Croton piriquetifolius M.J. Silva & Sodré, 2024

Silva, Marcos José Da, Sodré, Rodolfo Carneiro, Alonso, Alexandre Antonio & Santos, Igor Soares Dos, 2024, A new species of Croton sect. Geiseleria (Euphorbiaceae) from Brazil, supported by macro- and micromorphological data, Phytotaxa 646 (2), pp. 143-156 : 144-152

Croton piriquetifolius M.J. Silva & Sodré sp. nov. ( Fig. 1 )

TYPE:— BRAZIL. Bahia: Mucugê, estrada Igatu-Mucugê , a 3 km de Igatu , 12º53’53”S, 42º08’41”W, 960 m, 14 July 1997 (fl.), H.P. Bautista, N. Hind & S. Smith 3611 (holotype ALCB-051588 !; isotypes CEPEC-77382 !, SPF-123797 !, HUEFS-26109 !) .

Diagnosis:— Croton piriquetifolius is most similar to C. glandulosus , but differs in having leaves with acropetiolar patelliform sessile nectaries on the adaxial surface (vs. basilaminar, cupuliform or stipitate-patelliform nectaries on the abaxial surface in C. glandulosus ), pistillate flowers with pedicel 1.8–2.4 mm long and sepals 3–4.5 × 1.3–2.7 mm, hairy on both surfaces (vs. pedicel 0.2–0.5 mm and sepals 1−2.5 × 0.3−1.1 mm, hairy ventrally), capsules uniformly brownish (vs. green capsules with whitish color on the sutures of the septa and locules).

Description:—Subshrub or shrub 0.7–1 m tall, erect, monoecious, densely branched distally, adult branches brownish and green-brownish when young, both with stellate and stellate-porrect trichomes, the first ones sessile, with 9–11 rays; the second ones with 2 or 3 rays, with stipe measuring 0.2–0.3 mm long, and rays up to 0.5 mm long; latex scarce, hyaline. Leaves spirally alternate along the stems; petioles 0.9–3 cm long with 2 patelliform sessile nectaries 0.7–0.8 mm diam. at the apex on the adaxial surface; blades 4.8–5.5 × 1.6–2.6 cm, ovate, oval-oblong or ovallanceolate, base obtuse or truncate, apex obtuse and shortly mucronulate, margin serrate, with cupuliform nectaries in the sinuses, membranaceous, discolorous, adaxial surface light green and abaxial surface green-ferrugineous, the first ones with simple and stellate-porrect trichomes with 7–10 rays, the second ones multiradiate in 2 or 3 whorls, with stipe measuring 0.2–0.3 mm long, and rays up to 0.5 mm long, both, tomentose to the touch; brochidodromous venation, with 6–8 pairs of secondary veins, primary and secondary veins visible, both impressed on both surface; stipules 2.1–2.2 × 0.3–0.4 mm, lanceolate with 4 or 5 pyriform and sessile glands at the base, glabrous internally and with stellate trichomes externally. Inflorescences bisexual with 1.3–2.4 cm long, terminal, with 2 or 3 pistillate flowers at the base axis and 15 or 16 staminate flowers continuous along the inflorescence axis; staminate bracts 2–2.1 × 0.39–0.4 mm, lanceolate, with 4 pyriform glands at base, glabrous internally and externally stellate, persistent; pistillate bracts 2.7–2.8 × 0.49–0.5 mm, narrowly elliptic, similar to the staminates ones. Staminate flowers 5.7–5.9 mm long, yellowish, actinomorphic; pedicels 2.3–2.9 mm long; calyx 5-lobed, lobes 1.7–1.8 × 1.3–1.4 mm, equal, oval-triangular, with acute apex, slightly united at the base, ventrally glabrous, dorsally stellate; petals 2.1–2.2 × 0.9–1 mm, elliptic, with obtuse apex, villous internally until upper third and with sparse stellate trichomes externally, ciliate on the margins, the longest cilia at the base; stamens 11, 3.1–3.2 mm long, with filaments pubescent at base, anthers 0.5–0.6 mm long, oblong, glabrous; disk with 5 segments widely depressed obovoid, yellowish with margin lightly crenulate; receptacle villous. Pistillate flowers 7.6–7.7 mm long; pedicels 1.8–2.4 mm long; sepals 5, unequal, 3–4.5 × 1.3–2.7 mm, oblong-obovate, with obtuse or acute apex, margin entire, plane, eglandular with stellate trichomes externally, sparsely pubescent internally, free, prefloration valvate; petals 5, glanduliform; ovary 1.9–2 × 1.9–2 mm, widely ovoid, yellowish-ferrugineous with tomentose indument of stellate trichomes; styles 3, deeply bifid, 2.4−2.5 mm long, covered with stellate trichomes; disk united at base with 5 rectangular segments, receptacle glabrous. Capsules 5–5.2 × 3.9–4 mm, globose, ferruginous, the trichomes stellate, sepals accrescent, pedicels 3– 2.3 mm long; seeds 3–3.2 × 1.6–1.65 mm, oblongoid, grayish, with discretely dark spots; caruncle hat-shaped, sessile, yellow-whitish, visible on ventral side.

Distribution and habitat:—The species occurs in the municipalities of Andaraí and Mucugê, state of Bahia ( Fig. 2 ), where it grows in rock fields at elevations between 800 and 960 meters.

Etymology:—The specific epithet “ piriquetifolius ” alludes to the resemblance of the leaves of the new species to those of the genus Piriqueta Aublet (1775: 298) , Passifloraceae .

Phenology:—Collected with flowers and fruits from November to July.

Preliminary conservation status:—Species with Extension Occurrence of 1,196.562 km 2 and therefore, classified as Endagered, EN (B1ab). However, we chose to consider it as a Data Deficient Category (DD), since it is known from three collections from the same location. On the other hand, the region where it grows comprises heavily rugged terrain, inappropriate for cultivation and civil construction, and includes areas protected by law, which ensures its conservation.

Additional specimens examined (paratypes): — BRAZIL. Bahia: Andaraí, District of Igatu, estrada histórica Igatu-Mucugê , a 500 m de Igatu, 12º50’31”S, 41º30’82”W, 800 m, campo rupestre, 13 March 2007 (fl., fr.), M.J. Silva, A. Fortuna-Perez & Fidanza K. 978 ( UFG) ; ibid., estrada Chão sentido Mucugê , 12º54’00”S, 41º18’33”W, 861 m, 25 November 2016 (fl.), D.S. Carneiro-Torres, E.K. Brandão & R.B.M. Castro 1496 ( HUEFS) .

Systematic position and morphological relationships: — Croton piriquetifolius beside the other characters typical of the section Geiseleria (see Introduction), has subshrub or shrub habit, inflorescences congested with pistillate and staminate flowers continuous, the pistillate ones with 5 unequal sepals and bifid styles. For this reason, it can be placed in Croton sect. Geiseleria subsect. Geiseleria ( Riina et al. 2021) .

Croton piriquetifolius is morphologically closest to C. glandulosus because both share the usually ovate leaves with obtuse base and a pair of acropetiolar or basilaminar nectary glands, the inflorescence congested without a sterile gap between staminate and pistillate flowers, the bracts of flowers of both sexes with pyriform colleters ( Machado et al. 2015), the pistillate ones with 2-fid styles. However, C. piriquetifolius has leaves with acropetiolar patelliform sessile nectaries, 0.7–0.8 mm diam., on the adaxial surface (vs. basilaminar, cupuliform or stipitate-patelliform, with 0.3–0.5 mm diam., on the abaxial surface), staminate flowers solitary with 11 stamens, the filaments hairy (vs. 9–11, in cymules, glabrous), pistillate flowers with pedicel 1.8–2.4 mm long and sepals 3–4.5 × 1.3–2.7 mm, hairy on both surfaces (vs. pedicel 0.2–0.5 mm and sepals 1−2.5 × 0.3−1.1 mm, hairy only on ventral surfaces), capsules uniformly brownish (vs. green with whitish on the sutures of the septa and locules), and seeds 3–3.2 × 1.6–1.65 mm, oblong (vs. 3.8–4.2 × 2.2–2.4 mm, oblong-ellipsoid).

Croton piriquetifolius has also been confused in herbaria with C. adamantinus (D.S. Carneiro-Torres, E.K. Brandão & R.B.M. Castro 1496; HUEFS), and C. eremophilus (H.P. Bautista, N. Hind & S. Smith 3611; ALCB, CEPEC, HUEFS, SPF); the former species also belongs to C. sect. Geiseleria , and the latter to C. sect. Barhamia ( Klotzsch, 1853: 104) Baillon (1858: 367) . Croton piriquetifolius differs from C. adamaninus by its subshrubby or shrubby habit up to 1 m tall and lack of aromatic scent (vs. always shrubby with 1.2–4 m tall and aromatic scent), leaves with acropetiolar glands, base obtuse and margin serrulate without glands (vs. leaves with basilaminar glands, base cordate and margin dentate with stipitate-glands between the tooth), pistillate flowers with sepals unequal (vs. equal), stipules and flowers of both sexes with glands (vs. without glands), staminate flowers with sepals with hyaline glands and 11 pubescent stamens (vs. sepals with golden glands and 10 stamens, glabrous), and seeds 3–3.2 mm long, oblong (vs. 5–6 mm long, globose). When compared to C. eremophilus both species share a shrubby habit, brownish stems, and numbers of stamens. However, both species can be differentiated by several characters ( Table 1 ).

Anatomical data

Leaf blade: The studied species present simple, stellate and multiradiate trichomes. The adaxial surfaces of the leaves have simple ( Figs. 3A, B, N, R ) or stellate trichomes with a porrect ray ( Fig. 3C ), while on the abaxial surface stellate multiradiate subsessile trichomes were seen in C. glandulosus ( Fig. 3M ), and stipitate ones ( Figs. 3H, L, S, T ) in the others. Croton adamantinus , C. eremophilus and C. piriquetifolius have hypostomatic leaves ( Figs. 3D, I, U ), while C. glandulosus has amphistomatic leaves ( Fig. 3O ). The epidermis is unistratified, has a thin cuticle and rectangular and quadrangular common cells with walls straight or sinuous ( Figs. 3D, I, O, U ). The cells walls are thickened in C. adamantinus ( Fig. 3D ), while the periclinal internal wall is thickened in C. eremophilus (3I) and the external in other species. Secretory, unicellular, and subglobose trichomes were found on leaf surfaces of C. glandulosus and C. piriquetifolius ( Figs. 3O, T ).

The mesophyll is isobilateral with one layer of palisade parenchyma and three to five of spongy parenchyma in C. eremophilus ( Fig. 3I ), or dorsiventral, with one layer of palisade parenchyma and four to six layers spongy parenchyma in C. adamantinus , C. glandulosus and C. piriquetifolius ( Figs. 3D, O, U ). Idioblasts ( Figs. 3D, F, I, K, O, U, W ) and druses ( Figs. 3D, O ) were seen in the mesophyll of all species.

The leaves are homobaric ( Figs. 3D, E, I, J, O, P, U, V ) with vascular bundles collateral ( Figs. 3E, J, P, V ) located in the median portion of the mesophyll. Druses were found usually in the parenchymatic sheath in C. eremophyllus ( Fig. 3J ). The margin in all species has rounded and obtuse contour with parenchymatous cells in subepidermal position ( Figs. 3F, K, Q, W ).

Midrib: The midribs are biconvex in all species ( Figs. 4A, F, K, P ), conspicuous on adaxial surfaces of C. glandulosus ( Fig. 4K ) and C. piriquetifolius ( Fig 4P ), and inconspicuous on adaxial surfaces of C. eremophilus ( Fig. 4F ) and C. adamantinus ( Fig. 4A ). The common cells of epidermis and non-glandular trichomes are similar to those found on leaf blades; however, emergencies also occur in C. piriquetifolius ( Fig. 4P ). Glandular, subglobose and unicellular trichomes are found on the abaxial surface of all species ( Figs. 4D, N, S ) except in C. eremophilus ( Fig. 4I ). The cortex encompasses annular and angular collenchyma, and ground parenchyma with cells of different shapes and sizes, some of them with druses, especially near to the phloem, where laticifers were also seen ( Figs. 4B, C, G, H, L, M, Q, R ). Croton piriquetifolius has five layers of angular collenchyma on upper surface ( Fig. 4Q ) (vs. nine in C. adamantinus , Fig. 4B , two in C. eremophilus , Fig. 4G , and four in C. glandulosus , Fig. 4L ). On lower surfaces, three layers of angular collenchyma are present in C. adamantinus and C. eremophilu s ( Figs. 4C, H ), and two or three of annular collenchyma in C. glandulosus and C. piriquetifolius ( Figs. 4M, R ). All species have a cortex with 4 or 5 layers of ground parenchyma. Palisade parenchyma is noted on both surfaces of the leaf blade in C. eremophilus ( Figs. 4F and G ), C. glandulosus ( Figs. 4K and L ), and C. piriquetifolius ( Figs. 4P and Q ), except in C. adamantinus ( Figs. 4A, B ). The main vascular bundles in the species are collateral ( Figs. 4E, J, O, T ), however, in a circular closed arch in C. adamantinus ( Figs. 4A, E ) and a semilunar open arch in the others ( Figs. 4F, J, K, O, P, T ). Two accessory vascular bundles were found only in C. adamantinus ( Fig. 4A ). Druses were observed in the cortex (e.g., Figs. 4C, M ) and pith (e.g., Figs. 4J, O ). Laticifers near phloem occurs in all species ( Figs. 4B, C, E, G, H, J, M, O, R, T ). The pith in all species is parenchymatic.

Petiole: In all species they are concavo-convex ( Figs. 5A, F, K, P ) with ovoid contour in C. adamantinus ( Fig. 5A ) and orbicular in the others ( Figs. 4F, K, P ). The epidermis has rounded, elliptical, and quadrangular common cells with thin cuticle in C. glandulosus ( Figs. 5L–N ), and C. piriquetifolius ( Figs. 5Q–S ), and thickened in C. adamantinus ( Figs. 5B–D ), and C. eremophilus ( Figs. 5G, I ). Subglobose glandular trichomes were observed in all species ( Figs. 5G, L, N, Q ), except in C. adamantinus . The epidermis in all species has glandular and non-glandular trichomes, being emergencies also present in C. piriquetifolius (e.g., Fig. 5Q ).

The cortex comprises angular collenchyma in C. eremophilus ( Figs. 5G, I ) and C. glandulosus ( Figs. 5L, N ), and annular in C. adamantinus ( Figs. 5B, D ) and C. piriquetifolius ( Figs. 5R, S ), followed by 10 to 13 and 5 to 7 layers of ground parenchyma on upper and lower surfaces of C. andmantinus (vs. 4 or 5 and 3 to 5, in C. eremophilus and C. glandulosus , and 3 or 4, and 6 to 8 in C. piriquetifolius ). Rounded or globose parenchymatic cells are found in cortex of all species ( Figs. 5B, D, G, I, L, N, Q, S ).

The vascular bundles are collateral ( Figs. 5E, J, O and T ) in closed arc C. adamantinus and C. piriquetifolius ( Figs. 5E, T ) an open arc in C. eremophilus ( Fig. 5J ) and C. glandulosus ( Figs. 5J, O ) with three or four isolated vascular bundles ( C. glandulosus Fig. 5O ). The pericycle is parenchymatous in C. eremophilus and C. glandulosus ( Figs. 5H, J, M, O ) and sclerenchymatous in C. adamantinus and C. piriquetifolius ( Figs. 5C, E, R, T ). Two accessory vascular bundles are found on upper surfaces of C. adamantinus , C. glandulosus and C. piriquetifolius ( Figs. 5A, C, M, P, R ). The pith has six to eight layers of cells in C. adamantinus and C. glandulosus ( Figs. 5A, E, K, O ), and four or five in C. eremophilus and C. piriquetifolius ( Figs. 5F, J, P, T ). Laticifers are found in cortex of all species ( Figs. 5D, E, H, J, L, M, O, S, T ), while druses are found in the pith of C. eremophilus and C. glandulosus ( Figs. 5H, J, O ), and in the cortex of some of them (e.g., Figs. 5I , L-N, S), except in C. adamantinus ( Figs. 5 B-D).

The anatomical characteristics of the species studied repeat those found in other species of Croton and or other genera of Euphorbiaceae ( Solereder 1908, Metcalfe & Chalk 1983, Freitas et al. 2001, Sá-Haiad et al. 2009, Soares 2013, Riina et al. 2015, Vitarelli et al. 2016, Sodré et al. 2019a, 2022, Sodré & Silva 2020, 2022, Pinto-Silva et al. 2023), with some of them (e.g., presence of tiny substomatal chambers, emergencies, fibers associated with the phloem, hypostomatic leaves, densely hairy leaves, presence of phenolic compounds) related to xeromorphic environments ( Fahn & Cutler 1992, Sandquist & Ehleringer 1997, Bieras & Sajo 2009, Vitarelli et al. 2016).

Stomata located on the abaxial surface act to reduce excessive water loss ( Pyykkö 1966, Dickison 2000, Evert 2006), thickened cuticle acting to reduce the loss of water by evapotranspiration, minimizing the heating of the leaf surface ( Cen & Bornman 1993, Larcher 2006), as well as makes it difficult for pathogens and herbivores ( Juniper & Jeffree 1983, Mauseth 1988, Heredia et al. 1998, Castro et al. 2009). On the other hand, stomata present on both leaf surfaces, as in C. glandulosus , a species that grows in open areas, exposure to the light on very humid soils, acts by enabling an increase in photosynthetic rate, high leaf conductance CO 2, promoting a rapid growth ( Parkhurst 1978, Mott et al. 1982).

The glandular and non-glandular trichomes, and/or emergencies found in the species studied act in protection against herbivores (e.g., Gutschick 1999, Werker 2000, Tozin et al. 2016, Karabourniotis et al. 2020), in reduction of the fraction of radiation absorbed by leaves ( Fahn 1986, Karabourniotis & Fasseas 1996), in protection of stomata and reduction of water loss by evapotranspiration ( Fahn 1986), and chemical defense, in the case of glandular trichomes (e.g., Levin 1973, Weryszko-Chmielewska & Chwil 2014, Tozin et al. 2016, Dmitruk et al. 2019, Karabourniotis et al. 2020), as reported to C. gratissimus Burchell (1824: 263) by Naidoo et al. (2023).

Palisade parenchyma reaching more than half the length of the mesophyll facilitates the distribution of solar rays, helps the maintenance of the latter, and dynamizes the flow of substances (DeLucia et al. 1996, Carvalho et al. 2019). Druses, commonly found in the leaves of Croton species ( Barros & Soares 2013, Gancedo et al. 2022), act in defense against herbivory and are an important source of calcium (Ca) for cellular metabolism. Laticifers are common in Euphorbiaceae ( Rudall 1987, 1994) and responsible for the storage of latex, a complex secretion, whose composition involves the presence of compounds derived from primary and secondary metabolism ( Haberlandt 1914, Fahn 1979). This structure has several functions, such as, tissue healing, defense, or deterrent against predation by herbivores ( Fahn, 1979, Rudall 1987, 1994). Gelatinous and libriform fibers, and collenchyma provide mechanical support of internal tissues, aid in water retention, especially, gelatinous fibers, and prevent cell collapse under conditions of water stress ( Holtzmeier et al. 1998, Dickison 2000, Bieras & Sajo 2009).

Finally, the leaf anatomy of the species studied serves to differentiate them, as also reported for other Croton species ( Soares 2013, Barbosa et al. 2018, Feio et al. 2018, Sodré et al. 2019, Sodré & Silva 2020, 2022, Rosa et al. 2021), and reflect the biotic and biotic conditions where the species inhabit.

Figures

FIGURE 1. Croton piriquetifolius. a. Fertile branch; b. Stipule; c. Leaf; d. Basal portion of the leaf showing the acropetiolar nectary glands; e. Margin of the leaf, note the nectary glands; f. Inflorescence; g. Staminate flower; h. Stamen; i. Staminate bracts; j. Staminate petal, ventral view; k. Staminate petal, dorsal view; l. Pistillate bract; m. Pistillate flower; n. Pistillate flowers with ovary removed, note the glands in the position of petals; o. Gynoecium; p. Capsule; q. Seed in frontal view; r. Seed in dorsal view. Details from the holotype.

FIGURE 2. Distribution of Croton piriquetifolius. Map of South America highlighting Brazil with the species occurrences (stars) and vegetation. Abbreviations for states: AL = Alagoas; BA = Bahia; GO = Goiás; MG = Minas Gerais; PE = Pernambuco; PI = Piauí; SE = Sergipe; TO = Tocantins.

FIGURE 3. Cross sections of the leaf blade (a–e, g–j, l–p, r–v), and margin (f, k, q, w) of Croton adamantinus (a–f), C. eremophilus (g–k), C. glandulosus (l–q) and C. piriquetifolius M.J. Silva & Sodré (r–w). a–c, g, h, l–n and r–t. Detail of the trichomes; d, i, o and u. General aspect of the leaf blade highlighting the epidermis, palisade and spongy parenchyma, stomata, trichomes, druses, vascular bundles and idioblasts; e, j, p and v. Detail of the vascular bundles; f, k, q and w. Margin. ep = epidermis; gt = glandular trichome; id = idioblasts; ph = phloem; pp = palisade parenchyma; sp = spongy parenchyma; tr = non-glandular trichome; vb = vascular bundles; xy = xylem; yellow arrowhead = druse; arrows = stomata; 1 = simple trichomes; 2 = stellate trichomes with a porrect ray; 3 = multiradiate subsessile or stipitate trichomes. Scales: a–c, e–h, j–n, p–t, v, w = 50 µm; d, i, o, u = 200 µm.

FIGURE 4. Cross sections of the midrib of Croton adamantinus (a–e), C. eremophilus (f–j), C.glandulosus L. (k–o), and C.piriquetifolius (p–t). a, f, k and p. General aspect; b, g, l and q. Detail of the adaxial surface; c, h, m and r. Detail of the abaxial surface; d, i, n and s. Detail of the trichomes and epidermis; e, j, o and t. Vascular bundles. co = collenchyma; ep = epidermis; gt = glandular trichome; pa = parenchyma; ph = phloem; pi = pith; pp = palisade parenchyma; tr = non-glandular trichome; vb = vascular bundles; xy = xylem; yellow arrowhead = druse; * = laticifers. Scales: a, b, e, f, i, k, p = 200 µm; c, d, g, h, j, l–o, q–t = 50 µm.

FIGURE 5. Cross sections of the petiole of Croton adamantinus (a–e), C. eremophilus (f–j), C. glandulosus (k–o), and C. piriquetifolius (p–t). a, f, k and p. General aspect; b, g, l and q. Detail of the epidermis, collenchyma, trichomes and parenchyma of the adaxial surface; c, m and r. Detail of the accessory vascular bundles; d, i, n and s. Detail of the epidermis, collenchyma, fibers, phloem, xylem, idioblasts, laticifers, trichomes and parenchyma of the abaxial surface; e, h, j, o and t. Detail of the vascular bundles. co = collenchyma; em = emergences; ep = epidermis; fi = fibers; gt = glandular trichome; id = idioblasts; pa = parenchyma; ph = phloem; pi = pith; tr = nonglandular trichome; vb = vascular bundles; xy = xylem; arrows = stomata; yellow arrowhead = druse; * = laticifers. Scales: a, k = 500 µm; b, c, e, f, j, o, p, t = 200 µm; d, g–i, l–n, q–s = 50 µm.