Keywords

20.1 Introduction

The total number of species and the number of exclusive, endemic species inhabiting a geographic area or even a single environment are two fundamental elements in the sphere of management and conservation policies. For example, biodiversity hotspots are relatively small areas where species richness and endemism levels are high, and organisms are facing a strong threat of habitat loss (Reid 1998). Therefore, the biological diversity inventory is a mandatory first step that in a relatively small and geologically young lake such as Alchichica could resemble a simple task. However, it has been a quite complex and slow process.

20.2 Diversity and Endemic Species: A Fascinating, Never-Ending Story

The number of species that a single lake can host depends on several factors acting at different temporal and spatial scales. These factors range from local interactions such as competition and predation to long-term continental processes such as glaciation, speciation/extinction rates, and dispersal barriers originated by plate tectonics (Brönmark and Hansson 2005). Further, inside a lake itself, the environment is not homogeneous, and there are species with different adaptations to exploit different ecological opportunities. Usually, the littoral zone is the most heterogeneous due to the physical structures produced by riparian and submerged vegetation, different kinds of sediments, and substrates, among others. It hosts a higher number of species compared to the water column (Schindler and Scheuerell 2002). However, the diversity observed in the water column may increase when including detailed analyses of microstratified, microaerobic, and anaerobic zones of the water column, with plenty of resource-rich niches controlled by the position of thermocline, as well as the anoxic hypolimnion (see Chap. 11 Bacterioplankton and Chap. 13 Protozooplankton).

In Lake Alchichica, an additional element increases the environmental complexity, enhancing species richness. The ring of tufa (i.e., stromatolites) circling the littoral zone, which creates small, isolated ponds, offers a myriad of microhabitats itself, and forms high vertical, underwater walls (see Chap. 10, The littoral community, and Chap. 22, Microbialites: diversity hotspots in the Mexican Plateau).

There is, however, another factor that heavily influences the number of species we know in each environment: the human factor. Each human scholar has the free will to choose the biological group she/he will investigate. Some biological groups are more attractive than others, producing an uneven understanding of the different branches of the tree of life. Also, and for practical uses, each scholar decides what a species is, how to name it, how to classify it, and how, when, and where to look for it. Inadvertently, such decisions are strongly impinged not only by personal and academic backgrounds but by technical advances and even by philosophical and sociopolitical settings.

Throughout the years, the practice of identifying species within each biological group has evolved at a different pace and followed slightly different paths due to the available technology. For hundreds of years, the best-studied species were animals, land plants, and fungi, which were defined mainly in terms of morphological discontinuities (Paterlini 2007). The number of records of these three groups in current electronic catalogs of life is a testimony of this historical bias. However, thanks to the advent of the microscope first and molecular tools more recently, life has revealed an astonishingly diverse microbial treasure: the immense majority of life forms on Earth are eukaryotic single-celled species (traditionally called protists), Bacteria, and Archaea (Burki et al. 2020; Yilmaz et al. 2014). Although in many groups, identifications still rely heavily on morphological characters, the biologist’s toolkit nowadays can include cultures, molecular markers, ecophysiological experiments, and reproductive compatibility trials.

Following this historical path, the first records of the biological diversity in Lake Alchichica were animals and were based mainly on morphological characters. The copepod Leptodiaptomus (Diaptomus) garciai (Osorio-Tafall) and the silverside Poblana alchichica De Buen were described according to the current systematic standards and announced as new species in 1942 and 1945, respectively (Osorio-Tafall 1942; de Buen 1945; see also Chap. 14, Metazooplankton, and Chap. 15, Alchichica silverside). These two cases illustrate how systematics and personal points of view influence the perceived diversity and endemicity in an environment.

As early as 1953, Wilson and Yeats decided that the copepod inhabiting Alchichica was a population of the North American Diaptomus novamexicanus and considered D. garciai a synonym, extending the ecological range of the freshwater copepod to saline waters (Wilson and Yeats 1953). Later, when the genus Diaptomus underwent a major systematic revision and was split into smaller genera, it was assigned to Leptodiaptomus. Thus, the first paper on the ecology of the population inhabiting Alchichica was published as L. novamexicanus (Lugo et al. 1999). More than 50 years later, a study applying COI barcoding, reproductive trials, and ecophysiological tests showed that despite morphological differences are subtle, the copepod from Alchichica, now Leptodiaptomus garciai, was a valid name assigned to a species that is genetically, reproductively, and ecologically isolated from L. novamexicanus (Montiel-Martínez et al. 2008). Although he used only morphological traits, Osorio-Tafall was right from the start.

The silverside Poblana alchichica has been the subject of several studies regarding its taxonomic status and diversification patterns in Atherinidae in North America. There are other silversides in the neighboring lakes that were initially recognized as different, microendemic species: P. letholepis Alvarez, 1950 in Lake La Preciosa and P. squamata Alvarez, 1950 in Lake Quechulac. The status of the three species has been controversial because others have qualified their morphological divergence as non-significant, and their COI sequences are identical (Valdez-Moreno et al. 2009). Attending these criteria, they have been considered conspecific (P. alchichica with three subspecies) or members of the genus Menidia, given their low COI divergence with M. menidia. Later phylogenetic studies have shown that all members of the genus Poblana do form a monophyletic group closer to Chirostoma than to Menidia. However, the proper delimitation of the three genera and species within Poblana still awaits clarification (Bloom et al. 2009).

Meanwhile, the three species with their original names are regarded as valid in FishBase (Froese and Pauly 2020). To summarize, the story goes like this: the number of fish species in the three crater lakes went from three new species belonging to a new genus to a single species with three sub-species belonging to a pre-existing, widely distributed genus. In the end, the original taxonomic assignment prevailed, but the story is far from concluded.

From the early studies of the 1940s to recent years, the number of species found in Alchichica increased as new generations of researchers interested in the littoral, the stromatolites, the pelagic, and deep benthic zones (see next section). Remarkably, several species that in the subsequent decades would be recognized as new, endemic species, initially were misidentified: the now emblematic diatom Cyclotella alchichicana Oliva et al. 2006 was first identified as Stephanodiscus niagarae (Arredondo et al. 1984) or Cyclotella quillensis (Oliva et al. 2001); the rotifer Brachionus sp. ‘Mexico’ that inhabits Alchichica, Atexcac and La Preciosa (Alcántara-Rodríguez et al. 2012) appeared in a paper as Brachionus rotundiformis (Sarma et al. 2002); the insect Chironomus alchichica Acosta & Prat, 2017 was incorrectly identified as Chironomus stigmaterus (Alcocer et al. 2016); the ostracod Limnocytherina axalapasco Cohuo-Durán, Pérez & Karanovic (2014) was in a first moment confounded with Limnocythere inopinata (Hernández et al. 2010). Sometimes the discovery they were new, endemic species came after an observation during the peer-review process, or with a newcomer looking for cryptic diversity, or simply a well-trained eye that was able to see beyond the -apparently- obvious.

Other species have been uncovered straightforwardly, thanks to easily observable traits like in the case of the amphipod Caecidotea williamsi Escobar-Briones & Alcocer 2002, or by the intervention of young specialists as happened with Candona alchichica Cohuo, Hernández, Pérez & Alcocer (2017), or by renowned authorities in the field, like the description of Cletocamptus gomezi Suárez-Morales, Barrera-Moreno & Ciros-Pérez (2013), and the cyanobacterial species Entophysalis litophila, E. atrata, Chamaesiphon halophilus, Heteroleibleinia profunda, Mantellum rubrum and Xenococcus candelariae Tavera & Komárek (1996), and Gloeomargarita litophila Moreira et al. (2017).

Overall, up to date, there are 18 recognized endemic species (7 cyanobacteria, 11 eukaryotes) inhabiting Lake Alchichica (16 exclusive, 2 shared with neighboring lakes), but we can foreshadow that the list will grow in the short term. Systematic studies have invigorated recently with the use of molecular markers, as part of a polyphasic approach to uncover the diversity of prokaryotes in Alchichica (Aguila et al. 2021; Moreira et al. 2017; Chaps. 11 and 22, Bacterioplankton and Microbialites: Diversity hotspots in the Mexican Plateau). An ongoing project on metabarcoding suggests that there are nearly 8600 Amplicon Sequence Variants (ASVs of the 16S rRNA gene with 100% sequence identity) related to Bacteria and Archaea (unpublished data). These data suggest that from these sequences, 14 Archaea and 544 Bacteria genera are present in the sediment, microbialites, and water samples from the littoral and pelagic zones of Lake Alchichica. However, most of the sequences cannot be assigned at the genus level, leaving a considerable task pending identifying Lake Alchichica prokaryotes by polyphasic approaches in the future.

The preceding paragraphs show that knowing how many species there are in a lake is an arduous process. New, endemic species are frequently overlooked, and their status can be controversial. With such considerations in mind, we present the most comprehensive list ever published of the known specific diversity of Lake Alchichica.

20.3 How Many Species Do We Know in Lake Alchichica?

The species list that closes this chapter gathers the species richness of Lake Alchichica, known after 80 years of research. Most species have appeared previously in peer-reviewed papers, and others are mentioned for the first time in the preceding chapters of this book.

Modern systematics pursues a unified three-domain taxonomy, making classification consistent with phylogeny (Yilmaz et al. 2014). To organize the species list in a coherent whole, we adopted the phylogenomic classification framework of the SILVA rRNA database project (Yilmaz et al. 2014), which integrates the classification system of Eukarya proposed by Adl et al. (2005, 2012, 2019). Within the framework of the phylogenomic approach of Adl et al. (2019), the classification of unicellular organisms is well resolved. However, inevitably we had to draw upon the most recent Linnean-based classifications to integrate the names of Metazoa (animals) and Streptophyta (charophytes and plants) species. Current supraspecific classification, valid/correct binomina, and authorities were confirmed in Catalogue of Life (https://www.catalogueoflife.org/), World Register of Marine Species (http://www.marinespecies.org/), AlgaeBase (https://www.algaebase.org/) and the SILVA database (https://www.arb-silva.de/), using the version 138 released in November 2020.

Although some biological groups still await proper study (birds, fungi, parasites of invertebrates, etc.), the known biological diversity of Lake Alchichica encompasses distant branches of the three domains of life: Bacteria (37 genera and species reported), Archaea (8 genera identified) and Eukarya (196 genera and species), rendering a list of 241 taxa identified thus far. Inevitably, the length and composition of the list show not only the outcome of natural processes, but the expertise and experience of the researchers attracted to Lake Alchichica, in addition to the array of tools they had applied.

The task of comparing the taxonomic richness in the three domains of life is not straightforward due to the different species concepts and tools applied in each field (de Queiroz 2007). In prokaryotes, 18 bacterial and archaeal genera were detected exclusively with metabarcoding techniques. The remaining prokaryotes and eukaryotes were diagnosed with morphological or polyphasic approaches.

The most integral project for surveying Bacteria and Archaea in Lake Alchichica includes samples from the sediments, microbialites, and water column, all of them collected during the stratification period of the lake (unpublished data). Most of the identified bacterial taxa are Cyanobacteria (89%), with minor proportions of Bacteroidota and Proteobacteria (5.5% each). Members of the phylum Cyanobacteria are the most often identified due to their biogeochemical functions (C and N fixation) and relative abundance in the lake (see Chaps. 11 and 12). Archaeal diversity and its taxonomic affiliation are just being explored. In this case, the phylum Euryarchaeota was the most represented with 75% of the ASVs.

In Eukarya, the supergroup TSAR is by far the most diverse (Table 20.1). The largest share are ciliates (42) and diatoms (45). The second most important supergroup is Amorphea, which includes 66 metazoan species (animals). In Archaeplastida, six species are embryophytes (plants). Interestingly, 63% of all Eukarya species here reported are protists (unicellular eukaryotes), constituting a more balanced view of the actual distribution of life forms across the eukaryotic tree of life (Burki et al. 2020).

Table 20.1 Specific richness (S) of eukaryotic supergroups found in Lake Alchichica
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Concerning habitats, 150 species are considered exclusively littoral and amount a significant proportion of taxa (62%), as expected due to the heterogeneous composition and morphometry of Lake Alchichica. The reported taxa found in the microbialites constitute nearly 58% of the prokaryotic diversity. In Chap. 10 (The littoral benthic community), the number of species, including macroinvertebrates, protozoans, and diatoms, is considered moderate compared to other lakes. In contrast, the pelagic environment is inhabited by 53 species (22%), a number considered low regarding phytoplankton (15 species, Chap. 12, Phytoplankton of Alchichica), ciliates (25 species, Chap. 13, Protozooplankton), metazooplankton (3 species, Chap. 14), fish (1 species Chap. 15, Alchichica silverside). The parasites of the silverside P. alchichica amount to 4% of the species.

20.4 Concluding Remarks

Given the relatively low species richness in Lake Alchichica, the number of endemic species is a striking and attractive attribute. This geologically young (13.3 to 6.3 ka) and small (2.4 km2) lake holds a known overall richness of 241 taxa (Tables 20.2 and 20.3), among which 18 (7.5%) are endemic (Tables 20.2 and 20.3). Given the disparity in the sampling effort and the identification methods employed across biological groups, this figure is relative. For example, if only plants and animals were considered, endemicity rises to 14% (total richness = 73; endemic = 10). Even more, if we use the common approximation of focusing on particular taxa, the share of endemicity soars: if only vertebrates are accounted (P. alchichica, and A. taylori), then 100% of species are endemic; four out of six species (67%) of crustaceans thus far recorded (C. williamsi, L. garciai, C. gomezi, C. alchichica) are also exclusive of this lake. As more unique, endemic eukaryotic and especially prokaryotic taxa are found, species richness and global endemicity indicators will surely rise.

Table 20.2 Main Archaea and Bacteria detected in Lake Alchichica
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Table 3
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Table 4
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Table 20.3 Eukaryotic diversity in Lake Alchichica
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Table 6
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Table 7
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Table 8
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Table 9
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Table 10
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Table 11
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Table 12
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Table 13
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Table 14
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Table 15
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Table 16
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Table 17
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Table 18
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Another interesting indicator of the importance of endemic species in Lake Alchichica is that endemic species do not restrict to a single group but belong in several distant branches of the tree of life, including bacteria, diatoms, crustaceans, insects, and vertebrates. Additionally, they are present in – or even dominate – every functional community and possess unique biological or ecological features: the only pelagic predator, P. alchichica is endemic, as are the two main components of the plankton biomass: the copepod L. garciai and the diatom C. alchichicana (Chaps. 14 and 12, respectively). The amphipod C. williamsi is the first asellid recorded in saline environments and is highly specialized in inhabiting crevices in the stromatolites (Escobar-Briones and Alcocer 2002). G. litophila, associated with the microbialites, was the first known cyanobacterium with intracellular carbonate inclusions (Moreira et al. 2017). The salamander A. taylori is a model for the evolution of obligated paedomorphy (Percino-Daniel et al. 2016). The list goes on.

The evolution of neoendemic species is favored by high diversification rates, limited dispersal capabilities, and local conditions hampering the invasion of cosmopolitan taxa (Martens and Segers 2014). In Lake Alchichica, the study of the evolutionary processes behind endemicity began just a few years ago. As far as we know, the peculiar ionic conditions and geographical isolation could have played a key role in the diversification process, promoting local adaptation and genetic isolation from other populations (Percino-Daniel et al. 2016; Bloom et al. 2013; Chaps. 12, Phytoplankton of Alchichica, and Chap. 14, Metazooplankton). Moreover, ionic conditions also seem to restrict the establishment of species from geographically close lakes. To acquire a better understanding of these diversification processes, we should extend our efforts to, at least, the neighboring lakes. Surely, they will provide many answers and, we hope, new questions, so we can continue this never-ending story.

Finally, it is important to note that all this exciting effort to discover the wonders still hidden in Alchichica may be dramatically interrupted by the increasing threats to the conservation of the lake habitats and, with it, the peculiar biota adapted to this unique environment (see Chap 5, Hydrogeology and Hydrochemistry, and Chap. 21, Conservation actions).