Taxonomic Revision of Zamia in Mega-Mexico

Taxonomic revision of Zamia in Mega-Mexico

1 1 FERNANDO NICOLALDE-MOREJÓN ,ANDREW P. V OVIDES , 2 AND DENNIS W. STEVENSON

1 Departamento de Biología Evolutiva, Instituto de Ecología, A. C. km 2.5 Antigua Carretera a Coatepec No. 351, Xalapa 91070 Veracruz, Mexico 2 The New York Botanical Garden, Bronx, NY 10458-5120, USA; e-mail: [email protected]

Abstract. The genus Zamia is revised for Mega-Mexico, with 22 species recognized and described. The study presents a taxonomic clarification for the genus in Mesoa- merica, a contribution that provides the foundation for a future monograph for Zamia in the Neotropics. The largest proportion of species richness and endemism for the genus is concentrated in southeastern Mexico, among the states of Chiapas, Oaxaca, Tabasco, and Veracruz, an area that is considered highly diverse in floristic terms. Distribution maps and a key to species are also provided, as well as complete descriptions of the specimens examined, including information on nomenclatural types, habitats, synonymies, and etymologies. A lectotype is designated for Zamia loddigesii, and neotypes for Z. galeottii, Z. leiboldii var. angustifolia, and Z. variegata. Zamia spartea is illustrated for the first time, and chromosome numbers for Z. herrerae are reported and illustrated. Finally, scanning electron micrographs of leaflet trichome character states are presented, along with a discussion of their systematic implications within the group. Key Words: Endemism, Mexico, gymnosperms, cycads, floristic richness, Zamia. Resumen. El género Zamia es revisado para Mega-México, con 22 especies descritas y una species dubia. El estudio está orientado al esclarecimiento taxonómico del género en Mega-México, una contribución que siente los fundamentos para una futura monografía para Zamia en el Neotrópico. La mayor riqueza y endemismo para el género se concentra en el sureste de México, entre los estados de Chiapas, Oaxaca, Tabasco y Veracruz, área de alta biodiversidad florística. Mapas de distribución y una clave para las especies son presentadas, como también descripciones completas, tipos, hábitat, sinónimos, etimología y especimenes examinadas. Se designa un lectotipo para Zamia loddigesii, y neotipos para Z. galeottii, Z. leiboldii var. angustifolia y Z. variegata. Zamia spartea es ilustrada por primera vez y números cromosómicos para Z. herrerae son presentados. Finalmente, se presentan fotografías de tricomas al mi- croscopio electrónico y una discusión de sus implicaciones en la sistemática del grupo.

According to Stevenson (1992), Zamiaceae Central America that is ﬂoristically similar to comprises eight genera distributed in tropical the southern part of Mexico (Mega-Mexico) and subtropical Africa, Australia, Greater while Microcycas A. DC. (1 sp.) and Chigua Antilles, North, Central and South America. D.W. Stev. (2 spp.) are endemic to Cuba and Five genera with 94 species are known from Colombia, respectively. The type genus for the Neotropics (Hill et al., 2007). The genera the family, Zamia L. (59 spp.), is distributed Ceratozamia Brongn. (21 spp.) and Dioon throughout tropical and sub-tropical America Lindl. (13 spp.) are both endemic to Mexico as well as the Caribbean, with exception to and a neighboring biogeographic region of the Lesser Antilles.

Zamia is the widest distributed genus of the Mexico’ hereafter, given that the slight dif- order Cycadales in the Neotropics. Its northern ferences in the boundaries of ‘Mega-Mexico 1’ range starts in Georgia and Florida (U.S.A.), with respect to ‘Mega-Mexico 2’ do not affect reaching Bolivia and the Mato Grosso of the biogeographic aspects of our description Brazil in South America (Balduzzi et al., of the species. This study is intended to 1982;Sabato,1990; Norstog & Nicholls, provide a taxonomic clarification of the genus 1997; Stevenson, 2001a, b). A remarkable in Mesoamerica and to provide the basis for a morphological and cytological variation has future monograph of Zamia. been documented (Vovides, 1983; Moretti & Sabato, 1984; Moretti, 1990a, b; Stevenson et – al., 1995 1996a; Vovides & Olivares, 1996; Materials and methods Norstog & Nicholls, 1997), and also high levels of genetic variation (González-Astorga The present taxonomic revision is based on et al., 2006). As a consequence of this more than 450 specimens from the following complexity, the taxonomy of Zamia is contro- herbaria: B, BM, CIB, CHIP, CICY, ECOSUR, versial; although the genus comprises 75 ENCB, F, FCME, FLAS, FTG, HEM, IBUG, species, their circumscription and limits have IEB, K, LE, MEXU, MO, NY, SERO, U, yet to be determined (Hill et al., 2007). UADY, UAMIZ, US, W, WIS, XAL, XALU, The most recent exhaustive taxonomic and ZEA. Unfortunately, we were not able to treatment for Zamia was published by Schus- obtain vouchers on loan from NAP; therefore, ter (1932) and later work by Sabato (1990) material from this herbarium is not cited. and Stevenson (1987; 1991a, b; 1993; 2001a, Chromosome counts for Zamia herrerae b; 2004) underlined nomenclatural and taxo- Calderón & Standley were performed on five nomic anomalies in Zamia, principally owing individuals held at the Jardín Botánico Fco. to insufficient fieldwork and a scarcity of Javier Clavijero, Instituto de Ecología, A.C. good-quality botanical collections. The taxo- (JBC). These plants has been previously nomic history for the genus in Mexico began collected at the Acacoyagua and Tonalá with the publication of Zamia fufuracea L. f. regions, located in the state of Chiapas and in 1789 from the central-south coastal region represent the species range in southern Mex- of Veracruz, which also represents the first ico. Plants from its full biogeographic range, cycad species described from the American which would include El Salvador and Guate- continent. During the 19th century, six spe- mala, were not available for this study. A cies were subsequently described for Mexico; modified root-tip squash method was used for Z. fischeri Miq., Z. katzeriana (Regel) Rettig, examining somatic metaphase cells described Z. lawsoniana Dyer, Z. loddigesii Miq., Z. by Vovides (1983) with a 12 to 15 hour ice- spartea A. DC. and Z. verschaffeltii Miq., water (0°C) follow-up soak after the 0.2% whereas the remaining known species were colchicine pretreatment at ambient tempera- documented and characterized during the ture (Schutzman et al., 1988). Counts were 20th century, with a marked tendency for made from the best 10–15 metaphase cells taxonomic activity during the last thirty years and karyotype noted according to the classi- (Vovides et al., 1983; Schutzman et al., 1988; fication of Schlarbaum and Tsuchiya (1984). Stevenson et al., 1995–1996a, b; Schutzman Photomicrographs were produced using a & Vovides, 1998; Vovides, 1999). Zeiss Fomi III photomicroscope fitted with The present taxonomic revision includes planapochromatic objectives and Kodak Plus- endemic species of the cycad genus Zamia that X pan ASA 125 film. occur in ‘Mega-Mexico 2’, a term coined by Scanning electron micrographs (SEM) Rzedowski (1991) that associates the Central were taken on young leaflet material from American territories of Guatemala, Belize, living plants cultivated in the JBC. Samples Honduras and northern Nicaragua to the were placed on sample stubs with double Mexican states of Nayarit on the Pacificto sided adhesive tape and then introduced into southern Tamaulipas on the Gulf of Mexico using a dessicator for 24 hours. All samples were biotic (mainly floristic) criteria. Rzedowski’s sputter coated with gold-palladium at 1.5 kv concept will be referred to as simply ‘Mega- at 5 mA for 8 minutes with a Jeol Fine Coat 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 303

JFC 1100 sputter coater. Observations were notable, with branches reaching up to 80 cm made with a Jeol JSM-5600LV SEM. long in adult plants. In all cases, the types have been examined TRICHOMES.—Trichomes of cycads leaves by one or more of the authors. are bi-celled, consisting of a small basal cell and a longer free apical portion (Stevenson, Results 1981). All the trichomes analyzed here show the same bifurcate pattern, with one arm HABITAT proportionally longer than the other (Fig. 1A). Of the 22 species included in this revision, Each trichome presents a rounded basal cell 18 occur in specific habitats, accounting for and a more extensive cylindrical bifurcate free the restricted distribution of the majority of portion, which in most cases observed had the taxa. The species with the widest distri- evidence of collapse and twisting (Fig. 1B–F). bution are associated with two or more The pubescence was significantly denser in vegetation types, namely (a) Zamia paucijuga emerging than in older adult leaves with the Wieland, found in pine-oak, oak and tropical latter becoming completely glabrous. An dry forests; (b) Z. polymorpha D.W. Stev., A. exception to this condition is found in Zamia Moretti & Vázq. Torres, located in evergreen furfuracea, which maintains a great part of its tropical rainforest, sub-deciduous tropical original indument on the abaxial surface of forest and their secondary succession stages; each leaflet. (c) Z. herrerae, which occurs in evergreen According to Stevenson (1981), four types tropical rainforest, sub-deciduous tropical of trichomes occur in Zamia; of these, the forest and tropical dry forest and their transparent ramified and the colored ramified secondary succession stages and finally, to a are the types found in the present work. In lesser extent; and (d) Z. loddigesii, present in contrast to what was found in the aforemen- evergreen tropical rainforest, but more com- tioned study by Stevenson, no trend or monly in sub-deciduous tropical forest and its correlation was found between aerial stems secondary succession stages. (i.e., Z. soconuscensis or Z. inermis) and bifurcate trichomes with equal length branches. Trichomes with unequal sized MORPHOLOGY prevail among taxa with both aerial and HABIT.—All adult cycad stems are pachycau- subterranean stems. In this context, we lous and may be columnar and arborescent or consider that a more extensive and detailed subterranean and tuber-like. The genera Dioon, sampling of the genus Zamia across the Microcycas, Ceratozamia and Lepidozamia Neotropics would be necessary to corroborate Regel are usually columnar arborescent in habit, any correlation between trichome morpholo- while the subterranean forms are characteristic gy and stem habit. of Bowenia Hook. ex Hook. f., Chigua,and REPRODUCTIVE STRUCTURES.—Although the Stangeria T. Moore. Cycas L., Encephalartos characters employed for the identification of Lehm., Macrozamia Miq. and Zamia have both species of Zamia have been obtained from stem morphologies, either subterranean tuber- leaf morphology (Miquel, 1861, 1869; Regel, like or columnar arborescent (Stevenson, 1980). 1857, 1876; de Candolle, 1868; Schuster, In this context, the species of Zamia in 1932; Eckenwalder, 1980; Vovides et al., Mesoamerica represent both growth forms, with 1983; Newell, 1986; Schutzman & Vovides, the subterranean tuber-like habitat predominant. 1998; Schutzman et al., 1988; Stevenson, Only four species, Z. inermis, Z. onanreyesii, Z. 1993, 2001a, b, 2004; Nicolalde-Morejón et soconuscensis and Z. tuerckheimii,havearbo- al., 2008), the evaluation of reproductive rescent stems reaching up to 100 cm or more in characters, especially those corresponding to height. Some species branch dichotomously ovulate strobili, is essential to discriminate with age (namely, Z. fischeri Miq.,Z.furfuracea, among closely related taxa. Outstanding Z. inermis Vovides, Rees & Vázq. Torres, Z. attributes that should be considered in this soconuscensis Schutzman, Vovides & Dehgan, case are (i) the form and shape of the cone Z. loddigesii and Z. herrerae), with the coastal apex (Stevenson, 1987); (ii) the peduncle dune species Z. furfuracea being the most position with respect to the vertical axis of 304 BRITTONIA [VOL 61

FIG.1. Trichomes. A–B. Zamia furfuracea. C–D. Z. katzeriana. E–F. Z. polymorpha. the cone, when mature (Schutzman et al., ogy introduced by Mundry and Stützel (2003) 1988); and (iii) the overall color of the cone has been followed. (see descriptions and Figs. 2, 3). In contrast to CHROMOSOME NUMBERS.—Zamia shows the the ovulate strobili, pollen strobili show highest chromosome numbers and karyotype scarce variation at the species level, and their variation throughout the order Cycadales, utility to discriminate among species that with 2n counts of 16, 17, 18, 22, 23, 24, 25, might possess high degrees of genealogical 26, 27, and 28 (Marchant, 1968; Norstog, afﬁnity is relatively low. For the description 1980, 1981;Vovides,1983;Moretti& of the pollen reproductive axes, the terminol- Sabato, 1984; Moretti, 1990a, b; Vovides & 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 305

FIG.2. Illustrations of ovulate strobili. A. Zamia inermis. B. Z. vazquezii.C.Z. paucijuga. D. Z. lacandona. E. Z. spartea. 306 BRITTONIA [VOL 61

FIG.3. Illustrations of ovulate strobili. A. Z. ﬁscheri. B. Z. furfuracea. C. Z. cremnophila. D. Z. katzeriana. E. Z. polymorpha. 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 307

Olivares, 1996). In contrast, all Ceratozamia Zamia: first, Norstog’s hypothesis (Norstog, species studied so far have stable diploid 1980, 1981) relating karyotype simplification chromosome numbers (2n=16) and karyo- and symmetry with progressive fusion of types, as do all the Dioon species analyzed to telocentric chromosomes, which predicts low date with stable diploid chromosome numb- diploid number in taxa with a high number of ers (2n=18) and karyotypes (Marchant, 1968; metacentric chromosomes, and secondly that Vovides, 1983, 1985; Moretti, 1990a, b). of more recent research on Zamia, which Chromosome counts are presented and postulates centric fission rather than fusion illustrated (Fig. 4) here for the first time for producing a progressively higher diploid num- Zamia herrerae. This species has, but to a ber and asymmetric karyotypes with a high lesser extent, cytotype polymorphisms similar number of telocentric chromosomes (Moretti to those found for Z. paucijuga (Moretti & & Sabato, 1984; Vovides & Olivares, 1996; Sabato, 1984) and Z. polymorpha (Vovides & Caputo et al., 2004). For a more in-depth Olivares, 1996; Stevenson et al., 1995– discussion of mechanisms of chromosome 1996b). Zamia herrerae has 2n=23, 24 from evolution in seed plants, see Jones (1998). two populations along its Mexican range in The highly asymmetric karyotypes and Chiapas (Fig. 4). Both the m (median region somatic chromosome numbers in both Z. of the chromosomes) and T (telocentric) paucijuga and Z. polymorpha, which also chromosomes vary in number (6–11 T, 4– appear to be the pattern for Z. herrerae, seem 6 m) and are large (6–11 μm for T and 8–12 to be correlated with the highest morpholog- μm for m) and their arms can be longer than ical variation and widest geographic distribu- half the spindle axis, which can cause mitotic tion of the genus in Mesoamerica. Zamia instability during telophase (Schubert, 2007). herrerae has a range of about 1000 km, Karyotype differences are probably due to spanning El Salvador, Guatemala, and Chia- centric fissions occurring on some of the pas (Mexico); therefore, we suggest investi- larger m chromosomes, giving rise to telo- gating the distribution of chromosome centrics with part of the centromere still character states in this species throughout its present. In this context, there are two general range. This karyotype asymmetry contrasts hypotheses to explain karyotypic evolution in with their congeners of a more restricted

FIG.4. Chromosomes of Zamia herrerae. A. 2n=23. B. 2n=24. 308 BRITTONIA [VOL 61 distribution, which often have less morpho- Guatemala; (c) Z. loddigesii, ranging along logical variation and a tendency towards the Gulf of Mexico seaboard from Tamauli- constant chromosome number and karyotype, pas (northeast Mexico) to Tabasco (south- e.g., Z. cremnophila Vovides, Schutzman & east); and (d) Z. variegata Warsz., distributed Dehgan, Z. fischeri, Z. inermis, Z. katzeriana, between Guatemala and southern Mexico. Z. purpurea and Z. soconuscensis (all 2n=16), The southern and southeastern regions of as well as Z. furfuracea, Z. spartea and Z. Mexico, comprising the states of Veracruz, vazquezii (all 2n=18). Vovides and Olivares Oaxaca, Chiapas, and Tabasco, are the most (1996) and Jones (1998) comment that diverse area of Mexico for the genus Zamia, atypical chromosome number increase attrib- with seven endemic species (Z. cremnophila, uted to fission is probably a result of stressful Z. lacandona, Z. loddigesii, Z. katzeriana, Z. influences. purpurea, Z. polymorpha, and Z. spartea). The Gulf of Mexico region has three micro- endemics Z. furfuracea, Z. inermis and Z. DISTRIBUTION AND ENDEMISM vazquezii, whereas two micro-endemic spe- Seventy-five percent of the species in this cies, Z. fischeri and Z. soconuscensis, are revision are endemic to the type locality and known respectively from the Sierra Madre nearby areas. They are limited to two or three Oriental and the Sierra Madre de Chiapas. close populations with low population densi- Finally, in spite of the status of Z. pauci- ties. These attributes are consistent with juga as a Mexican endemic, its distribution is Rabinowitz’s(1981) evaluation criteria for extremely wide within Mega-Mexico, cover- species rarity, which mainly considers infor- ing a range of about 1000 km between the mation related to geographic range, habitat states of Oaxaca and Nayarit. The northern specificity and local population size. In limit of Z. paucijuga in the latter state congruence with these criteria, the endemic represents the northernmost distribution for Zamia species of Mesoamerica are considered the genus along the Pacific seaboard of the rare, threatened or endangered and are listed Neotropics. under the IUCN Red List (IUCN, 2005; Hill et al., 2007). Taxonomic treatment With 21 endemic cycad species in three genera, Mexico has the highest cycad diver- Zamia L., Sp. Pl. ed. 2: 1659. 1763. nom. sity and number of endemics of the region. cons. Type: Zamia pumila L. Six species of Zamia are known in Guate- Palma-Felix Adanson, Fam. Pl. 2: 21, 587. mala, two of which are endemic (Z. monticola 1763. Chamberlain and Z. tuerckheimii J. Donnell Aulacophyllum Regel, Gartenflora 25: 140. Smith); in Honduras, three species are known 1876. of which three recently described species are endemic (Z. oreillyi C. Nelson, Z. sandovalii Stems hypogeous and epigeous, erect to C. Nelson, and Z. onanreyesii C. Nelson & G. decumbent, sometimes dichotomously Sandoval). Two further species are known for branched in mature plants. Cataphylls charta- Belize, of which one is endemic (Z. prasina ceous to membranaceous, stipulate, persistent W. Bull) and finally, El Salvador is repre- or deciduous, base triangular, apex long sented by one broadly distributed species, Z. acuminate to aristate, tomentose, generally herrerae, with a range that runs along the reddish-brown to yellowish. Ptyxis erect to Pacific seaboard through Guatemala and the inflexed. Leaves stipulate, ascending to Sierra Madre de Chiapas in Mexico. Other descending to spreading, reddish-brown or species of the genus in Mexico with broad green when emerging; petiole sometimes distributions are (a) Z. paucijuga, distributed blackish in young leaves, terete or subterete, along the Pacific seaboard of Mexico ranging without prickles or heavily to lightly armed from Nayarit (northwest Mexico) to Oaxaca with straight or bifurcate prickles; rachis (southwest); (b) Z. polymorpha, distributed subterete generally with few prickles along widely throughout the Yucatán penninsula in the proximal third or without prickles, with Mexico, Belize, and the Petén region of up to 60 pairs of leaflets. Leaflets articulate, 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 309 sessile, papyraceous to coriaceous, linear, hexagonal, 0.3–0.55 cm long, fertile abaxial linear-lanceolate, lanceolate, ovate, obovate surface 2 lobed with 2–14 bisporangiate obpyriform to elliptic, opposite to suboppo- synangia per lobe, sporangia dehiscent by site, falcate or non-falcate, imbricate to longitudinal slit. Ovulate strobili usually non-imbricate, generally acute at apex and solitary, erect to decumbent, cylindrical to symmetric, attenuate at base, margins entire ellipsoid, purple to yellowish, generally to dentate along upper third, subrevolute, tomentulose, apex acute to apiculate; pedun- articulations green, yellowish or dark brown cle densely tomentose; ovulate sporangio- in young leaflets. Pollen strobili usually 1–2 phores cuneiform-peltate to scutiform, distal (−4), with sterile tip, erect, cylindrical to end truncate-hexagonal when not scutiform. conical, light brown to purple, tomentulose, Seeds ovoid, sarcotesta white to pink when apex acute to apiculate, generally with dense- immature, red at maturity, sclerotesta smooth ly tomentose peduncles; pollen sporangio- but sometimes with several furrows running phores cuneiform, distal face truncate longitudinally from micropylar end.

Key to the species of Zamia in Mega-Mexico

1. Leaflets chartaceous to papyraceous. 2. Leaflet margin dentate. 3. Leaflets elliptic, adaxial surface with yellow to cream variegation ...... Z. variegata 3. Leaflets long-lanceolate, without variegation. 4. Leaflets imbricate, peduncle of pollen strobili decumbent, up to 16 cm long...... Z. oreillyi 4. Leaflets not imbricate, peduncle of pollen strobili erect, up to 8 cm long ...... Z. herrerae 2. Leaflet margin serrulate to entire. 5. Leaflet margin entire, chartaceous. 6. Leaflets oblong-lanceolate, glossy, 4–6 cm wide; ovulate strobili iridescent blue-green at maturity...... Z. tuerckheimii 6. Leaflets linear-lanceolate, not glossy, 0.6–1.5 cm wide, ovulate strobili dark-brown at maturity...... Z. soconuscensis 5. Leaflet margin serrulate, papyraceous. 7. Leaflets sub-falcate basally, long-acuminate, strongly apically curved...... Z. monticola 7. Leaflets straight, acuminate, not curved at apex. 8. Leaflets elliptic to lanceolate, ovulate strobili cylindrical to ovoid, dark-green and glabrous when mature; from San Luís Potosí and Querétaro, Mexico ...... Z. fischeri 8. Leaflets ovate to obpyriform, ovulate strobili ovoid-cylindrical, gray to brown tomentulose when mature; endemic to Veracruz, Mexico ...... Z. vazquezii 1. Leaflets coriaceous. 9. Leaflet margin entire to serrulate. 10. Leaflet margin entire, petiole unarmed ...... Z. inermis 10. Leaflet margin serrulate, petiole prickly. 11. Leaflets long acuminate apically; stems arborescent ...... Z. onanreyesii 11. Leaflets rounded to acute apically; stems subterranean. 12. Leaflets obovate to oblanceolate, keeled adaxially, apex rounded . . . . Z. furfuracea 12. Leaflets linear to oblanceolate, flat adaxially, apex acute. 13. Leaflets linear, 0.4–0.6 cm wide ...... Z. spartea 13. Leaflets lanceolate, ≥0.7 cm wide. 14. Leaflets falcate ...... Z. sandovallii 14. Leaflets not falcate. 15. Leaflets lanceolate-oblanceolate, ovulate strobili dark-brown tomentulose...... Z. polymorpha 15. Leaflets linear-lanceolate, ovulate strobili brown to yellowish. 16. Ovulate strobili ellipsoid to cylindrical, apex acute to apiculate, yellowish-brown; from the Pacific seaboard of Mexico . . . Z. paucijuga 16. Ovulate strobili ellipsoid to conical, apex acute, yellowish; from the Gulf ofMexicoseaboard...... Z. loddigesii 9. Leaflet margin distinctly dentate. 17. Leaflets channeled adaxially between veins, appearing plicate . . . . Z. purpurea 17. Leaflets smooth, not channeled adaxially between veins, not appearing plicate. 18. Leaflets linear-lanceolate, imbricate, petiole strongly armed with straight or bifurcate prickles up to 6 mm long ...... Z. cremnophila 310 BRITTONIA [VOL 61

18. Leaflets lanceolate to oblanceolate, not imbricate, petiolearmed with small straight prickles, generally between 2–4 mm. 19. Leaflets with brilliantly shining cuticle on adaxial surface;ovulate strobili decumbent when mature ...... Z. katzeriana 19. Leaflets without brilliantly shining cuticle on adaxial surface; ovulate strobili erect when mature. 20. Distal leaflets sub-falcate, petiole with bulbous base, blackish in young leaves...... Z. lacandona 20. All leaflets straight, petiole with no bulbous base, greenish in young leaves. 21. Leaflets oblong to lanceolate, bright grass-green, without conspic- uously denticulate along margins; ovulate strobili green glabrous when mature, apex acuminate ...... Z. prasina 21. Leaflets long-lanceolate, conspicuous dentate, up to 4 mm long; ovulate strobili brown tomentulose when mature, apex long- apiculate...... Z. standleyi

Zamia cremnophila Vovides, Schutzman & when immature, red at maturity, 2–2.8 cm long, Dehgan., Bot. Gaz. 149(3): 351. 1988. Type: 1.4–2 cm in diam, sclerotesta smooth. Mexico. Tabasco: 18 Aug 1981, M. A. Chromosome number.—2n=16 (Schutzman Magaña & S. Zamudio 343 (holotype: MEXU; et al., 1988). isotypes: CSAT, FCME, MO, UAMIZ). Diversity and genetic structure.—The average of alleles per locus is A=1.98, the percentage of polymorphic loci is P=94.3, the Stem hypogeous, generally unbranched, 5– expected heterozygosity is HE=0.347 and 34 cm long, 4–11.3 cm in diam. Cataphylls the genetic differentiation between the two chartaceous, persistent, base triangular, apex populations currently under study is Fst= aristate, 5.4 cm long, 2.9 cm at base, reddish- 0.093 (González-Astorga et al. unpubl. data). brown tomentose. Ptyxis inflexed. Leaves 2–3 Distribution and habitat.—Endemic to (4), 57.5–179×40.2–76.1 cm, descending, red- Tabasco, Mexico (Fig. 5), on karstic rocks and dish-brown when emerging; petiole 10.2– cliffs of the Sierra El Madrigal, between 50– 95.3 cm long, blackish in young leaves, 150 m. The vegetation type where this species subterete, heavily armed with straight or bifur- grows is evergreen tropical rain forest or bosque cate prickles up to 6 mm long; rachis subterete, tropical perennifolio of Rzedowski (1978). up to 84 cm long, with few prickles along the Etymology.—The specific epithet is derived proximal third. Leaflets 5–28 pairs, sessile, from the Greek word for cliff-friend coriaceous, lanceolate, opposite to subopposite, (κρɛμνóσ = cremnos = cliff, and ιλοσ = imbricate, apex acute, base attenuate, margins filos = friend/lover; Schutzman et al., 1988), dentate along distal third, subrevolute; articula- because of its unusual habitat. tions dark brown in young leaflets, 0.8–1.2 cm; Distinguishing features.—The species is the median leaflets 22.7–38×3.1–4.4 cm wide. characterized by its exclusive habit on the Pollen strobili usually 1–2, erect, cylindrical, up rocky walls of limestone cliffs, in addition to to 8 cm long and 1.4 cm in diam, light brown, descendent leaves. Petioles are densely armed apex acute; peduncle densely light brown with prickles that are sometimes branched, tomentose, 4.5 cm long, 1.2 cm in diam; pollen and also lanceolate, imbricate leaflets that are sporangiophores cuneiform, distal face truncate- visibly dentate along the distal third. hexagonal, 0.35 cm long, fertile abaxial surface with 3 bisporangiate synangia per lobe. Ovulate Additional specimens examined.— MEXICO. strobili usually solitary, erect, ellipsoid, 13.2 cm TABASCO: Teapa, F. Nicolalde-Morejón et al. 1497 (XAL), M. A. Pérez-Farrera 293 (HEM), M. A. Pérez- long, 4.9 cm in diam, brown to reddish, Farrera 900 (HEM, MEXU). tomentulose, apex acuminate; peduncle densely brown tomentose, 2.9 cm long, 1.6 cm in diam; Zamia fischeri Miq. in Lem., Hort. Vanhoutt. 1: distal face hexagonal-truncate with a horizontal 20. 1845. Type: ex Horto Petropolitano in H. longitudinal depression, 1–1.2 cm high, 1.1– Houtte. vecta, Miquel s.n. (neotype, designated 1.4 cm wide. Seeds ovoid, sarcotesta white by Stevenson & Sabato, 1986: U). (Fig. 7) 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 311

FIG.5. Distribution of Zamia cremnophila ( ), Z. furfuracea ( ), Z. inermis (●), Z. katzeriana ( ), Z. lacandona (■), Z. monticola ( ), Z.onanreyesii ( ), Z. prasina ( ), Z. sandovallii (▲), Z. soconuscensis ( ), Z. vazquezii ( ).

Stem subterranean, dichotomously branching to ovoid, up to 9 cm long, 4.5 cm in diam, brown in older plants, up to 30 cm long, 4–8cmin to reddish tomentulose when young, dark-green diam. Cataphylls membranaceous, persistent, and glabrous when mature, apex acute; peduncle base triangular, apex aristate, 4.5 cm long, brown tomentose, 3 cm long, 1.1 cm in diam; 1.2 cm at base, yellowish tomentose. Ptyxis megasporangiophores peltate, distal face hexag- inflexed. Leaves 1–5(–8), 15–45×8–20 cm, onal-truncate when immature, scutiform when ascending to spreading, dark-brown when mature 0.8–1.2 cm high, 1.3–1.9 cm wide. Seed emerging; petiole 9–14 cm long, blackish in ovoid, 1.6 cm long, 1.3 cm in diam, sarcotesta young leaves, unarmed, terete; rachis subterete, pink when young and orange at maturity. up to 31 cm long, unarmed. Leaflets 20–35 Chromosome number.—2n=16 (Marchant, pairs, sessile, papyraceous, elliptic to oblanceo- 1968; Moretti et al., 1991; Stevenson et al., late, alternate to subopposite, apex acute sym- 1995–1996a). metric, base cuneate, margins serrulate along Distribution and habitat.—Zamia fischeri distal third, subrevolute; articulations light- is endemic to Mexico (Tamaulipas, San Luis brown in young leaflets, 0.3–0.4 cm wide, Potosí, Querétaro and Hidalgo; Fig. 5), be- median leaflets 5–9×1.5–4.5 cm. Pollen stro- tween 140–900 m elevation. The vegetation bili usually 1–3, erect, conical, 4–6cmlong, type of its habitat is pine-oak forest, tropical 1.5–2.2 cm in diam, gray tomentose, apex deciduous forest and mountain tropical forest acute; peduncle yellowish tomentose, 2.8 cm (sensu Rzedowski, 1978). long, 0.9–1.1 cm in diam; pollen sporangio- Etymology.—The specific epithet is in phores cuneiform, distal face hexagonal- honor of Friedrich Fischer, a German cycad truncate, 0.3 cm long, fertile abaxial surface horticulturist of the 19th century. with 3–4 bisporangiate synangia per lobe. Distinguishing features.—Zamia fischeri is Ovulate strobili usually 1–2, erect, cylindrical a small fern-like plant (up to 100 cm tall), 312 BRITTONIA [VOL 61 with papyraceous but serrulate leaflets and usually 2–4, erect, cylindrical, up to 17 cm unarmed petiole and rachis. Ovulate strobili long, 1.8 cm in diam, yellowish to brown, greenish upon maturity. apex acute; peduncle densely light-brown — tomentose, 12 cm long, 1.1 cm in diam; Additional specimens examined. MEXICO. pollen sporangiophores cuneiform, distal face QUERÉTARO: Jalopan, López 438 (XAL), Servín 1471 – (XAL), Vovides 330 (XAL). SAN LUIS POTOSÍ: O. M. hexagonal-truncate, 0.45 0.55 cm long, fer- Clark 6839 (MO), J. Rees 1686 (XAL), Stevenson et al. tile abaxial surface with 8–9 bisporangiate 566 (MEXU, NY), Vovides 753 (XAL); El Naranjo, F. synangia per lobe. Ovulate strobili usually 1 Nicolalde-Morejón & J. González Astorga 1614 (XAL), per crown, erect, cylindrical, up to 25 cm 1615 (XAL),1616(XAL),1617(XAL),1618(MEXU, XAL),1619(XAL); Ciudad Valles, F. Nicolalde-Morejón long, up to 10.5 cm in diam, yellowish-green & J. González-Astorga 1620 (XAL),1621(XAL),1622 tomentulose when immature, light brown (XAL),1623(MEXU, XAL),1624(MEXU, XAL),1625 upon maturity, apex apiculate; peduncle yel- (MEXU, XAL), 1626 (MEXU, XAL). HIDALGO: Pisa- lowish tomentose, up to 8 cm long, up to flores, O. Alcántara-Ayala & R. Mayorga-Saucedo 3325 (FCME). 1.3 cm in diam; megasporangiophores peltate, distal end hexagonal-truncate, 0.9 cm Zamia furfuracea L. f. in Aiton, Hortus high, 1.3 cm wide. Seeds ovoid, sarcotesta Kew. 3: 477. 1789. Type: Palma america- yellowish-green when immature turning red na crassis rigidisque foliis, pl. 210, in at maturity, 1.6 cm long, 1.2 cm in diam, sclerotesta smooth. Herm. Paradisus Batavus. 1698 (lectotype, — designated by Stevenson & Sabato, 1986: Chromosome number. 2n=18 (Moretti, pl. 210). 1990a, b) Diversity and genetic structure.—The average of alleles per locus is A=2.05, the Zamia muricata var. obtusifolia Miquel, Tijdschr. nat. Gesch. Physiol. 10(1): 71–72. 1843. Zamia latifo- percentage of polymorphic loci is P=90.7, the lia Loddiges ex Miquel, Tijdschr. wis-en natuurk. expected heterozygosity is HE=0.356 and Wet. 2(4): 298. 1849. Type: Tab. VII, fig. a in the genetic differentiation between the two Linnaea 19(4): 1847. (neotype, designated by fi populations currently under study is Fst= Stevenson & Sabato, 1986: Tab. VII, g. a). 0.161 (González-Astorga et al. unpubl. data). Zamia furfuracea var. trewii A. DC., Prodr. 16(2): — 541. 1868. Type: Palmifolia fructu clavato poly- Distribution and habitat. Endemic to pireno[polyspermo]. C. J. Trew, PI. Select. Tab. Mexico in central and south coastal Veracruz, 26. 1752 (holotype: Tab. 26, G; typotype, desig- along a coastal stretch of approximately150 km nated by Stevenson & Sabato, 1986: BM). in stable dunes and basalt cliffs (Fig. 5). Etymology.—The specific epithet alludes to Stem hypogeous, becoming epigeous with the persistent brown-yellowish trichomes of age, often dichotomously branched, up to the leaves throughout the developmental 60 cm long, 20 cm in diam. Cataphylls stages of the plant. coriaceous, persistent, base triangular, apex Distinguishing features.—Leaves strongly long aristate, up to 10×3–4.5 cm at base, keeled with highly imbricate and coriaceous yellowish tomentose. Ptyxis inflexed. Leaves obovate to oblanceolate leaflets with brown- 3tomany,45–190×10–30 cm, diffuse, yellowish indumentum persisting with age. brown-yellowish when emerging; petiole – 17 50 cm long, brown-yellowish when Additional specimens examined.—MEXICO. young, subterete, armed with small prickles VERACRUZ: Ibarra-Mariquez 316 (MEXU, MO), up to 3 mm long; rachis terete, up to 120 cm Ibarra-Mariquez 1952, 1959 (MEXU); Alvarado, Rees long, with few prickles along the proximal 1650, 1651, 1652 (XAL), M. Vázquez-Torres et al. 4871 third. Leaflets 8–18 pairs, sessile, coriaceous, (CIB); Catemaco, Calzada 1475 (MEXU), Calzada 2451 (XAL), Cedillo 2610 (MEXU, XAL), González-Quintero obovate to oblanceolate, opposite to subop- 1520 (ENCB), Ibarra 316 (MEXU), Lot 1277-14 (F, posite, imbricate, keeled, apex rounded to XAL), Menendez 115 (MEXU, MO, XAL), F. Nicolalde- sub-acute, base attenuate, margins slightly Morejón et al. 1484 (XAL), 1485 (XAL), 1486 (XAL), J. serrulate along the 1/2 distal portion, sub- Rees 1651 (IBUG, MEXU, XAL), J. Rees 1652 (XAL), Schatz & Nee 207 (XAL), Vovides 567 (MEXU, XAL); revolute; articulations yellow in young and Mecayapan, Calzada et al. 11325 (XAL), Castillo- juvenile leaflets, 0.4–0.7 cm wide; median Campos 12732 (XAL); Lerdo De Tejada, Vovides 828 leaflets 14–20×4–7.5 cm. Pollen strobili (XAL), 829 (XAL), 830 (XAL), 831 (XAL), 832 (XAL), 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 313

833 (XAL), 839 (XAL); San Andrés Tuxtla, Castillo- be found in secondary growth forests and Campos et al. 13881 (XAL), Chazaro B. 512 (XAL), pastures. Hammel & Merello 15499 (MO), Hernández-M 1216A — fi (F, MEXU), Lorence 4978 (MEXU), Sousa 3099 (F, Etymology. The speci c epithet honors MEXU, MO), Vovides & Iglesias 1148 (XAL). Hector Herrera, a scientist from El Salvador. Distinguishing features.—Zamia herrerae is distinguished by its long-lanceolate papyra- Zamia herrerae Calderón & Standl., Proc. ceous leaflets with dentate margins along the Wash. Acad. Sci. 14(4): 93. 1924. Type: El distal 2/3. Salvador. Vicinity of Sonsonate, 17 Jul 1923, S. Calderón 1682 (holotype: US). Additional specimens examined.—MEXICO. CHIAPAS: Escuintla, Matuda 16368 (MEXU), 16871 Stem hypogeous, bifurcate in adult plants, (MEXU), 17332 (MEXU), 18332 (MEXU), M. A. – – Pérez-Farrera 143 (HEM), Schutzman 526 (XAL), 527 6 26×4.5 13.5 cm in diam. Cataphylls char- (XAL), 528 (XAL); Tonalá, Farrera 2489 (CHIP), F. taceous, persistent, base triangular, apex Nicolalde-Morejón & J. González-Astorga 1579 (XAL), aristate, 4.6×1.2 cm wide at base, yellowish 1580 (XAL), 1581 (XAL), M. A. Pérez-Farrera 744 tomentose. Ptyxis inflexed. Leaves 2–4, erect, (CIB). green to light-brown when emerging, 61–96× GUATEMALA. P. C. Standley 67306 (F). 24.5–29.5 cm; petiole 19–34 cm long, brown- NICARAGUA. MANAGUA: Cultivated, A. Grijalva ish in young leaves, terete, armed with 3658 (MO). prickles up to 3 mm long; rachis subterete, up to 63 cm long, with few prickles along the Zamia inermis Vovides, J.D. Rees & Vázq. proximal third. Leaflets 15–32 pairs, sessile, Torres, Flora de Veracruz 26: 22. 1983. Type: papyraceous, lanceolate, alternate to subop- Mexico. Veracruz: 6 Jun 1981, Vovides 666 posite, apex acute, base symmetric attenuate; (holotype: XAL; isotype: F). (Fig. 8) margins dentate along distal 2/3, subrevolute; articulations dark brown when young, 0.3– Stem epigeal, erect, dichotomously branch- 0.5 cm wide; median leaflets 22–38×3.1– ing in mature plants, 15–43 cm long, 8.6– 4.4 cm. Pollen strobili usually 2–3, erect, 26.4 cm in diam. Cataphylls chartaceous, cylindrical to conical, 4.3–7.5 cm long, 1.3– persistent, base triangular, apex aristate, 2.1– 2.1 cm in diam, light brown tomentulose, 2.6×4.1–5.6 cm wide at base, yellowish apex mucronate; peduncle densely light- tomentose. Ptyxis inflexed to erect. Leaves 10– brown tomentose, 6.2–7.8 cm long, 1.1– 35, erect, light to yellowish-green when emerg- 1.4 cm in diam; pollen sporangiophores ing, 30–95×43.5–60 cm; petiole 18–41 cm long, cuneiform, distal face hexagonal, 0.35 cm greenish in young leaves, subterete, without long, fertile abaxial surface with 3–4 bispor- prickles; rachis subterete, 15–19 cm long, angiate synangia per lobe. Ovulate strobili unarmed. Leaflets 27–32 pairs, sessile, coria- usually solitary, erect, cylindrical to ovoid, ceous, linear-lanceolate, opposite to suboppo- 7.1–11.6 cm long, 4.1–4.9cmindiam, site, apex acute, base attenuate; margins entire, brown, tomentulose, apex acute; peduncle subrevolute; articulations 0.4–0.6 cm wide; densely brown tomentose, 3.5–4.2 cm long, median leaflets 20–30.5×0.9–1.2 cm. Pollen 1.1–1.3 cm in diam; megasporangiophores strobili cylindrical, usually 1–2 per crown, erect, peltate, distal face hexagonal-truncate, 1.3– up to 9.1 cm long, up to 2.8 cm in diam, beige- 1.6 cm high, 2.2–2.8 cm wide. Seeds ovoid, yellowish, apex acute; peduncle densely light- sarcotesta pink when immature, red at matu- yellowish tomentose, up to 4.5 cm long, 1.1 cm rity, 1.6–1.9 cm long, 1.2–1.5 cm in diam, in diam; pollen sporangiophores cuneiform, sclerotesta smooth. distal face hexagonal-truncate, 0.35 cm long, Chromosome number.—2n=23, 24 (Fig. 4). fertile abaxial surface with 5–6 bisporangiate Distribution and habitat.—The species synangia per lobe. Ovulate strobili usually 1–2 range is El Salvador, Guatemala, and southern percrown,erect,cylindrical,13–23 cm long, 8– Mexico in Chiapas, between 100–600 m 9.8 cm in diam, light-brown to beige tomentu- elevations (Fig. 6). It generally grows in lose, apex apiculate; peduncle brown tomentose, tropical deciduous forest (sensu Rzedowski, 6–8 cm long, 1.2–1.4cmindiam;megaspor- 1978) on deep clay soils. Also, this cycad may angiophores peltate, distal face hexagonal-trun- 314 BRITTONIA [VOL 61

FIG.6. Distribution of Zamia fischeri (●), Z. herrerae ( ), Z. loddigesii ( ), Z. oreillyi ( ), Z. paucijuga ( ), Z. polymorpha (■), Z. purpurea (▲), Z. spartea ( ), Z. standleyi ( ), Z. tuerckheimii ( ), Z. variegata ( ). cate, 0.7–0.9 cm high, 1.1–1.3 cm wide. Seeds Nicolalde-Morejón & Vovides 1415 (XAL), 1416 (XAL), ovoid, sarcotesta pink when immature, red at 1417 (XAL), Schutzman 570 (XAL), 571 (XAL), 572 – – (XAL), 575 (XAL), 576 (XAL), 577 (XAL), J. Rees et maturity, 1.7 2.5 cm long, 1.4 2.1cmindiam, al. 681 (XAL). sclerotesta smooth. Chromosome number.—2n=16 (Vovides, Zamia katzeriana (Regel) Rettig, Garten- 1983). flora 45: 148. 1896. Ceratozamia katzeri- Distribution and habitat.—Endemic to ana Regel, Acta Horti Petrop. 4(4): 298. Mexico in a small mountain range in central Veracruz (Fig. 5)at150–300 elevation on 1876. Type: ex Horto Katzer., Regel s.n. (lectotype, designated by Stevenson & basaltic soils. The vegetation type of the habitat Sabato, 1986: LE). is tropical deciduous forest (sensu Rzedowski, 1978). Etymology.—The specific epithet alludes to Zamia splendens Schutzman, Phytologia 55(5): 299. 1984. Type: Cultivated in Fairchild Tropical Garden, the absence of prickles on the petiole and Miami, accession no. FTG 76–1046, 11 Apr 1984, J. rachis and the entire leaflet margins. Watson s.n. (holotype: NY; isotypes: FLAS, FTG, Distinguishing features.—Zamia inermis MEXU). differs from its congeners in Mexico by a total absence of prickles along the petiole and Stem hypogeous, unbranched, up to 25 cm rachis, as well as having totally entire leaflets long, up to 7 cm in diam. Cataphylls charta- and light-yellowish to clear-beige tomentu- ceous, semidecidious, base triangular, apex lum on the pollen and ovulate strobili. aristate, 5.3×1.4 cm at base, yellowish tomentose. Ptyxis inflexed. Leaves 1–2 (3), Additional specimens examined.—MEXICO. 49–220×35–58 cm, ascending to descending, VERACRUZ: Actopan, Acosta & Acosta 234 (XAL), F. bright reddish-pink with lustrous cuticle when 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 315

FIG.7. Zamia ﬁscheri A. Habit. B. Leaﬂets. (From Stevenson 566, NY).

emerging, dark green when mature; petiole abaxial surface with 5–6 bisporangiate syn- 20–130 cm long, terete, armed with few angia per lobe. Ovulate strobili usually simple prickles; rachis subterete, up to solitary, decumbent to erect, elliptic, 8– 84 cm long, unarmed. Leaflets 3–7 pairs 12 cm long, 4.5–6 cm in diam, brown to sessile, coriaceous, oblong-lanceolate, oppo- yellowish tomentose, apex aristate; peduncle site to subopposite, adaxial surface with brown tomentose, 2.1–4.3 cm long, 1.1–1.3 cm brilliantly shining cuticle throughout life of in diam; megasporangiophores peltate, distal leaflet, apex acute, base attenuate; margins face hexagonal-truncate to scutiform, 1–1.2 cm dentate along distal third, subrevolute; artic- high, 1.1–1.3 cm wide. Seeds ovoid, sarcotesta ulations brown in young leaflets turning green pink when immature, red at maturity, 1.1– with age 0.6–1.6 cm wide; median leaflets 1.4 cm long, 1.6–1.8 cm in diam, sclerotesta 18–35×3.5–12 cm. Pollen strobili 1–5, con- smooth. ical, light-brown tomentulose, erect upon Chromosome number.—2n=16(Schutzman, emergence becoming prostrate to decumbent 1984;Moretti,1990a). upon maturity, up to 3.9 cm long, 1.1 cm in Diversity and genetic structure.—The diam, apex acute; peduncle light-brown to- average of alleles per locus is A=1.95, the mentose, up to 5.8 cm long, 1.2 cm in diam; percentage of polymorphic loci is P=84.4, pollen sporangiophores cuneiform, distal face the expected heterozygosity is HE=0.280 hexagonal scutiform, 0.35 cm long, fertile and the genetic differentiation between 316 BRITTONIA [VOL 61

FIG.8. Zamia inermis. A–B. Habit. C. Cataphyll. D. Pollen strobilus. E. Microsporophyll, abaxial and adaxial view. F–H. Ovulate strobilus. I. Ovulate sporangiophores. J. Seed. (From the holotype.) 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 317 the two populations currently under study is pairs, sessile, coriaceous, lanceolate, opposite Fst=0.194 (González-Astorga et al. unpubl. to subopposite, subfalcate, apex acute, base data). attenuate, margins dentate along distal third, Distribution and habitat.—Endemic to subrevolute; articulations dark-brown when Mexico and known from the states of young, 0.4–1.1 cm wide; median leaflets Chiapas, Tabasco and Veracruz (Fig. 5)at 15.6–37×2.9–6 cm. Pollen strobili usually 200–700 m in evergreen tropical forest (sensu 2–3, erect, conical, 5.4–6.6 cm long, 1.5– Rzedowski, 1978). 1.7 cm in diam, light-brown, apex acute; Etymology.—Specific epithet in honor of peduncle light-brown tomentose, 5.8–6.9 cm Katzer, inspector of the gardens in Paullowsk long, 1.2 cm in diam; pollen sporangiophores (Stevenson & Sabato, 1986). cuneiform, distal face hexagonal truncate, Distinguishing features.—Zamia katzeriana 0.35 cm long, fertile abaxial surface with 4– is easily distinguished from its congeners by 5 bisporangiate synangia per lobe. Ovulate having leaves with highly lustrous or shiny strobili usually solitary, erect, ellipsoid, cuticles. Emerging leaves are a bright reddish- 13.2 cm long, 4.9 cm in diam, dark-brown, pink. Both pollen and ovulate strobili are tomentulose, apex acute to slightly apiculate; borne on long peduncles that become descen- peduncle densely brown tomentose, 6.5 cm dent to prostrate. long, 1.2 cm in diam; megasporangiophores peltate, distal face hexagonal-truncate, 1– Additional specimens examined.—MEXICO. 1.2 cm high, 1–1.5 cm wide. Seeds irregularly VERACRUZ: Las Choapas, Martínez & Martínez-M. 825 ovoid, sarcotesta pink when immature, red at (HEM), F. Nicolalde-Morejón et al.1436 (XAL), 1437 maturity, 2–2.4 cm long, 1.3–1.9 cm in diam, (XAL). TABASCO: Teapa, Hdez-Najarro 622 (CHIP), M. A. Magaña 1905 (MEXU), M. A. Pérez-Farrera s.n. sclerotesta smooth. (XAL), M. A. Pérez-Farrera 899 (HEM, MEXU), Chromosome number.—2n=16, 17, 18 Walters s.n. (FTG accession 12-2, XAL). CHIAPAS: San (Schutzman & Vovides, 1998). Fernando, Vovides et al. 1266 (XAL), Palacios 383 Diversity and genetic structure.—The av- (CHIP), F. Nicolalde-Morejón & Pérez-Farrera 1420 (XAL), M. A. Pérez-Farrera s.n. (XAL), Walters s.n. erage of alleles per locus is A=1.78, the (FTG accession 23-2, XAL); Ocozocoautla, Gómez- percentage of polymorphic loci is P=67.9, the Pompa 705 (FCME, MEXU), F. Nicolalde-Morejón et expected heterozygosity is HE=0.191 and al. 1453 (XAL), 1454 (XAL), 1455 (XAL), 1456 (XAL), the genetic differentiation between the two 1457 (XAL), 1458 (XAL), 1459 (XAL), 1460 (XAL), M. populations currently under study is Fst= A. Pérez-Farrera 29 (CHIP, CIB, MEXU); Tila, Vovides et al. 1340 (XAL), 1343 (XAL), 1341 (XAL). 0.108 (González-Astorga et al. unpubl. data). Distribution and habitat.—Endemic to Chiapas (Fig. 5) in the vicinity of the Zamia lacandona Schutzman & Vovides, Lacandon forest at 80–200 m elevation, in Novon 8(4): 441. 1998. Type: Mexico. evergreen tropical forest (sensu Rzedowski, Chiapas: Selva Lacandona, July 1984, 1978). It is also found in secondary succes- Schutzman 517 (holotype: FLAS; isotype: sion stages of the tropical forest. XAL). Etymology.—The epithet is derived from the name of the 1.8 million hectare Selva Stem hypogeous, unbranching, 6–14 cm Lacandona (Lacandona Jungle) in southeast- long, 5–9 cm in diam. Cataphylls coriaceous, ern Chiapas, which itself bears the name of persistent, base triangular, apex long-aristate, the Lacandona Maya Indians who inhabit the 8.3×3.6 cm at base, reddish-brown tomen- forest. tose. Ptyxis inflexed, reddish-brown. Leaves Distinguishing features.—This species is usually solitary, up to 3 under cultivation, 46– distinguished by having a solitary large leaf 171×32–75 cm, ascending, reddish-brown (up to three leaves may be maintained on when emerging; petiole 14–95.3 cm long plants under cultivation) with a stout erect with bulbous base, blackish in young leaves, petiole and a strongly bulbous base. The leaf subterete, proximal section strongly chan- is reddish-brown at emergence and petiole neled, armed with prickles up to 5 mm long; dark purplish-brown turning dark-brown with rachis subterete, 31–76 cm long, with few age. Ovulate cone generally solitary, with prickles along proximal third. Leaflets 4–17 acute apex. 318 BRITTONIA [VOL 61

Additional specimens examined.—MEXICO. 1028b (lectotype, designated by Stevenson & CHIAPAS: Palenque, Schutzman 510 (XAL),511(XAL), Sabato, 1986: LE; isolectotype, LE). 512 (XAL), 513 (XAL), 514 (XAL), 515 (XAL), 516 Zamia loddigesii var. longifolia J. Schust., in Engl., (XAL), 517 (XAL), 518 (XAL), 519 (XAL), 520 (XAL), Pflanzenr. 4(1): 147. 1932. Type: Mexico. Vera- F. Nicolalde-Morejón & N. Martínez 1418 (XAL), M. A. cruz: Colipa, Karwinski 1029 (lectotype, designat- Pérez-Farrera 890 (HEM, MEXU), Walters s.n. (FTG ed by Stevenson & Sabato, 1986: LE; isolectotype: accession 14-2, XAL), M. Vázquez-Torres et al. 3925 LE). (CIB); San Jerónimo Tulija, Chavelas et al. ES=315 (ENCB, MEXU), Schutzman 521 (XAL), 522 (XAL), Stem hypogeous, branching dichotomously 524 (XAL), 523 (XAL), 525 (XAL). with age, 10–45 cm long, 8–15 cm in diam. Cataphylls chartaceous, persistent, base trian- Zamia loddigesii Miq., Tijdschr. Natuurl. gular, apex aristate, 8.4×3.7 cm at base, Gesch. Physiol. 10: 72. 1843. Type: culti- yellowish tomentose. Ptyxis inflexed. Leaves vated by Van Houtte 3374 (lectotype, here 2–3 (4) ascending to spreading, 45–96×30– designated: U). 41 cm, light-green when emerging, green to dark-green when mature; petiole 15–25 cm Zamia galeotti De Vriese, in Hoven & De Vries. long, green in young leaves, subterete, armed Tijdschr. Natuurl. Gesch. Physiol. 12: 24. 1845. with prickles up to 4 mm long; rachis Type: Mexico. Veracruz: 5 July 1983. D. W. subterete, up to 57 cm long, with few prickles Stevenson 538 (neotype, here designated: NY, fl – isoneotype: XAL). on the proximal third. Lea ets 12 23 pairs, Zamia leiboldii Miq., Linnaea 19: 425. 1847. Zamia sessile, coriaceous, linear-lanceolate, opposite loddigesii var. leiboldii (Miquel) A. DC., Prodr. 16 to subopposite, apex acute, base attenuate, (2): 541. 1868. Type: E. Mexico in Hortum margins serrulate along distal third, subrevo- Loehrianum Lipsiae attulit Liebold, 1845, Miquel lute; articulations 0.4–0.7 cm wide; median s.n. (holotype: U). leaflets 16–26×1.8–3.1 cm. Pollen strobili 1– Zamia loddigesii var. angustifolia Regel, Bull. Soc. Nat. Moscou 30(1): 190. 1857. Type: ex horto 2 per crown, up to 6 (7) when multiple Petropolitano, 1856, Regel s.n. (holotype: LE) crowned, erect, cylindrical, 8–14 cm long, Zamia loddigesii var. obtusifolia Regel, Bull. Soc. 1.8–3.5 cm in diam, light brown tomentulose, Nat. Moscou 30(1): 190. 1857. Type: t. 186, figs apex acute; peduncle light-brown tomentose, 27–28 in Gartenflora 6: 1857. (lectotype, designat- 6 cm long, 1.2 cm in diam; pollen sporangio- ed by Stevenson & Sabato, 1986: LE). phores cuneiform, distal face hexagonal- Zamia mexicana Miquel, Prodr. syst. Cycad. 13. 1861. truncate, 0.3 cm long, fertile abaxial surface Type: Eriozamia mexicana H. Belg., 1847, Miquel – s.n. (holotype: U). with 6 8 bisporangiate synangia per lobe. – Zamia leiboldii var. angustifolia Regel, Trudy Imp. Ovulate strobili usually 1 2 per crown, erect, S.-Petersburgsk. Bot. Sada 4(4): 307. 1876. Type: ellipsoid to conical, up to 16 cm long, up to Mexico. Oaxaca: 15 Jul 1983. D. W. Stevenson 559 6 cm in diam, beige-tomentulose, apex acute; (neotype, here designated: NY; isoneotype, XAL). peduncle brown-tomentose, up to 6 cm long, Zamia leiboldii var. latifolia Regel, Trudy Imp. S. 1.6 cm in diam; megasporangiophores peltate, Petersburgsk. Bot. Sada 4(4): 307. 1876. Type: ex – Horto Petropolitano, 1875, Regel s.n. (holotype: distal face hexagonal-truncate, 0.7 1 cm high, LE). 1.9–2.6 cm wide. Seeds ovoid, sarcotesta pink Zamia lawsoniana Dyer in Hemsley, Biol. Centr.- when immature, red at maturity, 1.4–1.8 cm Amer., Bot. 3(16): 195. 1884. Type: Mexico. long, 0.8–1 cm in diam, sclerotesta smooth. Oaxaca: Fielding 209 (holotype: OX; isotype: K) Chromosome number.—2n=18 (Norstog, Zamia cycadifolia Dyer in Hemsley, Biol. Cent.- 1980; Moretti, 1990a, b). Amer., Bot. 3(16): 195. 1884, non Jacquin 1809. Diversity and genetic structure.—The av- Zamia loddigesii var. cycadifolia Schuster, Pflan- zenreich 99: 148. 1932. Type: Mexico. Bourgeau s. erage of alleles per locus is A=1.8, the n. (holotype: K; isotype: C). nomen illegit. percentage of polymorphic loci is P=66.6, Zamia sylvatica Chamberlain, Bot. Gaz. 81: 223. the expected heterozygosity is HE=0.266 1926. Type: Mexico, Oaxaca, Tuxtepec, Sep 1910, and the genetic differentiation between the C. J. Chamberlain s.n. (lectotype, designated by two populations currently under study is Stevenson & Sabato, 1986: NY; isolectotype, F-3 sheets). Fst=0.179 (González-Astorga et al. unpubl. Zamia loddigesii var. angustifolia (Regel) J. Schust., data). in Engl., Pflanzenr. 4(1): 148. 1932. Type: México. Distribution and habitat.—Endemic to Veracruz: savanne bei Mundo nuevo, Karwinski Mexico and distributed widely within the 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 319 states of Tamaulipas, Hidalgo, Veracruz, Additional specimens examined.—MEXICO. Tabasco and parts of Oaxaca with a single CHIAPAS: Ocozocoautla, M. A. Pérez-Farrera 81 (CHIP, known locality in Chiapas (Fig. 6). The HEM). HIDALGO: Atlapexco, San Juan 15 (XAL),16 (XAL),17(XAL),18(XAL),19(XAL),20(XAL),21 vegetation types are evergreen tropical forest, (XAL). PUEBLA: Sarukán et al. 4632 (FCME, MEXU). tropical deciduous and sub-deciduous forests Oaxaca, Tuxtepec, J. Chamberlain s.n. (MO). TAMAULI- (sensu Rzedowski, 1978), as well as a variety PAS: R. L. Dressler 1858 (MO), Mayfiel et al. 791 of secondary succession and disturbed hab- (MEXU); Aldama, F. Nicolalde-Morejón & J. González- itats such as pastures and cornfields, as well Astorga 1585 (XAL), 1586 (XAL), 1587 (XAL), 1588 (XAL). VERACRUZ: Chavelas et al. ES-4231 (MEXU), as road-side vegetation. Dorantes et al. 964 (MEXU, MO), Dorantes et al. 1112 Etymology.—The specific epithet honors (MEXU), Lot 733 (MEXU), Medrano et al. 2725 Conrad Loddiges (1738–1826), a German (MEXU), Nevling & Gómez-Pompa 140 (MEXU), horticulturist who lived in London and Santos 353 (XAL, XALU); Acayucan, Vovides et al. 1376 (XAL), 1377 (XAL); Actopan, J. I. Calzada et al. cultivated American cycads. 6369 (MEXU, XAL), Lot 1027 (XAL), A. Vovides 754 Nomenclatural notes.—The description (XAL), 755 (XAL), 817 (XAL), 818 (XAL), 819 (XAL), of Zamia loddigesii was lectotypified by 820 (XAL), 821 (XAL), 822 (XAL), 823 (XAL), 824 Stevenson & Sabato (1986). However, it is (XAL); Alto Lucero, J. Rees 1627 (XAL), 1629 (XAL), 1630 (XAL), 1631 (XAL), 1632 (XAL), 1637 (XAL), no longer permissible to designate a descrip- Vovides 846 (XAL); Atoyac, Acevedo & Castillo- tion to serve as a type. Moreover, since then Campos 240 (XAL); Cotaxtla, González 82 (MEXU); a specimen, Van Houtte 3374 at U, was Chicontepec, J. Rees 1615 (MEXU, XAL); Choapas, found that was sent to Miquel by Van Vovides et al. 1373, 1374, 1735 (XAL); Coatepec, J. Houtte. This specimen predates the publica- Rees & Vovides 1670 (XAL); Coatzacoalcos, Castillo & Acosta 16220 (XAL); Colipa, J. Rees 1634, 1635 (XAL); tion of Z. loddigesii Miq. and matches the Cosautlan, Vovides 35 (XAL); Emiliano Zapata, J. Rees description. Thus, we are designating it the 1763 (XAL), Stevenson et al. 538 (MEXU, NY), M. lectotype. Vázquez-Torres 8071 (CIB); Huejultla, Stresser 291 Distinguishing features.—Zamia loddigesii (MEXU); Hueyapan de Ocampo, Gómez-Pompa 4424 (XAL), Vovides et al. 1378 (XAL), 1379 (XAL), 1380 in contrast to Z. paucijuga, has been widely (XAL); Jalcomulco, Castillo & Zamora C. 7542 (XAL), collected along the Gulf of Mexico seaboard Castillo & Gómez-Pompa 2588 (XAL), Castillo-Campos and on the Yucatan peninsula since the 19th 2727 (XAL); Mecayapan, Castillo et al. 13681 (XAL), century, largely by British and Russian 13792 (XAL), 13843 (XAL), 13861 (XAL),13865(XAL), botanists, and recently by Mexican and North 13866 (XAL), A. Calatayud & J. Martínez-Gándara 124 (CIB); Moloacan, J. Rees 1656 (XAL); Puente Nacional, American researchers. The high morphologi- Castillo & Medina 4261 (XAL); Papantla, R. Cuevas et al. cal variation presented by this species has 4652 (ZEA); Soteapan, Leonati 42 (MEXU); Soteapan, A. resulted in the publication of 10 affine names Calatayud & J. Benítez R 285 (CIB), M. A. Santos R. 352 (Hill et al., 2007) that at times, has been a (CIB); Tampico Alto, Ortega & Ortega O. 2437 (XAL); Tezonapa, Robles 370 (XAL); Totutla, J. Rees 1661 (XAL); basis for the separation of natural popula- Yecuatla, J. Rees 1633 (XAL). tions, i.e., that of the Yucatan peninsula (formerly Z. loddigesii sensu Vovides & Zamia monticola Chamb., Bot. Gaz. 81: Olivares, 1996) that is now a separate entity 219. 1926. Type: cultivated from a single Z. polymorpha (Stevenson et al., 1995– seed collected opposite the crater of Nao- 1996b), a decision based on both vegetative linco, near Xalapa, Veracruz, Mexico, Oct and reproductive characters that differ from Z. 1925, C. J. Chamberlain s.n. (holotype: loddigesii mainly on pollen and ovulate MO; isotype: NY). strobilus shape and indument color. Zamia loddigesii is similar to Z. polymorpha in leaf morphology; however, there are Stem epigeal, up to 30 cm tall, 18–20 cm in differences in the reproductive structures. diam. Cataphylls base triangular, apex linear- Pollen cones of Z. loddigesii are beige in lanceolate, 3–6×1–2 cm wide at base. Leaves color with a blunt apex whereas those of Z. 5–20, 100–200 cm long, erect to slightly polymorpha are dark reddish-brown or ma- curved; petiole 50–75 cm long, terete, armed roon with an acute apex. vulate cones of Z. with stout prickles in lower half; rachis terete, loddigesii are cylindrical and beige in color up to 100 cm long, with few prickles along and those of Z. polymorpha are ovoid and the lower half. Leaflets 30–40 pairs, sessile, dark maroon in color. chartaceous to papyraceous, linear-lanceolate, 320 BRITTONIA [VOL 61 opposite to subopposite, subfalcate near the 36×4 cm. Pollen strobili usually 1–3, erect, base, apex long-acuminate and often strongly cylindrical, up to 27.5 cm long, up to 4 cm in curved, base attenuate, margins serrulate only diam, light brown to tan, apex acute; pedun- near the base, subrevolute; articulations cle brown to tan, tomentose, up to 8.5 cm 0.4–0.7 cm wide; the median leaflets 25– long, up to 1.6 cm in diam; pollen sporan- 30×4–6cm.Pollen strobili usually 2–6, giophore cuneiform, distal face hexagonal erect, cylindrical to oblong, 12–20 cm long truncate, fertile abaxial surface with up to 9 and 2–4 cm in diam, cream to light brown, bisporangiate sori per lobe. Ovulate strobili apex acute; peduncle light brown tomentose, usually solitary, erect, cylindrical, up to 10–20 cm long; pollen sporangiophores cu- 43 cm long, 12 cm in diam, brown to neiform, distal face hexagonal, 0.4 cm long, greenish, tomentulose, apex conical; peduncle fertile abaxial surface 2-lobed with 10–16 densely brown tomentose, up to 5 cm long, bisporangiate synangia per lobe. Ovulate up to 2.5 cm in diam, distal face hexagonal- strobili unknown. truncate, 2.9 cm high, 4.7 cm wide. Seeds Chromosome number.—Unknown ovoid, sarcotesta red at maturity, up to 3 cm Etymology.—The specific epithet alludes to long, up to 2 cm in diam, sclerotesta smooth. its mountainous habitat type, originally Chromosome number.—Unknown. thought to be near Naolinco near the city of Distribution and habitat.—The species Xalapa, Veracruz in Mexico. It is now known range is Honduras (Fig. 6), between 0–1300 m that this species is not known from Mexico elevations in evergreen tropical forest. and is endemic to Guatemala. Etymology.—The specific epithet is in Distribution and habitat.—Endemic to honor of Onán Reyes, a Honduran biologist. Guatemala on rocky outcrops in primary and Distinguishing features.—Stems arbores- secondary evergreen tropical rainforest (Fig. 6). cent up to 2 m tall, leaflets coriaceous, long Distinguishing features.—Characterized by acuminate apically, with margin serrulate. its consistently chartaceous to papyraceous Nomenclatural note.—Both Z. onanreyesii long acuminate leaflets that are strongly and Z. busselllii were published in 2008. The curved near the apex with light serrulations. dates of issue are however different. The date of issue for Z. onanreyesii is 6 September Additional specimens examined.— GUATEMALA. 2008 and the date of issue for Z. bussellii is ALTA VERAPAZ: H. Förther 2621/592 (NY). 16 October 2008. Thus, under Article 29.1 of the Interantional Code of Botanical Nomen- Zamia onanreyesii C. Nelson & G. San- clature (McNeill et al., 2007), Z. onanreyesii doval. Ceiba 49(1): 135. 2008. Type: has priority and is used here. Honduras. Cortés, 7 Jan 2008, O. Reyes 406 (holotype: TEFH). Additional specimen examined.—HONDURAS. Departamento Cortés: J. Haynes et al. 044A, 044B (TEFH). Zamia bussellii Schutzman, R. S. Adams, J. L. Haynes & Whitelock. The Cycad Newsletter 31 – (2/3), 22. 2008. Type: Honduras. Cortés, June Zamia oreillyi C. Nelson, Ceiba 46(1 2): 56. 2003, Whittington 2003/01 (holotype: FLAS). 2005. Type: Honduras. Atlántida: 8 Apr 2006, G. Sandoval et al. 1157 (holotype: Stem up to 2 m tall, up to 16 cm in diam. TEFH). (Fig. 9) Ptyxis inflexed. Leaves 3–15(−44), 60–180× 15–50 cm, erect to slightly curved, tomentu- Stem hypogeous, non-branching, up to lose when emerging; petiole 15–40 cm long, 25 cm long, up to 7.5 cm in diam. Leaves terete, sparsely to moderately armed with usually 1(2), up to 78.2 cm long, 31–35 cm prickles; rachis terete, up to 40–120 cm long, wide, ascending to descending; petiole up to with few prickles along proximal third. Leaf- 47 cm long, subterete, armed with small lets up to 30 pairs, sessile, subcoriaceous, prickles; rachis subterete, up to 35–40 cm oblong-lanceolate, opposite to subopposite, long, with few prickles along the proximal long acuminate apically, base attenuate, mar- third. Leaflets 29–31 pairs, sessile, papyra- gins serrulate along distal third, subrevolute; ceous to sub-coriaceous, linear-lanceolate, articulations yellowish; median leaflets to opposite to subopposite, imbricate, apex 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 321

FIG.9. Zamia oreillyi. A. Habit.B.Cataphyll. C–E. Leaflet variability. C. Broad and imbricate with dentate margins. D. Narrow and imbricate with dentate margins. E. Narrow and slighly imbricate with entire margins. F. Ovulate strobilus.G.Pollen strobilus. H. Microsporophyll, abaxial view. (A-E, G-H from Balick 1711, NY). acuminate, base attenuate, margins dentate to apex acuminate; peduncle light brown tomen- rarely entire along distal third, up to 0.3 cm, tose, up to 15.9 cm long, 0.2 cm in diam; subrevolute; articulations brown in young pollen sporangiophores cuneiform, distal face leaflets, 0.3–0.5 cm wide; the median leaflets truncate-hexagonal, 0.4 cm long, fertile ab- up to 16 cm long, 1 cm wide. Pollen strobili axial surface, with 2–3 bisporangiate synan- usually solitary, decumbent, cylindrical, up to gia per lobe. Ovulate strobili unknown. 2.5 cm long and 1 cm in diam, light brown, Chromosome number.—Unknown 322 BRITTONIA [VOL 61

Etymology.—The specific epithet is in face hexagonal-truncate, 0.6–0.8 cm high, honor of Carlos Manuel O’Reilly, a Hon- 1.1–1.5 cm wide. Seeds ovoid, sarcotesta duran biologist. pink when immature, orange at maturity, 2– Distribution and habitat.—Endemic to 2.8 cm long, 1.5–1.7 cm in diam, sclerotesta Honduras, between 0–200 m in evergreen smooth. tropical rainforest (Fig. 6). Chromosome number.—2n=23, 34, 25, 26, Distinguishing features.—Characterized by 27, 28 (Moretti & Sabato, 1984). strongly imbricate linear-lanceolate to Distribution and habitat.—Endemic to oblong leaflets with dentate margins along Mexico. Known from the states of Nayarit, distal third; pollen strobili usually solitary, Jalisco, Colima, Michoacan, Guerrero, and decumbent, with fertile section up to 2.9 cm Oaxaca (Fig. 6). Found in varied habitats long and decumbent peduncle up to 15.9 cm from dry open woodlands to understory long. evergreen tropical forest. Etymology.—The specific epithet alludes to Additional specimen examined.—HONDURAS. few leaflet pairs per leaf. ATLÁNTIDA. Balick 1711 (NY, TEFH). Distinguishing features.—Zamia paucijuga is highly variable morphologically and in Zamia paucijuga Wieland, American Fossil chromosome number and karyotype (Moretti, Cycads 2: 212. 1916. Type: Fig. 86 in 1990a, b). This may represent more than one American Fossil Cycads 2: 212.1916. entity under the concept of Z. paucijuga (lectotype, designated by Stevenson & sensu stricto Wieland (1916). This species Sabato, 1986: Fig. 86). shares a number of characteristics with Z. loddigesii, being small plants with under- Stem hypogeous, branching dichotomously ground contractile stems and having coriaceous with age, 15–27 cm long, 8–13 cm in diam. leaflets with marginal teeth. Nevertheless, it Cataphylls coriaceous, persistent, base trian- differs from Z. loddigesii in having highly gular, apex aristate, 4.5×3.4 cm at base, coriaceous leaflets with longer marginal teeth, brown tomentose. Ptyxis inflexed. Leaves 2– and seeds with an orange sarcotesta at maturity 3, ascending to descending 41–95×29–36 cm as contrasted to the red sarcotesta of Z. wide, brownish when emerging; petiole 10.2– paucijuga. Zamia paucijuga occurs along the 32 cm long, green in young leaves, subterete, Pacific seaboard of Mexico whereas Z. loddi- armed with prickles up to 4 mm long; rachis gesii is known generally from the Gulf of subterete, up to 56 cm long, with few prickles Mexico seaboard. along the proximal third. Leaflets 5–28 pairs sessile, coriaceous, lanceolate, opposite to Additional specimens examined.—MEXICO. subopposite, apex acute, base attenuate, mar- COLIMA: McVaugh 15768 (FCME, MEXU). GUERRERO: Acapulco, N. Noriega-Acosta 463, 546 (FCME), W. gins serrulate to slightly dentate along distal Thomas & J. L. Contreras 3744 (FCME); Chilpancingo, third, subrevolute; articulations brownish in Kruse 902 (FCME, MEXU), R. M. Fonseca 1210 young leaflets, 0.4–0.6 cm wide; the median (FCME), F. Nicolalde-Morejón et al. 1566, 1567, 1568, leaflets 14–19×2.3–3.4 cm. Pollen strobili 1569 (XAL), José Azueta, Vovides et al. 1426 (XAL); usually 1–2, erect, cylindrical, 6.3–11 cm Petatlán, Vovides et al. 1427, 1428, 1429, 1430, 1431, – 1432, 1433, 1434 (XAL); Unión de Isidro Montes De long, 2.1 2.6 cm in diam, light brown Oca, Vovides et al. 1416, 1417, 1418, 1420, 1421 (XAL); tomentulose, apex acute; peduncle light- La Unión, G. Lozano-Valdez 331 (FCME), J. Jiménez brown tomentose, 6.3 cm long, 1.2 cm in 331 (FCME). JALISCO: Gómez-Pompa 4876 (MEXU); El diam; pollen sporangiophores cuneiform, dis- Arenal, Castillo et al. 9822 (XAL); Cabo Corrientes, Castillo et al. 10147, 11733, 10280, 10466 (XAL), J. tal face hexagonal-truncate, 0.3 cm long, Ceja et al 1437 (UAMIZ), J. Ceja et al. 1470 (UAMIZ), fertile abaxial surface with 6–8 bisporangiate F. Nicolalde-Morejón et al. 1524, 1525 (XAL); Cihuat- synangia per lobe. Ovulate strobili usually lán, J. Borocio R. s.n. (ZEA); Cuautitlán, Cochrane et al. solitary, erect, ellipsoid to cylindrical, 8.1 cm 10886 (IBUG, WIS, ZEA), R. Cuevas et al 7025 (ZEA), long, 5.2 cm in diam, brown-yellowish, L. Guzmán & J. Santana M. 745, 947 (ZEA), F. Nicolalde-Morejón et al. 1528, 1529 (XAL), Pérez de tomentulose, apex apiculate; peduncle dense- la Rosa 1039 (FCME, IBUG, MEXU), 1040 (FCME, ly brown tomentose, 3.9 cm long, 1.3 cm in IBUG, XAL), 1041 (CIB), 1518 (IBUG), Ramírez 425 diam; megasporangiophores peltate, distal (IBUG), M. Rosales & L. Cruz 75 (ZEA), J. Santana M. 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 323 et al. 5296 (ZEA); La Huerta, Cuevas et al. 4861 (IBUG, 0.4 cm long, fertile abaxial surface with 4–5 ZEA); San Sebastián, F. Nicolalde-Morejón et al. 1422 bisporangiate synangia per lobe. Ovulate (XAL), 1423 (XAL), 1424 (XAL), 1425 (XAL), 1426 (XAL), 1427 (XAL), Pérez de la Rosa 1084 (IBUG, strobili usually solitary, erect, cylindrical to FCME, MEXU) 1097, 1098 (IBUG); Tuito, A. Flores et ovoid, 8.7–16.3 cm long, 5–8.3 cm in diam, al. 614 (UAMIZ), F. Nicolalde-Morejón et al. 1429 dark-brown tomentulose, apex acute; peduncle (XAL), Pérez de la Rosa 1438, 1439 (IBUG); Vallarta, – fi brown tomentose, 4 7.5 cm long, 1.1 cm in Pérez de la Rosa 1413, 1415 (IBUG); Villa Puri cación, diam; megasporangiophores peltate, distal face Pérez de la Rosa 1885. (IBUG). NAYARIT: Gentry & Gilly 10496 (MEXU), McVaugh 19211 (FCME, MEXU), hexagonal-truncate, 0.8 cm high, 1.8–2.1 cm Vovides et al. 1487 (XAL), 1488 (XAL), 1489 (XAL), wide. Seeds ovoid, sarcotesta pink when 1490 (XAL), 1491 (XAL), 1493 (XAL); Compostela, F. immature, red at maturity, 1.4–2.1 cm long, Nicolalde-Morejón et al. 1521 (XAL), 1522 (XAL), 0.5–0.9 cm in diam, sclerotesta smooth. 1523 (XAL); Tepic, R. Dressler 1026 (MO), H. S. Gentry — & C. I. Gilly 10498 (FCME). Oaxaca: Miranda 4205 Chromosome number. 2n=17, 22, 23, 24, (MEXU), F. Nicolalde-Morejón et al. 1465 (XAL), 1466 25, 26, 27, 28 (Stevenson et al., 1995–1996b, (XAL), 1467 (XAL),1468(XAL), 1469 (XAL),1470 b; Vovides & Olivares, 1996). (XAL), 1471 (XAL),1472(XAL), 1473 (XAL); Pochutla, Distribution and habitat.—This species is Schutzman 543 (XAL),544(XAL), 545 (XAL),546(XAL), 547 (XAL), 548 (XAL), 550 (XAL),551(XAL),552(XAL), known from Belize, Guatemala and Mexico 553 (XAL), 554 (XAL), 555 (XAL),556(XAL),557(XAL), from 0–200 m elevation. In Mexico, its range 558 (XAL), 560 (XAL), 561 (XAL),562(XAL),563(XAL), includes the states of Quintana Roo, Yucatán, 565 (XAL), A. Nava-Zafra & J. Pascual 35 (SERO, FCME); Campeche, Tabasco and Chiapas (Fig. 6). Puerto Escondido, J. Rees 1603 (MO, XAL), Walters sn — fi – Etymology. The speci c epithet alludes to (FTG accession 7 14, XAL); San Gabriel Mixtepec, F. fl Nicolalde-Morejón et al. 1474 (XAL); San Pedro Pochulta, J. the extreme variation in leaf and lea et mor- Lomelí et al. 2967 (MEXU). phology presented by this species (Stevenson et al., 1995–1996b). Zamia polymorpha D.W. Stev., A. Moretti Distinguishing features.—Zamia polymor- & Vázq. Torres, Delpinoa n.s. 37–38: 4. pha shares many morphological attributes 1995–1996 (issued 1998). Type: Belize. with Z. loddigesii of the Gulf of Mexico Cayo: 22 Jan 1989, D. W. Stevenson et al. drainage. However, there are clear differences 1119 (holotype: NY; isotypes: BRH, FTG, in the pollen and ovulate reproductive struc- MO, NY, U). (Fig. 10) tures. In Z. loddigesii, the pollen strobili are beige in color with an acute apex and the Stem hypogeous, branching dichotomously ovulate strobili are beige and cylindrical with age, up to 32 cm long, up to 14 cm in whereas in Z. polymorpha the pollen strobili diam. Cataphylls chartaceous, persistent, base are maroon with an acuminate apex and the triangular, apex aristate, 3–6.4×1.3–2.6 cm at ovulate strobili are dark-maroon and ovoid. base, brown tomentose. Ptyxis inflexed. Leaves 2–3(4), ascending, 30–105×29– Additional specimens examined.—MEXICO. 45 cm, brown when emerging, green when CAMPECHE: Hernández et al. ES-184 (MEXU), Schutz- – man 502 (XAL), 503 (XAL),504(XAL), 505 (XAL), 506 mature; petiole 10.2 95.3 cm long, greenish in (XAL),507(XAL),508(XAL),509(XAL); Benito young leaves, subterete, armed with prickles Juárez, Vovides et al. 1312 (XAL), 1313 (XAL), 1314 up to 4 mm long; rachis subterete, up to 67 cm (XAL), 1315 (XAL), 1316 (XAL),1317(XAL); Calakmul, long, with few prickles along the proximal Madrid et al. 736 (MEXU), Martínez 30420-A (MEXU); third. Leaflets 3–12 pairs, sessile, coriaceous, Ciudad del Carmen, Flores et al. 9586 (XAL); Champoton, Chan 3719 (CICY, XAL), Vovides 853 (XAL), 854 (XAL), lanceolate to oblanceolate, opposite to sub- 855 (XAL),1326(XAL), 1328 (XAL),1329(XAL), opposite, apex acute, base attenuate, margins 1330 (XAL), 1331 (XAL), 1332 (XAL), 1333 (XAL), 1334 serrulate along upper third, subrevolute; artic- (XAL),1335(XAL),1336(XAL),1337(XAL),1338 ulations brown when young, green when (XAL),1339(XAL),1527(XAL); Hopelchen, Ortega & mature, 0.4–0.8 cm wide; the median leaflets Ucán 1562 (UADY, XAL), Ucán et al. 7293 (UADY, – – – XAL), 7307 (UADY, XAL), 7398 (UADY, XAL). 17 35×2 3.5 cm. Pollen strobili usually 1 2, CHIAPAS: Palenque, Aguilar & Aguilar 1355 (MEXU), F. erect, conical, 6.5–7.3 cm long, 1.1–1.4 cm in Nicolalde-Morejón & N. Martínez 1419 (XAL), Schutzman diam, light to dark-brown tomentulose, apex 508 (XAL), Walters s.n. (FTG accession 13-2, XAL); acute; peduncle light brown tomentose, 6.8 cm Ocosingo, Walters s.n. (FTG accession 17-2, XAL). QUINTANA ROO: Cabrera et al. 2574 (MEXU), Davidse et long, 1.2 cm in diam; pollen sporangiophores al. 20075 (MEXU, MO), Téllez 1415 (MEXU), Trejo 225 cuneiform, distal face hexagonal-truncate, (CICY, MEXU); Adolfo Huerta, Álvarez et al. 9495 324 BRITTONIA [VOL 61

FIG. 10. Zamia polymorpha. A. Habit (Stevenson et al. 1118, NY). B. Leaﬂets (from the holotype). C. Ovulate strobilus. D. Pollen strobilus. E. Cataphyll.

(MEXU); Chetumal, Vovides 852 (XAL), Flores & Burgos Tzucacab, Vovides et al. 1303 (XAL),1306(XAL),1307 9635 (XAL),9643(XAL), Othon P. Blanco, Vovides et al. (XAL), 1308 (XAL), Flores & Burgos 9642 (XAL); 1318 (XAL),1319(XAL),1320(XAL),1321(XAL),1322 Valladolid, Vovides 856, 857 (XAL), Vovides et al. 867 (XAL),1323(XAL),1324(XAL),1325(XAL). TABASCO: (XAL),868(XAL),869(XAL) 871 (XAL),872(XAL), Balancan, Matuda 3117 (MEXU), Méndez 214 (XAL), 873 (XAL),874(XAL),875(XAL),881(XAL),877 Novelo 169 (MEXU, XAL), Puig 788 (MEXU). Macu- (XAL), 870 (MEXU, XAL),876(MEXU, XAL),877 spana, Vovides et al. 1344, 1345 (XAL). Yucatán, G. F. (MEXU, XAL),878(MEXU, XAL),880(MEXU, XAL); Gaumer 2430 (MO), Lundell & Gentle 827 (MEXU), May Yaxcaba, Vovides et al. 1309 (XAL),1310(XAL), Vovides 743 (CICY, MEXU); Tekon, Enríquez 94 (MEXU); 1311 (XAL). 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 325

GUATEMALA. PETEN: W. E. Harmon & J. A. Etymology.—The specific epithet alludes to Fuentes 5735 (MO). the bright grass-green leaflets. BELIZE. BELIZE DISTRICT: Estrada 234 (CICY), D. Distinguishing features.—Plants with sub- L. Spellman 1548 (MO), C. Whitefoord 2603 (MO). terranean or epigeal stems, distinctly serrulate CAYO DISTRICT: D. W. Stevenson et al. 1121 (FTG, MO, fl fl NY, U), 1122 (FTG, MO, NY, U), M. J. Balick et al. lea et margins and bright-green lea ets; 1803 (MO, NY), M. J. Balick et al. 2058 (NY), T. B. ovulate strobili ovate, green and glabrous Croat 23732 (MO), D. R. Hotel & L. Thomas 1130 when mature. (NY), J. S. Huston s.n. (MO), R. W. Long 3238 (MO), J. A. Ratter 5195 (MO), D. L. Spellman 1974 (MO), D. L. Additional specimens examined.—BELIZE. Spellman & W. W. Newey 1962 (K), J. R. Wiley 333 TOLEDO: G. Davidse & A. E. Brant 32179 (MO), (MO). Orange Walk, G. Davidse & A. E. Brant 32768 (MO). Stann Creek, R. L. Walter 1099 (MO). Sin datos 32232 (MO). (K). Zamia purpurea Vovides, J.D. Rees & Vázq. Zamia prasina W. Bull, Retail List: 20. Torres, Flora de Veracruz 26: 28. 1983. 1881. Type: cultivated from Br. Honduras, Type: Mexico. Veracruz: 30 Jan 1982, W. Bull s.n. (holotype: K). Vovides 734 (holotype: XAL). (Fig. 11)

Stem hypogeous to epigeous, rarely Stem hypogeous, dichotomously branching branching. Cataphylls chartaceous, persistent, with age, up to 30 cm long, 4–6 cm in diam. base triangular, apex aristate, 3–4.5×1.2– Cataphylls membranaceous, deciduous, base 2.7 cm at base, brown tomentose. Ptyxis triangular, apex acuminate, 5.×1.8 cm at inflexed. Leaves 2–4(6), 57–100×25–35 cm, base, reddish-brown tomentose. Ptyxis in- ascending to spreading, brown when emerg- flexed. Leaves 1–6, ascending to spreading, ing; petiole 12–30 cm long, brown-greenish 34–90×32–38 cm, reddish-brown when young leaves, subterete, sparsely to densely emerging, turning green to dark-green at armed with prickles up to 4 mm long; rachis maturity; petiole 16–29 cm long, blackish in subterete, up to 70 cm long, with few prickles young leaves, subterete, armed with simple along the proximal third. Leaflets 12–18 prickles up to 4 mm long; rachis subterete, pairs, sessile, coriaceous, oblong to oblanceo- 17–45 cm long, with few prickles along the late, opposite to subopposite, apex acute to proximal third. Leaflets 3–4(6) pairs, sessile, acuminate, base cuneate, margins serrate to coriaceous, elliptic to lanceolate, opposite to denticulate in the upper two third, subrevo- subopposite, veins highly prominent on ad- lute; articulations brown-yellowish in young axial surface, though relatively inconspicuous leaflets, 0.3–0.6 cm wide; the median leaflets veins have been reported on some individu- 15–20×4–6 cm. Pollen strobili usually 1–2, als, apex acute, base attenuate, margins erect, cylindrical to ovoid, up to 6–10 cm dentate along upper third, subrevolute; artic- long and 2–4 cm in diam, light brown, apex ulations brown in young leaflets, 0.4–0.8 cm acute; peduncle densely light brown tomen- wide; the median leaflets 6–27×2–8.1 cm. tose, 2–4 cm long, 1.5 cm in diam. Ovulate Pollen strobili usually 1–2, erect, conical, 2– strobili usually solitary, erect, cylindrical, 10– 4.3 cm long, 0.5–1.1 cm in diam, light-brown 15 cm long, 5–7 cm in diam, green, glabrous tomentulose, apex acute; peduncle light- when mature, apex acute; peduncle brown- brown tomentose, 2–3.5 cm long, 0.7– greenish tomentose, 3.5 cm long, 1.5 cm in 0.9 cm in diam; pollen sporangiophores diam; megasporangiophores distal face hex- cuneiform peltate, distal hexagonal face and agonal-truncate, 1–1.4 cm high, 1.1–1.8 cm truncate to scutiform, 0.25 cm long, fertile wide. Seeds ovoid, sarcotesta light red when abaxial surface with 2 bisporangiate synangia immature, red at maturity, 1.5–2 cm long, per lobe. Ovulate strobili usually solitary, 0.5–0.8 cm in diam, sclerotesta smooth. erect, conical, 6–9 cm long, 3–4.5 cm in Chromosome number.—Not known. diam, purplish-brown tomentulose when im- Distribution and habitat.—Endemic to mature turning dark-purple glabrescent when Belize (Fig. 6) on rocky outcrops between mature, apex acute; peduncle densely dark- 100–200 m elevation in evergreen tropical brown tomentose, 2.9 cm long, 1.6 cm in rainforest. diam, distal face hexagonal-scutiform, 0.9– 326 BRITTONIA [VOL 61

FIG.11. Zamia purpurea. A. Habit. B. Pollen strobilus. C. Microsporophyll, abaxial view. D. Ovulate strobilus. E. Ovulate sporangiophores. F. Seed. (From Rees1 654, XAL.) 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 327

1.2 cm high, 1.6–2.1 cm wide. Seeds ovoid, along distal third, subrevolute; the median leaf- sarcotesta pink when immature, red at matu- lets 16–31×2–3cm.Pollen strobili usually 2, rity, 0.8–1.1 cm long, 0.6–0.8 cm in diam, erect, cylindrical, 11.2 cm long, 2.6 cm in diam, sclerotesta smooth. brown-reddish tomentulose, apex apiculate; pe- Chromosome number.—2n=16 (Vovides, duncle light-brown tomentose, 16.7 cm long, 1983) 1.2 cm in diam; pollen sporangiophores cunei- Diversity and genetic structure.—The form, distal face hexagonal truncate, 0.8 cm average of alleles per locus is A=2.10, the long, fertile abaxial surface with 2–3 bisporan- percentage of polymorphic loci is P=100, giate synangia per lobe. Ovulate strobili usually the expected heterozygosity is HE=0.481 and solitary, erect, ellipsoid to cylindrical, 12 cm the genetic differentiation between the two long, 4.5 cm in diam, brown-yellowish, tomen- populations currently under study is Fst= tulose, apex long-acuminate; peduncle densely 0.037 (González-Astorga et al. unpubl. data). brown tomentose, 1.5 cm long; megasporangio- Distribution and habitat.—Zamia pur- phores peltate, distal face hexagonal-truncate, purea is endemic to Mexico from the Río 2–2.5 cm high, 1.8–2cmwide.Seeds ovoid, Uxpanapa drainage system within the states sarcotesta white when immature, 1.2–1.8 cm of Veracruz and Oaxaca (Fig. 5) between 50– long, 0.5–0.7 cm in diam, sclerotesta smooth. 200 m in evergreen tropical forest (sensu Chromosome number.—Unknown Rzedowski, 1978) classification. Distribution and habitat.—Endemic to Etymology.—The specific epithet alludes to Honduras (Fig. 6), between 200–350 m in the dark purple color of the ovulate strobili. evergreen tropical forest. Distinguishing features.—Characterized by Etymology.—The specific epithet honors the prominent leaflet veins giving the coria- Germán Sandoval, biologist of the Universidad ceous leaflets a channeled appearance in Nacional Autonoma de Honduras (Nelson, contrast to the rest of its congeners in 2005). Mesoamerica, and the dark purple color of Distinguishing features.—This species is the ripe ovulate strobili. characterized by glabrous, sub-coriaceous, lanceolate, falcate leaflets; cylindric, ovulate Additional specimens examined.—MEXICO. strobili with a strongly acuminate apex; and OAXACA: Santa María Chimalapa, S. H. Salas M. 982 seeds with a white sclerotesta. (SERO), Sánchez et al. 40 (B, MEXU); Santa María Lachixio, Cerón et al. 266 (XAL); San Juan Guichicovi, F. — Nicolalde-Morejón & J. Torres 1503 (XAL),1404(XAL), Additional specimens examined. HONDURAS. M. Vázquez-Torres et al. 1470 (MO, XAL), Walters s.n. ATLÁNTIDA: J. Haynes et al. 37 (TEFH), G. Sandoval (FTG accession 10–1, XAL). VERACRUZ: M. Vázquez- et al. 1155 (TEFH), 1156 (TEFH). Torres 4038 (CIB); Hidalgotitlán, Calzada 8374 (XAL), M. Vázquez-Torres et al. 224 (MO); Jesús Carranza, A. Zamia soconuscensis Schutzman, Vovides & González-Christen s.n. (CIB), F. Nicolalde-Morejón & J. Dehgan, Bot. Gaz. 149(3): 347. 1988. Type: Torres 1502 (XAL), M. Vázquez-Torres et al. 2373 (CIB), M. Vázquez-Torres et al. V-2532 (CHAPA, CIB, XAL). Mexico. Chiapas: Feb 1939, Matuda 2659 (holotype: F; isotypes: CR, MEXU, MICH). Zamia sandovalii C. Nelson, Ceiba 46(1–2): 55.. 2005. Type: Honduras. Atlántida: Jan Stem epigeal, erect to decumbent in adult 2006, G. Sandoval et al. 1154 (holotype: plants, branching dichotomously with age, TEFH) 30–65 cm long, 10–31.5 cm in diam. Cata- phylls chartaceous, persistent, base triangular, Stem hypogeous, non-branching, 15.7 cm apex aristate, 7.1×2.6 cm at base, reddish- long, 10.1 cm in diam. Cataphylls persistent, brown tomentose. Ptyxis inflexed to erect. base triangular. Leaves 1–3, ascending to Leaves 3–15 or more per apex, 120–190×45– descending up to 210×0.55 cm; petiole 68 cm 62 cm, ascending, distal portion descending long, subterete, armed with small prickles; to spreading, brown when emerging turning rachis subterete, up to 140 cm long, unarmed. green at maturity; petiole 38–72 cm long, Leaflets 68 pairs sessile, sub-coriaceous, lance- green-yellowish in young leaves, terete, olate, opposite to subopposite, falcate, apex armed with prickles up to 5 mm long; rachis acuminate, base attenuate, margins serrulate subterete, up to 84 cm long, with few prickles 328 BRITTONIA [VOL 61 along the proximal third. Leaflets 41–52 (MEXU),2656(MEXU); Acacoyagua, García 149 pairs, sessile, coriaceous, linear-lanceolate, (CHIP, MEXU), M. A. Pérez-Farrera 141 (CIB, HEM, MEXU). alternate to subopposite, subfalcate, apex acute, base attenuate; margins entire, subrevolute; articulations brown in young leaflets, Zamia spartea A. DC., Prodr. 16 (2): 539. – fl – 1868. Zamia loddigesii var. spartea (A. 0.4 0.8 cm wide; the median lea ets 12 35× fl 0.6–1.5 cm. Pollen strobili usually 1–3 per DC.) Schuster, P anzenr. 99: 148. 1932. apex, erect, cylindrical to conical, 9–15 cm Type: Mexico. Oaxaca: prope Acayucam, long, 1.2–2.4 cm in diam, dark-brown tomen- Verapa, Chimalapi, 1832, Alaman s.n. tulose, apex apiculate; peduncle light-brown (holotype: G-DC). (Fig. 12). tomentose, up 7.2 cm long, 1.2 cm in diam; pollen sporangiophores cuneiform, distal face Stem hypogeous, branching dichotomously hexagonal-truncate, 0.45 cm long, fertile with age, 5–40 cm long, 5–8 cm in diam. abaxial surface with 5 bisporangiate synangia Cataphylls chartaceous, persistent, base trian- per lobe. Ovulate strobili usually solitary, gular, apex aristate, 6×1.4 cm at base, erect, cylindrical, 12–15 cm long, 6.1–7.3 cm yellowish tomentose. Ptyxis inflexed. Leaves in diam, dark-brown to reddish, tomentulose, 2–5(8) per crown, 35–60×38–52 cm, ascend- apex aristate; peduncle brown puberulent, ing to gracile, reddish-brown when emerging, 2.1 cm long, 1.2 cm in diam; megasporan- turning green at maturity; petiole 12–21 cm giophores peltate, distal face hexagonal- long, green-yellowish in young leaves, sub- truncate, 0.7–0.9 cm high, 1.6–1.8 cm wide. terete, heavily armed with straight to some- Seeds ovoid to angular, sarcotesta white when times bifurcate prickles up to 4 mm long; immature turning salmon-pink when mature, rachis subterete, up to 42 cm long, with few sclerotesta light-beige, smooth with 6–8 light prickles along the proximal third. Leaflets furrows running longitudinally and some- 15–27 pairs sessile, coriaceous, linear, alter- times dichotomizing, 2.1–2.6 cm long, 1.4– nate to subopposite, apex acute, base attenu- 1.9 cm diam. ate; margins serrulate along extreme distal Chromosome number.—2n=16 (Schutzman portion, subrevolute; articulations light- et al., 1988). orange when young, turning yellowish with Distribution and habitat.—Endemic to age, 0.3–0.4 cm wide; the median leaflets 20– Chiapas, Mexico, between 900–1400 m in 35×0.3–0.6 cm. Pollen strobili usually 2–3, the Soconusco mountain range of southern erect, cylindrical, 6.5–8.5 cm long, 1.4– Chiapas. It inhabits the understory herbaceous 1.9 cm in diam, yellowish-beige tomentulose, layer of the transition zone between evergreen apex acute; peduncle densely light-brown tropical forest and cloud forest (Fig. 5). tomentose, 6–8 cm long, 0.9–1.1 cm in diam; Etymology.—The specific epithet alludes to pollen sporangiophores cuneiform, distal face the Sierra del Soconusco mountain range also hexagonal-truncate, 0.3 cm long, fertile ab- known as the Sierra Madre de Chiapas, being axial surface with 10–14 bisporangiate syn- the region where this species is native angia per lobe. Ovulate strobili usually (Schutzman et al., 1988). solitary, erect, cylindrical to oval-cylindrical, Distinguishing features.—Zamia soconus- 9–12 cm long, 4.2–4.8 cm in diam, brown censis is the only species of the genus in tomentulose, apex acute; peduncle densely Mexico that approaches an arborescent habit brown tomentose, 3.4–3.8 cm long, 0.8– with leaves that can reach almost two meters 1.1 cm in diam; megasporangiophores peltate, long that gracefully arch toward the terminal distal face hexagonal-truncate, 0.8–1.1 cm portion. The linear-lanceolate leaflets have high, 1–1.3 cm wide. Seeds ovoid, sarcotesta totally entire margins; the only other Mexican pink when immature, red at maturity, 1.2– congener with entire margins is Z. inermis. 1.6 cm long, 0.7–0.9 cm in diam, sclerotesta Ovulate strobili are short-pedunculate and sol- smooth. itary with a dark-brown velvety tomentulum. Chromosome number.—2n=18 (Vovides, 1983; Moretti, 1990a). Additional specimens examined.—MEXICO. Distribution and habitat.—Endemic to CHIAPAS: Matuda 2087 (MEXU), 2535 (MEXU), 2590 Oaxaca, Mexico. Known in southern areas of 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 329

FIG. 12. Zamia spartea. A. Habit. B. Leaflet. C. Pollen strobilus. D–E. Microsporophyll, abaxial and adaxial view. F–G. Petiole and cataphyll. H. Ovulate strobilus and peduncle. I. Ovulate sporangiophore. J. Ovulate sporangiophores, distal end truncate hexagonal. K. Seed with sarcotesta. L–N. Seeds. 330 BRITTONIA [VOL 61 the Isthmus of Tehuantepec (Fig. 5), between ovoid, 8–12 cm long, 3–8 cm in diam, brown, 200–400 m elevation, associated with tropical tomentulose, apex long-apiculate; peduncle deciduous forests (sensu Rzedowski, 1978). densely brown tomentose, 2.5–4cmlong, Etymology.—The epithet is from the broom 1.3 cm in diam, distal face hexagonal-truncate, genus Spartium (Fabaceae), in reference to 0.7–1.2 cm high, 1.5–2.1 cm wide. Seeds the narrow and tapered leaflets of the cycad. ovoid, sarcotesta pink when immature, red at Distinguishing features.—Small gracile maturity, up to 3 cm long, up to 2 cm in diam, plants reaching up to 80 cm tall with very sclerotesta smooth. narrow-linear leaflets with an almost entire Chromosome number.—2n=16 (Schutzman, margin with a few very small serrulations 1989). only on the extreme distal portion. Distribution and habitat.—The species range is Honduras and Guatemala (Fig. 6), Additional specimens examined.—MEXICO. between 0–200 m in evergreen tropical forest. OAXACA: Meave del Castillo & García 2388 (MEXU); Etymology.—The specific epithet honors Matías Romero, F. Nicolalde-Morejón & J. Torres 1505 Paul C. Standley a prominent botanist of (XAL), 1506 (XAL), Schutzman 529 (XAL), 530 (XAL), fl 531 (XAL), 532 (XAL), 533 (XAL), 534 (XAL), 535 the ora of Mexico and Central America (XAL), 536 (XAL), 537 (XAL), 538 (XAL), 539 (XAL), (Schutzman, 1989). 540 (XAL), 541 (XAL), 542 (XAL), Vovides & Perales Distinguishing features.—Its falcate leaflets 600 (XAL), Walters s.n. (FTG accession 9–3, XAL); San andconspicuousmarginalteethupto4mm Juan Guichicovi, N. Antonio-Barrera 83b (CIB), Santa María Chimalapa, A. Espejo et al 6485 (UAMIZ), R. García long, and long-apiculate ovulate strobili as S. 341 (XAL, SERO), Torres 653 (XAL); San Miguel well as its cylindrical characterize this species. Chimalapa, M. Vázquez-Torres 4039 (CIB). Additional specimens examined.—GUATEMALA. Zamia standleyi Schutzman, Syst. Bot. 14 PROVINCIA IZABAL: H. Förther 10234/252 (MSB, W). (2): 214. 1989. Type: Honduras. Atlantida: HONDURAS. DEPARTAMENTO ATLÁNTIDA: Tela, V. Lanatilla Valley near Tela, Aug 1984, B. Severen 1450 (NA), Standley 53721 (F, US); Puerto Sierra, Wilson 537 (NY). DEPARTAMENTO SANTA BAR- Schutzman 449 (holotype: FLAS; isotypes: BARA: San Pedro Sula, Thieme 144 (US). Departamento ENA, FTG). Yoro, Coyoles, T. G. Yuneker et al. 8186 (F, G, GH, MO, NY). DEPARTAMENTO CORTES: Montaña Santa Ana, Stem hypogeous and tuberous, 6–14 cm Molina R. 3628 (F, GH). long, 5–9cmindiam.Cataphylls chartaceous, persistent, base triangular, apex long-aristate, Zamia tuerckheimii Donn. Sm., Bot. Gaz. to 12 cm×1.5 cm at base, reddish-brown (Crawfordsville) 35(1): 8. 1903. Type: tomentose. Ptyxis inflexed. Leaves 1–5, 20– Guatemala. Dept. Alta Verapaz: Cubilquitz, 100× to 55 cm, slightly to slightly recurved, Jul 1900, von Tuerckheim 7786 (holotype: tomentulose when emerging; petiole 35–60 cm US; isotype: K). long, terete, sparsely to heavily armed with prickles; rachis terete, up to 70 cm long, with Stem epigeal, rarely branched with age, up few prickles along proximal third. Leaflets 10– to 100 cm long, 10–12 cm in diam. Cata- 15 pairs, sessile, subcoriaceous-coriaceous, phylls chartaceous, persistent, base triangular, long-lanceolate, opposite to subopposite, re- apex aristate, 8.3×2.7 cm at base, light curved, apex acute, base attenuate, margins brown-greenish tomentose. Ptyxis inflexed to dentate along distal third, subrevolute; articu- erect. Leaves 8–15, 100–200×20–45 cm, lations dark brown when young, 0.3–0.5 cm ascending, distal portion descending to wide; median leaflets 20–45×1–4cm.Pollen spreading, green when emerging; petiole 30– strobili usually 1–3, decumbent, cylindrical, 50 cm long, green in young leaves, terete, 6–10 cm long, 1–2 cm in diam, light-brown armed with minute prickles to unarmed; tomentulose, apex acute; peduncle light-brown rachis subterete, up to 150 cm long, unarmed. tomentose, 2–4 cm long, 1.1 cm in diam; Leaflets 8–15 pairs, sessile, papyraceous, pollen sporangiophores cuneiform, distal face oblong-lanceolate, glossy, iridescent blue- hexagonal truncate, fertile abaxial surface with green, alternate to subopposite, apex abruptly 4 bisporangiate sori per lobe; Ovulate strobili acuminate, base attenuate; margins entire, sub- usually solitary, erect, cylindrical to slightly revolute; articulations green, 0.4–0.6 cm wide; 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 331 the median leaflets 14–18×4–6cmx.Pollen ole 35–177 cm long, dark-green with charac- strobili usually solitary, erect, cylindrical, 12– teristic yellow variegation; petiole subterete, 15 cm long, 2–4 cm in diam, gray-brown at heavily armed with prickles up to 5 mm long; maturity, apex acute; peduncle light-brown rachis subterete, up to 105 cm long, with few tomentose, up 6.5 cm long, 1.4 cm in diam. prickles along the proximal third. Leaflets 3– Ovulate strobili usually solitary, erect, cylindri- 10 pairs, sessile, papyraceous, elliptic, oppo- cal, 12–18 cm long, 4–8 cm in diam, brownish site to subopposite, dark-green with yellow or when young, iridescent blue-green at maturity, cream variegation, apex acute, base attenuate; apex aristate; peduncle light brown puberulent, margins dentate along distal third, subrevo- 3.4 cm long, 1.5 cm in diam; megasporangio- lute; articulations brown in young leaflets phores peltate, distal face hexagonal-truncate, turning green at maturity, 0.4–0.8 cm wide; 1.4–2cmhigh,3–3.6 cm wide. Seeds elongate- the median leaflets 12–22×3.1–8.8 cm. Pol- ovoid, sarcotesta light red when immature, red len strobili up to 6, erect, long-cylindrical, at maturity, smooth, 2.1–2.6 cm long, 1.3– 7–11 cm long, 1.9–2.5 cm in diam, yellow- 1.6 cm diam. ish-beige, apex acute; peduncle densely light- Chromosome number.—2n=16 (Moretti, brown tomentose, 3–6 cm long, 0.7–0.9 cm 1990b) in diam. Ovulate strobili 1–2 ovoid to Distribution and habitat.—Endemic to cylindrical, 12 cm long, 4.5 cm in diam, Guatemala, between 250–1000 m in the Alta gray-greenish tomentulose; megasporangio- Verapaz department mountain range. It inhab- phores peltate, distal face hexagonal-truncate, its the understory herbaceous layer of tropical 0.8–1.3 cm high, 1.7–2.1 cm wide. Seeds forest (Fig. 6). ovoid, red at maturity, 1.1–1.5 cm long, 0.7– Etymology.—The specific epithet honors 1 cm in diam, sclerotesta smooth. Hans von Tüerkheim, who collected this Chromosome number.—2n=21, 22 (Moretti species for the first time in Guatemala. et al., 1991). Distinguishing features.—The principal Diversity and genetic structure.—The distinguishing features of this species are average of alleles per locus is A=2.02, the arborescent stems up to one meter tall, percentage of polymorphic loci is P=97.3, papyraceous leaflets with entire margins and the expected heterozygosity is HE=0.355 and ovulate cylindrical strobilus with abruptly the genetic differentiation between the two acuminate apex and aristate apex, the cone populations currently under study is Fst = 0.085 becoming blue-green iridescent when mature. (González-Astorga et al. unpubl. data). Distribution and habitat.—Zamia varie- Additional specimens examined.—GUATEMALA. gata was described from plants collected in ALTA VERAPAZ: T. B. Croat 41647 (MO), H. Förther 11034 Guatemala by Warszewicz (Stevenson & (MSB, W), J. A. Steyermark 44484 (MO); Rubeltem, H. Förther 10918 (MSB, W). Sabato, 1986). In Mexico, this plant is known only from Chiapas, in lowland areas Zamia variegata Warsz., Allg. Gartenzeitung near the Montes Azules Biosphere Reserve 32: 253. 1845. Type: Mexico. Chiapas: (Fig. 5). Its habitat is evergreen tropical Lacandona, on border with Guatemala, 12 Jan rainforest (sensu Rzedowski, 1978). 1987 D. W. Stevenson 685 (neotype, here Etymology.—The specific epithet alludes to designated: NY; isoneotypes: U, XAL). the variegated nature of the leaflets, an attribute unique to this species of Zamia. Zamia muricta var. picta Miquel, Tijdschr. Wis-en Distinguishing features.—Its yellow-cream natuurk. Wet.1(4): 198–199. 1848, non Von Houtte variegated papyraceous leaflets easily distin- 1846. Zamia picta Dyer in Hemsley, Biol. Cent.-Amer., guish Zamia variegata. The variegations are in Bot. 3(16): 194. 1884. Type: ex Horto Amsterdam (Z. picta H. Belg.), Miquel s.n. (holotype, U) the form of irregular yellow blotches that are most apparent on the adaxial side of the lamina. Stem hypogeous, 9–16 cm long, 4–10.5 cm in diam. Cataphylls chartaceous, base trian- — gular, apex aristate, 4.6–7.1×2.1–2.4 at base, Additional specimens examined. MEXICO. fl Chiapas: Ocosingo, Castillo-Campos et al. 3848 yellowish tomentose. Ptyxis in exed. Leaves (XAL), 3855 (XAL), 3885 (XAL), M. Vázquez-Torres 1–2(3), 40–291×24–44 cm, ascending; peti- et al. 3924 (CIB); Margaritas, F. Nicolalde-Morejón et al. 332 BRITTONIA [VOL 61

FIG. 13. Zamia vazquezii. A. Habit. B. Leaﬂet. C. Ovulate strobilus. D. Pollen strobilus. E. Cataphyll. (From the holotype.)

1443 (XAL), 1444 (XAL), 1445 (XAL), 1446 (XAL), Zamia vazquezii D.W. Stev., Sabato, A. 1447 (XAL), 1448 (XAL), 1449 (XAL), 1450 (XAL), 1451 Moretti & De Luca, Delpinoa n.s. 37–38: (XAL), 1452 (XAL); Lacandona, Stevenson 692 (NY, – XAL). 14. 1995 1996 (issued 1998). Type: Mexico. GUATEMALA. Alta Verapaz: J. A. Steyermark Veracruz: 22 Jan 1989, M. Vázquez-Torres et 45048 (F, NY). Izabal: J. J. Castillo & D. R. Hodel 2138 al. 3990 (holotype: NY; isotypes: FTG, MO, (MO), M Véliz 6893 (BIGUA, MEXU). NY, U, CIB). (Fig. 13) 2009] NICOLALDE ET AL.: ZAMIA IN MEGA-MEXICO 333

Stem hypogeous, dichotomously branching Species dubium with age, 35 cm long, 12 cm in diam. Zamia verschaffeltii Miq., Verh. Kon. Ned. Cataphylls chartaceous, persistent, base trian- Akad. Wetensch., Afd. Natuurk. 2(4): 31. gular, apex aristate, 5.9×3.8 cm at base, 1870. Type: Mexico. “Zamia fusca latifolia brown tomentose. Ptyxis inflexed. Leaves 4– Versch.", Miquel s.n. (holotype, U). 6 to many, 35–100×16–29 cm, ascending, Zamia verschaffeltii forma latifolia Schuster, brownish when emerging, turning green at Pflanzenr. 99: 138. 1932. Type: description (lecto- maturity; petiole 21–45 cm long, terete, type, designated by Stevenson & Sabato, 1986). unarmed or rarely with prickles, rachis terete, fl – up to 65 cm long. Lea ets 14 26 pairs, Socorro is the locality mentioned by Schuster sessile, papyraceous, ovate to obpyriform, (1932)forMiquel’s(1870)sourceofZamia opposite to subopposite, apex acuminate, verschaffeltii, although no locality information base cuneate; margins with numerous serra- is given on the type specimen, which is the only tions along distal third, subrevolute, articu- specimen at U where Miquel’sherbarium lations brown in young leaflets, 0.5–0.7 cm resides (Stafleu, 1966). The original description wide; the median leaflets 7.1–14.6×2.8– by Miquel gives the source of material as “Ex 4.1 cm. Pollen strobili usually 1–2 per apex, imperio Mexicano introduxit A. Verschaffelt, erect, ovoid to ovoid-cylindrical, up to qui in Catalogis Z. fuscam latifoliam dixit” and 10.6 cm long and 2.6 cm in diam, light- makesnomentionofaspecific locality. brown tomentulose, apex acute; peduncle However, following the information given by densely light-brown tomentose, 4.5 cm long, Schuster (1932), we have conducted exhaustive 1.2 cm in diam; pollen sporangiophore distal searches over the years at two possible locali- face hexagonal-truncate. Ovulate strobili usu- ties with the name of El Socorro, one in ally solitary, erect, cylindrical to ovoid-cylin- Tabasco and the other at Ruta del Socorro in drical, up to 15 cm long, 7.3 cm in diam, gray Veracruz, It is important to note that the whole to brown tomentulose, apex apiculate; pedun- area and surrounding regions have been con- cle densely brown tomentose, 5.3 cm long, verted into vast sugar cane plantations so that 1.4 cm in diam; megasporangiophores pel- historically Zamia could have been present but tate, distal face hexagonal-truncate to scuti- would now be extirpated. We can confidently form, 1.2 cm high, 2.9 cm wide. Seeds ovoid, say that no species of Zamia were found in or sarcotesta pink when immature, orange-red to near the two localities of the name Socorro, and red at maturity, 1.6 cm long, 1.2 cm in diam, no other locality of this name was located sclerotesta smooth. Chromosome number.—2n=18 (Stevenson within the distribution range of this species complex in the study. Also, no individuals or et al., 1995–1996a). Distribution and habitat.—Endemic to populations of Zamia studied here conform to Veracruz, Mexico (Fig. 5), found between the original description of Z. verschaffeltii; fi 50–350 m in evergreen tropical forest sensu because we were unable to nd another record Rzedowski (1978) classification, on predom- of Z. verschaffeltii since its publication in 1870, inantly deep clayey soils. we believe that this species is probably extinct Etymology.—The specific epithet honors (Nicolalde-Morejón et al., 2008). It is interest- Mario Vázquez-Torres, a Mexican biologist ing that Schuster actually described a form and cycad specialist. latifolia Schuster does not cite any specimens Distinguishing features.—Zamia vazquezii of this form, but only that it is cultivated in has more leaves (up to six), longer with each “Garten Verschaffelt.” We have been unable to up to 100 cm long, and wider leaflets than Z. locate any specimens of this form that were fischeri. The two species are disjunct in seen by Schuster, and if one did exist at B it was distribution and have different chromosome destroyed. Therefore, all source material numbers, Z. vazquezii 2n = 18 and Z. fischeri remains enigmatic. 2n = 16 (Stevenson et al., 1995–1996a). Acknowledgments — Additional specimens examined. MEXICO. fi VERACRUZ: Papantla, M. Vázquez-Torres 4568 (CIB), The rst author thanks the Red Latin- Allen 1970–2141 (XAL); Tiguatlán, J. Rees 1617 (XAL). oamericana de Botánica for the award of a 334 BRITTONIA [VOL 61

Ph. D. fellowship (RLB-06-D2; Systematics Jones, K. 1998. Robertsonian fusion and centric fission Program, Instituto de Ecología, A.C., Xalapa, in karyotype evolution of higher plants. The Botan- ical Review 64: 273–289. Mexico) and the Mellon Foundation for a Marchant, C. J. 1968. Chromosome patterns and stipend for a six months residence at the New nuclear phenomena in the cycad families Stangeria- York Botanical Garden during 2002. This ceae and Zamiaceae. Chromosoma 24: 100–134. research was supported partially by CONA- McNeill, J., F. R. Barrie, H. M. Burdet, V. Demoulin, – D. L. Hawksworth, K. Marhold, D. H. Nicolson, J. CyT-SEMARNAT grant No. 2002-CO1 Prado, P. C. Silva, J. E. Skog, J. H. Wiersema & 0183 to AV and NSF Grants BSR-8607049 N. J. Turland. 2007. International Code of Botanical and EF-0629817 to DWS. The authors thank Nomenclature (Vienna Code), adopted by the Seven- Francisco Vergara Silva, Jorge González teenth International Botanical Congress. Vienna, Astorga, and Victoria Sosa for their com- Austria. July 2005. Gantner, Ruggell, Liechtenstein. Miquel, F. A. W. 1861. Prodromus systematics cycadea- ments on a previous version of this manu- rum. C. v. d. Post Jr. Utrecht, The Netherlands. script, and Pablo Carrillo-Reyes, Eduardo ———. 1869. Neiuwe bijdragen tot der kennis der Ruiz for their comments on the diagnostic Cycadeen. Vijfde gedeelte. Verslagen en medeelingen key to species of Zamia, Carlos Iglesias for van de afdeeling natuurkunde: koninkljkie akademie fi van wetenschappen. Amsterdam. ser. 2, 3(2): 196– assistance and guidance in the eld, and 206. Edmundo Saavedra for the illustrations of ———. 1870. Neiuwe bijdragen tot der kennis der Zamia spartea. We thank the Curators and Cycadeen. Zesde gedeelte.Verslagen en medeelingen staffs of the herbaria mentioned for making van de afdeeling natuurkunde: koninkljkie akademie their collections available for study, as well as van wetenschappen. Amsterdam. 2(4): 31. 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