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Dioon oaxacensis (Zamiaceae): a new cycad species from the arid central
valleys of Oaxaca (Mexico)

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 Phytotaxa 474 (1): 051–061 ISSN 1179-3155 (print edition)
https://www.mapress.com/j/pt/
Article PHYTOTAXA
Copyright © 2020 Magnolia Press ISSN 1179-3163 (online edition)

https://doi.org/10.11646/phytotaxa.474.1.5

Dioon oaxacensis (Zamiaceae): a new cycad species from the arid central valleys of
Oaxaca (Mexico)
JOSÉ SAID GUTIÉRREZ-ORTEGA1,6*, MIGUEL ANGEL PÉREZ-FARRERA2,7*, ANDREW P. VOVIDES3,8,
SILVIA H. SALAS-MORALES4,9 & JEFFREY CHEMNICK5,10
1
Department of Biology, Chiba University, Chiba 263-8522, Japan.
2
Herbario Eizi Matuda, Laboratorio de Ecología Evolutiva, Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de
Chiapas.
3
Departamento de Biología Evolutiva, Instituto de Ecología, A.C., 91070 Xalapa, Mexico.
4
Sociedad para el Estudio de los Recursos Bioìticos de Oaxaca, San Sebastiaìn Tutla, Oaxaca 71246, Mexico.
5
Ganna Walska Lotusland, Santa Barbara, CA 93108, USA.
6
josesgo@chiba-u.jp; https://orcid.org/0000-0003-4342-6215
7
perezfarreram@yahoo.com.mx; https://orcid.org/0000-0002-5329-1505
8
andrew.vovides@inecol.mx; https://orcid.org/0000-0002-3779-1374
9
sschibli@hotmail.com; https://orcid.org/0000-0002-4705-3615
10
jeffchemnick@cox.net; https://orcid.org/0000-0003-0200-6062
*Corresponding authors; these authors contributed equally to this study.

Abstract

Dioon oaxacensis sp. nov. (Zamiaceae), a new cycad species from Oaxaca, Mexico, is described. The morphological traits
of the new taxon are compared with its sister species, D. merolae. The species delimitation between the two species is
consistent with previously published genetic evidence. Dioon oaxacensis can be easily identified by its flat, stiff, straight
leaflets obliquely inserted to rachis, and by its large reproductive structures. Populations of D. oaxacensis usually occur in
dry habitats, growing on rocky hillsides, and co-habiting with plants well recognized to be adapted to aridity.

Keywords: arid zones, cycads, Mexico, Neotropical, Oaxaca

Introduction

The states of Oaxaca and Chiapas in southeastern Mexico, harbor the highest levels of biodiversity in the country
(Sánchez-Cordero 2001, García-Mendoza & Meave 2011). This has been particularly interesting for cycad taxonomists
since 77% of Zamia Linnaeus (1763:1659), 45% of Ceratozamia Brongniart (1846: 7−8), and 60% of Dioon Lindley
(1843: 59–60) species endemic to Mexico occur in either of these two states (Calonje et al. 2020). Thus, this area is
acknowledged to be one of the main centers of cycad diversification in the world (Vovides et al. 2003). The reasons
for such a great species diversity in Oaxaca and Chiapas have been attributed to the great variety of habitats where
many tropical and temperate biological groups evolved (Contreras-Medina & Luna-Vega 2007). This area contains
mountain chains, sky-islands, and valleys that have served as refugia or cradles for the maintenance or diversification
of plant communities from mesic or arid zones (Sosa et al. 2018). The contrasting conditions that meet in a relatively
narrow geographic area have been favorable for events of lineage divergence and speciation, as has been suggested for
many biological groups (Ornelas et al. 2013, Rocha-Mendez et al. 2019), including the cycad genus Dioon (Gregory
& Chemnick 2004).
Many Dioon species from Oaxaca were described in the late 1970s or early 1980s thanks to the efforts of the
Mexican botanist Mario Vázquez-Torres and the Italian botanists Paolo De Luca, Aldo Moretti, and Sergio Sabato
(e.g., De Luca et al. 1980a, 1980b, 1981). These authors contributed enormously to the delineation of the geographic
ranges and species delimitations. They also discussed the evolutionary trends in the genus and acknowledged Oaxaca
as a center of diversity for Dioon (Sabato & De Luca 1985). Since then, more new species have been described as the
result of expeditions and taxonomic reassessments in the genus (Chemnick et al. 1997, Gregory et al. 2003, Nicolalde-

Accepted by Francesco Roma-Marzio: 6 Nov. 2020; published: 27 Nov. 2020 51

Morejón et al. 2009, Salas-Morales et al. 2016, Gutiérrez-Ortega et al. 2018a), demonstrating that the species diversity
in Dioon was even higher than previously thought. Some species with very narrow distributional ranges can be easily
distinguished due to their conspicuous and unique morphological traits (Gregory et al. 2003, Salas-Morales et al.
2016). On the other hand, species with wide distributions tend to show higher inter-population variation, and this has
not been often considered in taxonomic circumscriptions (but see González-Astorga et al. 2003, Gutiérrez-Ortega et
al. 2018a, Gutiérrez-Ortega et al. 2018b).

Species delimitation in the Dioon merolae species complex

Dioon merolae De Luca, Sabato & Vázq.Torres (1981:180–184) was described based on the morphological
characteristics found in its type population at Tonalá, Chiapas, and it was long thought that this species was endemic
to Chiapas (De Luca et al., 1981). But later, Chemnick et al. (1997) suggested that some populations from the lower
Río Tehuantepec valley of eastern Oaxaca and the Isthmus of Tehuantepec that were discovered in the mid-1990s
should also be considered as D. merolae. This conclusion was reached based on general observations and unpublished
vegetative morphological analyses. More recent studies (e.g., Cabrera-Toledo et al. 2010, Dorsey et al. 2018, Gutiérrez-
Ortega et al. 2018c) considered that other Dioon populations from the Valles Centrales region of Oaxaca also belonged
to D. merolae. Gutiérrez-Ortega et al. (2020) showed evidence that morphological and genetic variation exists among
populations of D. merolae in Chiapas and Oaxaca. In that study, it was demonstrated that the concept of D. merolae,
as currently circumscribed, actually represents a species complex composed of three lineages in which a lineage called
“West-A” is sister to two lineages, “West-B” and “East”. The lineage “East” is comprised of all populations at the
eastern side of the Isthmus of Tehuantepec, consistent with the original description of D. merolae (De Luca et al., 1981).
At the western side of the isthmus, in Oaxaca, the lineage “West-B” shares many morphological and habitat similarities
with “East”. However, “West-A” greatly differs from the other two by having flat, imbricate leaflets arranged in a
slight keel on the leaf, as opposed to strongly abaxially curved, strongly imbricate leaflets arranged on the leaf with
deflexed tips as typically found in D. merolae, among other traits (Table 1). Notably, whereas populations of “West-B”
and “East” occur in mesic areas and both likely represent the concept of D. merolae, “West-A” populations usually
occur in arid environments, coexisting with xerophytes and growing on or among rocks. Due to the conspicuous and
unique characteristics of these populations, we decided to formally recognize “West-A” as a new species named Dioon
oaxacensis sp. nov.

TABLE 1. Distinction among the three known lineages in the Dioon merolae species complex.
Trait West-A (D. oaxacensis sp. nov.) West-B East (D. merolae type)

Linear and slightly deflected Linear and remarkably

Leaflet shape Linear and straight
apically deflected apically

Leaflet imbrication Slight Strong Strong

Angle of mid-leaflet insertion 55–60 60–65 60–65

Mid-leaflet width (mm) 7–14 9–13 7–13

Mid-leaflet length (mm) 63–144 68–132 48–111

Microstrobilus length (cm) 26–34 37–77 30–40

Microstrobilus diameter (cm) 16–21 11–13 8–10

Megastrobilus length (cm) 41–59 43–45 45

Megastrobilus diameter (cm) 19–25 24–25 25

Seed diameter (mm) 24–35 33–41 21–27

Basal megasporophylls Green, long, tomentose Green, short, tomentose Yellow, short, tomentose

Habit Rupicolous Terrestrial Terrestrial

Habitat Arid Mesic Mesic

52 • Phytotaxa 474 (1) © 2020 Magnolia Press GUTIÉRREZ-ORTEGA ET AL.

Description of a new species

Dioon oaxacensis Gutiérrez-Ortega, Pérez-Farrera & Vovides sp. nov. (Figs. 1–5)

Holotype:—MEXICO. Oaxaca, Sierra Sur, Pérez-Farrera M.A & Gutiérrez-Ortega J.S., 9 November 2016, 3467 ♂, (HEM!). Isotypes:
(XAL!, MEXU!).
Rupicolous plant with cylindrical trunk, erect when adult, decumbent with age. Leaves 33–62 per trunk forming an erect or ascending leaf
crown, 103–148 cm long, aspect flat to moderately keeled. Rachis yellowish when mature, glabrous. Leaflets opposite to subopposite,
224–257 pairs, imbricate close to the rachis, inserted at 50–60º in respect to the rachis, linear to linear-lanceolate, stiff, 1–3 prickles
on distal margin, 0–1 prickle on proximal margin, slightly pruinose, papyraceous when young, rigid and coriaceous when mature.
Microstrobilus solitary, erect, whitish and tomentulose when emergent, light brown at maturity, cylindrical. Megastrobilus ovoid,
solitary. Seed ovoid, sarcotesta cream when immature and orange-brown when mature, micropylar ridges 14–15.

FIGURE 1. Habit of Dioon oaxacensis sp. nov. in Tlacolula District, Oaxaca, Mexico. (A) Mature plants usually have long, erect trunks
growing on hillsides. (B) Plants are usually agglomerated growing in rocky sites.

Additional specimens examined (paratypes):—MEXICO. Oaxaca: Sierra Sur, 22 May 2015, Pérez-Farrera M.A.
& E. Nanga Castillo 3361 male (HEM); 10 November 2019, Pérez-Farrera M.A., Gómez Domínguez H., & P. Díaz
3761 female (HEM); Valle Central, Oaxaca, 20 July 2008, García-Mendoza et al. 9201 (MEXU!); Valle Central,
Oaxaca Castillo & Amezcua 829 (MEXU); Valle Central, 14 February 2000, Salas-Morales S. 2683 (SERO; MEXU!);
Ocotlán, 16 January 2004, Salas-Morales S. 5159 (SERO!); Yautepec, 14 March 2006, Velasco K. 1242 (SERO!);
Yautepec, 26 January 1995, Salas-Morales S. 764 (SERO!); Tlacolula, 19 May 1997, Salas-Morales S. 1437 (SERO!);
Tlacolula, 24 March 1988, Martin G. J. GJM-M309 (MEXU).
Rupicolous plant. Stem cylindrical, covered with persistent leaf bases, arborescent up to ca. 200–250 cm tall,
16–28 cm in diameter, erect, sometimes decumbent with age. Leaves numerous forming an apical crown, erect, olive
green, 33–62 per crown, 100–150 cm long, 17–28 cm wide, slightly papyraceous when young or immature, rigid to
coriaceous, ascendant when mature. Petiole 12–18 cm long, unarmed, semiterete to subterete, tomentose to pubescent
at the base, light-brown, tomentose. Rachis semiterete to subterete, erect, 85–125 cm long, yellowish when mature.
Leaflets opposite to subopposite, slightly imbricate, inserted at a 55–60º (median = 56º) angle at mid-section of rachis,
224–257 pairs, linear to linear-lanceolate, 1–3 prickles on the distal margin and 0–1 prickle on the proximal margin,

A NEW CYCAD SPECIES: DIOON OAXACENSIS Phytotaxa 474 (1) © 2020 Magnolia Press • 53
flat, 8–14 cm long, 8–10 mm wide in the median part of leaf, coriaceous, stiff when mature, lemon-green on the adaxial
surface, olive green on the abaxial, 9–11 veins, inter-vein distance 0.5–1 mm. Microstrobilus solitary, cylindrical,
erect, whitish tomentulose when emerging, light-brown when mature, 34–40 cm long, 8–9 cm diameter, peduncle
densely tomentose when immature, 3–4 cm long, 3–3.5 cm diameter. Microsporophylls cuneate, distal portion deltate
to triangular, ascendant, 26–34 mm long, 16–21 mm wide at the distal portion, sporangia zone on abaxial surface 18–
25 mm long, microsporangia grouped in sori of 3–4. Megastrobilus solitary, ovoid, 41–59 cm long, 19–25 cm diameter,
lanose, peduncle tomentose, 4.5–6 cm long, 3–3.7 cm in diameter. Megasporophylls spirally arranged on cone axis,
distal portion triangular, tomentose, except the apical part, apex acuminate, 11–14 cm long, 7–8.5 cm wide at the base,
peduncle 6.5–9 cm long. Megasporophylls at the apical section are loosely appressed against the cone when immature
and open upon maturity. Seed ovoid, sarcotesta cream when immature, orange-brown when mature, sclerotesta beige,
with 14–15 micropylar ridges, 24–35 mm in diameter, 30–45 mm long.

FIGURE 2. Details of leaf morphology of Dioon oaxacensis sp. nov.. (A) Leaf form. (B) Adaxial and (C) abaxial views at the mid-section
of leaves; notice that leaflets are linear, straight, opposite or semi-opposite, slightly imbricate, and inserted at an oblique angle (65°) to the
rachis. (D) Apical section of the leaf. (E) Petiole and basal section of the leaf. Scale: 10 cm.

Habitat description:—Dioon oaxacensis occurs in rocky or calcareous outcrops in the deciduous tropical
forest dominated by Senna holwayana (Rose) H.S. Irwin & Barneby (1982: 559), Xylosma flexuosa (Kunth) Hemsl.
(1879: 57), Karwinskia humboldtiana (Willd. ex Roem. & Schult.) Zucc. (1832: 353), Manfreda pringlei Rose (1903:
19), Echeandia longifolia (Weath.) Cruden (1993: 136), Acacia cochliacantha S.Watson (1886:427), A. farnesiana
(L.) Willd. (1806:1083), Amphipterygium adstringens (Schltdl.) Standl. (1923:673), Bursera morelensis Ramírez
(1896:17), B. schlechtendalii Engl. (1883:41), Ceiba parvifolia Rose (1905:320), Cercidium plurifoliolatum Micheli
(1903: 269), Nopalea auberi (Pfeiff.) Salm-Dyck (1849: 64), Plumeria rubra L. (1753:2009), Pseudosmodingium
multifolium Rose (1897:143), and Stenocereus weberi (JM Coult.) Buxb. (1961:101), according to Acosta et al.
(2003), between 930 to 1500 m above sea level. Northernmost populations in Valles Centrales, Oaxaca, occur in
oak forests composed of Quercus crassifolia Bonpl. (1809:49), Q. glaucoides M. Martens & Galeotti (1843:209),
Quercus castanea Née (1801:276), Q. magnoliifolia Née (1801:268) and Q. obtusata Bonpl (1809:26), less aboundant
P. teocote Schltdl. & Cham. (1830:76). Other species in this community are Arbutus xalapensis Kunth (1818:279),
Q. castanea Née (1801:276), Ceanothus coeruleus Lag. (1816:11), Myrtillocactus schenckii (J.A. Purpus) Britton &
Rose (1909:427), Calliandra grandiflora (L’Hér.) Benth. (1840:139), and Arctostaphylos pungens Kunth (1819:259).
Climate classification is dry-hot with summer rains and cool winter (García, 2004).
Etymology:—“Oaxacensis” makes reference to the State of Oaxaca, Mexico, one of the main centers of cycad
diversity in the world, where this species is endemic.

54 • Phytotaxa 474 (1) © 2020 Magnolia Press GUTIÉRREZ-ORTEGA ET AL.

FIGURE 3. Mature megastrobilus. (A) Lateral view of strobilus and peduncle, (B) top view, (C) view from below. Megasporophylls
surrounding the peduncle are green and orange. Scale: 10 cm. Photos by José García González.

Key to the Dioon species in the Purpusii clade:

1a. Leaves green when emerging.

2a. Leaflets curved at the apical section of leaflets ..................................................................................................................D. merolae
2b. Leaflets not curved at the apical section of leaflets.
3a. Leaflets imbricated.
4a. Leaflets inserted obliquely on the rachis ...........................................................................................................................D. califanoi
4b. Leaflets inserted not obliquely on the rachis ................................................................................................................. D. oaxacensis
3b. Leaflets not imbricated.
5a. Leaves keeled .................................................................................................................................................................... D. purpusii
5b. Leaves no keeled.
6a. Leaflets 4–5 mm wide, widely spaced along the rachis ......................................................................................................D. caputoi
6b. Leaflets > 5 mm wide, slightly spaced along the rachis
7a. Leaflets with 3–4 long spines like-teeth on the upper margin....................................................................................... D. holmgrenii
7b. Leaflets with margins entire (inerme) or with 0–2 long spine like tooth on the upper margin .................................... D. planifolium
1b. Leaves silver when emerging .........................................................................................................................................D. argenteum

A NEW CYCAD SPECIES: DIOON OAXACENSIS Phytotaxa 474 (1) © 2020 Magnolia Press • 55
FIGURE 4. Mature microstrobilus. (A) Detail of sporophylls, (B) top view, (C) view from below. Scale: 5 cm. Photos by José García
González.

Discussion

Dioon oaxacensis circumscribes the morphological and genetic variation observed in the Dioon populations in the upper
arid portions of the Río Tehuantepec Valley (Ocotlán, Yautepec, and Tlacolula Districts) in Oaxaca, Mexico. Dioon

56 • Phytotaxa 474 (1) © 2020 Magnolia Press GUTIÉRREZ-ORTEGA ET AL.

oaxacensis differs from D. merolae (its closest congener) in its lower degree of leaflet imbrication, its flat, linear, stiff,
non-deflected leaflets, yellowish rachis of mature leaves, and larger reproductive structures (Table 1). Among cycad
collectors and horticulturists in the United States, Australia, Europe, and southern Africa, D. oaxacensis has been
informally recognized as Dioon sp. “Oaxacensis” (Gregory et al. 2008), and Dioon sp. “El Camarón” for decades. The
habitat of D. oaxacensis is similar across its populations (Fig. 6), usually cohabiting with elements of the seasonally
dry tropical forest and xerophytic plants, such as cacti, Agave, and Crassulaceae species that utilize Crassulacean Acid
Metabolism (CAM). This is a metabolic pathway commonly found in plants adapted to arid environments that helps
reduce transpiration and water loss. It is also very likely that D. oaxacensis presents some variation of CAM since
CAM-cycling has been found in its congener D. edule Lindley (1843: 59–60) (Vovides et al. 2002) but more work
needs to be done to verify.

FIGURE 5. Vegetative and reproductive structures of Dioon oaxacensis sp. nov. in situ: (A) Female plant, (B) male plant.

Dioon oaxacensis has important morphological similarities with D. purpusii Rose (1909: 260–261). Superficially,
the two species are difficult to distinguish, especially in ex situ collections and herbarium vouchers. However, D.
oaxacensis has dagger-like leaflets often slightly glaucous, with marginal leaflet prickles more reduced than in D.
purpusii, which has leaflets that are more gradually attenuated, dark green, with more pronounced marginal leaflet
prickles. Furthermore, D. oaxacensis usually has flat or nearly-flat leaves in cross section with a pinna-pinna angle
of 170–180°, whereas D. purpusii has keeled leaves in cross-section with the pinna-pinna angles of 150–170°. In
addition, the pinna-rachis angle of D. oaxacensis is less acute (55–65°) than in D. purpusii (45–55°), giving D.
purpusii a conspicuous chevron pattern when the leaf is viewed from above. Also, although the shielding angle of
leaflet insertion on the rachis is similar in both species, they can be distinguished because the leaflets of D. oaxacensis
are generally broader and thus appear to overlap when viewed from above; D. purpusii typically lacks this imbricated
appearance. In addition, the two species differ in megastrobilus and seed size, with those of D. oaxacensis being much
larger. Also, the habitat of D. purpusii is in less arid areas, occurring in tropical deciduous thorn forests 180–200 km
northwest of the occurrence of D. oaxacensis, on the other side of the Sierra Norte. Another species, D. argenteum
Greg., Chemnick, Salas-Mor. & Vovides (Gregory et al. 2003: 471–476), occurs between the two species. However,
phylogenetic studies have suggested that the species pairs D. purpusii/D. argenteum and D. oaxacensis/D. merolae
are nested in different subgroups in the Purpusii clade (Dorsey et al. 2018, Gutiérrez-Ortega et al. 2018c). Thus, it is
likely that the morphological similarities of D. oaxacensis and D. purpusii are convergent or they both retain ancestral

A NEW CYCAD SPECIES: DIOON OAXACENSIS Phytotaxa 474 (1) © 2020 Magnolia Press • 57
traits from a common ancestor in the Purpusii clade. Further morphological, anatomical, and genetic analyses will be
required to test these hypotheses.

FIGURE 6. Habitat of Dioon oaxacensis sp. nov. across populations. (A–C) Different populations in Tlacolula District, Oaxaca, (D–E)
various populations in Yautepec District, Oaxaca. Photo (E): courtesy of Takuro Ito.

58 • Phytotaxa 474 (1) © 2020 Magnolia Press GUTIÉRREZ-ORTEGA ET AL.

 With the recognition of D. oaxacensis as a valid taxon, D. merolae remains monophyletic, conformed by the
lineages “West-B” (from Tehuantepec District, Oaxaca) and “East” (eastern side of the Isthmus of Tehuantepec) as
revealed in our previous study (Gutiérrez-Ortega et al. 2020). Yet, “West-B” plants show intermediate characteristics
between “West-A” (D. oaxacensis) and “East” (D. merolae) (Table 1). West-B has qualitative similarities to D. merolae
but similar morphometry to D. oaxacensis except in trunk diameter, petiole length, and mid-leaflet width (Gutiérrez-
Ortega et al., 2020). We do not preclude the possibility that West-B represents a different species. However, so far, we
have found only one population (Tenango, Oaxaca) with these traits. Further explorations in the Tehuantepec District,
Oaxaca, is necessary to delineate the variation among populations in this region to conclude whether West-B can be
considered as a distinct species.
Dioon merolae is currently listed as “threatened with extinction” (category “P”) in the Mexican Official Norm
NOM-059-ECOL (SEMARNAT, 2010). According to Section 6.2 of that Mexican law, if a taxon is subdivided, the
new taxon shall maintain the highest risk category of the original taxon. For this reason, D. oaxacensis should also
putatively be considered as “threatened with extinction” (category “P”). Regarding the IUCN Red List of Threatened
Species (2020), we recommend the inclusion of D. oaxacensis as Endangered, based on the criterion A2ce+4c; C1.
All D. oaxacensis populations visited are small and restricted to very narrow locations. However, this species is well
known and appreciated by the local people, who are aware of its conservation status. Access to the populations must
be approved by the “ejidal” communities in the Yautepec District, which own the lands where D. oaxacensis occur. In
Albarradas (Tlacolula District), the north-westernmost locality of D. oaxacensis, local people annually harvest leaves
from the plants for use as decoration in religious festivities (Pérez-Farrera & Vovides, 2006). The people report that
they only select a few mature long leaves to avoid further damage to the plants, and that the annual leaf collecting
enables monitoring of the populations they know. Therefore, we believe the populations are well protected.

Acknowledgments

Thanks to Takuro Ito for his assistance in fieldwork surveys and to José García González for taking photos of the strobili.
Thanks to anonymous donors to Montgomery Botanical Center for financial support to MAPF. JSGO acknowledges
support by the Japan Society for the Promotion of Science (Grant-in-aid No. 18F18076). Leaves and leaflets of D.
merolae specimens were collected under permit SGPA/DGVS/08722 from SEMARNAT, Mexico.

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