Plant communities on the islands of two Altiplanic salt lakes in the Andean region of Bolivia

This paper reports a quantitative survey of the composition, diversity and structure of the plant communities on six islands of Uyuni and Coipasa salt lakes (Bolivia). Plant communities on each island were examined via the use of 10 transects, along which species richness and abundance were recorded. Seventy-one species were found in total, representing pteridophytes (6%), gymnosperms (1%), monocotyledons (14%) and dicotyledons (79%). About 21% of the species were endemic or faced some degree of threat. The calculation of Shannon-Wiener α-diversity indices and comparisons of community structure revealed similarities between the islands. Indeed these analyses suggest the existence of a single floral assemblage; however, small differences in the plant communities were visually identified during fieldwork. These islands are home to a considerable subset of the Altiplano’s flora and appear to have been little disturbed. They should therefore be the subject of surveillance/conservation programs.


INTRODUCTION
The Altiplano is a high intermontane plateau (4,000 m above sea level) surrounded by the Western (Cordillera Occidental) and Eastern (Cordillera Oriental) branches of the Central Andes in South America (Richter et al. 1992).It encompasses the endorrheic Basin of the Bolivian Altiplano, which was formed by Pleistocene lakes that dried out due to evaporation and tributaries reduction.This process left the present day Titicaca and Poopó lakes, the Uyuni, Coipasa and Empexa salt lakes, several rivers, and borate deposits (Clapperton 1983(Clapperton , 1993)).
The Uyuni and Coipasa salt lakes have the largest salt crusts of the entire Andean region (Richter et al. 1992).
Over the extensive area they occupy, ground elevations are isolated from the adjacent ranges by salt crust, saline soils, and water.The small size and difficulty in accessing these "islands" have prevented human settlement, agriculture, and animal husbandry.The economic potential of the salt lakes, however, has led to government policies that promote resource exploitation and tourism.Along with poor land planning, water contamination, deforestation, and grazing, these policies have led to wider ecosystem deterioration in the region (Luque 2011;Machaca 2011;Flores 2011).
In recent years, comprehensive accounts of the Altiplano's flora have been published, but virtually no studies have been made on the ecosystems sheltered by the types of island described above.A few descriptions (Navarro and Maldonado 2002;Navarro and Ferreira 2004;Navarro 2011) assume these islands to have floral assemblages and plant communities that are no different of the vegetation in surrounding areas, but most studies have simply neglected them.
Despite the economic interest aroused by these salt lakes, the biodiversity of their islands has never been systematically described.The present work is the first to examine the plant communities on six islands in the Uyuni and Coipasa salt lakes.The results help show the importance of these islands in terms of the region's biodiversity, and provide a baseline for future studies.

Study site
The Uyuni salt lake is the largest lithium brine source in the world (10,582 km 2 ), while that of Coipasa is the second largest (2,218 km 2 ) within the Andean region (Richter et al. 1992;Montes de Oca 1997).Both are located in the southwest of the Bolivian Altiplano: Uyuni salt lake is located between 19°36′ S and 20°42′ S,  Rafiqpoor et al. 2008).The stress-tolerant vegetation is characterised by small pastures, resinous bushes, cacti, and in some areas Polylepis trees (Ibisch et al. 2008).

Lists of species
Interlayered sedimentary (Cordillera Oriental) and volcanic rocks (Cordillera Occidental) rise within these salt lakes to form islands of different size and altitude.For the present work, four islands of the Uyuni and two of the Coipasa salt lake (Figure 2) were chosen on the basis of their reaching a minimum altitude of 110 m above the level of the surrounding lake.This and between 066°55′ W and 068°16′ W at 3,660 m above sea level; Coipasa salt lake is located between 19°08′ S and 19°37′ S, and between 067°51′ W and 068°28′ W at 3,657 m above sea level (Figure 1).The area belongs to the mid-south of the Altiplanic Biogeografic Province (Navarro and Maldonado 2002); this has the lowest precipitation of the region (170 mm per year), a wide range of temperature (ranging from -30°C at night to 15°C during the day), intense solar radiation, strong winds, and saline soils (Ballivián and Risacher 1981; allowed their plant communities to be assessed along an altitudinal gradient.

Data collection and analysis
At the end of the wet season of 2011 (March to May), 10 transects of 60 m × 2 m (modified from Villarreal et al. 2006) were laid on each island in order to record the vegetation present.The total area sampled per island was 1,200 m 2 .Three transects were set up on the edge of each island (i.e., adjacent to the salt lake), five on the mountainsides, and two on the summit area.The required size, number and altitudinal distribution of the transects was established based on preliminary fieldwork and analyses (rarefaction curves).Plant species were collected for taxonomic examination.Species abundance was recorded by direct counting along the transects.
All specimens collected were processed and identified following conventional herbarium methods (Arrázola and Mercado 2004), and deposited at the Herbario Forestal Nacional Martín Cárdenas (BOLV).The habit (annual herb, perennial herb, shrub, or cactus) of each species was determined, along with its International Union for Conservation of Nature (IUCN) Red List Species richness (number of species) and the Shannon-Wiener α-diversity index (Magurran 1989) were calculated for each island.The vegetation on different islands was compared via Kruskal-Wallis tests and Sorensen β-diversity (Bray-Curtis) indices (Herrera 2000).Comparisons of species abundance among transects were also performed (Kruskal-Wallis tests) to identify changes along the altitudinal gradient of each island.Finally, the quantitative structure of the vegetation was described based on plant density.

RESULTS
Seventy-one species were recorded (Table 1) distributed across 26 families and 58 genera; pteridophytes (6%), gymnosperms (1%), mono cotyledons (14%), and dicotyledons (79%) were all represented.The families Asteraceae (19 species), Poaceae (7 species) and Cactaceae (5 species) were the most diverse, and together accounted for 44% of the species richness.Forty-nine genera were represented by a single species, the remaining nine by two or three species.Nine of the species recorded were identified as endemic to the Altiplano, and eight appeared classified under some IUCN Red List category (Table 1).The vegetation recorded included 34 species of herbs (48%), 32 species of shrubs (45%), and 5 species of cactus (7%).Herbaceous species were the most abundant on all islands, accounting for 86% of individual plants.Shrubs and cacti accounted for only 14%.

DISCUSSION
The species recorded make up some 30% of the 235 listed by Navarro and Maldonado (2002) for the Central Altiplanic Section, and are in line with other descriptions for this area (Navarro 1997;Montes de Oca et al. 2003;Navarro andFerreira 2004, Ibish et al. 2008).The most diverse families -Asteraceae, Poaceae and Cactaceaerecorded were also mentioned by Montes de Oca et al. (2003).Verbenaceae and Brassicaceae were the next most diverse, as Montes de Oca also reported.Altogether, 21% of the species recorded were endemic or faced some degree of threat.These islands are therefore home to important fragments of floral diversity in the region.
Compared to the Altiplano as a whole, the species richness values for the islands were low.The Shannon-Wiener α-diversity indices were similar to those published in previous reports for the region (Ortuño et al. 2006), however, other authors have reported higher values for the Altiplano (Muñoz and Bonacic 2006;Galán de Mera et al. 2010).Since the examined plant communities are isolated from the adjacent mountain ranges (the minimum distance to the closest is 3 km) and from each other (the minimum distance between islands is 6.5 km), the low species richness and α-diversity values might be thought explicable by the island biogeography theory.They might also be explained, however, by the absence of human settlements, agriculture and animal husbandry -all of which increase the species richness and α-diversity of plant communities (Galán de Mera et al. 2010).The present findings thus suggest these ecosystems have suffered little disturbance.This is reinforced by the fact that islands have been preserved as sanctuaries by the native human population (T.Vargas, pers. comm. March 2011).
The lack of any statistical differences among the transects for the same areas on different islands suggests that their plant communities are composed of a dominant or single species assemblage.Nevertheless, a smooth change in vegetation was perceived along the altitudinal gradient on each island, and different plant communities were visually identified related to changes in microhabitat.Thus, while the transect size was sufficient to record plant communities as a whole, it was insufficient to detect changes due to microhabitat.
In the border areas adjacent to the salt lakes, three plant communities were visually identified: (1) salt-flat  2002;Navarro and Ferreira 2004;Navarro 2011).Cacti and ferns were completely absent from these areas.The mountainsides were dominated by two types of xeromorphic scrub accompanied by columnar cacti and ferns similar to those of the alluvial terraces in the adjacent ranges.Two plant communities were identified: (1) succulent-spiny vegetation characterized by Trichocereus atacamensis and Baccharis boliviensis, and (2) the Thola resinous-scrub community characterized by Baccharis boliviensis, Fabiana densa, and Parastrephia quadrangularis (Meyen) Cabrera (Navarro and Maldonado 2002;Navarro and Ferreira 2004;Navarro 2011).Finally, the tops of the islands were formed by a subset of the mountainside communities with a reduction in terms of species richness and abundance, especially of herbs and ferns.
No community dominated by pastures was observed on any island.Such communities are characteristic of Altiplano landscapes but are thought to be a result of grazing (Genin and Fernández 1994).The observation reinforces the idea that these islands have suffered little disturbance.
The examined islands are important fragments in the maintenance of the Altiplano's floral diversity -they shelter several species assemblages as well as endemic and endangered species.Given that their plant communities show few signs of disturbance, these islands should be the subject of surveillance and conservation programs, especially in view of increasing human activity on the salt lakes.More work is needed to accurately describe their communities at the microhabitat level.

Table 1 .
List of species found on the studied islands.Life Form (a-h = annual herb, p-h = perennial herb, s = shrub, c=cactus), endemism, Red List category (EN = endangered, VU = vulnerable, LC = least concern, DD = deficient data), and voucher information is shown for each.Salazar et al. | Plant communities of islands in Altiplanic salt lakes, Bolivia