Corresponding author: Marcos José da Silva ( firstname.lastname@example.org )
Academic editor: Dmitry Geltman
© 2017 Marcos José da Silva, Thannya Nascimento Soares, Patrícia Rasteiro Ordiale Oliveira.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Silva MJ, Soares TN, Oliveira PRO (2017) Morphological characteristics and genetic evidence reveals a new species of Manihot (Euphorbiaceae, Crotonoideae) from Goiás, Brazil. PhytoKeys 77: 99-111. https://doi.org/10.3897/phytokeys.77.11738
During botanical expeditions between 2010 and 2015, as part of a taxonomic study of Manihot in the Midwest region of Brazil, approximately 500 specimens of the genus were collected. Some of these specimens presented similarities to M. irwinii. However, after careful morphological analyses, associated with genetic evidence, we propose here M. pulchrifolius as a new species. The new species is described, illustrated, and compared to M. irwinii, its most similar species. Furthermore, geographic distribution, conservation status, and period of flowering and fruiting of the novel species are also provided.
Endemism, Manihoteae, mountainous areas, speciation, taxonomy
Manihot Mill. encompasses over 100 Neotropical species, and therefore stands out as one of the largest genera of Euphorbiaceae in Brazil, with ca. 80 species (
During botanical expeditions to the Serra Dourada State Park, in the state of Goiás, Brazil, since October 2010, as part of a floristic survey of Euphorbiaceae, approximately 500 specimens of Manihot were collected, some of them showing similarities to M. irwinii D.J. Rogers & Appan regarding habit and foliage type. After careful morphological analyses of these collections, associated with genetic evidence, we propose herein the new species Manihot pulchrifolius. A detailed description, comments on flowering, fruiting, distribution, environmental preferences, conservation status, and comparisons with morphologically similar species are provided.
The description of the new taxa was based on observations of populations in the field since 2010, analyses of available specimens from herbaria UFG, NY, K, RB, and UB (acronyms follow
Leaves were sampled from 126 plants known as Manihot irwinii D.J. Rogers & Appan, collected in four localities in the state of Goiás (Table
Manihot irwinii sensu lato collected per site and their geographic coordinates.
|Municipalities/Localities||Number of specimens||Voucher/Herbarium||Geographic coordinates/elevation|
|Mossâmedes/Serra Dourada State Park||29||M.J. Silva 5801/UFG||16°05'35.4"S, 50°11'4.5"W, 972 m|
|Corumbá de Goiás/100 m above the waterfall Salto de Corumbá||33||M.J. Silva 5805/UFG||15°50'25"S, 48°46'7"W, 1,067 m|
|Pirenópolis/Serra dos Pireneus, near Serra dos Pireneus State Park||37||M.J. Silva 6389/UFG||15°43'15"S, 49°2'45"W, 730 m|
|Cocalzinho de Goiás/after Serra dos Pireneus State Park||27||M.J. Silva 6406/UFG||15°46'55"S, 48°50'00"W, 1,157 m|
The genetic diversity of the populations studied was assessed based on estimates of the average number of alleles per locus (A), rarefied allelic richness (AR), observed heterozygosity (Ho), expected heterozygosity under Hardy-Weinberg equilibrium (He), and intrapopulation fixation index (f). The genetic structure of the populations was evaluated according to Weir and Cockerham (1984). These analyses were conducted using the package Hierfstat for the statistical software R (
The pattern of differentiation among populations was evaluated by calculating the genetic distance between pairs of populations, based on estimates of pairwise by fixation index (FST). To visualize the pattern of differentiation among populations, the genetic distance matrix was subjected to a cluster analysis using the unweighted pair-group method with arithmetic averages (UPGMA). To assess the degree of representativeness of the dendrogram, the cophenetic correlation coefficient was estimated with 10,000 permutations. These analyses were conducted using R Hierfstat (
BRAZIL. Goiás: Mossâmedes, Serra Dourada State Park, near Pedra Goiana, Cerrado rupestre, on rocky crevices, 16°04'40,5"S, 50°11'20.8"W, 988 m, 21/XI/2014, fl., M. J. Silva & A. A. Alonso 6232 (holotype: UFG; isotypes: NY, F, K, UB).
Shrubs up to 2.5 m tall, erect, glabrous; young branches and young leaves reddish to purplish, green-vinaceous to violet; adult leaves 5-lobed at the plant base, 3-lobed along the stem, or rarely unlobed near inflorescence; long racemes or panicles (up to 27 cm long), erect to pendent, axes reddish to purplish; calyx of staminate flowers reddish or purplish with yellow margins, filaments pubescent; bracts and bracteoles of flowers of both sexes reddish to purplish; fruits dark green with violet to purplish wings.
Shrubs 1–2.5 m tall, monoecious, erect; stems and adult branches robust, cinereous, glabrous, waxy, and glossy; young branches and young leaves reddish to purplish, green-vinaceous to violet, including axes of inflorescences and petioles; branches dichotomously branched near apex, sometimes pendent in specimens taller than 1.2 m; latex yellowish, copious; petiole 4.5–13 cm long, robust, canaliculated above, dark purplish to violet. Stipules 1.9–2 cm long, linear, entire to discreetly serrate, caduceus. Leaves in alternate spiral arrangement; lamina firmly chartaceous, glabrous on both surfaces, the basal ones 5-lobed, the others 3-lobed, or unlobed near inflorescence, lobes conspicuously overlapping at sinus, 8.4–15 × 4.5–10 cm, widely oblong-obovate, elliptic-obovate to obovate, apex cuspidate, sometimes oblique, base cordate; venation camptodromous-brochydodromous, primary and secondary veins pinkish, purplish, violet, or rarely yellowish, the primary ones prominent on both surfaces, the secondary ones subparallel to the midrib, impressed on both surfaces, bifurcate or not at apex; adaxial surface dark green and opaque in adult leaves, or light green, castaneous, reddish to purplish in young leaves; abaxial surface opaque green to cinereous with a smooth wax pattern; racemes 5–17 cm long, or panicles 17–24 cm long, laxy, terminal or in the dichotomy of the branches, solitary or in clusters of 2 or 3, erect to pendent, bisexual; if racemes, they have two opposite pistillate flowers at the base and another staminate; if panicles, the secondary axes are similar to racemes, but sometimes without pistillate flowers at the base of secondary axes. Staminate flowers 21–25 mm long; buds 9–10 mm long, globoid to orbicular, reddish, obtuse at apex, glabrous and waxy externally; bracts 11–12 × 2.5–3.3 mm, oval, elliptic, entire, acuminate at apex, reddish, persistent, glabrous on both surfaces; bracteoles 5.7–7 × 1–2 mm, linear, subalternate, distributed on the lower third of the pedicel, glabrous on both surfaces, margins entire, not ciliate, caduceus; pedicels 8.5–12 mm long, cylindrical, reddish to purplish, waxy, glabrous; calyx 12–15 × 10–11 mm, widely campanulate, reddish with yellowish margins, glabrous externally and shortly tomentose internally, lobes widely triangular to ovate, apex obtuse; stamens 10, in two whorls of five, filaments 8–8.2 mm long, pubescent distally, anthers 3–3.2 mm long, oblongoid, yellowish; disk 10-lobed, dark yellow, lobes rounded. Pistillate flowers 19–25 mm long; buds 6–7 mm long, ovoid, glabrous, yellowish with reddish spots; bracts 8–15 × 2.4–3 mm, oval-lanceolate to lanceolate, vinaceous to purplish, entire, acuminate at apex, persistent, glabrous, not ciliate; bracteoles 10–12 × 2–3.5 mm, lanceolate, margin discreetly serrate, similar to the bracts in color; pedicels 13–16 mm long, cylindric-clavate, glabrous, greenish, sepals 8.2–11 × 3.3–5 mm, ovate to oval-elliptic, rarely lanceolate or triangular, shortly pubescent in the upper third internally, apex obtuse, yellowish with reddish pigmentation, margins involute; ovary 3–3.2 × 2–2.1 mm, oblongoid to globoid, glabrous, not winged, green, disk discreetly lobed, yellowish, styles 3, conspicuously united at the base, free portion 2.1–2.2 mm long, with papilose apex. Capsules 12–14 × 16–17 mm, globoid, smooth, glossy, winged, with septicidal and loculicidal dehiscence, green to purplish, slightly glossy. Seeds 8–10 × 4–5 mm, oblongoid, cinereous, with dark spots; caruncle 0.9–1 mm long, sessile, reniform, cream to whitish.
Manihot pulchrifolius. A Flowering branch B Stipule C Staminate bud D Staminate bract E Staminate bracteole F Staminate flower G Staminate flower with calyx split and open H Stamen I Pistillate bud J Pistillate bract K Pistillate bracteole L Pistillate flower M Fruit N Seed, ventral side O Seed, dorsal side. Drawn by Cristiano Gualberto from the holotype.
Manihot pulchrifolius. A Habit; note the plant growing between rocky crevices B Habit; detail of the waxy stem C Portion of the stem showing inflorescences in clusters at the dichotomy of the branches D Adult panicle E Portion of the panicle showing the staminate buds and flowers with vinaceous calyx and yellow margins F Staminate flowers G Pistillate flowers H Mature fruits; note the violet wings.
Manihot pulchrifolius is endemic to the state of Goiás, where it was found growing in Serra Dourada (Figure
The species has been collected with flowers and fruits from November to July. However, the flowers are more usual from January to March, whereas the fruits are more abundant from April to July.
The specific epithet “pulchrifolius” alludes to the beautiful foliage of the species, especially in the leaf flushing stage, when the leaves are reddish or purplish to green-vinaceous to violet.
Given that the populations have more than 50 individuals and the vegetation where they grow is commonly found in the central part of the state of Goiás (in the municipality of Goiás and neighboring municipalities), we consider M. pulchrifolius as Least Concern (LC) according to
BRAZIL. Goiás: Mossâmedes, Serra Dourada State Park, on the way to Pedra Goiana, 9 Dec 2009, fl., A. M. Teles 658 (UFG); ib., 30 Oct 2010, fl., M. J. Silva et al. 3138 and 3139 (UFG); ib., near Pedra Goiana, 16°04'34,7"S, 50°11'28"W, 994 m, 21 Nov 2014, fl., M. J. Silva & A. A. Alonso 6234 and 6235 (UFG); ib., 16°04'40,5"S, 50°11'20.8"W, 988 m, 21 Nov 2014, fl., M. J. Silva & A. A. Alonso 6230 and 6231 (UFG); District of Mirandópolis, Rildo Nogueira farm, 27 Nov 2010, fl., M. J. Silva 3194 and 3198 (UFG); ib., near the first gate that leads to the park headquarters, 16°04'46,9"S, 50°11'28,4"W, 985 m, 29 Jan 2011, fl., fr., M. J. Silva 3372 (UFG); ib., 4 km above the Piçarrão stream, 16°04'17,4"S, 50°11'26,1"W, 993 m, 30 Apr 2011, fl., fr., J. E. C. Júnior 15 and 18 (UFG); region after Areal, 16°04'00,9"S, 50°10'8,9"W, 953 m, 28 May 2011, fr., J. E. C. Júnior 51 (UFG).
Manihot pulchrifolius was identified by
Manihot pulchrifolius has leaves that are 5-lobed at the base of the stem, 3-lobed above the base of the plant or along the plant, or rarely unlobed near the inflorescence, with robust petiole, reddish to dark violet, and leaf blade cinereous, green-opaque, or reddish on lower surface (vs. 3-lobed leaves, and commonly unlobed near inflorescence, thin petiole, greenish, and leaf blade whitish in M. irwinii), racemes and panicles 5–17 cm and 17–24 cm long, respectively (vs. racemes 7–12 cm long), floral buds reddish (vs. yellowish green to greenish), staminate flowers 21–25 mm long, calyx widely campanulate, filaments pubescent distally, staminate bracts and bracteoles reddish, 11–12 × 2.5–3.3 and 5.7–7 × 0.1–0.2 mm, respectively (vs. staminate flowers 14–15 mm long, calyx narrowly campanulate, filaments glabrous, staminate bracts and bracteoles yellowish green with discreet purplish spots, 11–12 × 2.5–3.3 and 5.7–7 × 0.1–0.2 mm, respectively).
Systematically, the new species can be situated in Manihot section Quinquelobae Pax according to
A total of 50 alleles were found for the seven loci evaluated in populations of M. irwinii sensu lato, ranging from three to eleven alleles per locus. The populations studied showed high and similar genetic diversity, which was also observed in other species of the genus (
The population genetic structure analysis showed an estimated value of θ of 0.363, indicating that 36.3% of the genetic diversity is in the component between populations. This level of genetic structure is considered very strong (
This pattern of genetic differentiation between populations can be observed in the dendrogram constructed from the FST pairwise matrix, which clearly points out the separation from the population collected in Serra Dourada in a distinct group (Figure
Genetic diversity parameters estimated for four populations of Manihot irwinii sensu lato, based on seven microsatellite loci.
|Mossâmedes (n = 29)||3.714||3.38||0.454||0.389|
|Corumbá de Goiás (n = 33)||2.429||2.17||0.321||0.368|
|Pirenopólis (n = 37)||4.286||3.76||0.578||0.574|
|Cocalzinho de Goiás (n = 27)||3.143||2.952||0.434||0.464|
Genetic groups (K) estimated by attribution analysis using the software STRUCTURE. The highest ΔK indicates the most probable number (K) of groups formed by individuals sampled from putative populations of Manihot irwinii sensu lato herein analyzed using seven microsatellite markers.
Genetic assignment of four populations of Manihot irwinii sensu lato evaluated with seven microsatellite markers, based on Bayesian statistics using the software STRUCTURE.
The authors would like to thank: the curators and staff of all the aforementioned herbaria for providing loans of their collections; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the grant on productivity to the first author (Process no. 307371/2013_1); Cristiano Gualberto for the illustrations; and Suzana Oellers for English language editing.