Rotifers are widely recognized as being important components of freshwater ecosystems, and whether this assessment is based on numbers or biomass, their contribution to trophic dynamics in these waters is striking. In some instances their importance even exceeds that of the microcrustaceans: cladocerans and copepods [1]. In estuarine and marine habitats, rotifers are generally thought to play a minor role in community dynamics [2-5]. Therefore brackish and marine rotifers, with the notable exception of the Brachionus plicatilis species complex, have received little attention worldwide. Because of its value in aquaculture [6-8], this species complex has received special attention and this intense study has yielded valuable insights into evolutionary processes such as cryptic speciation and molecular phylogenetics [9-12] and genomics [13]. In addition, rotifer species inhabiting saline and subsaline lakes in northern Canada possessed greater haplotype diversity than their freshwater counterparts [14].

While quite a bit is known about zooplankton present in México (e.g., copepods [15,16]; cladocerans [17], few reports have been published on brackish and marine rotifers [3,18,19]. Although some of these studies have focused on species diversity and community dynamics [4], none of them have included the Chihuahuan Desert.

With increased exploitation of aquifers for agriculture, cattle, industry, and drinking water, we can expect an increase in the salinization of existing watersheds and water sources particularly in arid areas. These changes will negatively impact ecosystem processes [20]. Here we examine selected inland saline waters in the Chihuahuan Desert of México, a region renowned for its high biodiversity in terrestrial and aquatic systems [21-24]. We also present an initial species list of the rotifers, group sites by water chemistry, conduct pair-wise comparisons of rotifer community diversity between sites, and investigate ecological correlates of rotifer presence/absence.

Figure 1 Characterization of study sites by water chemistry. Upper left panel - conductivity, chloride, and sulfate; upper right panel - conductivity, hardness, and alkalinity; lower left panel - hardness, chloride, and alkalinity; lower right panel - hardness, (more ...)

Figure 2 RDA of all Méxican sites. Left panel: ordination of species; Right panel: ordination of samples. Sampling regions: black – San Luis Potosí; dark grey – Cuatro Ciénegas; white – Ojos Altos; light grey – (more ...)

Figure 3 RDA of Méxican sites with conductivity ≥2000 µS cm-1. Left panel: ordination of species; * these species share a vector with other species: BracBide with PolyDoli, PolyVulg, GastStyl; CollCrat with CephPan, LecaCorn; TrioTetr (more ...)

Figure 4 RDA of Méxican sites with conductivity ≥3000 µS cm-1. Left panel: ordination of species; * these species share a vector with other species: HeteHete with LecaCrep, LecaUndu; ColuUnci with TrioTetr, DicrForc, PlatQuad; CephForf (more ...)

Table 1 Species found in high salinity aquatic habitats in México (*found at salinities ≥ 3000 μS cm-1)

Table 2 Simpson's asymmetric percent similarity indices (SAI) for 10 selected sites* in the Méxican Chihuahuan Desert

Table 3 Jaccard Index for 10 selected sites* in the Méxican Chihuahuan Desert

Table 4 Summary of RDA statistics for the first four axes of all Méxican sites

Rotifer species that were ordinated together with the variable lakes/reservoirs included many planktonic species, such as Keratella cochlearis, Trichocerca rattus, T. similis, Polyarthra cf. luminosa, P. euryptera, P. vulgaris, P. remata, Asplanchna girodi, A. brightwellii, S. oblonga, and S. pectinata (Fig. 2, left panel). Species that were positively associated with chloride are Notholca acuminata, Dicranophorus forcipatus, Collotheca crateriformis, Cephalodella panarista, Lecane cornuta and Lepadella ovalis/patella.

The RDA performed on the dataset of sites with conductivity ≥ 2000 μS cm^-1 separates species assemblages at CC from those found in the Ojos Altos and at San Luis Potosí, respectively (Fig. 3, right panel), with 21.2% of the variance in the species data being explained by the first four canonical axes (Table 5). Species assemblages of different sites at CC vary more than those at the other sampling regions and are ordinated along gradients formed by the presence of macrophytes and chloride concentration, nitrate concentration, seasonality (summer) and TDS. Species found mostly in the Ojos Altos and San Luis Potosí and negatively correlated with chloride are L. aeganea, B. bidentatus, P. dolichoptera, and P. vulgaris (Fig. 2, left panel). In CC sites a large group of species is ordinated with presence of macrophytes and chloride concentration: L. bulla, Philodina megalotrocha, Cephalodella megalocephala, Lecane punctata and L. closterocerca. Another group of species was correlated with seasonality (summer): Lecane obtusa, L. lunaris, Lepadella triptera, Hexarthra oxyuris, Proalis similis, Eosphora ehrenbergi, and Euchlanis dilatata.

Table 5 Summary of RDA statistics for the first four axes of Méxican sites with a conductivity ≥ 2000 μS cm-1

The RDA of the dataset containing the sites with conductivity ≥ 3000 μS cm^-1 again identified chloride, the presence of macrophytes, alkalinity, and site order, as the most important variables explaining the variance in the species data (Fig. 3). Site order signifies that the waterbody consisted of a series of pools that were ordered downstream from the spring source. In this analysis 30.4% of the total variance can be explained by the first four canonical axes (Table 6). Occurrence of Lecane spinulifera, Colurella colurus, Hexarthra oxyuris, Eosphora ehrenbergi, Proales similis, and bdelloids at CC sites was positively correlated with alkalinity and chloride concentration, whereas the majority of species correlated with presence of macrophytes included Philodina megalotrocha, Cephalodella forficula, Colurella uncinata, Dicranophorus forcipatus, Lecane arcula, Platyias quadricornis, Scaridium bostjani, Trichocerca intermedia, Trichotria tetractis, and Tripleuchlanis plicata. Brachionus bidentatus, B. angularis, P. dolichoptera, P. vulgaris, and Gastropus stylifer were found in San Francisco cattle tank (San Luis Potosí) and were negatively correlated with chloride.

Table 6 Summary of RDA statistics for the first four axes of Méxican sites with a conductivity ≥ 3000 μS cm-1

While zooplankton inhabiting saline aquatic habitats have received some attention worldwide (e.g., China [5], Spain [26-29], Canada [14,30], Western US [31,32], Africa [33-36], Japan [37], Australia [38-41], Arabia [42]), there is a genuine need for additional studies of rotifers in saline and marine environments of México [3]. A recent study noted that 74% of rotifer species in México (n = 42) were cosmopolitan, 5% were restricted to North America, 10% were tropical, and 4% were shared with Europe-Asia-Africa [43]. Most work on rotifers in saline habitats in México has been done by Sarma and his colleagues. For example, Sarma & Elías-Gutiérrez [44] found 31 rotifer species in their survey of an estuarine lagoon; 11 of which were found in our study (Platyias quadricornis, Tripleuchlanis plicata, Colurella uncinata, Lepadella ovalis, Lecane bulla, L. closterocerca, L. hornemanni, L. luna, L. obtusa, L. pyriformis, and L. thalera). In addition, Sarma et al. [3] reported 37 species of rotifers in Mecoacan, a brackish (5–35 ‰) lagoon located in Tabasco. Our survey of 48 waterbodies in the Mexican Chihuahuan desert shared few of these species (Anuraeopsis fissa, Ascomorpha saltans, Brachionus angularis, Euchlanis dilatata, and Lecane bulla) all of which have reportedly cosmopolitan distributions [45]. Another recent study [19] reported 128 taxa from 36 aquatic sites in southeastern México including some brackish habitats. Of these species, 23 (A. fissa, B. bidentatus, C.obtusa, C. uncinata, E. dilatata, K. americana, L. arcula, L. bulla, L. closterocerca, L. cornuta, L. crepida, L. hornemanni, L. leontina, L. luna, L. lunaris, L. obtusa, L. spinulifera, L. thalera, L. triptera, Platyias quadricornis, Polyarthra dolichoptera, Scaridium bostjani and Tripleuchlanis plicata) also were found in our survey.

In a larger study of freshwater habitats in the Méxican Chihuahuan Desert that includes the sites reported here, Wallace et al. [25] note that many species occurred as singletons or doubletons, and species inhabiting particular sites are quite unique. Here we further address community similarity among high salinity habitats using the SAI, and again the uniqueness of communities is apparent (Table 2). While our study adds substantially to the characterization of rotifer communities, clearly much more research needs to be accomplished if we are to develop a good understanding of the biogeography of rotifers in saline waters in North America.

The saline systems in the Mexican part of the Chihuahuan Desert have less total dissolved solids and lower conductivity than some of the waters of the Northern Chihuahuan Desert in the United States, notably those at White Sands National Monument, New Mexico and the Bottomless Lakes near Roswell, New Mexico. Only few species typical for saline waters were found over a wide range of aquatic habitats in the Chihuahuan Desert, such as Proales similis. However, a redundancy analysis performed on the data of all the saline systems that we have sampled in the Chihuahuan Desert, showed that the presence or absence of macrophytes is an important variable in determining species composition in all of these systems (unpublished data).

High salinity and conductivity levels can have major impacts on zooplankton community structure. A study in coastal lakes found that salinity level had significant impacts on zooplankton [46], leading the authors to predict that relatively small increases in salinity levels will cause reduced biodiversity of freshwater ecosystems. In a mesocosm experiment manipulating salinity, Hart et al. [31] found dramatic shifts in zooplankton community structure and shifts in the abundance of many species. As salinity increased, densities of the dominant rotifer species decreased and at the highest salinities 2 species were reduced to very low numbers. Shiel and his colleagues found that salinity was a significant, but site-specific, factor in determining rotifer community composition in rivers in the Lake Eyre Basin [41]. Saline systems had reduced species richness compared to their freshwater analogs (0–4 versus 0–31). In the Mexican saline systems studied here, as salinity increases the number of species found decreases substantially (Table 1; Fig 1, 2, 3). Chloride is a significant factor in determining the occurrence of rotifers. Some species are positively correlated with chloride content and others negatively associated (see Results, Fig 2a, 3a). It appears in our systems that typical planktonic freshwater species (e.g., Asplanchna brightwellii, A. priodonta, K. americana, K. cochlearis, and Synchaeta pectinata) are replaced by salinity tolerant species such as Hexarthra oxyuris and Notholca acuminata.

Inland saline systems often harbor diverse and unique community assemblages. Unfortunately, human exploitation can be extremely disruptive to ecosystem processes and services provided by these important water sources. During our sampling efforts, several historical springs near Janos, México were dry. In addition, Ojo de la Casa has recently dried and Ojo en de Medio has dried and re-surfaced in the past year, probably due demands of a geothermal electrical plant for cooling water and agricultural and domestic uses. Increasing human population size and global climate change will only make this scenario more prevalent. Thus, it is imperative that governmental agencies establish policies that protect these fragile ecosystems [47].

Our sampling strategy attempted to provide an All Taxa Biological Inventory (ATBI) [51]; to accomplish this we collected samples from planktonic, littoral, and benthic habitats using plankton nets (64 μm), grab samples (e.g., aquatic plants for sessile forms), and aspirating samplers. We calculated species richness (S), Jaccard's Similarity Index and Simpson's Index of Asymmetry [52,53]. The keys used in this study were as follows: Monogononta [54-64] and Bdelloidea [65,66]. Additional details of our methodology are described in [25,48,49].

The authors declare that they have no competing interests.

EJW, TS, RLW, JVRA, and RRM all participated in collecting trips and in species identifications. EJW drafted the manuscript. TS ran the statistical analyses (three-way plots of water chemistry and Redundancy Analyses). RLW calculated the Jaccard's and Simpson's Asymmetric Indices. All authors read and approved the final manuscript.

M. Silva-Briano, A. Adabache, R. Galván-De la Rosa, N. Salas-Mercado, G. Santos-Medrano, R. deRegnier, A. Palomeque, G. Jimenez-Guerrero & M. Stensberg provided assistance in sampling. Adolfo Sosa & Hector Javier Gonzalez-Martínez helped locate several sampling sites at Cuatro Ciénegas, Chihuahua. Jeffrey Bennett at BBNP provided logistical support in sampling the hotspring in the lower canyons downstream of BBNP. H. Segers provided expert review of our species identifications. Collections were made under permit #09436 from the Secretario de Medio Ambiente y Recursos Naturales to M. Silva Briano. We thank the Comisión Federal de Electricidad for permission to sample Presa de la Boquilla. This material is based upon work partially supported by an American Association for the Advancement of Science Women's International Science Collaboration (WISC) travel grant award, the National Science Foundation under DEB #0516032, National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH) Grant Number 5G12RR008124. and ADVANCE #0245071 (UTEP), T & E, Inc., & Funds for Faculty Development (Ripon College). The contents are solely the responsibility of the authors and do not necessarily represent the official views of NSF, NCRR or NIH.