Abstract
The phytoplankton in Lake Alchichica show a relatively low species richness with divergent roles in the food web depending on their size. Picophytoplankton (APP <2–3 μm) are essential in the lake microbial loop, due to their outstanding abundance. In contrast, the nano- (2–3 to 20 μm) and microphytoplankton (>20 μm) show lower densities than APP but progressively higher biomasses with increasing size. It is striking that the larger species cannot be consumed by zooplankton, even though this type of phytoplankton drives the pelagic biogeochemical cycles. The outcome is a significant loss of nutrients to the bottom, mainly by the microendemic diatom Cyclotella alchichicana and the littoral during the short annual cyanobacterial bloom Nodularia aff. spumigena. With APP, only the smaller and more abundant nanophytoplankton species (Monoraphidium minutum, Oocystis parva, and Cyclotella choctawhatcheeana) enter the main food web. The situation impacts the pelagic realm’s overall functioning, resulting in a chronic condition of resource limitation for metazooplankton growth. In short, the uniqueness of Alchichica’s phytoplankton relates to low species richness, large sizes as drivers of carbon and nutrient sinking, small sizes as the basis for the pelagic food webs, the presence of a microendemism, and some variants in other species that could define them as new taxonomic categories.
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12.1 The Phytoplankton of Lake Alchichica
Phytoplankton supplies the organic biomass that primarily fuels the trophic web in the pelagic community, especially for deep aquatic systems, and plays an essential role in a myriad of biogeochemical processes (Benoiston et al. 2017). These processes include those associated with nutrient cycling (carbon, silicon, nitrogen, and phosphorus), oxygen generation, and the removal of gaseous carbon through photosynthesis, among others.
The size (Sieburth et al. 1978) and other characteristics of the biological units (e.g., solitary cells or in filaments, aggregates or colonies; with or without mucilage, with or without spines) in which phytoplankton species occur are very important for the role they play in food webs (Peštová et al. 2008; Ortega-Mayagoitia et al. 2011; Bautista-Reyes and Macek 2012; Ciros-Pérez et al. 2015; Macek et al. 2020). Their study’s optimal techniques also vary with size. Identification and quantification methods differ for smaller sizes (picophytoplankton cells below 2–3 μm) and relatively larger ones (nanophytoplankton, 2–3 to 20 μm; microphytoplankton, above 20 μm).
In Lake Alchichica, the smallest sizes (picophytoplankton or autotrophic picoplankton, APP) have been extensively studied (by autofluorescence-based counting, comparing phycobilins and chlorophyll-a) as part of the microbial loop. The most common species and the annual dynamics of phytoplankton, emphasizing nano- and microphytoplankton (Utermöhl-based counting), have also been explored.
12.2 Picophytoplankton
Autotrophic picoplankton (APP) and microorganisms included in the microbial loop, which are cycling their primary production, play an essential role in the plankton food web of tropical lakes (Sarmento 2012). However, the re-evaluated PEG model (Sommer et al. 2012) still underestimated their role, applied to define the plankton dynamics under different climatic conditions (De Senerport Domis et al. 2013). Moreover, exhaustive long-term and complete data are available only from non-tropical monomictic lakes such as Lake Constance (Gaedke and Weisse 1998), Kinneret, Israel (Malinsky-Rushansky et al. 1995; Sukenik et al. 2014), and Lake Biwa, Japan (Maeda et al. 1992; Wakabayashi and Ichise 2004; Sekino et al. 2007).
The APP has been studied in Lake Alchichica by Peštová et al. (2008), Macek et al. (2009), Hernández-Avilés et al. (2010), Bautista-Reyes (2011), Bautista-Reyes and Macek (2012), and Macek et al. (2020). APP abundances and biomasses were analyzed using their autofluorescence in green excitation and orange/red fluorescence observation and taking photographs for image analysis (ImageJ with specific macros). The images were compared with those taken with the chlorophyll-a filter set. Individual cyanobacterial cell volumes used for the organic carbon approximation (200 fg/μm3; Weisse 1993) were based on a 2003–2006 evaluation (González-Aguilar, unpublished). The representative carbon content of Alchichica’s cyanobacteria used to calculate biomasses was intermediate during mixing (46 fg/cell), lowest in the mixing layer during stratification (epilimnion, 32 fg/cell), and highest in the anoxic hypolimnion (64 fg/cell).
Oliva et al. (2001) and Rosiles-Gonzalez (2005) identified the cyanobacteria composition by their morphology, which has been subsequently acknowledged by Peštová et al. (2008), Macek et al. (2009), and Alcocer et al. (2014a, b). Synechocystis aquatilis was reported as the dominant picoplankton in Lake Alchichica (Oliva et al. 2001). Rosiles-González (2005) found Synechococcus nidulans and Synechocystis sp. in the mixing layer (the whole column in January, the epilimnion during early stratification), and at the metalimnion during the rest of the stratification; colonial cyanobacteria of the genera Epigloeosphaera, Cyanodictyon, Lemmermanniella, and Eucapsis appeared mainly during the stratification, either every month or restrained to a few of them.
Callieri et al. (2013) isolated and phylogenetically characterized three clones of phycoerythrin-rich Synechococcus from the lake; now Synechococcus sp. (PE) 8F6, which is classified as a member of Cyanobium/Synechococcus sub-cluster 5.2 (Sánchez-Baracaldo et al. 2019). Cyanobium/Synechococcus and Synechocystis are confirmed using molecular methods (see Chap. 11 Bacterioplankton). Cyanobium sp. was the most common OTU (Operative Taxonomic Unit), distributed in the epilimnion and below the oxycline layer. The diversity of OTUs is scarce to date, but it is supposed to be greater than that found in the consulted libraries.
Throughout the year, the APP in the whole column averages 1.5 × 105 cells/mL (2.6 × 103 to 9.1 × 105 cells/mL) with annual peaks just during and at the end of circulation, between the end of January and April (Fig. 12.1a). However, the APP distribution is heterogeneous; it follows a very similar annual pattern tightly linked to the lake’s warm-monomictic thermal regime, i.e. stratification and circulation periods (Fig. 12.1b). However, the local maxima, which peaked >1 × 106 cells/mL, has been observed in the upper zone of the mixed layer during the circulation (typically at 15–20 m).
In contrast, just after the stable stratification of the water column begun, APP numbers used to drop to a minimum in the epilimnion. They concentrated either throughout the thick metalimnion (frequently from July to August) or in the metalimnion upper limit (during the late stratification, from September or October to November), showing lower abundances (about 5 × 105 cells/mL). The abundance peaks do not usually correspond to the deep chlorophyll maxima (DCM) produced by Cyclotella alchichicana (Ortega-Mayagoitia et al. 2011).
An apparent relation to photosynthetically active radiation PAR was observed (Fig. 12.1b), with the deepest APP maxima found typically above 1% sPAR. On the other hand, APP were sometimes abundant even in the entirely dark layers that coincided with the oxycline in the years when January mixing was incomplete.
Generally, APP distribution relates to DO concentrations, but picocyanobacteria were also detected below the oxycline. Such behavior is better observed in the plot of estimated carbon biomass integrated below a surface area (Fig. 12.2), which considers differences in the specific cell biomass in distinct layers. Usually, the APP biomass observed in the anoxic hypolimnion was important, although smaller than that of the epilimnion and metalimnion biomass.
Typically, APP abundances correlate to other limnological variables. For example, in September 2018 (Fig. 12.3) the APP maximum numbers coincided with the upper metalimnetic limit, where the sPAR dropped to 1%. However, the first DCM peak coincided with oxygen depletion and the biomass maximum of APP colony feeding Euplotes euryhalinus. The APP-feeding Spirostomum teres biomass also peaked there. The second DCM coincided with a phycocyanin’s peak, indicating a local concentration of picocyanobacteria colonies and the second S. teres biomass peak. Where the Eh (redox potential) dropped to negative values, the maximum abundance of anoxygenic photosynthetic bacteria, APB (a purple sulfur bacteria, Thiocapsa sp.) peaked, which along with APP, supported S. teres growth (distribution and dynamics of pelagic bacteria are further explored in Chap. 11, Bacterioplankton, and 13, Protozooplankton).
12.3 Nano- and Microphytoplankton
12.3.1 Particularities on the Composition of the Lake Alchichica’s Larger Phytoplankton
A relevant feature in the phytoplankton of Lake Alchichica is their low species richness. The most abundant nano- and microphytoplankton species reported at any time of the year (Table 12.1) are limited to seven (referenced with authorship in Chap. 20, Diversity and Endemisms). All of them have remained dominant numerically and/or in biovolume up to the 2017–2019 timeframe (unpublished data).
Other species have been seen more rarely and/ or at lower abundances, such as the dinoflagellate Parvodinium (Glenodinium in Oliva et al. 2001, also detected in 2017–2019, unpublished data); the cryptophyte Cryptomonas sp. (Rosiles 2005, practically unobserved at present), and small flagellates that sometimes are hardly identifiable with Lugol fixative (see Chap. 13, Protozooplankton). Monoraphidium dybowskii has been recognized since 2003–2004 (Rosiles 2005 up to present). Recently (2017–2019), previously unreported species has been observed in Alchichica’s phytoplankton: the nanoplanktonic diatom Halamphora sp. (with scarcely silicified frustules and actively dividing in the water column; it should be noted that Halamphora is a typical benthic genus but presents a planktonic habit in Alchichica, as has also been found for other genera species in the Gulf of Mexico, Olivares et al. 2017). Finally, the cyanobacterium Pseudanabaena sp. shows cell diameters below 2 μm but formed in a row inside a filamentous mucilage that can be of a much longer size (see Chap. 20, Diversity and endemisms).
It is important to note how common it is to report benthic species that can be seen in the phytoplankton samples, in low numbers, with no distinction between the two. These are usually tychoplankton species of the type defined by Hutchinson (1967, in Cahoon 2016) as pseudoplankton, i.e., suspended in the water column by chance, due to mechanical effects as wind-generated turbulence. It should be emphasized that these species have been removed from the Alchichica phytoplankton species list and the others consulted (Table 12.2).
In summary, the specific richness of larger phytoplankton recognized so far for Alchichica does not exceed ca.15 species, a low number compared to the variety of its littoral autotrophic microalgal species (see Chap. 10, The Littoral Benthic Community). However, other lakes with a chemical signature similar to Alchichica (see Chap. 5, Hydrogeology and Hydrochemistry, and Table 12.2) show comparable specific phytoplankton richness. It is interesting that the species richness decreases with increasing salinity in alkaline environments (Sui et al. 2016, Table 12.2) and rises when there is a shift towards eutrophy (Fetahi et al. 2014) except for hypersaline environments (like the one exemplified by Bernard et al. 2019).
Therefore, the low species richness of large-sized phytoplankton in Alchichica mirrors the hydrochemical characteristics of its saline and soda-alkaline traits (see Chap. 5, Hydrogeology and Hydrochemistry).
The particular aspects of Lake Alchichica’s phytoplankton that make it unique are diverse. The ecologically dominant diatom C. alchichicana is microendemic to this lake (Oliva et al. 2006, 2019). C. choctawhatcheeana has a wide biogeographic distribution, but in Mexico has only been reported from Alchichica and the nearby Lake Atexcac (Oliva et al. 2008). Characteristic morphological arrangements such as the constancy in the linear shape for the filaments of Nodularia aff. spumigena (Oliva et al. 2009; Vilaclara and Oliva-Martínez 2019) suggest molecular changes that could lead to the definition of a new taxonomic category (based on finding, after a metagenomic study, a Nodularia sp. in the pelagic zone of Alchichica, not assimilable to any other Nodularia species published in the Silva database libraries; see Chap. 20, Diversity and Endemisms). The presence of a planktonic diatom from the Bacillariophycidae group, Halamphora sp., is an unexpected outcome for a mostly benthic genus.
Microendemicity also occurs in other groups of organisms in the lake, both pelagic and benthic (see Chap. 20, Diversity and Endemisms). In the case of phytoplankton, probably the composition and concentration of major ions in the water (see Chap. 5, Hydrogeology and Hydrochemistry), which on the one hand imposes restrictions on species richness, to some extent may also serve as a barrier isolating species from other lake environments in the Oriental basin and nearby water bodies. The latter could favor a rapid evolution of some species for such a young lake (late Pleistocene or Holocene origin; see Chap. 2, Geological Evolution), even despite the annual winter stay of migratory waterfowl (Saunders and Saunders 1981), which can act as transportation vectors for microscopic species coming from the intermediate water bodies where they have landed during their journey.
12.3.2 A Yearly Dynamics for Phytoplankton
Cuevas (2017) and Cuevas et al. (2017) summarize “a type year” of chlorophyll-a concentration and primary productivity in Lake Alchichica. Primary productivity rates and chlorophyll-a concentration show a recurrent annual, seasonal cyclicity. Two peaks stand out, one associated with the mixing period and related to the hemispheric winter diatom bloom. Another evidenced by a Deep Chlorophyll Maximum (DCM), related to C. alchichicana during the well-established stratification. The surface bloom of N. aff. spumigena during early stratification (sometime between April and June), of variable intensity depending on the year (Oliva et al. 2009), also marks a visible change in the annual lake dynamics, despite its relatively short duration.
Based on the composition and abundances of the larger phytoplankton community and associated physicochemical descriptors published in Oliva et al. (2001), the 1998 data were reanalyzed and presented according to the current knowledge on the phytoplankton composition. The abundance of the seven most common species (cells/mL) was transformed to biovolume (μm3/mL, Olenina et al. 2006) as a proxy for biomass (from now on, both terms are used interchangeably). The species biovolumes were integrated with the physicochemical descriptors (temperature, T°C; dissolved oxygen, DO mg/L; nutrients mg/L, N-NO3−, N-NO2−, N-NH3, and Soluble Reactive Phosphorus, SRP; chlorophyll-a, Chlor, μg/mL).
A Principal Component Analysis (PCA) was performed with R-Studio (Fig. 12.4). Greater variability in the vertical distribution of species and other limnological descriptors is observed during stratification, compared to a much lesser one during mixing, which tends to homogenize the water column. Components 1, 2, and 3 absorb 33, 14 and 11% of the variability, respectively. Axis 1 is interpreted as compartmentalization of the column in epilimnion on the one hand, with elevated temperatures and DO values, and congregates six of the species, all but C. alchichicana; on the other hand, it segregates nutrients into deeper, cooler, anoxic layers. Component 2 is explained as the bloom of the species with higher buoyancy and lower chlorophyll-a concentration (the cyanobacterium N. aff. spumigena) in the shallower zone of the epilimnion, with higher temperatures, versus the smaller chlorophyte species (M. minutum and O.parva) distributed throughout the mixing layer during stratification (epilimnion). Component 3 accounts for the deep maximum of chlorophyll-a associated with C. alchichicana in and around the metalimnion.
In short, results underscore the higher variability encountered during stratification and segregates species in the epilimnion (all but C. alchichicana) from nutrients in colder, deeper, and anoxic layers. It highlights the short but relevant N. aff. spumigena bloom in the epilimnion’s upper zone, and the deep chlorophyll-a maximum, associated with C. alchichicana, at the metalimnion. This pattern is consistent with a typical year (Cuevas et al. 2017; see Chap. 7, Physicochemical Characteristics).
A cluster analysis was also applied with R-Studio. Figure 12.5 shows the hierarchical clustering for the biomass of the seven species throughout the year. The dendrogram differentiates between C. alchichicana and the other six species mostly distributed at the epilimnion during stratification. The constellation plot arranges the species as endpoints. Each line’s length approximates the distance between species; the biovolume centroid lies between the two larger species, C. alchichicana, and N. aff. spumigena. Due to their contribution to the biomass throughout the year, both species stand out. However, they are differentiated from each other: C. alchichicana because it grows in or near the metalimnion during the established stratification and N. aff. spumigena because it blooms in the epilimnion during early stratification.
C. alchichicana has a significant impact on the biogeochemical cycles of the lake. As an autotrophic species, it is the leading exporter of nutrients to the bottom sediment, including biogenic C and Si (Ardiles et al. 2012). Despite being so important in nutrient cycling, it does not enter the grazing food webs because of its large size (35–63 μm in diameter during the sampling lapse): most of the year, adults of the copepod Leptodiaptomus garciai cannot feed on it, let alone smaller forms of zooplankton (Ortega-Mayagoitia et al. 2011; Ciros et al. 2015; Macek et al. 2020). Such characteristics could bestow on it the title of the “Queen of Alchichica” (sensu Ortega-Mayagoitia); C. alchichicana may be one of the famine story’s main culprits in the pelagic realm (see Chap. 14, Metazooplankton). In some way, this species acts as a symbolic exponent of the myth of Tantalus: much food is available, but it is impossible to feed on it, and it ends up being lost, dragging its nutrients to the bottom of the lake, while playing an essential role in the regional carbon balance (Alcocer et al. 2014a, b).
N. aff. spumigena is the second largest species in microphytoplankton (average cell diameter around 9–10 μm, but filaments up to several mm), blooming in the epilimnion’s upper layers for a short time during early stratification. Such an extensive growth relatively close to the water surface is attributed to the presence of aerotopes that give it a high buoyancy during an episode of environmental nitrogen limitation (see Chap. 7, Physicochemical Characteristics). Unlike C. alchichicana, an important proportion (84%) of the biomass is carried by the wind to the littoral zone, where it decomposes (Alcocer et al. 2012; Oseguera et al. 2013). It does not enter the grazing food web either but directly into the microbial loop’s decomposition route. It can be found in low numbers and shorter filaments (less than 100 μm) during the established and late stratification.
Given the importance of these two species of microphytoplankton for the biogeochemical cycles and linked to the thermal regime and the dissolved oxygen vertical gradients (Time-depth plots, Fig. 12.6a), their distribution throughout the year is depicted in Fig. 12.6b.
Another category of microphytoplankton comprises two species whose individual cell size qualifies them as nanoplankton, Chaetoceros elmorei and Oocystis submarina. However, organized into biological units, they become microplankton. C. elmorei develops as chains of cells with intertwined spines during mixing; nevertheless, they are more frequently found as solitary cells or in pairs during stratification, but their four long spines per cell equally hinder zooplankton feeding. Colonies of O. submarina develop some firm layers of mucilage, so they also function as larger biological units; the latter does not facilitate their consumption in grazing herbivores’ food webs either.
The nanophytoplankton species C. choctawhatcheeana, Oocystis parva, and Monoraphidium minutum make up the third category. The three species enter the trophic web as food for heterotrophs, such as some ciliates (see Chap. 13 Protozooplankton), the rotifer Brachionus sp. ‘Mexico’ and possibly various life stages of the copepod Leptodiaptomus garciai (see Chap. 14, Metazooplankton).
12.4 Conclusions
Large phytoplankton dominate the biomass of Lake Alchichica all year round. Their size prevents them from being consumed by protozooplankton and metazooplankton, resulting in a significant nutrient loss through their primarily transfer to the deep bottom and secondarily into the littoral zone. Thus, large phytoplankton (mostly C. alchichicana) drive biogeochemical cycles. For example, a large amount of carbon and nutrients are exported below the thermocline into the sediments, where they accumulate and preserve. The latter impacts the pelagic system’s overall functioning in Lake Alchichica, resulting in a key factor regulating zooplankton ecology (e.g., through food limitation) and, most likely, their evolution.
The importance of the small-sized phytoplankton or APP on the microbial loop is relevant by integrating into the food webs of heterotrophic species. However, the relative importance of carbon flux through the microbial loop may appear minor regarding a comparatively lower biomass.
This divergence in phytoplankton functional adaptation (large species as drivers for nutrient loss out of the pelagial zone, small species at the base of the pelagic food webs), together with the low species richness, the presence of a microendemism, and morphotypes that could be new species, confer the peculiar characteristic of uniqueness to Lake Alchichica and its autotrophic producers in the water column.
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Acknowledgments
To Laura Peralta for her technical support in the chlorophyll analysis. Luis A. Oseguera for field sampling (2017–2019). Omar Rivera for helping in statistical analyses and some graphics. Cecilia López-Vázquez thanks CONACYT for her MSc studies’ scholarship. G. Vilaclara and M. Macek were supported in the manuscript’s preparation through a DGAPA/PAPIIT grant IN231820 and IN219220 (2020–2022). support for the long-term analysis of Lake Alchichica data was granted as UNAM DGPA/PAPIIT IN225517. Previous studies were granted to M. Macek through CONACYT 52387 (2007), SEP-CONACYT 79893 (2009); CONACYT 131689 (2011–2013), CONACYT Mexico - DLR Germany bilateral grant 1203801, DGAPA IN208502 (2003–2005), DGAPA IN207206 (2006–2008), DGAPA IN222709 (2009–2011), and as internal UNAM FES grants PAPCA 2002–2003, PAPCA 2003–2004, PAPCA 2006, and PAPCA 2009.
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Vilaclara, G., Oliva-Martínez, M.G., Macek, M., Ortega-Mayagoitia, E., Alcántara-Hernández, R.J., López-Vázquez, C. (2022). Phytoplankton of Alchichica: A Unique Community for an Oligotrophic Lake. In: Alcocer, J. (eds) Lake Alchichica Limnology. Springer, Cham. https://doi.org/10.1007/978-3-030-79096-7_12
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