Some aspects of the pollination biology of middle eocene angiosperms

Review of Palaeobotany and Palynology, 27 (1979): 213--238

213

© Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands

SOME ASPECTS O F T H E P O L L I N A T I O N B I O L O G Y O F M I D D L E EOCENE ANGIOSPERMS

WILLIAM L. CREPET

Biological Sciences Group U-42, University of Connecticut, Storrs, Conn. 06268 (U.S.A.) (Received August 28, 1978)

ABSTRACT Crepet, W.L., 1979. Some aspects of the pollination biology of Middle Eocene angiosperms. Rev. Palaeobot. Palynol., 27 : 213--238. Angiosperms are characterized by their sophisticated adaptations for wind and insect pollination. Modern relations between the angiosperms and anthophilous insects and the fossil records of both groups suggest that co-evolution was important in the radiation and perhaps even the origin of the angiosperms. An integral part of understanding the evolution of the angiosperms is understanding the evolution of their pollination mechanisms. Enough well-preserved flowers and inflorescences have now been assembled from the Claiborne Formation to allow a consideration of the types of floral morphology and of probable pollination systems that had evolved by the Middle Eocene. Flowers and inflorescences with floral and pollen morphology well adapted for wind pollination are common in the Claiborne Formation. Among these are representatives of two important extant families of the "Amentiferae". These had diversified by the Middle Eocene and were as well adapted for wind dispersal of pollen as modern representatives of the families. Furthermore, it appears that significant evolution has taken place within the two families since the Middle Eocene. Flowers and inflorescences with morphology suggestive of pollination by all four orders of anthophilous insects are present in sediments of the Claiborne Formation. Several of the trends commonly postulated to have taken place with increasing specialization for insect pollination have progressed to a significant degree by the Middle Eocene, but evidence for certain features thought to be characteristic of more sophisticated insect pollination mechanisms is missing from the fossil flower record of that time. In addition, the fossil flower record of the Middle Eocene suggests that there has been significant evolution within certain extant families since the Middle Eocene and that certain families of angiosperms have originated since the Middle Eocene. INTRODUCTION O n e o f t h e d i s t i n g u i s h i n g f e a t u r e s o f t h e a n g i o s p e r m s is t h e d i v e r s i t y o f p o l l i n a t i o n m e c h a n i s m s w i t h i n t h e g r o u p . While g y m n o s p e r m s are e x clusively w i n d - p o l l i n a t e d [with rare e x c e p t i o n s a m o n g e x t i n c t and e x t a n t g y m n o s p e r m s (Crepet, 1974; R a t t r a y , 1 9 1 3 ) ] , included a m o n g the angiosperms are those a d a p t e d to p o l l i n a t i o n by four orders of a n t h o p h i l o u s i n s e c t s , b i r d s , a n d b a t s ( F a e g r i a n d van d e r Pijl, 1 9 7 1 ; P r o c t o r a n d Y e o , 1 9 7 2 ) . A d a p t a t i o n s t o w i n d p o l l i n a t i o n in t h e a n g i o s p e r m s are m o r e

214 efficient than those of the gymnosperms (e.g., the Gramineae and the "Amentiferae" have smaller more easily dispersed pollen grains than gymnosperms and often have better means of trapping wind borne grains). Abiotic pollination mechanisms in the angiosperms also include hydrophily. Wind and insect pollination are by far the most important mechanisms in the angiosperms. Co-evolution with insects is often considered particularly important in angiosperm history since insects act as prime selective agents in the diversification of floral structure (Baker and Hurd, 1968 ; Regal, 1977). Also suggestive of co-evolution is the dependence of insects on angiosperm blossoms. The four orders of anthophilous insects (the Coleoptera, Diptera, Hymenoptera, and Lepidoptera) include approximately 90% of the known species of insects ; the geographical and ecological distribution of the Hymenoptera is similar to that of the angiosperms, and over 25,000 species of Hymenoptera depend exclusively on angiosperm pollen as a food source (Baker and Hurd, 1968). The fossil record is consistent with and suggests the possibility of coevolution between the angiosperms and the insects. All of the orders to which anthophilous insects belong originated well in advance of the appearance of the angiosperms in the fossil record. The Coleoptera first appear in the Permian (Riek, 1970) and many dominant modern families appeared in the Early Mesozoic (Britton, 1970). The Diptera are known from the Permian and seem m o d e m by the Eocene (Riek, 1970). The most important contemporary pollinators, the hymenopterans, radiated during the Cretaceous along with the angiosperms, although they are known from the Triassic (Riek, 1970). The first undisputed remains of the Lepidoptera are from the Cretaceous of Canada (MacKay, 1970). It is considered likely that a simple proboscis had already evolved by the time the angiosperms appeared and that the major radiation of the ditrysian forms (the suborder Ditrysia contains the most important of the lepidopteran pollinators today) paralleled that of the angiosperms (Common, 1975). M o d e m observations of complex interrelationships between insects and flowers and morphological modifications of both in addition to the fossil record suggest that co-evolution with insects was important during the radiation of the angiosperms. The fossil record also suggests that co-evolution with insects may have been important to the origin of the angiosperms. Interactions between insects, probably coleopterans, and the Mesozoic genus Cycadeoidea suggest that insect pollination was one aspect of cycadeoidean reproduction (Crepet, 1972, 1974). Evolutionary trends in the bisporangiate strobilus of the cycadeoids during the Mesozoic suggest that similar interactions existed between cycadeoids and insects throughout the Mesozoic (Crepet, 1974). Further evidence that insect pollination evolved before the angiosperms is the existence of bisporangiate cones in the Cycadeoidales as early as the Jurassic (Williamsoniella, Thomas, 1915). The evolution of the bisporangiate cone must have been an extremely complicated process (Delevoryas, 1968) that presumably came about as a result of intensive selective pressure, and offers no advantage to a wind-pollinated

215 species. The bisporangiate condition is most advantageous where there is biotic pollination (Baker and Hurd, 1968). The existence of as complex a structure as the strobilus of Williamsoniella by the Jurassic suggests selection for the bisporangiate condition (and presumably for insect pollination) before the Jurassic. The ability of the angiosperms to develop a diversity of pollination mechanisms, particularly insect, may have given them an evolutionary advantage over other groups of plants. Reliable insect pollination permits energy conservation that is not possible with random wind pollination by allowing fewer ovules and less pollen to be produced. Insect pollination may also promote speciation, since insect foraging behavior, characterized by varying degrees of flower constancy and specificity, is a potential isolating mechanism {Grant, 1949; Levin, 1971). There is no doubt that understanding the evolution of pollination mechanisms in the angiosperms and insect--angiosperm co-evolution will improve our knowledge of angiosperm evolution. Understanding of certain aspects of insect--angiosperm co-evolution may even provide insights into the origin of the angiosperms. In order to elucidate these processes it is necessary to know how angiosperm flowers have changed through time. This would require a usable fossil record of angiosperm flowers. Until recently, it was generally considered that there was little hope of obtaining useful information about the history of the angiosperm flower from the fossil record (e.g., Cronquist, 1968). However, recent studies of flowers and inflorescences from the Middle Eocene Claiborne Formation indicate that detailed morphological information can be derived from fossil angiosperm flowers and that the number of fossil angiosperm flowers available for analysis is relatively high (Crepet et al., 1974, 1975; Crepet and Dilcher, 1977; Crepet, 1978). Furthermore, there has been increasing interest in morphological and anatomical studies of fossil angiosperm flowers (Basinger, 1976; Tiffney, 1977). Investigations of the Middle Eocene Claiborne Formation have now progressed to the point where there are several hundred examples of fossil flowers and inflorescences in the University of Connecticut Palleobotanical Collection and a consideration of the types of floral morphology and pollination mechanisms that had evolved by that time is possible. Before discussing the range in floral morphology that is known to have existed during the Middle Eocene, it is appropriate to consider floral morphology as it is related to pollination mechanisms. Although color, chemical attractants, and nutritional rewards are important components in exploiting pollinators, floral morphology determines the pollination mechanism. Regardless of color and odor, a flower must be structurally suited to a particular pollinator in order for effective pollination to take place. Morphology of the flower or inflorescence is even more important in wind-pollinated genera where adaptation is primarily to physical factors. The morphology and the size of the pollen grains must also be generally suited to the particular means of pollination. Wind-dispersed grains fall within a certain size range (typically

216 less than 30 ~m in diameter) and are often morphologically suited for sustained suspension in air (Whitehead, 1969). Biotically dispersed grains must be adapted in some way to adhere to the pollinator to maximize effective dispersal. The correspondence between pollen type and pollinator, however, appears to be much less striking than that between floral morphology and pollinator (Taylor and Levin, 1977). It is important to be conservative in suggesting a particular mechanism of pollination for a particular fossil flower or inflorescence type, because only floral and pollen morphology are available for consideration. Only flowers or inflorescences with features that are clearly typical of a certain pollination mechanism are used to suggest that that type of pollination was occurring during the Middle Eocene. As a prelude to the various fossil forms, the syndromes of pollination of anemophily and of the four orders of anthophilous insects are outlined (Table I). The syndromes, as presented here, are taken from Faegri and Van der Pijl (1 e '1) and are modified in stressing primarily the structural features that characterize a syndrome. The various fossil flowers and inflorescences can be considered in the broad context of the table with specific cases and details discussed separately. While the table emphasizes the particular syndrome that is most characteristic of pollination by a specific order of anthophilous insects, it also includes blossom classes that are frequently, but not necessarily exclusively, pollinated by the order in question. RESULTS

Anemophily (wind-pollinated blossoms) There are catkins, heads, and individual flowers that conform to the structural syndrome of anemophily. The rr , s t c o m m o n of these are catkins. Many catkins have been the objects of separate morphological studies or are in the process of being investigated. As a result, the affinities of several types of fossil catkins are known or suspected. At least two families of the " A m e n t i f e r a e " were diversified during the Middle Eocene and these had inflorescences well adapted for wind pollination. One family, the Juglandaceae, has an extensive microfossil and megafossil record. One complex of genera in the Juglandaceae is particularly well TABLE I Syndromes of wind and insect pollination I WIND POLLINATION SYNDROME 1. Perianth reduced or absent, anthers and stigmas exposed, attractants absent. 2. Stamen filaments frequently elongated, stigmas frequently enlarged. 3. Pollen buoyant, usually 20--30 pm in diameter, with smooth exine. 4. Pollen produced in great quantities and pollen-arresting mechanisms frequent.

217 TABLE I (continued) COLEOPTERAN POLLINATION SYNDROME (BEETLE SYNDROME) 1. Pollination units with few visual attractants, no special or definite shape, no depth effect, generally large, fiat, shallow bowl~shaped, closed. 2. Sexual organs exposed, attractants (pollen, food bodies, or nectar) easily accessible. DIPTERAN POLLINATION SYNDROME ( F L Y SYNDROME)

Small fly blossoms 1. Regular, simple, no depth effect. 2. Sexual organs well exposed. 3. Generally small size.

Sapromy ophily 1. Pollination units generally radial, but frequently with great depth effect. 2. Often developed as traps ; frequently lantern types with the presence of filiform appendages. 3. Sexual organs usually hidden in the interior o f the blossoms. HYMENOPTERAN POLLINATION SYNDROME (specifically, bumble bee and hive bee blossoms) 1. Bilaterally symmetrical with great depth effect, mechanically strong with adequate facilities for landing and a surface that gives a good foothold. 2. Frequently intricate - - partially closed. Nectar hidden, but not deeply. 3. Stamens few, many ovules/ovary, and sex organs often concealed.

Other blossom classes frequently pollinated by hymenopterans 1. Brush. 2. Blossoms with bell/funnel-shaped corollas. LEPIDOPTERAN POLLINATION SYNDROME

Psycophily (BUTTERFLY SYNDROME) 1. 2. 3. 4.

Corolla trumpet-shaped or a narrow tube with a fiat rim. Blossom radially symmetrical, erect. Anthers fixed. Nectar well hidden in tubes or spurs.

Phalaenophily (MOTH SYNDROME) 1. 2. 3. 4.

Tubular corolla with deeply dissected lobes or fringed petals. Blossoms horizontal or pendant. Zygomorphy, if present, caused by the bending back of the lower rim o f the corolla. Nectar well hidden in tubes.

Other blossom types frequently lepidopteran pollinated 1. Brush. 1Adapted from Faegri and Van der Pijl (1971) in stressing primarily structural floral and pollen features.

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PLATE I

219

represented in the Claiborne Formation; the Alfaroa--Oreomunnea--Engelhardia complex. In addition to a variety of winged fruits and leaves (Dilcher et al., 1976), two types of staminate catkins of this complex are now known from this formation [Eokachyra (Crepet et al., 1975) and another type that has not yet been described separately]. Both are similar in morphology to the staminate catkins of extant genera of the complex. Specimens of Eokachyra are well preserved (Plate I, 1) and the morphology of these catkins is well understood. Florets consist of three small obovate floral envelope parts with fifteen almost sessile anthers that are subtended by three-lobed bracts (Crepet et al., 1975). The pollen is triporate with finely scabrate exine and the average diameter is 19.6 pm (Plate I, 3). The pollen is morphologically similar to the pollen of extant Engelhardia sect. Psilocarpeae, but is larger (Crepet et al., 1975; Whitehead, 1965). A second type of staminate catkin has smaller florets (average length of 2.5 mm vs. average length of 3.3 mm) with four rounded floral envelope parts subtended by more acutely lobed three-lobed bracts (Plate I, 2, 5). Pollen of these inflorescences is substantially smaller than the pollen of Eokachyra (av. diam. 14.8 pm) and is even more triangular (Plate I, 4). Pollen is an important diagnostic feature in the Juglandaceae and the magnitude of the average size difference between the pollen of these two types of catkins and the differences in floral size and structure suggest that they represent different genera (Whitehead, 1965). Both types of fossil staminate inflorescence are well suited for wind dispersal of pollen. Floral envelopes are small, allowing unimpeded exposure of the anthers to potentially dispersing air currents, and the abundant pollen is well adapted for sustained suspension in air currents (Whitehead, 1969). The differences between the fossil staminate inflorescences and those of the modern genera of the complex are small and probably have little functional significance. The Middle Eocene representatives of the Alfaroa-Oreomunnea--Engelhardia complex appear to have been just as well adapted for wind dispersal of pollen as the modern genera. The level of adaptation attained by the staminate inflorescences of the Alfaroa---Oreomunnea-Engelhardia complex during the Middle Eocene considered with the fruit and pollen record of the Juglandaceae suggests that the entire family was at least as diverse and as well adapted to wind pollination as it is today (e.g., Scott, 1954; Nichols, 1973; Wolfe, 1973). There is also evidence indicating that the Fagaceae were diversified during the Middle Eocene. There are three types of inflorescences having fioret PLATE I

1. Eokachyra, showing anthers and floral envelope parts. × 1.6. IUPC NW2204. 2. Another type o f juglandaceous catkin allied with the Alfaroa---Oreomunnea--Engelhardia complex. × 1.6. UCPC P1. 3. Pollen grain o f Eokachyra. × 1020. Slide C I A 7 . 4. Pollen grain from an anther of catkin P1. × 1020. Slide 110. 5. Higher magnification view o f several florets of catkin P1. × 4.5.

220

PLATE II

221

morphology and pollen suggestive of the Fagaceae; two types of catkins and a Fagus.like staminate head (Plate II, 1, 2; III, 1). One type of staminate catkin has florets that are nearly sessile (Plate II, 1). Florets tend to be poorly preserved, but a small, highly carbonized floral envelope can be noted in certain specimens (Plate II, 1). The stamens must be sessile or have extremely short filaments because the bases of the anthers do not extend beyond the floral envelope. The anthers are well preserved and are broad rounded with a cordate base (Plate II, 1). Pollen is preserved within the anthers and is tricolpate, tectate, and prolate--spheroidal (Plate II, 3, 4). The colpi do n o t extend into the polar region which is often flattened (Plate II, 3, 4). The average size of the pollen is 21.6 × 16.8 ~m. The simple florets and pollen morphology suggest the Fagaceae (Hjelmqvist, 1948; Erdtman, 1966; Abbe, 1974). It has been suggested that anther morphology is a good diagnostic character in the Fagaceae (Hjelmqvist, 1948) and the morphology of the anthers of this type of catkin is suggestive of Quercus (Hjelmqvist, 1948). The pollen morphology is consistent with the possibility that these catkins are related to the extant genus Quercus, but more structural information is necessary in order to evaluate this possibility ~. A second type of catkin that appears to be allied with the Fagaceae has much larger floral envelope parts than the first and anthers that extend slightly beyond the floral envelope (Plate II, 2). The florets appear crowded as though they might have been borne in dichasia (Plate II, 2); investigation of this possibility is presently in progress. Pollen is tricolporate, prolatesomewhat spindle-shaped, with lalongulate pores and colpi that extend into the polar region (Plate II, 5). The grains are tectate with a thicker sexine than nexine (Plate II, 5) and average 25.4 × 16.6 ~m. The simple staminate florets and pollen morphology of these catkins are suggestive of the Fagaceae, but further studies are necessary to elucidate possible relationships with extant genera of the family. 1 Since this manuscript has been submitted, an extensive survey of the pollen of the extant Fagaceae and studies of new fossil inflorescences have contributed more to understanding the possibility that these catkins might be allied with the Fagaceae and have further elucidated the status of the Fagaceae during the Middle Eocene. The results will soon be published.

PLATE II 1. Catkin with one detached floret showing a small carbonized floral envelope (f) and anthers (a). x 4.75. IUPC P2232. 2. Portion of a catkin with conspicuous floral envelopes (f) and anthers protruding beyond the floral envelopes (a). × 8.5. UCPC W14a. 3. Scanning electron micrograph of the tricolpate pollen from the anthers of catkin P2232. Note the reticulate exine. × 2000. 4. Nomarski-phase micrograph of the pollen of catkin P2232 showing the colpi and tectate exine. × 850. Slide 101. 5. Nomarski-phase micrograph of pollen of catkin W14a showing colpi and lalongulate pores. × 850. Slide 102.

222 PLATE

III

1. Fagus-like staminate inflorescence, x 5. IUPC P2256. 2. Catkin with simple florets and Betula--Myrica-type pollen, x 3.3. UCPC P27a.

223

A third type of inflorescence is a head of florets with exserted stamens (Plate III, 1). Florets are staminate, appear to have diminutive floral envelopes, and anther morphology similar to Fagus (Plate III, 1; Hjelmqvist, 1948). The pollen, however, is different from that of Fagus in being tricolpate instead of tricolporate (Plate III, 4; IV, 4). The pollen is similar to that of Fagus in being subprolate--suboblate with a tectate reticulate exine and in having a sexine thicker than the nexine (Plate III, 4 ; IV, 4). Average size of pollen grains is 20 X 20 pm. All three types of inflorescences have general morphological features and palynological features suggestive of the Fagaceae. While the structure and possible taxonomic affinities of these inflorescences will receive further investigation, it is clear that at least one of them (the Fagus-like head) is in some ways distinctly different from the modern genus it appears to be most closely related to. These inflorescences support the leaf record of the Fagaceae in illustrating that the family was diversified during the Middle Eocene and has apparently undergone a significant degree of evolution since that time. At least two genera of Middle Eocene fagaceous leaves appear to represent extinct genera (Anderson and Dilcher, 1967; Dilcher and Mehrotra, 1969). Further investigations of fagaceous inflorescences from the Middle Eocene will improve the understanding of the evolutionary position of the family at that time. It is already apparent that certain members of the family were well adapted to wind pollination by the Middle Eocene. All of these inflorescences have small floral envelopes, pollen produced in copious quantities well exposed to potentially dispersing air currents, and pollen grains that are within the optimal size range for wind pollination (Whitehead, 1969). Some genera of the extant Fagaceae include certain tropical species that are insect-pollinated (e.g., Castanea, Quercus; Faegri and Van der Pijl, 1971). These insect-pollinated species are characterized by having upright catkins with robust axes (Faegri and Van der Pijl, 1971). There is no indication that any of the fossil catkins had axes robust enough to suggest the upright habit. Another type of catkin from the Claiborne Formation has florets that are extremely simple in structure (Plate III, 2;IV, 1, 2). The florets appear to consist only of short pedicels bearing clusters of anthers. There is no evidence of any floral envelope parts or of any subtending bracts and several well-preserved specimens have been available for study (Plate III, 2; IV, 1, 2). Pollen is preserved within the anthers and is triporate and aspidote with rounded, slightly lalongulate pores (Plate III, 3; IV, 3). The exine is finely scabrate and the average diameter of the grains is 23.4/~m. The general morphological features of the pollen and the exine stratification at the 3. Scanning electron micrograph of Betula--Myrica-type pollen from catkin P2231. Note the scabrate exine and slightly lalongulate, aspidote pores, x 1400. 4. Scanning electron micrograph of pollen from P2256 showing the tectate reticulate exine. X 2600.

224 PLATE IV

225 pores are characteristic of pollen of the Betula--Myrica type (Erdtman, 1966). Both the Betulaceae and the Myricaceae have staminate catkins with florets subtended by relatively robust bracts (Hjelmqvist, 1948; Abbe, 1974), and it seems unlikely that evidence of these bracts would be lacking if they were once part of these inflorescences. It seems most likely that if these fossils correctly represent the actual catkins, then the catkins must be those of an extinct genus. As the structure of these catkins is presently understood, their level of adaptation to wind dispersal of pollen is very high. The florets offer no impediment to wind and the pollen is optimal in size, exine ornamentation, and morphology for wind dispersal (Whitehead, 1969). In addition to the various inflorescences, there are two types of individual flowers with morphological features conforming to the syndrome of wind pollination. One of these was described by Berry (Combretanthites eocenica, 1916). This flower has a small floral envelope and at least twelve exserted stamens that extend 5 mm beyond the floral envelope (Plate V, 2). A second type of flower that has not been previously described also has a small floral envelope and has at least eight exserted stamens (Plate V, 1). Pollen is preserved within the anthers of this flower and is tricolpate and tectate with an average diameter of 24 ~m (Plate IV, 5). Both of these flowers are structurally suited for wind pollination. The floral envelopes are small and the anthers are exposed to air currents. It is clear that wind pollination was very well developed by the Middle Eocene. Floral and inflorescence morphology as well as pollen morphology have reached a level of adaptation to wind dispersal of pollen that is comparable with well,adapted extant anemophilous genera.

Entomophily Cantharophily (beetle-pollinated blossoms) There are several types of flowers from the Claiborne Formation that have structures suggestive of coleopteran pollination. One type, in particular, epitomizes the syndrome. These flowers are relatively large (average diameter 6 cm), and have five sepals that are connate at the base and five petals (Plates V, 3; VI, 1, 2, 3). The petals are narrowest at the base and flare to a broadly rounded apex (Plate VI, 1, 2). The margins of the petals are often preserved as if they were crumpled in life (Plate VI, 2). This does not appear PLATE IV 1. Catkin IUPC P2231a. Another example of the type o f catkin illustrated in Plate HI (2).

× 1.5. 2. Higher magnification view o f P2231b illustrating the lack of bracts and floral envelope parts. The florets (fl) appear to be composed only of short stalks bearing anthers. × 7. 3. Light micrograph o f pollen in situ in a transfer preparation of an anther from P2231. Note the exine stratification in the pore area. x 1400. 4. Nomarski-phase micrograph of a pollen grain from P2256 (Plate HI, 1) showing a colpus and a tectate exine with sexine thicker than nexine, x 850. Slide 106. 5. Nomarski-phase micrograph o f a pollen grain and some anther cuticle fragments from P2202 (Plate V, 1) showing colpi and tectate reticulate exine. × 1000. Slide F2NS6.

226 PLATE V

227

to be an accident of preservation because the matrix around the crumpled part of the petals is smooth (Plate VI, 2). Petal venation is distinctive. There are several more or less parallel veins in the base of the petals (Plate VI, 1, 2). These veins diverge and dichotomize as they enter the expanded distal portion of the petals (Plate VI, 2). Petals are often found dispersed in the matrix (Plate VI, 2), or separated slightly from the receptacles of compressed flowers, indicating that they may have been caducous (Plate VI, 1). Cuticle of the pedicels, sepals, and petals is preserved. Stomata are found only on the cuticle of the petals and are paracytic (Plate VI, 5). There are numerous elongate anthers and in one instance, what appears to be the impression of a small superior ovary (Plate V, 3). Although the anthers are not unusually well preserved, they contain pollen. Pollen grains are tricolpate, tectate with a reticulate exine, granular colpus membranes, and a nexine the same thickness as the sexine (Plate VI, 4). Average pollen diameter is 29 ~m. These flowers conform in morphology, number and size of floral parts, pollen morphology, and stomatal subsidiary cell pattern to the flowers of several genera of the Parietales (Lawrence, 1951). The petals of the fossil flowers are strikingly similar to those found in certain families of the Parietales (e.g., DiUeniaceae), in venation, in being crumpled at the margins, and in apparently being caducous. Further details of the structure and the possible affinities of these flowers will be considered elsewhere, but their morphology is archetypal of the coleopteran pollination syndrome. Flowers are large, shallow bowl-shaped, radially symmetrical, and have easily accessible reproductive structures and numerous stamens. A second type of flower with morphology suggestive of coleopteran pollination is radially symmetrical with five petals that are connate at the base (Plate VII, 1). The corolla is moderate in size (average diameter 2.8 cm) and dish-bowl shaped. The petals expand slightly toward their rounded apices (Plate VII, 1). Little is known at present about the other features of these flowers, but the corolla is typical of those that are coleopteranpollinated (Faegri and Van der Pijl, 1971 ; Table I). There are several other types of radially symmetrical flowers that could also be pollinated by coleopterans (some of these are considered under the "small fly syndrome" of myophily), but none are as typical of the syndrome as these two examples.

Myophily (fly-pollinated blossoms) Although the Diptera exhibit more variation in methods and in habits of pollination than any other group of anthophilous insects (Faegri and Van der PLATE V 1. A flower with a small floral envelope and exserted stamens. × 9. IUPC P2202. 2. C o m b r e t a n t h i t e s e o c e n i c a (Berry, 1916). × 5.3. U.S.N.M. 3455. 3. Large laterally compressed flower showing sepals (s), petals (p), pedicel (pd), and ovary (o). × 2.6. UCPC P8a.

228

PLATE VI

229

Pijl, 1971), there are two blossom classes that are probably the most characteristic of myophily: those demonstrating the syndrome of sapromyophily and the syndrome of "small fly blossoms" (Table I). Myophily, especially sapromyophily, is common in the Araceae (Faegri and Van der Pijl, 1971). Aroid spadices have frequently been reported from the Tertiary (e.g., Berry, 1930; R~sky, 1964), but until recently none of the cuticular or morphological details necessary to confirm the existence of fossil aroid spadices have been provided. Studies of spadix-like fossils from the Claiborne Formation have now shown that they have the cuticular features, type of ovary, and other morphological details characteristic of the Acoreae (Crepet, 1978) (Plate VII, 2). Aroid leaves of the modern genus Philodendron are also known from the Claiborne Formation (Dilcher and Daghlian, 1977). The facts that the aroid spadix was well developed by the Middle Eocene and that leaves representing an advanced (Hutchinson, 1973), modern genus have been found in strata of the same age suggest that the Araceae were rather modern at the time. There is no reason why dipteran pollination should not have been as important in the group then as it is now. The pollinators were available (Riek, 1970), and the reproductive structures were similar or in some cases probably identical with those of extant aroid genera. The group of fossil flowers demonstrating the syndrome of "small fly blossoms" is diverse and evidently represents a variety of families or genera. These flowers have small size and regular shape in common and lack notable specializations aside from a small number of perianth parts (Plate VII, 3, 4, 5; VIII, 1). The flowers are open and the sexual organs are exposed with presumably easily accessible nectar and/or pollen. Although these blossoms conform to the syndrome of small fly blossoms, their open and relatively unspecialized nature presumably allowed them to be pollinated by a variety of anthophilous insects. Coleopterans as well as hymenopterans may pollinate extant "small fly blossoms" (Faegri and Van der Pijl, 1971). So while these are typical of the small fly blossom and lend support to the possibility of myophily during the Middle Eocene, they were probably not exclusively pollinated by dipterans.

PLATE VI 1. Large radially symmetrical flower similar to P8 (Plate V, 3; Plate VI, 3) showing the sepals (s) and petals. Note the slightly detached petal (p). x 1.7. UCPC 12a. 2. Dispersed petal similar to those of P8 and P12. Note the venation, point of abscission (ab), and crumpled margin (m). x 2.9. UCPC P26. 3. Counterpart of P8a (Plate V, 3) showing anthers (a), sepals (s), and petals (p). x 3.5. 4. Nomarski-phase micrograph of tricolpate pollen found in the anthers of P8 and P12 type flowers. Note the granular colpus membrane and the tectate exine with sexine and nexine of equal thickness. X 950. Slide 111. 5. Cuticle of the petals of P8 showing the epidermal cells and stomata with paracytic subsidiary cells, x 950.

230

PLATE VII

231

Melittophily (bee-pollinated blossoms) Several fossil flowers and a type of fossil inflorescence from the Claiborne Formation suggest that hymenopteran pollination was well developed during the Middle Eocene. One type of flower is small and the corolla has five perianth parts (Plate VIII, 2). These flowers are bilaterally symmetrical with two types of corolla parts inserted at the same level (Plate VIII, 2). Three of the corolla parts are the same size and the same shape (Plate VIII, 2). The other two perianth parts are lateral and are narrow proximally, but expand into a rounded, concave, distal portion (Plate VIII, 2). A single bilocular anther is compressed on the rounded concave portion of each of these petals and there is no evidence that these flowers had more than two stamens (Plate VIII, 2). Pollen is sparsely preserved within the anthers, and has been studied by making collodion peels of the entire anthers (as in Crepet and Dilcher, 1977). Pollen grains are tectate, triporate, and 26.4 pm in diameter. The pores are markedly lalongulate (Plate VIII, 4). Bilateral symmetry is most characteristic of hymenopteran pollinated flowers (Proctor and Yeo, 1972). Bilateral symmetry serves to orient the hymenopteran as it approaches the flower. This enables the insect to operate the pollination mechanism properly and also may function as a nectar guide (Faegri and Van der Pijl, 1971). This is the earliest example of a bilaterally symmetrical flower now known from the fossil record. Another type of flower that has structure suggestive of hymenopteran pollination has a bell-shaped sympetalous corolla (Plate VIII, 5). The corolla has shallow rounded lobes and the calyx is small and connate (Plate VIII, 5). This type of corolla is typical of flowers that are hymenopteran pollinated today (Faegri and Van der Pijl, 1971; Table I). An inflorescence type that suggests hymenopteran pollination is a spike of sessile, perfect florets with small perianths and exserted stamens (Plate VIII, 6). These inflorescences have been studied separately and are allied with the Mimosoideae (Crepet and Dilcher, 1977). Hymenopterans do pollinate "brush" flowers such as these mimosoid spikes and are among the important pollinators of contemporary mimosoids with similar inflorescences (Elias, 1974). The pollen configuration of these flowers is also indicative of pollination by sophisticated anthophilous insects. Pollen grains are in permanent tetrahedral tetrads (Plate VIII, 7) (Crepet and Dilcher, 1977). It should be noted that lepidopterans and birds may also pollinate such inflorescences (Elias, 1974). There is strong evidence that hymenopteran pollination was important PLATE VII 1. Large radially symmetrical flower, x 2.3. IUPC W2233. 2. Aroid spadix, x 5. IUPC NL2238. 3--5. Small regular flowers with no notable specializations other than low numbers of parts. 3. X 5. IUPC W2237.4. x 6.9. IUPC M2203. 5. X 5. UCPC P17.

232

PLATE VIII

233

and diversified during the Middle Eocene. Bilateral symmetry, brush flowers and blossoms with bell-shaped corollas are all characteristic of hymenopteran pollination today.

Psycophily (butterfly-pollinated blossoms) Those flowers typically pollinated by butterflies have a narrow elongate corolla tube which prevents other insects from gaining access to the nectar and a rim of some type that serves as a landing platform (Faegri and Van der Pijl, 1971). One type of flower from the Claiborne Formation shares these features. The corolla of this flower is fused into a tube that is narrowest near the ovary (0.5 mm diam.) and flares distally to its widest point (2 mm diam.) before the corolla becomes acutely lobed (Plate VIII, 3). The calyx is connate and does not appear to be deeply lobed (Plate VIII, 3). This trumpetshaped type of blossom is most typical of butterfly pollination (Faegri and Van der Pijl, 1971; Table I). It has been noted that lepidopterans are also important pollinators of brush-type blossoms and the mimosoid inflorescence supports the trumpet blossom in suggesting Middle Eocene lepidopteran pollination. No flowers are known from the Claiborne Formation, however, that demonstrate the specific syndrome of phalaenophily (moth-pollinated blossoms). F U R T H E R CONCLUSIONS AND DISCUSSION

Entomophily is diverse by the Middle Eocene. Flowers or inflorescences with outstanding features typical of those pollinated by each of the four orders of anthophilous insects today are found in the Claiborne Formation. Many of the trends frequently postulated to have taken place in floral evolution with increasing specialization in response to more sophisticated insect pollinators are far along by this time (e.g., Sporne, 1948; Leppik, 1957; Eames, 1961; Davis and Heywood, 1963). It is evident from the fossil record of the Middle Eocene that: (1) Nectar production is already important and the reduction of stamen

PLATE VIII 1. Small, regular, laterally compressed flower. × 4. IUPC P1949a. 2. Bilaterally symmetrical flower with one anther compressed on each o f the larger lateral floral envelope parts (a). × 7.5. IUPC LK2246. 3. Flower with trumpet-shaped corolla and connate calyx (c). Note the ovary (o). × 5.4. IUPC P2226. 4. Nomarski-phase micrograph of a pollen grain suspended in a collodion peel of an anther from LK2246 s h o w i n g one lalongulate pore. × 650. 5. Flower with a bell~haped sympetalous corolla (co) and a connate calyx (c). × 2.9. UCPC W16b. 6. Eomimosoidea. × 1.5. IUPC W2316. 7. Scanning electron micrograph o f a tetrad o f pollen grains in situ in an anther from W2316. × 1875.

234 n u m b e r with the c o n c o m i t a n t s u b s t i t u t i o n o f n e c t a r as an a t t r a c t a n t has already t a k e n place in several taxa. This is indicated b y the existence o f t r u m p e t - and bell-shaped blossoms w h i c h p r o b a b l y had n e c t a r as the p r i m a r y a t t r a c t a n t ; small flowers with few anthers, again suggesting n e c t a r as t h e p r i m a r y a t t r a c t a n t ; and by m i m o s o i d inflorescences with m o r p h o l o g y similar to m i m o s o i d s t h a t are nectar producers today. (2) R e d u c t i o n o f p e r i a n t h parts with i m p r o v e d recognizability and d e v e l o p m e n t o f the restrictive corolla (i.e., o n e excluding certain a n t h o philous insects) has already t a k e n place. The existence o f m a n y flowers with few p e r i a n t h parts illustrates t h a t e v o l u t i o n for r e c o g n i z a b i l i t y (sensu Faegri and Van der Pijl, 1 9 7 1 ) has already t a k e n place b y t h e Middle Eocene. Flowers with bilateral s y m m e t r y are readily r e c o g n i z e d and are restrictive in the sense t h a t o n l y certain a n t h o p h i l o u s insects are capable o f orienting themselves to bilateral symm e t r y . T r u m p e t flowers are also restrictive and prevent insects t h a t lack an elongate stylet f r o m having access t o the nectar. (3) Perianth parts are already w h o r l e d and fused in certain taxa. There are flowers in the Middle E o c e n e s h o w i n g a range in degree o f fusion o f corolla parts f r o m entirely free (Plate VI, 1) to w h o r l e d and fused into bell-shaped and t r u m p e t - s h a p e d corollas (Plate VIII, 5; Plate VIII, 3). Insect pollination is well d e v e l o p e d by the Middle E o c e n e y e t the fossil flower record, as it is p r e s e n t l y u n d e r s t o o d , suggests t h a t m o d i f i c a t i o n for insect p o l l i n a t i o n had n o t r e a c h e d m o d e r n levels. Evidence t h a t certain features characteristic o f sophisticated m o d e r n pollination m e c h a n i s m s had evolved b y the Middle E o c e n e is lacking in the Middle E o c e n e flower record. These features are: (1) Radically z y g o m o r p h i c flowers. 1 ~The possible existence of radically zygomorphic flowers by Middle Eocene times is suggested by leaflets and fruits considered to represent the subfamily Faboideae ef the Leguminosae (e.g., Berry, 1930). These identifications are not based on details of morphology or fine venation and must be considered inconclusive (Dilcher, 1974). Furthermore, inferring the existence of certain floral features from the leaf record is indirect and weakened by the lack of knowledge of relative rates of evolution in different plant organs. Also suggestive of the possibility that certain flowers may have been radically zygomorphic by the Middle Eocene are remains from the Green River Formation described by MacGinitie (1969) as fruits of Lomatia. These "fruits" also look superficially like certain zygomorphic caesalpinioid flowers. Similar fruits were illustrated in Audubon magazine attached to leafy twigs (Moore and Ratcliffe, 1971). As a result of this, MacGinitie placed these fruits in incertae sedis with the suggestion that they might represent an extinct genus of the Polygalaceae (MacGinitie, 1974). Since the identity of these fruits remained in question, several examples were obtained for direct examination at the University of Connecticut. At this time, there is no evidence to suggest that these fruits might actually be the remains of caesalpinioid flowers. Until the accuracy of the reports of Middle Eocene remains of the Faboideae and the true nature of the "fruits" of the Polygalaceae are determined, or new fossil material discovered, it must be assumed that there is not yet good evidence for radically zygomorphic flowers during the Middle Eocene.

235

(2) Pollen grains in permanent polyads (see Crepet and Dilcher, 1977). (3) Flowers with very elongate corolla tubes suggestive of phalaenophily or ornithophily. In addition to these features, there are several families characterized by having blossoms or inflorescences with very sophisticated adaptations for insect pollination that are missing from the flower record of the Middle Eocene (e.g., Compositae, Orchidaceae). The fact that features characteristic of advanced insect pollination mechanisms are missing from the spectrum of Middle Eocene floral structure suggests that pollinators have undergone significant structural and/or ethological evolution since the Middle Eocene 1. It is likely that the more advanced adaptations for entomophily and some of the families that demonstrate them today evolved in response to increasingly more sophisticated and reliable pollinators. Presumably these events took place after the Middle Eocene, although they may have been initiated during the Middle Eocene or earlier [as is apparently the case in the evolution of multiple pollen grain configurations in the Mimosoideae (Crepet and Dilcher, 1977)]. The diversity of flowers and of inflorescences conforming to the wind pollination syndrome and the advanced state of adaptation to wind dispersal found in some of these inflorescences and in their pollen suggests the possibility that anemophily had a long evolutionary history previous to the Middle Eocene. This is supported by the record of the dispersed pollen flora. Grains well suited for wind dispersal are not uncommon in the Upper Cretaceous (Nichols, 1973). The fossil record also suggests that there has been significant evolution in certain predominantly anemophilous families since the Middle Eocene. Certain fossils similar to the inflorescences of some modern Amentiferae, e.g., Fagus-like heads; catkins with Myrica-like pollen, have many characteristics in common with extant genera, but have enough significant differences to suggest that they represent extinct genera. In addition, it is known that the Alfaroa----Oreomunnea--Engelhardia complex of the Juglandaceae was more diversified during the Middle Eocene than at present (Dilcher et al., 1976). It is noteworthy that those inflorescences having the most advanced wind pollination mechanisms during the Middle Eocene are comparable in level of adaptation to modern inflorescences with advanced wind pollination mechanisms while modern insect pollination mechanisms are in some cases clearly more advanced than those of the Middle Eocene even though entomophily seems to have preceded anemophily in the history of the angiosperms. This suggests that wind pollination attained advanced levels of adaptation before insect pollination, perhaps because, as a reciprocal process, co-evolution involves certain restraints. It would obviously be impossible for a particular type of floral morphology to evolve before the potential pollinators had acquired the appropriate structural or ethological features. i Recent studies of Tertiary insect faunas from North America b y M.V.H. Wilson (published while this manuscript was in press, 1978) strongly support these possibilities.

236 Diversification of wind pollination mechanisms would involve adaptation to primarily physical factors and would not encounter the restraint of being "tied" to the evolution of pollinators. Even if the rate of evolution of wind-pollinated species was lower than the rate of evolution of insectpollinated species, wind-pollinated species could conceivably achieve a level of adaptation to wind pollination comparable to advanced modern levels at a time when the range of floral morphology of the insect-pollinated species could only reflect adaptation to the available pollinators. This Middle Eocene flora provides the earliest comprehensive information about the level of evolution of the angiosperm flower in the fossil record. It is possible to assess the level of pollination mechanisms in the angiosperms directly without having to rely on inferences from the leaf and pollen fossil records. Uncertainty of relative rates of evolution of different plant parts and the difficulties involved in identifying certain types of pollen and leaves make such an approach equivocal at best. Certainly, studies of flowers and inflorescences supported by what is known from the leaf and pollen fossil records is the best approach to illuminating the pollination spectrum of the Middle Eocene. The study of angiosperm floral remains from the Claiborne Formation suggests that evolution in the angiosperms since the Middle Eocene (the approximate 3/5ths point in angiosperm evolution) has been significant in the following ways: (1) There has clearly been evolution within certain extant families. (2) Certain floral and pollen features characteristic of advanced insect pollination mechanisms appear to have originated since the Middle Eocene. (3) Certain families of angiosperms have originated since the Middle Eocene. Further studies of the Middle Eocene from the Claiborne Formation and the correlation of this information with the flower, leaf, and pollen records of other Middle Eocene localities will determine whether all of these points are valid. Further studies of Middle Eocene flowers and inflorescences will also expand our general understanding of the level of adaptation of pollination mechanisms at that time and provide information about the evolution of specific families. Understanding the level of adaptation of certain pollination mechanisms during the Middle Eocene provides another reference point in addition to the present to use in attempting to understand the evolution of pollination mechanisms in the angiosperms. What will be necessary in the future in order to understand the evolution of pollination mechanisms and even the evolution of the angiosperms is the consolidation of similar information from a variety of points in the past. ACKNOWLEDGEMENTS The author gratefully acknowledges the assistance of the following: Professors T. Delevoryas and Donald A. Levin, Department of Botany,

237 University o f Texas, Austin, a n d Professor J a m e s A. Slater, Biological Sciences G r o u p , T h e University o f C o n n e c t i c u t , Storrs, f o r invaluable suggestions a n d discussion in t h e p r e p a r a t i o n o f the m a n u s c r i p t ; Dr. David L. Dilcher, D e p a r t m e n t o f Biology, I n d i a n a University, B l o o m i n g t o n , for the loan o f specimens f r o m t h e I n d i a n a University P a l e o b o t a n i c a l Collection; Dr. T o d F. Stuessy, D e p a r t m e n t o f B o t a n y , Ohio State University, C o l u m b u s , f o r t h e c o n t r i b u t i o n o f s p e c i m e n L K 2 2 4 6 ; and Dr. Leo J. H i c k e y f o r t h e loan o f t y p e s p e c i m e n s f r o m the U.S. N a t i o n a l Museum. Research was s u p p o r t e d b y N S F G r a n t D E B 7 6 - 0 2 8 8 6 a n d University o f C o n n e c t i c u t R e s e a r c h F o u n d a t i o n G r a n t 3 5 - 8 4 5 t o W.L. Crepet. REFERENCES Abbe, E.C., 1974. Flowers and inflorescences of the "Amentiferae". Bot. Rev., 40: 159--261. Anderson, G.J. and Dilcher, D.L., 1967. Cuticular analysis of the extinct genus Dryophyllum. Proc. Indiana Acad. Sci., 77: 130--131. Baker, H.G. and Hurd, P.D., 1968. Intrafloral ecology. Annu. Rev. Entomol., 13: 385--414. Basinger, J.F., 1976. Paleorosa similkameenensis, gen. et sp. nov., permineralized flowers (Rosaceae) from the Eocene of British Columbia. Can. J. Bot., 54: 2293--2305. Berry, E.W., 1916. The lower Eocene floras of southeastern North America. U.S. Geol. Surv. Prof. Pap., 91: 1--481. Berry, E.W., 1930. Revision of the lower Eocene Wilcox flora of the southeastern states. U.S. Geol. Surv. Prof. Pap., 156: 1--196. Britton, E.B., 1970. Coleoptera. In: The Insects of Australia, Melbourne University Press, Melbourne, Vic., pp.495--621. Common, I.F.B., 1975. Evolution and classification of the Lepidoptera. Annu. Rev. Entomol., 20: 183--203. Crepet, W.L., 1972. Investigations of North American cycadeoids: pollination mechanisms in Cycadeoidea. Am. J. Bot., 59: 1048--1056. Crepet, W.L., 1974. Investigations of North American cycadeoids: the reproductive biology of Cycadeoidea. Palaeontographica, 148B: 144--169. Crepet, W.L., 1978. Investigations of angiosperms from the Eocene of North America: an aroid inflorescence. Rev. Palaeobot. Palynol., 25: 241--252. Crepet, W.L. and Dilcher, D.L., 1977. Investigations of angiosperms from the Eocene of North America: a mimosoid inflorescence. Am. J. Bot., 64: 714--725. Crepet, W.L., Dilcher, D.L. and Potter, F.W., 1974. Eocene angiosperm flowers. Science, 185: 781--782. Crepet, W.L., Dilcher, D.L. and Potter, F.W., 1975. Investigations of angiosperms from the Eocene of North America: a catkin with juglandaceous affinities. Am. J. Bot., 62: 813--823. Cronquist, A., 1968. The Evolution and Classification of Flowering Plants. Houghton Mifflin Company, Boston, Mass. Davis, P.H. and Heywood, V.H., 1963. Principles of Angiosperm Taxonomy. D. van Nostrand Company, Princeton, N.J. Delevoryas, T., 1968. Some aspects of cycadeoid evolution. J. Linn. Soc. (Bot.)., 61: 137--146. Dilcher, D.L., 1974. Approaches to the identification of qangiosperm leaf remains. Bot. Rev., 40: 1--157. Dilcher, D.L. and Daghlian, C.P., 1977. Investigations of angiosperms from the Eocene of southeastern North America: Philodendron leaf remains. Am. J. Bot., 64: 526--534. Dilcher, D.L. and Mehrotra, B., 1969. A study of leaf compressions of Knightiophyllum from Eocene deposits of southeastern North America. Am. J. Bot., 56: 936--943.

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