triuridaceae fossil flowers from the upper cretaceous of new jersey1

American Journal of Botany 89(12): 1940–1957. 2002.

TRIURIDACEAE FOSSIL FLOWERS FROM THE UPPER CRETACEOUS OF NEW JERSEY1 MARIÁ A. GANDOLFO,2 KEVIN C. NIXON,

AND

WILLIAM L. CREPET

L. H. Bailey Hortorium, 462 Mann Library, Cornell University, Ithaca, New York 14853-4301 USA We report here on a series of fossil flowers exhibiting a mosaic of characters present in the extant monocot family Triuridaceae. Phylogenetic analyses of morphological data from a broad sample of extant monocots confirm the affinities of the fossils with modern Triuridaceae. The fossil flowers were collected from outcrops of the Raritan Formation (Upper Cretaceous, ;90 million years before present), New Jersey, USA. These are the oldest known unequivocal monocot flowers. Because other reports of ‘‘earliest’’ monocots are all based on equivocal character suites and/or ambiguously preserved fossil material, the Triuridaceae fossils reported here should also be considered as the oldest unequivocal fossil monocots. Flowers are minute and unisexual (only male flowers are known); the perianth is composed of six tepals, lacking stomata. The unicyclic androecium is of three stamens with dithecal, monosporangiate, extrorse anthers that open by longitudinal slits. The endothecium has U-shaped type thickenings. Pollen grains are monosulcate. The triurid fossil flowers can be separated into three distinctive species. On the basis of phylogenetic analyses of morphological characters, the fossil taxa nest within the completely saprophytic achlorophyllous Triuridaceae supporting the interpretation that the extinct plants were also achlorophyllous and saprophytic. If so, this represents the earliest known fossil occurrence of the saprophytic/mycotrophic habit in angiosperms. Key words: daceae.

cladistics; Cretaceous; flowers; fossils; monocotyledons; paleobotany; Raritan Formation, New Jersey, USA; Triuri-

For many years, knowledge of primitive monocots has been based on putative monocot fossil leaves and pollen; but unfortunately these have often been only equivocally assigned to the monocots (Daghlian, 1981; Herendeen and Crane, 1995; Gandolfo, Nixon, and Crepet, 2000). Recently, Gandolfo et al. (1998) reported the discovery of fossil flowers with a suite of features characteristic of the monocotyledonous family Triuridaceae. Here, we describe these fossils in depth and include the formal and complete descriptions of distinct species and their taxonomic positions. The relationships of these fossils have been determined by a two-tiered parsimony analysis, first including a broad family-level sample of monocots and second with a more focused analysis within the family Triuridaceae. The monocotyledonous family Triuridaceae includes from seven to nine genera of achlorophyllous herbs that live symbiotically with mycorrhizal fungi. Since the family was initially proposed by Gardner in 1845, it has been treated in reviews by Beccari (1889), Hooker (1894, 1898), Smith (1927), Sandwith (1932, 1933), Giesen (1938), Larsen (1961, 1972), van de Meerendonk (1984), Maas and Ru¨bsamen (1986), Maas (1988), Ru¨bsamen-Weustenfeld (1991), and Martıńez and Go´mez (1994) among others. Miers (1852) divided the family into two tribes, Sciaphileae Manuscript received 9 October 2001; revision accepted 27 June 2002. The authors thank Jennifer L. Svitko for her assistance with laboratory, photographic, and scanning electron microscopy work; the curators of B, BH, BM, BR, C, CAS, CAY, COL, DUKE, E, F, FI, GB, HUH, JEPS, L, M, MICH, MY, OXF, R, RB, S, SP, US, VEN, WAG, and WU for sending important and scarce material of Triuridaceae; M. Harley and M. Zavada for discussions on pollen morphology and development; Charles Daghlian and Bruce Tiffney for comments that improved the manuscript; and the staff of the Interlibrary Loan Section of Mann Library, Cornell University, for their generous help during the bibliographic search. Because extant triurid collections are very limited in number and quality, we did not remove any flowers from specimens for illustrations in the plates. Photos and drawings of extant material can be consulted following the original literature cited in the text. This research was supported by NSF grant DEB 0108369 to W. L. C. and K. C. N. 2 E-mail for reprint request: [email protected]. 1

and Triurideae, a classification maintained to the present time (Maas-van de Kamer, 1995). The tribe Sciaphileae is characterized by unappendaged tepals and a basal style and comprises the genera Sciaphila Blume 1825 (;35 species), Soridium Miers 1852 (one species), Hyalisma Champion 1847 (one species), and Seychellaria Hemsley 1907 (three species). Members of the tribe Triurideae are characterized by appendaged tepals and lateral styles and include Triuris Miers 1852 (three species), Peltophyllum Gardner 1845 (two species), and Triuridopsis H. Maas and Maas 1994 (one species). The taxonomic positions of the genera Andruris Schlechter 1913 and Lacandonia Martıńez and Ramos 1989 are still in dispute. Andruris has been included within the genus Sciaphila by van de Meerendonk (1984). The 15 species that have been described by Giesen (1938) as belonging to Andruris have been placed in synonymy with several species of Sciaphila. Maas-van de Kamer and Maas (1994) and Maas-van de Kamer and Weustenfeld (1998) still consider Andruris, with five species, as best placed within the tribe Sciaphileae. Lacandonia is characterized by an inverted arrangement of the stamens and carpels (the three stamens are surrounded by the numerous carpels). Martıńez and Ramos (1989), Ma´rquez-Guzmań et al. (1989, 1993), and Va´zquez-Santana et al. (1998) segregated Lacandonia in the monogeneric family Lacandoniaceae because of the distinctive and unique position of the sexual organs, their introrse anthers, preanthesis cleistogamic fertilization, and the type of female gametophyte development. In contrast, Maas-van de Kamer and Maas (1994), Maas-van de Kamer (1995), and Maas-van de Kamer and Weustenfeld (1998) placed Lacandonia within the tribe Triurideae because it shares appendaged tepals, an apical style, indehiscent fruits, and bisporangiate anthers with other members of that group. For the purposes of our study, we treat Andruris as part of the genus Sciaphila (following van de Meerendonk, 1984) and Lacandonia as belonging to the tribe Triurideae (following Maasvan de Kamer and Maas, 1994), even though both assignments warrant further study.

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TABLE 1. Data matrix used in morphological analysis of the extant members of Triuridaceae and the two fossil genera. The genus Petrosavia was used as outgroup. Charactera Taxon

0

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

Petrosavia Sciaphila Soridium Hyalisma Seychellaria Peltophyllum Triuris Triuridopsis Lacandonia MABELIA NUHLIANTHA

0 0 0 0 0 1 1 1 0 ? ?

0 * 1 1 1 1 * 1 0 1 1

0 $ 1 3 0 0 2 2 0 0 0

0 0 0 0 0 1 1 1 1 0 0

0 $ 3 1 2 2 $ 0 2 2 2

0 0 0 0 0 1 * 1 1 0 0

0 0 0 0 0 0 * 1 1 1 1

0 * 1 1 0 1 0 1 1 * 0

0 2 2 2 2 1 1 1 1 1 1

0 0 0 0 1 0 0 0 0 1 1

0 1 1 1 1 0 0 0 0 ? ?

0 0 1 0 0 1 1 1 1 ? ?

0 0 ? ? 0 1 1 ? ? ? ?

0 0 0 0 0 1 1 ? ? ? ?

0 * 0 0 0 1 1 0 0 0 0

0 1 1 ? 2 0 0 ? ? ? ?

0 0 0 0 1 0 0 0 0 ? ?

0 0 0 0 1 0 0 0 0 0 0

0 0 0 0 * 0 0 0 1 0 0

0 1 1 0 0 0 0 0 1 * 1

a Characters and character states: 0. Sexuality: 0 5 monoecious; 1 5 dioecious. 1. Flowers: 0 5 bisexual; 1 5 unisexual. 2. Tepal number: 0 5 six, 1 5 four; 2 5 three; 3 5 eight. 3. Tepal processes: 0 5 noncaudate; 1 5 caudate. 4. Stamen number: 0 5 six; 1 5 four; 2 5 three; 3 5 two. 5. Thecae number: 0 5 two; 1 5 one. 6. Sporangia per stamen: 0 5 four; 1 5 two. 7. Filament: 0 5 present; 1 5 absent. 8. Anther dehiscence: 0 5 introrse; 1 5 extrorse; 2 5 transverse. 9. Connective appendages: 0 5 absent; 1 5 present. 10. Style: 0 5 apical; 1 5 basal. 11. Fruit: 0 5 dehiscent; 1 5 indehiscent. 12. Embryo sac: 0 5 monosporic; 1 5 tetrasporic. 13. Endosperm starch: 0 5 absent; 1 5 present. 14. Androphore: 0 5 absent; 1 5 present. 15. Tapetum: 0 5 secretory; 1 5 periplasmodial; 2 5 intermediate. 16. Druses: 0 5 absent; 1 5 present. 17. Staminodes: 0 5 absent; 1 5 present. 18. Tepal abaxial (outer) surface: 0 5 glabrous; 1 5 glandular. 19. Tepal adaxial (inner) surface: 0 5 glabrous; 1 5 glandular.

All the genera within Triurideae are Neotropical, whereas members of Sciaphileae are found in the Old World (Seychellaria, Africa; Hyalisma, India and Sri Lanka) and the New World (Soridium spruceanum Miers [1850] and seven species of Sciaphila; Giesen, 1938; van de Meerendonk, 1984; Maas and Ru¨bsamen, 1986). MATERIALS AND METHODS Fossil collection and preparation—The fossils described in this paper were collected from the Old Crossman Clay Pit locality in Sayreville, New Jersey, USA. The stratigraphic position is the South Amboy Fire Clay, Raritan Formation. On the basis of stratigraphic and palynological data, these outcrops are Turonian in age (Upper Cretaceous, ;90–94 million years before present [myBP]; Doyle and Robbins, 1977; Harland et al., 1989). The Old Crossman Clay Pit locality has yielded mosses (Crepet, Nixon, and Gandolfo, 2001), ferns (Gandolfo et al., 1997, 2000), gymnosperms (Crepet, Nixon, and Gandolfo, 2001; Gandolfo, Nixon, and Crepet, 2001), and numerous angiosperm flowers, fruits, and seeds (Crepet et al., 1992; Herendeen, Crepet, and Nixon, 1993, 1994; Nixon and Crepet, 1993a, b, 1994a, b; Crepet and Nixon, 1994, 1998a, b; Weeks, Nixon, and Crepet, 1996; Gandolfo, Nixon, and Crepet, 1998a, b; Zhou, Crepet, and Nixon, 2001). Fossils are charcoalified with threedimensional morphology and excellent anatomical details. We prepared them following the method described by Nixon and Crepet (1993a), with the modifications suggested by Gandolfo et al. (1997). Selected fossils were mounted on stubs and sputter-coated with gold/palladium in preparation for examination with an Hitachi 4500 scanning electron microscope (SEM). All fossils are deposited in the L. H. Bailey Hortorium Paleobotany Collection, Department of Plant Biology, Cornell University (CUPC 1204–1289, 1297–1330). Cladistic analyses—Two different cladistic analyses were performed: one analysis to determine the overall phylogenetic placement of the fossil taxa and their relationships with extant monocot taxa and a second analysis to explore the relationships of the fossil taxa in more detail with the extant members of the Triuridaceae. After careful comparison of the fossils with both dicot and monocot taxa, we concluded that the broad affinities were with the monocotyledons (the inclusion of the fossil in various broad angiosperm matrices confirmed this and will not be presented here). For the first analysis, we used the data matrix published by Stevenson and Loconte (1995; see original work for discussion of characters) that includes 103 monocot taxa (families and/or genera) and

101 morphological characters. We combined our fossil taxa into a single terminal for the purposes of this analysis. For this combined fossil terminal the following characters were coded: 28 (stomata absent), 31 (floral expression diclinous), 32 (perianth petaloid undifferentiated), 34 (perianth connation present), 35 (perianth curvature absent), 36 (zygomorphy absent), 37 (perigonal nectaries absent), 39 (staminodia absent), 40 (connate stamen filament absent and present), 41 (connective protrusion present), 42 (anther attachment dorsifixed), 43 (anther dehiscence orientation extrorse), 44 (anther dehiscence longitudinal), 45 (sporangia per anther bisporangial), 46 (endothecial wallthickenings girdle like), 50 (pollen units monads), 51 (pollen apertures sulcate), 52 (number of pollen apertures one), 53 (pollen aperture margin nonannulate), and 54 (pollen sculpturing reticulate and psilate). The matrix was constructed using the program WinClada (Nixon, 1999), and parsimony analyses performed with the program NONA (Goloboff, 1997). For each analysis, extensive tree searches were conducted using thousands of random starting points and tree bisection-reconnection (TBR) swapping holding 20 trees, followed by TBR swapping of shortest trees holding up to 50 000 trees (mult* and max* commands of NONA). For the second analysis, we developed a matrix that included the genus Petrosavia Beccari 1871 (Petrosaviaceae) as the outgroup and all the extant Triuridaceae genera (including Lacandonia) and the fossil taxa treated as discrete genera (Mabelia and Nuhliantha), totaling 11 terminals. We used Petrosavia as the outgroup because in the Stevenson and Loconte analysis, Petrosavia is resolved as the sister group of the Triuridaceae. We coded 20 morphological characters based on original descriptions from the literature and personal observations from herbarium specimens (Table 1). We used the same programs and tree search methods as for the first analysis.

SYSTEMATICS Family—Triuridaceae Gardner. Genus—Mabelia Gandolfo, Nixon, et Crepet, gen. nov. Type species—Mabelia connatifila Gandolfo, Nixon, et Crepet, sp. nov. Generic diagnosis—Minute, unisexual, male flower, actinomorphic; tepals six, basally fused no more than one-third of their length and free one from another the rest of their length, valvate aestivation, stomata lacking; androecium unicyclic,

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stamens three; dithecal anthers, apparently monosporangiate, extrorse, opening by a longitudinal slit, endothecium one-layered with U-shaped type thickenings, connective extensions present, pollen prolate and monosulcate. Etymology—The genus Mabelia is erected in honor of Mabel I. Me´dica (1937–1995). Description—Male flowers minute, unisexual, actinomorphic, and six-merous, 0.7–1.5 mm in diameter in bud and 1.8– 2.7 mm in diameter when opened. Flowers pedicellate, pedicel 0.085–0.2 mm long. Perianth of six tepals, basally connate not more than two-thirds of their length. Tepals triangular to oblong with recurved apex and margins, 0.57–1.4 mm long and 0.28–0.8 mm wide, adaxial (inner) and abaxial (outer) surfaces glabrous or smooth, lacking stomata. Buds with valvate aestivation. Androecium of one whorl composed of three stamens. Stamens opposite to tepals, 0.3–0.74 mm long and 0.08–0.3 mm wide, with well-differentiated filament and anther or sessile anthers, free one from another and immersed in the receptacle. Anthers dithecal, monosporangiate, ornamented or not ornamented, 0.16–0.23 mm wide, extrorse, dehiscence by longitudinal slits, one-layered endothecium with U-shaped type thickenings. Connective extensions well developed, beyond the pollen sacs, pores present or lacking, 0.07–0.22 mm wide. Pollen grains prolate and monosulcate, exine psilate or with reticulate sculpture, and tectate structure; 7–15 mm in diameter. Receptacle flat or elevated, when elevated, it is glandular, 0.4–1.05 mm in diameter. Female flowers and vegetative parts unknown. Mabelia connatifila Gandolfo, Nixon, et Crepet, sp. nov. Holotype—L. H. Bailey Hortorium Paleobotanical Collection CUPC 1255. Figs. 8, 9. Paratypes—L. H. Bailey Hortorium Paleobotanical Collection CUPC 1206, 1211–1213, 1216, 1219, 1224, 1231, 1239, 1240, 1242, 1246, 1248, 1249, 1251, 1253, 1254, 1256, 1257, 1263, 1265, 1266, 1268, 1270, 1272, 1274, 1275, 1279, 1283, 1285, 1286, 1289, 1302–1305, 1307, 1310, 1311, 1315, 1317, 1320, 1322, 1324, 1328, 1334–1336. Repository—Cornell University Paleobotany Collection, L. H. Bailey Hortorium, Department of Plant Biology, Cornell University, Ithaca, New York, USA. Type locality—Old Crossman Clay Pit, Sayreville, New Jersey, USA. Stratigraphic position—South Amboy Fire Clay, Raritan Formation. Age—Turonian, Late Cretaceous. Etymology—The epithet connatifila refers to the fusion of the filaments of the stamens. Specific diagnosis—Stamens with well-developed filaments, connate at their base. Anthers with conical tubercles. Cells of connective extensions with pores. Tepals with outer and inner surfaces glabrous. Receptacle flat and glabrous.

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Description—Male flowers minute, unisexual, actinomorphic, six-merous, 0.74–1.35 mm in diameter in bud and 1.8– 2.7 mm in diameter when opened. Flower are pedicellate, pedicel 0.14–0.2 mm long. Perianth of six tepals, basally connate no more than two-thirds of their length (Figs. 1, 2). Tepals triangular with incurved apices and margins, 0.62–1.38 mm long and 0.28–0.75 mm wide, adaxial (inner) and abaxial (outer) surfaces smooth, lacking stomata (Fig. 3). Buds with valvate aestivation (Figs. 1, 2). Androecium of one whorl composed of three stamens (Figs. 4, 5). Stamens opposite to tepals (Fig. 4), with well-developed filaments and anthers, filaments fused at bases (Figs. 5, 7) and attached to the receptacle at a single point (Fig. 6), 0.33–0.6 mm long and 0.14–0.17 mm wide. Anthers dithecal, monosporangiate (Figs. 7, 8, 11), ornamented by three conical projections or tubercles (Figs. 8– 10), extrorse, 0.21–0.22 mm wide; dehiscence by longitudinal slits (Fig. 4), endothecium one-layered with U-shaped thickenings (Figs. 5, 7, 11). Connective extensions well developed beyond pollen sacs (Figs. 4, 10, 11), with polygonal epidermal cells bearing pores (interpreted as hydathodes) (Figs. 12–13), 0.1–0.2 mm wide. Pollen grains prolate, monosulcate, exine tectate and psilate, 11–15 mm (Figs. 14–17). Receptacle flat and glabrous (Fig. 5), 0.4–0.88 mm in diameter. Female flowers and vegetative parts unknown. Mabelia archaia Gandolfo, Nixon, et Crepet, sp. nov. Holotype—L. H. Bailey Hortorium Paleobotanical Collection CUPC 1269. Figs. 20, 23, 24. Paratypes—L. H. Bailey Hortorium Paleobotanical Collection CUPC 1204, 1205, 1209, 1215, 1217, 1218, 1221, 1225, 1227, 1229, 1230, 1235, 1236, 1237, 1241, 1244, 1245, 1247, 1250, 1258–1261, 1264, 1271, 1273, 1276–1278, 1280, 1281, 1282, 1284, 1287, 1288, 1297–1300, 1306, 1312, 1314, 1316, 1318, 1319, 1321, 1323, 1325–1327, 1329, 1330, 1331. Repository—Cornell University Paleobotany Collection, L. H. Bailey Hortorium, Department of Plant Biology, Cornell University, Ithaca, New York, USA. Type locality—Old Crossman Clay Pit, Sayreville, New Jersey, USA. Stratigraphic position—South Amboy Fire Clay, Raritan Formation. Age—Turonian, Late Cretaceous. Etymology—The epithet archaia is from the Greek for ‘‘old, ancient.’’ Specific diagnosis—Anthers sessile, free from one another, sunken in an elevated receptacle. Anthers lacking tubercles. Cells of connective extensions without pores. Tepals with outer surfaces smooth and inner surfaces glandular. Receptacle elevated and glandular. Description—Male flowers minute, unisexual, actinomorphic, six-merous, 0.7–1.5 mm in diameter in bud and 1.8–2.6 mm in diameter when opened. Flower pedicellate, pedicel 0.08–0.3 mm long. Perianth of six tepals, basally connate only one-third of their length (Figs. 18, 21). Tepals oblong with

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Figs. 1–6. Mabelia connatifila Gandolfo, Nixon, et Crepet. 1. Overall lateral view of a pedicellate bud. Note the valvate aestivation of the basally fused tepals and their tips incurved toward the center of the flower. CUPC 1212. 360. Bar 5 167 mm. 2. Top view of the same specimen showing the valvate aestivation of the tepals. CUPC 1212. 360. Bar 5 167 mm. 3. Detail of two tepals showing the incurved margins and tips. Note the smooth inner surface. CUPC 1224. 390. Bar 5 111 mm. 4. Top view of a dissected flower in which part of the tepals has been removed to reveal the androecium. Note the three stamens with the filaments fused and placed at the center of the flower. CUPC 1256. 370. Bar 5 143 mm. 5. Side view of a dissected flower showing the fused filaments of the stamens. CUPC 1253. 370. Bar 5 143 mm. 6. Detail of the unique point of insertion of the fused filaments on the receptacle (the filaments have been removed). CUPC 1268. 390. Bar 5 111 mm.

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Figs. 7–11. Mabelia connatifila Gandolfo, Nixon, et Crepet. 7. Top view of a dissected flower showing the monothecal anthers. CUPC 1251. 3180. Bar 5 56 mm. 8. Close side view of the androecium. Note the fused filaments, the pollen sacs, and the connective extensions. CUPC 1255. 3110. Bar 5 91 mm. 9. Detail of a closed pollen sac showing the three conical tubercles. CUPC 1255. 3350. Bar 5 28.5 mm. 10. Detail of the endothecium with U-shaped thickenings and a conical tubercle at the external surface of the pollen sac. CUCP 1256. 31000. Bar 5 3 mm. 11. Detail of a dissected stamen in which part of the anthers has been removed to show that each anther is monothecal. CUPC 1310. 3250. Bar 5 40 mm.

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Figs. 12–17. Mabelia connatifila Gandolfo, Nixon, et Crepet. 12. Detail of an extended connective extension. CUPC 1322. 3300. Bar 5 33 mm. 13. Closeup of the same connective extension showing the polygonal cells and the ‘‘hydathodes.’’ CUPC 1322. 31100. Bar 5 9 mm. 14. Pollen sac with clumps of pollen grains in situ. CUPC 1216. 3180. Bar 5 56 mm. 15. Close-up of the same pollen sac. CUPC 1216. 31000. Bar 5 10 mm. 16. Monosulcate psilate pollen grain. CUPC 1216. 37000. Bar 5 1.4 nm. 17. Detail of a broken pollen grain showing the tectate exine. CUPC 1242. 380 000. Bar 5 125 nm.

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Figs. 18–23. Mabelia archaia Gandolfo, Nixon, et Crepet. 18. Overall lateral view of a pedicellate bud. Note the valvate aestivation of the basally fused tepals and their tips incurved toward the center of the flower. CUCP 1225. 360. Bar 5 167 mm. 19. Top view of the same specimen showing the valvate aestivation of the tepals. CUCP 1225. 360. Bar 5 167 mm. 20. Detail of a tepal showing the incurved margins and tips. Note the smooth outer (abaxial) surface and the glandular inner (adaxial) surface. CUPC 1269. 3110. Bar 5 250 mm. 21. Top view of an open flower showing the central androecium. Note the three stamens with large connective extensions and open anthers. CUPC 1287. 340. Bar 5 91 mm. 22. Side view of a dissected flower showing the apparently sunken stamens. CUPC 1241. 360. Bar 5 167 mm. 23. Detail of the three points of insertion of the each of the filaments on the receptacle (filaments have been removed). CUPC 1269. 3120. Bar 5 67 mm.

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incurved margins and apices, 0.5–1.2 mm long and 0.31–0.8 mm wide, adaxial (inner) surface glandular and abaxial (outer) surface smooth, lacking stomata (Figs. 20, 21). Buds with valvate aestivation (Figs. 18, 19). Androecium of one whorl composed of three stamens (Figs. 21, 26). Stamens opposite to three of the tepals (Figs. 21, 22), anthers sessile (Figs. 22, 26), free one from another, immersed in the receptacle (Fig. 23). Anthers dithecal, monosporangiate, lacking ornamentation, extrorse, 0.3–0.74 mm long and 0.08–0.3 mm wide, dehiscence by longitudinal slits (Figs. 21, 22, 25, 26), endothecium onelayered with U-shaped thickenings (Fig. 27). Connective extensions well developed beyond pollen sacs (Figs. 21, 22, 26, 28), with polygonal epidermal cells without pores or ‘‘hydathodes’’ (Figs. 28, 29), 0.07–0.22 mm wide. Pollen grains prolate and monosulcate, with tectate and reticulate exine, 7–13 mm (Figs. 30–34). Receptacle elevated and glandular (Fig. 24), 0.46–1.05 mm in diameter. Female flowers and vegetative parts unknown. Nuhliantha Gandolfo, Nixon, et Crepet; gen. nov. Type species—Nuhliantha nyanzaiana Gandolfo, Nixon et Crepet, sp. nov. Generic diagnosis—Minute, unisexual, male flower, actinomorphic; tepals six, basally fused one-third of their length, valvate aestivation, stomata lacking; androecium unicyclic, stamens three; dithecal anthers, monosporangiate, extrorse, opening by longitudinal slits, endothecium one-layered with U-shaped thickenings, connective extensions not developed beyond pollen sac, pollen monosulcate. Central pistillode surrounded by androecium. Receptacle elevated and glandular. Etymology—The genus Nuhliantha is erected in honor of Natalie W. Uhl, Emeritus Professor of the L. H. Bailey Hortorium, Cornell University, for her many contributions to the knowledge of monocotyledons. The epithet nyanzaiana is proposed in honor of Nyanza Rothman, daughter of Michael Rothman. Holotype—L. H. Bailey Hortorium Paleobotanical Collection CUPC 1267. Figs. 35–44. Repository—Cornell University Paleobotany Collection, L. H. Bailey Hortorium, Department of Plant Biology, Cornell University, Ithaca, New York, USA. Type locality—Old Crossman Clay Pit, Sayreville, New Jersey, USA. Stratigraphic position—South Amboy Fire Clay, Raritan Formation.

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vate aestivation. Androecium of one whorl composed of three stamens. Stamens opposite to the tepals (Figs. 35, 37, 38), free one from another, anthers sessile. Anthers dithecal, monosporangiate, 0.18–0.23 mm wide, extrorse, opening by longitudinal slit, endothecium one-layered with U-shaped thickenings. Connective extensions not developed beyond the pollen sacs, 0.14–0.23 mm wide (Figs. 39–41). Pollen grains prolate, monosulcate, exine finely reticulate, and 17–19 mm (Fig. 42). Pistillode triangular in cross section (0.2 mm 3 0.18 mm 3 0.18 mm), 0.35 mm in height, surrounded by the androecium, centered on receptacle (Figs. 43–44). Receptacle elevated and glandular, 0.86 mm in diameter (Fig. 36). Female flowers and vegetative parts unknown. RESULTS Relationships of fossil taxa with the extant monocotyledonous families—Although all the characters preserved in the fossils indicate close affinities with the extant family Triuridaceae, we elected to investigate the phylogenetic placement of the fossil taxa and to precisely explore their relationships with extant monocotyledons through parsimony-based phylogenetic analysis. The published morphological matrix for monocotyledon families of Stevenson and Loconte (1995, see for character discussion) was used without modification except for addition of the fossil terminal. This matrix was selected because it is the only complete morphological matrix for monocotyledons that covers the breadth of the group with sufficient detail. Chase et al. (2000), based on molecular data, proposed that the family Triuridaceae is closely related to the families Pandanaceae, Cyclanthaceae, Velloziaceae, and Stemonaceae, but the study used only the genus Sciaphila to represent the Triuridaceae. Nonetheless, work based on morphological as well as molecular data of selected taxa within the monocots is confirming the relationship suggested by Chase et al. (F. Vergara et al., Instituto de Biologıá, Universidad Nacional Autońoma de Mexico, unpublished data); however, additional analyses that include other genera of Triuridaceae are required to unequivocally confirm the position of Triuridaceae. Our purpose was not to consider overall monocot relationships per se, but rather to place the fossils with their nearest relatives in an objective fashion on the basis of character distribution. Analysis of the Stevenson and Loconte matrix with a compound fossil taxon (representing all the fossil species) resulted in 16 equally most parsimonious trees, with a length of 845 steps, a consistency index of 22, and a retention index of 64. The fossil taxon is nested ‘‘above’’ the genus Petrosavia Beccari as a sister taxon of the family Triuridaceae in the strict consensus (Fig. 45). The clade formed by Petrosavia (fossil taxon [Triuridaceae]) is stable in all most parsimonious trees as well as in the consensus tree. The result of this analysis supports the taxonomic relationship of the fossils to the Triuridaceae.

Age—Turonian, Late Cretaceous. Specific diagnosis—As for the genus Nuhliantha. Description—Male flower minute, unisexual, actinomorphic, six-merous, 1.32 mm in diameter (Figs. 35, 36). Pedicel unknown. Perianth of six tepals basally fused one-third of their length. Tepals triangular with incurved apex, 1.3 mm long and 0.7 mm wide, adaxial (inner) and abaxial (outer) surfaces glabrous, lacking stomata (Figs. 35–37). Bud with probably val-

Relationships of the fossil taxa with the members of the family Triuridaceae—Because of the results of our initial cladistic analysis, in which the fossils, treated as a single terminal, are placed as a sister taxon to the single terminal representing the family Triuridaceae, we decided to explore the relationships of the fossil taxa to the extant members of the Triuridaceae. A matrix of morphological characters was constructed for extant genera of Triuridaceae, and the fossils treated as two separate terminals, Mabelia and Nuhliantha. We scored 20 morpholog-

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Figs. 24–29. Mabelia archaia Gandolfo, Nixon, et Crepet. 24. Side view of the elevated and glandular receptacle. CUPC 1269. 3150. Bar 5 91 mm. 25. Top view of the androecium showing the free stamens. CUPC 1299. 3200. Bar 5 50 mm. 26. Side view of the androecium. Note the three stamens with extrorse opened anthers and connective extensions beyond the pollen sacs. CUPC 1260. 3100. Bar 5 91 mm. 27. Detail of the endothecium. Note the Ushaped thickenings. CUPC 1217. 31000. Bar 5 10 mm. 28. Detail of an extended connective extension. CUPC 1264. 3120. Bar 5 40 mm. 29. Close-up of a connective extension showing the polygonal cells. Note the lack of ‘‘hydathodes.’’ CUPC 1312. 3350. Bar 5 29 mm.

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Figs. 30–34. Mabelia archaia Gandolfo, Nixon, et Crepet. 30. Clumps of pollen grains found within a pollen sac. CUPC 1225. 31000. Bar 5 10 mm. 31. Equatorial view of a prolate monosulcate pollen grain. CUPC 1298. 39000. Bar 5 1 mm. 32. Polar view of a pollen grain. CUPC 1236. 310 000. Bar 5 1 mm. 33. Detail of the surface of the sulcus. CUPC 1225. 340 000. Bar 5 250 nm. 34. Detail of the foveolate exine. CUPC 1225. 340 000. Bar 5 250 nm.

ical characters for the extant genera; of those, the following were scored as missing for both fossil taxa: 0 (sexuality), 10 (style), 11 (fruit), 12 (embryo sac), 13 (endosperm starch), 15 (tapetum), and 16 (druses). Analysis of this matrix resulted in two equally most parsimonious trees, with a consistency index of 72, a retention index of 72, and a length of 36 steps. The differences between the two are the positions of Peltophyllum, Triuris, and Triuridopsis. The consensus tree of the two most parsimonious trees is presented in Fig. 46. In this analysis, we obtained two well-defined clades. One

includes all the members of the tribe Sciaphileae (Seychellaria, Hyalisma, Sciaphila, and Soridium), and the other includes the fossil taxa and the extant members of the tribe Triurideae. The fossil genera, Mabelia and Nuhliantha, form a clade that is the sister group of the clade formed by Triuris, Triuridopsis, Peltophyllum, and Lacandonia. On the basis of this analysis, Mabelia and Nuhliantha belong to the tribe Triurideae. Lacandonia is nested within this last clade, supporting the hypothesis that Lacandonia belongs to the family Triuridaceae and is a member of the tribe Triurideae.

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Figs. 35–40. Nuhliantha nyanzaiana Gandolfo, Nixon, et Crepet. 35. Top view of the flower showing the remains of the perianth composed of six tepals, probably with valvate aestivation. Note the central pistillode surrounded by the three stamens. CUPC 1267. 353. Bar 5 190 mm. 36. Side view showing the elevated receptacle and one of the stamens. Note that the anthers are extrorsely open. CUPC 1267. 353. Bar 5 190 mm. 37. Other side view, showing the incurved tip of the tepal, the central pistillode, and remains of stamens. CUPC 1267. 353. Bar 5 190 mm. 38. Close-up of one stamen. Note the connective extension and the groups of pollen grains within the anther. CUPC 1267. 3113. Bar 5 89 mm. 39. Frontal view of a stamen. Note the monothecal anther and the clumps of pollen grains. CUPC 1267. 3135. Bar 5 7.4 mm. 40. Close-up of the endothecium with U-shaped thickenings. CUPC 1267. 31500. Bar 5 7 mm.

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Figs. 41–44. Nuhliantha nyanzaiana Gandolfo, Nixon, et Crepet. 41. Close-up of the connective extension. CUPC 1267. 3300. Bar 5 33 mm. 42. Equatorial view of a prolate monosulcate pollen grain. CUPC 1267. 36000. Bar 5 1.7 mm. 43. Top view of the flower showing the triangular pistillode surrounded by the androecium. CUPC 1267. 3110. Bar 5 91 mm. 44. Side view of the triangular pistillode. CUPC 1267. 3300. Bar 5 33 mm.

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Fig. 46. Consensus tree of two equally most parsimonious trees found by analyzing the extant members of the family Triuridaceae and the two fossil genera. Fig. 45. Relevant part of the consensus tree of 16 equally most parsimonious trees found by analyzing the Stevenson and Loconte (1995) monocot morphological matrix and the fossil taxa.

DISCUSSION As noted above, the Triuridaceae are mycotrophic (the intercellular fungal tissues are digested by the plant), achlorophyllous herbs. Characters that diagnose the family are the absence of vessels and reduced scale-like leaves without stomata. The plants can be monoecious (as in the tribe Sciaphileae) or dioecious (as in Triurideae), with the inconspicuous flowers aggregated in 1–120 flowered racemose inflorescences (Tomlinson, 1982; Maas and Ru¨bsamen, 1986; Maas-van de Kamer, 1995). One of the most relevant characteristics of the modern Triuridaceae is the extensive variation in floral morphology (Maas-van de Kamer, 1995). Sexuality—Although the flowers of Triuridaceae are considered to be mostly unisexual, there are many exceptions, such as the presence of uniformly hermaphroditic flowers (Lacandonia schismatica Martıńez and Ramos 1989 and Sciaphila rubra Maas 1979; Maas, 1979; Maas and Ru¨bsamen, 1986; Martıńez and Ramos, 1989), female and hermaphroditic flowers (Sciaphila picta Miers 1852, and Sciaphila takakumensis Ohwi 1965; Ohwi, 1938, 1965; Walker, 1976; Go´mez, 1982; Maas, 1988; Maas and Ru¨bsamen, 1986; Martıńez and Go´mez, 1994), and male and hermaphroditic flowers (Sciaphila tenella Blume 1825 and Sciaphila maculata Miers 1850; Schlechter, 1913; Smith, 1927, Giesen, 1938; Backer and Bakhuizen van den Brink, 1968; van de Meerendonk, 1984). Hyalisma janthina Champion 1847, also within Sciaphileae, is considered to be monoecious, but sometimes has only male flowers (Champion, 1847). Maas-van de Kamer and Maas (1994) and Maas-van de Kamer (1995) assert that flowers of members of the tribe Triurideae are always unisexual and therefore dioecious. However, this assumption proved incorrect because Ru¨bsamen-Weustenfeld (1991) observed that Triuris hyalina can be dioecious or hermaphroditic. In addition, Martıńez (1994) described specimens of the species Triuris brevistylis (T. hyalina of Maas and Ru¨bsamen, 1986) as hermaphroditic based on the study of numerous collections. One of us (M. A. Gandolfo) has examined the specimens studied by Martıńez (1994) and confirmed the presence of hermaphroditic flowers (MEXU, Martıńez nros. 23995, 24511, 24522). If Lacandonia, invariably hermaphroditic (Martıńez and Ramos, 1989; Martıńez, 1994), belongs to the tribe Triurideae, as suggested by Maas-van de Kamer and Maas (1994) and Maas-van de Kamer

(1995), it unequivocally illustrates that the tribe includes taxa with hermaphroditic flowers. We do not know the sexuality of the plants that produced the triurid fossil flowers, because we have found only isolated male flowers. At a minimum, Mabelia and Nuhliantha produced unisexual flowers, the most common type of sexuality encountered in extant triurids, but this does not preclude the possibility of undiscovered hermaphroditic flowers in these taxa. Flower morphology—The flowers of modern Triuridaceae range in diameter from 1 to 8 mm, including the tepal processes such as tails (Tomlinson, 1982; Maas and Ru¨bsamen, 1986), and are subtended by bracts. In bud, they exhibit valvate aestivation, and the flowers are often stellate and patent at anthesis (Ru¨bsamen-Weustenfeld, 1991; Maas-van de Kamer, 1995). The flowers of the triurid fossil taxa Mabelia connatifila, M. archaia, and Nuhliantha are also minute (between 1.3 and 2.7 mm in diameter), with valvate aestivation (Figs. 1–2, 18–19, 35–36). After anthesis, they display the characteristic stellate shape (Fig. 20). Perianth—The perianth of extant and fossil Triuridaceae is composed of a single cycle of tepals, with diverse morphology depending on the species. The most common number of tepals per flower is six in modern species, although it can vary. For members of the tribe Sciaphileae the number of tepals can vary between two and ten, while in the tribe Triurideae, there are between three and eight (Giesen, 1938; van de Meerendonk, 1984; Maas-van de Kamer, 1995). There are always six tepals in the fossil taxa, constant within the three species (Figs. 1– 4, 19–21, 35), as in most extant Triuridaceae. As in the modern Triuridaceae, the six tepals of the fossils are basally fused for at least one-third of their length (Figs. 1–2, 18–21, 35). Tepal morphology—Although all species of Triuridaceae are characterized by the absence of stomata on the tepals, the size and shape of the tepals (including margins and apices), their indumenta, and the processes at the tips vary within the living members of the family. These characters have been used to divide the family into two tribes. Within the tribe Sciaphileae, tepals are described as ovate-lanceolate or broadly ovate to deltoid, of equal or unequal size, glabrous or papillate, with or lacking distinctive processes at the tips, and with or without revolute margins at maturity (Champion, 1847; Hemsley, 1907; Giesen, 1938; Vollesen, 1981, 1985; van de Meerendonk, 1984; Maas and Ru¨bsamen, 1986). For the tribe Triur-

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ideae, tepal variability is also extensive. Tepals can be glabrous or ciliate, deltoid to triangular, apically tridentate or with tails or short appendices (Gardner, 1845; Poulsen, 1884–1886; Schumann, 1894; Giesen, 1938; Brade, 1943; Maas and Ru¨bsamen, 1986; Maas-van de Kamer and Maas, 1994; Martıńez and Go´mez, 1994). Like modern Triuridaceae, Mabelia connatifila, M. archaia, and Nuhliantha lack tepal stomata and vary in the indumentum, but their tepals are morphologically quite uniform in shape. They are always triangular to oblong with revolute margins, and their apices are acuminate and revolute lacking any type of appendages. These features are also encountered in many extant species of the tribe Sciaphileae (see discussion above). With respect to the indumentum, tepals of Mabelia connatifila (Figs. 1–4) and Nuhliantha (Fig. 35) are glabrous on both surfaces, whereas those of Mabelia archaia are adaxially glandular and abaxially glabrous (Figs. 19– 21), as in some extant species of both tribes. Androecium—The androecia of extant and fossil Triuridaceae are similarly arranged in a single whorl. The position of the stamens relative to the tepals is difficult to determine (Maas-van de Kamer, 1995). On the basis of developmental studies, Ru¨bsamen-Weustenfeld (1991) suggests that stamens are opposite to the outer tepals in members of Sciaphileae, while in members of Triurideae they are opposite to the inner tepals. In the fossil species, there are always three stamens, opposite to one set of three tepals (Figs. 4, 21, 35), but we cannot determine if this set represents the inner or outer tepal series. The number of stamens is usually three in extant species, but other numbers, from two to six, occur in some species. The stamens of Mabelia connatifila have basally connate filaments attached as a single unit to the receptacle (Figs. 5, 6, 8). This pattern is common in members of the modern tribe Sciaphileae, e.g., in Hyalisma (Champion, 1847), Seychellaria thomassettii Hemsley 1907 (Hemsley, 1907; Giesen, 1938), and some extant species of Sciaphila, such as S. arfakiana Becc. 1889, S. consimilis Bl. 1851, and S. multiflora Giesen 1938 (van de Meerendonk, 1984). In contrast, the stamens of M. archaia and Nuhliantha have very short filaments, free one from another and individually inserted in the receptacle (Figs. 23, 35). This occurs in two monotypic genera of the modern tribe Triurideae—Lacandonia (Martıńez and Ramos, 1989) and Triuridopsis (Maas-van de Kamer and Maas, 1994)—and in several species of Sciaphila (e.g., S. aneitensis Hemsley 1907 and S. micranthera Giesen 1938 [van de Meerendonk, 1984]). The stamens of Nuhliantha (Figs. 37, 43) and Triuridopsis (Maas-van de Kamer and Maas, 1994) are arranged around the central pistillode, which is lacking in the other two fossils. The number of thecae and sporangia per stamen varies within both modern tribes (Maas-van de Kamer and Maas, 1994). Members of the tribe Sciaphileae have two thecae and four sporangia per stamen, with the exceptions of Soridium, which can have two sporangia (Standley and Steyermark, 1958; Maas, 1988), and about one-third of the species of Sciaphila, which are trisporangiate (Giesen, 1938; Green and Solbrig, 1966; van de Meerendonk, 1984; Maas-van de Kamer, 1995). Members of the tribe Triurideae exhibit more variation (e.g., one theca and four sporangia per stamen, one or two thecae and two or four sporangia per stamen, one theca and two sporangia, and one theca and three sporangia; Schumann, 1894; Jonker, 1943; Standley and Steyermark, 1958; Martinez and Ramos, 1989; Ma´rquez-Guzmań et al., 1993; Maas-van de Ka-

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mer and Maas, 1994). The stamens of Mabelia and Nuhliantha are always dithecal, and each theca appears to be monosporangiate (Figs. 7, 11, 25, 26, 39), as in some modern Triurideae. Mabelia connatifila is distinct from all living and fossil species because it has three conical tubercles on the external wall of each pollen sac (Figs. 9, 10). One character often used to separate the two tribes even though there is some intergradation is the mode of dehiscence of the anthers (Mass-van de Kamer, 1995). The three fossil species always have longitudinal dehiscence (Figs. 10, 26, 38) as in Lacandonia (Martıńez and Ramos, 1989), Triuris hyalina (Giesen, 1938; Standley and Steyermark, 1958), and Peltophyllum luteum (Fiebrig, 1922) from the tribe Triurideae. All Sciaphileae anthers open by transverse dehiscence except for Neotropical Sciaphila rubra that has longitudinal slits (Maas, 1979; Maas and Ru¨bsamen, 1986; Maas-van de Kamer, 1995). All fossil (Figs. 4, 8, 26, 28, 36, 38) and extant (Tomlinson, 1982; Ru¨bsamen-Weustenfeld, 1991; Maas-van de Kamer, 1995) Triuridaceae are extrorse with the exception of P. luteum and Lacandonia, both of which are introrse (Martıńez and Ramos, 1989; Ma´rquez-Guzmań et al., 1993; Maas-van de Kamer, 1995). All Triuridaceae, extant and fossil, have endothecial cells with U-shaped wall thickenings (Ru¨bsamen-Weustenfeld, 1991; Maas-van de Kamer, 1995; Figs. 10, 27, 40). One important stamen character of the fossil species is the connective extension, because it allows the discrimination of three species. Connective extensions have been described in Seychellaria madagascarensis Wright 1912 (Giesen, 1938) and three species of Sciaphila: S. arfakiana, S. multiflora, and S. wariana Schlechter 1913 (Schlechter, 1913; Fosberg and Sachet, 1980; Maas-van de Kamer, 1995). In S. multiflora the extension is described as large ‘‘resembling a third anther cell’’ (Fosberg and Sachet, 1980, p. 25). For the rest of the species, the connective extensions are described as filiform (Schlechter, 1913; Giesen, 1938). The connective extensions of the two species of Mabelia are very well developed, prolonged beyond the pollen sacs, globose, and formed by polygonal cells (Figs. 4, 11, 12, 22, 26, 28). In M. connatifila the connective extensions are characterized by pores (Figs. 12, 13) while those of M. archaia lack pores (Figs. 28, 29), a difference that allows us to distinguish the two species. In Nuhliantha the connective extensions are well developed, but they are not prolonged beyond the pollen sacs (Figs. 35, 43). Pollen grains—There are few reports detailing the palynology of Triuridaceae. Pollen grains of Triuridaceae are produced in square or decussate tetrads and, at maturity, are shed as monads. These are three-celled and inaperturate or onecolpoid, with exine that is psilate, finely reticulate, finely to coarsely granulose, or verrucose (Ru¨bsamen-Weustenfeld, 1991). Within Sciaphileae, pollen grains of Sciaphila are spherical to elliptical or boat-shaped, inaperturate or one-colpate (monosulcate for van de Meerendonk [1984] and Sahashi et al. [1991]), 14–40 mm, with psilate or granular to finely verrucose exine (Wirz, 1910; Erdtman, 1952; Ru¨bsamenWeustenfeld, 1991); in several species, such as S. densiflora, S. tenella Blume 1825, and S. winkleri Schlechter 1913, the exine is very thin and covered with microverrucae (van de Meerendonk, 1984). Chuma (1990) and Sahashi et al. (1991) described pollen grains of S. japonica as having a well-defined sulcus and exine with gemmate to verrucate protrusions. Those of Seychellaria and Soridium are similar to those of Sciaphila (Ru¨bsamen-Weustenfeld, 1991), whereas Hyalisma pollen

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Comparisons among the three fossil species. Species Character

Sexuality Symmetry Aestivation Perianth Tepal morphology Tepal adaxial surface Tepal abaxial surface Androecium; no. stamens Stamen filament Filament Attachment to receptacle Anther Anther ornamentation Dehiscence Endothecium Connective extensions Pores in connective Pollen grains Exine Pollen grain size ‘‘Pistillode’’ Receptacle

Mabelia connatifila

Unisexual, male Actinomorphic Valvate Six-merous Triangular, basally fused Glabrous Glabrous Whorl; 3 Present Fused one to another Single point Dithecal, monosporangiate Present Extrorse, longitudinal slit One-layered, U-shaped thickening Present, beyond pollen sacs Present Prolate, monosulcate Psilate 11–15 mm Absent Flat, glabrous

Mabelia archaia

Unisexual, male Actinomorphic Valvate Six-merous Oblong, basally fused Glandular Glabrous Whorl; 3 Absent — Three points Dithecal, monosporangiate Absent Extrorse, longitudinal slit One-layered, U-shaped thickening Present, beyond pollen sacs Absent Prolate, monosulcate Reticulate 7–13 mm Absent Elevated, glandular

grains are quite different in having echinate exine sometimes with gemmae (Ru¨bsamen-Weustenfeld, 1991). Within the Triurideae, the pollen grains of Triuris and Peltophyllum are smaller than those of Sciaphileae (between 15 and 25 mm), spherical to elliptical, and inaperturate, with finely granular to granular, microverrucate or finely reticulate exine (van de Meerendonk, 1984; Ru¨bsamen-Weustenfeld, 1991). There is no published information on the morphology of the pollen grains of Triuridopsis or Lacandonia, although E. Martıńez (Instituto de Biologıá, Universidad Nacional Autońoma de Me´xico, personal observation) describes the pollen grains of Lacandonia as similar to those of Triuris. Pollen grains of the fossil species of Triuridaceae resemble those of modern Triuridaceae. They are prolate, monosulcate (rarely preserved in a folded fashion that might be mistaken for different aperture configurations), 7–19 mm in diameter (in equatorial view) with psilate to finely reticulate exine sculpture (Figs. 15, 16, 31, 32, 34, 42). All these characters are found in pollen of extant genera. Pollen grains of Mabelia connatifila are tectate (Fig. 17). Among the three species, Nuhliantha has the largest grains (19 mm in diameter in equatorial view), while M. archaia has the smallest (7 mm in diameter in equatorial view). Pistillode(?)—Of the three fossil species, only Nuhliantha has a central triangular structure (Figs. 35, 37, 43, 44), which is similar to the central triangular structure of Triuridopsis (Maas-van de Kamer and Maas, 1994). The latter, known only from Peru, is characterized by a central triangular structure that is surrounded by six stamens with well-developed filaments, each with two pollen sacs. Triuridopsis and Nuhliantha are the only two genera within the family that have this presumed pistillode. Comparisons among the three fossil species—The flowers of the three Triuridaceae fossil species are inconspicuous, unisexual, actinomorphic, and male (Table 2). In bud they have valvate aestivation. Their perianth configuration is always sixmerous, with tepals basally fused and lacking stomata. The

Nuhliantha nyanzaiana

Unisexual, male Actinomorphic Valvate Six-merous Triangular, basally fused Glabrous Glabrous Whorl; 3 Present Free one from another Three points Dithecal, monosporangiate Absent Extrorse, longitudinal slit One-layered, U-shaped thickening Present, not beyond pollen sacs Absent Prolate, monosulcate Finely reticulate 17–19 mm Present Elevated, glandular

androecium in all the species is arranged in a single whorl and is composed of three stamens. The anthers are dithecal, each theca presumably monosporangiate, and extrorse, and they open by longitudinal slits, leaving exposed the one-layered endothecium with U-shaped thickenings. The pollen grains are prolate and monosulcate. Mabelia connatifila is characterized by stamens with basally connate filaments, ornamentated anthers, pores or ‘‘hydathodes’’ on the connective extensions, psilate pollen grains, and a flat glabrous receptacle. Mabelia archaia differs from M. connatifila in having sunken anthers, no ornamentation on the anthers, and no pores (‘‘hydathodes’’) on the connective extensions, reticulate pollen grains, and an elevated glandular receptacle. Nuhliantha is the only fossil that has a central pistillode surrounded by the stamens; the connective extensions, although present, do not extend beyond the pollen sacs, and the pollen micromorphology is finely reticulate. Comparison with other fossil taxa—Herendeen et al. (1999) described trimerous staminate flowers as ‘‘cf. Triuridaceae.’’ These flowers are one component of the Allon flora (Georgia, USA, Late Santonian). The Allon Triuridaceae fossil flowers are actinomorphic, the perianth is composed of six basally fused tepals, the androecium has three stamens, and the anthers are extrorse and open by longitudinal slits, have thick and extended connective extensions, and produce monosulcate pollen grains. Although there is no formal description, the authors identify two different taxa: one characterized by the sunken anthers on the receptacle and the other by a thick central column that bears the anthers. The Allon Triuridaceae are similar to the ones we describe in this paper, and at least one taxon is comparable to Mabelia archaia, because it shares the sunken anthers. The other taxon mentioned by Herendeen et al. (1999) has not been found in the Raritan flora. However, the presence of anthers in a central column or cylindrical androphore is characteristic of the Neotropical species S. purpurea Bentham 1855 (Maas and Ru¨bsamen, 1986).

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Habitat—As mentioned previously, the Triuridaceae have a tropical and subtropical distribution, with each species restricted to a single continent (Maas-van de Kamer, 1995). They are mostly found at elevations 0–1400 m in rain forests and in wet, frequently flooded areas along river and creek banks, growing on dead and rotten leaves. All the genera within the tribe Triurideae have Neotropical distribution. Lacandonia and Triuridopsis grow in restricted areas—Lacandonia in the Selva Lacandona (Mexico) and Triuridopsis in Peru—and the other genera are found in Central America and northern South America. Members of Sciaphileae are found principally in the Paleotropics. Seychellaria is found only in Africa (Tanzania, Madagascar, and the Seychelles). Hyalisma is restricted to India and Sri Lanka. Almost all Sciaphila species grow in the South Pacific. Soridium spruceanum Miers 1850 and seven species of Sciaphila are exceptions in the tribe, as they are found entirely in the Neotropics (Giesen, 1938; van de Meerendonk, 1984; Maas and Ru¨bsamen, 1986). There are reports of Soridium growing on ant nests and Sciaphila purpurea on termite nests (Maas, 1981). The environment in which the Old Crossman Clay Pit sediments were deposited has been described as fluvial and the climate tropical to subtropical (Brenner, 1963). Triuridaceae fossils were found in association with a diverse assemblage, including tropical elements such as Schizaeaceae, Gleicheniaceae, Clusiaceae, Chloranthaceae, Lauraceae, and ‘‘basal’’ Fagaceae. This complex assemblage supports the climate conditions proposed by Brenner (1963). There are also several gymnosperms such as Pinaceae and Cupressaceae. Gandolfo, Nixon, and Crepet (2001) compared the environment where the fossil species once grew to the tropical lowland coastal Mosquitia region of Honduras, which Clewell (1986) described as open forest (including Pinus) interdigitating with tropical evergreen gallery forest and creek-side assemblages. Modern Triuridaceae are often found in this type of habitat. The presence of Triuridaceae fossils in the assemblage strengthens the tropical characterization of the paleoclimate. Conclusions—Unequivocal monocots are not well represented in the early Cretaceous. These triurid fossils represent the earliest unequivocal record for monocotyledons and possibly the earliest known occurrence of the saprophytic/mycotrophic habit in angiosperms. In addition, these fossils are the most complete in terms of characters and best understood putative early monocotyledonous fossils. Thus, they raise the interesting possibility that triurids are a very early branch within the monocots. Alternatively, these fossils might suggest that monocots are actually much older. There are no older monocot fossils that stand rigorous examination because reports of early Cretaceous monocots are compromised by preservation that fails to provide the diagnostic characters necessary to verify monocotyledonous affinities and to rule out affinities with various ‘‘basal’’ dicotyledonous angiosperm taxa (Gandolfo, Nixon, and Crepet, 2000). Thus we might infer that if the monocots are indeed much older, as seems likely based on the sequence of appearance of unequivocally monocotyledonous taxa throughout the remainder of the Cretaceous, then bona fide monocots are not represented in older sediments because of ecological or preservational bias. Either interpretation invites careful scrutiny of both the fossil record and phylogenetic analyses of extant flowering plants based on morphological and molecular data.

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