 1909, Vattimo-Gil 1978 Dioclea spp.; Galactia jussiaeana HBK; Schnella spp. (Fabaceae- Faboideae) P. boyacensis Colombia (Eastern González and Pabón-Mora Dalea cuatrecasasii Barneby2 F. González & Pabón- Cordillera) 2014 Mora Bellot and Renner 2013, P. coccoidea K. R. Jacksonia (Fabaceae-Faboideae) Western Australia 2014, Filipowics and Renner Thiele 2010, Thiele et al. 2008 Gastrolobium spp., Oxylobium Bellot and Renner 2013, P. collina Dell Western Australia spp. (Fabaceae-Faboideae) 2014, Thiele et al. 2008 Bellot and Renner 2013, P. hamiltonii C. A. Daviesia sp. (Fabaceae- Western Australia 2014, Filipowics and Renner Gardner Faboideae) 2010, Thiele et al. 2008 124 González y Pabón-Mora Actual Biol Volumen 36 / Número 101, 2014 Tabla 1: Continued Species1, autor Host Country Reference/voucher3 Astragalus pycnocladus Boiss. Bellot and Renner, 2013, P. haussknechtii & Hausskn. ex Boiss.; A. spp., 2014, Harms, 1935, Heide- Iran, Syria Boiss. Halimodendron spp.; Onobrychis Jørgensen, 2008, Solms- spp. (Fabaceae-Faboideae) Laubach 1874 Calliandra grandiflora Benth. Guatemala, Honduras, Bellot and Renner 2013, P. mexicana Rose (Fabaceae-“Caesalpinioideae”) Mexico 2014, Rose 1909 Dalea bicolor Humboldt & Barneby 1977, Blassingame Bonpland ex Willdenow var. 1968, Bellot and Renner canescens (M. Mart. & Galeotti) 2013, 2014, Cerros-Tlatilpa Barneby, D. formosa Torr., D. Mexico, Southern and Espejo-Serna 1998, frutescens A. Gray; D. hospes P. thurberi Gray United States of Felger 1988, Filipowics and (Rose) Bullock; D. lutea America Renner 2010, Harms 1935, (Cavanilles) Willdenow var. Kuijt et al. 1985, Laudermilk lutea; Psorothamnus emoryi (A. 1945, Robinson 1891, Rose Gray) Rydberg, and P. schottii 1909, Yatskievych 1993 (Torr.) Barneby2 and the central column of the flower (e.g., Brown, 1845; Although members of Apodanthaceae from the United States, Endlicher, 1841; Eichler, 1878; Eliasson, 1994; Engler, 1912; Mexico, Venezuela, Brazil and Chile have been collected and Gómez, 1983; Harms, 1935; Hutchinson, 1959; Karsten, are thus relatively well documented, they remain poorly known 1856; Kuijt, 1969; Meijer, 1993; Melchior, 1964; Mitchell, and undercollected in Colombia. This is mainly because of 2004; Takhtajan, 1997; Yatskievych and Meijer, 2004) or their small flowers, the endophytic life form, the absence of related to Malvales (Blarer et al. 2004; Heide-Jørgensen, conspicuous hypertrophy of the infected tissues in the host, 2008) based on floral development and morphology. and the short flowering time. Thus, the goals of this work are: However, recent molecular-based phylogenetic analyses (1) to report new findings of Apodanthaceae in Colombia, (2) have shown that Rafflesiaceae s.l. is polyphyletic, and to update and revisit historical data regarding the presence placed Apodanthaceae as sister to the remaining seven of the family in Colombia, (3) to contribute to the ongoing families of the order Cucurbitales (Filipowicz and Renner, discussion of the homology of the perianth, the central column, 2010; Nickrent, 2008; Nickrent et al. 2004; Schaeffer and the androecium, and the fruit and (4) to provide guidelines Renner, 2011). According to Filipowicz and Renner (2010), to help Colombian botanists collect and make careful field inferior ovaries, parietal placentation and dioecy support observations of this extremely undercollected family. At the inclusion of the Apodanthaceae within Cucurbitales. present, limited collections prevent detailed developmental, Thus, Apodanthaceae and the redefined Rafflesiaceae s. morphological, ecological and taxonomic studies of these str. (now part of Malpighiales) represent two of the 12 interesting holoparasitic flowering plants. independent origins of parasitism among flowering plants (Barkman et al. 2007; Nickrent, 2008). MATERIALS AND METHODS At a specific level, the equivocal morphological characters in Apodanthaceae have led some authors (e.g., Harms, We examined
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