Sapranthus Seemann is a Neotropical genus comprising nine species of small- to medium-sized trees distributed in Mexico, Central America, and Colombia (Schatz et al., 2018; Ortiz-Rodriguez & Martínez-Velarde, 2021). Species of Sapranthus can be distinguished from other Neotropical genera of Annonaceae by their leaves with pocket domatia in the axils of the secondary veins, trimerous flowers with several carpels, with large, fleshy and distinctly veined petals, often with reddish color, unpleasant smells, and food bodies at the base of inner petals, as well as their large, fleshy, spherical or cylindrical (apocarpic) fruits (Schatz et al., 2018). Almost all Sapranthus species (except Sapranthus viridiflorus) occur in dry forests and are deciduous trees (Schatz, 1998). Similar to other groups of plants (e.g., Amphitecna, Bignoniaceae; Gómez-Dominguez et al., 2021), the distributional range of Sapranthus encompasses two regions within Mesoamerica having high species endemism, the northern region (from Mexico to Nicaragua) with six species, and the southern region (from Costa Rica to Colombia) with two species (Table 1). Only two species (S. violaceus and S. microcarpus) can be considered widely distributed, and they are also the ones with the greatest morphological variation (Schatz et al., 2018). The morphologies of Sapranthus species are quite variable, with most exhibiting clear differences in leaves, flowers, and fruit morphology (Schatz et al., 2018; Ortiz-Rodriguez & Martínez-Velarde, 2021). Among the most variable of these features in Sapranthus are the presence of hairs on the leaves, the number of secondary veins, the position of the inflorescences, the size of the sepals and petals, the arrangement and number of ovules, and the ornamentation of the fruit surface (Schatz, 1998; Schatz et al., 2018; Ortiz-Rodriguez & Martínez-Velarde, 2021). Other important features for species identification include the number of flowers per inflorescence, the length of the pedicels, the shape of sepals and petals, the number of veins in the petals, and petal color (Schatz, 1998; Vélez-Arango & Cogollo-Pacheco, 2007; Schatz et al., 2018).

Table 1 Species currently recognized in Sapranthus (Annonaceae) and their respective geographical distributions. The species are ordered by the morphological groups recovered in the clustering analysis.
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In earlier studies, phylogenetic analyses placed Sapranthus within the tribe Miliuseae (subfamily Malmeoideae), where together with the Neotropical genera Desmopsis, Stenanona and Tridimeris, it forms the subtribe Sapranthinae (Ortiz-Rodriguez et al., 2016a). Within Sapranthinae, Sapranthus is the sister group of Tridimeris, and both genera share leaves with pocket domatia in the axils of the secondary veins (often hidden by leaf pubescence in Sapranthus) and large and fleshy fruits, but differ markedly in the morphology of their flowers, since species of Tridimeris have dimerous flowers with a reduced number of carpels (Ortiz-Rodriguez et al., 2016b). So far, neither the phylogenetic relationships nor the morphological similarities between Sapranthus species have been fully studied.

Here, a new species of Sapranthus with non-foetid flowers and large-sized individuals (used as shade trees in coffee plantations of Guatemala and El Salvador) is illustrated and described, and we carried out multivariate cluster analyses of all nine currently recognized species of the genus to infer the morphological affinities.

Materials and methods

To infer the morphological similarities among the ten species of Sapranthus, we performed a hierarchical clustering analysis on a matrix that included 17 leaf and flower traits (Supplemental Table S1). The data were analyzed using the unweighted pair group method with arithmetic mean (UPGMA, Sokal & Michener, 1958) and the Gower index (Gower, 1971), allowing a simultaneous use of binary and continuous characters (Tuler et al., 2017; Svoboda and Ballard Jr., 2018; Wahlsteen & Tyler, 2019; Gómez-Dominguez et al., 2021). All morphological characters were obtained from original species descriptions (Schatz et al., 2018), herbarium specimens deposited at MEXU (www.ibdata.ib.unam.mx), and type specimens available online (https://www.gbif.org/ and https://plants.jstor.org/). The UPGMA results were contrasted with those derived from other clustering algorithms, specifically Ward, single linkage, complete linkage, WPGMA, WPGMC, and UPGMC, implemented in the R-package stats, using the function hclust (R Core Team 2020: https://www.r-project.org/). We then determined the similarities and differences among the various clustering dendrograms by calculating the cophenetic correlation (a Pearson’s measure) between each clustering result using the cor.dendlist and the corrplot functions from the corrplot R-package (Wei & Simko, 2017). For each dendrogram, the agglomerative coefficient was calculated using the agnes function from the cluster R-package (Maechler et al., 2019). The agglomerative coefficient measures the amount of clustering structure, with values closer to 1 suggesting stronger clustering structure. Also, the Fowlkes-Mallows Index (from the dendextend R-package, Galili, 2015) was used to compare the species composition within clusters (k = 3–8) obtained from the UPGMA analysis and other algorithms. The optimal number of morphological clusters in Sapranthus was determined based on the greater similarity between clustering algorithms (values closer to 1). We further performed an internal clustering validation (a cluster stability test) by calculating the average silhouette width (Si) for each cluster (k = 3–8) resulting from each of the algorithms used. While Si values greater than 0.71 suggest strong structure and cluster stability, values between 0.51 and 0.70 are interpreted as reasonable, values between 0.26 and 0.50 indicate weak structure, and values lower than or equal to 0.25 are not worth further discussion (Kaufman & Rousseeuw 2005). The graphical representation of the UPGMA dendrogram was carried out in the R software, using the function hclust and the R-packages ape, and ggtree (Yu et al., 2017; Paradis & Schliep, 2018).

The newly described species was recognized by a unique combination of features (Donoghue, 1985) identified through comparisons with morphologically similar taxa and literature review (Schatz, 1998; Schatz et al., 2018). We then assessed the conservation status of the new species by calculating the extent of occurrence (EOO) and the area of occupancy (AOO, based on user defined cell width of 2 km) using the GeoCAT tool (Bachman et al., 2011) and applying the IUCN Red List Categories and criteria (IUCN, 2022).

Results

The UPGMA dendrogram is shown in Fig. 1. The results of this analysis are very similar to those obtained using other clustering algorithms (correlation values between 0.77 and 0.98, Supplemental Fig. S1). The agglomerative coefficient value for the UPGMA dendrogram was 0.76 (between 0.71 and 0.86 in analyses conducted with other approaches), suggesting a moderate to strong structure among species of Sapranthus. The Fowlkes-Mallows Index showed that five groups (k = 5) show significantly similar clusters when the UPGMA is compared to the other clustering algorithms (mean FM value= 0.91). Silhouette width values consistently showed the highest values (Si value 0.49) when UPGMA dendrogram was divided into five clusters.

Fig. 1
figure 1

Morphological similarities among the 17 specimens of Sapranthus (Annonaceae). Dendrogram based on the results from an UPGMA analysis. Groups are color-coded: the Sapranthus violaceus group (brown), the Sapranthus viridiflorus group (green), the Sapranthus palanga group (red), and the Sapranthus microcarpus complex (orange). Dashed boxes indicate the three main clusters, from top to bottom, the Sapranthus violaceus complex (brown, green and red), the Sapranthus microcarpus complex (orange), and a representative species of the genus Tridimeris (blue).

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The UPGMA results indicate that the genus Sapranthus can be divided into four morphological sub-groups arranged in two main clusters (Fig. 1). The first cluster (named here as the Saprathus violaceus complex) consists of seven species characterized by the combination of large leaves (with more than 10 secondary veins per side) that are sparsely to densely covered by long hairs below, and large flowers (with sepals greater than 10 mm long, and petals greater than 30 mm long and more than 15 mm wide). The Saprathus violaceus complex is further divided into three subgroups: (1) the Sapranthus violaceus group, composed of S. foetidus, S. hirsutus and S. violaceus, and characterized by single-flowered and leaf-opposed inflorescences and red flowers with several carpels and ovules; (2) the Sapranthus palanga group consisting of two species, S. palanga and S. chiapensis, with multi-flowered inflorescences borne on the leafless parts of the branches (ramiflory) or along the main trunk (trunciflory), and flowers with red petals and several carpels and ovules; and (3) the Sapranthus viridiflorus group, which also consists of two species (S. isae and S. viridiflorus) having leaf-opposed and single-flowered inflorescences, and flowers with green petals and a reduced number of carpels and ovules (Table 1). The second cluster (named here as the Saprathus microcarpus complex) is composed of three species, Sapranthus campechianus, S. microcarpus and the newly described species. All three of these species have relatively short leaves with fewer than 10 secondary veins per side, usually sparsely covered by short hairs below or glabrous, and solitary flowers that are leaf-opposed with sepals less than 10 mm long, petals less than 30 mm long and less than 10 mm wide, and a reduced number of carpels and ovules (Fig. 2 and Table 1).

Fig. 2
figure 2

Sapranthus pinedai Ortiz-Rodr. (Annonaceae). A. Habit, a tree more than 15 m tall. B. Twig, fruit and seeds, note the greyish stem on the twigs and the fruits with very thick testa. C. Tree bark. D. Lunate to wedge-shaped seeds. Photos by José Linares.

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Discussion

The results presented here show that Sapranthus can be divided into four morphological groups within two main clusters (Fig. 1). These groups do not necessarily represent lineages and, according to internal clustering validation (Si value= 0.49), their stability should be tested with additional data. Thus, the resulting groupings provide new insights into the sectional classification of the genus Sapranthus, on the geographic distribution of its species, and on the morphological affinity of the putative new species.

Sectional classification in Sapranthus

The results presented here do not support the current sectional classification of the genus Sapranthus (Schatz et al., 2018). As it is currently circumscribed, sect. Microsapranthus includes only S. microcarpus, characterized on the basis of its verrucose leaves, pocket domatia in the axils of secondary veins, carpels with uniseriate ovules, orange fruits with a thin testa (bird-adapted), and discoid seeds (Schatz et al., 2018). By contrast, sect. Sapranthus includes all other species of Sapranthus, having non-verrucose leaves without domatia, carpels with biseriate ovules, large, fleshy fruits of dull colors (mammal-adapted), and wedge-shaped seeds (Schatz et al., 2018). Detailed analysis of various specimens and species of Sapranthus (Supplemental Table S2) revealed that the presence of verrucose leaves is not constant in Sapranthus microcarpus and that the presence of pocket domatia in the axils of the secondary veins is a feature present in all species of Sapranthus. In some species the domatia are hidden by pubescence, but are easily detected if searched; in other species, such as Sapranthus microcarpus, they are quite conspicuous. Orange fruits are not common, but they are also present in S. campechianus (https://www.naturalista.mx/observations/10594267) and probably in other species, such as S. violaceus, for which ripe fruits are poorly known. Moreover, our morphological similarity analyses showed that Sapranthus microcarpus is nested in a morphological cluster that also includes Sapranthus campechianus and the new species S. pinedai (Fig. 1). Thus, based on the morphological evidence newly provided, S. campechianus and the new species are likely to enlarge the monotypic section Microsapranthus sensu Schatz et al. (2018). These results are consistent with an old delimitation of sect. Microsapranthus (Fries 1930), where species with small flowers, reduced carpel and ovule number, and less conspicuous petal venation compared to the rest of the species, were included. The results presented here suggest that additionally the size of the leaves, the number of secondary veins, and leaf pubescence could be important characteristics for the circumscription of sect. Microsapranthus. Further studies based on molecular data are needed to test this hypothesis.

Sapranthus morphology and distribution

The results of the morphological similarity analysis showed that several morphological groups can be identified in Sapranthus based on leaf and flower characteristics (Fig. 1 and Table 1). The green flowers of the Sapranthus viridilforus group are unusual in the genus and are only present in two species endemic to southern Mesoamerica (from Costa Rica to Colombia). The small leaves with fewer than ten secondary veins per side and small flowers (petals less than 30 mm long and less than 10 mm wide) with few carpels and ovules are present only in the species of the S. microcarpus complex, distributed in northern Mesoamerica (from Mexico to Honduras and El Salvador). While large leaves and flowers (most with several carpels and ovules) are present in five species (S. palanga group and S. violaceus group) distributed from Mexico to Colombia. Most of the species in the violaceus complex have flowers with dark-red petals that release an unpleasant odor during anthesis (Schatz et al., 2018). That unpleasant odor is absent in the species of the S. microcarpus complex and in S. isae (of the S. viridiflorus group) (Schatz et al. 2018), so the differences in the characteristics of the flowers in each morphological group probably is related to differences in the reproductive ecology of their species.

Most species of Sapranthus are distributed in northern Mesoamerica, with Mexico having the greatest species richness. Based on biogeographic analysis, northern Mesoamerica has been hypothesized as the region of origin for the genus Sapranthus and its relatives (Ortiz-Rodriguez et al., 2018).

A new species of Sapranthus with non-foetid flowers

The results of the similarity analysis show that the putative new species belongs to the Sapranthus microcarpus complex along with S. microcaparpus and S. campechianus. The three species share many floral and foliar characteristics, such as the small number of secondary veins and the size of the petals and sepals, but also exhibit noticeable differences in their size of the individuals, abaxial leaf pubescence, the number of carpels and ovules, the arrangement of the ovules, and especially in their characteristics of the fruits and seeds. Hence, the putative new species is best treated as a separate taxon, which is described below and compared to its morphologically similar taxa (Table 2).

Table 2 Comparison of diagnostic morphological features among Sapranthus pinedai (Annonaceae) and its close relatives.
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TAXONOMIC TREATMENT.

Sapranthus pinedai Ortiz-Rodr. & J. Linares, sp. nov.—Type: El Salvador. Departamento de Santa Ana: Cafetales de la hacienda San Marcelino, en los alrededores del Cerro Chino, [13.805120°, −89.602453°], 1400 m, April 23, 1994, fl., J.L. Linares & C.A. Martínez 1296 (holotype: MEXU [!]; isotypes: MEXU[!], EAP [!]). (Figs. 2, 3 and 4).

Fig. 3
figure 3

Sapranthus pinedai Ortiz-Rodr. (Annonaceae). A. Small flower with narrow and elongated petals. B. Internal view of flower, in the center, a few carpels and stamens (exudate on the carpels indicates a mature flower), the inner petals with a yellow blotch at the base, just above the food bodies (six ridges separated by furrows). C. Few large monocarps, sessile or nearly so, with a smooth and glabrous surface. D. Monocarps inside, a very thick testa, and seeds in two rows. Photos by José Linares.

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Fig. 4
figure 4

Geographic distribution of Sapranthus pinedai (Annonaceae). A. Northern Mesoamerican region. B. Location of the two known localities of Sapranthus pinedai.

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Diagnosis.—Similar to Sapranthus microcarpus and Sapranthus campechianus, but differing from both species by its essentially glabrous leaves, short pedicels, fewer carpels, more ovules per carpel, biseriate ovules, larger sessile fruits with a thick testa, and by its several seeds, which are lunate to wedge-shaped (Table 2).

Trees 10–20 m tall, 40 cm diameter; young twigs, young leaves and petioles densely covered with appressed and erect golden hairs, soon glabrous, branches often covered with dot-like warts and lenticels, greyish in vivo. Leaves with petioles 4–10 mm long, 1 mm diameter; lamina elliptic, 6–18 cm long, 3–8 cm wide, slightly coriaceous to chartaceous, shiny dark green above, dark green below, glabrous above, except with golden brown hairs at base of primary vein, essentially glabrous below, with only a few scattered golden brown hairs on the veins, usually verruculose, then black-dotted below; base obtuse to rounded (rarely acute), slightly decurrent; apex acute to acuminate (acumen 5–10 mm long); venation weakly brochidodromous, primary vein impressed above and canaliculate towards the base, strongly raised below, secondary veins 8–10 on either side of primary vein, slightly raised above, strongly raised below, with pocket domatia below in the axils between the secondary and primary veins, tertiary veins slightly percurrent, primary and secondary veins yellow in vivo. Inflorescence indument, peduncles, pedicels and outer side of bracts and sepals densely to sparsely covered with appressed and erect, golden-brown hairs, petals sparsely so, with the highest density of hairs on petal venation. Inflorescence one- flowered, leaf-opposed or rarely on the leafless part of branches (ramiflory); pedicels (including the peduncle) 10–15 mm long, up to 1 mm diameter, up to 20 mm long and 3–4 mm diameter in fruit; bract leafy, ovate to narrowly triangular in flower, orbicular in fruit due to the abscission of the bract apex, 4–8 mm long, 2–3 mm wide. Flowers pendant, trimerous; sepals 3, free, distinctly 4–6-veined, ovate to triangular, 5–10 mm long, 3–5 mm wide, spreading to reflexed; petals 6, free, in two subequal whorls, narrowly ovate to triangular, aristate at apex, 20–30 mm long, 4–6 mm wide, membranous, red, 5–6-veined, inner petals with a cream-yellow blush at the base inside, also with 6 ridges separated by 5 furrows (the food bodies) above the blush; carpels 6–8, 1.5–2 mm long, ovary densely covered with appressed hairs, ovules 7–12, in two rows, stigma subglobose to ellipsoid, 0.5–1 mm diameter, sparsely covered with appressed hairs, yellow during anthesis; stamens around 50, 1–1.5 mm long, extrorse, filament very short, apical part of connective expanded over the thecae, shield-shaped, ellipsoid to angulate, glabrous, red during anthesis. Monocarps 4–7, green, subglobose to ellipsoid, 40–80 mm long, 30–60 mm wide, wall 10–20 mm thick, stipes up to 0.5 mm long (almost sessile), surface smooth, initially densely covered with erect and appressed hairs, glabrescent. Seeds 10–11 per monocarp, in two rows, lunate to wedge-shaped, 20–26 mm long, 10–15 mm wide, 0.5–0.8 mm high, lamellate ruminations.

Habitat and ecology.—The species inhabits the western montane cloud forests of Guatemala and El Salvador. This vegetation type, also called lower moist broadleaf and semideciduous forest, [IA3c(1)] in the UNESCO classification, is characterized by the dominance of oak (Quercus) and broadleaf species of Lauraceae, Annonaceae, Fabaceae, and Rubiaceae. In the type locality, Sapranthus pinedai forms part of the tree stratum together with species of Quercus (Fagaceae), Ilex (Aquifoliaceae), Styrax (Styracaceae), Maytenus (Celastraceae), Cojoba (Fabaceae), Lonchocarpus (Fabaceae), Schoepfia (Schoepfiaceae), Prunus (Rosaceae), and Symplococarpon (Pentaphylacaceae). Sapranthus pinedai is a large-sized tree used as a shade tree in coffee plantations. Due to constant pruning, individuals growing in coffee plantations do not exceed 15 m in height.

Recent field observations and collection notes show that the flowers of Sapranthus pinedai lack the typical unpleasant odor recorded in several Sapranthus species. However, it has been mentioned that both flowers and leaves have a faint “sea smell” (possibly due to amines).

Phenology.—The species was found in full bloom and with immature fruits from April to June and with few flowers and ripe fruits in December.

Etymology.—This species is named to honor Luis Armando Pineda Peraza (b. 1982) from the Ministry of Environment and Natural Resources of El Salvador. Luis Pineda has worked tirelessly for the preservation of the western forests of El Salvador, where the type locality of the new species is found.

Additional specimens examined.— EL SALVADOR. Departamento de Santa Ana: from the type locality, December 08, 2022; fl., fr.; J.L. Linares & C.A. Martínez s.n. (CURLA). GUATEMALA. Departamento de Chiquimula: Municipio de Esquipulas, 4 Km al sur de Esquipulas, por la carretera a la frontera con El Salvador, [14.527475°, −89.347536°] 1400 m., June 02, 2004, fl., J.L. Linares & C.A. Martínez 7457 (MEXU).

Preliminary conservation assessment.—There are only two known subpopulations of Sapranthus pinedai, which are located within a discontinuous fragment of montane cloud forest (Fig. 4) at the border between Guatemala and El Salvador. Both subpopulations appear isolated from each other by more than 85 km. The area of occupancy (AOO) of Sapranthus pinedai was estimated at 8.0 km2 and the extent of occurrence (EOO) at 0.0 km2, suggesting a very restricted overall distribution. However, at the type locality, the species is used as a shade tree for coffee plantations and through this activity it has been preserved for almost 30 years since its first collections. Based on the above and according to the criteria established by the IUCN, it is possible to tentatively determine that the species is Endangered [(EN B1ab (iii) +2ab (iii))].

Notes.—Sapranthus pinedai is probably the most robust species known to date. Individuals more than 10 m tall with d.b.h. of more than 30 cm are unusual in Sapranthus. Its essentially glabrous leaves are also unusual in the genus, where most species (including S. microcarpus and S. campechianus) have leaves sparsely to densely pubescent below. Few species have flowers with a reduced number of carpels, and S. pinedai joins S. viridiflorus (Sapranthus violaceus complex) in having the lowest number of carpels known to date. The fruits of S. pinedai are among the largest within the genus, standing out from all the species due to its much thicker testa. Lastly, habitat preferences in S. pinedai are uncommon. The only other species known to inhabit montane forests above 1200 m elevation is S. viridiflorus. In the case of S. pinedai, its distribution in montane cloud forests with pine-oak associations is unique within Sapranthus.

KEY FOR THE IDENTIFICATION OF SPECIES OF SAPRANTHUS (ANNONACEAE) FROM NORTHERN MESOAMERICA (FROM MEXICO TO NICARAGUA).

  1. 1.

    Multi-flowered inflorescences (flowers maturing in succession) borne on perennial short shoots, ramiflorous or trunciflorous.………………………………………………2

  2. 2.

    Single-flowered inflorescences (flowers solitary), leaf-opposed, opposite leaf scar or occasionally trunciflorous……………………………………..…………………….…...3

  3. 3.

    Pedicels 7–10 mm long in flower; outer petals 28–36 mm long, 10–16 mm wide; monocarps (fruits) bearing lamellar, lacerate, plate-like excrescences to 10 mm high on their surface —Mexico..……………….……………………………………S. chiapensis

  4. 4.

    Pedicels 15–40 mm long in flower; outer petals 70–110 mm long, 15–40 mm wide; monocarps smooth on their surface —Nicaragua………………….………….S. palanga

  5. 5.

    Sepals less than 10 mm long; outer petals 15–40 mm long, 3–10 mm wide; 6–13 carpels per flower..............................................................................................................4

  6. 6.

    Sepals more than 10 mm long; outer petals 40–190 mm long, 12–70 mm wide; 15–25 carpels per flower………………………………………..………………………....……5

  7. 7.

    Leaves with 5–8 secondary veins on each side; pedicels 20–40 mm long in flower; the ovules in each carpel arranged in one row; monocarps cylindrical or nearly so, stipes 3–4 mm long; seeds discoid—Mexico, Guatemala, El Salvador, Honduras………………………………………………….S. microcarpus

  8. 8.

    Leaves with 8–10 secondary veins on each side; pedicels 10–20 mm long in flower; the ovules in each carpel arranged in two rows; monocarps globose or nearly so, stipe minute (up to 0.5 mm long) or absent (sessile); seeds wedge-shaped………………………………………………………………….6

  9. 9.

    Sepals more than 18 mm long; the general pubescence consists of long hairs up to 2 mm long—Honduras, Nicaragua...…………………………………….……...S. hirsutus

  10. 10.

    Sepals less than 15 mm long; the general pubescence consists of short hairs up to 1 mm long…………………………………………………..……………………7

  11. 11.

    Leaves densely covered with erect and appressed hairs below; carpels 9–13, ovules 6–8 per carpel; monocarps 10–35 mm long—Mexico, Belize, Guatemala, Honduras……………………………………S. campechianus

  12. 12.

    Leaves glabrous or nearly so; carpels 6–8, ovules 7–12 per carpel; monocarps 40–80 mm long—El Salvador, Guatemala………..S. pinedai

  13. 13.

    Fruit surface smooth—Mexico, Guatemala, El Salvador, Honduras, Nicaragua…………………………………………………………………S. violaceus

  14. 14.

    Fruit surface with lamellar, lacerate, plate-like excrescences—Mexico.................................................................................................S. foetidus