Eduardo A. Morales1,2,3 Morgan L. Vis4, Erika Fernández5, J. Patrick Kociolek6
1 Herbario Criptogámico, Departamento de Ciencias Exactas e Ingenierias Universidad Católica Boliviana, 2 Patrick Center for Environmental Research, The Academy of Natural Sciences of Philadelphia, 3 Unidad de Limnología y Recursos Acuáticos Renovables, Universidad Mayor de San Simón, 4 Department of Environmental and Plant Biology, 5 Centro de Biodiversidad y Genética, Universidad Mayor de San Simón, 6 Diatom Collection, California Academy of Sciences.
e-mail: morales@acnatsci.org, vis-chia@ohio.edu, erika_fer2003@yahoo.es, pkociolek@calacademy.org.
Abstract
A total of seven epilithic samples were collected from streams along an altitudinal gradient within the Bolivian Cloud Forest region near the capital La Paz. The diatom flora is diverse and no clear altitudinal trends were found. The flora is composed of cosmopolitan species and taxa restricted in distribution to the Andes with the genera Gomphonema, Nitzschia, Encyonopsis, and Encyonema containing the greatest number of species and individuals with higher frequencies in samples. Diatoms from this region are also represented by several alkaliphilous and alkalibiont taxa reflecting the high pH of the streams. General characteristics of the sampled sites as well as a list of taxa and figures of representative taxa are presented herein.
Key words: Diatoms, Bacillariophyta, Taxonomy, Sorata, Bolivia.
Resumen
Un total de siete muestras de epiliton fueron colectadas en ríos dentro de un gradiente altitudinal en el bosque nublado de Bolivia, cerca de la capital La Paz. La flora diatomológica es diversa y no se encontraron patrones altitudinales claros. Tal flora está compuesta por especies cosmopolitas y taxa restringidos a los Andes con los géneros Gomphonema, Nitzschia, Encyonopsis y Encyonema agrupando al mayor número de especies e individuos con mayores frecuencias. La flora está también representada por varios taxa alcalifilos y alcalibiontes, reflejando los altos valores de pH de los ríos. Las características de los sitios muestreados, así como una lista de taxa y figuras representativas se presentan en este trabajo.
Palabras clave: Diatomeas, Bacillariophyta, Taxonomía, Sorata, Bolivia.
Bolivian diatoms have been poorly studied and a review of the literature (in preparation) shows that most research has been restricted to the Altiplano. Only a fraction of this literature is taxonomic in nature, which hinders the potential use of diatoms for bioindication. Only a few articles have focused on the diatoms from the Bolivian Cloud Forest [21] [28], which are insufficient to cover this extensive ecosystem.
The South American Cloud Forest (or Yungas) is one of the most biologically diverse ecosystems in South America [5] [23] located between 13°-17°S and 69°-63°W and running along the Eastern Cordillera of the Andes in Bolivia and Peru, between the high Puna or Altiplano and the Amazonian lowlands. In Bolivia, the Yungas has a wide altitudinal range (200-3500 m), and a wide range in temperature (annual means: 7°-30°C) and humidity (800-7000 mm per year). The geology of the Yungas is also varied, composed of four different geological formations [23], resulting in a mixture of landscapes with great influence on the vegetation and fauna of the region. Navarro & Maldonado [23] state that the Yungas is dominated by riverine systems with few lakes. First order streams with fast flowing waters of varied chemical composition predominate at higher altitudes while there is a predominance of second and third order streams with increased load of particulates at lower elevations.
Biologically, the diversity of plants and certain groups of animals such as birds, mammals and amphibians in the Yungas is the best documented [3] [22] [24] and shows high endemism in these groups e.g., Birds [1], Ferns [6] [7]. Within the algae, Thérézien [31] reported 243 soft algae taxa from a few samples collected in a small region of the Yungas, 8 of them being taxa new to science. McClintic et al. [15] studied 13 samples collected from different sites and reported more than 40 taxa of soft-bodied algae, of which 17 were new records for Bolivia. A study of the diatoms present in 6 of these 13 samples showed that about a quarter of the species are not found in any bibliographical reference for South America or similar regions of the world [21].
The current paper presents a taxonomic assessment of the periphytic diatom flora in seven streams located in Sorata, Province of Larecaja, Department of La Paz and it constitutes a preliminary contribution before the initiation of a larger sampling project throughout the Yungas region.
2 Materials and Methods
2.1 Study area
Collection of samples took place in the vicinity of Sorata, about 100 km from the capital La Paz. Seven streams were sampled from an altitudinal range of ca. 2 600-4 060 m. Coordinates and physico-chemical characteristics of each sampling point are presented in Table 1 (samples 27-33) in McClintic et al. [15]. Four of the streams fell within the altitudinal range given for the Yungas by Navarro & Maldonado [23], while the remaining three correspond to the elevation usually given for the Puna. Despite the altitude difference there are no clear patterns in the physical and chemical characteristics of the streams, except for specific conductance which is lower in the higher streams [15].
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2.2 Methods
At each site, five rocks were randomly selected and scraped with a stiff toothbrush. Scraped material from the rocks was rinsed with stream water, collected as a composite sample, and preserved with 2.5% CaCO3-buffered glutaraldehyde. Data for the first two samples (27 and 28) was presented in [21] and are pooled here in order to provide a more complete list of diatoms.
For light microscopy (LM) analysis, a 10 ml periphyton subsample was extracted and cleaned using 30% H2O2 and concentrated HNO3 [30]. Cleaned samples were suspended in glass-distilled water and air-dried. Dried samples were mounted on glass slides using NAPHRAX®. A Nikon Microphot-FXA microscope equipped with DIC was used to identify and measure diatoms at a magnification of 1 250X. A Spot Insight color digital camera was used to capture images of selected specimens. Identification of specimens present in two preparations from each sample was performed to the lowest taxonomic level possible using pertinent literature [14] [16] [17] [18] [27].
For scanning electron microscopy (SEM) studies, aliquots of clean material were air dried onto 15 X 15 cm pieces of aluminum foil. Smaller pieces were trimmed and mounted on aluminum stubs with double-sided tape. The stubs were coated with gold-palladium using a Polaron Sputter Coater for ca. 1 min at 1.8 kV. A Leo-Zeiss 982-DSM electron microscope was used for SEM analyses. LM and SEM digital images were directly captured into a computer file and plates were assembled using Adobe Photoshop v. 7.0.
]]> 3 Results and DiscussionA list of all taxa encountered is presented in Table 1. In total, 190 infrageneric taxa were identified. Of these, 53 entities could not be determined based on the literature for the region or from other parts of the world [8] [9] [10] [11]. Many of these entities probably represent taxa new to science, but none were sufficiently abundant to permit detailed studies. The majority of the undetermined species belonged to Gomphonema (20%), Nitzschia (16%), Encyonopsis (9%), and Encyonema (6%). These four genera were also the most common in samples. Navicula taxa accounted for 9% of the undetermined species, due to the inclusion of small unknowns whose features were not clear in LM and may be placed in Adlafia, Eolimna and Mayamaea after thorough SEM analysis.
The streams were clear, small (width 0.85-8.3 m), and shallow (max. depth 12-40 cm). The smaller streams located at higher altitudes had a periphytic flora, which is characteristic of montane regions worldwide with cosmopolitan taxa, such as Encyonema minutum (Hilse) Mann, Hannaea arcus (Ehrenberg) Patrick and Tabellaria flocculosa (Roth) Kützing. Stream water specific conductance was generally low (20-210 µS/cm), with higher values potentially representing more human activity. In streams located at lower elevations, cosmopolitan taxa characteristic of more elevated trophic conditions were present (e.g., Encyonema silesiacum (Bleisch) Mann, Melosira varians Agardh, Reimeria sinuata (Gregory) Kociolek et Stoermer, Rhoicosphenia abbreviata (Agardh) Lange-Bertalot). The stream water pH was alkaline (7.4-8.6) with no clear altitudinal trend. Alkaliphilous (occurring at pH > 7 [32]) taxa were present: Achnanthidium exiguum var. heterovalvum (Krasske) Czarnecki, Frustulia vulgaris (Thwaites) De Toni, and Planothidium lanceolatum (Brébisson ex Kützing) Lange-Bertalot. In addition, several alkalibionts (living exclusively at pH > 7) were collected such as Epithemia adnata (Kützing) Brébisson, Pleurosira laevis (Ehrenberg) Compère, Stephanodiscus cf. minutulus (Kützing) Cleve et Möller. A few taxa, reported only from the Andes (possible endemics), were present in the Sorata flora as follows: Encyonema jemtlandicum var. venezolanum Krammer, Gomphonema punae Lange-Bertalot et Rumrich and Staurosira laucensis var. vulpina Lange-Bertalot et Rumrich, a species herein transferred to Pseudostaurosira (see later).
In general, the streams at higher altitudes (streams 29 and 30) harbored more diverse floras (81 and 78 taxa, respectively) and lower streams (No. 27, 28 and 31) contained fewer taxa (range 37-45 taxa) (Table 1). Stream 33 is located at higher elevation, but contained fewer taxa (21). Water temperature (16°C) and pH (8.4) were higher in stream 33 than in streams of similar altitude, while the current velocity (6.1 cm/sec) and conductivity (20 µS/cm) were lower. These conditions might favor the development of other groups of algae since McClintic et al. [15] reported high numbers of soft-bodied macro- and microalgae in this stream. In contrast, stream 32 was lower in elevation, but contained high diatom diversity (61 taxa). This stream was the shallowest (12 cm) of all streams sampled and had the fastest current velocity (52.6 cm/sec). Apart from these two factors, the stream appears similar in conditions to the other lower altitude streams and, thus, it is difficult to pinpoint the reason for its high diversity. For this same stream, McClintic et al. [15] report only three species of macroalgae.
Taxonomic section
The taxa listed in Table 1 represent the finest level of taxonomic resolution we can provide to date. Several of these are represented in Figures 1-68. Of interest is the presence of taxa whose specific epithets cannot yet be determined, and may represent species new to science. The identity and distribution of these potentially new taxa, in addition to a broader perspective on the diatoms from lotic systems throughout the Bolivian Yungas region, will be the focus of future collaborative research, funded in part by the California Academy of Sciences.
Figure 1-43: LM images of diatoms from Sorata. 1. Orthoseira roseana. 2. Melosira varians. 3. Stephanodiscus cf. minutulus. 4. Diatoma moniliformis. 5. Diatoma hyemalis. 6-7. Frankophila similioides. 8. Staurosirella leptostauron. 9. Pseudostaurosira laucensis var. vulpina. 10-11. Tabellaria ventricosa. 12-13. Tabellaria flocculosa. 14-15. Achnanthidium modestiforme. 16-17. Achnanthidium minutissimum var. jackii. 18-19. Eucocconeis quadratarea. 20. Psammothidium subatomoides. 21-22. Psammothidium grischunum. 23. Eunotia tecta. 24. Eunotia boreoalpina. 25-26. Eunotia tenella. 27. Eunotia paludosa. 28. Mayamaea atomus var. permitis. 29. Mayamaea cf. atomus var. alcimonica. 30. Adlafia minuscula. 32. Adlafia suchlandtii. 32. Cavinula pseudoscutiformis. 33. Brachysira lehmanniae. 34. Brachysira neoexilis. 35. Kobayasiella cf. parasubtilissima. 36. Diploneis kahlii. 37-38. Encyonopsis cf. krammerioides. 39. Encyonopsis cf. krammeri. 40. Gomphonema exilissimum. 41. Gomphonema parvulum. 42. Gomphonema punae. 43. Gomphonema micropus.
Figures 44-62. LM images of diatoms from Sorata. 44. Navicula angusta. 45. Navicula trivialis. 46. Navicula rhynchocephala. 47. Navicula arkona. 48. Navicula libonensis. 49. Navicula cryptocephala. 50. Navicula cf. lundii. 51. Navicula reichardtiana. 52. Caloneis molaris. 53. Caloneis hendeyi. 54. Pinnularia divergens var. linearis. 55. Pinnularia obscura. 56-57. Chamaepinnularia soehrensis var. hassiaca. 58. Chamaepinnularia evanida. 59. Cymbella excisa. 60. Encyonema neogracile. 61. Encyonema schneideri. 62. Cymbella peraspera.
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Figures 63-68. SEM images of diatoms from Sorata. 63. Adlafia minuscula. 64. Navicula arkona. This taxon has been misidentified in Morales & Vis [21] as Navicula capitatoradiata (Figs 103, 104, and 122). 65. Neidium longiceps. 66. Pinnularia obscura. 67. Gomphonema micropus. 68. Surirella angusta.
Presence of one taxon in our samples requires a nomenclatural transfer. We present:
Pseudostaurosira laucensis var. vulpina (Lange-Bertalot et Rumrich) Morales comb. nov. (Fig. 9).
Basionym: Staurosira laucensis var. vulpina Lange-Bertalot et Rumrich in Rumrich et al., 2000, Diatoms of the Andes from Venezuela to Patagonia/Tierra del Fuego, Iconographia Diatomologica 9, p. 223-224, Plate 10, Figs 1-11.
Morales & Vis [21] presented a new combination for Staurosira laucensis Lange-Bertalot et Rumrich within the genus Pseudostaurosira Williams et Round [33] based on the resemblance of this taxon with other species included in the latter genus. The combination presented herein is a follow up to that work. Based on the discussion presented by Morales & Vis [21], several species recently described and transferred by Lange-Bertalot and collaborators within Staurosira Ehrenberg must be moved into other genera. This is because the concept of Staurosira handled by Lange-Bertalot is untenable and does not comply with extensive studies presented by several subsequent authors regarding the distinctiveness of genera erected and resurrected by Williams & Round [33] to better delimit the formerly widely circumscribed genus Fragilaria Lyngbye ([4] [13] [19] [20], among others).
4 Conclusion
The diatom flora from Sorata, Bolivia is diverse and comprises a variety of cosmopolitan and geographically restricted diatoms with many species adapted to alkaline habitats. This is in agreement with two previous studies showing high diversity for different localities within the Yungas [21] [28]. Many of the diatoms observed in collected samples could be new, but their description should be postponed until additional data are collected.
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