Facilitation of the non-native annual plant Mesembryanthemum crystallinum (Aizoaceae) by the endemic cactus Eulychnia acida (Cactaceae) in the Atacama Desert

The Atacama Desert is one of the most stressful environments worldwide and represents a strong barrier for the establishment of native and non-native plants. In this study, we report the establishment of a non-native annual plant through facilitation by a native endemic cactus in a relatively undisturbed coastal area in north-central Chile. Soil collected under Eulychnia acida contained more available nutrients (N, P and K), water, and soluble salts than soils collected away from E. acida. Co-occurrence analyses showed a strong positive spatial association (facilitation) between the native cactus E. acida and the non-native annual, Mesembryanthemum crystallinum. The aboveground biomass of M. crystallinum individuals was 4-fold higher under the influence of E. acida. Native halophytes occasionally shared the cactus understory with the non-native species, but dominant native shrubs and perennial herbs did not co-occur with the cactus at scales of 1 and 4 m². All these results support facilitation of the native cactus on the non-native herb. The combination of direct and indirect positive effects could explain the assembly of the non-native annual plant in these undisturbed areas of the Atacama Desert and have major implications on M. crystallinum capacity to colonize new areas.     

Introducing the Atacama Desert

This brief introduction is intended to orientate the reader with respect to the principal environmental and historical features of the Atacama Desert, the oldest and continuously driest non-polar temperate desert on Earth. Exploration of its microbiology is relatively recent but both fundamental and applied research activities have grown dramatically in recent years reflecting the substantial interest in its microbial diversity, ecology, biogeochemistry, natural product potential and Mars-analogue properties of this unique and invigorating environment.     

Ultraviolet radiation in the Atacama Desert

The world’s highest levels of surface ultraviolet (UV) irradiance have been measured in the Atacama Desert. This area is characterized by its high altitude, prevalent cloudless conditions, and a relatively low total ozone column. In this paper, we provide estimates of the surface UV (monthly UV index at noon and annual doses of UV-B and UV-A) for all sky conditions in the Atacama Desert. We found that the UV index at noon during the austral summer is expected to be greater than 11 in the whole desert. The annual UV-B (UV-A) doses were found to range from about 3.5 kWh/m² (130 kWh/m²) in coastal areas to 5 kWh/m² (160 kWh/m²) on the Andean plateau. Our results confirm significant interhemispherical differences. Typical annual UV-B doses in the Atacama Desert are about 40% greater than typical annual UV-B doses in northern Africa. Mostly due to seasonal changes in the ozone, the differences between the Atacama Desert and northern Africa are expected to be about 60% in the case of peak UV-B levels (i.e. the UV-B irradiances at noon close to the summer solstice in each hemisphere). Interhemispherical differences in the UV-A are significantly lower since the effect of the ozone in this part of the spectrum is minor.     

Fungal diversity in the Atacama Desert

Fungi are generally easily dispersed, able to colonise a wide variety of substrata and can tolerate diverse environmental conditions. However, despite these abilities, the diversity of fungi in the Atacama Desert is practically unknown. Most of the resident fungi in desert regions are ubiquitous. Some of them, however, seem to display specific adaptations that enable them to survive under the variety of extreme conditions of these regions, such as high temperature, low availability of water, osmotic stress, desiccation, low availability of nutrients, and exposure to high levels of UV radiation. For these reasons, fungal communities living in the Atacama Desert represent an unknown part of global fungal diversity and, consequently, may be source of new species that could be potential sources for new biotechnological products. In this review, we focus on the current knowledge of the diversity, ecology, adaptive strategies, and biotechnological potential of the fungi reported in the different ecosystems of the Atacama Desert.     

Geology and geochemistry of the Atacama Desert

The Atacama Desert, the driest of its kind on Earth, hosts a number of unique geological and geochemical features that make it unlike any other environment on the planet. Considering its location on the western border of South America, between 17 and 28 °S, its climate has been characterized as arid to hyperarid for at least the past 10 million years. Notably dry climatic conditions of the Atacama Desert have been related to uplift of the Andes and are believed to have played an important role in the development of the most distinctive features of this desert, including: (i) nitrates and iodine deposits in the Central Depression, (ii) secondary enrichment in porphyry copper deposits in the Precordillera, (iii) Li enrichment in salt flats of the Altiplano, and (iv) life in extreme habitats. The geology and physiography of the Atacama Desert have been largely shaped by the convergent margin present since the Mesozoic era. The geochemistry of surface materials is related to rock geochemistry (Co, Cr, Fe, Mn, V, and Zn), salt flats, and evaporite compositions in endorheic basins (As, B, and Li), in addition to anthropogenic activities (Cu, Mo, and Pb). The composition of surface water is highly variable, nonetheless in general it presents a circumneutral pH with higher conductivity and total dissolved solids in brines. Major water constituents, with the exception of HCO₃^?, are generally related to the increase of salinity, and despite the fact that trace elements are not well-documented, surface waters of the Atacama Desert are enriched in As, B, and Li when compared to the average respective concentrations in rivers worldwide.     

Description and life cycle of a new Physarum (Myxomycetes) from the Atacama Desert in Chile

A new species of Physarum (Myxomycetes), Physarum atacamense is described in this paper, and details are provided on its life cycle as observed in spore-to-spore culture in agar. The new species was collected during studies of the Atacama Desert in Chile. It has been collected directly in the field and isolated in moist chamber cultures prepared with material from an endemic cactus. The combination of characters that make this species unique in the genus are its large fusiform nodes of the capillitium, its long, bicolored stalk and the very dark brown and densely warted angular spores. The morphology of specimens of this myxomycete was examined with scanning electron microscopy and light microscopy, and micrographs of relevant details and life cycle stages are included in this paper. The importance of resistant stages in the life cycle of this myxomycete is stressed, and the close association of this myxomycete with its plant substrates is discussed.     

Microbial colonization of the salt deposits in the driest place of the Atacama Desert (Chile)

The Atacama Desert (Chile), one of the most arid places on Earth, shows hostile conditions for the development of epilithic microbial communities. In this study, we report the association of cyanobacteria (Chroococcidiopsis sp.) and bacteria belonging to Actinobacteria and Beta-Gammaproteobacteria and Firmicutes phyla inhabiting the near surface of salt (halite) deposits of the Salar Grande Basin, Atacama Desert (Chile). The halite deposits were investigated by using optical, confocal and field emission scanning electron microscopes, whereas culture-independent molecular techniques, 16S rDNA clone library, alongside RFLP analysis and 16S rRNA gene sequencing were applied to investigate the bacterial diversity. These microbial communities are an example of life that has adapted to extreme environmental conditions caused by dryness, high irradiation, and metal concentrations. Their adaptation is, therefore, important in the investigation of the environmental conditions that might be expected for life outside of Earth.     

Stem anatomy of Rhipsalis (Cactaceae) and its relevance for taxonomy

We used paternally inherited chloroplast microsatellites (cpSSR) to study population genetic structure in the endemic and highly restricted Serbian spruce Picea omorika. Fragment size polymorphism at the five cpSSR regions that could be amplified out of the nine tested combined into only four different haplotypes in the seven populations studied. Mean total haplotypic diversity was H _T = 0.395, and mean within-population diversity was H _s = 0.279. Haplotypic variation was lower than in most conifers described so far and partitioned into two geographical groups. All northern P. omorika populations were fixed or nearly fixed for the common haplotype, while southern populations exhibited two to three haplotypes. We suggest that current P. omorika populations are shaped by extreme demographic bottleneck and random genetic drift linked to Quaternary glacial cycles. P. omorika thus belongs to the small group of genetically depauperate tree species.     

Natural product diversity of actinobacteria in the Atacama Desert

The Atacama Desert of northern Chile is considered one of the most arid and extreme environment on Earth. Its core region was described as featuring “Mars-like” soils that were at one point deemed too extreme for life to exist. However, recent investigations confirmed the presence of diverse culturable actinobacteria. In the current review, we discuss a total of 46 natural products isolated to date representing diverse chemical classes characterized from different actinobacteria isolated from various locations in the Atacama Desert. Their reported biological activities are also discussed.     

Stem anatomy of Rhipsalis (Cactaceae) and its relevance for taxonomy

Several species of the genus Rhipsalis (Cactaceae) are extremely important as ornamentals and are endangered in their natural habitat. However, only a few studies have addressed its taxonomy, morphology (including anatomy), phylogeny and evolutionary history. Consequently, the limited knowledge of the genus coupled with the problematic delimitation of species had led to problems in the identification of taxa. In the current work six species of Rhipsalis, R. cereoides, R. elliptica, R. grandiflora, R. paradoxa, R. pentaptera and R. teres were studied to evaluate the relevance of anatomical characters for the taxonomy of the genus. An anatomical characterization of the primary structure of the stem of Rhipsalis is provided highlighting the differences between species. Features of the stem epidermis are found to discriminate best between species and therefore provide clear and useful characters for the separation of species.     

Fundamental drivers for endolithic microbial community assemblies in the hyperarid Atacama Desert

In hyperarid deserts, endolithic microbial communities colonize the rocks’ interior as a survival strategy. Yet, the composition of these communities and the drivers promoting their assembly are still poorly understood. We analysed the diversity and community composition of endoliths from four different lithic substrates – calcite, gypsum, ignimbrite and granite – collected in the hyperarid zone of the Atacama Desert, Chile. By combining microscopy, mineralogy, spectroscopy and high throughput sequencing, we found these communities to be highly specific to their lithic substrate, although they were all dominated by the same four main phyla, Cyanobacteria, Actinobacteria, Chloroflexi and Proteobacteria. Our finding indicates a fine scale diversification of the microbial reservoir driven by substrate properties. The data suggest that the overall rock chemistry and the light transmission properties of the substrates are not essential drivers of community structure and composition. Instead, we propose that the architecture of the rock, i.e., the space available for colonization and its physical structure, linked to water retention capabilities, is ultimately the driver of community diversity and composition at the dry limit of life.     

Species Richness and Abundance of Naked Amebae in the Rhizoplane of the Desert Plant Escontria chiotilla (Cactaceae)

ABSTRACT. The species richness and quantity of naked amebae were determined in the bulk soil and rhizoplane of the desert plant Escontria chiotilla in the Valley of Tehuacan, Mexico. Samples from bulk soil were taken at 10-cm and 30-cm depths in April, May and July, 1993, and from roots and soil at a 10-cm depth in June and July, 1994. Quantity of amebae obtained by Most Probable Number method increased in the rhizoplane by two orders of magnitude after rains. Likewise, the countable population of amebae doubled in numbers at both the 10- and 30-cm depths after rains. We isolated 163 strains from both root and soil environments, which were grouped into 40 bactivorous and/or generalist species belonging to 19 genera. Species richness showed no clear dominance of a particular genus in either bulk soil or root. Acanthamoeba (groups II and III, Pussard & Pons) and Vahlkampfia accounted for 12.5% and 15% of the total number of species, respectively. However, greater species richness was found in bulk soil than on root surfaces. We concluded that the diversity of naked amebae, taken as numbers of individuals (or as biomass) of each species and its evenness, is still needed to assess the ecological roles of Acanthamoeba and Vahlkampfia in the soil environment.     

Multiscale climate change impacts on plant diversity in the Atacama Desert

Comprehending ecological dynamics requires not only knowledge of modern communities but also detailed reconstructions of ecosystem history. Ancient DNA (aDNA) metabarcoding allows biodiversity responses to major climatic change to be explored at different spatial and temporal scales. We extracted aDNA preserved in fossil rodent middens to reconstruct late Quaternary vegetation dynamics in the hyperarid Atacama Desert. By comparing our paleo‐informed millennial record with contemporary observations of interannual variations in diversity, we show local plant communities behave differentially at different timescales. In the interannual (years to decades) time frame, only annual herbaceous expand and contract their distributional ranges (emerging from persistent seed banks) in response to precipitation, whereas perennials distribution appears to be extraordinarily resilient. In contrast, at longer timescales (thousands of years) many perennial species were displaced up to 1,000 m downslope during pluvial events. Given ongoing and future natural and anthropogenically induced climate change, our results not only provide baselines for vegetation in the Atacama Desert, but also help to inform how these and other high mountain plant communities may respond to fluctuations of climate in the future.     

Water availability shapes edaphic and lithic cyanobacterial communities in the Atacama Desert

In the Atacama Desert, cyanobacteria grow on various substrates such as soils (edaphic) and quartz or granitoid stones (lithic). Both edaphic and lithic cyanobacterial communities have been described but no comparison between both communities of the same locality has yet been undertaken. In the present study, we compared both cyanobacterial communities along a precipitation gradient ranging from the arid National Park Pan de Azúcar (PA), which resembles a large fog oasis in the Atacama Desert extending to the semiarid Santa Gracia Natural Reserve (SG) further south, as well as along a precipitation gradient within PA. Various microscopic techniques, as well as culturing and partial 16S rRNA sequencing, were applied to identify 21 cyanobacterial species; the diversity was found to decline as precipitation levels decreased. Additionally, under increasing xeric stress, lithic community species composition showed higher divergence from the surrounding edaphic community, resulting in indigenous hypolithic and chasmoendolithic cyanobacterial communities. We conclude that rain and fog water, respectively, cause contrasting trends regarding cyanobacterial species richness in the edaphic and lithic microhabitats.     

Desert species adapted for dispersal and germination during floods: Experimental evidence in two Astrophytum species (Cactaceae)

Dispersal of organisms by water is known as hydrochory and is an important means of seed transportation. Here we present experimental evidence of possible dispersal and germination of seeds in water for arid land cacti. Seeds from Astrophytum spp. have unusual traits for plants from arid environments, traits that are typical of water dispersed seeds. Astrophytum capricorne and A. ornatum seeds disperse by floating in the Chihuahuan Desert. Seeds of other native species (Acacia farnesiana, Opuntia streptacantha and Prosopis laevigata (mesquite) were used as control, as well as commercial beans (Phaseolus vulgaris). Seed structures of A. capricorne and A. ornatum are consistent with water dispersal (hat shape, a funicular envelope covering a prominent hilum, and air chambers throughout the tegument). Seeds of A. capricorne showed the greatest water permeability, higher than those of A. ornatum which had similar permeability to common beans and mesquite. Acacia farnesiana and Opuntia streptacantha had the lowest permeability. Seeds of A. capricorne without a funicular layer floated more than those with a funicular layer. All seeds of A. ornatum floated initially, but 10% of those with funicular layer sank after a 30 days floating period. P. laevigata seeds floated also, but less than those of Astrophytum spp., and seeds of A. farnesiana and Phaseolus vulgaris did not float. Germination of A. capricorne was high under all treatments, both when immersed in a water layer or only moistened. Germination of A. ornatum was generally low (<30%), with <5% germination for seeds immersed in water and for those placed on a water film. Seeds of A. capricorne germinated slower in a water layer than in other treatments. No difference in germination rate was found across all treatments in A. ornatum.     

Evidence for nonallopatric speciation among closely related sympatric Heliotropium species in the Atacama Desert

The genetic structure of populations of closely related, sympatric species may hold the signature of the geographical mode of the speciation process. In fully allopatric speciation, it is expected that genetic differentiation between species is homogeneously distributed across the genome. In nonallopatric speciation, the genomes may remain undifferentiated to a large extent. In this article, we analyzed the genetic structure of five sympatric species from the plant genus Heliotropium in the Atacama Desert. We used amplified fragment length polymorphisms (AFLPs) to characterize the genetic structure of these species and evaluate their genetic differentiation as well as the number of loci subject to positive selection using divergence outlier analysis (DOA). The five species form distinguishable groups in the genetic space, with zones of overlap, indicating that they are possibly not completely isolated. Among‐species differentiation accounts for 35% of the total genetic differentiation (F_ST = 0.35), and F_ST between species pairs is positively correlated with phylogenetic distance. DOA suggests that few loci are subject to positive selection, which is in line with a scenario of nonallopatric speciation. These results support the idea that sympatric species of Heliotropium sect. Cochranea are under an ongoing speciation process, characterized by a fluctuation of population ranges in response to pulses of arid and humid periods during Quaternary times.     

Desert travels in the Atacama: making place through movement (c. 2500-1500 cal BP)

Social worlds are constituted by movement. Mobility entails the circulation not only of people, but also of material goods, imaginaries, experiences, flows of information, and knowledge. In this article, we examine different forms of movement in the Atacama Desert during the Formative Period (c. 2500-1500 cal BP), such as pedestrian travels, llama caravans, and navigation on sea lion-skin vessels along the Pacific, incorporating various material means and encompassing a wide array of incentives. We present different case studies that challenge monolithic assumptions about mobility in the South-Central Andes, commonly understood through the lens of ecological complementarity and primarily driven by economic exchange. Extending Binford's classic distinction between residential and logistical mobility as two ideal types of hunter-gatherers’ settlement systems to include groups of early farmers, in combination with the territorial categories of local and extra-local, we interrogate the spatial and temporal scale of these journeys – from daily to seasonal, from short to long distance – and its materialization. In these examples, we approach movement and travel as a way of life, expanding the traditional view of mobility through an exploration of the varied ways in which it was practised and integrated into the social lives of desert dwellers.