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Paleobotany |
L. H. Bailey Hortorium, 462 Mann Library, Cornell University, Ithaca, New York 14853-4301 USA
Received for publication October 9, 2001. Accepted for publication June 27, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSSYSTEMATICSRESULTSDISCUSSIONLITERATURE CITED |
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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: cladistics • Cretaceous • flowers • fossils • monocotyledons • paleobotany • Raritan Formation, New Jersey, USA • Triuridaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSRESULTSDISCUSSIONLITERATURE CITED |
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; 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 Rübsamen (1986)
, Maas (1988)
, Rübsamen-Weustenfeld (1991)
, and Martínez and Gómez (1994)
among others.
Miers (1852)
divided the family into two tribes, Sciaphileae 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 Martínez 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). Martínez and Ramos (1989)
, Márquez-Guzmán et al. (1989
, 1993)
, and Vázquez-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 Maas-van de Kamer and Maas, 1994
), even though both assignments warrant further study.
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 Rübsamen, 1986
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSRESULTSDISCUSSIONLITERATURE CITED |
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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 three-dimensional 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 wall-thickenings 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.
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SYSTEMATICS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSRESULTSDISCUSSIONLITERATURE CITED |
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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, 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. Médica (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 µm 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.
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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.
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 µm (Figs. 14–17). Receptacle flat and glabrous (Fig. 5), 0.4–0.88 mm in diameter. Female flowers and vegetative parts unknown.
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Holotype
L. H. Bailey Hortorium Paleobotanical Collection CUPC 1269. Figs. 20, 23, 24.
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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 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 one-layered 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 µm (Figs. 30–34). Receptacle elevated and glandular (Fig. 24), 0.46–1.05 mm in diameter. Female flowers and vegetative parts unknown.
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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.
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Type locality
Old Crossman Clay Pit, Sayreville, New Jersey, USA.
Stratigraphic position
South Amboy Fire Clay, Raritan Formation.
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 valvate 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 µm (Fig. 42). Pistillode triangular in cross section (0.2 mm x 0.18 mm x 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.
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RESULTS |
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, 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 Biología, Universidad Nacional Autónoma 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.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSRESULTSDISCUSSIONLITERATURE CITED |
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; Maas and Rübsamen, 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 Martínez and Ramos 1989
and Sciaphila rubra Maas 1979
; Maas, 1979
; Maas and Rübsamen, 1986
; Martínez and Ramos, 1989
), female and hermaphroditic flowers (Sciaphila picta Miers 1852
, and Sciaphila takakumensis Ohwi 1965
; Ohwi, 1938
, 1965
; Walker, 1976
; Gómez, 1982
; Maas, 1988
; Maas and Rübsamen, 1986
; Martínez and Gómez, 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 Rübsamen-Weustenfeld (1991)
observed that Triuris hyalina can be dioecious or hermaphroditic. In addition, Martínez (1994)
described specimens of the species Triuris brevistylis (T. hyalina of Maas and Rübsamen, 1986
) as hermaphroditic based on the study of numerous collections. One of us (M. A. Gandolfo) has examined the specimens studied by Martínez (1994)
and confirmed the presence of hermaphroditic flowers (MEXU, Martínez nros. 23995, 24511, 24522). If Lacandonia, invariably hermaphroditic (Martínez and Ramos, 1989
; Martínez, 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 Rübsamen, 1986
), and are subtended by bracts. In bud, they exhibit valvate aestivation, and the flowers are often stellate and patent at anthesis (Rübsamen-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 Rübsamen, 1986
). For the tribe Triurideae, 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 Rübsamen, 1986
; Maas-van de Kamer and Maas, 1994
; Martínez and Gómez, 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, Rübsamen-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 (Martínez 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
; Márquez-Guzmán et al., 1993
; Maas-van de Kamer 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 (Martínez 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 Rübsamen, 1986
; Maas-van de Kamer, 1995
). All fossil (Figs. 4, 8, 26, 28, 36, 38) and extant (Tomlinson, 1982
; Rübsamen-Weustenfeld, 1991
; Maas-van de Kamer, 1995
) Triuridaceae are extrorse with the exception of P. luteum and Lacandonia, both of which are introrse (Martínez and Ramos, 1989
; Márquez-Guzmán et al., 1993
; Maas-van de Kamer, 1995
). All Triuridaceae, extant and fossil, have endothecial cells with U-shaped wall thickenings (Rübsamen-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 one-colpoid, with exine that is psilate, finely reticulate, finely to coarsely granulose, or verrucose (Rübsamen-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 µm, with psilate or granular to finely verrucose exine (Wirz, 1910
; Erdtman, 1952
; Rübsamen-Weustenfeld, 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 (Rübsamen-Weustenfeld, 1991
), whereas Hyalisma pollen grains are quite different in having echinate exine sometimes with gemmae (Rübsamen-Weustenfeld, 1991
). Within the Triurideae, the pollen grains of Triuris and Peltophyllum are smaller than those of Sciaphileae (between 15 and 25 µm), spherical to elliptical, and inaperturate, with finely granular to granular, microverrucate or finely reticulate exine (van de Meerendonk, 1984
; Rübsamen-Weustenfeld, 1991
). There is no published information on the morphology of the pollen grains of Triuridopsis or Lacandonia, although E. Martínez (Instituto de Biología, Universidad Nacional Autónoma de México, 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 µm 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 µm in diameter in equatorial view), while M. archaia has the smallest (7 µm 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 six-merous, with tepals basally fused and lacking stomata. The 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.
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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 Rübsamen, 1986
).
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 Rübsamen, 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.
Even though we lack vegetative material representative of the fossil taxa, the principle of parsimony and the fact that in our analysis the fossil taxon is nested within a completely saprophytic Triuridaceae strongly support the interpretation that the extinct plants were also saprophytic. If so, these are the earliest known angiosperms with the saprophytic habit. Based on our cladistic analysis of all genera of the Triuridaceae, the fossil genera Mabelia and Nuhliantha are best placed within the tribe Triurideae, although Mabelia connatifila, M. archaia, and Nuhliantha nyanzaiana share characters with members of both tribes.
The discovery of these taxa is consistent with the previous hypothesis that the climate prevailing during the Upper Cretaceous in New Jersey was tropical to subtropical.
