New Species of Virola (Myristicaceae) from South America Author Santamaria-Aguilar, Daniel https://orcid.org/0000-0002-6339-8250 Shirley C. Tucker Herbarium, Department of Biological Sciences, Louisiana State University, 103 Life Sciences Building, Baton Rouge, Louisiana 70803 - 1705, USA & Missouri Botanical Garden, St. Louis, Missouri, USA daniel.santamaria366@gmail.com Author Lagomarsino, Laura P. Shirley C. Tucker Herbarium, Department of Biological Sciences, Louisiana State University, 103 Life Sciences Building, Baton Rouge, Louisiana 70803 - 1705, USA text PhytoKeys 2022 2022-05-30 197 81 148 http://dx.doi.org/10.3897/phytokeys.197.81367 journal article http://dx.doi.org/10.3897/phytokeys.197.81367 1314-2003-197-81 37EA452A15155D1CB85CA350AF70A112 6. Virola cumala D. Santam. sp. nov. Type . Peru . Amazonas : Bagua , distrito Imaza , Region Nororiental del Maranon , Comunidad de Kampaenza , Ribera de la quebrada Shimutaz , Rio Maranon , 04°55'S , 078°19'W , 320 m , 09 Sep 1994 (fr), N. Jaramillo , R. Apanu , G. Apanu 388 ( holotype : MO! [accession 5096935, barcode MO-254989]; isotypes: UPCB [n.v.]). Fig. 11 Figure 11. Virola cumala A branch with leaf blades, with detail of abaxial surface showing trichomes and tertiary venation B part of staminate inflorescence C lateral view of staminate perianth with detail of trichomes (top) D medial section of staminate flower and androecium (right) E fruits with detail of trichomes (left), and open fruit showing seed covered with laciniate aril. Drawn by Bobbi Angell based on R. Vasquez & C. A. Grandez 17532 ( A-D MO), and N. Jaramillo et al. 388 ( E MO). Diagnosis. Virola cumala is most similar to V. decorticans and V. multinervia ; all these species have large leaves, numerous lateral veins, dense indument of dendritic brown to ferruginous trichomes in almost all parts of the plant, and large fruits. Morphologically, it differs from V. decorticans in having leaf blade on upper surface glabrous (vs. pubescent), the staminate perianth is subcarnose, without lines or dots (vs. submembranous, and with lines), long filament column (0.5-0.7 mm vs. 0.3-0.4 mm), and anthers (0.7-0.9 mm vs. 0.5-0.6 mm), and narrow fruits (2.3-2.9 cm vs. 1.7-2.2 cm). It differs from V. multinervia in the staminate perianth subcarnose (vs. membranous), densely pubescent on all the surface (vs. glabrous or pubescent only at the base and apex), long anthers (0.7-0.9 mm vs. 0.3-0.4 mm), and large fruit (2.3-2.9 cm vs. 1.5-2.5 cm). Tree 15-35 m x 38 cm diameter; inner bark and exudate not described. Twigs 0.52-1.2 cm thick, laterally flattened to angled, densely tomentose, trichomes dendritic, branched from the base (1-2 mm long) with short lateral branches (0.1-0.2 mm long), brown, sometimes the bark in mature twigs cracks and flakes in small pieces. Leaves young terminal bud 2-2.5 x 0.6-2 cm; petiole 0.9-2.2 x 0.43-0.9 cm, strongly canaliculate, densely pubescent, trichomes dendritic; leaf blades 33.1-50.7 (-56.5) x (9.5-) 11.7-15.5 cm, elliptic-oblong to elliptic to obovate, sometimes gradually tapering towards the base; adaxial surface of mature leaves (usually) drying brown to dark grayish, glabrous, smooth; abaxial surface drying brown to pale brown, densely pubescent, the trichomes dendritic, yellowish to pale brown, shortly pediculated (branched almost at the base), with 5-8 branches, the branch 0.3-0.7 mm long, persistent; lateral veins 49-65 per side, with 5-7 (-11) veins per 5 cm, spaced 0.4-1.1 cm apart, the same color as the adaxial surface or sometimes slightly contrasting in color, impressed, on abaxial surface the same color as the surface, very conspicuous and raised, slightly straight to arcuate distally, anastomosing very near the margin, forming an intramarginal vein; tertiary veins slightly prominent adaxially, very prominent abaxially; midvein adaxially flat, pubescent, abaxially raised, rounded, pubescent; base cordate to subcordate, not revolute, flat; margin flat; apex acute to cuspidate. Staminate inflorescences 7.5-12 cm long, axes slightly flattened at the apex of the defoliated branches, densely pubescent, the trichomes dendritic (1-1.6 mm long), ferruginous; peduncle 1.3-1.5 x 0.34-0.47 cm; bracts 0.4-0.7 x 0.2-0.4 cm, ovate, sometimes triangular, with 3 vertical lines, pubescent on both sides, caducous. Staminate flower not very dense, terminal fascicles of 13-21+ flowers, on a receptacle ca. 2 mm wide; pedicel 1.5-2 mm long, pubescent; perianth 2-3 mm long, elongate, subcarnose, brown when fresh, connate to 0.6-1 mm in length, external surface densely pubescent with brown trichomes, internal surface glabrous; lobes 3, 1.1-1.5 x 0.4-0.6 mm, 0.1-0.2 mm thick, without resinous punctuations when rehydrated; stamens 3, the filament column 0.5-0.7 mm long and 0.1-.0.2 mm wide, thin, straight, not constricted at the apex; anthers 0.7-0.9 mm long, and ca. 0.2 mm wide; apiculus inconspicuous or obtuse. Pistillate inflorescences and flowers not seen. Infructescence 3.5-5.5 cm long, with 1-3 fruits, peduncle 1-2.7 x 0.4-07 cm. Fruits 3-3.5 x 2.3-2.9 cm, brown (possibly by the indumentum) when fresh, rounded to ellipsoid, densely and persistently pubescent with a layer of trichomes of 1-2.3 mm thick, the trichomes dendritic, brown to ferruginous, the surface not seen, the line of dehiscence not carinate, the base and apex obtuse; pericarp 3-6 mm thick; pedicel ca. 0.5 mm long. Seed (1.9-) 2.3-2.5 x (0.8-) 1.1-1.9 cm, the testa pale brown to brown reddish when dry, grooved ( N. Jaramillo 550 ), aril when fresh not described, brown to blackish when dry, the texture dry and thin, laciniate in very narrow bands, almost to the base. Distinctive characters. The most distinctive characteristic of Virola cumala is the dense indument of dendritic brown to ferruginous trichomes that cover almost all parts of the plant. Vegetatively, this species also has large leaves with numerous lateral veins that are prominent (including the tertiary veins, especially below), thick twigs, and bark that sometimes cracks and flakes into small pieces. Further, the staminate flowers have a subcarnose perianth that is densely and uniformly pubescent outside and glabrous inside with narrow lobes, a filament column that is straight and similar in length to the anthers, and large fruits that are covered with a thick layer of trichomes, thick pericarp, and a seed covered by an aril that is laciniate in very narrow bands almost to the base (Fig. 12D ). Figure 12. Diversity of fruits from Virola species that have numerous and close lateral veins, notice the shape, indument, and pericarp thickness A V. caducifolia ( W. Rodrigues & D. Coelho 8700 , MO) B V. chrysocarpa ( B. Hammel et al. 16864 , MO) C V. crebrinervia ( N. A. Rosa 4446 , NY) D V. cumala ( C. Gra [n]dez et al. 4919 , MO) E V. decorticans ( C. A. Cid Ferreira et al. 9961 , MO) F V. koschnyi ( L. D. Gomez et al. 22725 , MO) G V. megacarpa ( G. de Nevers 5184 , MO) H V. multinervia ( C. A. Sothers & E. D. C. Pereira 1069 , MO) I V. multicosta ( R. Vasquez & C. Grandez 17507 , MO). Scale bars: 1 cm. Etymology. The specific epithet is taken from the common name on the label of R. Vasquez & N. Jaramillo 7879 , MO). This common name is often used in Peru to refer to various species of Virola , as well to other species in Otoba (A. DC.) H. Karst., Iryanthera (A. DC.) Warb., and Osteophloeum Warb. (e.g. Vasquez Martinez 1997 ; Zarate-Gomez et al. 2019 ). Distribution. Virola cumala is known only from Peru (in the Amazonas, Loreto, and Pasco departments) (Fig. 18C ). It occurs in primary forests in non-inundated, lateritic soil. It ranges in elevation from 120-320 m, although one collection from Pasco reaches 700-800 m ( H. van der Werff 20095) . It is possible that this species also occurs in Ecuador, as some collections were made close to the border of Peru and Ecuador. Phenology. Staminate flowers of Virola cumala have been recorded in July; pistillate flowers were not seen in the studied material. Fruits have been collected in May, August to October, and December. Common name and uses. Cumala negra (Peru; R. Vasquez & N. Jaramillo 7879 , MO). Preliminary conservation status. Virola cumala is Endangered following IUCN criterion B2a. It is known from five localities, has an EOO of 219,024 km2, and an AOO of 20 km2. Justifying its status, the western Amazonian region where this species occurs is modeled to be modestly impacted by new road construction, a threat that is likely to be superseded by the development of oil palm plantations in the region ( Arima 2016 ). Discussion. Virola cumala is found among a morphological group of ca. 17 species (personal count) that correspond to the group Rugolosae of Smith and Wodehouse (1938) . Generally, this group is characterized by leaves with numerous, closely adjacent lateral veins, percurrent tertiary veins that are usually conspicuous, cordate bases, and dendritic trichomes; staminate inflorescences often with large bracts that cover flowers; staminate flowers that are small and usually densely aggregated with membranous to sub membranous perianth, the tube almost split to the base, and a slender filament column. Within this group, the new species is most similar to V. decorticans Ducke and V. multinervia Ducke, both from South America, and V. megacarpa A. H. Gentry from Panama. All four species have large leaves, numerous lateral veins, dense indument of dendritic brown to ferruginous trichomes in almost all parts of the plant, large fruits with a thick layer of trichomes (thin in V. megacarpa ), and thick pericarp. Virola cumala further shares bark that cracks and flakes into small pieces and the thick young terminal bud of leaves. These species are distinguished by the characteristics presented in Table 8 . Table 8. Comparison of Virola cumala , with three other morphologically closely related Virola species. ‡‡From Rodrigues (1980) . Perianth information for V. decorticans is from C. Grandez et al. 2525 , MO), and fruits from C. A. Cid Ferreira 7307, 9961 , MO); while those of perianth, filament column and anthers presented for V. multinervia are from C. A. Cid Ferreira et at. 7537 , MO; W. Rodrigues & D. Coelho 9617 , MO; J. E. L. S. Ribeiro 1249 , MO; and W. Thomas et al. 5239 , MO).

Morphological character	V. cumala	V. decorticans	V. megacarpa	V. multinervia
Leaf blade upper surface	Glabrous	Pubescent	Glabrous	Glabrous
No. of lateral veins	49-65	45-60‡‡	(32-) 40-50	40-60‡‡
Staminate perianth texture, and pubescence on external surface	Subcarnose, without lines or dots, densely pubescent on all the surface	Submembranous, with lines, pubescent	Subcarnose, without lines or dots, densely pubescent on all the surface	Membranous, with lines, glabrous or pubescent only at the base and apex
Filament column length	0.5-0.7 mm	0.3-0.4 mm‡‡	0.9-1.3 mm	0.3-0.5 mm
Anther length	0.7-0.9 mm	0.5-0.6 mm‡‡	0.8-0.9 mm	0.3-0.4 mm
Fruit size and apex	3-3.5 x 2.3-2.9 cm, obtuse (Fig. 12D )	2.7-3.5 x 1.7-2.2 cm‡‡, acute to apiculate (Fig. 12E )	4-5.7 x 2-2.9 cm, acuminate to rostrate (Fig. 12G )	2-3 x 1.5-2.5 cm, apiculate‡‡ (Fig. 12H )
Pericarp thickness	3-6 mm	4-5 mm	3-6 mm	1.5-4 mm

Virola cumala can be distinguished from other species with numerous lateral and relatively close veins (e.g., V. caducifolia W. A. Rodrigues, V. chrysocarpa D. Santam. & Aguilar, V. flexuosa A. C. Sm., V. guggenheimii W. A. Rodrigues, V. koschnyi Warb. and V. polyneura W. A. Rodrigues) by its fruits: these are large (3-3.5 x 2.3-2.9 cm vs. 1.6-3 x 1.3-2.5 cm), covered with a thick layer of trichomes (vs. tomentose or glabrescent), and have a thick pericarp (3-6 mm vs. 1-4 mm). The fruits of Virola divergens , V. loretensis A. C. Sm., and V. mollissima (species of Mollissimae group in Smith and Wodehouse 1938 ) are also covered by a dense layer of trichomes that is similar to V. cumala (cf. Fig. 3E ). However, these species have fewer lateral veins (15-30 vs. 49-65), anthers with an apiculate apex (vs. inconspicuous or obtuse), and thin pericarp (0.3-0.7 vs. 3-6 mm). Notes. The type specimen of V. cumala ( N. Jaramillo et al. 388 , MO) was cited as V. multinervia in Vasquez et al. (2018) . Peruvian specimens identified as V. multinervia are very variable, likely representing a combination of misidentifications and undescribed species. Within these, we identified three morphologically distinct groups. The first group corresponds to V. cumala . The second, represented by the fruiting specimens A. H. Gentry et al. 42594 (MO), C. Grandez et al. 4929 (MO), R. Vasquez & C. Grandez 17507 (MO-2 sheets), we tentatively identify as V. multicostata Ducke (due to lack of flowers). This group is characterized by scant pubescence covering twigs, petioles, and axes of the infructescence, large leaf-blades (28-37 x 8.1-10 cm) with numerous lateral veins (54-62), the tertiary veins prominent below, and inconspicuously pubescent to glabrescent fruits that are 2.1-2.3 x 1.5-1.8 cm (Fig. 12 ) with a rugose surface and thin pericarp (1.3-1.5 mm). Finally, the third group is represented by the specimens A. H. Gentry et al. 19014 (♂ fl.), A. H. Gentry et al. 21736 (very young fl. bud.; F [image], MO!), and R. Vasquez & N. Jaramillo 9379 (♀ fl; MO!). This group is characterized by deciduous (i.e. all leaves fall off the tree), oblong leaves (32.7-44 x 8.5-12.6 cm), brown trichomes that cover the entire plant, staminate inflorescences with bracts that are 0.9-1.5 x 1-1.2 cm, staminate flowers with a ca. 2 mm long perianth which is connate to 0.5 mm in length and densely pubescent externally, glabrous internally, and without dots or lines when rehydrated, perianth lobes that are ca. 1.5 x 0.6 mm, and a filament column ca. 0.4-0.5 mm long with anthers 0.4-0.6 mm long. Specimens examined. Peru . Amazonas : Bagua , distrito Imaza , Region Nororiental del Maranon , Comunidad de Kampaenza , Ribera de la quebrada Shimutaz , Rio Maranon , 04°55'S , 078°19'W , 320 m , 10 Oct 1994 (fr), N. Jaramillo & C. Peas 550 (MO!, UPCB [n.v.]) . Loreto : Yanamono , Explorama Tourist Camp on Rio Amazonas between Indiana and mouth of Rio Napo , 03°28'S , 072°48'W , 120 m , 26 July 1980 ( ♂ fl), A. H. Gentry et al. 29027 (INPA [image!], MO!); ExplorNapo Camp ( Rio Sucusari ), 03°15'S , 072°54'W , 140 m , 29 July 1991 ( ♂ fl), R. Vasquez & C. A. Grandez 17532 (MEXU [image!], MO-2 sheets); Maynas, IQ [ Iquitos ]- Nauta , Km 32, 150 m , 20 Aug 1986 (fr), R. Vasquez & N. Jaramillo 7879 (MO!); Maynas , Distrito Las Amazonas , Explor Napo ( Suwzari ), 03°20'S , 072°55'W , 124 m , 5 Dec 1992 (fr), C. Gra [n]dez et al. 4919 (MO!) . Pasco : Distr. Palcazu , El Paujil , 10°20'12"S , 075°15'39"W , 700-800 m , 13 May 2005 (fr), H. van der Werff 20095 (F [image!]) .