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Research Article
Eugenia sarahchazaroi (Myrtaceae, Myrteae), a new species from the cloud forest of Mexico
expand article infoAntonio Francisco-Gutiérrez, Miguel Cházaro-Basáñez, Rodrigo Carral-Domínguez§, Héctor Narave-Flores, Luis Islas-Tello§
‡ Universidad Veracruzana, Xalapa, Mexico
§ Dirección de Recursos Naturales, Secretaría de Medio Ambiente del Estado de Veracruz, Xalapa, Mexico
† Deceased author
Open Access

Abstract

Following the description of Eugenia naraveana in 2016 from the cloud forest of the Cofre de Perote volcano, Mexico, the doubt about the existence of another unlocalized and sympatric species of Eugenia remained. After years of searching, the second endemic species of the Cofre de Perote volcano, Eugenia sarahchazaroi, is presented here. It belongs to the section Umbellatae, and is described, illustrated, and compared with E. naraveana and E. coetzalensis, recently described from Veracruz, the second state with the highest diversity of Eugenia in Mexico. The species is only known from the type locality and is classified in the Critically Endangered CR B1+B2(a,biii) category of the IUCN Red List conservation assessments.

Key words

Cloud forest, Cofre de Perote, endemic species, Eugenia naraveana, Umbellatae, Veracruz

Introduction

Myrtaceae Juss. is a diverse family with ca. 6000 species distributed in tropical and subtropical regions (Lucas et al. 2019). It is classified into the subfamilies Psiloxyloideae (with two tribes) and Myrtoideae (with 17 tribes) (Wilson et al. 2005; Wilson 2010; Giaretta et al. 2019; Uc-Gala et al. 2023). From the latter, the tribe Myrteae is the most diverse within the family, with 2690 species (Stevens 2023). About 109 species of Myrtaceae are distributed in Mexico, of which 87 correspond to Eugenia L. (Uc-Gala et al. 2023), a monophyletic genus, one of the most hyperdiverse genera with 1218 species (Giaretta et al. 2022; POWO 2023), and the second largest genus of tree species in the world (Beech et al. 2017; Uc-Gala et al. 2023).

Eugenia currently circumscribes ca. 1218 species (POWO 2023). They are distributed mainly from Mexico to northern Argentina and Uruguay (including the Caribbean), with fewer species in New Caledonia, the Philippines, India, Sri Lanka, Madagascar, Mauritius, and Comores. Based on phylogenetic analyses, Eugenia has been classified into nine sections: Eugenia, Hexachlamys, Phyllocalyx, Pilothecium, Pseudeugenia, Racemosae, Schizocalomyrtus, Speciosae, and Umbellatae, which can be determined with morphological characters (Mazine et al. 2016; Giaretta et al. 2021).

This year, Uc-Gala et al. (2023) performed the most comprehensive checklist of Eugenia species from Mexico. They reported 87 species of Eugenia, 46 endemic to this country. Veracruz is the second state with the highest Eugenia species richness in Mexico, with 31 of them (Uc-Gala et al. 2023). Also, Eugenia occupies the fourth place among the richest tree genera in Mexico (Téllez et al. 2020; Uc-Gala et al. 2023). The species of Eugenia from Veracruz were studied in the taxonomic treatment of Myrtaceae for the Flora of Veracruz series (Sánchez-Vindas 1990). In the last decade, two new and endemic species of Eugenia were described from the same state, E. naraveana Cházaro & Franc.Gut. (Cházaro-Basáñez and Francisco-Gutiérrez 2016), and E. coetzalensis Durán-Esp. & Cast.-Campos (Durán-Espinosa et al. 2018).

After botanical explorations in the Cofre de Perote Volcano in Veracruz, Mexico, a new suspected species of Eugenia is studied here. The aims of this work are: 1) to describe a new species of Eugenia; 2) to compare it with the sympatric and endemic E. naraveana; and 3) to evaluate the conservation status of the species.

Materials and methods

Field work

In 2014, during the fieldwork for describing E. naraveana, Macario Córdova-Cortina guided the authors to one population of trees with morphological characters similar to the species collected by Miguel Cházaro-Basáñez in 1987, known as “guayabo” (guajava), but with a different vernacular name, “guayabillo” (small guajava), but it was not explored because it was decided to find the species first collected three decades ago, since both populations were considered to belong to the same taxon, the differences in fruit size being attributed to phenotypic variation. After having described and published the species (Cházaro-Basáñez and Francisco-Gutiérrez 2016), the work of the author mainly focused on the description of the species of Agave (Arzaba-Villalba et al. 2018, 2023) and parasitic Orobanchaceae (Francisco-Gutiérrez et al. 2019, 2023a). In July 2021, during the lockdown of the coronavirus pandemic, the fieldwork was resumed with an expedition by Miguel Cházaro-Basáñez and Héctor Narave-Flores. Finally, the species was found in the locality of Encinal II, municipality of Acajete, Veracruz, Mexico, and subsequent visits were made to collect biological and photographic material.

Taxonomic determination

Fresh specimens of the species were collected, photographed, and dried or preserved in a solution 1:1 of ethanol and water. Measurements were made on living and preserved specimens. Voucher specimens are deposited in the cited herbaria, these cited by the acronyms following Thiers (2023). The sectional placement was determined following the sectional key provided by Mazine et al. (2016). The checklist of accepted species of Eugenia in Mexico (Uc-Gala et al. 2023), the taxonomic treatment of Myrtaceae in Veracruz (Sánchez-Vindas 1990), and articles of recently described species in the state (Cházaro-Basáñez and Francisco-Gutiérrez 2016; Durán-Espinosa et al. 2018) were consulted for taxonomic determination and morphological comparisons.

Conservation assessments

Geographic coordinates were obtained in the field with a Garmin eTrex10 GPS. The data were used to estimate the geographic ranges of the extent of occurrence (EOO) and area of occupancy (AOO) with the Geospatial Conservation Assessment Tool (GeoCAT, Bachman et al. 2011) at the website http://geocat.kew.org/. The obtained values and literature on threats in the species’ distribution area were weighted to evaluate the conservation status following the Categories and Criteria of the IUCN Red List of Threatened Species (IUCN Standards and Petitions Committee 2022).

Distribution map

The polygon of the Cofre de Perote Volcano National Park was extracted from the World Database on Protected Areas and Other Effective Area-based Conservation Measures (WDPA–WDOECM) of the United Nations Environment Programme World Conservation Monitoring Centre (UNEP-WCMC and IUCN 2021), available at https://www.protectedplanet.net/en. Digital elevation models correspond to the layer provided by WorldClim 2.1 (Fick and Hijmans 2017) with resolution of 2.5 min, and the model Continuo de Elevaciones Mexicano 3.0 of the Instituto Nacional de Estadística y Geografía (INEGI) of Mexico with resolution of 130 m, available at https://www.inegi.org.mx/app/geo2/elevacionesmex/. Map was designed in QGIS 2.15 (QGIS Development Team 2016).

Taxonomic treatment

Eugenia sarahchazaroi Cházaro, Franc.Gut. & J.R.Carral, sp. nov.

Diagnosis

Eugenia sarahchazaroi is morphologically similar to E. naraveana but differs by having shorter and smaller leaves (37.3–59.7 × 14.4–21.3 mm vs. 57–116 × 22–55 mm in E. naraveana), reduced number of flowers per fascicle (4–6 vs. 3–16), absence of bracteoles (vs. presence), shorter pedicels (1–1.7 × 0.6–1 mm vs. 6–12 × 1–2.6 mm), smaller staminal disc (1.6–2 mm vs. 3–5 mm wide), presence of central cavity in staminal disc (vs. absence), shorter style (3.4–7 mm vs. 7.5–9.7 mm), and shorter fruits (1.4–1.8 cm vs. 1.1–4.3 cm). The species is also similar to E. coetzalensis but it can be distinguished by its inflorescence (axillary fascicles vs. axillary racemes in E. coetzalensis).

Type

Mexico. Veracruz: Municipio Acajete, Paraje La Cieneguilla, cerca del Encinal II, 19.517372, -97.043692, elev. 2400 m, 01 July 2021, fl., M. Cházaro-Basáñez & H. Narave-Flores 11226 (holotype: XAL!; isotypes: CIB!, CITRO!, ENCB!, IBUG!, MEXU!, XALU!).

Description

Tree 4.5–20 m tall. Bark exfoliating, the outer layer fissured and covered by lichens, the inner layer smooth and pink to reddish. Twigs terete, some covered by lichens, apical leaves paired. Internodes 15.8–21.6 mm long, 1.1–2.1 mm in diam., not exfoliating, shortly lanose to glabrescent in apical leaves. Cataphylls absent. Leaves opposite, petioles curved and adpressed, later the terminal petioles parallel to the main axis of the branches, sometimes straight and perfectly aligned one in front of the other, simulating a cross, 2.4–7.2 × 0.9–1 mm, shortly lanose. Blades 37.3–59.7 × 14.4–21.3 mm, lanceolate or elliptical, chartaceous and glossy, discolorous when dry, glabrous adaxially and abaxially, oil glands present; base cuneate, apex acuminate, 5.6–10.7 mm long, margin entire and sinuate; midvein slightly impressed adaxially, prominent abaxially, glabrous in both surfaces; secondary veins 7–14 at each side, leaving the midvein at angles of 53–76°, slightly conspicuous adaxially; one marginal vein, 0.6–1.4 mm from the margin. Inflorescences axillary fascicles, frequently 2 per node, rarely 1, 4–6 flowers each, bracts, and bracteoles absent. Pedicels of floral buds: 1.0–1.7 × 0.6–1 mm, straight to slightly curved, sometimes thickened at the base. 2-ribbed, pubescent, trichomes strigose. Flower buds ovoid to spherical, 1.1–3 mm diam., hypanthium campanulate, 1.2–2.3 × 1.5–2.2 mm, light green, shortly pubescent, trichomes simple. Flowers at anthesis with hypanthium, 1.08–1.5 × 1.4–1.9 mm, glabrous, pale green to reddish. Calyx lobes 4, free, one pair slightly less developed than the other, lobes 0.44–0.77 × 1.2–1.91 mm, widely triangular or orbicular, apex obtuse, abaxially, and adaxially glabrous, margin ciliate, trichomes 0.04–0.07 mm long, green to reddish. Petals 4, 2.4–3.2 × 2.7–2.9 mm, orbicular to elliptical, with few circular brown glands, apex widely rounded, glabrous. Staminal disc a circular ring, sometimes square with rounded corners, 1.6 mm in diameter or 1.6–2.0 mm in diameter, central cavity with no stamens inserted, 0.79–1 mm in diameter, glabrous. Stamens 31–76, deciduous, filaments 2.1–5 × 0.16–0.18 mm, glabrous; anthers 0.38–0.51 × 0.31–0.64 mm, oblong to ellipsoid, glabrous. Style 3.4–7 × 0.33–0.44 mm, glabrous, white, sometimes reddish, deciduous. Ovary locules 2, 2 ovules each. Fruit a drupe; peduncles straight or slightly curved, 4.2–4.7 × 1.9–3.8 mm; immature fruit globose to ellipsoid with some prominent and longitudinally parallel veins, 9–17.9 × 11.3–14.8 mm, smooth to reticulate, partially green, yellow or red-tinged, glabrous, not crowned at the apex with calyx lobes, pulp yellow with red granules; ripe fruit globose to ellipsoid with no veins, 14.1–18.2 × 14.7–17.2 mm, smooth, dark purple to black, glabrous; mesocarp 3.1 mm wide, salmon to dark purple; one seed per fruit, spherical to elliptical, 13.5–13.8 × 12–12.5 mm, testa smooth (Fig. 1).

Figure 1. 

Eugenia sarahchazaroi A inflorescence B twig with fruitsC detail of flowersD fasciclesE floral budsF staminal discG adaxial surface of a leafH abaxial surface of a leafI immature fruitJ ripe fruit, and K seedling. All photographs were taken by Rodrigo Carral-Domínguez and edited by Antonio Francisco-Gutiérrez.

Phenology

The species was collected with floral buds, flowers, and mature fruits from April to July.

Etymology

The specific epithet honors Sarah Magyari Cházaro-Hernández, the beloved daughter of Miguel Cházaro-Basáñez, who has accompanied him on numerous botanical expeditions. As a child, Sarah Cházaro developed an interest in botany by learning to identify several plant genera on field trips with her father (Fig. 4). This new species is the third dedicated to his children, with Agave paskynnellchazaroi Arzaba, Cházaro & Franc.Gut. (Arzaba-Villalba et al. 2023), and Valeriana rudychazaroi Cházaro, Franc.Gut. & J.R.Carral (Francisco-Gutiérrez et al. 2023b). These eponyms were the last will of Miguel Cházaro before he passed away on April 04, 2023. The obituary with a review of his life and work can be found in Francisco-Gutiérrez and Vázquez-García (2023).

Distribution and habitat

The Cofre de Perote volcano, has been botanically explored since 1804 by Humboldt & Bonpland and many subsequent botanists. The mountain and its periphery house rare and new species recorded and described since the 1980’s (for a detailed review, see Cházaro et al. 2016). Eugenia sarahchazaroi is only known from the type locality. Other species inhabiting the cloud forest near the new species are Quercus corrugata Hook., Q. acherdophylla Trel. (Fagaceae), Eugenia naraveana Cházaro & Franc.Gut., Myrsine penduliflora A.DC. (Primulaceae), Ilex discolor Hemsl., Peperomia tenerrima Schltdl. & Cham. (Piperaceae), Lamourouxia xalapensis Kunth, Pedicularis canadensis L. (Orobanchaceae), Oreomunnea mexicana (Standl.) J.-F.Leroy (Juglandaceae), Echeveria secunda Booth ex Lindl., E. rosea Lindl. (Crassulaceae), Turpinia occidentalis (Sw.) G.Don (Staphyleaceae), Ocotea disjuncta Lorea-Hern. (Lauraceae), Citharexylum hidalgense Moldenke (Verbenaceae), Cestrum fasciculatum Miers (Solanaceae), Symplocos coccinea Bonpl. (Symplocaceae), Oreopanax flaccidus Marchal (Araliaceae) and Aporocactus flagelliformis (L.) Lem. (Cactaceae), among many other species. It is close to the also endemic E. naraveana, which was only known from the type locality. Recent data allow for the expansion of its distribution, reported in the municipality of Zongolica, Veracruz (David Jimeno-Sevilla, curator of ZON herbarium, pers. comm.). An updated distribution map of E. sarahchazaroi and related species is provided in Fig. 3.

Vernacular name

“Guayabillo” (Macario Córdova-Cortina and Héctor Narave-Flores, pers. comm.).

Paratypes

Mexico. Veracruz: Municipio Acajete, Rancho de Martín Sangabriel, camino El Zapotal – El Encinal 2, km 1.52, 19.512869, -97.04118, 2320 m, 18 April 2022, fr., R. Carral-Domínguez, L. Islas-Tello, I. Gómez-Escamilla & B. Téllez-Baños RCD-852 (IBUG!, MEXU!, XAL!); Municipio Acajete, Rancho de Martín Sangabriel, camino El Zapotal – El Encinal 2, km 1.52, 19.512974, -97.040498, 2312 m, 18 April 2023, R. Carral-Domínguez, E. Marinero-Sobal & L. Abrajan-Cortés RCD-853 (XAL!, MEXU!); Municipio Acajete, Rancho de Martín Sangabriel, camino El Zapotal – El Encinal 2, km 1.52, 19.513025, -97.040499, 2306 m, 07 May 2023, R. Carral-Domínguez, D. Canales-Suardíaz & A. Seedorf-Anaya RCD-854 (XAL!, MEXU!, IBUG!).

Conservation status

The species has geographic ranges of Extent of Occurrence (EOO) of 0 km2, and Area of Occupancy of 4 km2. The species grows in the foothills of the Cofre de Perote Volcano, about 7.5 km from the limit of the protected area under the national park category (Fig. 3), a location that threatens it because the vicinity of the volcano has experienced constant overexploitation of forests and illegal logging since the 20th century (Hoffmann 1989). Because of EOO < 100 km2, AOO < 10 km2, number of locations = 1, and continuing decline observed in the extent and quality of habitat, we evaluate the new species E. sarahchazaroi in the category critically endangered CR B1+B2(a,biii). This species is currently the target of conservation efforts being reproduced in the greenhouses of the Secretary of Environment and Natural Resources (SEDEMA) of Veracruz.

Discussion

Eugenia sarahchazaroi belongs to the section Umbellatae through having bracteoles and calyx lobes not foliaceous, calyx open in the bud, and flowers 4-merous arranged in fascicles. This section has the largest species richness in Eugenia, with about 680 species (Mazine et al. 2016).

The species of Eugenia from Veracruz, Mexico, were studied in the issue of Myrtaceae of the Flora of Veracruz series (Sánchez-Vindas 1990). These species were considered for the morphological comparisons with E. naraveana (Cházaro-Basáñez and Francisco-Gutiérrez 2016), the most similar species. Besides, only the species E. coetzalensis was later described for Veracruz. Because of it, the new species presented here is compared with both.

Eugenia sarahchazaroi is distinguished from E. coetzalensis mainly by the type of inflorescence (fascicle vs. racemes, respectively). The paratype of E. coetzalensis, E. Guízar-N. & J.C. Echeverría 5688 (MEXU1075426) can be electronically consulted at https://datosabiertos.unam.mx/IBUNAM:MEXU:1075426. Eugenia sarahchazaroi is similar to E. naraveana but it differs in several morphological characters, which can be analyzed in the Table 1. Overall, this new species’ leaves, pedicels, hypanthium, staminal discs, and fruits are smaller than those of the E. naraveana. Additionally, the number of leaves and fruits are notably higher than in E. naraveana, as seen in photographs of Fig. 2. The staminal disc also shows a suppressed central area with no stamens where the style inserts, which is lacking in the staminal discs of E. naraveana. These features allow us to determine this taxon as a different species.

Table 1.

Morphological comparison among Eugenia sarahchazaroi and similar species E. naraveana and E. coetzalensis.

Character E. sarahchazaroi E. naraveana E. coetzalensis
Leaf size (mm) 37.3–59.7 × 14.4–21.3 57–116 × 22–55 23–60 × 18–33
Petiole orientation Curved and adpressed or sometimes straight Straight Straight
Number of secondary veins per side 7–14 7–13 11–16
Angle of secondary veins 53–76° 60–70° 40°
Indumentum of leaf surfaces Glabrous Glabrous Adpressed-strigose when newly formed, glabrescent when mature
Inflorescence and number of flowers Axillary fascicles, frequently 2 per node, rarely 1; 4–6 flowers Axillary fascicles, 1–2 per node; 3–16 flowers Axillary racemes, 1 per axil, 2 per node; 2–4 flowers
Bracteoles shape Absent Ovate Lanceolate
Pedicels size (mm) 1.0–1.7 × 0.6–1.0 6–12 × 1.0–2.6 8–17 × 0.4–0.5
Hypantium length (mm) 1.08–2.3 2.6–3.4 1.6–2.6
Staminal disc shape Rounded, sometimes square with rounded corners Quadrangular Square
Staminal disc size 1.6 mm in diameter or 1.6–2.0 mm per side 3–5 × 3–5 mm 2 × 2 mm
Central cavity in staminal disc Present Absent Unknown
Number of stamens 31–76 70–131 60–100
Style length (mm) 3.4–7 7.5–9.7 3.4–5.6
Fruit shape Globose to ellipsoid Subglobose Globose
Fruit size (cm) 1.4–1.8 × 1.4–1.7 1.1–4.3 × 0.9–3.4 1.3 × 2
Fruit indumentum Glabrous Glabrous Faintly strigose
Source This study Cházaro-Basáñez and Francisco-Gutiérrez (2016) Durán-Espinosa et al. (2018)
Figure 2. 

Morphological comparison between Eugenia sarahchazaroi and E. naraveana. All photographs of E. sarahchazaroi were taken by Rodrigo Carral-Domínguez; photographs of E. naraveana were taken by Antonio Francisco-Gutiérrez, except for the branch with fruits by Jose Luis Ramírez-Pacheco.

Figure 3. 

Distribution map of Eugenia sarahchazaroi and similar species in Mexico. The colored square corresponds to the Cofre de Perote volcano and its natural protected area under the category of National Park, delimited with the yellow line.

Figure 4. 

Miguel Cházaro and his beloved daughter, Sarah M. Cházaro-Hernández A learning her first botanical knowledge at three years old at home B botanical expedition in El Chico National Park, Hidalgo, Mexico, in 2018. Photographs taken by Patricia Hernández-Romero.

Acknowledgments

The authors are grateful to Azul Seedorf-Anaya, Ivonne G. Escamilla, Diego Canales-Suardíaz, Esteban Marinero-Sobal, Bruno Téllez, and L. Abrajan-Cortés for their companionship during field trips for the description of this new species and with Macario Córdova-Cortina for providing information about the presence of this species during field trips for the description of E. naraveana.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This research was partially funded by the National Researchers Fellowship Program of the National Council of Science and Technology of Mexico (SNI–CONACYT), awarded to Miguel Cházaro-Basáñez. The wife of Miguel Cházaro, Mrs Patricia Hernández-Romero shared photographs of her family and sponsored the open access fee.

Author contributions

Conceptualization: MCB, HNF. Data curation: RCD, LIT, AFG, MCB. Formal analysis: AFG. Funding acquisition: MCB. Methodology: AFG, RCD. Project administration: MCB. Visualization: RCD, AFG. Writing - original draft: AFG. Writing - review and editing: HNF.

Author ORCIDs

Antonio Francisco-Gutiérrez https://orcid.org/0000-0003-2013-9811

Miguel Cházaro-Basáñez https://orcid.org/0000-0003-3709-2394

Rodrigo Carral-Domínguez https://orcid.org/0000-0002-3347-5753

Héctor Narave-Flores https://orcid.org/0000-0002-3686-165X

Data availability

All of the data that support the findings of this study are available in the main text.

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1† Deceased
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