Scarab Beetle Pollination of the Neotropical Aroid Taccarum Ulei (Araceae: Spathicarpeae)
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bs_bs_banner Biological Journal of the Linnean Society, 2013, 108, 22–34. With 5 figures The cowl does not make the monk: scarab beetle pollination of the Neotropical aroid Taccarum ulei (Araceae: Spathicarpeae) ARTUR CAMPOS DÁLIA MAIA1*, MARC GIBERNAU2, AIRTON TORRES CARVALHO3, EDUARDO GOMES GONÇALVES4† and CLEMENS SCHLINDWEIN4 1Departamento de Química Fundamental, Universidade Federal de Pernambuco, 50740-560 Recife, Brazil 2CNRS – Ecofog (UMR 8172), Campus Agronomique BP 316, F-97379 Kourou cedex, France 3Programa de Pós-graduação em Ciências Biológicas (Zoologia), Universidade Federal da Paraíba, 58059-900 João Pessoa, Brazil 4Departamento de Botânica, Universidade Federal de Minas Gerais, 31270-901 Belo Horizonte, Brazil Received 19 May 2012; revised 28 June 2012; accepted for publication 28 June 2012 Taccarum ulei (Araceae, Spathicarpeae) is a seasonal geophytic aroid, native to north-eastern Brazil, that flowers during two months of the rainy season. Patterns of floral thermogenesis, pollination biology, and floral traits associated with pollination syndromes were studied and compared with those of other Araceae. Two species of cyclocephaline scarabs (Scarabaeidae, Cyclocephalini) were recognized as effective pollinators: Cyclocephala celata and Cyclocephala cearae. Larvae of an unidentified species of fruit fly (Melanoloma spp., Richardiidae, Diptera) were also frequently observed in inflorescences at various maturation stages, feeding on the connectives of male florets and fruits, and thus lowering the reproductive success of individual plants. Beetles were attracted by odoriferous inflorescences in the early evening of the first day of anthesis, during the female phase. The emission of attractive volatiles was coupled with intense thermogenic activity in the entire spadix, unlike other aroids in which only certain zones of the spadix heat up. Pollen release, which marks the beginning of the male phase on the subsequent evening, was not related to floral thermogenesis. Comparative multivariate analysis of the floral traits of T. ulei points to a beetle-pollinated aroid, although some of the observed traits of the species are not common to other taxa sharing this pollination strategy. Such incongruence might be explained by the evolutionary history of the tribe Spathicarpeae and potential pollinator shifts. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 108, 22–34. ADDITIONAL KEYWORDS: flower predation – nocturnal pollinators – pollination syndromes – Scarabaeidae – thermogenesis. INTRODUCTION ponderantly entomophilous, aroid inflorescences have co-evolved in their interactions with arthropod visi- The aroids (Araceae) are a rich group of cosmopolitan tors, both generalist and highly specialized, from flies monocots that presently encompass over 3300 species and beetles to bees, thrips, and perhaps even mites of herbs and vines, mostly found in tropical and (Grayum, 1990; Mayo, Bogner & Boyce, 1997). Accord- subtropical environments (Haigh et al., 2012). Pre- ing to the most recent overview of the family, however, our knowledge of effective pollinators is restricted to less than 50% of the currently described *Corresponding author. genera (Gibernau, 2011). E-mail: [email protected] th †Current address: Pro Reitoria de Pesquisa e Pós Graduação, It has been known since the end of the 19 century Universidade Católica de Brasília, 70790-160 Brasilia, Brazil. that several aspects of basic floral structure are 22 © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 108, 22–34 POLLINATION OF TACCARUM ULEI 23 directly associated with the reproductive biology of dieae (~150 spp.), and several of the Spathicarpeae angiosperms (Müller, 1873; Vogel, 1954). Such floral (~165 spp.) (Gibernau, 2011). characters have been selected through evolution by Although rather diverse and taxonomically well- the increasing effectiveness of pollen transfer to the defined, the tribe Spathicarpeae has been commonly stigmas, and as such are also particularly influenced disregarded with respect to their reproductive biology by the strategies that optimize the use of specific and phenology (Grayum, 1990; Mayo et al., 1997; Gib- pollen vectors (Fenster et al., 2004). Among aroids, ernau, 2011). The tribe is mostly restricted to extra- Chouteau, Gibernau & Barabé (2008) and Gibernau, Amazonian South America, and is presently composed Chartier & Barabé (2010) have presented associations of 13 genera: Asterostigma (10 spp.), Bognera (1 sp.), between a wide set of floral traits and specific polli- Croatiella (1 sp.), Dieffenbachia (~135 spp.), Gearum nation syndromes, to the point that a few extrapola- (1 sp.), Gorgonidium (5 spp.), Incarum (1 spp.), Loren- tions could be safely assumed when enough of these zia (1 sp.), Mangonia (2 spp.), Spathantheum (2 spp.), characters are understood. For instance, large pollen Spathicarpa (4 spp.), Synandrospadix (1 sp.), and grains sticky with stigmatic exudates, typical of Taccarum (6 spp.) (Gonçalves, 2002, 2012; Gonçalves aroids pollinated by large scarab beetles, are unlikely et al., 2007). The monophyly of the Spathicarpeae is to be carried efficiently by smaller-sized insects. On strongly supported by the most recent molecular phy- the other hand, the glabrous body surface of beetles is logenies of the Araceae family (Cabrera et al., 2008; inadequate to carry the loads of powdery pollen found Cusimano et al., 2011). in some fly-pollinated taxa (Sannier et al., 2009). The Together with the Anchomanes clade and the pollen to ovule ratio (P : O) of bee- and fly-pollinated Homalomena clade, the Spathicarpeae form the Zant- species is similar, suggesting that bees and flies have edeschia clade, a pantropical, heterogeneous group of comparable pollination efficiency (Chouteau et al., evergreen or dormant ground and climbing herbs 2008). The much higher P : O of beetle-pollinated (Mayo et al., 1997; Cusimano et al., 2011). From species lends credence to the hypothesis that beetles the standpoint of reproductive biology, the Zantede- may be less efficient pollinators, thus requiring a schia clade is intriguing. Pollination within the much higher investment in pollen production by their Anchomanes clade is mainly achieved by flies and/or plant hosts (Gibernau et al., 2010). beetles, whereas in the Homalomena clade flies are Adaptations towards specific sets of pollinators also the main pollinators of Indo-Malayan species, and result in deeper modifications of flower morphology only cyclocephaline scarab beetles have been impli- and physiology, and this is clearly evident in the cated in the reproductive success of the Neotropical Araceae (Grayum, 1990; Mayo et al., 1997). Mediter- taxa (Gibernau, 2011; Fig. 1). In this phylogenetic ranean Helicodiceros muscivorus (L. f.) Engl., polli- context, the study of pollination systems of the most nated by blowflies, bears foul-smelling inflorescences derived genera of the Spathicarpeae may provide new that closely resemble the anal orifice of a large insights into the evolution of floral characters in mammalian carcass (Angioy et al., 2004). The kettle- relation to pollinator selection within the tribe. shaped inflorescences of European Arum and Indo- The genus Taccarum Brongn. ex Schott, one of Malayan Arisaema are designed to entrap small the most derived taxa within the Spathicarpeae pollinating flies to enhance their contact with recep- (Gonçalves et al., 2007; Cusimano et al., 2011), com- tive female flowers (Vogel & Martens, 2000; Gibernau, prises six species of seasonally dormant geophytes Macquart & Przetak, 2004), whereas the funnel- found in most of the extra-Amazonian Brazilian ter- shaped inflorescences of all known species of the large ritory, as well as in Peru, Bolivia, Paraguay, and Neotropical genus Philodendron offer food and warm northern Argentina. These plants can be recognized shelter for mating scarab beetles (Gottsberger & by the usually large and solitary leaf that is strongly Amaral, 1984; Gibernau et al., 1999; Seymour, White bipinnately divided. They grow preferably in well- & Gibernau, 2009; Maia et al., 2010). drained soils and at low-to-medium altitudes (up to In the Neotropics, the diverse scarab beetles of 850 m a.s.l.), usually in areas with pronounced sea- the tribe Cyclocephalini (Scarabaeidae, Dynastinae; sonality. Populations often consist of scattered indi- ~350 spp.) comprise one of the most preponderant viduals, seldom bearing inflorescences (Gonçalves, groups of scent-driven pollinators of several Mag- 2002). noliaceae, Annonaceae, Cyclanthaceae, Arecaceae, We studied the flowering, phenology, and the pol- Nymphaeaceae, and Araceae (Gottsberger, 1986; lination biology of Taccarum ulei Engl. & K. Krause, Schatz, 1990; Bernhardt, 2000). Among the latter a geophytic aroid native to north-eastern Brazil, and group of plants, these night-active pollinators are addressed the following questions: (1) what is the directly involved with the reproductive success of floral cycle and the pattern of floral thermogenesis the Montrichardieae (two species) and Philo- for the species; (2) what are the flower visitors and dendreae (over 500 spp.), the majority of the Cala- effective pollinators; (3) how do the floral traits © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 108, 22–34 24 A. C. D. MAIA ET AL. Indo-Malaya / Australasia Anchomanes Aglaonema fly Afrotropic Aglaodorum fly / beetle Nephthytis fly / beetle clade Afrotropic Anchomanes fly / beetle Homalomena Culcasia