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Ecología en 52(1): 21-32. Mayo 2017. ISSN 1605-2528.

New insights on herzogii (, ), 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: [email protected] 3 Laboratorio de Cultivo de Tejidos, Departamento de Producción Agrícola, Universidad de Guadalajara. Apartado postal 1-139, Zapopan 45101, Jalisco, México.

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 , 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.

21 A. Castro C., G. Vargas A., J. J. Castañeda N., M. Harker, F. Santacruz R. & A. Rodríguez

Introduction for potential conservation and reveal patterns of endemism and species richness in the The tribe Coreopsideae, Asteraceae, is a Bolivian Cerrado. monophyletic lineage with 24 genera and 600 species (Panero & Funk 2002, Panero Methods 2007, Crawford et al. 2009). The tribe has a cosmopolitan distribution, although its Bidens herzogii was collected in the type greatest diversity is found in the Americas. locality and other sites nearby. Extensive Two diverse genera of Coreopsideae sampling captured much of its morphological, are Bidens L. and Cosmos Cav. which are ecological, and geographic variation. Vouchers frequently confused, and as a consequence were deposited at USZ, IBUG and MEXU. several synonymies exist between them (e.g. The morphological data was complemented Hemsley 1881, Sherff 1929, 1932, Melchert with the revision of specimens at BOLV, G, 1975, 1990, 2010a-b, Melchert & Turner 1990). IBUG, MEXU, and USZ (herbarium acronyms A recent case is the proposal of Hind (2013) following Thiers 2013). to transfer Cosmos herzogii Sherff to Bidens. For chromosome counts, mitotic Based on this work and on a recent systematic metaphase cells from root tips were observed. study of Cosmos (Vargas-Amado et al. 2013; The root tips were obtained from three Castro-Castro et al. 2014, Castro-Castro 2015) individuals obtained from the type locality and cultivated under greenhouse conditions and field work we support this last decision. (see in specimens examined for analyzed Bidens herzogii, the new combination, is material). Root tips were pretreated with 0.002 endemic to Eastern Bolivia and it grows M 8-hydroxyquinoline for 5 h at 5-10°C. Then, on the Cerrado or Cerradense Occidental the material was hydrolyzed in 5 N HCl at biogeographic provinces (Morrone 2001 and room temperature for 25 min and washed in Navarro & Ferreira 2009, respectively). This distilled water. The root-tips were squashed region is distinguished by its unique flora, and stored at -20°C for 3 days. The slides singular abiotic characteristics, and several were subsequently dried at room temperature biological endemisms (Suárez 2000, Wood et and then stained with 1% acetorcein. Mitotic al. 2011, Pozo et al. 2013, Fig. 1A). metaphase figures were photographed with a Nevertheless, after a revision of herbarium Zeiss Axiostar microscope and AxioCam ICc1 material and live in the field, and digital camera equipped with Axiovision 4.8 confronting our observations with previous software. analyses of Bidens herzogii (Sherff 1934, Hind Geographic information attached to 2013), we note important morphological herbarium specimens and the localities variations and measurement ranges of stems, obtained from the field work were used for roots, , heads, florets, and niche modeling, implemented in MaxEnt achenes, that here we would like to provide. At (Phillips et al. 2006) and following the the same time, we discuss on morphological protocols described by Cruz-Cárdenas et al. boundaries between Cosmos and Bidens and (2012). We used 19 climatic variables from the infrageneric taxonomic relationship of B. WorldClim dataset (Hijmans et al. 2005) and herzogii based on morphology and the first eight occurrence points of Bidens herzogii. chromosome count for the species. Finally, There are various regionalization proposals based on our biogeographic work, we detect for Bolivia (Olson et al. 2001, Morrone 2004, that potential geographical distribution of Flores-Baltazar 2013, Ledezma-Kravarovic Bidens herzogii could predict key similar areas 2013). According to Flores-Baltazar (2013),

22 New insights on Bidens herzogii (Coreopsideae, Asteraceae), an endemic species from the Cerrado biogeographic province in Bolivia the Chaco and the are two thin, glabrous, 2.5-8(-15) cm long. Capitula different biogeographic provinces and Bidens radiate, (2.5-)3-4.5 cm wide across extended herzogii has been collected in both of them. rays (Fig. 1D). Involucre campanulate, 0.3- Unfortunately, the author did not offer a 0.6 mm wide. Phyllaries biseriate; outer digital mask. Alternatively, Morrone (2004) series (8-)14-22,­ green, foliaceous, (4-)5-7.5 recognized only the Chaco biogeographic mm long, 0.5-0.8 mm wide, linear, sigmoid, province and provided a mask. All points of extended or reflexed, glabrous, lustrous, occurrence are located at the Chaco province with 1(-3) inconspicuous resiniferous ducts (Morrone 2004). In order to define the on abaxial face, obtuse; inner series 12- potential range of B. herzogii, we employed 22, scarious, membranaceous, translucent, the maximum sensitivity test plus specificity pale yellow, hyaline margins, with 5-8 suggested by Liu et al. (2005). According to this fine resiniferous and conspicuous ducts criterion, greater probability values represent on abaxial face, 8-10 mm long, 2-2.2 mm the potential area of the species. The area wide, lanceolate, acute (Fig. 1E). Receptacle obtained was divided into three categories, flat, convex when dry, palaceous, 2-4 based on areas of potential distribution with mm diameter. Paleae translucent yellow, medium, high and very high occurrence 8-10 mm long, 1-2 mm wide, persistent, probabilities. This procedure was achieved resembling inner phyllaries. Ray florets dividing by three the range of probability 6-12 (frequently deciduous), uniseriate, values of the species (J.L. Villaseñor-Ríos, sterile, yellow (brown when dry), lanceolate pers. com., 2013). limb, obtuse, entire or 2-lobulate, (1.3-)2.3- 2.8 cm long, 0.3-0.8(-1) cm wide, with 3-8 Results conspicuous ribs, glabrous, tube 3 mm long, 0.5 mm wide, glabrous. Disk florets (16-)26- Notes on morphological description and 32, hermaphrodite, yellow; corollas tubular, chromosome count occasionally urceolate in peripheral florets in material from Santiago [Castro-Castro et Bidens herzogii (Sherff) D.J.N. Hind, Kew al. 3701 (USZ, IBUG, MEXU)], 0.8-11 mm Bulletin: 68. 2013. Fig. 1. long, 1.5-2.2 mm wide, glabrous, 5-lobed; Suffrutescent herb, (30-)50-130 cm (Fig. lobes triangular, erect, acute, glabrous, 1.5 1B), xylopodium 7.5-15 cm long, 3.5-7 cm mm long, 1 mm wide. Frequently, outer wide, with rhizome extending horizontally disk florets tend to a ray form, anthers are and connecting nearby subterranean reduced or absent and gynoecium is normal branches. Stems erect, terete, glabrous, 0.3-2 (Fig. 1E). Anthers 5, brownish yellow, 2.5-3 cm wide, with marked nodes on more mature mm, sagittate, appendices acute; filaments branches, internodes 1-2 cm. Petiole 2-5.5 laminar, glabrous. Pollen orange. Style 1.2- cm long. opposite, 1-3 pinnatisect, 1.5 cm, brownish yellow; style branches membranaceous, light green, concolorous, 1.8-2.1 mm, penicillate, papillose. Achenes glabrous, ovate to deltoid in general outline, tetragonal to flattened, fusiform, falcate, 4 (4-)7.5-13.5 cm long, (3.5-)5-7.5 cm wide. thick ribs alternating with 4 thin ribs, (9-)1.2- Primary segments opposite, entire, deeply 1.8 cm long, 1.6-1.8 mm wide, greenish brown and irregularly lobate or serrate, lanceolate to black at maturity, glabrous, muricate; to ovate, attenuate, acuminate, (0.7-)1-5.5 cm carpopodium annular; pappus awns 2-3, long, 0.3-1.8 cm wide; margins entire or 1-9 2-2.2 mm, each awn with 6-8 retrorse barbs, dentate, teeth 1-2 mm (Fig. 1C). persistent (Fig. 1F). Chromosome number 2n corymbiform, (1-)2-5(-9) heads. Peduncles = 48 (Fig. 2).

23 A. Castro C., G. Vargas A., J. J. Castañeda N., M. Harker, F. Santacruz R. & A. Rodríguez

Figure 1. Bidens herzogii. A. Habitat, B. habit, C. variation, D. capitulum, from above, E. capitulum, lateral view and F. fruiting capitulum. Based on Castro-Castro et al., 3701 and 3702 (IBUG, USZ, MEXU).

24 New insights on Bidens herzogii (Coreopsideae, Asteraceae), an endemic species from the Cerrado biogeographic province in Bolivia

El 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, 18º22’11’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. Figure 2. Chromosomes counts of Bidens Its geographic range is restricted to the central herzogii, based on Castro-Castro et al. 3701 part of Department (Fig. (IBUG, USZ, MEXU). A) x = 12, 2n = 48. Bar 3). It grows on rocky fields with thin alluvial = 10 µm. soils accumulated in the rock crevices. The area is dominated by xeric scrubs and were Specimens examined evident Astrocaryum arenarium Barb. Rodr., Cleistocactus samaipatanus (Cárdenas) D.R. BOLIVIA. Santa Cruz. Prov. Chiquitos, NO Hunt, Deuterocohnia longipetala (Baker) Mez, de Roboré, 18º14’14’S, 59º42’18’’W, 1,053 m, Echinopsis calochlora K. Schum., Hippeastrum 3-May-2008 (fl, fr), Wood et al. 24685 (K, USZ!). spp., Mimosa auriculata Benth., Paepalanthus Santiago de Chiquitos. Chochis, zone of chiquitensis Herzog, Pitcairnia chiquitana R. pass across Chochis range climbing up from Vásquez & Ibish, Smilax campestris Griseb., Chochis-Matacuzal trail, 18º03’S, 59º34’48’’W, Vellozia variabilis Mart. ex Schult. f., and 18-March-2005 (fl, fr), Wood et al. 21908 (BOLV!, several species of Poaceae (Fig. 1a). K, LPB!, USZ!); Cerro Chochis, on the meseta The herbarium vouchers analyzed and at the summit, 18º07’S, 60º00’W, 1,200 m, the field observations were recorded from 22-February-2006 (fl, fr), Wood 22243 (K, USZ!); the Chiquitos and Cordillera provinces. But Cerca de La Antena, 3-4 km de Santiago de the modeling analysis extended its potential Chiquitos, arriba de San Juanama, 18º20’5’S, distribution to the José Miguel de Velasco and 59º07’42’’W, 697 m, 9-April-2008 (fl, fr), Wood Ñuflo de Chávez provinces (Fig. 3). The area et al. 24315 (K, USZ!); Camino de Santiago de comprised 2,805 km2 with occurrence values Chiquitos a Soledad-Aguas Calientes, poco of 44.8-62.5%, 62.6-80.2% and 80.3-100%, for antes de llegar a Soledad, 18º21’S, 59º36’W, median, high and very high probabilities, 3-December-2003 (fl, fr), Wood et al. 20152 respectively. The median probability area (BOLV!, K, LPB!, USZ!); Serranía de Santiago, included 1,693 km2, of which 60% was located camino a La Cueva y a la altura de El Arco, at Puerto Suárez and a significant part of San 18º40’S, 59º15’W, 800 m, 13-November-1997 Matías municipalities (Fig. 3B). Meanwhile, (fl, fr), Mamani & Jardim 1288 (USZ!); Sendero the high probability area extended across 882

25 A. Castro C., G. Vargas A., J. J. Castañeda N., M. Harker, F. Santacruz R. & A. Rodríguez km2, with 32% of its area located at the Roboré annual precipitation varies between 1,069-1,201 municipality. This area harbored the majority mm (Fig. 4D-G). According to Navarro (2011), of herbarium records. Finally, the very high these climatic conditions persist throughout probability covered 229 km2 and 8% of them the Chiquitanía region, where the climate is belonged to the Concepción and San Matías markedly seasonal, with a time of intense municipalities (Fig. 3A). rainfall, and mostly humid the rest of the year. First, we used the 19 climatic variables of WorldClim to create a potential distribution Discussion model of Bidens herzogii. However, only seven climatic variables were employed in Morphological boundaries between Cosmos the final analysis after the mean test. These and Bidens and the infrageneric taxonomic variables were isothermality, temperature relationship of B. herzogii seasonality, temperature annual range, annual precipitation, precipitation of wettest The boundaries between Bidens and Cosmos month, precipitation of wettest quarter and are complex in some cases and their separation precipitation of warmest quarter (Fig. 4). requires a combination of characters. A Thus, only seven climatic variables predicted reliable character to separate both genera is the the presence of Bidens herzogii. filament indument of the stamens. In Cosmos, Usually, Bidens herzogii grows on sites with the filaments are pubescent whereas these are media isothermality (67 and 68%, Fig. 4A), some glabrous in all known taxa of Bidens. Other seasonal temperature (Fig. 4B), and relatively useful morphological characters identified by lower temperatures than the rest of Eastern Castro-Castro et al. (2014) are indicated in the Bolivia (18.5°C and 19.4°C, Fig. 4C). In addition, Table 1.

Figure 3. Potential and known geographic distribution of Bidens herzogii in eastern Bolivia.

26 New insights on Bidens herzogii (Coreopsideae, Asteraceae), an endemic species from the Cerrado biogeographic province in Bolivia

Figure 4. Relevant climatic variables predicting the potential distribution of Bidens herzogii in eastern Bolivia. A. Isothermality (in percent), B. temperature seasonality (standard deviation X 100), C. temperature annual range (in °C), D. annual precipitation (in mm), E. precipitation of wettest month (in mm), F. precipitation of wettest quarter (in mm) and G. precipitation of warmest quarter (in mm). The area of potential distribution is shown in blue and herbarium records as black dots.

27 A. Castro C., G. Vargas A., J. J. Castañeda N., M. Harker, F. Santacruz R. & A. Rodríguez

Table 1. Morphological boundaries between the genera Cosmos and Bidens.

Character Cosmos Bidens Habit upright herbs trailing or climbing herbs Stem terete tetrangonal or terete Leaves opposite alternate or opposite Phyllaries glabrous, 5-8(-10) per series, with mostly pubescent or glabrous, 4-22 conspicuous resiniferous ducts on per series, may or may not have the abaxial face inconspicuous resiniferous ducts on the abaxial face Capitulum heterogamous heterogamous or homogamous Ray florets sterile fertile or sterile Stamen filament pubescent glabrous Achenes tetragonal, with a single 3-4-angled or dorsally flattened longitudinal groove on each side with 2-4 grooves on each side Pappus awns retrorsely barbed antrorsely or retrorsely barbed

Many chromosomal changes are common correlation between morphological and evolutionary processes in Coreopsideae chromosomal data and identified three main (Crawford et al. 2009, Watanabe 2014). The species complexes within the genus. A major basic chromosome number in the tribe is x = evolutionary dichotomy occurred with the 12–14, but Crawford et al. (2009) considered ancestor that gave rise to the two perennial x = 16 with an important chromosome complexes. In the suffruticose species of reduction to x = 12 in three clades. One clade Cosmos sect. Mesinenia Sherff, x = 11 (n = 11, groups the genera Richard, 22, 33). In contrast, all other perennials in two lineages of L., Cosmos sect. Discopoda (DC.) Sherff, x = 12 (n Cass., Less., Henricksonia B.L. = 12, 24, 36). In annual species of Cosmos sect. Turner and Cav. A second clade Cosmos, x = 12 (n = 12, 24). includes the genera Hook, Narvalina In Bidens, there also exists a wide Cass., Sherff, R. Br. and chromosome series 2n = 20, 22, 24, 34, Selleophytum Urb. The third clade comprises 36, 48, 96 (Panero 2007, Watanabe 2014). Bidens, Benth., two lineages of Bidens herzogii is a tetraploid, as the somatic Coreopsis, Cosmos and Less. chromosome number was 2n = 48 (Fig. 2). Around 60% of Bidens species, for which The chromosomal counts agreed with other the chromosomal numbers are known, have data for Bidens species from South America x = 12 or multiples, but deviations from this (Solbrig et al. 1972, Powell et al. 1974, Turner et value exist (x = 10, 11, 17, 18; Watanabe 2014). al. 1979, Keil et al. 1988, Grombone-Guaratini On this basis, it is possible to hypothesize et al. 2006, Crawford et al. 2009, Watanabe that x = 12 is the basic number for the genus. 2014). A similar scenario occurred in Cosmos, in Based on infrageneric classification which both dysploidy and polyploidy has proposed by de Candolle (1836) and Sherff been associated with its evolution and (1937), Bidens herzogii can be included in Bidens diversification. Melchert (1968) found a section Psilocarpaea DC. It is the largest section

28 New insights on Bidens herzogii (Coreopsideae, Asteraceae), an endemic species from the Cerrado biogeographic province in Bolivia of Bidens, comprises much of the American Our results indicate that reasonable models species, and includes annual and perennial can be generated for some rare species like herbs and shrubs, with simple or segmented Bidens herzogii and it should encourage leaves, discoid or radiate heads, tetragonal conservationists to add distribution modeling and aristate achenes. Sherff (1937) and Kim tools to their research programs. et al. (1999) argued that this section does not For example, the Noel Kempff National represent a natural lineage and future studies Park and the Tucavaca Natural Protected Area, may indicate the advisability of splitting this in Santa Cruz department (SERNAP 2013, section into several smaller groups. Robinson et al. 2002), could direct their efforts in order to protect new areas or extend their Potential distribution of Bidens herzogii and geographic limits, considering the potential its implications for the conservation distribution of B. herzogii and by modeling the distribution of other associated species The herbarium records and potential projected restricted to the region based on methods distribution of Bidens herzogii coincided in the used in our work. This proposal coincides Chiquitanía region, in the plains identified with Pozo et al. (2013) in the identification of as Occidental Cerradense by Navarro & conservation hotspots areas in Eastern Bolivia, Ferreira (2009). Navarro (2011) remarked that containing high environmental heterogeneity, La Chiquitanía constitutes a natural region high diversity and endemism. Finally, in Southeastern Bolivia, and extends into we recommend its application for defining northern Paraguay and Western Brazil at the conservation priorities in Eastern Bolivia. boundaries of the Amazon River and La Plata River basins. The region is part of the Brazilian Acknowledgments Precambric Shield, also known as the “Cratón de Guaporé” (Suarez 2000, Montes de Oca We are grateful to curators and staff of the 2001) and it is distinguished by its unique following herbaria: B, G, IBUG, JUA, LIL, LP, flora, singular abiotic characteristics, and LPB, MCNS, MEXU, and USZ. The authors several biological endemism (Suarez 2000, thank Laurent Gautier and Venera Fonjallaz, Wood et al. 2011, Pozo et al. 2013). of the Conservatoire et Jardin Botaniques de la Ville de Genève, for providing the type Conclusions material image of Bidens herzogii. We thank Roxana Ledezma-Vargas, Thamara Chuvirú- We propose that the potential geographical Castro, Tatiana Martínez e Iván Linneo- distribution of B. herzogii (Figs. 2-3), could Foronda from the USZ Herbarium for their predict key areas for others restricted plants help during field work of ACC in Bolivia. To and indicate potential areas for conservation. Denice Azunta Fernández-Cabello and Osvair Species distribution models estimates the Palacios-Torrico, from the Tucavaca Natural spatial distributions of species requiring Protected Area in Santiago de Chiquitos, attention, due to its rarity or limited known Roboré, Bolivia, they are great young field occurrences. According to Hernández et guides; for their support, enthusiasm and al. (2006), out of four modeling methods, discipline, thank you. Maxent was the best in producing useful results with sample sizes as small as 5, 10 References and 25 occurrences. The accuracy of models is greater for species with small geographic Castro-Castro, A. 2015. Filogenia y evolución del ranges and limited environmental tolerance. género Cosmos (Asteraceae, Coreopsideae).

29 A. Castro C., G. Vargas A., J. J. Castañeda N., M. Harker, F. Santacruz R. & A. Rodríguez

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30 New insights on Bidens herzogii (Coreopsideae, Asteraceae), an endemic species from the Cerrado biogeographic province in Bolivia

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31 A. Castro C., G. Vargas A., J. J. Castañeda N., M. Harker, F. Santacruz R. & A. Rodríguez

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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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