New insights on Bidens herzogii (Coreopsideae, Asteraceae), an endemic species from the Cerrado biogeographic province in Bolivia
Novedades en el conocimiento de Bidens herzogii (Coreopsideae, Asteraceae), una especie endémica de la provincia biogeográfica del Cerrado en Bolivia
Arturo Castro-Castro1, Georgina Vargas-Amado2, José J. Castañeda-Nava3, Mollie Harker1, Fernando Santacruz-Ruvalcaba3 & Aarón Rodríguez2,*
1 Cátedras CONACYT - Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad Durango (CIIDIR-Durango), Instituto Politécnico Nacional.
2 Herbario Luz María Villarreal de Puga (IBUG), Instituto de Botánica, Departamento de Botánica y Zoología, Universidad de Guadalajara. Apartado postal 1-139, Zapopan 45101, Jalisco, México. *Author for correspondence: aaron.rodriguez@cucba.udg.mx ]]>
Abstract
The morphological limits among some Coreopsideae genera in the Asteraceae family are complex. An example is Bidens herzogii, a taxon first described as a member of the genus Cosmos, but recently transferred to Bidens. The species is endemic to Eastern Bolivia and it grows on the Cerrado biogeographic province. Recently collected specimens, analysis of herbarium specimens, and revisions of literature lead us to propose new data on morphological description and a chromosome counts for the species, a tetraploid, where x = 12, 2n = 48. Lastly, we provide data on geographic distribution and niche modeling of B. herzogii to predict areas of endemism in Eastern Bolivia. This area is already known for this pattern of endemism, and the evidence generated can be used to direct conservation efforts.
Key words: Bolivian Chiquitanía, Niche modeling, Western Cerrado.
Resumen
Los límites morfológicos entre algunos géneros de la familia Asteraceae tribu Coropsideae son complejos. Un ejemplo es Bidens herzogii, especie descrita en principio como Cosmos herzogii, pero recientemente transferida al género Bidens. La especie es endémica del este de Bolivia, en la provincia biogeográfica del Cerrado. Colecciones recientes, análisis de ejemplares de herbario y la revisión de literatura, nos llevan a la necesidad dar a conocer nuevos datos sobre la descripción morfológica de B. herzogii y un conteo cromosómico para la especie, un tetraploide, donde x = 12, 2n = 48. Por último, a partir de datos sobre su distribución geográfica y un modelo de su nicho ecológico es posible predecir áreas de endemismo en el este de Bolivia. Esta región del país es reconocida por este patrón y la evidencia aquí generada puede ser útil para dirigir esfuerzos de conservación.
Palabras clave: Cerrado Occidental, Chiquitanía boliviana, Modelación de nicho.
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Introduction
The tribe Coreopsideae, Asteraceae, is a monophyletic lineage with 24 genera and 600 species (Panero & Funk 2002, Panero 2007, Crawford et al. 2009). The tribe has a cosmopolitan distribution, although its greatest diversity is found in the Americas. Two diverse genera of Coreopsideae are Bidens L. and Cosmos Cav. which are frequently confused, and as a consequence several synonymies exist between them (e.g. Hemsley 1881, Sherff 1929, 1932, Melchert 1975, 1990, 2010a-b, Melchert & Turner 1990). A recent case is the proposal of Hind (2013) to transfer Cosmos herzogii Sherff to Bidens. Based on this work and on a recent systematic study of Cosmos (Vargas-Amado et al. 2013; Castro-Castro et al. 2014, Castro-Castro 2015) and field work we support this last decision. Bidens herzogii, the new combination, is endemic to Eastern Bolivia and it grows on the Cerrado or Cerradense Occidental biogeographic provinces (Morrone 2001 and Navarro & Ferreira 2009, respectively). This region is distinguished by its unique flora, singular abiotic characteristics, and several biological endemisms (Suárez 2000, Wood et al. 2011, Pozo et al. 2013, Fig. 1A).
Nevertheless, after a revision of herbarium material and live plants in the field, and confronting our observations with previous analyses of Bidens herzogii (Sherff 1934, Hind 2013), we note important morphological variations and measurement ranges of stems, roots, inflorescences, heads, florets, and achenes, that here we would like to provide. At the same time, we discuss on morphological boundaries between Cosmos and Bidens and the infrageneric taxonomic relationship of B. herzogii based on morphology and the first chromosome count for the species. Finally, based on our biogeographic work, we detect that potential geographical distribution of Bidens herzogii could predict key similar areas for potential conservation and reveal patterns of endemism and species richness in the Bolivian Cerrado.
Methods
Bidens herzogii was collected in the type locality and other sites nearby. Extensive sampling captured much of its morphological, ecological, and geographic variation. Vouchers were deposited at USZ, IBUG and MEXU. The morphological data was complemented with the revision of specimens at BOLV, G, IBUG, MEXU, and USZ (herbarium acronyms following Thiers 2013).
For chromosome counts, mitotic metaphase cells from root tips were observed. The root tips were obtained from three individuals obtained from the type locality and cultivated under greenhouse conditions (see in specimens examined for analyzed material). Root tips were pretreated with 0.002 M 8-hydroxyquinoline for 5 h at 5-10°C. Then, the material was hydrolyzed in 5 N HCl at room temperature for 25 min and washed in distilled water. The root-tips were squashed and stored at -20°C for 3 days. The slides were subsequently dried at room temperature and then stained with 1% acetorcein. Mitotic metaphase figures were photographed with a Zeiss Axiostar microscope and AxioCam ICc1 digital camera equipped with Axiovision 4.8 software.
]]> Geographic information attached to herbarium specimens and the localities obtained from the field work were used for niche modeling, implemented in MaxEnt (Phillips et al. 2006) and following the protocols described by Cruz-Cárdenas et al. (2012). We used 19 climatic variables from WorldClim dataset (Hijmans et al. 2005) and eight occurrence points of Bidens herzogii. There are various regionalization proposals for Bolivia (Olson et al. 2001, Morrone 2004, Flores-Baltazar 2013, Ledezma-Kravarovic 2013). According to Flores-Baltazar (2013), the Chaco and the Chiquitania are two different biogeographic provinces and Bidens herzogii has been collected in both of them. Unfortunately, the author did not offer a digital mask. Alternatively, Morrone (2004) recognized only the Chaco biogeographic province and provided a mask. All points of occurrence are located at the Chaco province (Morrone 2004). In order to define the potential range of B. herzogii, we employed the maximum sensitivity test plus specificity suggested by Liu et al. (2005). According to this criterion, greater probability values represent the potential area of the species. The area obtained was divided into three categories, based on areas of potential distribution with medium, high and very high occurrence probabilities. This procedure was achieved dividing by three the range of probability values of the species (J.L. Villaseñor-Ríos, pers. com., 2013).
Results
Notes on morphological description and chromosome count
Bidens herzogii (Sherff) D.J.N. Hind, Kew Bulletin:68. 2013. Fig. 1.
Suffrutescent herb, (30-)50-130 cm (Fig. 1B), xylopodium 7.5-15 cm long, 3.5-7 cm wide, with rhizome extending horizontally and connecting nearby subterranean branches. Stems erect, terete, glabrous, 0.3-2 cm wide, with marked nodes on more mature branches, internodes 1-2 cm. Petiole 2-5.5 cm long. Leaves opposite, 1-3 pinnatisect, membranaceous, light green, concolorous, glabrous, ovate to deltoid in general outline, (4-)7.5-13.5 cm long, (3.5-)5-7.5 cm wide. Primary segments opposite, entire, deeply and irregularly lobate or serrate, lanceolate to ovate, attenuate, acuminate, (0.7-)1-5.5 cm long, 0.3-1.8 cm wide; margins entire or 1-9 dentate, teeth 1-2 mm (Fig. 1C). Inflorescence corymbiform, (1-)2-5(-9) heads. Peduncles thin, glabrous, 2.5-8(-15) cm long. Capitula radiate, (2.5-)3-4.5 cm wide across extended rays (Fig. 1D). Involucre campanulate, 0.3-0.6 mm wide. Phyllaries biseriate; outer series (8-)14-22, green, foliaceous, (4-)5-7.5 mm long, 0.5-0.8 mm wide, linear, sigmoid, extended or reflexed, glabrous, lustrous, with 1(-3) inconspicuous resiniferous ducts on abaxial face, obtuse; inner series 12-22, scarious, membranaceous, translucent, pale yellow, hyaline margins, with 5-8 fine resiniferous and conspicuous ducts on abaxial face, 8-10 mm long, 2-2.2 mm wide, lanceolate, acute (Fig. 1E). Receptacle flat, convex when dry, palaceous, 2-4 mm diameter. Paleae translucent yellow, 8-10 mm long, 1-2 mm wide, persistent, resembling inner phyllaries. Ray florets 6-12 (frequently deciduous), uniseriate, sterile, yellow (brown when dry), lanceolate limb, obtuse, entire or 2-lobulate, (1.3-)2.3-2.8 cm long, 0.3-0.8(-1) cm wide, with 3-8 conspicuous ribs, glabrous, tube 3 mm long, 0.5 mm wide, glabrous. Disk florets (16-)26-32, hermaphrodite, yellow; corollas tubular, occasionally urceolate in peripheral florets in material from Santiago [Castro-Castro et al. 3701 (USZ, IBUG, MEXU)], 0.8-11 mm long, 1.5-2.2 mm wide, glabrous, 5-lobed; lobes triangular, erect, acute, glabrous, 1.5 mm long, 1 mm wide. Frequently, outer disk florets tend to a ray form, anthers are reduced or absent and gynoecium is normal (Fig. 1E). Anthers 5, brownish yellow, 2.5-3 mm, sagittate, appendices acute; filaments laminar, glabrous. Pollen orange. Style 1.2-1.5 cm, brownish yellow; style branches 1.8-2.1 mm, penicillate, papillose. Achenes tetragonal to flattened, fusiform, falcate, 4 thick ribs alternating with 4 thin ribs, (9-)1.2-1.8 cm long, 1.6-1.8 mm wide, greenish brown to black at maturity, glabrous, muricate; carpopodium annular; pappus awns 2-3, 2-2.2 mm, each awn with 6-8 retrorse barbs, persistent (Fig. 1F). Chromosome number 2n = 48 (Fig. 2).
Specimens examined
]]> BOLIVIA. Santa Cruz. Prov. Chiquitos, NO de Roboré, 18º14'14'S, 59º42'18"W, 1,053 m, 3-May-2008 (fl, fr), Wood et al. 24685 (K, USZ!). Santiago de Chiquitos. Chochis, zone of pass across Chochis range climbing up from Chochis-Matacuzal trail, 18º03'S, 59º34'48"W, 18-March-2005 (fl, fr), Wood et al. 21908 (BOLV!, K, LPB!, USZ!); Cerro Chochis, on the meseta at the summit, 18º07'S, 60º00'W, 1,200 m, 22-February-2006 (fl, fr), Wood 22243 (K, USZ!); Cerca de La Antena, 3-4 km de Santiago de Chiquitos, arriba de San Juanama, 18º20'5'S, 59º07'42"W, 697 m, 9-April-2008 (fl, fr), Wood et al. 24315 (K, USZ!); Camino de Santiago de Chiquitos a Soledad-Aguas Calientes, poco antes de llegar a Soledad, 18º21'S, 59º36'W, 3-December-2003 (fl, fr), Wood et al. 20152 (BOLV!, K, LPB!, USZ!); Serranía de Santiago, camino a La Cueva y a la altura de El Arco, 18º40'S, 59º15'W, 800 m, 13-November-1997 (fl, fr), Mamani & Jardim 1288 (USZ!); SenderoEl Arco-Las Cuevas de Juan Miserandino, Cerro San Miserato, 18º20'54.9"S, 59º33'30"W, 820 m, 12-May-2013 (fl, fr), Castro-Castro et al. 3701 (USZ!, IBUG!, MEXU!; material used for chromosomal counts); Sendero Soledad, camino entre El Arco de Soledad y el Río Soledad, alrededores de las rocas El Búho y La Tortuga, 18º22'll'S, 59º35'16.8'W, 574 m, 13-May-2013 (fl, fr), Castro-Castro et al. 3702 (USZ!, IBUG!, MEXU!); summit of Cerro San Miserate, Chiquitos, 900 m, May-1907 (fl), Herzog 496 (G!).
Potential geographical distribution of Bidens herzogii
Bidens herzogii is endemic to the Cerrado biogeographic province, in Eastern Bolivia. Its geographic range is restricted to the central part of Santa Cruz de la Sierra Department (Fig. 3). It grows on rocky fields with thin alluvial soils accumulated in the rock crevices. The area is dominated by xeric scrubs and were evident Astrocaryum arenarium Barb. Rodr., Cleistocactus samaipatanus (Cárdenas) D.R. Hunt, Deuterocohnia longipetala (Baker) Mez, Echinopsis calochlora K. Schum., Hippeastrum spp., Mimosa auriculata Benth., Paepalanthus chiquitensis Herzog, Pitcairnia chiquitana R. Vásquez & Ibish, Smilax campestris Griseb., Vellozia variabilis Mart. ex Schult. f., and several species of Poaceae (Fig. 1a).
The herbarium vouchers analyzed and the field observations were recorded from the Chiquitos and Cordillera provinces. But the modeling analysis extended its potential distribution to the José Miguel de Velasco and Ñuflo de Chávez provinces (Fig. 3). The area comprised 2,805 km2 with occurrence values of 44.8-62.5%, 62.6-80.2% and 80.3-100%, for median, high and very high probabilities, respectively. The median probability area included 1,693 km2, of which 60% was located at Puerto Suárez and a significant part of San Matías municipalities (Fig. 3B). Meanwhile, the high probability area extended across 882 km2, with 32% of its area located at the Roboré municipality. This area harbored the majority of herbarium records. Finally, the very high probability covered 229 km2 and 8% of them belonged to the Concepción and San Matías municipalities (Fig. 3A).
First, we used the 19 climatic variables of WorldClim to create a potential distribution model of Bidens herzogii. However, only seven climatic variables were employed in the final analysis after the mean test. These variables were isothermality, temperature seasonality, temperature annual range, annual precipitation, precipitation of wettest month, precipitation of wettest quarter and precipitation of warmest quarter (Fig. 4). Thus, only seven climatic variables predicted the presence of Bidens herzogii.
Discussion
Morphological boundaries between Cosmos and Bidens and the infrageneric taxonomic relationship of B. herzogii
The boundaries between Bidens and Cosmos are complex in some cases and their separation requires a combination of characters. A reliable character to separate both genera is the filament indument of the stamens. In Cosmos, the filaments are pubescent whereas these are glabrous in all known taxa of Bidens. Other useful morphological characters identified by Castro-Castro et al. (2014) are indicated in the Table 1.
Many chromosomal changes are common evolutionary processes in Coreopsideae (Crawford et al. 2009, Watanabe 2014). The basic chromosome number in the tribe is x = 12-14, but Crawford et al. (2009) considered x = 16 with an important chromosome reduction to x = 12 in three clades. One clade groups the genera Chrysanthellum Richard, two lineages of Coreopsis L., Glossocardia Cass., Isostigma Less., Henricksonia B.L. Turner and Heterosperma Cav. A second clade includes the genera Fitchia Hook, Narvalina Cass., Oparanthus Sherff, Petrobium R. Br. and Selleophytum Urb. The third clade comprises Bidens, Coreocarpus Benth., two lineages of Coreopsis, Cosmos and Thelesperma Less.
Around 60% of Bidens species, for which the chromosomal numbers are known, have x = 12 or multiples, but deviations from this value exist (x = 10, 11, 17, 18; Watanabe 2014). On this basis, it is possible to hypothesize that x = 12 is the basic number for the genus. A similar scenario occurred in Cosmos, in which both dysploidy and polyploidy has been associated with its evolution and diversification. Melchert (1968) found a correlation between morphological and chromosomal data and identified three main species complexes within the genus. A major evolutionary dichotomy occurred with the ancestor that gave rise to the two perennial complexes. In the suffruticose species of Cosmos sect. Mesinenia Sherff, x = 11 (n = 11, 22, 33). In contrast, all other perennials in Cosmos sect. Discopoda (DC.) Sherff, x = 12 (n = 12, 24, 36). In annual species of Cosmos sect. Cosmos, x = 12 (n = 12, 24).
In Bidens, there also exists a wide chromosome series 2n = 20, 22, 24, 34, 36, 48, 96 (Panero 2007, Watanabe 2014). Bidens herzogii is a tetraploid, as the somatic chromosome number was 2n = 48 (Fig. 2). The chromosomal counts agreed with other data for Bidens species from South America (Solbrig et al. 1972, Powell et al. 1974, Turner et al. 1979, Keil et al. 1988, Grombone-Guaratini et al. 2006, Crawford et al. 2009, Watanabe 2014).
]]> Based on infrageneric classification proposed by de Candolle (1836) and Sherff (1937), Bidens herzogii can be included in Bidens section Psilocarpaea DC. It is the largest section of Bidens, comprises much of the American species, and includes annual and perennial herbs and shrubs, with simple or segmented leaves, discoid or radiate heads, tetragonal and aristate achenes. Sherff (1937) and Kim et al. (1999) argued that this section does not represent a natural lineage and future studies may indicate the advisability of splitting this section into several smaller groups.Potential distribution of Bidens herzogii and its implications for the conservation
The herbarium records and potential projected distribution of Bidens herzogii coincided in the Chiquitanía region, in the plains identified as Occidental Cerradense by Navarro & Ferreira (2009). Navarro (2011) remarked that La Chiquitanía constitutes a natural region in Southeastern Bolivia, and extends into northern Paraguay and Western Brazil at the boundaries of the Amazon River and La Plata River basins. The region is part of the Brazilian Precambric Shield, also known as the "Cratón de Guaporé" (Suarez 2000, Montes de Oca 2001) and it is distinguished by its unique flora, singular abiotic characteristics, and several biological endemism (Suarez 2000, Wood et al. 2011, Pozo et al. 2013).
Conclusions
We propose that the potential geographical distribution of B. herzogii (Figs. 2-3), could predict key areas for others restricted plants and indicate potential areas for conservation. Species distribution models estimates the spatial distributions of species requiring attention, due to its rarity or limited known occurrences. According to Hernández et al. (2006), out of four modeling methods, Maxent was the best in producing useful results with sample sizes as small as 5, 10 and 25 occurrences. The accuracy of models is greater for species with small geographic ranges and limited environmental tolerance.
Our results indicate that reasonable models can be generated for some rare species like Bidens herzogii and it should encourage conservationists to add distribution modeling tools to their research programs.
For example, the Noel Kempff National Park and the Tucavaca Natural Protected Area, in Santa Cruz department (SERNAP 2013, Robinson et al. 2002), could direct their efforts in order to protect new areas or extend their geographic limits, considering the potential distribution of B. herzogii and by modeling the distribution of other associated species restricted to the region based on methods used in our work. This proposal coincides with Pozo et al. (2013) in the identification of conservation hotspots areas in Eastern Bolivia, containing high environmental heterogeneity, high plant diversity and endemism. Finally, we recommend its application for defining conservation priorities in Eastern Bolivia.
Acknowledgments
]]> We are grateful to curators and staff of the following herbaria: B, G, IBUG, JUA, LIL, LP, LPB, MCNS, MEXU, and USZ. The authors thank Laurent Gautier and Venera Fonjallaz, of the Conservatoire et Jardin Botaniques de la Ville de Genève, for providing the type material image of Bidens herzogii. We thank Roxana Ledezma-Vargas, Thamara Chuvirú-Castro, Tatiana Martínez e Iván Linneo-Foronda from the USZ Herbarium for their help during field work of ACC in Bolivia. To Denice Azunta Fernández-Cabello and Osvair Palacios-Torrico, from the Tucavaca Natural Protected Area in Santiago de Chiquitos, Roboré, Bolivia, they are great young field guides; for their support, enthusiasm and discipline, thank you.
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Artículo recibido en: 12 de enero de 2017
Manejado por: Ramiro Pablo López ]]>
Aceptado en: 18 de abril de 2017
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