For example, obligate associations between extant cycad species and their pollinators (Schneider & al., 2002) are at least as old and. Pollination declines are shown for Sequoiadendron giganteum (Pinopsida: Cupressaceae) in (D) abbreviation: mp, micropyle) (Takaso & Owens, 1996); Phyllocladus glaucas (Pinopsida: Podocarpaceae) in (E) (abbreviation: c, ovule cone) (Tomlinson et al., 1997); Ginkgo biloba (Ginkgoopsida: Ginkgoaceae) in (F); Taxus baccata (Pinopsida: Taxaceae) in (G) (Proctor et al., 1996); unidentified species of Ephedra (Gnetopsida: Ephedraceae) in (H) (Gifford & Foster, 1989);. Pollinators are usually small insects, especially flies (Bino & al., 1984a; . Meeuse, 1990), but also hymenopteran parasitoid wasps such as chalcidoids (Moussel, 1980) and small drop honey bees (Ordetx, 1952) .
Cheirolepidiaceae also exhibit distinct and unique specializations of the ovuliferous scale that strongly suggest insect pollination (Cerceau & al., 1976; Clement-Westerhof &. Such mouth structures were convergent with certain elements of the homologous but proboscis brachyceran diptera. to glossae of lepidopterans (Eastham & Eassa, 1955) which evolved significantly later, during the middle Cretaceous period (Kristensen & Nielsen, 1981; Labandeira & al., 1994).
TWO PROBABLE MESOZOIC POLLINATION SYNDROMES
As a channel to direct pollen toward the tube, the funnel acted as an “inverted stigma” and was lined throughout with prominent multiseriate trichomes ( Fig. 3E ), laden mostly with Classopollis but also with other pollen types. In the deeper recesses of the funnel, large, cylindrical, multicellular protrusions or papillae appeared that were significantly larger than the adjacent trichomes (Fig. 3D). Beneath the funnel and oblique ridge was the main body of the ovuliferous scale, in the axil of which a single, large, transversely elongate ellipsoid bract (removed in Fig. 3F ) was attached, extending all the way to the lower rim of the funnel opening. .
The pollen cone, Frenelopsis alata (Fig. 3G), was the source of Classopollis pollen which pollinated A. . bohémica ovules. The microsporophyll each had two (perhaps more?) pollen sacs (Fig. 3H), one on each side of its base. When the cones were mature, the pollen sacs released multiple pollen tetrads (Fig. 3J), either by sac wall degradation, insect disturbance during trichome manipulation, or direct insect consumption, or a combination of these. .
Insect-mediated bennettitalean damage, found on taxa such as Cycadeoidea dacotensis from the Upper Lower Cretaceous of South Dakota (Fig. 6A), but also on several other taxa belonging to the Cycadeoideaceae and Williamsoniaceae, provide rare autecological snapshots of the life histories of insect larvae as they progressed from egg hatching, to early larval penetration of external strobilar tissues, to consumption of various internal bennettitalean vegetative and reproductive tissues, to eventual emergence from the host plant and subsequent transformation to the adult stage. These fossil data are collectively integrated into a general account of insect consumption of living tissues in Cycadeoidea strobili and their associated pollination (Fig. 6), using the reconstruction of Crepet (1974) as a basis for mapping the larval life history. As subsequent larval stages underwent size increases, the third stage was initiated with the establishment of a tunnel system that occurred in the stalk (Fig. 6D) and thence into the zone between the inner ovule-bearing and interseminal scales originating from the receptacle. axis and the outer, more peripheral pollen-bearing microsporophylls (Figs. 5E; 6E).
The fifth and final stage of larval development was when the last instar built a relatively large tunnel that was established toward the outer, exposed tissues and where emergence occurred (Fig. 6H, I).
THE BROADER PALEOBIOLOGICAL CONTEXT
There are also three clades of basal weevils•Belidae, Nemonychidae and Eccoptarthridae as well as the enigmatic Obrieniidae•which rarely occur together with bennettitaleans in certain Late Jurassic and Early Cretaceous deposits (Doludenko & Orlovskaya, 1976 & al. Arnol'76; ., 1977 ; Zherikhin & Gratschev, 1997; Sun & al., 2001; Gratschev & Zherikhin, 2003). The widespread geographic distribution, targeting of a particular plant host clade, and highly stereotyped damage of this association together suggest a distinctive pollination strategy of beetles similar to that of extant cycads (Stevenson & al., 1998). It is also possible that this syndrome of beetle pollination of relatively closed reproductive structures was common during the Mesozoic, evidenced early on by Middle Triassic insect consumption of pollen in cycad reproductive organs (Fig. C; Klavins et al. , 2005), and evidence provided by a Late Cretaceous permineralized fructification probably referable to the closely related Pentoxylales, which harbored a completely preserved larva in a chamber adjacent to seeds in the soil tissue (Fig.
This larva was assigned to the beetle family Nitidulidae, for which adults of modern representatives are frequent pollen feeders (Gazit & al., 1982; Ekblom &. These palynivores include early taxa of insects that consumed pollen from peltasperma and ferns of glossopterid seeds, chordates, conifers and gnetopsids (Rasnitsyn & Krassilov, 1996; . Krassilov & Rasnitsyn, 1999; Krassilov & al., 2006) Paleozoic evidence for feeding on plant secretions is much less and indirect, such as the existence of the pollination mechanism .(Rothwell and the presence of epidermal secretory glands adjacent to reproductive structures (Mamay, 1976; Krings & al., 2002).
During the Late Jurassic and Early Cretaceous there is considerable documentation of gymnosperm polnivores from Eurasia (Fig. For example, the presence of a convoluted, inverted stigma-like structure considerably distant from the micropyle but connected to it by a tubular structure that resulted in final pollination, may have been inefficient compared to early angiosperm structures, such as simple stigmatic exudates secreted before flowering (Frame, 2003a), small and perfect flowers with nectaries (Gottsberger, 1988; Thien & al., 2000), or even more complex floral mechanisms involving pollinator capture (Thien & al., 2003; Gandolfo & al, 2004).Notably, insect exploitation of the pollination decline was not fully transferred to or terminated with the ecological expansion of angiosperms during the Late Cretaceous.
It currently survives or has re-evolved in the form of various small insects, especially flies, moths and parasitic wasps that have shortened labellate and sponging probóscides, on gnetopsid and, to a lesser extent, cycadopsid plants that provide micropylar secretions (Kato & al., 1995; Tang, 1995).
B SUMMARY AND CONCLUSIONS
The Chekarda locality from the Lower Permian of the Russian Central Ural Mountains contains several species of different lineages of insects that have pollen in their guts associated with equally diverse plant hosts (Krassilov & Rasnitsyn, 1999; Afonin, 2000). By the end of the Paleozoic, insect targeting of fern spores and seed pollen was well established and a common occurrence in at least some terrestrial habitats. There is little evidence of pollen or nectar consumption in the Triassic, other than pollen-laden coprolites in the pollen organs of a taxon that is "extremely similar" to that of extant cycads (Fig.
In contrast, Phase 4 of these associations is the most recent expansion of plant-palynivore and related associations, which began during the mid-Early Cretaceous expansion of angiosperms and continued until the Recent. The disappearance of at least some of the older, Mesozoic lineages of gymnosperms and their pollinating insects can probably be attributed to the appearance of angiosperms in the Early Cretaceous. Angiosperms provided a nutritionally more efficient system for surface fluid consumption and transfer of pollen rewards between conspecific hosts compared to older entomophilous gymnosperm lineages, an idea compatible with Frame's (2003b) hypothesis of a general higher edibility of angiosperms.
Entomophilic cheirolepidiaceous taxa became extinct during the Late Cretaceous, perhaps because they were disadvantaged in the context of more efficient angiosperm insect pollination systems. It currently survives or has re-evolved in the form of various small insects, especially flies, moths and parasitoid wasps with shortened labellates and spongy probóscides, on gnetopsids and, to a lesser extent, breadfruit plants that provide micropylar secretions (Kato et al., 1995 .There is emerging evidence for a largely extinct phase of preangiospermic pollination syndrome involving several major clades of seed plants and insect pollinators.
The modern perspective is based on a very selective, small sample of recent gymnosperms and their insect relatives.
B ACKNOWLEDGEMENTS
The Coleóptera, Mecopteroidea and Diptera provide the most convincing evidence for an early pollinator role, with nectar or pollen being the main rewards. One reason for this replacement was that some gymnosperm taxa possessed structurally and functionally complex pollination systems that were replaced by more efficient angiosperm systems. For the Cheirolepidiaceae, long proboscis flies with a small or alternatively large body carried aerial pollen from other plants, foreshadowing the evolution of pollination mechanisms in angiosperms.
For the Cycadeoideaceae, in situ beetle larvae consumed internal vegetative and reproductive tissues and in the process transported pollen within the closed strobilus, analogous to pollination mechanisms in breadfruit trees. This long-running third phase involved a characteristic colonization of gymnosperm plant hosts by insects, followed by extensive reduction and replacement by mid-Cretaceous angiosperms.
B LITERATURE CITED
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B FIGURE CREDITS
