A taxonomic synopsis of Virola (Myristicaceae) in Mesoamerica, including six new species Author Santamaria-Aguilar, Daniel Author Aguilar, Reinaldo Author Lagomarsino, Laura P. text PhytoKeys 2019 134 1 82 http://dx.doi.org/10.3897/phytokeys.134.37979 journal article http://dx.doi.org/10.3897/phytokeys.134.37979 1314-2003-134-1 05B0E5AA9A175E549730B523BCD54C03 1. Virola allenii D.Santam. & Aguilar sp. nov. Figs 5 , 6 , 7A Diagnosis. Species resembling Virola macrocarpa in its leaf blades that are whitish on the abaxial side and covered with stellate, sessile trichomes with the centre reddish and contrasting with the hyaline branches to reddish-clear in colour and lateral veins that are not densely arranged, as well as large fruits that are covered with ferruginous trichomes. It differs in its narrow leaf blades (3.2-7.3 cm vs. 7-11 cm wide) with acute or obtuse to rounded bases (vs. broadly obtuse), fruits with thick pericarp (3.2-3.8 mm vs. 1.8-3 mm thick) and preference for humid lowland forests at 0-350 (-1350) m elevation (vs. montane forests in Andes of Colombia at around 1100 m elevation). Type. Costa Rica. Puntarenas: Esquinas forest preserve, 0 m, 10 Jan 1951 (♂ fl), P. H. Allen 5763 (holotype: F-2 sheets* [1394346!, 1679106!]; isotype: USJ [9016]). Figure 5. Virola allenii A leaves B fruit C partial inflorescences. Drawn by Pedro Juarez based on P. H. Allen 6727 ( A ), R. Aguilar 2224 ( B ) and R. Aguilar ( C ) from a photo, physical specimen not seen. Figure 6. Virola allenii A treetop B branching C lower trunk and buttress D branch with leaves, showing the adaxial surface E leaf blades on abaxial surface F exudate of the trunk G leaf blade surfaces, adaxial (above) and abaxial (below) H petiole and leaf base I mature fruit, inset left and arrow showing the galls on leaves and branches, respectively J fruits K fruit close-up. Photos by Reinaldo Aguilar. Figure 7. Comparisons of Virola macrocarpa with similar species in Mesoamerica A V. allenii ( P. H. Allen 5763 , F; inset fruits, from P. H. Allen 6727 , GH) B V. amistadensis ( G. McPherson 9717 , MO; inset fruits, from G. McPherson 9715 , MO) C V. macrocarpa ( A. E. Lawrance 675 , MO) D V. otobifolia ( J. P. Folsom 1440 , MO). Image courtesy of Field Museum ( A ). Description. Tree 13-30 m x 10.4-50 cm DBH; bark sometimes described as smooth and reddish or dark brown. Exudate sometimes described as abundant and reddish or watery, but without specifying from where or red in the trunk. Twigs 0.16-0.22 cm thick, terete to slightly flattened laterally, puberulent, trichomes stellate to irregularly stellate, ferruginous. Leaves : petiole 0.5-1.4 x 0.13-0.24 cm, slightly canaliculate, tomentose, the trichomes stellate to irregularly stellate; leaf blades 16.2-29.2 x 3.2-7.3 cm, oblong-elliptic or rarely elliptic; adaxial surface of mature leaves olive or light brown (sometimes shining) when dry, glabrous or with scattered stellate trichomes, the surface smooth; abaxial surface pale brown to whitish when dry, densely but inconspicuously pubescent, trichomes stellate, sessile, the central part of the trichome reddish and contrasting in colour with the hyaline branches to reddish-clear, with 4-10 branches, the branches +/- 0.01-0.05 mm long, persistent; lateral veins 15-20 per side, 4-5 veins per 5 cm, 1.2-1.8 cm apart, the same colour as the adaxial surface or slightly transparent, on adaxial side flat to sunken, on abaxial side slightly elevated, arcuate-ascending, slightly anastomosing near the margin and without forming a very marked intramarginal vein; tertiary veins barely visible on both sides; midvein adaxially slightly elevated (sometimes flat, distally), abaxially raised, rounded to somewhat triangular, tomentose to glabrate; base acute or obtuse to rounded, not revolute, flat; margin flat; apex acuminate or rarely rounded. Staminate inflorescences 3.5-5.5 cm long, axillary, axes flattened, tomentose, with trichomes irregularly stellate, ferruginous; peduncle 1.2-1.9 x ca. 0.1 cm long; bracts not seen; terminal fascicles dense, with 15-40+ flowers. Staminate flowers with the pedicel 0.3-1.2 mm long; receptacle 1.2-2 mm wide; perianth 2-2.8 mm long, infundibuliform, yellow when fresh, connate by 1.1-1.7 (-2.3) mm long, external surface pubescent, with brown trichomes, internal surface glabrous or with few trichomes close to the margin of the lobes; lobes 3 (4), 0.8-1.5 x 0.6-0.9 (-1.2) mm; stamens 3, the filament column 0.5-0.6 mm long, glabrous, straight, thin, sometimes slightly thickened at the base, not constricted at the apex; anthers 0.6-0.9 mm long; apiculus 0.06-0.1 mm long, acute to apiculate, connate. Pistillate inflorescences and pistillate flowers not seen. Infructescence 2.5-7.5 cm long, with 2-13 fruits, peduncle 2-3.5 x ca. 0.47 cm. Fruits 2.7-3.5 x 1.5-2.5 cm, usually ellipsoid or rarely ovoid, stipitate, densely tomentose, the trichomes dendritic, ferruginous and falling very easily to the touch (as dust), the surface rugose or smooth when dry, the line of dehiscence usually carinate, but not very conspicuous, the base obtuse, the apex acute to obtuse, green or golden and ferruginous by the pubescence when fresh; pericarp 3.2-3.8 mm thick; pedicel 0.4-0.7 cm long; seed ca. 2.5 x 1.3 cm, the testa when dry whitish-greyish, markedly grooved; aril usually described as red when fresh, pale brown when dry, membranaceous, the texture dry and thin, laciniate in narrow bands distally. Germination epigeal, seedling cryptocotylar, the first pair of leaves (sub)opposite ( Ley Lopez and Chacon Madrigal 2017 ; as V. macrocarpa ). Distinctive characters. Virola allenii is recognised by its narrow leaf blades with lateral veins that are well separated ( Fig. 8A ) with a whitish abaxial surface and covered with stellate, sessile trichomes with the central portion of the trichome reddish and contrasting in colour with the hyaline branches to reddish-clear ( Figs 3A , 6F ); the staminate flowers with the lobes of the perianth almost glabrous on the inner surface, the column of filaments straight and not constricted at the apex, anthers that are usually longer (0.6-0.9 mm long) than the column of the filaments (0.5-0.6 mm long) and an apiculus that is 0.06-0.1 mm long. It is also distinctive for its large, usually ellipsoid fruits ( Figs 4A , 6 I-K ) with thick pericarp that are green when ripe and covered by ferruginous trichomes that fall very easily to the touch ( Fig. 6K inset); and seeds with the testa markedly ribbed. Figure 8. Pattern of the lateral veins in Mesoamerican Virola A Virola allenii ( K. Thomsen 1284 , NO) B V. amistadensis ( G. McPherson 8703 , MO) C V. chrysocarpa ( B. Hammel et al.16864 , MO) D V. elongata ( M. Correa & R. L. Dressler 1078 , MO) E V. fosteri ( G. de Nevers 7226 , MO) F V. guatemalensis ( G. Ibarra 957 , MO) G V. koschnyi ( J. Miller & J. C. Sandino 1110 , MO) H V. laevigata ( N. Zamora & T. D. Pennington 1583 , MO) I V. megacarpa ( G. de Nevers 5184 , MO) J V. montana ( E. Lepiz & J. F. Morales 284 , MO) K V. multiflora ( J. Manzanares 3561 , MO) L V. nobilis from Barro Colorado ( R. J. Schmalzel 320 , MO) M V. otobifolia ( G. de Nevers et al. 7530 , MO) N V. sebifera ( T. B. Croat 5959 , MO) O V. nobilis from Osa Peninsula ( R. Aguilar 11186 , MO). Etymology. The specific epithet honours the collector of the type specimen, Paul H. Allen (1911-1963), who was probably the first person to collect this species 67 years ago ( P. H. Allen 5763 ; 10 Jan 1951). During his five-year residency in Palmar Norte, Puntarenas, Costa Rica ( Grayum et al. 2004 ), Allen made important collections and publications in this region (e.g. The Rain Forests of Golfo Dulce, Allen 1956 ). Distribution. Virola allenii is known only from Costa Rica (Puntarenas and San Jose ) ( Fig. 9A ). It is found on the Pacific slope, at 0-350 (-1350) m elevation. Figure 9. Geographic distribution of Virola allenii ( A ), V. amistadensis ( B ), V. chrysocarpa ( C ), V. elongata ( D ), V. fosteri ( E ) and V. guatemalensis ( F ). Preliminary conservation status. Virola allenii is Vulnerable following IUCN critera B1a and B2a. Justifying its status, it is known from seven localities and has an EOO of 3,424 km2 and an AOO of 40 km2. Specimens have been collected regularly since the 1990s during botanical expeditions in the Osa Peninsula of Costa Rica, though only 22 specimens have been verified. Common names. None recorded. Phenology. Flowering of Virola allenii has been recorded in January, March, April and December. Fruits have been observed in January, August to October. Pistillate flowers were not seen in the studied material. Field characters. The bark is described as brown and smooth or as peeling in small pieces, sometimes with a strong, spicy scent. Twigs and leaves often have galls (e.g. Fig. 6I ). Leaf blades are adaxially lustrous and abaxially whitish. Staminate flowers are yellow and fragrant. Fruits, which are ca. 5 x 3.2 cm when fresh, are green at maturity and covered with brown trichomes that fall very easily when touched and have a pericarp that is ca. 6 mm thick. The aril of mature fruits is red and white in immature fruits. Seeds have a white testa. Discussion. Virola allenii is most similar to V. macrocarpa , a species from montane forests at 1100 m elevation in the Andes of Colombia ( Boyaca ) and this name has been previously applied to the species described here (e.g. Jimenez 2007 ; Cornejo et al. 2012 ; Aguilar et al. 2017 onward ). It is differentiated from V. macrocarpa by the characteristics presented in the diagnosis and in Table 2 . The comparison presented hereafter for Virola macrocarpa ( Fig. 7C ) is strictly based on the protologue (except for the pericarp thickness), from which we have been able to study two physical duplicates deposited at MO ( A. Lawrance 675 , MO-2 sheets!, fr [ Fig. 4D ]) and the images at A! (st), F! (2-sheets, fr), G! (2-sheets, st.), K! (st), S (fr) and US! (2-sheets, fruits likely in the packet, but not seen). We confirmed all measurements from the protologue on Lawrance 675 (MO) and found them consistent with the exception of pericarp thickness; while 2-4 mm was stated in the protologue, our measurements ranged from 1.8-3 mm, which we present in Table 2 below. In our estimation, all other observed South American specimens, annotated with this name, represent an amalgamation of different identities (D. Santamaria-Aguilar , in prep.). Based on a number of features listed in the diagnosis of V. alleni , including colour of the abaxial leaf blade, sessile trichomes, degree of separation of lateral veins and the length of the anther apiculus, V. allenii is similar to V. calophylla ( Fig. 10A, B ) and V. calophylloidea from South America; the latter was recently included as a synonym of V. calophylla (see notes below). Furthermore, Virola allenii also shares narrow oblong-elliptic leaf blades (3.2-8 cm broad) and short inflorescences with V. calophylloidea . However, it is distinguished from both species by the filament column that is constricted at or towards the apex (vs. not constricted in V. allenii ) and the tendency towards short anthers (0.4-0.7 mm vs. 0.6-0.9 mm long). Additional differences amongst these three species are presented in the Table 2 . Figure 10. Virola calophylla A branch with leaves, showing both sides B branch with inflorescences. Virola elongata C leafy branch with inflorescences, inset fruit D inflorescences. Virola guatemalensis E, F leaf blades showing adaxial ( E ) and abaxial ( F ) surface. G young twigs and petioles. Photos by Robin Foster ( A, B) , from https://plantidtools.fieldmuseum.org/en/nlp; Steven Paton ( C, D) , Rolando Perez ( C inset), from https://stricollections.org/portal/index.php and Angela Rojas ( E-G ). In Mesoamerica, Virola allenii can be confused with V. amistadensis and V. otobifolia (which are formally described as new below). All these species have lateral veins that are well spaced ( Fig. 8A, B, M ) and an abaxial leaf surface that is usually whitish with sessile stellate trichomes; for differences between these species see Table 3 . Some of the first specimens of this new species were confused with other taxa, though they differ based on their trichomes: Otoba (e.g. L. J. Poveda 887 , CR!) with malpighiaceous trichomes (vs. stellate trichomes), Virola sebifera (e.g. N. Zamora et al. 1440 , CR!) with dendritic to dendritic-stellate and generally pediculate trichomes (vs. stellate and sessile) ( Fig. 3A, N ); or V. guatemalensis (e.g. P. H . Allen 6727 , F, GH) with the central part of the trichome colourless (vs. reddish) and with more compressed lateral veins (0.6-1.1 cm vs. 1.2-1.8 cm of separation between veins) ( Figs 3A , 8A, F ). Table 2. Comparison of Virola allenii with the morphologically most similar species.

Character	V. allenii	V. calophylla	V. calophylloidea *	V. macrocarpa
Leaf blade	16.2-29.2 x 3.2-7.3 cm; base acute or obtuse to rounded	(15-) 20-60 x 10-16 cm; base (usually) deeply cordate to truncate (obtuse)	16-33 x 4.5-8 cm; base cordate to rounded or broadly obtuse	20-40 x 7-11 cm; base broadly obtuse†
Length of staminate inflorescences	3.5-5.5 cm	6-30 cm	1-4 cm	Unknown
Length of perianth of staminate flowers	2-2.8 mm	1-2.1 mm	1.7-2 mm	Unknown
Filament column	0.5-0.6 mm long; not constricted at apex	0.2-0.6 mm long; constricted at apex	0.7-0.8 mm long; abruptly narrowed at apex	Unknown
Anther length	0.6-0.9 mm	0.4-0.5 mm	0.5-0.6 mm	Unknown
Fruit	2.7-3.5 x 1.5-2.5 cm; base obtuse	2.5-3 x 1.2-2.5 cm; base usually truncate	1.8-2.1 x0.8- 1.1 cm; base obtuse	2.7-3.3 x 2-2.3 cm; base obtuse†
Pericarp thickness	3.2-3.8 mm	0.5-5 mm	0.5-0.8 mm	1.8-3 mm

*From Smith 1938. Table 3. Comparison of Virola allenii with the two other morphologically most similar species in Mesoamerica.

Characters	V. allenii	V. amistadensis	V. otobifolia
Leaf blades	16.2-29.2 x 3.2-7.3 cm	12.3-22.8 (-27) x 4.4-9.5 (-12.5) cm	(14-) 18.2-42.5 x (4.1-) 7.3-14.2 cm
Lateral veins	15-20 per side	9-15 per side	10-16 per side
Length of staminate inflorescence	3.5-5.5 cm	3-7.5 cm	3.5-9.5 cm
Length of perianth of staminate flowers	2-2.8 mm	1.5-2.2 mm	2.5-2.8 mm
Filament column	0.5-0.6 mm; not constricted at apex	0.2-0.4 mm; constricted at the apex	0.9-1 mm; constricted at the apex
Anther length	0.6-0.9 mm	0.6-0.7 mm	0.6-1 mm
Fruit	2.7-3.5 x 1.5-2.5 cm ( Fig. 4A )	2.1-3.8 x 1.7-2 cm ( Fig. 4B )	(2.7-) 3.5-4.5 x (1.9-) 2.3-2.9 cm ( Fig. 4C )
Pericarp thickness	3.2-3.8 mm	1-2 mm	(2.7-) 3-4.7 mm
Seed	ca. 2.5 x 1.3 cm	1.6-2.2 x 1.4-1.6 cm	2.5-2.8 x 1.5-1.7 cm

Notes. The holotype, deposited at Field Museum (F), represents two sheets with hand written annotation ("Sheet 1 of 2," "Sheet 2 of 2"), which suggests that they represent a multi-sheet specimen of the same plant (ICN Art. 8.3) ( Turland et al. 2018 ). The specimen B. Hammel et al. 24041 (CR!; fr) from 1370 m elevation in the Tarrazu region of San Jose province (Costa Rica) differs from other members of this new species by its more rounded and pubescent fruits and its occurrence at a higher elevation than other specimens. It is included here with some reservation. This specimen is most similar to E. Alfaro 492 (CR!, LSU!, MO!; ♂ fl), which was also collected in montane forests on the Pacific slope of the Cordillera de Talamanca (1240 m elevation). E. Alfaro 492 differs from the rest of V. alleni in its larger staminate perianth (ca. 3.8-4 mm vs. 2-2.8 mm long) that is fleshy with dense pubescence on the entire adaxial surface (vs. glabrous or with sparse trichomes close to the margin of the lobes in V. allenii ) and the column of the filaments (ca. 0.5-0.7 mm vs. 0.5-0.6 mm long) that is shorter than the anthers (ca. 1.2 mm vs. 0.6-0.9 mm long). This specimen was also discussed by Jimenez (2007) as V. macrocarpa . The specimens [ P. H .] Allen 5763 (type; F, USJ) and [ P. H .] Allen 6727 (F, GH), cited as V. guatemalensis in The Rain Forests of Golfo Dulce (Allen, 1956), correspond with this new species. Virola calophylloidea has recently been considered synonymous with V. calophylla (e.g. Rodrigues 1980 ; Jaramillo et al. 2004 ; ter Steege et al. 2019 ). However, here, it is treated as a morphologically distinct species. This is due to its smaller leaves, more compact staminate and pistillate inflorescences and infructescences, staminate flowers with the filament column longer than the anthers and smaller fruits (see Table 2 ). Some representative collections of V. calophylloidea include: Brazil. Acre : Rio Jurua & Rio Moa, Serra da Moa, 30 Apr 1971 (♂ fl), P. J. M. Maas et al. P12659 (MO). Amazonas : Rio Urubu , 04 Aug 1979 (♂ fl), C. E. Calderon et al. 2922 (MO); Km 500 on Manaus-Humaita road, 17 Sep 1980 (fr), S. R. Lowrie et al. 54 (MO); Km. 133, Manaus-Itacoatiara Road, 11 Sep 1974 (♂ fl), T. D. Pennington & O. P. Monteiro P22638 (MO); Rio Cuieras, 12 Sep 1973 (♂ fl), G. T. Prance et al. 17790 (MO); Reserva Experimental Station of INPA, 30 Aug 1974 (♂ fl), G. T. Prance et al. 21689 (MO); Rio Javari, Rio Curaca , 8 miles above mouth, 26 Oct 1976 (♀ fl), G. T. Prance et al. 24133 (MO). Para : Km 133, Madeira-Mamore Railway, 15 Sep 1963 (♂ fl), B. Maguire et al. 56666 (MO); Itaituba, Km 60 da estrada Itaituba, 16 Nov 1978 (fr), M. G. da Silva & C. S. Rosario 3775 (MO). Rondonia : Basin of Rio Madeira, 23 Nov 1968 (fr), G. T. Prance et al. 8775 (MO). Specimens examined. Costa Rica. Puntarenas : Golfito, alrededores de la estacion Agujas, 300 m elev., 22 May 2000 (st), L. Acosta et al. 1389 (CR!); Golfito, Piro, 100 m elev., 14 Oct 1991 (st), R. Aguilar 511 (CR!); Golfito, estacion Los Patos, 200 m elev., 02 Sep 1993 (imm fr), R. Aguilar 2224 (CR-2 sheets!, LSU!, MO!); Osa, Bahia Chal, La Parcela, 150 m elev., 12 Dic 1996 (st), R. Aguilar 4735 (CR!, MO!); Peninsula de Osa, Rancho Quemado, sendero a Cerro Brujo, 343 m elev., 30 Jul 2013 (st), R. Aguilar 14519 (CR!); area between Rio Esquinas & Palmar, 60 m elev., 18 Feb 1963 (fr, dupl. in GH), P. H. Allen 6727 (F!*, GH!*); Osa, Sierpe, 1 km antes de la Villa de Banegas, 55 m elev., 14 Oct 2007 (fr), E. Chacon et al. 885 (USJ!); Osa, fila Casa Loma, Aguabuena Sur, 07 Oct 1992 (fr), 50-150 m elev., A. Fernandez 410 (CR!, MO!); Osa, Playa Campanario o San Josecito, 1-10 m elev., 29 Dec 1991 (fl bud), P. Harmon 291 (CR-2 sheets!); Golfito, bosque de los Austriacos, La Gamba, 300 m elev., 09 Jan 1994 (fr), W. Huber & A. Weissenhofer 136 (CR!, LI*); Golfito, near the Tropenstation La Gamba on the fila, 200 m elev., 27 Jan 2002 (fl), H. Huber 3012 (LI-2 sheets!*); Golfito, Jimenez , Piro, no elev., 20 Jan 2012 (fr), J. M. Ley-Lopez 69 (USJ!); Golfito, montana aledana al campo de aterrizaje, 07 Jun 1994 (st), L. J. Poveda 887 (CR!); Osa, 3 km despues de la quebrada Banegas, camino a Rancho Quemado, 200 m elev., 10 Jan 2018 (fr), D. Santamaria & R. Aguilar 9865 (CR!); Peninsula de Osa, Aguabuena, 3.5 km W of Rincon , 350 m elev., 14 Jun 1993 (st), K. Thomsen 746 (CR!); Peninsula de Osa, Aguabuena, 3 km W of Rincon , 130 m elev., 15 Apr 1993 (♂ fl), K. Thomsen 857 (CR!, MO!, NY!*); Peninsula de Osa, Aguabuena, 3 km W of Rincon , 130 m elev., 05 May 1993 (st), K. Thomsen 915 (CR!); Peninsula de Osa, Aguabuena, 3.5 km W of Rincon , 150 m elev., 06 Oct 1994 (fr), K. Thomsen 1049 (CR!); Peninsula de Osa, Aguabuena, 2.5 km W of Rincon , 150 m elev., 10 Mar 1995 (fl), K. Thomsen 1283 (NY!*); Peninsula de Osa, Aguabuena, 2.5 km W of Rincon , 150 m elev., 10 Mar 1995 (♂ fl), K. Thomsen 1284 (NO!, NY!*). San Jose : Tarrazu , del puente de San Marcos 18 km camino hacia Quepos, 1370 m elev., 13 Jan 2006 (fr), B. Hammel et al. 24041 (CR!); Esquipulas, base del Cerro San Isidro, alrededores del rio Naranjo, 400 m elev., 28 Aug 1987 (fr), N. Zamora et al. 1440 (CR!, MO!).