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Gynoecium, Fruit and Seed Structure of Paullinieae (Sapindaceae)

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Gynoecium, Fruit and Seed Structure of Paullinieae (Sapindaceae) Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2005? 2005 1472 159189 Original Article FRUIT STRUCTURE OF PAULLINIEAE C. S. WECKERLE and R. RUTISHAUSER Botanical Journal of the Linnean Society, 2005, 147, 159–189. With 90 figures Gynoecium, fruit and seed structure of Paullinieae (Sapindaceae) CAROLINE S. WECKERLE* and ROLF RUTISHAUSER Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland Received January 2004; accepted for publication August 2004 Despite an emphasis on fruit characters in Paullinieae taxonomy, few detailed morphological and anatomical studies of the gynoecia, fruits and seeds exist. The aims of the present study were (1) to provide a detailed documentation of gynoecium, fruit and seed structure and ontogeny in selected Paullinieae taxa; (2) to determine whether the gyno- ecium, seed and seedling provide additional characters of systematic value within the tribe; and (3) to relate the structural findings to mechanisms of fruit dehiscence and dispersal within these taxa. Newly described characters of systematic value within Paullinieae are shape and surface of the obturator, type of pollen tube transmitting tract, indumentum of the inner and outer surface of the carpels, ovary wall anatomy, aril anatomy, pseudo-hilum form, seedling germination mode and structure of first leaves. The fruits of Paullinia are septifragal, and conspicuous colour contrasts between the pericarp, aril and seed in most species of this genus are suggestive of a bird dispersal syndrome. Interestingly, it appears that relatively minor structural changes are associated with switches to rodent dispersal in Paullinia sphaerocarpa and water dispersal in P. clathrata and P. hystrix. Anemochorous fruits are sep- tifragal (Cardiospermum and Urvillea) or schizocarpic (Houssayanthus, Lophostigma, Serjania). They are structur- ally similar and Cardiospermum with septifragal capsules may also show septicidal dehiscence. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 159–189. ADDITIONAL KEYWORDS: Cardiospermum – fruit biology – gynoecium and fruit morphology – Paullinia – Serjania – Urvillea. INTRODUCTION cies; Sapindaceae). Considerable research has been done on the biology and systematics of Sapindaceae PAULLINIEAE – A POORLY KNOWN TRIBE OF from Australasia (Leenhouts, 1967; Leenhouts & SAPINDACEAE Vente, 1982; Reynolds & West, 1985; Adema, 1991; In recent years, biodiversity research has gained van Welzen, 1991; van Welzen, Piskaut & Windadri, increased attention both within and outside the scien- 1992; Adema & van der Ham, 1993; Adema, Leen- tific community, mainly because of the awareness that houts & van Welzen, 1994; Etman, 1994), yet less is vast areas of natural habitats, predominantly in the known about the Neotropical taxa. In recent years tropics, are rapidly being lost. A central objective of many new taxa have been described from tropical biodiversity research is species inventory, a task that America (e.g. Ferrucci & Acevedo-Rodríguez, 1997; involves detailed morphological study to allow for Somner & Ferrucci, 1997; Acevedo-Rodríguez, 1998, identification and classification. Such research lays 2003; Acevedo-Rodríguez & Ferrucci, 2002; Weckerle the foundations for further systematic, ecological, evo- & Reynel, 2003). These new taxa have been distin- lutionary and applied research. guished primarily on the basis of fruit morphology. Large groups of tropical plants are still poorly Few detailed studies of fruit and seed structure exist, known and among such groups are the mainly Neotro- and even fewer studies have attempted to relate dif- pical liana of the tribe Paullineae (six genera/430 spe- ferences in these structures to differences in dispersal biology (Weckerle & Rutishauser, 2003). The Paullin- ieae display a high diversity of fruit and seed morphol- *Corresponding author. E-mail: [email protected] ogy, and so are particularly ripe for such a study. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147, 159–189 159 Downloaded from https://academic.oup.com/botlinnean/article-abstract/147/2/159/2420185 by guest on 09 February 2018 160 C. S. WECKERLE and R. RUTISHAUSER The most comprehensive studies involving morpho- diospermum also occur. All genera bear spirally logical and anatomical characters of Paullinieae were arranged, imparipinnately compound leaves with conducted by Radlkofer over one hundred years ago stipules. The pinnate leaves are often five-foliolate, (Radlkofer, 1875, 1886, 1895a, b). In addition to vege- but may vary from three-foliolate (Urvillea) to tative and floral characters, he provided information multifoliolate. on the shape of fruits and seeds as well as the indu- Paullinieae are characterized by unisexual, mentum and anatomy of the pericarp (e.g. Radlkofer, obliquely monosymmetric flowers with four to five 1895a). His generic and infrageneric classification of, sepals, four petals with basal appendages, and two to for example, Paullinia is mainly based on pericarp four cushion-like extrastaminal nectaries. Male flow- characters. Because Radlkofer mainly investigated ers have eight functional stamens and a rudimentary herbarium material, detailed analyses of gynoecium pistil whereas female flowers show (besides indehis- characters, aril structure and fruit dehiscence were cent anthers) a three-carpellate gynoecium with a sin- not possible. In 1993, Acevedo-Rodríguez published gle ovule per carpel. The plants are monoecious revisions of two Paullinieae groups: one section of (rarely dioecious; C. S. Weckerle, pers. observ.). The Serjania (Acevedo-Rodríguez, 1993a) and the genus genera and species are separated mainly by fruit Lophostigma (Acevedo-Rodríguez, 1993b). The sec- characters. Houssayanthus, Lophostigma and Serja- tions of Serjania as defined by Radlkofer (1875) and nia are characterized by schizocarpic fruits with Acevedo-Rodríguez (1993a) are based chiefly on fruit winged (samaroid) mericarps, Cardiospermum and morphology. Urvillea by papery, inflated capsules, and Paullinia by Macromorphological descriptions of Paullinieae can capsules. be found in floras (e.g. Macbride, 1956; Croat, 1976; Usually the capsules in Paullinia contain dark Reitz, 1980; Ferrucci, 1991) and in the dissertation of seeds that are partly or completely enveloped by a Beck (1991a) regarding the generic limits in the tribe. translucent or white ‘aril-like structure’. Use of the Palynological studies are provided by Muller & Leen- term ‘aril-like structure’ in Paullinia and other Sapin- houts (1976), Ferrucci & Anzótegui (1993) and van der daceae is inconsistent and disputable (e.g. Radlkofer, Ham & Tomlik (1994). 1878, 1895b; van der Pijl, 1957; Corner, 1976; Werker, The aims of the present study were (1) to provide a 1997). Avoiding these terminological problems the detailed documentation of gynoecium, fruit and seed terms ‘aril’ and ‘sarcotesta’ are used here with the fol- structure and ontogeny in selected Paullinieae taxa; lowing definitions suited for Sapindaceae: ‘sarcotesta’ (2) to determine whether the gynoecium, seed and for fleshy layers that are produced by the entire seed seedling provide additional characters of systematic surface (testa), ‘aril’ for the usually fleshy and white value within the tribe; and (3) to relate the structural outgrowths that are produced by certain regions of the findings to mechanisms of fruit dehiscence and dis- seed surface. The testa region to which the aril is persal within these taxa. attached we term ‘pseudo-hilum’, consistent with van der Pijl (1957). The term ‘hilum’, referring to the scar- like mark on a seed where it was inserted, is not used DISTRIBUTION OF PAULLINIEAE AND MORPHOLOGICAL in our paper. The shiny dark seed coat, which may be BACKGROUND partially enveloped by the aril, will be labelled as ‘dry The almost exclusively neotropical Paullinieae har- testa’. bour most of the sapindaceous climbers and comprise The ovules of Sapindaceae are campylotropous, the species-rich genera Serjania (220 spp.) and Paull- crassinucellar and bitegmic. In most Sapindaceae, no inia (180 spp.), and the small genera Cardiospermum clear distinction between placenta and funicle is pos- (14 spp.), Houssayanthus (three spp.), Lophostigma sible. We follow the terminology of Corner (1976), who (two spp.) and Urvillea (17 spp.) (Radlkofer, 1933; Fer- describes similar ovules as shortly and thick funicu- rucci, 1987). A few species of Cardiospermum show a late (see Discussion: ‘Ovules’). pantropical distribution. Paullinia pinnata L. is the only member of its genus occurring in America as well as in tropical Africa and Madagascar (Irvine, 1961). SYSTEMATIC BACKGROUND The species-rich genera Paullinia and Serjania form Pantropical Sapindaceae (140 genera/1800 species) woody lianas. There is some overlap in the distribution are by far the largest family of the order Sapindales of Paullinia and Serjania, but the vast majority of (Judd et al., 2002). Molecular analyses restrict the Paullinia species occupy humid dense tropical forests, order to the following six major families: Anacardi- especially in Amazonia, whereas the anemochorous aceae, Burseraceae, Meliaceae, Rutaceae, Sapin- Serjania occurs in drier areas, along forest edges and daceae (including Aceraceae and Hippocastanaceae) in weedy and disturbed areas (Acevedo, 1993a). In the and Simaroubaceae (Gadek et al., 1996; Chase, Mor- latter habitats the more
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