Arapatiella psilophylla (Harms) R. S. Cowan. Proc. Biol. Soc.

Rodrigues, Ana Tereza Novaes Parga, Falcão, Marcus José De Azevedo & Mansano, Vidal De Freitas, 2023, A Taxonomic Revision of Arapatiella (Fabaceae: Caesalpinioideae): An Endemic and Threatened Genus from the Brazilian Coast, Phytotaxa 606 (4), pp. 273-286 : 276-282

Arapatiella psilophylla (Harms) R. S. Cowan. Proc. Biol. Soc. Washington 86(39): 447 (1973). ( Figures 1 – 3 )

≡ Tachigalia psilophylla Harms, Notizbl. Königl. Bot. Gart. Berlin 59: 305–306. (1915). ≡ Dicymbe psilophylla (Harms) Dwyer, Ann. Missouri Bot. Gard. 41: 223–224 (1954). Type:— BRAZIL, Bahia, in silvis pr. Esperanza. VI–1822. Riedel 804 barcode K000057195 (Lectotype, designated here: K; isolectotypes: E; F; K; MNHN; US; W).

= Arapatiella trepocarpa Rizzini & A. Mattos, Revista Brasil. Biol. 32(3):323–333. IX-1972. Type :— BRAZIL, Bahia, Camacan-Mascote. V-1970. T. S. dos Santos 834 RB barcode RB00585685 (Lectotype, designated here: RB!; isolectotypes: HUEFS; K; RB!).

Trees small to medium-sized, heartwood reddish brown, lenticels small and sparse; bark rough, gray to brownish to reddish; branches cylindrical, gray, usually glabrous, sometimes sparsely puberulent in terminal regions, indumentum gray to brown. Leaves paripinnate, alternate, coriaceous, (2 –) 3 – 4 (– 5) pairs, opposite leaflets, elliptic to oval to oblong, less frequently ovate or rotund, rarely obovate, apex almost always acuminate to cuspidate, less frequently acute to truncate to emarginate, rarely retuse, sometimes with a small mucron, base cuneate, margin entire, glabrous to sparsely puberulent at the base of the abaxial side and central vein, rarely puberulent at the base of the adaxial side, distal half always glabrous, coriaceous to subcoriaceous, green, often matte, sometimes glossy; rachis, petioles and petiolules cylindrical to slightly conical, glabrous to sparsely puberulent, indumentum golden to brown, leaflets progressively larger from proximal to distal, rarely the opposite; stipules persistent, one pair per bud, reniform to semicircular to orbicular, glabrous to sparsely puberulent at the base of both sides; axillary and terminal buds ovate to semicircular, rounded apex, pubescent, golden to brown indumentum. Inflorescences in racemes organized in fascicles that may or may not be compound, axillary, densely flowered at the apex of the rachis, less frequently sparsely flowered, alternate spiral flowers, rachis quadrangular to cylindrical, densely strigulate, indumentum green to golden to brown, less frequently reddish brown; bracts similar to the stipules, persistent, in pairs at the base of fascicles, reniform to semicircular to orbicular, glabrous to puberulent at the base on both sides; bracteoles deciduous, one per pedicel, ovate, apex acute, base truncate, pubescent, indumentum brown; pedicel cylindrical with quadrangular base, strigulate, light green to golden to brown indumentum. Flower buds pyriform, erect, apex rounded, with four of the five sepals commonly not touching each other at their apices; flowers dichlamydeous, heterochlamydeous, actinomorphic, with campanulate hypanthium, glabrous; sepals 5, partially gamosepalous, free from the hypanthium upwards, unequal, sepals from the outermost to the innermost progressively larger in length and width, less coriaceous at their margins, imbricate, light green to brown, densely strigulate externally and on the basal ⅓ internally, indumentum golden to brown to reddish brown, base truncate, apex acute to rounded to truncate, margin entire, erect, coriaceous with membranous margin; petals 5, free, erect, equal, unguiculate, blade glabrous, strigulate nail on the outer side, golden indumentum, margin wavy to lobed, obtuse to truncate, blades rather imbricated in the pre anthesis, white; stamens 10, outer antesepalous and inner antepetalous whorls, equal, free; filaments erect, glabrous, strigulate at the base, golden indumentum, filiform, white; anthers dorsifixed, introrse, erect, glabrous, cream, rounded to oblong, apex truncate to acute to acuminate, with two thecae, 4 sporangia, rimose; gynoecium monocarpellate, ovary laterally compressed, polygonal, stipitate, brown, densely strigose, indumentum golden to coppery to brown, erect, partially included in the hypanthium, apical style, emerging slightly displaced to one side of the ovary, glabrous, strigose at base, white, stipe glabrous at base and strigose at top, stigma peltate, glabrous, 6 – 10 ovules. Fruits legumes, dehiscent, lignified, green when young, brown to dark brown when mature, laterally compressed, oblanceolate to lanceolate, with reduced stipe, base slightly asymmetric, cuneate, apex slightly asymmetric, acute to rounded to obtuse, densely strigulate, golden to dark brown indumentum, epicarp, mesocarp and endocarp lignified, thicker at its margins, mainly when young, the fruit curls at dehiscence forming a spiral; seeds chamber usually occupying the last ⅔ of the fruit, inconspicuous venation. Seeds 4 – 6, 3–4.5 × 1.5–2.5 cm, not arillate, ellipsoid, brown to black, slightly flattened laterally, asymmetrical, testa glabrous, slightly to strongly rugose, endosperm solid, brown; hypocotyl-radicular axis diagonally, displaced somewhat from the base.

Diagnosis: — Arapatiella can be differentiated from other Leguminosae genera by its large and numerous persistent semicircular to reniform stipules in the axils of the branches, leaves, and inflorescences, its paripinnate leaves with usually 3 – 4 opposite pairs of leaflets, inflorescences in fascicles of racemes, flowers with slightly heteromorphic calyx, white petals, and its large lanceolate spiral-shaped fruits when ripe.

Distribution and habitat: — Arapatiella psilophylla is endemic to Brazil and to the Atlantic Forest biome, with distribution along the coast of Bahia state, especially from the center to the south of the state. It predominates in dense ombrophilous and tableland forests, often occurring in Restinga regions, although at lower relative density ( Fernandes & Queiroz, 2015). A. psilophylla occurs in areas of primary forest, but it is also common in cocoa plantations and regenerating areas. Sambuichi et al. (2009) indicated occurrence north of Espírito Santo state; however, no occurrence records were observed for this region ( Figure 4 ).

Ecology: — Lorenzi (2016) describes A. psilophylla as a perennial plant, usually under shade environments, but can also be a heliophyte. It occurs predominantly in more interior portions of the forest. Still, it can also occur at edge areas, especially in regions disturbed by anthropic action. It also occurs on gentle slopes ( Rocha & Amorim, 2012), hilltops and riverbanks. Commonly reported in clay and sandy-clay soil substrates, but also humic and sandy-siliceous soil. There are no studies regarding the pollination patterns of Arapatiella , and the only mention of it is made in the collection S. A. Mori 14130, reporting the plant as visited by hummingbirds. However, its floral morphology indicates a possible bee pollination syndrome. The flowers are commonly described as very odoriferous (Hatschbach 53496; M. T. Monteiro 23085).

Etymology: —The genus name was given by Rizzini & Mattos (1972) in the function of the vernacular name “arapati”. Other names are also given, such as “faveca-vermelha” and, less commonly, “brinco de cabocla” and “quiri” ( Bondar , G. 2351). The same popular names are given to both varieties. The term psilophylla does not have its attribution justified by Harms (1915). However, the word’s etymology and description suggest that it refers to bare (=psilo) leaves (=phylla), due to the leaves’ glabrous adaxial surface.

Uses: — Arapatiella psilophylla is a species of great local economic importance ( Sambuichi et al. 2009) due to its rigid hardwood being widely used in civil and hydraulic construction ( Lorenzi, 2016) by local people in its region of occurrence. The wood is used to make beams, stakes, and other structures ( Rizzini & Mattos, 1972). In addition, studies demonstrate its potential for reincorporating nutrients into the soil ( Montagnini et al. 1995; Gama-Rodrigues et al. 2007), and its cultivation is profitable in rehabilitating worn-out soils and mixed planting cultures.

Conservation: —An EOO of about 72.782 km ² was estimated for A. psilophylla , and also for the type variety A. psilophylla var. psilophylla , since the distribution of A. psilophylla var. emarginata is completely contained within the distribution of the type variety. The EOO alone is insufficient to indicate a degree of threat according to IUCN criteria; however, most of the 125 records of the species are considerably old, with only 22 in the last ten years. The species is rarely mentioned as common (Mattos, A. 507; Rocha & Amorim 2012), with records commonly in anthropized areas, although they can also be found in primary forests. There are numerous mentions of the high quality of its wood, which is widely used (Duarte, A. P. 8018; Mattos, A. 507; Rizzini & Mattos, 1972; Lorenzi, 2016). It is also worth noting that the species is endemic to the Atlantic Forest, one of the most threatened and fragmented biomes in Brazil, occurring uniquely in a region that has been suffering intense deforestation for agricultural and urban expansion for centuries, but with renewed intensity in the last 30 years ( Ranta et al. 1998; Landau 2003; INPE 2020).

Given this, and seeing that only a few records of the species are found in protected areas such as Rebio UNA (Amorim, A. M. 2641; Hage, J. L. 804), Monte Pascoal National Park (Hatschbach, G. G. 53496), and Pau Brasil National Park (Matos, F. B. 172), considering IUCN (2019) criteria A, C, and D, we indicated vulnerable status for both A. psilophylla and its type variety: A. psilophylla var. psilophylla , corroborating the result obtained by WCMC (1998).

Concerning A. psilophylla var. emarginata , we obtained a significantly reduced EOO of 211 km 2, with only nine known specimens, only two of them collected after 2000. Having this and associating the inferences mentioned for the species, according to the A–D criteria of IUCN (2019), we indicate the preliminary category of threatened for the variety, highlighting the importance of further studies about its conservation.

Taxonomic comments: —In the present work, two groups of morphologically distinct specimens were identified, here recognized as two varieties. Different gradations were observed regarding the characteristics that separate them, evidencing some level of intersection between these two groups and, therefore, their incomplete separation. Our analysis did not corroborate some of the delimiting characters that Cowan (1981) pointed out, while others proved accurate and are reiterated here. In addition, other distinguishing characters not pointed out by Cowan (1981) are added and may be helpful in a more precise delineation of the groups.

Cowan (1981) pointed out characteristics that were not considered useful here, such as 1) the length of the petioles and rachis, which is quite variable in many specimens of the psilophylla variety, sometimes longer than in the emarginata variety. It should be noted that the petiole and rachis are often longer in emarginata variety; however, due to the significant overlap in the length range of these structures in the two groups, this characteristic is not good in differentiating them; 2) the variety emarginata would have more pairs of leaflets; however, the variety psilophylla often presents four pairs of leaflets, with variation in the number of pairs even in the same specimen.

The characteristics pointed out by Cowan (1981) that are supported here as distinctive for the two groups are: 1) the emarginate to truncate apex of the leaflets of the emarginata variety compared to the acuminate or cuspidate apex of the psilophylla variety. Although we observed that, sometimes, the apex could vary among the leaflets of the same specimen (J. G. Jardim 294), this character is stronger in separating both taxa, and it was used here to identify the specimens which present intermediate states in other characters; 2) the color of the indumentum covering the inflorescences and sepals, whose shade of brown is much darker, sometimes being reddish in emarginata . However, there is a subtle transition of colors between the two taxa; 3) the oblong shape of the leaflet in emarginata . Although Cowan states that such character defines the taxon, such a type of leaflet is commonly found in psilophylla . However, the elliptical form commonly found in most of the specimens of psilophylla is never found in emarginata ; 4) finally, the size of the flowers, even in the bud, is longer and wider in emarginata . However, a specimen identified here as belonging to emarginata presents flowers like those of psilophylla . Among the specimens of psilophylla , there is a variation in the size of the flowers, but it never reaches the size observed in the specimens of emarginata .

The differences not highlighted by Cowan (1981) and observed here are: 1) the greater length and width of the stipules in emarginata that can reach 10 cm in length, while in psilophylla they do not exceed 6 cm, except one intermediate specimen (Gomes, F. S. 1599). However, emarginata also present smaller stipules like those of psilophylla ; 2) the length of the inflorescence is higher in emarginata , reaching 30 cm, while most of the fertile specimens of psilophylla do not have inflorescences longer than 15 cm. Only a few individuals of psilophylla have inflorescences similar in size to those observed in emarginata (Mattos-Silva, L. A. 3109); 3) the rachis and petioles of emarginata are commonly thicker, besides always being glabrous, unlike psilophylla that can present these structures glabrous or puberulent. 4) var. emarginata commonly has glossier leaflets with a subcoriaceous consistency, which contrasts with the often matted and leathery leaflets of psilophylla . However, there are also intermediate cases, with some emarginata more like the psilophylla pattern. Therefore, seven of the eight characters separating the two taxa show higher or lower levels of intersection between them. They cannot support the two groups as distinct species, with only the leaflet apex being a strong delimitation between them.

We considered factors other than the phenetic approach to determine the most appropriate ranking for the allocation of the identified taxa since many delimiting morphological characters overlapped in the specimens. Thus, we considered the hypothesis of an incomplete separation between the two groupings, with the possibility of gene flow still occurring between them. To evidence that, five specimens analyzed were considered to have intermediate characteristics between the two groupings, making it difficult to define them as one of the two varieties, three were here included as var. psilophylla: Gomes, F. S. 1599 , Loureiro, D. M. 578, W. W. Thomas 8081, and two as var. emarginata: W. W. Thomas 8167, and W. W. Thomas 10913 ( Figure 3 ).

We observed that territorial and environmental occurrences overlap, including in different habitats and substrates. The phenology of both also overlaps, despite the reduced availability of flowering specimens of emarginata .

Given these factors, we chose to recombine infra-specific taxa within Arapatiella psilophylla , defining the two clusters delimited in the present work as two varieties: Arapatiella psilophylla var. psilophylla and Arapatiella psilophylla var. emarginata . The most striking characters to differentiate them are the size of the flowers, stipules, and inflorescences, the color of the indumentum of the inflorescences, and the shape of the apex of the leaflets.

Polhill & Vidal (1981), as well as Rizzini & Mattos (1972) and Cowan (1973) mentioned that the species might have paripinnate or imparipinnate leaves, but we observed here only paripinnate leaves. Cowan (1981) indicates that the inflorescences of the genus were racemes or panicles of racemes. Here we identified that Arapatiella inflorescences are racemes organized in fascicules that can be composed.

Identification key to the varieties of Arapatiella psilophylla :

1 Leaflets commonly elliptic, sometimes oval to oblong, with apex acuminate to cuspidate, rarely acute; stipules 0.7 – 6 × 0.7 – 6.5 cm; inflorescences 4 – 14 (– 20) cm long, indumentum golden to brown; flower buds up to 1.4 cm long, pedicels 2 – 10 (– 14) mm long, petals 9 – 14 (– 16) mm long, ovary 4 – 6 mm long ................................................................. Arapatiella psilophylla var. psilophylla

- Leaflets never elliptic, being oblong to rotund, apex emarginate to retuse, sometimes truncate; stipules 1.1 – 10 × 1 – 10 cm; inflorescences 20 – 30 cm long, indumentum dark brown to reddish brown; flower buds up to 1.7 cm long, pedicels 8 – 22 mm long, petals 13 – 18 mm long, ovary 9 – 11 mm long ...................................................................... Arapatiella psilophylla var. emarginata

Figures

FIGURE 1. A–B. A. psilophylla var. emarginata; C–P. A. psilophylla var. psilophylla. A. Leaf and stipule; B. Detail of leaflet apex; C. Leaf and stipule with young leaf emerging; D. Detail of leaflet apex; E. Detail of the stipule; F. Inflorescence; G. Flower bud; H. Flower; I. Detail of hypanthium with gynoecium; J Detail of the calyx; K. Petal; L. Anther; M Detail of the carpel; N. Detail of the stigma; O. Fruit; P. Seed.A–B. Pinheiro 1548; C–D. Santos 729; E. Amorim 1402; F–G; I–N. Aona 2304; H. Mansano 2022-6; O–P. Amorim 2641. Drawn by Marcus Falcão.

FIGURE 2. Arapatiella psilophylla var. psilophylla. A. Habit. B. Detail of the trunk. C. Detail of the pair of stipules. D. Flowers and young fruits. E. Flowers and buds. F. Leaf. G. Inflorescence with young fruits and bracts. H. Fruits. I. Leaf and inflorescence. J. Open fruit with seeds. Image authors: A–D, F–H, J: A. T. Novaes and M. J. Falcão; E, I: SpeciesLink. A–C, E–F. Lima, H. C. 8228; D, G–H. Mansano 2022-6; I. Aona, L. Y. S. 2034; J. Matos, F. B. 1732. Scale bar: A:1 m; B: 20 cm; C–E, G, J: 1 cm; F, I: 5 cm; H: 10 cm.

FIGURE 3. A–H, J–L. Arapatiella psilophylla var. emarginata. I. Arapatiella psilophylla var. psilophylla.A. Holotype; B. Detail of inflorescence indumentum; C. Flower bud; D. Flower; E. Anther; F–H. Variation in leaflet apex from emarginate to truncate to obtuse; I. acuminate apex in var. psilophylla; J. Stipule; K. Leaves and fruits; L. opened and spiral fruits. Image authors:A. Reflora; B–I, K. A.T. Novaes; J, L. SpeciesLink. A. R. S. Pinheiro 1548; B–E, H. J.G. Jardim, 294; F, J–L. A. M. Amorim, 1402; G. W. W. Thomas 8167; I. F. S. Gomes 1599. A, K. 10 cm; B–D. 5 mm; E. 2 mm; F, H–I. 1 cm; G, J, L. 5 cm.

FIGURE 4. Distribution map of Arapatiella psilophylla varieties. Source: Arc Gis with modifications.