Zanthoxylum L. is one of the most diverse genera in the Rutaceae, with about 225 species (Appelhans et al., 2018). It has a primarily pantropical distribution (Kubitzki et al., 2011). In the Neotropics, 86 species are recorded (Groppo & Pirani, 2017; Reynel, 2017, 2020), with a center of diversity in the Andean-Amazonian area but also with some species in Canada and Chile (Appelhans et al., 2018).

A review of the Neotropical species of the genus recognized four sections: Macqueria Comm. ex Triana & Planch., Pterota (P. Browne) Triana & Planch., Tobinia (Desv. ex Ham.) Griseb. and Zanthoxylum L. (Reynel, 2017). Section Macqueria is the most diverse, with 65 species (Reynel, 2020), at present it is divided into seven subgroups. Recent molecular studies, however, show that Macqueria is polyphyletic (Appelhans et al., 2018).

In Colombia, 28 species of Zanthoxylum occur from sea level to 3300 m elevation (Reynel, 2016, 2017, 2020), indicating the country as one of the most diverse for the genus in the Neotropics. Eleven of these species inhabit the Tropical Dry Forest biome (TDF; Pizano & García, 2014); this is one of most threatened ecosystems in the world (Pizano & García, 2014) and includes the Northern inter-Andean Valleys, one of the richest of the 12 floristic subdivisions of this biome in the Neotropics (DRYFLOR, 2016).

Zanthoxylum magnifructum Reynel was described from only a single fruiting specimen collected in the TDF of the Magdalena River valley in the department of Huila in Colombia (Reynel, 2020). It is characterized by having the largest fruit of any Neotropical species of the genus. Recent research in Colombia has added to the knowledge of the morphology, ecology and distribution of Z. magnifructum. The original description is emended here to include descriptions of the seeds and the male and female flowers, which were heretofore unknown. Some previously described characters not present in examined specimens are included in square brackets.

Comments about its geographical distribution, taxonomic affinities, and sexual dimorphism are included, and its conservation status according to IUCN criteria is evaluated. Additionally, a key to the species of Zanthoxylum that occur in the TDF of Colombia is provided.

Zanthoxylum magnifructum Reynel. Type: Colombia. Huila: Cordillera Oriental, E of La Bodega, on foot trail up río Venado to jct. with río Venadito, 2700 ft. [820 m], 22 Nov. 1944 [fr], E. Little, Jr. 8980 (holotype: NY-n.v.; isotype: US03305487 [digital image!]). (Figs. 1 and 2.)

Fig. 1
figure 1

Zanthoxylum magnifructum. A. Fruiting branch and leaves. B. Staminate flower with two petals removed. C. Pistillodes. D. Petal of staminate flower. E. Stamen. F. Pistillate flower with two petals removed. G. Pistillate flower with sepals and petals removed. H. Petal of pistillate flower. I. Types of staminodes. J. Dehiscing fruit with seed inside, lateral view. K. Mature fruit in top view. (A, J, K from Jiménez & Guzmán 2072, HUA; B–H from Jiménez et al. 2139, HUA; I from Londoño et al. 296, HUA; drawing by Diego A. Zapata, HUA illustrator.)

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Fig. 2
figure 2

Zanthoxylum magnifructum (photographs). A. Fruiting branch and leaves. B. Detail of the zones of clustered leaf and bud-scale scars. C. Staminate flowers. D. Pistillate flowers. E. Immature fruits. F. Dehiscing fruit. (A from Jiménez et al. 2280, CUVC; B, D from Londoño et al. 296, HUA; C from Jiménez et al. 2139, HUA; E from Londoño et al. 297, HUA; F from Idárraga el al. 6988, JAUM; A, C, F by J. Jiménez; B, D, E by A. Trujillo.)

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Trees 15 m tall, gynodioecious [dioecious], semi-deciduous, trunk armed or partially armed; indumentum of simple short straight hairs; branches with growth proleptic, with short zones of clustered leaf and bud-scale scars, glabrous with terminal buds puberulent, with leaves evenly distributed on branches, unarmed or with sparse, straight to slightly incurved spines 2.8–4.1 × 4.2–6.2 mm; lenticels present, up to 2 mm long, periderm peeling off in parts when dry. Leaves (8–) 13–22 (–26) cm long, 4–6 (–9)-foliolate, paripinnate or occasionally imparipinnate, lateral leaflets opposite, less frequently subopposite toward the leaf base, medial pair usually longer than other leaflets; petiole 3–7.1 (–10.5) cm long; rachis 3.4–13.3 cm long, 1–2 mm thick, terete, glabrous, unarmed, interjuga 2.2–5.5 (–8) cm long; petiolule 3.3–7.4 mm long; leaflets (3.6–) 5.7–13.2 × (1.6–) 2.2–5.5 (–9) cm, ovate to elliptic or less often oblong, occasionally obovate or orbicular, base acute to obtuse, straight or rounded, decurrent, asymmetrical, apex acute to obtuse, attenuate to acuminate or short-acuminate, occasionally rounded, acumen (3–) 9–12 × 4–6 (–8) mm, chartaceous, glabrous, usually drying olive-green on both surfaces or pale green below; margin glandular, crenate, entire toward the base, the teeth 3–8 mm apart at the middle; midvein prominulous on both surfaces, secondary veins 5–11 (–12) pairs, prominulous on both surfaces, tertiary veins perpendicular to midvein, reticulate, prominulous on both surfaces; glands 3.7–4 mm diam., rounded, close to the primary vein. Inflorescences terminal and subterminal, axes puberulent; bracts 1 (–2) × 0.8–1 (–1.5) mm, triangular-deltoid, glabrous, occasionally absent. Staminate inflorescences 2–9 cm long, panicles branched 2–3 times, with more than (30–) 60 flowers, erect; peduncle (0.6–) 2.5–4.5 cm long; secondary axes alternate, forming a 30°–60° (–90°) angle with main axis; pedicels 0.6–0.8 mm long or absent, puberulent; bracteoles 0.4–0.6 mm long, deltate, apex acute, straight or acuminate, glabrous. Staminate flowers 5-merous; sepals 1–2 × 1 mm, connate to 1/2 their total length, lobes elliptical, apex acute, straight, convex or rounded, margin erose, glabrous, with one gland 0.5 mm diam., round, medial; petals 3–3.5 × 1.5–1.8 mm, free, elliptical, apex acute, straight or convex, margin erose, saccate, glabrous, with one gland 0.5 mm diam., elliptical or round, apical; stamens 5, exserted 1/3–1/2 their total length, glabrous, filaments 4–4.5 mm long, slender, anthers 1.5 × 0.5 mm, ovate, thecae oblong, free at the base; nectary conical-truncate, lobes 1 × 1.5–2 mm; pistillodes 2–3.1 × 0.6–0.8 mm, pyriform, free. Pistillate inflorescences 0.5–4 cm long, racemes, 3–8-flowered, erect; peduncle 0.3–1.4 cm long; pedicels 0.5–2.9 × 1 mm, puberulent; bracteoles 2–7, 0.6–0.8 mm long, deltate, glabrous. Pistillate flowers 5 (–6)-merous; sepals (1–) 1.3–2 × 1.2–1.7 mm, connate to 1/2 their total length, lobes elliptic, apex acute, straight, convex or rounded, thick, margin erose, glabrous to glabrate, persistent in fruit, with one gland 0.5 mm diam., round, apical; petals 5–5.3 × 2.5–3 mm, free, elliptic, acute, straight, convex or rounded, glabrous, margin erose, with one gland 0.5 mm long, elliptic or round, apical; staminodes 1–5 or absent, 0.5–1 (–2) × 0.5 mm, ovate to oblong, membranaceous, occasionally with antherodes 0.5–1 × 0.5 mm; gynophore 2 × 2–2.6 mm, long-conic; carpels [2–] 3 [–4], 1.8–2 × 2–2.2 mm, oblong to ovate, 2-lobed at the apex, basally connate 1/3 their total length, obliquely inserted on gynophore, glabrous; style 0.2 × 0.8 mm; stigma 2.2–2.4 mm diam., 0.2–0.4 mm thick. Fruit 17–19.3 (–22.7) mm diam., up to 24 mm diam. in vivo, [2–] 3 [–4]-follicular [when 3- to 4-follicular, 1 follicle aborting]; gynophore 4.5–6.2 (–7) mm tall, follicles 10.5–13.8 mm long, in vivo up to 16.9 mm long, ovate to subglobose, connate to 2/3 their total length and 1/2 laterally, pericarp 4.2–6.3 mm thick, up to 8 mm thick in vivo, fleshy; seed 5.6–7.2 × 3.2–5.5 mm, ellipsoid, funicular scar 2.4–3.5 × 1.1–1.5 mm, ovate.

Distribution and habitat.—Zanthoxylum magnifructum is endemic to TDF of northern inter-Andean valleys in Colombia (DRYFLOR, 2016), at 399–1060 m elevation. Specifically, this species has been collected in the Cauca River canyon in the department of Antioquia (Holdridge, 1967; Espinal, 2011), and in the Magdalena River valley in the departments of Huila and Tolima (Fig. 3).

Fig. 3
figure 3

Distribution of Zanthoxylum magnifructum. Departments from north to south: Antioquia, Tolima and Huila (type locality marked).

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Phenology.—The species is known to flower between January and May and fruit between March and November.

Conservation status.—We recommend that this species be listed under the IUCN Red List category of Endangered (EN; see IUCN, 2012) due to its small area of occupancy (32 km2), and extent of occurrence (15.101 km2) as estimated by the R packpage “ConR” (Dauby, 2019; Protected Planet, 2019; R Core Team, 2019), its only 4 registered subpopulations, and continuous decrease in the quality of its habitat (i.e., small habitat fragments <500 km2, mainly in a matrix of disturbance and severe erosion due to human activity; criteria B1ab (iii) + B2). All subpopulations are less than 20 km from some human population center and occur outside protected areas; three of them are less than 12 km from gold mining concessions, and one, in the valley of the Cauca River, was partially affected by a hydroelectric project. Paradoxically, that project may currently represent a weak conservation measure for this taxon through the protection of the adjacent forests in the area. Priority should be given to detailed ecological studies of the populations to determine precise conservation measures needed in the species’ highly disturbed habitat.

Additional specimens examined. COLOMBIA. Antioquia: Mun. Buriticá: corregimiento La Angelina, 6°42′15.51′′N, 75°51′30.53′′W, 711 m, 30 May 2019 [fr], J. Bohórquez et al. 1 (HUA). Mun. Liborina: quebrada La Sucia, s.m., 20 Jun 2013 [fr], O. Uribe 5 (MEDEL). Mun. Sabanalarga: Llanos de Niquia, 1.5 km bajando desde el alto Llanos de Niquia, 6°51′33.7′′N, 75°50′15.3′′W, 523 m, 6 Nov 2018 [fr], A. Idárraga et al. 6988 (JAUM); ibid., 30 Sep 2017 [fr], J. Jiménez & V. Guzmán 2072 (HUA, JAUM, MEDEL); ibid., 3 Feb 2018 [fl], J. Jiménez et al. 2139 (HUA, COL, CUVC, JAUM, MO); ibid., 3 Mar 2018 [fl], J. Jiménez & L. Zapata 2204 (FAUC); ibid., 10 Jun 2018 [fr], J. Jiménez et al. 2280 (CUVC); ibid., 4 Aug 2018 [fr], J. Jiménez et al. 2332 (ICESI); ibid., 9 Oct 2018 [fr], J. Jiménez et al. 2359 (FAUC); Llanos de Niquia, 6°51′48.8′′N, 75°50′6.1′′W, 565 m, 9 Oct 2018 [st], J. Jiménez et al. 2371 (HUA); Llanos de Niquia, 1.5 km bajando desde el alto Llanos de Niquia, 6°51′33.7′′N, 75°50′15.3′′W, 523 m, 6 Nov 2018 [fr], Y. Londoño et al. 285 (HUA, JAUM); ibid., 5 May 2019 [fl], Y. Londoño et al. 296 (HUA, COL, JAUM, MO); ibid., 5 May 2019 [im fr], Y. Londoño et al. 297 (HUA, JAUM); vereda Membrillal, 6°53′9.23′′N, 75°49′52.11′′W, 399 m, 14 Mar 2018 [im fr], P. Morales 1320 (HUA); hacienda El Jagüe, 6°55′53.7′′N, 75°48′40.5′′W, 600 m, 4 Sep 2006 [fr], C. Velásquez-Rúa et al. 5361 (JAUM). Mun. Santa Fé de Antioquia: vereda Cativo, 6°40′46.67′′N, 75°50′31.54′′W, 620 m, 26 May 2016 [im fr], Z. Cordero 2368 (MEDEL). Huila: Mun. Yaguará, vereda La Floresta, finca Las Mercedes, parcela 21, 12 Dec 2001 [st], J. Puerta & E. Mahecha 116 (TOLI10741 [digital image]). Tolima: [Mun. Armero]: corregimiento de Méndez, inmediaciones de Guayabal de Armero y Mariquita, hacienda El Cardonal, parcela permanente 1, 5°5′7.6′′N, 74°46′52.7′′W, 420 m, 14–25 Jun 2013 [st], R. González et al. 1848 (UDBC033849 [digital image]). Mun. Natagaima: 10 Feb 2007 [st], A. Guzmán 25 (TOLI9052 [digital image]).

Discussion

Taxonomic affinities.—In keeping with its name, Zanthoxylum magnifructum has the largest fruits known in Neotropical Zanthoxylum. Within the genus, it is morphologically allied with the species of the Petiolare group of section Macqueria (Reynel 2017, 2020) due to its simple hairs, apical branchlets with clustered bud-scale and leaf scars, terminal and subterminal inflorescences, predominantly 5-merous flowers, perianth differentiated in two whorls, discoid stigma, calyx persistent in fruit, and follicles laterally connate.

In addition to the similarities with Zanthoxylum petiolare A. St.-Hil. & Tul. observed by Reynel (2020), Z. magnifructum is similar to Z. gentryi Reynel, a species that occurs in TDF in the department of Valle del Cauca in Colombia, at 600–1500 m elevation, but in contrast to that species Z. magnifructum has the lateral leaflets petiolulate (vs. sessile), the leaflet margin crenate (vs. entire), the pericarp 4.2–6.3 mm thick (vs. 1.9–2.4 mm thick), the carpels connate axially and laterally (vs. connate only laterally) and the follicles 10.5–13.8 mm long (vs. 4–8 mm long).

Connate follicles are also present in Zanthoxylum quinduense Tul., but Z. magnifructum has a lower elevational range than that species (399–1060 m vs. 1500–3000 m) and also differs in the leaf bud scales clustered, leaf scars present (vs. absent), the petioles terete (vs. canaliculate), the follicles laterally connate to 1/2 their length (vs. 1/3), and the fruits fleshy (vs. leathery).

Sterile material of Zanthoxylum magnifructum can be confused with Z. pucro D. M. Porter because of the similar blade shape, the leaflet margin crenate and the tertiary veins reticulate, but Z. magnifructum differs by having smaller leaf size [(8–) 13–22 (–26) cm long vs. 35–70 cm long] and fewer [4–6 (–9) vs. 7–15] and smaller leaflets [(3.6–) 5.7–13.2 × (1.6–) 2.2–5.5 (–9) cm vs. 10–23 × 4–7 cm].

Sexual dimorphism.—The Neotropical species of Zanthoxylum are mostly dioecious with some polygamodioecious exceptions (Reynel, 2017), which present male or female individuals with unisexual and hermaphrodite flowers in the same inflorescence (Geber et al., 1999; Reynel, 2017). Zanthoxylum magnifructum appears to be a gynodioecious species (Geber et al., 1999), with some individuals that bear only pistillate inflorescences and other individuals that produce mostly staminate inflorescences but have a low percentage of branches bearing pistillate inflorescences, with the pistillate flowers having reduced androecia (Fig. 1I). Although Reynel (2020) considered the pistillate inflorescences to be panicles, we consider them to be axillary racemes, where the subtending leaves show a gradual reduction to bracts towards the branch apex.

Gynodioecy has not been reported previously in Neotropical Zanthoxylum, maybe because it is not common in the genus or because it can be difficult to detect or interpret; it is reported more frequently in temperate herbaceous lineages than in woody or tropical lineages (Caruso et al. 2016). In this system, the proportions of pistillate flowers on hermaphrodite plants can have subtle and continuous fluctuations inside a population, between populations, or even in one individual from one season to another (Geber et al., 1999). Typically, in arboreal species there is only a low probability that a specimen collected from a hermaphrodite individual will include pistillate flowers.

Key to the species of Zanthoxylum that occur in the Tropical Dry Forest of Colombia

  • 1. Leaves unifoliolate…………………………….….…………………....…...………........................……...…….….Z. schreberi

  • 1. Leaves with 3 or more leaflets.

  • 2. Petiole winged at least at apex…….......................................................................………………..……………...….Z. fagara

  • 2. Petiole unwinged.

  • 3. Apical buds with simple curled hairs, perianth whorls not differentiated, all perianth segments deciduous in fruit............................................................................................................................................................Z. mollissimum

  • 3. Apical buds glabrous or with simple straight or stellate hairs, perianth whorls differentiated into calyx and corolla, calyx persistent in fruit.

  • 4. Leaves with stellate hairs………………………………………….…………….........……………Z. rhoifolium

  • 4. Leaves with simple straight hairs or glabrous.

  • 5. Perianth whorls 3–4-merous, carpels 1–2, stigma globose.

  • 6. Leaflets with basal domatium, perianth whorls 4-merous………......................................….Z. limoncello

  • 6. Leaflets without basal domatium, perianth whorls 3-merous...........…….……….……….Z. acuminatum

  • 5. Perianth whorls 5-merous, carpels (2–) 3–5, stigma discoid.

  • 7. Branchlet apices with short zones of clustered leaf and bud-scale scars, follicles partially connate.

  • 8. Lateral leaflets sessile, follicles 4–8 mm long, pericarp 1.9–2.4 mm thick ……....................Z. gentryi

  • 8. Lateral leaflets petiolulate, follicles 10.5–13.8 mm long, pericarp 4.2–6.3 mm thick ........................................................................................Z. magnifructum

  • 7. Branchlet apices without short zones of clustered leaf and bud-scale scars, follicles free.

  • 9. Leaves glabrous, inflorescences axes with transverse lenticels. …………………..........Z. caribaeum

  • 9. Leaves with simple hairs, at least in the base of petiole and rachis adaxially, inflorescences axes without transverse lenticels.

  • 10. Leaves with more than 8 leaflets, follicles D-shaped. …………..................…....Z. martinicense

  • 10. Leaves typically with 4 (–6) leaflets (but leaves from regenerative branches with up to 10 leaflets), follicles ovoid to sub-globose ….……….…….……………....…………..Z. rigidum