reconstruction of the leaves of two new species of pseudosmodingium (anacardiaceae) from oligocene...

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Reconstruction of the Leaves of Two New Species of (Anacardiaceae) from PseudosmodingiumOligocene Strata of Puebla, Mexico Author(s): José L. Ramírez, Sergio R. S. Cevallos‐Ferriz and Alicia Silva‐Pineda Source: International Journal of Plant Sciences, Vol. 161, No. 3 (May 2000), pp. 509-519Published by: University of Chicago PressStable URL: http://www.jstor.org/stable/10.1086/314261Accessed: 12-02-2016 23:58 UTC

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509

Int. J. Plant Sci. 161(3):509–519. 2000.� 2000 by The University of Chicago. All rights reserved.1058-5893/2000/16103-0016$03.00

RECONSTRUCTION OF THE LEAVES OF TWO NEW SPECIES OF PSEUDOSMODINGIUM(ANACARDIACEAE) FROM OLIGOCENE STRATA OF PUEBLA, MEXICO

Jose L. Ramırez,* Sergio R. S. Cevallos-Ferriz,1,† and Alicia Silva-Pineda†

*Facultad de Ciencias, Departamento de Biologıa, Universidad Nacional Autonoma de Mexico, Ciudad Universitaria, Circuito Exterior, 04510Mexico D.F., Mexico; and †Departamento de Paleontologıa, Instituto de Geologıa, Universidad Nacional Autonoma de Mexico,

Ciudad Universitaria, Circuito de la Investigacion Cientifica, 04510 Mexico D.F., Mexico

Leaves of two new plants are reconstructed from their isolated leaflets collected from the Oligocene LosAhuehuetes locality near Tepexi de Rodrıguez in Puebla, Mexico. The leaves of Pseudosmodingium mirandaeRamırez-Garduno et al. are compound imparipinnate with leaflets of variable morphology. The leaflets of fiveleaf morphotypes vary from narrow elliptic to lanceolate or lorate; they are symmetrical to slightly asym-metrical, with acute to attenuate apex, acute to cuneate base, and entire to serrate margin. Venation is simplepinnate craspedodromous, with secondary veins slightly curved near their base; secondary veins may dichot-omize near the margin to become tertiary veins, and intersecondary veins are small and oblique to the secondaryveins. A small number of leaflets assigned to Pseudosmodingium terrazasiae Ramırez-Garduno et al. aredistinguished from P. mirandae by the leaflet shape, length : width ratio, base shape, and apex angle. Mor-phological comparison of the fossil leaves with leaves of extant species of Anacardiaceae based on numericalanalyses indicates a close similarity between P. mirandae and Pseudosmodingium multifolium Rose, while P.terrazasiae is more similar to Pseudosmodingium perniciosum (HBK) Engl. The presence of fossil species withextant relatives that are endemic to Mexico, along with previous reports, indicates that by the Oligocene,some lineages were already in place, although today they form part of the more xeric communities in southernNorth America.

Keywords: Anacardiaceae, leaf, Mexico, Oligocene, Pseudosmodingium.

Introduction

As one reads about the history of extant vegetation in Mex-ico, it is rare to find information based on macrofossils thatdeals with its Tertiary, or earlier, precursors. This history usu-ally goes back only hundreds or thousands of years; therefore,the lack of knowledge of the plants that lived in the geologicalpast in Mexico has limited this discussion. Extrapolationsbased on neobotanical studies or on paleobotanical informa-tion gathered from other parts of the world, especially northernNorth America and Europe, have been used to explain thepresence of a variety of plants and vegetation types in thesouthern latitudes of North America. This method has gen-erated several hypotheses related to the origin of the extantvegetation of Mexico; however, only the study of fossils col-lected in southern latitudes of North America will test thesehypotheses.

Although paleobotanical studies in Mexico began ca. 1 cen-tury ago, research was focused mainly on Paleozoic and Meso-zoic plants. Tertiary plants were sporadically reported by for-eign researchers who deposited the original material in themuseums of Europe and the United States (e.g., Bose 1906;Arsene and Marty 1923; Berry 1923; Mullerried 1947; Mir-anda 1963).

More recently, research on this group of plants in the Ge-

1 Author for correspondence; e-mail [email protected].

Manuscript received June 1999; revised manuscript received November 1999.

ological Institute of the Universidad Nacional Autonoma deMexico (UNAM) has produced new data on the history of thevegetation of low-latitude North America (Weber 1972; Loz-ano-Garcıa 1974; Magallon-Puebla and Cevallos-Ferriz 1993,1994a, 1994b, 1994c; Rodrıguez de la Rosa and Cevallos-Ferriz 1994; Cevallos-Ferriz and Ricalde-Moreno 1995). Onlythree dicotyledonous leaves have been identified as part of thisproject: Magdalenophyllum (Magallon-Puebla and Cevallos-Ferriz 1994c; the probable leaf of the plant that bore the Ced-relospermum fruits, with which it co-occurs), Cercocarpus,and Karwinskia (Velasco de Leon and Cevallos-Ferriz 1995a,1995b). In this article, isolated leaflets are used to reconstructleaves that are described and compared with the leaves ofextant Pseudosmodingium and closely related taxa. Amongthe extant plants studied, large variation within the leaves andleaflets in a single species, or even within a single individual,prompted the use of a numerical analysis that allowed detailedcomparisons and reconstructions of the fossil material. Aftera numerical analysis, the presence of two new spe-cies—Pseudosmodingium mirandae Ramırez-Garduno et al.and Pseudosmodingium terrazasiae Ramırez-Garduno etal.—are recognized, thereby adding two taxa to the endemicMexican extant plants, for which a relatively long geologicalhistory is documented.

Material and Methods

The fossil plants were collected from the Los Ahuehueteslocality, a continental sedimentary deposit interpreted as be-



510 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 1 Location of the Pie de Vaca Formation, near Tepexi deRodrıguez in Puebla, Mexico, at 18�35�N, 97�55�W. Shaded area cor-responds to the state of Puebla.

longing to the lowermost member of the Pie de Vaca Formation(Pantoja Alor 1992). The locality is 4.5 km north-northwestof the town of Tepexi de Rodrıguez in the southern part ofthe state of Puebla, Mexico, at 18�35�15�N, 97�55�30�W (fig.1). The sedimentary sequence is formed by horizons of volcanicash, shale, and fine-grained sandstone; this sequence representsa lacustrine or low-energy fluvial environment where fossilplants are preserved as carbonized compressions in the lowerlayers.

Plant fossils include primarily the detached and often frag-mentary organs of mainly angiosperms (Magallon-Puebla andCevallos-Ferriz 1994a, 1994b, 1994c). However, there areremnants of fern fronds and an earthstar fungus (Magallon-Puebla and Cevallos-Ferriz 1993).

The stratigraphic relation of the Pie de Vaca Formation withan underlying sequence indicates that its maximum age is Ol-igocene (J. Pantoja Alor, personal communication, 1992). Re-cent palynological analysis of the Los Ahuehuetes deposit in-dicates an Eocene to Oligocene age for the sequence(Martınez-Hernandez and Ramırez Arriaga 1996). Based onthe stratigraphic and palynological data, an Oligocene age forthe Los Ahuehuetes deposit is most likely, but this still needsto be confirmed by radiometric dating.

The fossil leaves were studied with an Olympus SZH ste-reoscopic microscope and camera lucida. Some leaflets weretransferred to cellulose acetate film and observed using anOlympus BH-2 compound microscope to search for preservedtissues or cuticles. The terminology of Hickey (1973) was usedto describe the foliar characteristics.

The leaves were identified by consulting the literature, di-rectly observing herbarium specimens at the National Her-barium of Mexico (MEXU), and using extant field popula-tions. When similarity with a particular taxon was noticed,this taxon and closely allied plants were surveyed. Among thenatural populations surveyed were those of Pseudosmodin-gium multifolium Rose, Pseudosmodingium virletii (Baill.)Engl., and Achtinocheitia filicina Barkl., located in the sur-roundings of Tepexi de Rodrıguez in Puebla; Rhus pachyr-rhachis Hemsl., located near Ciudad Valles, San Luis Potosı;Schinus molle L. and Schinus therebentifolius L., located inMexico City; and Spondias mombin L., located near Cuer-navaca, Morelos.

Numerical taxonomic analyses were conducted using theNTSYS-PC 1.80 program (Rohlf 1993). Two techniques wereutilized to confirm the identification of the fossil material: phe-netic analyses for classification and an ordination technique,principal component analysis, to understand the patterns ofrelationship between the operative taxonomic units (OTUs).The phenetic analysis was performed to better understand andclarify the identification of the fossil plants based on theirleaflets. This analysis included 11 OTUs; five leaflet morpho-types of Pseudosmodingium mirandae (Mi1, Mi2, Mi3, Mi4,and Mi5); the leaves of the extant P. multifolium (Mu), Pseu-dosmodingium perniciosum (Pe), and R. pachyrrhachis (Pa);and some leaflets of Pseudosmodingium terrazasiae (Te). In theanalysis, three leaf morphotypes of P. multifolium (Mu1, Mu2,and Mu3) were recognized instead of a single leaflet type, in-dicating the natural variability of the leaflets in this species.Based on table 1, we elaborated the basic data matrix withnine multistate and continuous characters. The Manhattan

similarity coefficient was applied by columns in order to obtainthe similarity matrix. The technique applied was the agglom-erative technique, not the hierarchical technique with averagelinkage; we used the simple matching coefficient, from whichphenograms, using the unweighted pair-group method usingarithmetic averages, were obtained. This method produces lessdistortion in the phenograms (Crisci and Lopez 1983) andallows all characters to have equal weight.

All the fossil material used in this study is deposited in thepaleobotanical collection of the Paleontological Museum ofthe Instituto de Geologıa, UNAM.

To provide a frame for comparing the leaflets of the fossilmaterial to the modern taxa, we first present a description ofthe leaflets of key extant taxa, with which the reconstructedfossil leaves were compared.

Rhus pachyrrhachis

As observed in the community of Ciudad Valles, San LuisPotosı, R. pachyrrhachis has compound imparipinnate leaveswith leaflets of variable morphology. Terminal leaflets dis-play the following characteristics: obovate, slightly asymmetriclaminae; acuminate to attenuate apex (31�–36�); decurrentto rounded base (44�–66�), entire margin; 59–73 mm inlength # 32–42 mm wide, with a length : width ratio of1.8–1.7 : 1; simple pinnate craspedodromous venation;slightly curved secondary veins, with insertion angle to themain vein of 45�–75�; secondary veins that dichotomize nearthe leaf margin, giving rise to tertiary veins; veins of the in-tercostal area that anastomose to form a random reticulatepattern; and a petiolule of !1 mm in length.

Lateral leaflets display the following characteristics: elliptic,asymmetric laminae; acuminate to attenuate apex (30�–39�);rounded base, entire margin; 32–57 mm in length # 22–43mm wide, with a length : width ratio of 1.4–1.3 : 1; simple



Table 1

Comparison of Characters among OTUs, from Which Character States (Multiple and Continuous) Were Deduced

Character and

leaflet

Morphotypes of

Pseudosmodingium mirandae

Morphotypes of

Pseudosmodingium multifolium

Rhus

pachyrrachis

Pseudosmodingium

terrazasiae

(fig. 4.20)

Pseudosmodingium

perniciosum

(fig. 2.2)

Morphotypes of

Schinus therebentifolius

Mi1

(fig. 4.15)

Mi2

(fig. 4.16)

Mi3

(fig. 4.17)

Mi4

(fig. 4.18)

Mi5

(fig. 4.19)

Mu1

(fig. 2.5)

Mu2

(fig. 2.6)

Mu3

(fig. 2.7)

No. 1

(fig. 3.10)

No. 2

(fig. 3.11)

No. 3

(fig. 3.12)

Shape of leaflets:

Terminal . . . . . . . . . . . . . . Narrow

elliptic

Lanceolate Elliptic Narrow

elliptic

Lorate Narrow

elliptic

Narrow

elliptic

Very narrow

elliptic

Elliptic Lanceolate

and ovate

Elliptic Lanceolate Obovate Elliptic

Lateral . . . . . . . . . . . . . . . . Narrow

elliptic

Elliptic Elliptic Narrow

elliptic

Narrow

elliptic

Narrow

elliptic

Narrow

elliptic

Very narrow

elliptic

Obovate Lanceolate

and ovate

Elliptic Elliptic Obovate Elliptic

Apex shape:

Terminal . . . . . . . . . . . . . . Acute Attenuate ) Acute Acute Attenuate Acute Attenuate Attenuate and

acuminate

Acute Obtuse Acute Emarginate Acute

Lateral . . . . . . . . . . . . . . . . Acute Acute Acute Acute Acute Attenuate Attenuate Attenuate Obtuse Acute Obtuse Acute Emarginate Acute

Apex angle:

Terminal � lateral . . . . . . 31�(23�–36�) 46�(25�–68�) 28�(16�–39�) 33�(28�–36�) 38�(25�–49�) 21� 30� 22.5� 33.5� 89.0� 93.0� 68.0� ) 32.0�

Base shape:

Terminal . . . . . . . . . . . . . . Cuneate Cuneate Acute Slightly

decurrent

Acute Cuneate Cuneate Decurrent Cuneate Cuneate Acute Cordate Acute Acute

Lateral . . . . . . . . . . . . . . . . Cuneate Acute Acute Slightly

decurrent

Acute Cuneate Cuneate Decurrent Rounded Cuneate Acute Rounded Acute Acute

Base angle:

Terminal � lateral . . . . . . 36�(24�–43�) 49�(39�–60�) 36�(25�–47�) 35�(33�–36�) 44�(32�–58�) 49.0� 54.0� 24.5� 62.4� 54.5� 68.0� ) 59.0� 32.0�

Margin:

Terminal � lateral . . . . . . Serrate Serrate Serrate Entire Serrate Serrate Serrate Serrate Entire Serrate and

entire

Serrate and

entire

Entire Entire Serrate

Length/width ratio:

Terminal � lateral . . . . . . 6.0–7.9 : 1 3.8–5.2 : 1 5.5–6.8 : 1 6.4–11.0 : 1 3.4–6.0 : 1 3.2 : 1 3.7 : 1 6.3 : 1 1.9 : 1 1.8 : 1 1.5 : 1 1.9 : 1 1.7 : 1 4.8 : 1

Petiolule (mm):

Terminal � lateral . . . . . . 2 12 Apetiolulated

lamina

11 Apetiolulated

lamina

1.0 1.0 1.0 1.0 2.0 18.0 ) ) )

Average of IAMV:a

Terminal � lateral . . . . . . 65.7 63.2 61.0 56.7 63.0 43.5 72.5 55.0 61.7 56.0 54.0 71.8 62.6 66.7

a IAMV = insertion angle to the midvein.




pinnate craspedodromous venation; secondary veins with aninsertion angle to the main vein of 45�–66�; veins of the in-tercostal area that anastomose to form a random reticulatepattern; and a petiolule that is short, !1 mm in length.

Pseudosmodingium perniciosum

As observed from the 12 herbarium specimens (MEXU) col-lected from Puebla and Morelos, P. perniciosum have com-pound imparipinnate leaves (figs. 2.2–2.4). Terminal leafletsdisplay the following characteristics: elliptic, slightly asym-metric laminae; obtuse to rounded apex (98�–115�); decurrentbase, entire to serrate margin; 22–47 mm in length # 21–30mm wide, with a length : width ratio of 1.5–1.0 : 1; simplepinnate craspedodromous venation, with insertion angle to themain vein of 43�–65�; veins in the intercostal area that aresmall and oblique with respect to secondary veins; and a pet-iolule that is 13 mm in length.

Lateral leaflets display the following characteristics: elliptic,asymmetric, slightly recurved laminae; obtuse to rounded apex(96�–115�); decurrent base (29�–32�), entire to serrate margin;39–42 mm in length # 19–22 mm wide, with a length : widthratio of 2.0–1.9 : 1; simple pinnate craspedodromous vena-tion; secondary veins straight to the margin, with insertionangle to the main vein of 43�–65�; intersecondary veins thatare small and oblique, not forming a reticulum; and a petiolulethat is 7 mm in length.

Pseudosmodingium multifolium

Observed from the community near Los Ahuehuetes locality,P. multifolium have compound imparipinnate leaves (figs.2.5–2.7). Terminal leaflets display the following characteris-tics: narrow elliptic to elliptic, symmetric to slightly asym-metric laminae; acute to attenuate apex (21�–36�); acute todecurrent base, serrate margin; 28–48 mm in length # 6–16mm wide, with a length : width ratio of 4.6–3.0 : 1; simplepinnate craspedodromous venation; secondary veins that areslightly curved, with insertion angle to the main vein of46�–75�; intersecondary veins that are small and oblique withrespect to secondary veins and that are free (figs. 3.8, 3.9); anda short petiolule (fig. 3.8).

Lateral leaflets display the following characteristics: narrowelliptic to elliptic, asymmetric, slightly recurved laminae; acuteto attenuate apex (22�–35�); acute to cuneate base (21�–46�),serrate margin; 33–42 mm in length # 6–14 mm wide, witha length : width ratio of 5.5–3.0 : 1; simple pinnate craspe-dodromous venation; secondary veins that are slightly curved,with insertion angle to the main vein of 47�–74�; intersecon-dary veins that are small, oblique, and free; and a short ornearly absent petiolule.

In table 1, characters of three morphotypes of Schinus ther-ebentifolius (figs. 3.10–3.12) and P. multifolium (figs. 2.5–2.7),as observed in Mexico City from a single population and fromthe fossiliferous outcrop, respectively, P. mirandae, P. terra-zasiae, P. perniciosum, and R. pachyrrhachis, are listed to dis-play the morphological variability in Anacardiaceae. Only onespecies was used to exemplify variation, because in Anacar-diaceae, as observed in the field, this is similar among thestudied taxa. Pseudosmodingium multifolium was chosen for

this purpose because it is most similar to the fossil specimensand shows a high amount of variability.

Systematic Description

Class—Magnoliopsida

Order—Sapindales

Family—Anacardiaceae

Genus—Pseudosmodingium Engler

Species—Pseudosmodingium mirandae Ramırez,Cevallos-Ferriz, and Silva-Pineda sp. nov.

(Figs. 3.13, 4.14)

Holotype. Paleontological Collection of the Instituto deGeologıa, Universidad Nacional Autonoma de Mexico, IGM-PB 985.

Locality. Los Ahuehuetes locality, Pie de Vaca Formation,southern bank of the Axamilpa River, 1.5 km northwest ofTepexi de Rodrıguez in Puebla, Mexico, at 18�35�15�N,97�55�30�W.

Age. Oligocene.Etymology. The specific epithet is for Faustino Miranda,

a Spanish immigrant who developed the study of the tropicalvegetation in Mexico and who recognized the value of fossilplants to understand their history.

Diagnosis. Compound imparipinnate leaves with leafletsof variable morphology. Terminal leaflets with narrow elliptic,lanceolate to lorate, symmetric to slightly asymmetric laminae,acute to attenuate apex, acute to cuneate base, entire to serratemargin; 24–33 mm in length # 4–6 mm wide; simple pinnatecraspedodromous venation, secondary veins slightly curvednear their base, with insertion angle to the midvein of 48�–80�,some secondary veins dichotomize near the leaf margin to formtertiary veins, intersecondary veins small and oblique; petiolule1–2 mm in length or absent.

Lateral leaflets with narrow elliptic, asymmetric, straight toslightly recurved laminae, acute apex, acute to cuneate base,entire to serrate margin; 20–55 mm in length # 3.7–16 mmwide; simple pinnate craspedodromous venation, secondaryveins slightly curved near their base, with insertion angle tothe main vein of 36�–80�, some secondary veins dichotomizenear the leaf margin, giving rise to tertiary veins, intersecon-dary veins small and oblique; petiolule 1–2 mm in length oralmost absent.

Description. It is difficult to provide a single descriptionfor all leaflets because their variation is well marked (table 1).The reconstruction of the five morphotypes in which this var-iation is exemplified simplifies their description, allows thegrouping of leaflets with some similarity, underscores the dif-ferences between lateral and terminal leaflets (table 1; figs.4.15–4.19), and facilitates the discussion presented in the nextsection.

Species—Pseudosmodingium terrazasiae Ramırez,Cevallos-Ferriz, and Silva-Pineda sp. nov.

(Figs. 4.20, 4.21)

Holotype. Paleontological Collection of the Instituto deGeologıa, UNAM, IGM-PB 984.



RAMIREZ ET AL.—OLIGOCENE PSEUDOSMODINGIUM FROM MEXICO 513

Fig. 2 Figs. 2.2–2.4, Cleared leaflets of Pseudosmodingium perniciosum. Fig. 2.2, General view of the leaflet. Bar = 5 mm. Fig. 2.3, Close-up of the intercostal and marginal areas of a leaflet with high-order veins ending free in leaflet with entire margin (arrow). Bar = 2.5 mm. Fig.2.4, Close-up in a different leaflet (with toothed margin [arrow]) of the intercostal and marginal areas with high-order veins ending free in aleaflet. Bar = 1.5 mm. Figs. 2.5–2.7, Leaf variability of Pseudosmodingium multifolium from individuals near Los Ahuehuetes locality. Bar = 5cm.

Locality. Los Ahuehuetes locality, of the Pie de Vaca For-mation, on the southern bank of the Axamilpa River, 1.5 kmnorthwest of Tepexi de Rodrıguez in Puebla, Mexico, at18�35�15�N, 97�55�30�W.

Age. Oligocene.Etymology. The specific epithet is for Teresa Terrazas-

Salgado, in recognition of her outstanding work on the familyAnacardiaceae.

Diagnosis. Lanceolate leaflets, ovate to narrow elliptical,slightly asymmetrical laminae, acute to attenuated apex, cu-neate base, entire to serrate margin, with simple teeth; 44 mmin length # 19 mm wide in the widest portion of the leaflet;




Fig. 3 Figs. 3.8, 3.9, Cleared leaflets of Pseudosmodingium multifolium. Fig. 3.8, General view of the leaflet. Bar = 5 mm. Fig. 3.9, Close-up of the intercostal and marginal areas of a leaflet with high-order veins ending free (arrow). Bar = 1 mm. Figs. 3.10–3.12, Samples of leafvariation of Schinus therebentifolius in a single population. Bar = 5 cm. Fig. 3.13, General view of the leaflet of Pseudosmodingium mirandae,holotype IGMPB985. Bar = 1 cm.

pinnate craspedodromous venation, secondary veins straightto the margin, with insertion angle to the main vein of 52�–63�,some secondary veins dichotomize near the leaf margin to formtertiary veins, intercostal veinlets small and oblique; petiolule1 mm in length.

Description. Leaflets with ovate, narrow elliptic, lanceo-

late laminae, with their widest part at ca. 30% of their totallength, acute apex (84�), cuneate asymmetrical base (32�), withone of the sides having a more pronounced curvature; entireto serrate margin; with simple teeth of convex-concave andconcave-convex shape; the largest leaflet is 44 mm ( ) inx = 18length by 19 ( ) mm wide, with a length : width ratio ofx = 22




2.0 : 1; pinnate craspedodromous venation; strong, straightmidvein, five to seven pairs of straight or slightly curved sec-ondary veins, with insertion angle to the midvein ranging from52� to 63�, some secondary veins dichotomize near the leafmargin and end either at the base or apex of the teeth, inter-costal veins are small and oblique, little ramified, althoughsome fuse and are sinuous, but they never form areoles; veinletsof higher order near the margin are free and do not fuse (figs.4.20, 4.21); petiolule 1 mm long (fig. 4.20).

In contrast with P. mirandae, in which terminal and lateralleaflets were detected, in P. terrazasiae, their smaller number(16) makes this determination difficult; thus, we assume thatin the actual collection, only lateral leaflets are present.

Numerical Analysis

In order to give more support to the identification based onthe similarity of the morphological characters preserved in thefossil material and their correlation to those seen in the extantplants, a numerical analysis was performed. Since comparisonis based on the reconstruction of a single plant organ, it waspreferable to use as many characters as possible, even if theyoverlapped somewhat, and therefore a phenetic analysis waschosen to demonstrate the relationships among the plants stud-ied. For example, although using apex shape (e.g., obtuse,acute, etc.) and range of apex angle (e.g., 25�–30�, 31�–36�)seems to duplicate character states, stating that a leaflet hasan acute apex (with an angle of 90� or less) is not the sameas stating that the angle is 25� or 85�. In this sense, althoughthey share one character, variability in this character is alsotaken into consideration.

From the phenogram (fig. 5) it becomes evident that the leafmorphotypes of P. mirandae (Mi1, Mi2, Mi3, Mi4, and Mi5)form a cohesive group that is distinct from P. terrazasiae (Te).The five reconstructed leaves of P. mirandae share high simi-larity values, reaching a maximum between leaf morphotypesMi3 and Mi4 (fig. 5), strongly indicating the cohesiveness ofthe group. Pseudosmodingium multifolium (Mu) and R. pa-chyrrhachis (Pa) form a second group that is distinct from thethird group, which is composed of P. terrazasiae and P. per-niciosum (Pe). The analysis also demonstrates the presence oftwo phenetic groups, each with a single fossil plant. Thus, wesuggest that the recognition of the two new species of Pseu-dosmodingium is well supported. However, the phenetic po-sition based on the morphological similarity of R. pachyr-rhachis and P. multifolium is ambiguous, since the former isused as an alien species of the four species of Pseudosmodin-gium discussed in this study. We expected P. terrazasiae andP. perniciosum to occupy a position closer to P. mirandae andP. multifolium. Therefore, leaf variability in P. multifolium wasintroduced into the analysis (fig. 5) by recognizing three leafmorphotypes (Mu1, Mu2, and Mu3; table 1). By doing this, P.mirandae is associated with the morphotype Mu3 of P. mul-tifolium, while P. terrazasiae continues to be associated withP. perniciosum (fig. 5).

Discussion

Systematic Comparison

Among the numerous leaflets collected from the Los Ahue-huetes locality, those discussed in this article can be included

in Anacardiaceae based on their asymmetric laminae, serratemargin, pinnate craspedodromous venation, secondary veins(which dichotomize close to the teeth base or the leaf margin),and thin tertiary intercostal veins (J. A. Wolfe, personal com-munication, 1998). These characters are useful not only todefine in a general way some members of the family, but theyalso have been used to identify taxa like Rhus (e.g., MacGinitie1953; Axelrod 1956; Lakhanpal 1958; Ozaki 1980). Based onthese general characters, comparison of the leaflets of the newplants from Puebla indicates a close affinity not only with Rhusbut also with Schinus and Pseudosmodingium. However, bycomparing the higher-order venation, like the tertiary inter-costal veins, and by comparing how the tertiary veins end nearthe leaflet margin, a stronger relationship to Pseudosmodin-gium becomes evident.

In Schinus, the secondary veins curve near the margin, whereclose to the teeth they dichotomize to form slender archedtertiary veins, whereas the intercostal veinlets ramify in a per-current fashion (Wolfe 1964). Furthermore, some intercostalveinlets that seem to be admedial veins, especially in the SouthAmerican species, do not form complete areoles. In contrast,some species of Rhus have intercostal tertiary veins with ir-regular patterns, and there is a tendency in the genus for theirfusion and for the formation of areoles; however, in some cases,these are of the incomplete type (Becker 1972). The closestaffinity of the Los Ahuehuetes leaflets is with those of Pseu-dosmodingium. The two share unfused high-order veins, wheretertiary and quaternary veins are freely ending, even close tothe leaflet margin, and where intercostal tertiary veins occa-sionally branch but do not form areoles.

The morphologic variability among the analyzed leaflets ofPseudosmodingium mirandae from the Los Ahuehuetes local-ity raises the question of whether they represent a single specieswith large variability or whether they in fact represent morethan one species. Observation of natural populations ofSchinus molle L., Schinus therebentifolius L. (figs. 3.10–3.12),Pseudosmodingium multifolium (figs. 2.5–2.7), Pseudosmo-dingium virletii (Baill.) Engl., Achtinocheitia filicina Barkl.,Rhus pachyrrhachis Hemsl., and Spondias mombin L. showsthat there is a large amount of variability in terms of the leavesand leaflets of these species. All are highly variable in termsof the size, shape, number, and type of teeth as well as in termsof the length : width ratio, the number of secondary veins perside, and the shape of the leaflet base and apex.

The variability observed among extant plants of the familywas used to separate the leaflets that corresponded to each ofthe five fossil morphotypes of P. mirandae. The laminae shapeand the length : width ratio of the leaflets, the number of sec-ondary veins, the presence or absence of teeth, the type ofteeth, and the degree of petiolule development were especiallyuseful in grouping the leaflets. Of minor but useful importancewas the arrangement of high-order veins. To distinguish be-tween terminal and lateral leaflets, the symmetry of the leafletsand the length of the petiolule were used. Terminal leaflets aremore symmetrical and generally have longer petiolules.

Although Pseudosmodingium terrazasiae shows some sim-ilarity with P. mirandae, it has distinctive characters that sup-port its recognition as a different species. The leaflet shape,especially the length : width ratio, of P. terrazasiae, which is!4.0 : 1, contrasts with that of P. mirandae (figs. 3.13, 4.20).




Fig. 5 Phenogram based on nine characters and 11 OTUs. TheOTUs are Pseudosmodingium mirandae (Mi1, Mi2, Mi3, Mi4, and Mi5),Pseudosmodingium multifolium (Mu1, Mu2, and Mu3), Pseudosmo-dingium terrazasiae (Te), P. perniciosum (Pe), and Rhus pachyrrhachis(Pa).

Fig. 4 Fig. 4.14, Leaflet of Pseudosmodingium mirandae, holotype IGMPB985. Close-up showing the intercostal and marginal areas of aleaflet with high-order veins ending free (arrows). Bar = 1 mm. Figs. 4.15–4.19, Reconstruction of foliar morphotypes of P. mirandae based onfoliar characters. Bar = 2 cm. Fig. 4.15, Based on paratypes IGM-PB 986–996. Note presence of long petiolule (arrows) and teeth size. Fig.4.16, Based on paratypes IGM-PB 997–1007. Note presence of long petiolule (arrows). Fig. 4.17, Based on paratypes IGM-PB 1008–119. Noteabsence of petiolule (arrows) and the scarcity of the teeth. Fig. 4.18, Based on paratypes IGM-PB 1020–1029. Note entire margin and smallpetiolule. Fig. 4.19, Based on paratypes IGM-PB 1030–1040. Note absence of petiolule and size and scarcity of teeth. Figs. 4.20, 4.21, Leafletof Pseudosmodingium terrazasiae, holotype IGMPB 984. Fig. 4.20, General view of the leaflet. Bar = 5 mm. Fig. 4.21, Close-up of holotype,showing the intercostal and marginal areas of a leaflet with little ramification and free ends of high-order veins (arrows). Bar = 1 mm. Fig. 4.25,Tracheal elements, IGM-PB 1041. Bar = 30 mm.

As a consequence, their base and apex angles are distinct. Also,the tertiary intercostal veins in P. terrazasiae are sinuous andbecome fused, whereas in P. mirandae, these veins are shortand little ramified and do not fuse. Applying the criteria ofvariability mentioned above, the distinction between these twospecies demonstrates the interspecific variability within the An-acardiaceae. In contrast, by not applying this criteria, the rangeof variability in the fossil material would greatly surpass thatseen in natural extant populations.

The relationships in the phenogram (fig. 5) indicate that leafvariability in P. multifolium crosses the limits of the species.The phenetic location of R. pachyrrhachis further indicatesthat variability within the family is large and that at least someleaf characters may overlap when one is comparing differenttaxa above the species level. Variability in at least some of theextant and fossil plants seems to be a little different. In at leastone fossil species, P. mirandae, the leaves form a cohesivegroup. In contrast, variability in the leaf and leaflets of extantP. multifolium crosses generic limits, indicating that for theidentification of the fossil material with Anacardiaceae affin-ities, detailed comparisons with both fossil and extant materialare needed. Although leaf and leaflet variability are recognizedin the Anacardiaceae of Tepexi de Rodrıguez in Puebla, byboth morphological and numerical comparison, our resultsstrongly support the recognition of two distinct fossil speciesof Pseudosmodingium.

The grouping of R. pachyrrhachis with morphotypes Mu1

and Mu2 of P. multifolium is less clear. This grouping may beexplained as a consequence of the way in which the previoustwo groups are formed. However, based on the data in table1, it may be suggested that leaflet shape as well as apex andbase angles are important to linking these taxa. The wide rangeof variability in terms of the characters of these plants is re-sponsible for the overlapping of the OTUs. It is most likelythat if high-order venation patterns were used in the study, therelationships of similarity would be more distant in these taxa,and the OTUs would be better defined. Unfortunately, thisinformation is not available for all the fossil specimens; there-fore, it was not used in the analysis.

Although some anatomical characters have been observedin the transferred and cleared leaflets, their use in the systematicdiscussion is restricted because not all characters are knownfrom all leaves. It is important, however, that tracheary ele-ments (fig. 4.25), stellate trichomes (figs. 6.26, 6.27), epidermalcells (fig. 6.28), and cells of the mesophyll (fig. 6.29) have beenobserved in the fossil Pseudosmodingium. However, stellatetrichomes were not found in the reviewed extant material ofthe genus. Only filiform trichomes have been reported in sev-

eral genera of Anacardiaceae (including Schinus), but our ob-servations revealed the presence of some stellate trichomes inthis genus. This indicates that stellate trichomes may be presentin other members of the Anacardiaceae, even though they arenot listed in the review by Metcalfe and Chalk (1979).

Paleoclimatic Interpretation

Compared with other angiosperms, extant members of theAnacardiaceae have very high seed viability, which enhancestheir potential for germination and colonization of new hab-itats. As a consequence of this characteristic, many of the mem-bers of the family live in disturbed areas, both in Mexico andmore distant regions, such as the Chaco region in South Amer-ica (T. Terrazas-Salgado and F. Gonzalez-Medrano, personalcommunication, 1995). The extreme climatic conditions underwhich extant Pseudosmodingium grows in both xeric and se-mixeric areas along with its capability to invade disturbedareas provide some insight into the environment in which thefossil plants grew and were fossilized during the Oligocene. Inthe Los Ahuehuetes locality, in addition to these two speciesof Pseudosmodingium, the presence of other leaves and leafletsreferable to Anacardiaceae (and which are currently understudy) indicates the presence of at least four other taxa. Theirabundance and variability indicate the adaptive success ofsome members of the family during the Oligocene in tropical




Fig. 6 Figs. 6.26–6.29, Anatomical features of fossil Pseudos-modingium mirandae. Fig. 6.26, Stellate trichome with five arms, IGM-PB 1043. Bar = 70 mm. Fig. 6.27, Stellate trichome with 12 arms, IGM-PB 1043. Bar = 50 mm. Fig. 6.28, Epidermal cells, IGM-PB 1043. Bar= 25 mm. Fig. 6.29, Polyhedral cells of the mesophyll, IGM-PB 1044.Bar = 30 mm.

North America; however, to further support this hypothesis,some insights into the taphonomic process in the fossiliferouslocality are needed.

The abundance of volcaniclastic material in the outcrop andthe geographic distribution of this volcaniclastic stratigraphicunit are suggestive of constant disturbance to the environment,the soil, and the organisms that inhabited the area. An extinctplant widely distributed during Eocene-Oligocene times, Ced-relospermum (Ulmaceae), has been reported from the LosAhuehuetes locality (Magallon-Puebla and Cevallos-Ferriz1994c). The localities in which this plant has been reportedcorrespond mostly to lacustrine sediments, in which volcanicash is an important component, indicating that this plant wasa colonizer in areas affected by volcanic activity (Manchester1989). Thus, the presence of a group of plants from the LosAhuehuetes locality strongly indicates that the environmentalconditions around the outcrop during the Oligocene favoredthe presence of fast-growing early colonizer plants, like thetwo species of Pseudosmodingium presented here, as well asCedrelospermum and perhaps the other members of Anacar-diaceae. The presence of some Leguminosae taxa (Prosopis,Mimosa, Lysiloma, and Sophora) in the Los Ahuehuetes lo-cality further tends to supports this idea, although this presencecannot be taken as a precise environmental index (Magallon-Puebla and Cevallos-Ferriz 1994b).

Another component of climate, indicated by the leaves ofPseudosmodingium, is the presence of seasonality during thetime of deposition of the fossiliferous strata. The tendency inextant evergreen plants to have well-developed areoles in theleaves correlates with certain climatic conditions (such as highhumidity). This characteristic, which in the schemes of Hickeyand Wolfe (1975) or Takhtajan (1991) may be considered a“primitive” condition, seems, rather, to be an adaptive strategy.However, in the case of Anacardiaceae with or without poorlydeveloped areoles, the condition may be related to the presenceof deciduous plants growing under marked seasonal conditions(T. Terrazas-Salgado, personal communication, 1995). Thesetwo explanations are not mutually exclusive. The presentknowledge related to the Los Ahuehuetes flora indicates thatit is not a xeric community but, rather, a chaparral-like com-munity or a dry tropical forest. However, only through futurework in this and other localities of the Tertiary of tropicalNorth America will it be possible to further discuss the evo-lution of some lineages as well as of their communities.

Acknowledgments

We would like to acknowledge the assistance of the person-nel of the National Herbarium (MEXU), who assisted us incomparing the fossil leaves and leaflets with those of extantplants. Hector Hernandez Campos and Antonio Altamirahelped during the photographic process. The NTSYS-PC 1.80program was facilitated by Dr. Javier Caballero Nieto, JardınBotanico, Instituto de Biologıa, UNAM. We greatly appreciatethe valuable comments to a previous version of this manuscriptthat were provided by Dr. Leo Hickey, Yale University; Dr.Patrick Fields, Michigan State University; Dr. Robin Burnham,University of Michigan; Dr. Diane Erwin, University of Cali-




fornia, Berkeley; Dr. Jay H. Jones, University of La Verne; andDr. Peter R. Crane, Royal Kew Gardens. The Direccion Gen-eral de Asuntos del Personal Academico, UNAM, and Consejo

Nacional de Ciencia y Tecnologıa partially financed this studythrough projects IN207294, IN205597, and 1005PT,respectively.

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reconstruction of the leaves of two new species of pseudosmodingium (anacardiaceae) from oligocene...

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