The Paleobiology of Pollination and Its Precursors

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The Paleobiology of Pollination and Its Precursors IN: Gastaldo, R.A. and DiMichele, W.A., (eds.), 2000. Phanerozoic Terrestrial Ecosystems. Paleontological Society Papers 6: 233-269. THE PALEOBIOLOGY OF POLLINATION AND ITS PRECURSORS CONRAD C. LAB ANDEIRA Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560 USA and University of Maryland, Department of Entomology, College Park, MD 20742-4454 USA. PERHAPS THE MOST conspicuous of to the earlier Cenozoic and later Mesozoic, there is associations between insects and plants is a resurgence in understanding the evolutionary pollination. Pollinating insects are typically the first history of earlier palynivore taxa (spore, prepollen and most obvious of interactions between insects and pollen consumers), which led toward pollination and plants when one encounters a montane as a mutualism (Scott et al., 1992). meadow or a tropical woodland. The complex Almost all terrestrial vascular plants have two ecological structure of insect pollinators and their opportunities during their life cycle to disperse to host plants is a central focus within the ever- new localities. These events are spore or pollen expanding discipline of plant-insect interactions. dispersal to fertilize a megagametophyte at the The relationships between plants and insects have haploid phase, and the dispersal of the fertilized, provided the empirical documentation of many diploid megagametophyte after it has been case-studies that have resulted in the formulation transformed into a seed in seed-bearing plants. of biological principles and construction of Agamic modes of plant colonization also occur, theoretical models, such as the role of foraging such as vegetative propagation through strategy on optimal plant-resource use, the disseminules including root fragments or leaves advantages of specialized versus generalized host with adventitious rootlets. However, these preferences as viable feeding strategies, and mechanisms lack the genetic advantages conveyed whether "pollination syndromes" are meaningful by sex. These two crucial junctures in the life-cycle descriptions that relate flower type to insect of a stationary plant are indispensable for extending mouthpart structure and behavior (Roubik, 1989; its geographic range, colonizing new habitats, and OUerton, 1996; Waser et al., 1996; Johnson and maintaining genetic variability through Steiner, 2000). Much of the recent extensive outcrossing, thus avoiding the perils of inbreeding discussion of plant-insect associations has centered depression. Fertilization of the female gamete by on understanding the origin, maintenance, and a motile male gamete is important because it evolutionary change in plant/pollinator establishes the gametophyte phase of the life associations at ecological time scales and cycle. Once fertilization has occurred, the increasingly at longer-term macroevolutionary resulting zygote develops into the ephemeral time intervals (Armbruster, 1992; Pellmyr and sporophyte generation, which produces spores in Leebens-Mack, 1999). Such classical plant-insect plants such as lycopods, ferns, and sphenopsids, association studies•cycads and cycad weevils, figs or seeds and pollen in gymnosperms and and ñg wasps, and yuccas and yucca moths•^were angiosperms. Thus, the sporophyte generation explored at modem time scales and currently are gets a second chance for dispersal through the being examined through a long-term geologic abiotic broadcasting of these propagules by agents component that involves colonization models based such as wind, water, gravity, fire, or animals. This on cladogenetic events of plant and insect associates, review will focus on the first phase of this twofold buttressed by the fossil record (Farrell, 1998; dispersal process, addressing how it originated Pellmyr and Leebens-Mack, 1999; A. Herre, pers. and evolved into the assorted associations and comm.). In addition to tracing modem pollination magnificent mutualisms of today. 233 PALEONTOLOGICAL SOCIETY PAPERS, V. 6, 2000 TYPES OF EVIDENCE insects in seed-fern prepoUen organs such as Bernaultia (Fig. IC), or the consumption by The fossil history of plant-insect associations mandibulate insects of sterile megasporophyll and can be viewed as three relatively distinct, but linked fertile ovular tissues in bisporangiate cycadeoid fossil records. The two obvious candidates are the cones, involving tunneling behavior (Crepet, separate plant and animal body-fossil records. The 1974). Because of the often highly patterned and third is the record of plant-insect associations, stereotyped nature of plant damage, it also can subdivided into five principal types of evidence: reveal certain behavioral attributes of interacting (1) plant reproductive biology, (2) plant damage, insects, including palynivores. However, plant (3) dispersed coprolites, (4) insect gut contents, and damage by itself is insufficient for attributing (5) insect mouthparts (Labandeira, 2001). A sixth damage to a specific insect culprit, and often type of evidence, discussed herein incidentally, is requires supplemental information for a more taxonomic assignment to a modem descendant for certain identification. which reliable ecological data exist. Each of these Plant morphology, especially the structure of five types of evidence provides data for the reproductive units, is critical for assessing the identities of either the plant hosts or their insect possibility of insect palynivory or the participation palynivores, or both, in unique circumstances. of insects in pollination mutualisms. Several, often These five types of evidence are a continuum from co-occurring, structures of extinct plants provide the plant-host end member (plant reproductive circumstantial evidence for insect pollination. biology) to an emphasis on the insect as the Evidence from plant morphology includes: the size dominant type of evidence (mouthpart structure). and surface properties of pollen; accessibility of Each type of evidence has a very uneven the female reproductive structures to the ambient spatiotemporal distribution and taphonomic environment or to insects; presence of food, nesting occurrence in the fossil record (Labandeira, 2001). materials, or other rewards to lure potential For example, the value of dispersed coprolites, pollinating agents; general advertisements to particularly in coal-ball deposits of Pennsylvanian potential pollinators through modifications of age (Fig. 1A,B), is that they reveal the reproductive structures; and features that promote microanatomy of consumed plants in exquisite pollen transfer or enhance certain types of detail, albeit the identities of the palynivores are pollination. All these attributes have been found murky due to limitations in attributing coprolite in the plant fossil record and have been inferred to shape, size, and texture to insects beyond major indicate the presence of insect-mediated taxonomic divisions. Gut contents, by contrast, pollination. Some are linked to each other, such as occur in fine-grained compression deposits where the association of relatively large pollen size to highly refractory pollen exines are resistant to reproductive structures inaccessible to wind in degradation and preserved in a similar manner to Paleozoic medullosan seed ferns. Similarly, in insect chitin and plant cuticle (Fig. ID). Occasional modern orchids the presence of nectaries (a examples from younger amber deposits also are nutritional reward) occurs in association with deep- known (Grimaldi et al., 1994). Insect gut contents throated flowers (a structural modification) and represent the most secure class of evidence, distinctive floral scents (an advertisement), resulting in precision of taxonomic identification attracting insects with long, projecting mouthparts for both the host plant and insect culprit, (Darwin, 1877). particularly because pollen can be linked to a Structural modifications in insects indicative source plant clade and a palynivore is identifiable of palynivory and imbibation of nectar, which may by external body characters. result in pollination, involve principally the Plant damage rarely reveals the exact identities mouthparts and accompanying features of the head of the insect associates of plants. Examples are region (Fig. IE; Labandeira ,1997a). Otherrelevant damage by stylet-bearing paleodictyopteroid structures related to the acquisition of food in some 234 LABANDEIRA-PALEOBIOLOGY OF POLUNATION s«r^"45!&3y6áaay»^fe^ FIGURE 1.•Evidence from dispersed coprolites, plant damage, insect gut contents, and mouthpart structure for palynivory in Evolutionary Assemblage 2. These examples are from the Late Pennsylvanian Calhoun Coal of the Illinois Basin (A-C) and the late Early Permian Koshelevo Formation of the central Urals, Russia (D, E). A, Coprolite containing abundant spores {Convolutispora or Apiculatosporis) of the marattlalean tree fern Psaronius; from NMNH peel BV9-Dtop, slide 499151. B, Coprolite containing abundant cordaite prepollen, Florenites; from NMNH peel BV18-ltop, slide 483986. C, Stylet track of a piercing-and-sucking paleodictyopteroid insect (arrow) on the bell- shaped prepollen organ {Bernaultia) of the medullosan seed fern Medullosa. Approximately transverse section perpendicular to median axis; redrawn from Schopf (1948) plate 104, fig. 3, coal ball 129A. D, Gut contents of the insect Idelopsocus diradiatus (Hypoperlidae) containing pollen of Lunatisporites (Coniferales) and Protohaploxypinus (Glossopteridales); redrawn from SEM photograph
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