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All issues Volume 56 (2020) Ann. Limnol. - Int. J. Lim., 56 (2020) 7 Full HTML
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Ann. Limnol. - Int. J. Lim.
Volume 56, 2020
Article Number 7
Number of page(s) 9
DOI https://doi.org/10.1051/limn/2020005
Published online 17 April 2020

© EDP Sciences, 2020

1 Introduction

Cladocera is a group of microcrustaceans that play an important ecological role in the energy transfer between trophic levels and represent a large portion of the secondary productivity of aquatic ecosystems (Allan, 1976; Elmoor-Loureiro and Soares, 2010). The importance of this group is related to its biological characteristics, such as parthenogenetic reproduction and dormancy of egg production (Allan, 1976). These characteristics are known to provide advantages to the group in the face of adverse environmental conditions (Santangelo et al., 2011).

Recently, studies on freshwater cladoceran biodiversity from the Neotropical region have increased significantly (Kotov and Fuentes-Reines, 2014; Alonso and Kotov, 2017; Sousa and Elmoor-Loureiro, 2017). More than 700 species of cladocerans are currently known in the world, of which 186 species of the orders Anomopoda and Ctenopoda occur in the Neotropical region (Forró et al., 2008; Kotov et al., 2013). At the beginning of this century, 112 species were known in Brazil, according to the latest survey conducted by Elmoor-Loureiro (2000). This number has increased in recent years and currently the Cladocera fauna of Brazil is estimated to exceed 140 species. This estimate is based on recently published studies that included the description of new species, genera, and the elaboration of regional catalogs (Sinev and Elmoor-Loureiro, 2010; Soares and Elmoor-Loureiro, 2011; Elmoor-Loureiro, 2014; Zanata et al., 2017; Sousa and Elmoor-Loureiro, 2019a,b).

Despite the evident progress in the investigations of the group, there are still some regions of Brazil where freshwater Cladocera biodiversity is not well known (Elmoor-Loureiro et al., 2018), as is the case of the state of Mato Grosso. Located in Central Brazil, Mato Grosso has its territory divided into three distinct Hydrographic Regions (HR), Paraguay, Amazon and Tocantins-Araguaia (ANA, 2015). Mato Grosso could be considered the most diverse state in Brazil, where the Cerrado biodiversity hotspot (Myers et al., 2000) meets the Pantanal and Amazon forest. At the same time, the state has a great diversity of aquatic habitats and, therefore, the region should be considered of high importance for biodiversity conservation of aquatic species.

Located in the Paraguay HR, the Pantanal is considered the largest floodplain in the world (Junk et al., 2006). Nevertheless, information on the biodiversity of its aquatic fauna is incipient and scattered in a few publications, including unpublished academic data (Brandorff et al., 2011). Specifically for cladocerans, only a few studies have been carried out in the Pantanal of Mato Grosso when compared to its southern portion, located in the state of Mato Grosso do Sul (Tab. 2), where 20 studies have already been published (Zanata et al., 2017). In the north of Mato Grosso, where the Amazon HR is located, there are also few studies related to cladoceran fauna. Recently in the upper Xingu Basin, Sousa and Elmoor-Loureiro (2018) described a new genus and new species of the Chydoridae family, which reveals that this region represents high potential for the discovery of new species. Conversely, we unaware of studies that investigate the diversity of cladocerans in the Tocantins-Araguaia HR of Mato Grosso state.

Biogeographers have pointed out two main gaps that jeopardize macroecological studies of biodiversity. The Linnean shortfall concerns the many species there are still unknown to science, while the Wallacean shortfall concerns the problems of the lack of knowledge on species distribution (Lomolino et al., 2010). Thus, in order to reduce the gaps in the knowledge of the group for the state, the aim of this study was to investigate the cladoceran richness and composition (Crustacea, Branchiopoda) in 50 lakes of the Pantanal of Mato Grosso state (Paraguay HR), Brazil. In addition, we sought to compile the information published on cladoceran species in each hydrographic region of the state, in order to digest the knowledge of cladoceran biodiversity and distribution in Brazil.

2 Material and methods

2.1 Collection, sorting and identification of cladocerans

This study was based on two sources, namely literature data and field sample collection. Data from the literature on cladocerans were obtained by searching Google Scholar, Web of Science and Scopus databases and with the help of the specialist Lourdes M. Abdu Elmoor-Loureiro's personal database. We considered only papers that include species lists, excluding monographs, theses and dissertations (and other gray literature).

We also added information on cladocerans that we sampled in 50 lakes distributed across of the Cuiabá river watercourse in the Pantanal region of Mato Grosso. In all lakes, the sampling was performed at a point of the littoral zone with high influence from macrophytes. The samples were obtained by filtering 600 liters of water in a 68 µm plankton net, with the aid of a graduated bucket. The presence of macrophytes in the littoral zone is known to provide greater heterogeneity and availability of niches for organisms, related to higher species richness (Choi et al., 2014; Maloufi et al., 2016). Due to this, the samples were always collected near the macrophyte beds which, in most of the studied lakes, was characterized by the presence of the species Eichhornia azurea (Sw.) Kunth, E. crassipes (Mart.) Solms, Salvinia auriculata Aubl., Ludwigia helminthorrhiza Mart., including other species from the floating group.

Afterwards, samples were preserved in a 4% formaldehyde solution buffered with calcium carbonate. In the laboratory, cladoceran samples were analyzed in a Sedgewick-Rafter chamber and the organisms were identified at the lowest possible taxonomic level by specialized literature (Korovchinsky, 1992; Elmoor-Loureiro, 1997). We performed quantitative analysis by counting a minimum of three subsamples, provided there was a minimum of 50 individuals (Bottrel et al., 1976); if this proportion was not fulfilled, ten subsamples were counted. We counted in full all samples with few individuals.

2.2 Data analyses

The occurrence data of the species obtained by searching the literature and through analyzing the collected samples were used in the elaboration of a list of cladoceran species in each HR from the state of Mato Grosso. Extrapolation sampling curves for the entire state of Mato Grosso (literature data, N = 12), and only for Paraguay HR (N = 50) were performed using Hill numbers through the function “iNEXT” available at iNEXT package. We used q = 0 to estimate species richness (Hsieh et al., 2019). The Hill numbers calculate theoretical species richness; that is, the asymptote in an infinite sample size from a known number of sample units. The maximum extrapolated size was double the reference sample size. This package used Chao2 (for incidence data) to estimate the number of undetected species in the reference sample.

We used a PERMANOVA analysis (“adonis” function) to test for differences in cladoceran assemblages between the two hydrographic regions (Pantanal and Amazon) (Anderson and Walsh, 2013). After that, we also analyzed which HR is more heterogeneous in terms of species composition (i.e. higher beta diversity) through a PERMDISP analysis (Anderson and Walsh, 2013) based on “Jaccard” dissimilarity. We also performed a Principal Coordinate Analysis (PCoA) to visualize the differences and dispersion of studies in the different hydrographic regions. All analyses were performed using the Vegan package (Oksanen et al., 2018) in software R (R Core Team, 2018).

3 Results

Table 1 lists the studies about the cladoceran fauna conducted in the state of Mato Grosso, followed by a numerical identification code and study location. The Paraguay HR was the one that presented the largest number of studies on cladoceran fauna, followed by the Amazon HR. No study was found in the portion of the Tocantins-Araguaia HR located in Mato Grosso (Fig. 1; Tab. 1).

In total, considering all the data obtained from the literature, and the samples collected in the 50 lakes of the Pantanal, 120 cladoceran species are known in Mato Grosso state, distributed in eight families: Bosminidae, Chydoridae, Daphniidae, Ilyocryptidae, Macrothricidae, Moinidae, Holopedidae and Sididae (Tab. 2). The sampling of the 50 Pantanal lakes allowed us to identify 17 species considered new records for Mato Grosso, such as Coronatella paulinae Sousa, Elmoor-Loureiro & Santos, 2015, Dunhevedia crassa King, 1853, D. odontoplax Sars, 1901, D. colombiensis Stingelin, 1913, Nicsmirnovius paggii Sousa & Elmoor-Loureiro, 2017, Pseudochydorus globosus (Baird, 1850), among others (Tab. 2).

The sample-size-based extrapolation curves estimated a higher richness than observed, both for the Paraguay HR and for all of Mato Grosso state (Fig. 2A and B). The estimated richness obtained from twice the known sampling units was 146 for the Paraguay HR and 166 species for Mato Grosso. In other words, considering only the Paraguay HR, the observed richness represented 72.6% of the estimated richness, while all studies performed in the state allowed the estimated knowledge of 72.2% of cladoceran richness.

Species composition did not differ between Paraguay and Amazon HRs (Pseudo-F = 0.77; p = 0.73) but there are differences in the assemblage variability between the two regions (F = 5.8; p = 0.03; Fig. 3). The species that most contributed to the similarity between the two HRs, according to SIMPER analysis, were Macrothrix elegans Sars, 1901 (p = 0.009), Chydorus eurynotus Sars, 1901 (p = 0.02) and Karualona muelleri (Richard, 1897) (p = 0.02).

Table 1

Code of references and localization of studies carried out in the state of Mato Grosso, Brazil.

thumbnail Fig. 1

Map of the state of Mato Grosso, Brazil. Highlight to the division of the territory into hydrographic regions (Amazon, Paraguay and Tocantins-Araguaia) and the approximate location where cladoceran biodiversity studies were conducted (samples collected for this study in the Pantanal, corresponding to only one study, and location of the other studies).
Table 2

List of species of cladocerans, by hydrographic region, from the state of Mato Grosso, Brazil. Numeric codes refer to the study in which the species was cited (see Table 1). *asterisks represent new occurrences for the state.

thumbnail Fig. 2

Sample-size-based rarefaction (solid line) and extrapolation (dashed lines) for Hill numbers (q = 0, species richness) from cladoceran species considering (A) the Paraguay hydrographic region (N = 9) and (B) state of Mato Grosso (N = 13). The 95% confidence intervals were obtained by a bootstrap method.
thumbnail Fig. 3

Dispersion of studies conducted in the state of Mato Grosso obtained through the PCoA (Principal Coordinate Analysis) for each of the hydrographic regions.

4 Discussion

Our study revealed that despite the increase in recent years (i.e. Padovesi-Fonseca et al., 2016; Branco et al., 2018; Elmoor-Loureiro et al., 2018), there are still few studies focused on better understanding the biodiversity of cladocerans in the state of Mato Grosso (Tab. 1). The search allowed us to estimate a total richness of 166 species for the state and 146 for the region of Paraguay. An estimated high richness was already expected, as only thirteen studies were carried out throughout the state and only four in the Amazon HR. Possibly these study numbers were not enough to cover all aquatic ecosystems and access all the cladoceran biodiversity of the region. It is also possible that this result was influenced by the lack of sampling in the Tocantins-Araguaia HR. In this scenario, even with the increase of new records obtained from the collections performed in the Pantanal in this study (Paraguay HR), the rarefaction curve showed no asymptotic tendency for the State (Fig. 2B). Overall, in biodiversity studies, there is no sampling or method capable of accessing the total species richness of an ecosystem and, according to Williams et al., (2007), the adequacy of the inventory is dependent on obtaining more than 50% of the estimated number of species.

Despite being far from reaching the richness estimated, the richness observed for Mato Grosso can still be considered higher than that recorded for other states: Mato Grosso do Sul (101 spp), Minas Gerais (94 spp), São Paulo (84 spp) and Pernambuco (32 spp) (Santos-Wisniewski et al., 2011; Rocha et al., 2011; Soares and Elmoor-Loureiro, 2011; Zanata et al., 2017). Among the registered families, the Chydoridae family presented the highest species richness considering the data analyzed together or only for the Paraguay HR (Tab. 2). This is a relatively common pattern in inventories of cladoceran fauna and is related to the self-ecological characteristics of the species that compose the family (Santos-Wisniewski et al., 2011; Soares and Elmoor-Loureiro, 2011; Zanata et al., 2017). For example, members of the Chydoridae family have reduced swimming capacity, but have specialized appendices for locomotion under substrates and for scraping organic material (Sousa and Elmoor-Loureiro, 2008; Sousa et al., 2017). These characteristics allow this group to present greater abundance and diversity associated with macrophytes in littoral regions (Castilho-Noll et al., 2010) and water bodies with high vegetation cover. The relevance of Chydoridae in this study becomes even more evident when we observe the high number of new records for Mato Grosso (Tab. 2).

However, of all Chydoridae registered for the state, five species found have a delicate taxonomic context and some information should be taken into consideration when analyzing this species list: In Brazil, the only species of the affinis-group is Alona ossiani. Therefore, it is likely that Alona affinis records belong to its Neotropical congeners (Sousa and Elmoor-Loureiro, 2019b). The occurrence of Alona broaensis was also recorded; however, this species was considered by Van Damme et al. (2010) to be a junior synonym of Alona dentifera. After the creation of the genus Magnospina, which includes the dentifera-group, Sousa et al. (2016) confirmed the status suggested by Van Damme et al. (2010) for Alona broaensis. Coronatella rectangula has restricted distribution in the Palearctic region. In the Neotropical region, the name may have been attributed to different species such as C. paulinae, C. undata, C. poppei and C. monacantha or even to Ovalona kaingang (Sousa et al., 2015a, b). Finally, Chydorus sphaericus was cited as a valid species in Elmoor-Loureiro (1997). This species is currently known to have Holarctic distribution (Smirnov, 1996) and records outside this region are related to cryptic diversity. On the other hand, it may represent a biological invasion process, as already described in Australia (Sharma and Kotov, 2014). Both possibilities must be tested in the future.

Similarly to some species of Chydoridae, Ilyocryptus sordidus and Grimaldina brazzai have some indications regarding taxonomic status. The first species also has a Palearctic distribution, and records in Brazil probably belong to Ilyocryptus sarsi (Sousa and Elmoor-Loureiro, 2019a). Recently, the genus Grimaldina, previously considered cosmopolitan, has been revised using material from different continents, including the South American (Neretina and Kotov, 2017). The main result of this work indicates that the G. brazzai species does not occur in the Neotropics and, therefore, the records possibly belong to Grimaldina freyi Nerentina & Kotov, 2017.

The Sididae were also prominent in relation to species richness, considering all studies conducted in the state. A similar result was found by Rocha et al., (2011) in the state of São Paulo. On the other hand, the low richness observed in Moinidae and Daphniidae is related to the fact that they are groups consisting of typically planktonic species, found most predominantly in the pelagic region of aquatic ecosystems (Elmoor-Loureiro, 1997).

The similarity between the regions was marked by the species: Macrothrix elegans, one of the most common anomopod species in the Neotropics (Kotov et al., 2004); Chydorus eurynotus, most frequently observed in vegetated regions (Battauz et al., 2017); and Karualona muelleri, a common species in shallow lakes with low dissolved oxygen (Panarelli et al., 2019). Despite this similarity, the few studies ever conducted for the state showed that the cladoceran community of the Amazon HR can be considered a subset of the Paraguay HR, whose species showed the highest variance (Fig. 3). These results should be evaluated, taking into account the effect of sampling, since there is a large difference in the number of literature studies for each hydrographic region, which is reflected in the species richness (Tabs. 1 and 2). Considering only the four studies found for the Amazon HR, we cannot rule out the possibility of distinct communities in relation to other hydrographic regions, due to the potential for high diversity. For example, a single inventory of a few water bodies in the Upper Xingu Basin revealed a new genus and new species of Chydoridae for the Amazon HR (Sousa and Elmoor-Loureiro, 2018). Therefore, we consider it necessary to carry out further studies in the different hydrographic regions found in Mato Grosso in order to improve the knowledge of cladoceran biodiversity.

Finally, even with the high number of species observed in the Paraguay HR influenced by the sampling of 50 lakes in the Pantanal, we can conclude that the state's aquatic ecosystems are still poorly studied. We therefore suggest a greater sampling effort in the Mato Grosso ecosystems, especially in areas of the Amazon and Tocantins-Araguaia HRs. This sampling should take particular account of the littoral zones of aquatic ecosystems, as such regions are marked by the presence of macrophyte beds, where aquatic invertebrate biodiversity tends to be higher due to increased resource availability (Choi et al., 2014).

Acknowledgements

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior − Brasil (CAPES) − Finance Code 001. We also thank CAPES for a doctoral scholarship awarded to the first author. The authors thank Dr. Lourdes M. A. Elmoor-Loureiro for permission to use the Brazilian Cladocera database and Enezio Francisco and co-workers for help with fieldwork. We thank the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT) for the financial support through Edital N° 037/2016–Redes de Pesquisa em Mato Grosso. VLL is supported by a research fellowship from CNPq, process 307961/2017-6.

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Cite this article as: Brito MTS, Diniz LP, Pozzobom UM, Landeiro VL, Sousa FDR. 2020. Cladocera (Crustacea: Branchiopoda) from the state of Mato Grosso, Brazil. Ann. Limnol. - Int. J. Lim. 56: 7

All Tables

Table 1

Code of references and localization of studies carried out in the state of Mato Grosso, Brazil.

In the text
Table 2

List of species of cladocerans, by hydrographic region, from the state of Mato Grosso, Brazil. Numeric codes refer to the study in which the species was cited (see Table 1). *asterisks represent new occurrences for the state.

In the text

All Figures

thumbnail Fig. 1

Map of the state of Mato Grosso, Brazil. Highlight to the division of the territory into hydrographic regions (Amazon, Paraguay and Tocantins-Araguaia) and the approximate location where cladoceran biodiversity studies were conducted (samples collected for this study in the Pantanal, corresponding to only one study, and location of the other studies).
In the text
thumbnail Fig. 2

Sample-size-based rarefaction (solid line) and extrapolation (dashed lines) for Hill numbers (q = 0, species richness) from cladoceran species considering (A) the Paraguay hydrographic region (N = 9) and (B) state of Mato Grosso (N = 13). The 95% confidence intervals were obtained by a bootstrap method.
In the text
thumbnail Fig. 3

Dispersion of studies conducted in the state of Mato Grosso obtained through the PCoA (Principal Coordinate Analysis) for each of the hydrographic regions.
In the text

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