Abstract
North Patagonian lakes are characterized by their oligotrophic or oligo-mesotrophic status. These conditions bring with them, respectively, the presence of abundant mixotrophic ciliates and a low species number of crustacean zooplankton under oligotrophic status, and low numbers of mixotrophic ciliates and a high species number of zooplankton under oligo-mesotrophic status. The aims of the present study are, (1) to use remote sensing techniques for determining abundances of mixotrophic ciliates and crustacean zooplankton, and (2) to characterize these mixotrophic and zooplankton communities by using null models. The sensing was accomplished from a satellite, i.e., by measuring the reflectance of the sunlight on a waterbody, which result will vary according to the contents of the water column. The results of Principal Component Analysis (PCA) revealed that sites with low reflectance of all bands have a high abundance of Stentor accompanied by low zooplankton absolute abundance, whereas a markedly opposite situation was observed under high reflectance, where Stentor has low abundance in conjunction with high zooplankton absolute abundances. The null models revealed that the communities in the studied sites do not have structured species associations, and that there is an overlap of niches. These results obtained agree with similar observations for Argentinean Patagonian lakes.
Introduction
The situation of mixotrophy, i.e., when organisms are capable of both autotrophy and heterotrophy, has been thoroughly described for the marine environment. There, mixotrophic organisms are important under an oligotrophic status, because if the availability of nutrients is limiting, the mixotrophics survive by photosynthesis, whereas if bacteria are abundant, the mixotrophics predate on bacteria; in addition, mixotrophics constitute prey for zooplankton (Ptacnik et al., 2016; Fischer et al., 2017; Moorthi et al., 2017; Stibor et al., 2019). The phenomenon of mixotrophy has also been reported in North Patagonian lakes (39-41°S) that show presence of mixotrophic ciliates and a low species number of crustacean zooplankton grazers (De los Ríos-Escalante et al., in press a). In contrast, if in these lakes a transition occurs from oligotrophy to mesotrophy, the mixotrophic ciliates are replaced by phytoplankton, and the crustacean zooplankton grazers increase in abundance and species richness (Thomasson, 1963; Wölfl, 1995; Woelfl, 2007; De los Ríos-Escalante, 2010; De los Ríos-Escalante & Woelfl, 2017; De los Ríos-Escalante et al., in press a, b).
In North Patagonian lakes (38-41°S) located in Chile, the transition from oligotrophy to mesotrophy has been rather marked during the last four decades (Soto, 2002; Woelfl et al., 2003; De los Ríos-Escalante et al., 2017a). In this scenario, these changes involved alterations in food webs in the pelagial, mainly in terms of zooplankton assemblages in restricted areas of which the trophic status got altered (De los Ríos-Escalante et al., 2017a). A different situation would occur in the case of the central and southern Chilean Patagonian lakes (De los Ríos-Escalante, 2010, 2016), and the Argentinean Patagonian lakes (Modenutti, 2014; Trochine et al., 2015), that have a marked oligotrophic status and a low number of crustacean grazer species as well as low abundances of individuals. Other important topics observed in Patagonian lakes are related with the optical properties of the water in situ, in terms of spectral properties in the visible spectrum, that can characterize marked oligotrophic lakes in mountain zones with difficult access (De los Ríos-Escalante et al., 2017b, c, d). Also, the use of spectral properties revealed correlations between the composition of the grazer zooplankton in glacier lakes and characteristic water coloration as a function of the presence of glacier sediments (De los Ríos-Escalante et al., 2013; De los Ríos-Escalante & Acevedo, 2017a, b). In this scenario, it would be possible to find some correspondence between the optical properties of lakes with mixotrophic ciliates, and the grazer zooplankton community in North Patagonian lakes. The aims of the present study thus are, first to analyse the potential correspondence between optical properties in terms of visible light as recorded on LANDSAT ETM+ bands with mixotrophic communities and the composition of the crustacean zooplankton grazer community, and subsequently analyse potential structural patterns in the mixotrophics and the studied grazer assemblage, using null models.
Optical properties and mixotrophic ciliates (Stentor spp.) at the sites considered in the present study
Citation: Crustaceana 93, 9-10 (2020) ; 10.1163/15685403-bja10022
Crustacean zooplankton abundances (ind/l) at the sites considered in the present study
Citation: Crustaceana 93, 9-10 (2020) ; 10.1163/15685403-bja10022
Map of the sites studied that are included in the present study. (Modified after Thomasson, 1963; Woelfl, 2007).
Citation: Crustaceana 93, 9-10 (2020) ; 10.1163/15685403-bja10022
Material and methods
Sampling procedures.— Mixotrophic ciliates and zooplankton from North Patagonian lakes (tables I and II, fig. 1), were collected between January 2009 and February 2010. Samples were taken from the pelagial environment at approximately 1500 m off the shore, and approximately at noon. Mixotrophic ciliates were collected and quantified by filtering 1 l of lake water into GFC fibre glass filter paper according to the descriptions of Woelfl & Geller (2002). Zooplankton was collected using 20 m vertical hauls with a zooplankton net of 20 cm mouth diameter and 80 μm mesh; the collected specimens were fixed in 96% ethanol and identified in accordance with the descriptions of Araya & Zúñiga (1985) and Bayly (1992), and quantified under the stereo-microscope.
Sites.— The studied sites were North Patagonian lakes, formerly called Araucanian lakes, located between 39-40°S (Woelfl, 2007): Villarrica (
Remote sensing procedures.— Satellite data were obtained from LANDSAT/ETM+ image, as recorded between January 2004 and February 2009 (tables I and II) and provided by the Land Processes Distributed Active Archive Center (LP DAAC), U.S. Geological Survey (http://LPDAAC.usgs.gov; De los Ríos-Escalante et al., 2017b, c, d).
Bands.— The bands of visible light (B1, visible-blue, 452-514 nm; B2, visible-green, 519-601 nm; B3, visible-red, 631-692 nm) as well as of near-, and mid-infrared (B4, near-infrared, 772-898 nm; B5, mid-infrared, 1547-1748; and B7, mid-infrared, 2065-2346 nm) were calibrated radiometrically to spectral irradiance and then to reflectance, with atmospheric correction being applied (tables I and II; De los Ríos-Escalante et al., 2017b, c, d).
Exploratory multivariate data analysis.— All data analysis was applied using the R software package (R Development Core Team, 2009). As a first step, data analysis was applied as a matrix correlation analysis using the Hmisc R package (Harrell, 2016) for determining the correlations between the studied variables. As a second step, a principal component analysis (PCA) was executed, and for this statistical analysis the HSAUR R package (Everitt & Hothorn, 2016) was applied.
Null models in ecology data analysis.— According to the viewpoint of null models, which detect the absence of regulator factors in community structure by determining the random presence or absence of distinct elements in the community (Gotelli & Graves, 1996), two kinds of aspects were considered: species co-occurrence and niche sharing.
For the first type of null model analysis, a species presence/absence matrix was constructed, with the species in rows and the sites in columns. First, we calculated a Checkerboard score (“C-score”), which is a quantitative index of occurrence that measures the extent to which species co-occur less frequently than expected by chance (Gotelli, 2000). A community is structured by competition when the C-score is significantly larger than expected by chance (Gotelli, 2000; Tondoh, 2006; Tiho & Josens, 2007; Gotelli & Entsminger, 2009); it compares co-occurrence patterns with null expectations via simulation. Gotelli & Ellison (2013) suggested as the most useful statistical null model the model Fixed-Fixed: in this model, the row and column sums of the matrix are preserved. Thus, each random community contains the same number of species as the original community (fixed column), and each species occurs with the same frequency as in the original community (fixed row). The null model analyses were performed using the package EcosimR (Gotelli & Ellison, 2013; Carvajal-Quintero et al., 2015).
For niche overlap analysis, an individual matrix was built in which rows and columns represented species and sites, respectively, and then it was tested if niche overlap significantly differed from the corresponding value under the null hypothesis (in an example random assemblage); this approach was applied for data from the second field period. In this analysis the Pianka index was used. That model is based on a median table that shows the probability of niche sharing as this is compared with the niche overlap in the community simulated (Gotelli & Graves, 1996). The niche amplitude can be retained or reshuffled; when it is retained, it preserves the specialization of each species. However, when it is reshuffled according to normal distribution, it uses a much wider utilization gradient and, in fact, it will indicate a wider niche overlap in the simulated community in comparison to the real community. Also, the zero states can be retained or simulated, which means that the zero participation in the observed matrix is either maintained, or not, in each simulated matrix. In the present study, we used the algorithm RA3 (Gotelli & Ellison, 2013; Carvajal-Quintero et al., 2015). This model RA3 retains the amplitude and reshuffles the zero conditions (Gotelli & Entsminger, 2009). This null model analysis was carried out using the software EcosimR (Gotelli & Ellison, 2013; Carvajal-Quintero et al., 2015).
Results
The studied sites have a wide range of mixotrophic abundance, that can even be arranged into a gradient. The mixotrophic ciliates present were primarily Stentor amethystinus Leidy, 1880, with in addition the low abundances of S. araucanus Foissner & Wölfl, 1994, at sites with high mixotrophic abundance and low abundance of zooplankton species, which sites also gave high reflectance values. By contrast, at sites with low values of reflectance, we found low mixotrophic abundance and an increased abundance of crustacean grazer zooplankton (tables I and II).
The results of the correlation matrix, revealed significant, direct correlations between B1 and B2, B1 and B3, B1 and B4, B1 and B5, B1 and B7, B1 and B3/B4, B2 and B3, B2 and B4, B2 and B5, B2 and B7, B2 and B3/B4, B3 and B4, B3 and B5, B3 and B7, B3 and B3/B4, B4 and B5, B4 and B7, B4 and B3/B4, B5 and B7, B5 and B3/B4, Daphnia pulex Leydig, 1860 with total individuals (table III) and significant inverse correlations between Stentor and B1, Stentor and B2, Stentor and B3 (table III).
Correlation matrix of variables considered in the present study
Citation: Crustaceana 93, 9-10 (2020) ; 10.1163/15685403-bja10022
The PCA revealed that the main contributor variables for axis 1, were the reflectance of B1, B2, B3, B4, B5, B7, and the reflectance ratio B3/B4, and Stentor abundances; whereas for the second axis the main contributor variables were Stentor, D. pulex, species number, and total crustaceans. The sites Villarrica 1, Villarrica 2, Caburgua 1, Ranco, and Riñihue, have low mixotrophic abundance (<10 ind/l), and sites Pirihueico 2 and Panguipulli 1 have 50 and 45 ind/l of mixotrophic ciliates, respectively. Both groups of sites show high reflectance values and moderate zooplankton abundances. In contrast, low reflectance was observed for Caburgua 2, Pirihueico and Neltume, that have high mixotrophic abundance (55-107 ind/l, table II, fig. 2). Finally, Maihue Lake has high zooplankton abundance and also a high number of zooplankton species (fig. 2).
Results of the PCA executed for variables and sites included in the present study. For further explanation, see text.
Citation: Crustaceana 93, 9-10 (2020) ; 10.1163/15685403-bja10022
The results of the null model analysis revealed that the species associations (in fact: communities) are not structured, whereas there is a marked niche overlap (table IV).
Results of the null model analyses (species co-occurrence and niche sharing) for crustacean zooplankton species reported in the present study
Citation: Crustaceana 93, 9-10 (2020) ; 10.1163/15685403-bja10022
Discussion
The present results would agree with literature observations about mixotrophic organisms in marine environments, because first of all, mixotrophic abundance is high under oligotrophic regimes (Ptacnik et al., 2016; Fischer et al., 2017; Moorthi et al., 2017; Stibor et al., 2019), which is similar to earlier observations for lakes with high mixotrophic abundance, such as lakes Caburgua and Pirihueico (Woelfl & Geller, 2002; Woelfl, 2007; Woelfl et al., 2010). The results of high abundance of mixotrophic ciliates being associated with low reflectance, probably would be caused by the marked oligotrophy of these sites (De los Ríos-Escalante et al., in press a). This correlation between high mixotrophic ciliates and low reflectance bands probably associated to oligotrophy, and the respective correspondence with low zooplankton absolute abundances, would agree partially with observations of spectral properties and zooplankton abundances in lakes such as were observed for the lakes General Carrera and Tagua Tagua (De los Ríos-Escalante et al., 2013; De los Ríos-Escalante & Acevedo, 2017a, b). In this context, the present results reveal that the optical properties of waterbodies can identify zooplankton assemblages, and the zooplankton community structure observed, i.e., the marked, direct association between daphniids and cyclopoid copepods, would agree with observations for North Patagonian lakes with a marked gradient in the abundance of mixotrophic ciliates (Wölfl, 1995; Woelfl, 2007; Woelfl et al., 2010; Kamjunke et al., 2012; De los Ríos-Escalante & Woelfl, 2017). Under oligotrophy, the high abundance of mixotrophic ciliates consists of mixotrophic nanoflagellates, and in this scenario, the zooplankton would graze on nanoflagellates (Modenutti et al., 2000), which probably would explain the correlation between the abundance of mixotrophic ciliates and that of crustacean zooplankton. These results would be similar to previous observations in marine environments (Ptacnik et al., 2016; Fischer et al., 2017; Moorthi et al., 2017; Stibor et al., 2019).
These results do not agree with species co-occurrence, i.e., where the present result revealed the absence of a structured pattern. Nevertheless, similar results have been reported for zooplankton observations in Patagonian lakes, and the potential cause would be the presence of only a few species, but which species are observed to be recurring in many sites (De los Ríos-Escalante, 2016). In this context, the results on niche overlap observed in this study would agree with trophic interactions in Argentinean and Patagonian lakes, where under an abundance of mixotrophic ciliates a gradient could be recognized that indicates a gradual change in the structure of the crustacean zooplankton grazer community (Modenutti et al., 1998; Balseiro et al., 2001, 2004; Woelfl, 2007; Modenutti, 2014). This is because, if zooplankton abundance increases, specifically in terms of large cladocerans and cyclopoid copepods, the mixotrophic ciliates will decrease in abundance (De los Ríos et al., 2019).
As a conclusion, the above results would indicate the need for a detailed study of the trophic interactions in the pelagial of Patagonian lakes, because under a gradient of abundance of mixotrophic ciliates, there would be an inverse correlation with the abundance of crustacean zooplankton, in particular with with cyclopoid copepods. Those results have now quite strongly been indicated, but need to be confirmed in a much broader study, in which remote sensing can again play a significant role.
Corresponding author; e-mail: prios@uct.cl
Acknowledgements
The present study was funded by projects FONDECYT 1080456, and MECESUP UCT 0804. The authors also recognize the valuable comments of M.I. and S.M.A. for improving the manuscript.
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