Plants in Mesozoic Time: Morphological Innovations, Phylogeny, Ecosystems

3. Pollen and Coprolite Structure in Cycadeoidea (Bennettitales): Implications for Understanding Pollination and Mating Systems in Mesozoic Cycadeoids

35 Pollen and CoProlite StruCture in CyCadeoidea (BennettitaleS): imPliCationS For underStanding Pollination and mating SyStemS in meSozoiC CyCadeoidS Jeffrey m. osborn and mackenzie l. taylor The Mesozoic seed plant group Bennettitales is most comprehensively known from permineralized fossils of Cycadeoidea from the Early Cretaceous of North America. Cones were bisporangiate and have been interpreted as remaining closed at maturity. Consequently, self-pollination has been hypothesized in Cycadeoidea through developmental disintegration of the fused cones. Additionally, entomophily has been hypothesized as a secondary pollination syndrome because extensive beetle tunnel and gallery systems occur within reproductive tissues. In what is to our knowledge the first study of the structure and contents of coprolites and frass pellets extracted from beetle tunnels within Cycadeoidea cones, pollen grains and pollen wall fragments were found to be absent. New data on direct insect interactions, combined with data on pollen ultrastructure, are discussed here as they relate to interpretations of pollination mechanisms and mating system biology in Cycadeoidea and the Bennettitales. Because pollination biology determines the frequency and diversity of mating opportunities, the two pollination syndromes would potentially have had different consequences for mating systems in Cycadeoidea. Selfpollination alone would have almost certainly resulted in obligate selfing, whereas occasional to predominant insect pollination would have likely resulted in a mixed mating system. The Mesozoic seed plant group Bennettitales is most comprehensively known from permineralized fossils of Cycadeoidea from the Lower Cretaceous of North America. Fossils have been collected from a wide range of localities, and many taxonomic species have been described. However, the majority of data on Cycadeoidea are derived from investigations of specimens collected in the Black Hills of South Dakota and Wyoming, U.S.A. (Wieland 1906, 1916; Crepet 1974). The reproductive structure and pollination system of Cycadeoidea have received much attention over the years. Wieland’s (1906) early introduction 3 Osborn and Taylor 36 anatomical and morphological work characterized the reproductive organ of Cycadeoidea as flowerlike, and he reconstructed the plant with open “flowers” protruding from the surface of the stem. At maturity, each open “flower” was interpreted to consist of pinnately compound, pollenbearing microsporophylls surrounding a centrally positioned ovulate receptacle (Wieland 1906). Such an open structure would have permitted wind pollination, as has also been hypothesized for some members of the Williamsoniaceae, the second and more ancient (Late Triassic–Late Cretaceous) family within the Bennettitales (e.g., Watson and Sincock 1992; Labandeira et al. 2007; Taylor et al. 2009). Wieland’s (1906) interpretation and reconstruction were subsequently shown to be incorrect. Upon further investigation of Wieland’s specimens, as well as of other unstudied fossils, Delevoryas (1968) and Crepet (1974) demonstrated that all Cycadeoidea cones were bisporangiate and remained permanently closed at maturity. The cones were shown to have a highly complex ontogenetic structure. The pinnate microsporophylls did not open but rather recurved during development, and the distal tips became ontogenetically fused near the base of the ovulate receptacle (Delevoryas 1968; Crepet 1974). Consequently, self-pollination has been hypothesized in Cycadeoidea through developmental disintegration of the fused cones (Crepet 1972, 1974). In addition, entomophily has been hypothesized as a secondary pollination syndrome because extensive beetle tunnel and gallery systems occur within reproductive tissues of Cycadeoidea cones (Crepet 1972, 1974). Labandeira et al. (2007) have recently proposed a generalized plant– insect association between Cycadeoidea and beetles (likely belonging to suborder Polyphaga, or its subclade Phytophaga) analogous to the association that characterizes extant cycads (Stevenson et al. 1998) and perhaps extinct cycads as well (Klavins et al. 2005). The model of Labandeira et al. (2007) is based on cone structure and other anatomical characters for Cycadeoidea, a range of data on fossil beetles, and the commonality of insect damage to bennettitalean cones described from a range of geographically and geologically disjunct localities (Reymanówna 1960; Bose 1968; Saiki and Yoshida 1999; Stockey and Rothwell 2003). However, there is actually very little direct information about the fossil insects associated with Cycadeoidea or other bennettitaleans (see Labandeira et al. 2007 and references therein). The objective of the present study is to investigate the structure and contents of coprolites and frass pellets extracted from beetle tunnels within Cycadeoidea cones, as well as to review and reexamine the pollen structure of Cycadeoidea. The new data on insect evidence of phytophagy, combined with the pollen data, are then discussed as they relate to interpretations of pollination mechanisms and mating system biology in Cycadeoidea and the Bennettitales. Pollen and...