The Root Holoparasite Thonningia Sanguinea (Balanophoraceae) and an Inflorescence-Feeding fly in the Tropical Rainforests Of
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bs_bs_banner Plant Species Biology (2012) 27, 164–169 doi: 10.1111/j.1442-1984.2011.00338.x NOTES AND COMMENTS A novel brood-site pollination mutualism?: the root holoparasite Thonningia sanguinea (Balanophoraceae) and an inflorescence-feeding fly in the tropical rainforests of West Africapsbi_338 164..169 RYUTARO GOTO,* GEN YAMAKOSHI† and TETSURO MATSUZAWA‡ *Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo, Kyoto 606-8501, Japan, †Graduate School of Asian and African Area Studies, Kyoto University, 46 Shimo-Adachi-cho, Sakyo, Kyoto 606-8501, Japan and ‡Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan Abstract The Balanophoraceae is a unique angiosperm family that fully parasitizes the roots of trees. Although the pollination systems of several genera in this family have been reported, little is known of their diversity. In the present study, we investigated the pollination biology of Thonningia sanguinea (Balanophoraceae) in the tropical rainforests of Guinea, West Africa. Female flies of the families Muscidae and Calliphoridae as well as Technomyrmex ants frequently visited flowers to consume nectar secreted from inflo- rescences. While feeding, their bodies attached to anthers or pollen grains. The most abundant flower-visiting fly, Morellia sp. (Muscidae), was observed laying eggs on T. san- guinea, and the larvae fed only on the vegetative tissue of decaying male inflorescences. Our findings provide a new candidate of pollination mutualism involving plants that provide brood sites for their pollinators. Keywords: Balanophoraceae, brood-site pollination, male-plant-biased herbivory, Morellia, Thonningia. Received 14 December 2010; revision received 1 April 2011; accepted 11 April 2011 Introduction three decades, various brood-site pollination systems have been discovered in various plant groups Pollination mutualisms involving plants that offer pollen, (Silberbauer-Gottsberger 1990; Sakai 2002; Kato et al. nectar or both to pollinating insects as a reward for pol- 2003; Ishida et al. 2009; Kawakita 2010; Luo et al. 2010). lination are common in angiosperms (Protocor et al. Nevertheless, little is known about the diversity of this 1996). However, pollination mutualisms involving plants unusual pollination system among the great diversity of that offer a brood site to insects as the pollination reward angiosperms. In the present study, we provide a new are very rare (Sakai 2002). Nevertheless, these mutual- brood-site pollination system candidate from the African isms are often treated as model systems of coevolution Balanophoraceae. and mutualism because they often exhibit highly intimate The Balanophoraceae is a subtropical to tropical family interactions or extreme co-specialization between plants of obligate parasitic angiosperms, consisting of 18 genera and pollinating insects (Thompson 1994, 2005). The obli- and approximately 50 species (Shumei & Murata 2003). gate mutualisms of the fig–fig wasp and yucca–yucca The family is characterized by unique fungus-like inflo- moth systems, whereby the plants offer seeds or ovules rescences, with numerous tiny unisexual flowers (Holza- as brood sites for pollinators, are the best-known pfel 2001; Kawakita & Kato 2002). All members of this examples (Janzen 1979; Pellmyr 2003). Over the past family are entirely non-photosynthetic and parasitize the roots of host trees, depending exclusively on nutrients Correspondence: Ryutaro Goto exploited from the host. Although detailed information is Email: [email protected] limited to several genera, previous studies suggest that © 2011 The Authors Journal compilation © 2011 The Society for the Study of Species Biology POLLINATION IN AFRICAN BALANOPHORACEAE 165 the pollination system is diverse in this family. In Balano- female (dioecious) and produce inflorescences at approxi- phora, an Indian species is pollinated by small honeybees mately 4 cm above ground level (Fig. 1a–d,g). Inflores- (Govindappa & Shivamurthy 1975), whereas Japanese cence tops are densely covered with numerous minute species are pollinated by ants and pyralid moths (Kawa- flowers. Both male and female flowers essentially lack kita & Kato 2002). The two genera of pyralid moths use perianths (Hutchinson & Dalziel 1958), and the inflores- the nutritive tissue of the flowers as brood sites (Kawakita cence is covered by protruded anthers in male plants and & Kato 2002). In contrast, some Costa Rican species (e.g. styles in female plants, giving overall white and yellow Helosis and Corynaea) are pollinated by tachinid flies appearances, respectively, to the flowers (Fig. 1a–d,g). The (Gomez 1983), a New Zealand species, Dactylanthus tay- plants are surrounded by thick, red, scaly leaves (Fig. 1), lorii, is pollinated by short-tailed bats (Ecroyd 1996), and and the infructescence is reddish, spherical and covered an Amazonian species, Lophophytum mirabile, is pollinated with numerous seeds (Fig. 1h). by small beetles (Chrysomelidae, Nitidulidae, Staphylin- idae and Curculionidae; Borchsenius & Olesen 1990). The latter species is believed to offer the beetles nutritive Field observations, collection of flower visitors and tissue for brood sites or mating sites, although detailed insect rearing observations are lacking. Interestingly, despite a paucity of Observations were basically limited to male inflorescences pollination studies, two different brood-site pollination because of the very low density of female inflorescences in systems have been discovered in this family (Borchsenius August 2005. On the gloomy forest floor in the Guein & Olesen 1990; Kawakita & Kato 2002). Certain morpho- Hills, we observed two patches of T. sanguinea, one com- logical characters of Balanophoraceae, such as the fleshy posed of a single male inflorescence and one inflorescence axis of the inflorescence, may perhaps favor the evolution bud (Fig. 1a) and the other comprising one female inflo- of brood-site pollination mutualism. To further clarify the rescence. Flower visitors to the male inflorescences were ecological conditions under which brood-site pollination observed for 11 h (07.00–18.00 hours) on 31 August 2005 evolved and the reproduction biology of this unusual and those to the female inflorescence for 0.5 h (12.00– parasitic plant family, investigations of more genera in 12.30 hours) on 1 September 2005. We recorded flower- Balanophoraceae are required. visiting insects and collected each species for Thonningia, a dioecious genus of Balanophoraceae, is identification, mainly in the late afternoon. Insect visits to endemic to the tropical rainforests of Africa (Hutchinson the flowers were counted when any body part of the & Dalziel 1958; Letouzey 1986). This genus includes only visiting insect contacted the anther. We also recorded one variable species, Thonningia sanguinea, which parasit- insects visiting the inflorescence bud that adjoined the izes the roots of a wide range of host trees (Olanya & Eilu male inflorescence (Fig. 1a). After field observations, dried 2009). In the present study, we investigated the pollination specimens of the collected flower visitors were observed system of T. sanguinea and the biology of the muscid flies under a microscope to check for pollen attachment to their that use T. sanguinea as a brood site. bodies. To investigate insect feeding on T. sanguinea, nine male inflorescences, one female inflorescence and eight fruits Materials and methods were collected from six patches of T. sanguinea. Soon after Study species and study sites collection, we dissected a subset of the samples and looked for insects feeding on them. If such insects were The study site is located in the tropical rainforest of the found, we recorded the number and stored them in 100% Gban and Guein Hills, near Bossou village in southeast- ethanol for subsequent identification. The remaining ′ ′ ern Guinea, West Africa (7°39 N, 8°30 W; 500–700 m a.s.l.). inflorescence and fruit samples were kept at local tem- Traditionally the forests of this area have been protected perature in separate plastic bags to obtain adult insects. by the local village people as part of their religion (Yama- koshi 2011). The local temperature averages 20–30°C and rainfall is 2000–2500 mm per year (Yamakoshi 1998; Take- Results moto 2004). The climate is characterized by distinct rainy Observations of flower visitors (March–October) and dry (November–February) seasons Yamakoshi 1998). This site is well known for long-term During the 11-h observation period of a male inflores- field studies of wild chimpanzees that began in 1976 (Sug- cence, flies made 66 floral visits, and massive ant floral iyama 1981; Matsuzawa et al. 2011). visits were observed several times (Figs 1a–d and 2a). Thonningia sanguinea is a low-growing perennial plant Both flies and ants fed on nectar secreted from the inflo- that parasitizes the roots of a wide range of host trees rescences (Fig. 1a–d). While feeding, their bodies fre- (Fig. 1; Olanya & Eilu 2009). Plants are either male or quently contacted an anther (Fig. 1a–d). Floral visits by Plant Species Biology 27, 164–169 © 2011 The Authors Journal compilation © 2011 The Society for the Study of Species Biology 166 R. GOTO ET AL. Fig. 1 Thonningia sanguinea and its pollinators. (a) One male inflorescence and one bud of T. sanguinea; (b) Morellia sp. (Muscidae) visiting a male inflorescence of T. sanguinea; (c) Calliphora sp. 1 (Muscidae) visiting a male inflorescence of T. sanguinea; (d) Technomyrmex sp. (Formicidae) visiting a male