A diverse assemblage of Anacardiaceae from Oligocene sediments, Tepexi de Rodriguez, Puebla, Mexico

American Journal of Botany 89(3): 535–545. 2002.

A DIVERSE ASSEMBLAGE OF ANACARDIACEAE FROM OLIGOCENE SEDIMENTS, TEPEXI DE RODRIGUEZ, PUEBLA, MEXICO1 JOSE´ L. RAMI´REZ2

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SERGIO R. S. CEVALLOS-FERRIZ3

Facultad de Ciencias, Departamento de Biologı´a, Universidad Nacional Auto´noma de Me´xico, Ciudad Universitaria, Circuito Exterior, Del. Coyoacan, 04510 Me´xico D.F., and 3 Departamento de Paleontologı´a, Instituto de Geologı´a, Universidad Nacional Auto´noma de Me´xico, Ciudad Universitaria, Circuito de la Investigacio´n Cientı´fica, Del. Coyoacan, 04510 Me´xico D.F. 2

Among the plants collected from the Pie de Vaca Formation of the Oligocene, of Tepexi de Rodrı´guez, Puebla, Me´xico are five plants of Anacardiaceae, Haplorhus medranoensis, Rhus toxicodendron, Rhus sp., Comocladia intermedia, and Pistacia marquezii represented by their leaves and/or leaflets. The past and present diversity and geographic distribution of one of these genera, Rhus, demonstrate its capability to adapt and diversify in a wide variety of environments. Leaf architecture characters of this taxon overlap with those of other genera in the family, suggesting a high degree of phenotypic plasticity. The presence in the Pie de Vaca Formation of a type of Pistacia with leaf architecture characters similar to those of Asian plants further supports a long history of exchange between low-latitude North America and Asia. Links between low-latitude North and South America and the Caribbean are suggested by the presence of Comocladia and Haplorhus. Whereas Comocladia highlights the long history of regional endemics in the area, Haplorhus, today an endemic monotypic genus of Peru, suggests exchange mechanisms between North and South America. The morphologic characters of these taxa, and those of Pseudosmodingium (Anacardiaceae), some Rosaceae, Leguminosae, and Berberidaceae, suggest that the Pie de Vaca community was established and evolved in harsh environmental conditions. The Pie de Vaca flora thus provides significant new insights into the biogeographic relationships of the low latitude vegetation of North America. Key words:

Anacardiaceae; Oligocene; Pie de Vaca Formation; Puebla, Mexico.

The family Anacardiaceae, an important component of the deciduous and evergreen tropical forest, has a pantropical distribution, with some species found in temperate regions (Cronquist, 1981). Although the family has an important fossil record of wood, fruits, leaves, and pollen (e.g., Cevallos-Ferriz and Barajas-Morales, 1992; Collinson, Boulter, and Holmes, 1993; Taylor, 1993; Wolfe, 1964), its taxonomic, evolutionary, and biogeographic relationships have been rarely discussed. Mexico and some areas of South America (e.g., the Chaco region of Argentina), are postulated as important centers of diversification due to their high diversity and high level of endemism (T. Terrazas-Salgado, Colegio de Posgraduados, personal communication). Fossil remains of anacardiaceous plants collected in Mexico (present study) and Oregon (Manchester, 1977) may help to evaluate such hypotheses. For example, two species of the genus Tapirira grow naturally in Chiapas and Oaxaca, Mexico, and extend south to Belize, Costa Rica, Panama, Colombia, Venezuela, Guyana, Ecuador, Peru, and Brazil (Terrazas and Wendt, 1995). This distribution might be interpreted to indicate that South America is the center of diversification of Tapirira with a later arrival to Mexico. However, the Tertiary fossil record of Tapirira suggests the opposite: a northern origin with a

later movement towards the south. This conclusion is based on the presence of wood in the Eocene Clarno Formation (Oregon, USA; Manchester, 1977) and in the Oligocene and Oligocene-Miocene San Gregorio and El Cien Formations (Baja California and Baja California Sur, Mexico; CevallosFerriz and Barajas-Morales, 1992), as well as on Miocene flowers from Chiapas, Mexico (Miranda, 1963). Another genus, Pseudosmodingium, illustrates the long history of endemic plants in low-latitude North America, suggesting a different biogeographic history from that of Tapirira. Although a relatively old (Oligocene) fossil record is recognized for Pseudosmodingium, only two fossil species, P. miranda Ramı´rez and Cevallos-Ferriz and P. terazasii Ramı´rez and Cevallos-Ferriz (Ramı´rez, Cevallos-Ferriz, and Silva, 2000) and four extant species (Barkley and Merton, 1940) have been recognized. All these taxa are distributed today in the southern and northern central part of Mexico, further suggesting their long and geographically restricted history. That Mexico has been an important area for the evolution and radiation of taxa in Anacardiaceae is further suggested by the presence of two extant endemic monotypic genera, Achtinochaetia and Bonetiella, which are restricted to two relatively small areas. The evolutionary relationships of these two genera with other taxa in the family remain unclear. In the Oligocene Los Ahuehuetes locality of Puebla, Me´xico (Magallo´n-Puebla and Cevallos-Ferriz, 1993, 1994a, b, c; Velasco de Leo´n and Cevallos-Ferriz, 1997), an assemblage of leaves and leaflets with asymmetric laminae, pinnate craspedodromous venation, freely ending secondary veins near the margin, a tendency to the thinning of the tertiary veins, and imperfect development of the areoles has been identified to the Anacardiaceae. These fossils demonstrate that the Anacardiaceae was diverse in low-latitude North America by the Oligocene. The establishment, diversification, and biogeographic

1 Manuscript submitted 2 November 2000; manuscript accepted 23 August 2001. The authors thank CONACyT-Mexico (1005P) and DGAPA-UNAM (IN208500) for financial support to SRSCF and a student grant to JLR. Comments and suggestions on a previous manuscript by J. A. Wolfe, University of Arizona, Tucson, S.R. Manchester, University of Florida, Gainesville, K. Pigg, Arizona State University, Tempe, and T. Terrazas-Salgado, Colegio de Posgraduados, Mexico, helped to improve it. Photographic assistance by Antonio Altamira and Hector Herna´ndez are appreciated, as well as the facilities received by the personnel of the National Herbarium (MEXU).

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ing diagnoses and descriptions it is assumed that the fossil material has an organization similar to the extant material to which it is related. Since within the family Anacardiaceae, simple leaves are considered rare and compound leaves are the dominant form, most of the fossil material is described as leaflets; however, since there is always some uncertainty, the term lamina is used here indiscriminately to refer to a leaflet or simple leaf.

SYSTEMATIC DESCRIPTION Class—Magnoliopsida Order—Sapindales Family—Anacardiaceae Fig. 1.

Map of the Los Ahuehutes locality in central Mexico.

patterns of five new fossil taxa and the two Pseudosmodingium species previously described from the area (Ramı´rez, CevallosFerriz, and Silva, 2000) are discussed in relation to extant taxa, broadening the historical understanding of the family in lowlatitude North America. MATERIALS AND METHODS The fossil plants were collected from a continental sedimentary deposit known as the Los Ahuehuetes locality, which has been interpreted as belonging to the lowermost member of the Pie de Vaca Formation (J. Pantoja-Alor, Universidad Nacional Auto´noma de Me´xico, personal communication). The Los Ahuehuetes locality is 4.5 km north-northwest of the town of Tepexi de Rodrı´guez, in the southern part of the state of Puebla, Mexico, at 188359150 N, 978559300 W (Fig. 1). The sedimentary sequence is formed by horizons of volcanic ash, shale, and fine-grained sandstone, representing a lacustrine, or low-energy fluvial environment, where fossil plants are preserved as impressions and carbonized compressions. The stratigraphic relationship of the Pie de Vaca Formation with an underlying sequence indicates that its maximum age is Oligocene (J. Pantoja-Alor, Universidad Nacional Auto´noma de Me´xico, personal communication). The results of a recently undertaken palynological analysis of the Los Ahuehuetes deposit indicate an Eocene to Oligocene age for the sequence (Martı´nez-Herna´ndez and Ramı´rez-Arriaga, 1996). Considering the stratigraphic and palynological data, an Oligocene age for the Los Ahuehuetes deposit is suggested. However, the age still needs to be confirmed by radiometric dating. In collaboration with Gilberto Silva (Facultad de Ingenierı´a, Universidad Nacional Auto´noma de Me´xico), four samples of volcanic material, two of them directly associated with the fossil plants, are being prepared for fission track and/or whole rock dating. The fossil plants are represented by detached and often fragmentary organs, mainly of angiosperms (Magallo´n-Puebla and Cevallos-Ferriz, 1994a, b, c). Remains of fern fronds are rare, and an earthstar fungus has been also reported from the locality (Magallo´n-Puebla and Cevallos-Ferriz, 1993). Morphological observations of the fossil leaves were made with an Olympus SZH stereoscopic microscope and camera lucida. Terminology used to described the foliar characteristics is based on Hickey (1973). The leaves were identified through consultation of the literature, observation of specimens from herbarium collections, and direct observation of extant populations in the field. When similarity with a particular taxon was noted, this and closely allied plants were surveyed. The collection of the National Herbarium of Mexico, Mexico City, Mexico (MEXU) was especially useful at this stage. The clearing, staining, and mounting techniques of leaves of extant plants, modified by Payne (1969), were very important to the comparison of extant venation patterns with the fossil material. All the fossil material used in this study is deposited in the Paleobotanical Section of the Paleontological Collection of the Instituto de Geologı´a, Universidad Nacional Auto´noma de Me´xico, Mexico City, Mexico. In the follow-

Genus—Haplorhus Engler Species—Haplorhus medranoensis n.sp. Ramı´rez and Cevallos-Ferriz Holotype—Paleobotanical Section of the Paleontological Collection of the Instituto de Geologı´a, Universidad Nacional Auto´noma de Me´xico, catalog number IGM-PB 1078 (Figs. 2–3). Locality—Los Ahuehuetes locality, Pie de Vaca Formation, southern bank of the Axamilpa River, northwest of Tepexi de Rodrı´guez, Puebla, Mexico, at 188359150 N, 978559300 W. Age—Oligocene. Etymology—The specific epithet honors M.Sc. Francisco Gonza´lez Medrano, a friend, teacher, and excellent colleague, whose work and words have guided many generations of Mexican botanists. Diagnosis—Narrow leaf with narrow elliptic laminae, widest portion in the upper one-third, 81 mm in length by 9 mm in width, length/width radio of 9 : 1, entire margin, decurrent base (48), acute apex (258); venation simple craspedodromous; midvein stout, slightly curved; 27 pairs of straight secondary veins with insertion angle to the midvein (IAMV) 398 (338– 578), dichotomizing close to the margin to produce short, straight, marginal tertiary veins; some secondary veins divide before reaching midway to the margin; higher-order veins free near the margin, short and without ramification in intercostal zone; some tertiary veins directed admedially. Discussion—The leaves of Haplorhus medranoensis are most similar to those of Bonetiella anomala Rzedowski (Fig. 16) and Haplorhus peruviana Engler (Fig. 18). They share entire margins, pinnate secondary venation that tends to be cladodromous (end freely near the margin), acute intersection of the secondary veins with the midvein, free higher-order veins in the intercostal area that do not form areoles, and a slender lamina (length/width ratio .4.0 : 1). However, the density of secondary veins and the orientation of the tertiary veins in H. peruviana and B. anomala differ from each other. Haplorhus has more and regularly spaced secondary veins and tertiary veins with admedial direction (see Fig. 19), as described for the fossil material. In contrast, tertiary veins in Bonetiella follow a parallel trajectory with respect to the midvein (Fig. 17).

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Figs. 2–9. Leaf of Haplorhus (Figs. 2–3) and leaflets of Rhus toxicodendroides (Figs. 4–6), Rhus sp. (Figs. 7–8), and Comocladia intermedia (Fig. 9). 2. Leaf with elliptic shape, entire margin (arrow), decurrent base, and primary and secondary craspedodromous venation. Bar 5 10 mm. IGM-PB 1078. 3. Terminal zone of the secondary veins and tertiary veins with exmedial orientation (arrow) in intercostal areas. Bar 5 1 mm. IGM-PB 1078. 4. Almost sessile leaf with acute apex, lobed margin (upper arrow), pinnate primary, and craspedodromous secondary venation (lower arrow). Bar 5 5 mm. IGM-PB 1079. 5. A vein derived from a secondary vein reaches the lobule apex (arrow). Bar 5 1 mm. IGM-PB 1079. 6. Fourth-order veins with orthogonal disposition (arrows). Bar 5 4 mm. IGM-PB 1079. 7. Fragmentary leaflet with concave-concave teeth (arrow) and well-marked midvein. Bar 5 2 mm. IGM-PB 1080. 8. Tertiary vein (arrow) with percurrent trajectory. Bar 5 1 mm. IGM-PB 1080. 9. Lamina with serrate margin composed of small teeth (upper arrow), acute asymmetric base (lower arrow), pinnate primary and craspedodromous secondary venation. Bar 5 5 mm. IGM-PB 1081.

Genus—Rhus (Tourn.) Miller Species—Rhus toxicodendroides n.sp. Ramı´rez and Cevallos-Ferriz Holotype—Paleobotanical Section of the Paleontological Collection of the Instituto de Geologı´a, Universidad Nacional

Auto´noma de Me´xico, catalog number IGM-PB 1079 (Figs. 4–6). Locality—Los Ahuehuetes locality, Pie de Vaca Formation, southern bank of the Axamilpa River, northwest of Tepexi de Rodrı´guez, Puebla, Mexico, at 188359150 N, 978559300 W.

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Figs. 10–17. Laminae of Comocladia intermedia (Fig. 10) and Pistacia marquezii (Figs. 11–15) and leaf of Bonetiella anomala (Figs. 16–17). 10. Primary and secondary veins forming almost right angles (medial arrow); secondary veins dividing close to the margin, one branch reaching a tooth; short, oblique, and little ramified tertiary veins; and long intersecondary veins (upper and lower arrows). Bar 5 5 mm. IGM-PB 1081. 11. Elliptic leaflet with entire margin (upper arrow), decurrent base (lower arrow), and pinnate primary venation. Bar 5 2 mm. IGM-PB 1082. 12. Lanceolate leaflet with widened acute base on one side, attenuated apex (upper arrow), peciolule (lower arrow), and some intersecondary veins. Bar 5 5 mm. IGM PB 1083. 13. Secondary veins that tend to be craspedodromous toward the apex (upper arrow) and cladodromous toward the base. The lower arrow in the intercostal area signals ramification of high-order veins. The areoles are incomplete. Bar 5 1 mm. IGM-PB 1083. 14. Elliptic leaflet with decurrent base and acute apex (arrow). Bar 5 3 mm. IGM-PB 1084. 15. Leaflet with thick ramifications (arrows) where veins have a tendency to become cladodromous. Bar 5 1 mm. IGM-PB 1084. 16. Leaf with entire margin (upper arow), decurrent base, craspedodromous venation (lower arrow), and little ramified secondary veins. Bar 5 2 mm. 17. Close-up displaying scarce ramification of secondary and high order veins (upper arrow). The basal arrow signal in the intercostal area tertiary veins with parallel orientation with respect to the midvein. Bar 5 0.5 mm.

Age—Oligocene. Etymology—The specific epithet refers to the leaf architecture character similarity between the fossil and the extant Rhus toxicodendron.

Diagnosis—Very asymmetric leaflet with ovate lamina; one side of the lamina convex with a pronounced curve, the other side slightly concave; 25 mm in length by 15 mm in width, length/width radio of 1.6 : 1; lobulate margin; obtuse asymmetric base (1158); apex acute (588), petiolule missing; teeth

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Figs. 18–25. Leaf of Haplorhus peruviana (Figs. 18–19) and leaflets of Rhus toxicodendron (Figs. 20–21), R. glabra (Fig. 22), Actinocheitia potentillaefolia (Fig. 23), R. sylvestris (Fig. 24), and Comocladia glabra (Fig. 25). 18. Linear leaf with attenuated apex, decurrent base, and entire margin. Bar 5 10 mm. 19. Note acute angle formed by the secondary veins when departing from the midvein (lower arrow), the distal zone of secondary veins showing dicotomies, and the exmedial trajectory of the tertiary veins (medial and upper arrows). Bar 5 1 mm. 20. Fragment with entire margin, secondary venation tending to be eucamptodromous, and ramified high-order veins tending to an orthogonal pattern (arrows). Bar 5 2 mm. 21. Fragment with lobed margin, in which a secondary vein enters a tooth (upper arrow) and with ramified and joined tertiary veins (lower arrow) in intercostal area. Bar 5 5 mm. 22. Note the secondary veins enter teeth (medial arrow), the thinning of tertiary veins in intercostal areas (upper arrow), and the incomplete areols (lower arrow). Bar 5 5 mm. 23. Note the typical rounded marginal teeth, the ramification in the teeth of secondary veins (upper arrow), the ramified and scarcely fused tertiary veins in intercostal areas (lower arrow), and the short fourth-order veins with constant angles with respect to the tertiary veins. Bar 5 2 mm. 24. Entire margin, pinnate primary venation, craspedodromous secondary venation, ramified free tertiary veins in intercostal areas (arrows) and short fourth-order veins with constant angles with respect to the tertiary veins. Bar 5 5 mm. 25. Note secondary craspedodromous veins ending as prominent spiny teeth, fused ramified tertiary veins, little ramified quaternary veins (upper arrow), and thick intersecondary veins that may fuse with the tertiary veins (lower arrow). Bar 5 6 mm.

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with broad base, convex-convex; venation stout, simple craspedodromous; midvein straight, ten pairs of slightly curved secondary veins dichotomizing close to the margin ending in a tooth or occasionally in a sinus, with IAMV 678 (608–728), intercostal tertiary veins ramified, some fusing to produce a reticulate pattern; high-order intercostal veins forming a reticulum, but areoles absent. Discussion—Based on extant and fossil plants the foliar morphology of Rhus has the highest variability of any genus in the family. Although the leaves of most species are pinnately compound and some have a ternate arrangement, variability is easily observed in the shape and type of base of the leaflets and size and spacing of the teeth and is also obvious in the diversity of venation patterns. Nevertheless, within the family the presence of aserrate margin and the variable behavior of the secondary veins, among other characters, are good indicators of a Rhus pattern (Wolfe and Wehr, 1987). This variability is observed in the material from the Los Ahuehuetes locality, where two different species of Rhus are recognized and a third type of leaflet has some characters that suggest a relationship with this genus. Rhus toxicodendroides with leaflets of ovate shape, lobulate margin and short petiolule (Fig. 4) has the greatest similarity with R. toxicodendron (Figs. 20, 21). They share an obtuse base, about seven pairs of slightly curved secondary veins, some secondary veins ending in the apex of a tooth, intersecondary veins with different grades of development, little ramified tertiary intercostal veins with acute angles pointing towards the margin, and higher order veins forming a random reticulate pattern. Differences between the leaflets of these two taxa are found in the shape of the apex and the size of the lobules, which are smaller in the fossil. Furthermore, the development of the higher-order vein reticulum seems to include higher-order veins in the extant plant; however, this variability may be due to the fossilization process rather than an actual architectural difference. Species—Rhus sp. Sample—Paleobotanical Section of the Paleontological Collection of the Instituto de Geologı´a, Universidad Nacional Auto´noma de Me´xico, catalog number IGM-PB 1080 (Figs. 7– 8). Locality—Los Ahuehuetes locality, Pie de Vaca Formation, southern bank of the Axamilpa River, northwest of Tepexi de Rodrı´guez, Puebla, Mexico, at 188359150 N, 978559300 W. Age—Oligocene. Description—The incomplete apical portion of lamina is 11 mm long by 11 mm wide, with a dentate margin. The marginal teeth are simple and have a convex-convex shape. Venation is pinnate simple craspedodromous, with a thin and slightly curved midvein, and secondary veins that are slightly curved toward the margin, end in a tooth, with IAMV of 528 (478– 618). The intercostal tertiary veins may fuse and become percurrent. Discussion—This sample has several morphological characteristics that resemble the Pseudosmodingium described from the same locality (Ramı´rez, Cevallos-Ferriz, and Silva,

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2000). Among these are the tooth shape and the trajectory of the secondary veins that enter the teeth. However, there is a distinctive character shared by the fossil specimen and Rhus that corresponds with the trajectory of the tertiary veins. In the fossil specimen and some extant species of the genus such as R. glabra some adjacent tertiary veins fuse and become percurrent (Fig. 8). In contrast, the tertiary veins neither ramify nor fuse, as they are free in the intercostal areas of Pseudosmodingium. Another characteristic shared by the fossil and R. glabra is the tooth shape (Fig. 22). The descriptions of fossil Rhus in the paleontological literature commonly lack details on the high-order veins. This may be explained due to the fact that these veins are less stout and have smaller diameters than the preserved veins, as we inferred from observation on extant material. Genus—Comocladia Loes. Species—Comocladia intermedia n.sp. Ramı´rez and Cevallos-Ferriz Holotype—Paleobotanical Section of the Paleontological Collection of the Instituto de Geologı´a, Universidad Nacional Auto´noma de Me´xico, catalog number IGM-PB 1081 (Figs. 9–10). Locality—Los Ahuehuetes locality, Pie de Vaca Formation, southern bank of the Axamilpa River, northwest of Tepexi de Rodrı´guez, Puebla, Mexico, at 188359150 N, 978559300 W. Age—Oligocene. Etymology—The specific epithet refers to the fact that some leaf architectural characters of the fossil are found in several genera including Rhus, Comocladia, and Achtinochaetia. Diagnosis—Elliptic shaped laminae; up to at least 45 mm long by 17 mm wide, rounded to an acute (608) slightly asymmetric base, large well-developed petiolule (7 mm), margin serrate, regularly spaced simple teeth, of convex-convex type; venation pinnate simple craspedodromous; midvein stout and straight; 19 pairs of regularly spaced straight or slightly curved near the margin secondary veins, with IAMV 848 (788–94), some dichotomizing close to the margin to produce short, straight, marginal tertiary veins; intercostal veins very short, little ramified, and curved. Discussion—Although this third type of leaflet has characteristics that resemble those of Rhus, its secondary veins depart from the midvein at almost a right angle. This is a rare character in Anacardiaceae that may be found in species of Comocladia and Achtinochaetia (Fig. 23). Among the extant species of Rhus, the fossil resembles Rhus silvestris (Fig. 24) in the angle of divergence of the secondary veins from the midvein, the pattern of high-order venation, the poorly ramified tertiaries, and a semi-alternate pattern of secondary veins with some areas where secondaries are opposite (Fig. 24). However, these species differ in that the fossil has serrate margin with small regularly spaced teeth, while in R. silvestris there are small emergences hardly distinguishable as teeth. In the fossil the trajectory of the secondary veins is straight, while in the extant form most secondary veins are slightly curved. The fossil material also has more intersecondary veins

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compared with R. silvestris, and the angle of divergence of the tertiary veins with respect to the midvein is more variable in the fossil than in the leaflets of the extant plants. Although the divergence angle of the secondary veins in the fossil plant are similar to those of the Mexican monotypic and endemic genus Achtinochaetia, the leaflets of this extant plant have a regularly spaced lobulate margin (Fig. 23) absent in all other genera in the family, while the fossil material has small regularly spaced teeth. Comocladia is other extant genus with which the fossil material share characters. Although the angle of divergence of the secondary veins is slightly more acute in the extant material compared with the fossil leaflets, they share the general architectural pattern of the tertiary veins, especially the scarce ramification of the intercostal tertiary veins. Among the extant species of Comocladia, those of continental Mexico are more similar to the fossil material. The species from the Caribbean region have large spiny teeth on the margin of the leaflets (e.g., C. eckmaniana; Fig. 25), (similar leaf morphotype is known from the Republic Flora; J. A. Wolfe, Arizona University, personal communication). In contrast, in the Mexican species the margin is smooth or has very small emergences (e.g., C. glabra, C. mollisima; Figs. 26–27). An important character present in C. eckmaniana and absent in C. glabra and the fossil material is that some tertiary veins fuse, including those derived from secondary or intersecondary veins (Fig. 25). Among the continental Comocladia species (Figs. 28–30), C. mollisima is most similar to C. intermedia; however, the tertiary veins of the leaves of the extant plant change their original trajectory to exhibit an orthogonal pattern. As is clear in Fig. 28, the tertiary veins in C. mollisima tend to be subparallel to the secondary veins for a short distance and then curve toward the intercostal area, where they follow a straight pattern. In contrast, the tertiary veins in C. intermedia originate and follow a straight pattern directly from the secondary veins into the intercostal area (Fig. 10). Genus—Pistacia L. Species—Pistacia marquezii n.sp. Ramı´rez and CevallosFerriz Holotype—Paleobotanical Section of the Paleontological Collection of the Instituto de Geologı´a, Universidad Nacional Auto´noma de Me´xico, catalog number IGM-PB 1082 (Figs. 11–15). Locality—Los Ahuehuetes locality, Pie de Vaca Formation, southern bank of the Axamilpa River, northwest of Tepexi de Rodrı´guez, Puebla, Mexico, at 188359150 N, 978559300 W. Age—Oligocene. Etymology—The specific epithet is for Dr. Judith Ma´rquez Guzma´n who has helped to develop anatomical, morphological, and embryological studies in Mexico and who has been an active promoter of paleobotanical studies in the Science Faculty Universidad Nacional Auto´noma de Me´xico. Diagnosis—Asymmetric, lanceolate leaflets, with expansion in one side near the midportion of lamina, some laminae slightly curved in their general shape, 1.6–4.0 mm long by 4.0–8.0 mm wide, length/width radio of 2.8–5.0 : 1, margin

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entire, base decurrent (14–448), apex acute (148–408), lacking petiolule; pinnate stout slightly curved simple craspedodromous venation; 7–12 pairs of curved secondary veins, with IAMV 628 (358–778), some dichotomizing at about one-third of the distance to the margin; tertiary veins thin, ramified, and fused forming a reticulum; fourth-order veins of similar diameter as third order, their last ramification, close to the margin, slightly curved, areoles of the imperfect type. Discussion—The leaflets have characters shared with Sapindus (Sapindaceae, a family close to Anacardiaceae) such as a lanceolate lamina, entire margin, and attenuate apex. However, the venation pattern of some fossils from the Los Ahuehuetes locality identified as Sapindus are clearly different from those of the anacardiaceous leaflets under discussion. Although there are some Rhus species whose leaflets have an entire margin (e.g., R. virens Lindh.), their laminar shape, apex, and length/width ratio are different from the fossil material. The most similar leaflets among extant anacardiaceous plants are those of Pistacia. In Mexico, two species of Pistacia grow naturally, P. texana Swingle and P. mexicana Swingle; however, the leaflets of these plants have little similarity with the fossil ones. Pistacia texana has serrate margin with short teeth, and in contrast, the fossil material has an entire margin. Although P. mexicana also have an entire margin, the length/ width ratio of its leaflets is different from that of the fossil material. Furthermore, a high percentage of the tertiary veins in P. mexicana have an exmedial trajectory (Fig. 32), a characteristic that is absent in the fossil leaflets. Among the leaves of other extant species of Pistacia, those of P. chinensis Bunge (Fig. 33) from occidental Asia (including the occidental Himalayan region) have great morphological similarity to P. marquezii. The most important similarities are lanceolate shape, acute base, marked asymmetry in the base of the leaflet, entire margin, attenuate apex (very rare in extant and fossil species), and a tendency to have cladodromous venation recognized by the slight ramification of the secondary veins at two-thirds of their length. In both species, the higher-order veins form a random reticulum that is best developed in P. marquezii. Despite all these similarities, in P. chinensis the secondary veins form arcs that fuse with adjacent veins, a pattern that has not been observed in P. marquezii (Fig. 34). Weyland (1941) found that Pistacia rottensis from the Oligocene of Germany has many similarities with the extant species P. chinensis, P. philippinensis M. & R., and P. khinjuk Stocks. These three and other extant taxa have been combined in a single species, P. chinensis, with a large geographic distribution and morphological variability. The large variability observed in the material of P. marquezii is comparable to that documented for P. rottensis, as would be expected from the new definition of the occidental Asiatic plants. DISCUSSION Biogeographic relationships—Previous work on the plants of the Los Ahuehuetes locality has demonstrated that by the time this fossiliferous outcrop was deposited, low-latitude North America shared a group of plants with the vegetation of high-latitude North America, including Eucommia (Eucommiaceae), Cedrelospermum (Ulmaceae), Karwinskia (Rhamnaceae), Cercocarpus (Rosaceae), and Mimosoideae (Magallo´n-Puebla and Cevallos-Ferriz, 1994a, b, c; Velasco de Leo´n

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Figs. 26–36. Leaflets of Comocladia ekmaniana (Fig. 26), C. mollisima (Figs. 27–28), C. engleriana (Fig. 26), C. palmeri (Fig. 30), Pistacia mexicana (Figs. 31–32), P. chinensis (Figs. 33–34), and incertae sedis samples (Figs 35–36). 26. Close-up of a lateral portion of a leaflet of Comocladia ekmaniana. Secondary veins are craspedodromous and slightly curved near the margin. Tertiary veins are oblique respect the midvein and ramify into short quaternary veins (arrow). The margin has some emergences that do not develop into teeth. Bar 5 2 mm. 27. Leaflet with subrounded apex, rounded base, wide teeth with wide apex, secondary craspedodromous veins ending in the tooth after ramifying near the margin. Bar 5 10 mm. Figs. 28–30. Close-ups of the midvein in C. mollisima, C. engleriana, and C. palmeri, respectively. Arrows show the point where secondary veins depart toward the margin. Note how they change trajectory forming first an acute angle and later an obtuse one. Bars 5 0.5 mm. 31. Subsessile leaflet with elliptic shape and acute base and apex. Venation tends to be

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and Cevallos-Ferriz, 1997; Velasco de Leo´n, Cevallos-Ferriz, and Silva, 1998). Among the Anacardiaceae, we know that Rhus was also present in both high- and low-latitude North America, further suggesting a continuity of the Tertiary flora on the continent. Eucommia, Cedrelospermum, some legumes and especially Statzia are examples of plants that were also shared with other regions of the world, such as Europe and Asia (Magallo´nPuebla and Cevallos-Ferriz, 1994a, b, c). Among the anacardiaceous plants from the Los Ahuehuetes, Pistacia marquezii has many similarities with species from Europe (Weyland, 1941) and Asia. The discovery of these fossil elements in the Los Ahuehuetes locality and their wider geographical distribution document the influence in the development of low-latitude North American and possibly South American vegetation of these floral elements. Besides the plants shared with other geographic regions, it is now known that some extant endemics of Mexico have a long history. Lysiloma, Sophora (Leguminosae), and some species of Karwinskia (Rhamnaceae) are good examples (Magallo´n-Puebla and Cevallos-Ferriz, 1994b; Velasco de Leo´n and Cevallos-Ferriz, 1997). Among the anacardiaceous plants, Pseudosmodingium and some species of Comocladia can be included in this category of extant Mexican endemics with a long history (Ramı´rez, Cevallos-Ferriz, and Silva, 2000). Although Comocladia can be found in the Antilles, the species of continental Mexico are more similar to the fossil. The presence of these plants suggests that although Tertiary low-latitude vegetation of North America was greatly influenced by high-latitude elements, it had some endemic plants that gave it its own unique characteristics. Other important plants being documented from the Los Ahuehuetes locality and other Mexican areas are those related to plants from South America. As with the case of fossil Tapirira in Mexico (Terrazas and Wendt, 1995), additional anacardiaceous taxa documented from the Los Ahuehuetes locality provide new information about the familys past distribution, allow for a greater understanding of the environmental parameters where they grew and additional insights about their diversification. For example, although the evolutionary relationships of the extant monotypic genus Haplorhus still have to be documented, its presence in the Los Ahuehuetes locality gives some hints about how this plant attained its extant distribution. More fossil records are needed to further substantiate the claim that Haplorhus originated in North America and ‘‘moved’’ later to South America, but its known past distribution pattern strongly suggests that this may be the case. The southern trend on time in the geographic distribution of Tapirira may be compared with that of Haplorhus, and both raise questions on the timing and nature of the floristic exchange between North and South America. Some examples from the Los Ahuehuetes locality, such as Prosopis, Mimosa, Berberis, and Karwinskia are known to extend their extant geographic distribution to South America.

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This current pattern and distribution somewhat resemble that of Larrea, an important component of Quaternary vegetation in xeric mid-latitudes of North America that is also present in South America. However Larrea is thought to have arrived in Mexico via South and Central America. This type of relationship between the arid regions of North and South America suggests that they are of relatively recent development. However, the proposal has some problems. Perhaps one of the most important problems is that by the Pleistocene, some extant geographic barriers in both North and South America were well established, and if the plants followed this route from South to North they had to face serious natural obstacles. Long-distance dispersal could explain the distribution of Larrea, but this seems unlikely, as a similar pattern of geographic distribution is also observed in many other taxa that would need to have similar ecological requirements. Furthermore, unpublished data of V. Page shows Larrea to have been present prior to the Pleistocene, in the Miocene of southern California (J. A. Wolfe, Arizona University, personal communication). Thus, the uncertainties of the historical biogeography of Larrea parallels that of many others; however, comparison of both its fossil and extant record can be used to further sustain the distribution history emerging from the analysis of Anacardiaceae. In contrast to this hypothesis, some extant plants have been used to emphasize a long history of the floristic exchange between some areas of North and South America. These include Condalia, Fagonia, Hoffmanseggia, Lycium, Menodora, Nicotiana, Zizyphus, and several lineages of Cactaceae (Rzendowski, 1991). Most probably the geographic distributions of the plants under discussion were wider in the past, and the development of the extant physiographic characters of North Central and South America were important in restricting their areas of distribution. In recent years, geologists have documented the break-up of the Pacific plate into the Izanagi, Pacific, Kula, and Farallon plates (e.g., Woods and Davis, 1982; Engebretson, Cox, and Gordon, 1985; Guerrero-Garcı´a and Herrero-Bervera, 1997). Isotopic ages of crystalline rocks along the Pacific coast of Mexico indicate a systematic decrease in Rb/Sr mineral ages from 80 million years (my) in Jalisco to 11 my in Oaxaca. This signal is apparently related to the migration of the Chortis Block (Honduras and Nicaragua) that was detached from Mexico and transported by the Farallon plate toward the southeast (Guerrero-Garcı´a and Herrero-Bervera, 1993, 1997). If further work continues to document this movement of the Chortis Block, at least part of the biogeographic problems raised by the plants under discussion could be solved. The Chortis Block may have been used by plants expanding their geographic distribution from continental Mexico during the Tertiary, avoiding many of the natural barriers that they otherwise would have to overcome. While this alternative proposal may explain the presence of some of the taxa found in low-latitude North

← cladodromous. Bar 5 5 mm. 32. Close-up of lateral portion of a leaflet showing ramification of secondary veins near the margin (middle and lower arrows) and fusion of tertiary veins in intercostal areas (upper arrow). Bar 5 2 mm. 33. Lanceolate leaflet with one side widened, decurrent base, and attenuate apex. Secondary veins tends to be brochydodromous. Bar 5 5 mm. 34. Close-up showing the trajectory of the secondary veins (basal arrow), its division (middle arrow), and the fusion of tertiary veins in intercostal areas (upper vein). Bar 5 1 mm. 35. Size and angle variation (arrows) in teeth. Bar 5 5 mm. 36. Basal portion of a leaflet showing characteristics shared with C. intermedia such as the straight secondary veins and the orthogonal pattern of the tertiary veins; however, this leaflet has an entire margin and a wide lobule at the base, an atypical condition in Anacardiaceae. Bar 5 4 mm.

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America during the Tertiary that today have relatives in South America, it is far from solving the problem for taxa that moved in the opposite direction. Further work in low-latitude North American and in South American floras will help to understand the relationship of these Tertiary floras. The hypothetical explanation for the distribution of Haplorhus not only provides insights into understanding the distribution of the fossil plants discussed above but offers a plausible explanation for other extant plants lacking a fossil record. For example, a close relationship has been proposed for the families Anacardiaceae and Julianiaceae (sensu Cronquist, 1981). There are opinions suggesting that members of Julianiaceae may have evolved from an anacardiaceous taxon, perhaps Rhus, based on morphological and anatomical comparisons. The geographic distributions of Orthopterygium in Peru and Amphipterygium in Central America and southern Mexico have a pattern similar to that of Haplorhus. The similarity in their biogeographic patterns is suggestive of the antiquity and phylogenetic patterns of these two families. Furthermore, the Schinus plant described from the Miocene of Nevada (Wolfe, 1964) is now believed to represent a member of Juliana (Julianaceae; J. A. Wolfe, personal communication), adding an additional taxon that suggests an important north-to-south distribution trend for some extant Neotropical groups of plants. Synecological relationships—We do not have a clear idea on the type of paleocommunity represented by the Los Ahuehuetes locality. However, some environmental conditions may be inferred based on floristic composition (Magallo´n-Puebla and Cevallos-Ferriz, 1994a, b, c; Martı´nez-Herna´ndez and Ramı´rez-Arriaga, 1996; Velasco de Leo´n and Cevallos-Ferriz, 1997; Velasco de Leo´n, Cevallos-Ferriz, and Silva, 1998; Ramı´rez, Cevallos-Ferriz, and Silva, 2000). Some extant members of the taxa represented are components of the extant deciduous tropical forest (e.g., Pseudosmodingium, Mimosa, Lysiloma, Sophora), and others are more common in the chaparral today (e.g., Cercocaprus, Pistacia, Karwinskia, Berberis, Mahonia, Rhus), still others are typical of xeric areas (Prosopis, Cardiospermum, Sapindus, Ephedra, Vauquelinia, Haplorhus), and in contrast, a few suggest mesic conditions (Eucommia and Cedrelospermum). Although it may be argued that the plants in the Los Ahuehuetes locality represent more than a single community or that this paleocommunity has no modern counterpart, some geological features of the outcrop give clues about the particular environmental conditions under which this taphoflora may have developed. The presence of Pseudosmodingium has been discussed along with the pyroclastic material that compose the fossiliferous outcrop (Ramı´rez, Cevallos-Ferriz, and Silva, 2000), stressing that this genus may be a pioneer plant, an ecological strategy common in its extant relatives. Another pioneer plant found in the Los Ahuehuetes locality is Cedrelospermum, which has been described from several localities in which volcanism is a common factor (Manchester, 1987, 1989; Magallo´n-Puebla and Cevallos-Ferriz, 1994a). Other taxa for which a pioneer character may be assumed are some Rosaceae and Salicaceae, as suggested by their rapid establishment in strongly disturbed areas, such as the environs of the Santa Elena Volcano, as well as in several Tertiary localities in western North America (Myers, 1996). The association of plants in the Los Ahuehuetes locality may not represent a climax community but rather a successional stage that promoted the diversification of taxa like Le-

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guminosae and Anacardiaceae, due to the adverse conditions. The continuous volcanic disruption and high temperatures (suggested by the presence of important deposits of gypsum) may have selected for different reproductive and vegetative strategies. For example, the difficulty in explaining differences in the high-order venation patterns of the fossil material with respect to extant relatives is based upon a lack of understanding of the processes that alter their organizational grades. There is, however, an hypothesis that suggests that a regression to lower organizational levels may occur as plants enter more xeric environments (Hickey, 1972). Further research on this topic may help to reach a better understanding with respect to the evolution of these taxa and of the differences observed in the high-order venation patterns in Pistacia marquezii and Comocladia intermedia. Other fossil leaves or leaflets collected in the Los Ahuehuetes locality (Figs. 35–36) support the idea of an important and intense diversification process among the Anacardiaceae (Ramı´rez, 1999). These have not been included here because their identification is restricted to lower taxonomic levels because of poor preservation. Nevertheless, the observable morphological characters on their leaves or leaflets distinguish them from the plants described here (Ramı´rez, 1999). Further work in the area and other localities in low-latitude North America will help us to further explain the response of the plants to changing environmental conditions, generating a better understanding of the lineages that compose the extant vegetation of Mexico. LITERATURE CITED BARKLEY, F. A., AND J. R. MERTON. 1940. Pseudosmodingium and Mosquitoxylum. American Midland Naturalist 24: 666–679. CEVALLOS-FERRIZ, S. R. S., AND J. BARAJAS-MORALES. 1992. Fossil woods from the El Cien Formation in Baja California Sur, Mexico. American Journal of Botany 78: 26. COLLINSON, M., M. BOULTER, AND P. HOLMES. 1993. Magnoliophyta (Angiospermae). In M. J. Benton [ed.], The fossil record 2, 811–812. Chapman and Hall, London, England. CRONQUIST, A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York, New York, USA. ENGEBRETSON, D. C., A. COX, AND R. G. GORDON. 1985. Relative motions between oceanic and continental plates in the Pacific Basin. Geological Society of America Special Paper 206. GUERRERO-GARCI´A, J., and E. Herrero-Bervera. 1993. Timing of break-up and sense of motion along the Pacific margin of southwestern Mexico. First Circum Pacific and Circum Atlantic Terrane Conference Proceedings, 58–60. GUERRERO-GARCI´A, J., and E. Herrero-Bervera. 1997. The position of the Kula-Farallon ridge against North America during the Late Cretaceous. In J. D. Bradshaw and S. D. Weaver [eds.], International Conference on Terrane Geology. Conference abstracts, 77–78, Department of Geological Sciences, University of Canterbury, New Zealand. HICKEY, L. J. 1972. Stratigraphy and paleobotany of the Golden Valley formation (Early Tertiary) of western North Dakota. Geological Society of America Memoirs 52. HICKEY, L. J. 1973. Classification of the architecture of dicotyledoneous leaves. American Journal of Botany 60: 17–33. MAGALLO´N-PUEBLA, S., AND S. R. S. CEVALLOS-FERRIZ. 1993. A fossil earthstar (Geasteraceae; Gasteromycetes) from the Late Cenozoic of Puebla, Me´xico. American Journal of Botany 80: 1162–1167. MAGALLO´N-PUEBLA, S., AND S. R. S. CEVALLOS-FERRIZ. 1994a. Latest occurrence of the extinct genus Cedrelospermum (Ulmaceae) in North America: Cedrelospermum manchesteri from Me´xico. Review of Palaeobotany and Palynology 81: 115–128. MAGALLO´N-PUEBLA, S., AND S. R. S. CEVALLOS-FERRIZ. 1994b. Fossil legume fruits from Tertiary strata of Puebla, Mexico. Canadian Journal of Botany 72: 1027–1038.

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MAGALLO´N-PUEBLA, S., AND S. R. S. CEVALLOS-FERRIZ. 1994c. Eucommia constans n. sp. fruits from upper Cenozoic strata of Puebla, Mexico: morphological and anatomical comparison with Eucommia ulmoides Oliver. International Journal of Plant Science 155: 80–95. MANCHESTER, S. R. 1977. Wood of Tapirira (Anacardiaceae) from the Paleogene Clarno Formation of Oregon. Review of Palaeobotany and Palynology 23: 119–127. MANCHESTER, S. R. 1987. Extinct ulmaceus fruits from the Tertiary of Europe and western North America. Review of Palaeobotany and Palynology 52: 119–129 MANCHESTER, S. R. 1989. Attached reproductive and vegetative remains of the extinct American-European genus Cedrelospermum (Ulmaceae) from the early Tertiary of Utah and Colorado. American Journal of Botany 76: 256–276. MARTI´NEZ-HERNA´NDEZ, E., AND E. RAMI´REZ-ARRIAGA. 1996. Palaeocorologı´a de angiospermas de la flora Mexicana durante el Mesozoico y Terciario. Algunas evidencias palinolo´gicas. Boletı´n de la Sociedad Bota´nica de Me´xico 58: 87–97. MIRANDA, F. 1963. Two plants from the amber of the Simojovel, Chiapas, Me´xico area. Journal of Paleontology 37: 611–614. MYERS, J. A. 1996. Volcanic arcs and vegetation. Washington Geology 24(2): 37–39. PAYNE, W. W. 1969. A quick method for clearing leaves. Ward’s Bulletin 8: 4–5. RAMI´REZ, J. L. 1999. Ana´lisis foliar de Anacardiaceae, Berberidaceae, y Salicaceae en Los Ahuehuetes (Oligoceno), Tepexi de Rodrı´guez, Puebla. Master’s thesis, Facultad de Ciencias, Universidad Nacional Auto´noma de Me´xico, Mexico, City, Mexico. RAMI´REZ, J. L., S. R. S. CEVALLOS-FERRIZ, AND A. SILVA. 2000. Reconstruc-

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tion of the leaves of two new species of Pseudosmodingium (Anacardiaceae) from Oligocene strata of Puebla, Mexico. International Journal of Plant Science 161: 509–519. RZENDOWSKI, J. 1991. Diversidad y orı´genes de la flora faneroga´mica de Me´xico. Acta Bota´nica Mexicana 14: 3–21. TAYLOR, D. W. 1993. Paleobiogeographic relationships of angiosperms from the Cretaceous and early Tertiary of the North American area. Botanical Review 56: 393. TERRAZAS, S. T., AND T. WENDT. 1995. Systematic and wood anatomy of the genus Tapirira Aublet (Anacardiaceae): a numerical approach. Brittonia 47: 109–129. VELASCO DE LEO´N, P., AND S. R. S. CEVALLOS-FERRIZ. 1997. Leaves of Cercocarpus (Rosaceae) in Tertiary sediments of Tepexi de Rodrı´guez, Puebla, Mexico. American Journal of Botany 84: 144 (Abstract). VELASCO DE LEO´N, P., S. R. S. CEVALLOS-FERRIZ, AND A. SILVA. 1998. Leaf of Karwinskia axamilpense n. p. (Rhamnaceae) from Oligocene sediments, near Tepexi de Rodrı´guez, Puebla, Me´xico. Canadian Journal of Botany 76: 410–419. WEYLAND, H. 1941. Beitra¨ge zur Kenntnis der Rheiniscehin Tertiarflora: V. Dritte Erganzungen und Berichtigungen zur Flora der Bla¨tterkohle und des Polierschiefers von Rott im Siebengebirge. Palaeontographica Abt. B 86: 79–112. WOLFE, J. A. 1964. Miocene floras from Fingerrock Wash, southwestern Nevada. U.S. Geological Survey Professional Paper 454-N. WOLFE, J. A., AND W. WEHR. 1987. Middle Eocene dicotyledonous plants from Republic, northeastern Washington. U.S. Geological Survey Bulletin 1597. WOODS, M. T., AND G. F. DAVIS. 1982. Late Cretaceous genesis of the Kula plate. Earth and Planetary Science Letters 58: 161–166.