Spondias tuberosa Arruda in Koster, Trav. Brazil: 496. 1816.

Mitchell, John D. & Daly, Douglas C., 2015, A revision of Spondias L. (Anacardiaceae) in the Neotropics, PhytoKeys 55, pp. 1-92 : 46-51

Spondias tuberosa Arruda in Koster, Trav. Brazil: 496. 1816. Figs 2, 13, 15, 16

Type.

BRAZIL. Bahia: Mun. Rio das Contas, km 7 Rio de ContasLivramento do Brumado road, 13°38'S, 41°50'W, 12 Dec 1988, R. M. Harley, B. Stannard, J. R. Pirani, A. Furlan & J. Prado 27127 (neotype: SPF!, here designated; iso-neotypes: CEPEC!, K!, NY!).

Description.

Hermaphroditic (sometimes andromonoecious) trees or shrubs, often deciduous for extended periods, reproductive size 2-10 m tall × 11.5-41 cm diam, with dense, low, tortuous branching, often the crown broader than tree height, often the outer branches forming a weeping habit, these sometimes rooting in the ground; short shoots often present and sometimes becoming spinose. Roots tuberous. Outer bark gray, frequently with wavy fissures, surface irregular but relatively smooth, apparently shed in rectangular plates. Trichomes of two types: (1) flexuous to curved white hairs to 0.6 mm long; and (2) erect to ascending hairs to 0.25 mm long. Leaves 1-4 (5)-jugate, 6-17 cm long; petiole 1.7-5 cm long, petiole and rachis glabrous or sometimes with sparse to scattered (rarely dense) flexuous hairs; lateral petiolules 0-4 mm long, sometimes reddish, the terminal one 0.3-1.4 cm long, petiolules with sparse to dense flexuous hairs; basal leaflets 2.5-5.1 × 1.5-3.2 cm, (broadly) elliptic to ovate, the other laterals 2-6.5 × 1.2-3.5 cm, (broadly) ovate or sometimes broadly elliptic, terminal leaflet 3-5.5 × 1.6-2.7 cm, obovate to (broadly) elliptic, leaflets often plicate; leaflet apex sharply but usually gradually acuminate (then the acumen 2-7 mm) or less often acute to obtuse or rounded, rarely emarginate, mucronate; lateral lamina usually medially and basally (sub)symmetrical, the base obtuse to subcordate, basal insertion usually (sub)symmetrical and excurrent, leaflets chartaceous to membranaceous, both surfaces dull; leaflet margin sometimes slightly revolute and thickened (sometimes red on juvenile leaflets), usually entire, occasionally 1-2 crenulations on a leaflet, densely ciliate with flexuous hairs to 0.4 mm long, especially on young leaflets. Inflorescences terminal, initiated with or before a new flush of leaves or sometimes on branchlets with mature leaves, 5.5-20 cm long, 1-1.4 mm diam near base, broadly branched, secondary axes to 4.8 cm long, the axes glabrous or more often provided with sparse erect to ascending hairs or with flexuous hairs, the latter to 1 mm long near base; bracts on axes 1-8.5 mm long, bracteoles to 0.6 (1.5) mm long, all bracts linear to lanceolate and ciliate, sometimes with ascending hairs abaxially; pedicel 2.2-3.5 mm long, portion distal to articulation 1.5-2.4 mm long, with hairs as on axes. Calyx (0.3) 0.4-0.7 mm long overall, aestivation apert, lobes (0.1) 0.25-0.35 mm long, (depressed-)deltate, glabrous or more often provided with pubescence as on pedicel and ciliate, the longer hairs sometimes stiff; petals (1.2) 2-2.7 × (0.65) 0.8-1.5 mm, lanceolate to almost elliptic, less often ovate, apex acute, white or cream, abaxial surface glabrous or provided with scattered stiff hairs to 0.25 mm long, petals (slightly) reflexed at anthesis; stamens spreading, antesepalous and antepetalous ones 1.5-2.1 and (1.35) 1.5-1.85 mm long, respectively, the anthers 0.5-0.9 mm long, in dorsiventral view elliptic, in lateral view oblong, yellow, sometimes the antesepalous ones larger than the antepetalous ones,the filaments white; disk 0.2-0.5 mm tall, 0.4 mm thick, summit markedly undulate and outer margin deeply sulcate, (greenish-)yellow, markedly papillate; pistil 0.65-1.1 mm long, subcylindrical overall, divided almost to base into subulate, apically connivent styles 0.45-0.5 mm long, the stigmas extrorse, vertically oblong. Fruits 2.6-3.3 × 1.5-2.2 cm (dry, see note below regarding umbu-cajá), obovoid to subglobose, the apex obtuse to truncate, often the widely separated style scars raised and still evident at maturity, the base usually truncate, sometimes substipitate, maturing (greenish to whitish) yellow, surface smooth and dull; mesocarp thick and fleshy; endocarps 2-2.5 × 1.3-2 cm, essentially obliquely obovoid but laterally compressed and very slightly 1-carinate, entirely enveloped by a smooth, skin-like layer that when peeled away reveals a smooth, hard inner layer with four small and one larger peri-apical, fiber-filled, circular pores and two smaller pores straddling the keel near the proximal end; fruits often 1-seeded.

Leaflet venation: Fimbrial vein absent; secondary veins in 10-20 pairs, straight, attenuate at both ends, spacing uniform, angle nearly perpendicular, insertion on midvein abruptly decurrent; intersecondaries and epimedial tertiaries absent; intercostal tertiaries with some irregular-reticulate veins but primarily composite-admedial departing from secondaries or the intramarginal vein, usually attenuate at both ends; quaternaries irregular-reticulate and freely ramified, areolation at tertiary and quaternary ranks, FEVs 3-4+-branched, dendritic, terminating in only slightly thickened tracheoid idioblasts (see Fig. 3, p. 253 in Silva 1973); marginal ultimate venation looped; on both surfaces the midvein narrowly prominulous (seldom prominent abaxially or flat adaxially), secondaries and higher-order veins flat to prominulous on both sides, sometimes impressed adaxially, the surface glabrous or when young with dense flexuous hairs, often glabrescent except hairs persisting on midvein and toward leaflet base; adaxial side glabrous or when young with scattered flexuous hairs, glabrescent with age.

Distribution.

The native range of Spondias tuberosa is from Maranhão E to Paraíba and south to Minas Gerais in Brazil; it is also cultivated in SE Brazil (see below).

Ecology.

This species is a constituent of the arid caatinga in NE Brazil, known to flower in Aug-Mar and fruit Oct-May ( Machado et al. 1997, plus data from exsiccatae). Nadia et al. (2007) suggested that this species can be andromonoecious, and recent observations of the current senior author in Canudos, Bahia, Brazil indicate that this may be correct.

In Paraíba state, Brazil, two species of bee and one species of wasp were the principal pollinators of Spondias tuberosa flowers ( Nadia et al. 2007). The fruits are dispersed principally by mammals ( Griz and Machado 2001), notably collared peccaries ( Olmos 1993); in anthropic landscapes, cattle can be important dispersal agents ( Griz and Machado 2001).

Common names.

Brazil, Bahia: cajá do sertão (Arbo et al. 7239, GH, NY), imburana (V. Souza 329, NY), caya (Arbo et al. 5776, COL, GH, NY); Maranhão: umbu, umbuzeiro (Eiten & Eiten 10810, NY); Minas Gerais: imbu verdadeiro (Ratter et al. 2702, E), umbu (Andrade & Figueiredo 115, NY); Pernambuco: imburana de cambão (Costa 176, NY), imbuzeiro (Costa 17, NY).

Economic botany.

In the species’ native range, its fruits are often wild-collected or collected from managed (spared) trees ( Popenoe 1948). It is cultivated in SE Brazil, propagated by cuttings or seeds in home gardens or occasionally in orchards (e.g., Lorenzi et al. 2006). It was illustrated in Piso and Markgraf’s (1648) Historia naturalis brasiliae, suggesting a long pre-Columbian history of use. The fruit pulp is used primarily to make a popular juice and ice cream, also to make a drink called umbujada made by boiling the pulp with milk, curds and sugar ( Koster 1816, Popenoe 1948, both as imbuzada; Lins Neto et al. 2010). The fruits and roots are high in Vitamin C ( Cavalcanti et al. 2000). The seeds have potential as a source of cooking oil due to the high oil content, high mineral concentration, and fatty acid composition ( Borges et al. 2007). The roots have been used as a famine food in times of drought ( Nascimento et al. 2012).

Like other species of the genus, Spondias tuberosa has several medicinal uses. In Bahia, the leaves have been used for medicinal baths and a tea of the bark is used to treat colds and dysentery (Mattos Silva 2301, NY).

The species could be a valuable addition to the economic flora and diet of many other dry tropical regions.

Selected specimens examined.

BRAZIL. Bahia: Mun. Uauá, Serra do Jerônimo, 9°43'23"S, 39°19'56"W, 30 Mar 2000, Alves et al. s.n. (ALCB 47955) (CEPEC); Mun. Andaraí, 33 km NE of Mucujé, toward Nova Redenção, approx. 12°49'S, 41°12'W, ca. 450 m, 25 Nov 1992, Arbo et al. 5776 (COL, GH, NY); Mun. Candeal, 8 km N of Tanquinho, trail to Ichu, elev. 200-300 m, approx. 11°54'S, 39°06'W, 15 Jan 1997, Arbo et al. 7239 (CEPEC, GH, NY); Mun. Iaçu, Fazenda Lapa, 12°42'S, 39°56'W, 26 Feb 1983, Bautista 727 (MG); Japirá, Vila do Barra, 1840, Blanchet 3078 (GH, NY, W)(syntype of S. venulosa); Quijingue, Serra das Candéias, 5 km W of Quixabá do Mandacaru village, 10°55'20"S, 39°04'59"W, 350-632 m, 13 Nov 2005, Cardoso et al. 876 (NY); Tucano, Pedra Grande village, road to Serra do Pai Miguel, 11°07'24"S, 38°46'25"W, elev. 224 m, 20 Dec 2007, Cardoso & Ferreira 2234 (NY); Riacho Congú, Cachoeira, valley of Paraguaçu and Jacuipe rivers, 12°32'S, 39°05'W, Nov 1980, Cavalo et al. 942 (NY); Novo Remanso, 9°17'S, 41°32'W, 520 m, (w/o date), Coradin et al. 5945 (K); Andorinha, road to pond, 10°12'44"S, 39°54'46"W, 430-470 m, 18 Feb 2006, França et al. 5464 (NY); road to Manoel Vitorino from Jequié, 14°00'S, 40°10'W, 9 Feb. 1985, Gentry & amp; Zardini 49965 (MO, NY); Mun. Paramirim, km 10-16 ParamirimLivramento do Brumado road, 13°33'S, 42°12'W, 2 Dec 1988, Harley & Taylor 27064 (K, NY, SP); Mun. Rio de Contas, by road 11.5 km from Rio de Contas toward Marcolino Moura, 13°35'52"S, 41°45'22"W, 1 Nov 2004, Harley et al. 55198 (NY); Mun. Bom Jesús da Lapa, Rio das Rãs, elev. 450 m, 15 Nov 1991, Hatschbach et al. 55163 (US); Mun. Glória, Raso da Catarina [ca. 9°40'S, 38°40'W], 31 Jan 1982, Rocha et al. 790 (GUA); caatinga near Caldeirão, Oct 1906, Ule 7255 (K). Ceará: near Lavras da Mangabeira, povoado São Francisco, 30 Jan 1968, Carauta 552 (GUA, NY); Espírito Santo: pasture near corral of Sr. Wilson Machado, km 7, 15 Dec 1992, Folli 1757 (NY); Maranhão: Mun. Loreto, "Ilha de Balsas," region between Balsas and Parnaíba rivers, ca. 35 km S of Loreto, 7°23'S, 45°05'W, elev. 300 m, 9 Feb 1970, Eiten & Eiten 10523 (K, NY), Loreto city, 1 Mar 1970, Eiten & Eiten 10810 (K, NY, US); Minas Gerais: Mun. Januária, district of Fabião, road to Abrigo Bichos, 15°00'-14°57'S, 44°24-30'W, 25 Oct 1997, Lombardi 2080 (NY); Paraíba: W of Campina Grande, between Sta. Luzia and Joazeiro (= Taperoá)[ca. 7°12-13'N, 35°52'-36°49'W], 8 Oct 1927, Ginzberger 1489 (WU); Mun. Barra de Santa Rosa, Fazenda Quandu, region of Curimatan, 30 Jan 1970, Souto 43 (RB); Pernambuco: Mun. Venturosa, Parque Pedra Furada, 8°34'30"S, 36°52'45"W, elev. 783 m, 28 Feb 1998, Costa 17 (NY), Bodocó, near town, 12 Feb 1991, Lisboa & Silva 4521 (MG); Paruaru [Caruaru] (cult.), 4 Nov 1931, D. B. Pickel 590 (GH); Piauí: Mun. Teresina, near Rio Paty, 4 Jul 1907, Ducke 799 (MG); São Miguel do Tapuio, 22 May 1979, Fernandes s.n. (EAC 6044)(NY); Mun. São Raimundo Nonato, Fundação Ruralista, +/- 8-10 km NNE of Curral Novo and 220 km ENE of Petrolina, ca. 9°00'S, 42°00'W, elev. 320 m, 22 Jan 1982, Lewis & Pearson 1154 (K); Rio de Janeiro: Jardim Botânico (cult.), 2 Oct 1939, Kuhlmann s.n. (RB 40595) (RB); Campos, Atafona (cultivated), Apr 1939, Sampaio 8219(R); São Paulo: Cajuru, Fazenda Sta. Carlota (cult.?), 13 Nov 1986, Bernacci 174 (SPF). UNITED STATES. Florida: Miami-Dade County, Homestead, 611 West Pierce Ave. (cult.), elev. 10 m, 3 May 1928, Fisher s.n. (BRIT).

Conservation status.

We consider this species to be of Least Concern. It is broadly distributed in the caatinga vegetation of NE Brazil, and even where its habitats are highly disturbed, it is spared because of its highly prized fruits. Moreover, it is cultivated both within and beyond its range. On the other hand, one must consider the possibility that native populations are declining due to disturbance.

Discussion.

This species first appeared in print (as Spondias tuberosa ) in the appendix of Koster’s Travels in Brazil (1816), in which Koster translated text and a large number of nomina nuda ascribed to "Arrud. Cent. Plant. Pern." These referred to Manuel Arruda Câmara’s Centuriae plantarum pernambucensium , which was never published but formed the foundation for Pinto’s (1873) Diccionario de Botanica Brasileira (see summary in Kirkbride 2007, also Britten 1896). Although no type exists, the plant’s distribution, common names, and uses leave no doubt as to its identity, so a neotype has been selected.

The circumscription of Spondias tuberosa is complicated by the occurrence in Bahia of an entity - most or all of whose individuals are cultivated - that is recognized by local people as distinct enough to merit a different common name, umbu-cajá or cajá-umbu. The fruit is indeed distinct: the pyrene is larger (2.7-2.8 × 1.8-1.9 cm vs. 2-2.5 × 1.3-2 cm); more significantly, the stony endocarp is overlain by a thinner fibrous matrix, moreover the five peri-apical pores are subequal in size (vs. four small and one larger), larger than in Spondias tuberosa , and oblong (vs. circular), and the pyrene has four (vs. 1) keels or trabeculae (beams)(based on Mattos Silva et al. 2299, NY). The fresh fruit is ca. 4-4.7 × 3.2-3.4 cm and the pyrene 2.7-2.8 × 1.8-1.9 cm ( Lorenzi et al. 2006).

On the other hand, the vegetative and floral morphology of the material referred to umbu-cajá is almost indistinguishable from those of Spondias tuberosa , although the leaflets tend to be larger and more broadly ovate, and the apex to be narrowly acuminate. The revolute leaflet base with rather dense long hairs more closely resembles that of Spondias venulosa . We are not aware of any differences in habit or in bark morphology.

The fruits of umbu-cajá are consistently obovoid, but this is within the range of variation of Spondias tuberosa s.s.; the fruit surface is sparsely lenticellate, which we have not observed in Spondias tuberosa s.s. (Marlon Marchado, pers. comm., 4/2013).

In his book on Brazilian fruits, Lorenzi et al. (2006) treated umbu-cajá (e.g., Lorenzi 6074, NY) as a separate entity from Spondias tuberosa , observing that it produces only sterile seeds, that it is propagated only by cuttings, and that it is known only in cultivation in Bahia, Alagoas, and Pernambuco states.

Silva Júnior et al. (2004) suggested that umbu-cajá is a hybrid between Spondias tuberosa and Spondias mombin , but Almeida et al. (2007) examined karyology and genomic in situ hybridization of Spondias spp. and concluded that the umbu-cajá (1) is not of hybrid origin and (2) is distinct from both putative parents. In the present treatment, this entity is considered a variant of Spondias tuberosa unless and until further genetic/molecular investigations suggest otherwise.

Several collections can be referred to umbu-cajá. Brazil. Bahia: Mun. Itabuna, city center, 2 Apr 1998, Carvalho & Kersul 6493 ( cajá-umbu, NY); Mun. Cruz das Almas, cultivated at EMBRAPA, 14 Feb 2006, Lorenzi 6074 (E, HPL, MO, NY); Mun. Maracás, Fazenda Tanquinho (entrance at km 23 of MaracásPalnaltino road), 3 Mar 1988, Mattos Silva et al. 2299 ( cajá-imbu, CEPEC, NY), 3 Mar 1988, Mattos Silva et al. 2301 ( umbu-cajá, CEPEC, NY).