Avicennia bicolor Standl., J. Wash. Acad. Sci. 13: 354. 1923. TYPE .— PANAMA : Coclé

Daniel, Thomas F., 2016, Avicennia (Acanthaceae: Avicennioideae) in North America and Mesoamerica, Proceedings of the California Academy of Sciences 63 (5), pp. 163-189 : 167-171

1. Avicennia bicolor Standl., J. Wash. Acad. Sci. 13: 354. 1923. TYPE.— PANAMA: Coclé : Aguadulce, outskirts of tidal belt, 5 XII 1911, H. Pittier 4968 (holotype: US!; isotypes: F-image!, K-image!, BM! NY! P! US!) .

Figures 1A–C, 2 , 3D .

Shrubs to 3 m tall or trees to 10 (–23) m tall. Young stems of reproductive shoots glabrous (trichomes sometimes persisting around leaf scars, but internodes glabrous). Leaves petiolate, blades ovate to elliptic to broadly elliptic (to obovate), 62–175 mm long, 31–86 mm wide, length:width = 1.2–2.6, (emarginate to) rounded to subacute at apex, rounded to acute to subattenuate at base, surfaces often conspicuously discolorous (abaxial surface lighter), punctate-pitted (sometimes inconspicuously so abaxially), adaxial surface lacking trichomes, abaxial surface covered with a dense scurfy layer that sometimes includes longer ± appressed eglandular trichomes. Inflorescence of axillary (from distalmost leaves) and terminal pedunculate panicles of elongate spikes, panicles ± open, to 115 mm long (including peduncle and excluding corollas) and to 120 mm wide, peduncles 25–40 mm long, glabrous or distally becoming pubescent like branches and rachises, panicle branches subtended by triangular-concave inflorescence bracts (sometimes caducous) 1–3 mm long, pubescent like rachises, fertile portion of spike 12–35 mm long, rachises clearly visible, internodes near midspike 3.5–7 (–9) mm long, densely pubescent with minute (˂ 0.05 mm long) glandular trichomes and with antrorse (to flexuose) eglandular trichomes to 0.1 mm long. Bracts triangular-ovate to subcircular, 1–2. 3 mm long, abaxially pubescent like rachis. Bracteoles similar to bracts. Flowers mostly 8–10 per spike (but up to 22 per spike). Calyx 2–4 mm long, lobes broadly ovate to subcircular, abaxially pubescent like rachis. Corollas 4. 5–7 mm long, internally white to cream, externally glabrous (proximal 2/3 of tube) and densely pubescent with appressed eglandular trichomes to 0.2 mm long (distal 1/3 of tube and limb), tube 2– 2.5 mm long, limb ± 2-labiate with 4–5 lobes, upper lip apically 2-parted (with division up to 2 mm long) and/or wider than lobes of lower lip, all lobes oblong to obovate, glabrous internally, 3–4. 5 mm long. Stamens 4, inserted at midpoint or in proximal half of corolla tube, 2 exserted from mouth of corolla tube and 2 included in or only partially exserted from corolla tube, oriented in pairs near upper lip of corolla with thecae opening toward lower lip, 2– 2.5 mm long, filaments 1.5– 2 mm long, anthers presented at 2 heights, thecae 0.3– 0.6 mm long; pollen suboblate to oblate spheroidal, polar diameter ( P) 19–22 µm, equatorial diameter ( E) 19–24 µm, P: E = 0.86–0.92. Style not evident, stigma lobes 0.2– 0.4 mm long. Fruit greenish yellow, black when dry, ovoid to ellipsoid, 15–29 mm long, 7–17 mm wide, ± sparsely pubescent with antrorsely appressed eglandular trichomes to 1 mm long, these sometimes more or only evident distally on mature fruits.

PHENOLOGY.— Flowering: September–May; fruiting: February–August.

DISTRIBUTION AND HABITATS.— Pacific coast of southern Mexico (Chiapas, ca. lat. 16°02ʹ26ʺN) , Central America , to southern Panama (Los Santos and Darién, ca. lat. 7.98°N; Fig. 2 ) ; plants occur along and near shorelines in coastal mangrove swamps (mangals) and salt marshes at elevations at or near sea level. In addition to the provinces and departments of Central American nations from which specimens have been examined (noted below), this species potentially also occurs or occurred in the following Pacific coastal political units: Guatemala (Escuintla, Jutiapa, Retalhuleu, San Marcos, Santa Rosa, Suchitepequez) , El Salvador (La Libertad, La Paz , La Unión, San Miguel, San Vicente, Sonsonate, Usulután) , Nicaragua (Carazo, Managua) , and Panama (Chiriquí, Veraguas) . Gibson (1970) included Avicennia bicolor Standl. in her account of the Guatemalan taxa because of its expected occurrence in the country. Although it undoubtedly occurred or still occurs there, the species has yet to be collected in Guatemala .

The southernmost occurrence of Avicennia bicolor has been attributed to the Pacific coast of Colombia (e.g., Sanders 1997; Duke 2010; Aymard 2015). The sole collection cited by Aymard (2015; Forero & Gentry 794 at COL) and another Colombian collection identified as this species (Gentry & Juncosa 41115 at COL), both appear to pertain to A. germinans based on images of these collections supplied by COL. Unless other collections that conform to A. bicolor have been made in Colombia, the southern extent of this species appears to be in Panama at ca. 7.98°N, on both sides of the Gulf of Panama (i.e., in the provinces of Los Santos [Dwyer 5079 A] and Darién [Duke 5488]).

LOCAL NAMES.— “Madre sal” (DeRiemer s.n.); “madresal prieto” (Santamaría D. & Romero B. 1a); “palo de sal” (Sediles 457); “palo de sal hoja ancha” (Sediles 455, 460).

CONSERVATION STATUS.— The extent of occurrence ( EOO) of Avicennia bicolor is 262,479 km 2, although a major portion of that area consists of open ocean and inhospitable upland habitats. The species has been assessed as VU (vulnerable) by the IUCN (Duke 2010) based on a documented continuing decline in population under criterion A.

DISCUSSION.— This species is readily recognized by the combination of its glabrous young stems, relatively remote dichasia in the inflorescence ( Fig. 3C ), bilaterally symmetric flowers with internally glabrous corolla lobes, and black fruits (when dry; Fig. 3D ).

The Mexican occurrence of this species has sometimes been overlooked (e.g., Breedlove 1986; Spalding et al. 1997) or minimized (e.g., treated as a synonym of A. germinans for practical purposes; López P. and Ezcurra 2002). Throughout its distributional range it often grows with A. germinans (e.g., Pittier 4968, the type, grows with Pitier 4969, a collection of A. germinans from the same locale). Rabinowitz (1978) noted that where these species are sympatric there is apparently no zonation between them. Like those of A. germinans , flowers of A. bicolor have been noted to be fragrant (e.g., Knapp 1244). Corollas are usually described by collectors as white to cream; they are sometimes noted to have a yellow throat (like A. germinans ; e.g., Borg and Schöenenberger 2011). Williams 78 from Panama shows exceptionally long and floriferous inflorescences with the fertile portion of spikes to 65 mm long and with up to 22 flowers (vs. usually 4–8) per spike.

Tomlinson (1986) treated A. tonduzii as a synonym of A. bicolor , and others have followed his influential taxonomic account (e.g., Aymard 2015). In his key to species of Avicennia and description of A. bicolor, Tomlinson indicated that corollas of this species were conspicuously pubescent within (as they are on the type of A. tonduzii , but not on the type of A. bicolor ). Distinctions, if any, between A. tonduzii and A. germinans are not readily apparent, and others have treated these names as synonymous. Additional information about A. tonduzii is provided below under A. germinans .

ADDITIONAL SPECIMENS EXAMINED.— COSTA RICA. Guanacaste: Nandayura, Península de Nicoya , Playa Bejuco, 09°49ʹ56ʺN, 085°20ʹ34ʺW, A. Fernández 1762 ( MO); Abangares, Cuenca del Abangares, San Buenaventura , 10°10ʹ29.8253ʺN, 085°09ʹ31.4524ʺW, L. González & A . Garita 3909 ( MO); Tamarindo , Playa Tamarindo, 10°18ʹN, 085°51ʹW, W. Haber & W . Zuchowski 8961 ( F, MO); Port Parker , J. Howell 10242 ( CAS); Refugio Silv. Tamarindo, Estero Tamarindo, Santa Cruz , 10°19ʹ40ʺN, 85°49ʹ20ʺW, Q. Jiménez 859 ( K, MO); P. N . Santa Rosa, Cantón de La Cruz, Península de Santa Elena , Estero Grande, 10°54ʹ59ʺN, 085°47ʹ03ʺW, J. Morales 4142 ( F, MO); P. N . Santa Rosa, Playa Naranjo, 10°47ʹ53ʺN, 085°40ʹ44ʺW, J. Morales et al. 1262 ( F); Puerto Jesús, R. Pohl & G . Davidse 10588 A ( F, MO, US) ; Cantón La Cruz , P. N . Santa Rosa, Peninsula de Santa Elena , Murciélago, 10°55ʹ20ʺN, 85°44ʹ15ʺW, F. Quesada 84 ( K, MO); P. N . Santa Rosa, Playa Naranjo, N. Zamora et al. 1140 ( F, MO) . Puntarenas: Golfo de Nicoya Externo , Isla San Lucas, Punta Cañón, J. Morales & D. Santamaria 12387 ( MO); Garabito, Cuenca del Jesús María, Garabito , alrededores de Playa Punta Loros, 09°51ʹ26.3900ʺN, 084°41ʹ29.8110ʺW, A. Rodríguez & V . Ramírez 6688 ( MO) .

EL SALVADOR. Ahuachapán: without locale, Padilla 333 ( US); Las Salinas, K. DeRiemer 1625 ( US), 1626 ( US); Las Chacaras, en La Barra de Santiago, K. DeRiemer s.n. ( US).

HONDURAS. Choluteca: Playas de Cedeño, F. Padilla 101 ( BM). Valle: Puerto Soto, 12 km from El Tular, A. Molina R. 21457 ( BM, NY, UC, US); Puerto Soto, 15 km WSW de San Lorenzo, C. Nelson 1323 ( MO).

MEXICO. Chiapas: Paderón, Tonala, E. Matuda 16353 ( US) ; Mpio. Pijijiápan, Estero San José , 15°43ʹ39.50ʺN, 093°29ʹ50.20ʺW, S. Santamaría-Damián & E . Romero-Berny 1a ( MEXU), 1b ( MEXU) .

NICARAGUA. Chinandega: Mpio. El Viejo, Reserva Natural de Cosigüina, San Remigio entre El Congo y Bella Vista, 13°01ʹN, 097°35ʹW, I. Coronado G. & R. Rueda 3626 ( MEXU, MO); Mpio. Puerto Morazán, de Morazán hasta 5 km en dirección Ttonalá, 12°49ʹN, 087°09ʹW, R. Rueda et al. 17322 ( MEXU, MO). León: Isla del Venado, 3.3 km de Las Peñitas, Barrera 8 ( CAS); Las Peñitas, Isla Juan Venado, 12°13ʹN, 086°53ʹW, I. Coronado G. & R. Rueda 4943 ( MO); Las Peñitas, Isla Juan Venado, 12°17ʹN, 086°53ʹW, I. Coronado G. et al. 6979 ( MO); Isla del Venado, 8.2 km de Las Peñitas, 60 m del Estero Las Peñitas, Sediles 445 ( NY), 456 ( NY); 3.3 km de Las Peñitas, Isla del Venado, Sediles 454 ( MO), 459 ( MO), 461 ( CAS); 3 km de Las Peñitas, en la Isla del Venado, Sediles 455 ( F), 460 ( K); 8.1 km de Las Peñitas, en la Isla del Venado, 60 m del Estero Las Peñitas, Sediles 457 ( P); 8.3 km del Las Peñitas, en la Isla del Venado, 80 m del Estero Las Peñitas, Sediles 458 ( US). Rivas: “Marsella,” 11°16–17ʹN, 85°52–53ʹW, M. Araquistain 3828 ( MO, P); San Juan del Sur, entre Las Playas de Marsella y Rivas, 11°17ʹN, 085°54ʹW, R. Rueda et al. 1435 ( MO).

PANAMA. Coclé: ca. 2 km del Puerto, camino entre el puerto de Aguadulce hasta el pueblo, M. Correa A. 4314 ( MO); Isla del Pozo, salinas of Río Estero Salado, 08°11ʹN, 080°30ʹW, S. Knapp et al. 3401 ( MEXU, MO); below Aguadulce, E. Tyson 7262 ( FSU, MO). Darién: ca. 10 mi S of El Real on Río Pirre, J. Duke 5488 ( MO). Herrera: Cienega El Mangle, NE of Paris, S. McDaniel 8020 ( FSU, MO). Los Santos: Monagre Beach, J. Dwyer 5079 A ( MO). Panamá: Isla Casaya, J. Duke 10372 ( MO); San José Island, ca. 55 mi SSE of Balboa, Playa Grande, I. Johnston 1259 ( DUKE, MO, P, US); Porto Posada, R. Williams 78 ( NY). Panamá Oeste: Punta Chame, W. D’Arcy 10241 ( MO); Punta Chame, 10–15 mi from Pan American Hwy., 08°40ʹN, 079°45ʹW, S. Knapp 1244 ( MEXU, MO).

Figures

FIGURE 2. Map showing distribution of Avicennia spp. in North America and Mesoamerica. The generalized distribution of A. germinans is shown. The distribution of A. germinans in Cuba and other West Indian islands is not shown.

FIGURE 3. Avicennia spp. A. Flower of A. germinans in Florida (photo by Bob Peterson, cropped, creative commons license, <https://www.flickr.com/photos/pondapple/7270558948/in/photostream>). B Flower of A. marina subsp. australasica in Australia (photo by M. Fagg, cropped, source: Australian National Botanic Gardens at <http://www.anbg. gov.au/photo>). C. Inflorescence of A. biflora (Sediles 461, CAS). D. Fruits of A. bicolor (top; Barrera 8, CAS), A. germinans showing dehiscence (middle; Ferris 5396, DS), and A. marina subsp. australasica (bottom; Nickerson 6445a from New Zealand, CAS).