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All issues Volume 56 (2020) Ann. Limnol. - Int. J. Lim., 56 (2020) 25 Full HTML
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Ann. Limnol. - Int. J. Lim.
Volume 56, 2020
Article Number 25
Number of page(s) 22
DOI https://doi.org/10.1051/limn/2020023
Published online 13 October 2020

© EDP Sciences, 2020

1 Introduction

Assessing the zooplankton species distribution across freshwater ecosystems generates biological (i.e., taxonomic and phylogenetic) and biogeographic information about inland plankton biodiversity, which support studies of management/conservation in lacustrine ecosystems (Yurista et al., 2005; Aranguren-Riaño et al., 2011). Geographic, environmental and biological factors affect the species presence or absence in specific areas and this variation is a crucial aspect to be considered in conservation programs and management plans to avoid generalizations about zooplankton distribution in lentic ecosystems. Additionally, zooplankton species distribution helps us to understand the aquatic food web complexity, the functioning of lacustrine ecosystems (Walseng et al., 2006) and, ultimately, their potential to drive ecosystem service delivery (Winfree et al., 2015; Lohbeck et al., 2016).

The zooplankton in freshwaters consists primarily of heterotrophic protists (e.g., flagellates and ciliates) and metazoans, such as rotifers and crustaceans (e.g., cladocerans and copepods) (Likens, 2010). The zooplankton acts as a strategic functional trophic group in aquatic food webs linking energy and materials from primary producers to upper trophic-level consumers (Suthers and Rissik, 2009; Harris et al., 2000). Due to its high diverse life-forms and fast generation time, zooplankton is also an efficient bioindicator of environmental changes occurring in aquatic systems (Walseng et al., 2006; Dodson et al., 2007). Despite their relevance, there are many gaps in our knowledge about zooplankton species distribution across lentic freshwater ecosystems (Merrix-Jones et al., 2013), especially in tropical ecosystems.

In Brazil, a country recognized as having one of the highest biodiversity of the planet (Myers et al., 2000), most of the studies about microcrustaceans and rotifers biodiversity is from São Paulo, Minas Gerais and Paraná states (Brandorff, 1976; Silva and Matsumura-Tundisi, 2005, 2011; Souza-Soares et al., 2011; Silva and Perbiche-Neves, 2017). Meanwhile, although the number of studies about freshwater ecosystems in the Brazilian Northeast have increased in recent years (Diniz et al., 2020), many of them are still difficult to find and access, being found in grey literature as particular libraries and collections (de Melo Júnior et al., 2007a; Paranhos et al., 2013). The Brazilian Northeast region has a significant number of lakes (Rosenberg et al., 2000; Lazzaro et al., 2003; Moss, 2009) with different geomorphological origins, human uses and it is subjected to an unique climatic and environmental variations that can act as active ecological filters to zooplankton species selection (Crossetti et al., 2008; Arthaud et al., 2012).

This region comprises two main biomes: the Caatinga and Atlantic Forest. The Caatinga biome is located in the semiarid climate, which covers most of Brazil's northeast (912,529 km2) (IBGE, 2004). The term Caatinga refers to “white forest” (Tupi language) that characterizes its predominant vegetation: seasonally dry tropical forest (SDTF) (Prado, 2003; Pennington et al., 2009). The Caatinga biome is used for multiple anthropogenic uses that include urban/developed zones and agriculture areas (cropland and pasture) (Ribeiro et al., 2015). This semiarid area has the highest population density of any dryland in the world (Marengo, 2008; Medeiros et al., 2012) but is the most underdeveloped region in Brazil (Buainain and Garcia, 2013). The majority of the population is poor and dependent on forest resources for subsistence (Gariglio et al., 2010). The Atlantic Forest biome, in contrast, is a hotspot of biodiversity distributed in humid climate along the coastline that extended originally over 1.5 million km2 along the South American Atlantic coast across highly heterogeneous conditions (Myers et al., 2000; Ribeiro et al., 2011). However, as Ribeiro et al. (2011) says, “the forest is now reduced to around 12% of its original extent, including regeneration areas and degraded forests, which are mostly spread in small fragments. As a result, many species are currently threatened to extinction, with populations collapsing on local and regional scales”. The causes of deforestation include pasture, agriculture and urban growth (Dean, 2010).

Especially in the Caatinga biome, where the reliance of local populations on water resources imposes a strong pressure on aquatic systems (Nobre et al., 2020), the climate determines water shortages and the lakes are subjected to detrimental effects of irregular rainfall and high evaporation (Sousa et al., 2008; da Costa et al., 2016). The lakes in this region have suffered by the impacts of increased nutrient concentrations causing eutrophication (Chellappa and Costa, 2003; Costa et al., 2006), which may act as an environmental filter selecting species adapted to eutrophic and hypereutrophic conditions (Crossetti et al., 2008; Arthaud et al., 2012). It is expected the disappearance of small lakes and ponds across dryland areas (e.g., Caatinga biome) around the world due to a higher frequency of extreme droughts in these regions (Pekel et al., 2016). These changes increase the need for constructions of new artificial water bodies as man-made lakes (by damming rivers) to attend the human demands for water, increasing their relative proportion at the landscape (Pekel et al., 2016).

The implementation of man-made lakes, also known as reservoirs, occurred recently (∼50–100 years) in northeast Brazil usually to fulfill a variety of human needs (e.g., recreation, hydroelectricity production, waste disposal, drinking water, and irrigation) (Rosenberg et al., 2000; Lazzaro et al., 2003; Havel et al., 2005; Moss, 2009), while natural lakes are ancient ecosystems formed by natural geomorphological processes (Havel et al., 2005; Dodson et al., 2007). The origin type (e.g., age and basin morphology) and hydrodynamic changes (e.g., hydrological processes and human use) that occurred throughout the history of the natural and man-made lakes have subjected their biological communities to different processes of adaptive selection (Albrecht and Wilke, 2008) influencing the zooplankton distribution (Pinto-Coelho et al., 2005; Simões et al., 2015; Cabral et al., 2019).

The horizontal compartmentalization of lake habitats, which creates distinct environmental conditions within a single ecosystem, is an additional factor capable of affecting zooplankton distribution. In comparison with the littoral habitat, the limnetic habitat is usually deeper with possible vertical stratification of the physicochemical variables. At the littoral habitat solar radiation reaches the substrate, and consequently promotes the dominance of submerged macrophytes and the colonization of terrestrial animals (Naiman and Décamps, 1990; Esteves and Caliman, 2011; Vadeboncoeur et al., 2002). Although there are considerable differences between limnetic and littoral habitats, historically limnological studies focus their efforts primarily on the limnetic ones (Schindler and Scheuerell, 2002; Vadeboncoeur et al., 2002), disregarding the possible role of the littoral region as an environmental filter on species selection.

In general, lakes in northeastern Brazil are vulnerable due to intensified anthropic influence, such as the severe loss and destruction of the surrounding habitat (i.e., Caatinga and Atlantic Forest biomes − da Silva et al., 2017; Nobre et al., 2020), the high eutrophication rates (Chellappa and Costa, 2003; Costa et al., 2006), and exotic species introduction for fish farming (Silva et al., 2014). The coupled effect of these factors has impacted many lakes, and in some cases, the ecosystems have disappeared even before we know their biodiversity (Pekel et al., 2016).

Recognizing the lacustrine vulnerability of Brazilian northeast, the zooplankton importance to aquatic ecosystems and the lack of consistent information about the tropical zooplankton species distribution, particularly to Brazilian northeast region, we conducted a freshwater zooplankton survey in northeastern Brazil. We sampled and identified the zooplankton from 180 tropical shallow lakes considering the main lacustrine zooplankton groups Rotifera, Copepoda, and Cladocera. The purpose of our study was to provide an updated species list of freshwater zooplankton from lakes in northeastern Brazil, classifies the species according to their frequency of distribution, and compare patterns of frequency, species richness and community composition considering different biomes (i.e., Caatinga vs Atlantic Forest), origin of lakes (i.e., natural vs. man-made lakes), and lake habitat (i.e., pelagic vs. littoral). This study can, therefore, allow us to assess whether and how some environmental factors that describe landscape at the regional level (i.e., biome) and ecosystems at the local level (i.e., lake origin and lake habitat) affect the zooplankton community structure. We conducted the largest freshwater zooplankton survey in northeastern Brazil with the highest number of sampled lakes distributed over a large spatial scale.

2 Material and methods

2.1 Study area

We used zooplankton samples from 180 tropical natural and man-made shallow lakes (depth <4 m) located across the states of Rio Grande do Norte (n = 99) and Pernambuco (n = 81), both in northeastern Brazil (Fig. 1). The lakes are distributed across 27 hydrographic basins (16 into the Rio Grande do Norte and 11 in Pernambuco), in two distinct biomes. The Caatinga biome is situated to the west of the Brazilian Atlantic Forest and occupies a larger area of Rio Grande do Norte and Pernambuco, presenting a semiarid climatic subdomain (annual precipitation ≈400–800 mm). The Brazilian Atlantic Forest is located along the eastern Atlantic Ocean coast with a tropical humid and semi-humid tropical climatic subdomain (annual precipitation ≈800–1200 mm) (Diniz and Pereira, 2015; INMET, 2015). The lakes' distribution occupies a total area of 115,000 km2, being 36,000 km2 in Rio Grande do Norte and 79,000 km2 in Pernambuco.

To classify the ecosystems in biomes types, we analyzed the coverage area of the Brazilian Atlantic forest for tropical humid climate and Caatinga biome for the tropical semiarid climate (SUDENE, 2017). To verify the ecosystems' origin, we check for the presence of artificial dams. The sampled man-made lakes consisted of systems formed by stream damming, constructed from 1915 by the National Department of Works for Drought Control (DNOCS, 2015), or in some cases, the man-made lakes were built by the local population in the last century (Cabral et al., 2019). They were built to store water so that there is no water outflows unless the water level rises above the dam. These man-made lakes show low outflow and high water residence time associated with a negative hydric balance and high temperatures during most of the hydrological cycle (Barbosa et al., 2012). They are generally surrounded by shallow and low-permeable soils, which prevent groundwater accumulation (Junger et al., 2019). The sampled natural lakes are mostly coastal systems originating from the tertiary period with subsequent quaternary sediment deposition, and are mainly surrounded by sandy soils, and primarily supplied by groundwater (Esteves et al., 2008).

thumbnail Fig. 1

Map of the study area showing the 180 natural and man-made shallow lakes distributed across the states of Rio Grande do Norte and Pernambuco, in northeast Brazil. The grayscale on the map indicates the transition between the Atlantic Forest (on the right) and Caatinga biome (on the left)

2.2 Sampling procedures and analysis

The sampled natural and man-made shallow lakes were not stratified. Therefore, water samples for zooplankton and physical and chemical analysis were collected from the subsurface (approximately 0.3-m deep) portion of the water column with a transparent Van Dorn bottle (capacity = 3 L) during the diurnal photoperiod. The zooplankton from Rio Grande do Norte and Pernambuco was sampled, respectively, during 2012 and 2016 at six different spots in each ecosystem. Three sampling spots were randomly positioned near the shore of the littoral region, and the other three were taken from pelagic habitats (i.e., limnetic), near to the central portion of the water body.

Zooplankton samplings were performed by filtering a known volume of water (30–200 L varying according to suspended particles in the water) from the bucket through a plankton net (45 or 50-μm mesh, used in Pernambuco and Rio Grande do Norte, respectively). The samples were rapidly fixed with a sugar formaldehyde solution (4% final concentration) and stored in 150-ml glass flasks. Zooplankton individuals (Rotifera, Copepoda, and Cladocera) were identified to the species level using a Sedgewick-Rafter camera and microscope (for Rotifera), a Bogorov camera and a stereo microscope (for Copepoda and Cladocera), and specific taxonomic guides (e.g., Koste, 1978; Reid, 1985; Matsumura-Tundisi, 1986; Elmoor-Loureiro, 1997; Santos-Silva, 2000; Perbiche-Neves et al., 2015). Identification was performed on three replicates per sample with at least 100 individuals of the most abundant organisms in each. The samples have been thoroughly evaluated to search for rare species. For 132 lakes, we identified the Rotifera, Cladocera, and Copepoda at the taxonomic level of species, while for the other 48 lakes (all of them in Pernambuco), we identified just a particular taxonomic group. In this case, we assessed the composition of Rotifera in these 48 lakes and Cladocera in 22 of these lakes. The zooplankton collections used in our study are in two central institutions: Department of Ecology − Federal University of Rio Grande do Norte, Natal / RN, and Department of Biology − Federal Rural University of Pernambuco, in Recife / PE.

We estimated the frequency of occurrence (FO) based on the species distribution in each lake set (i.e., biome, origin, and habitat type), being Oc = the number of lakes that the species occurs, and TS = total lakes sampled. We classify species as “frequent” when FO > 40%, “accessory” FO = 10–40%, and “accidental” FO <10%. We performed sample-based rarefaction curves to compare the species richness by biome, lake origin and habitat type (Gotelli and Colwell, 2001) and the 95% confidence interval was estimated by the bootstrap method with 100 replications (Chao and Jost, 2012). We conducted permutational multivariate analysis of variance (PERMANOVA − Anderson, 2001) based on the Jaccard index with 999 permutations to test whether biomes (Caatinga and Atlantic Forest), lake origin (natural and man-made lakes) and habitat type (pelagic and littoral) differed in species composition, and a principal coordinate analysis (PCoA) to assist visualizing the multivariate structure of the data considering these studied categories. Characteristic and distinguishing species between lake groups were determined by similarity percentages procedure (SIMPER − Clarke 1993) performed on presence/ absence data. Species were only listed if they accounted for at least 70% of the overall dissimilarity between lake groups.

The analyses were carried out in R 3.1.3 (R Core Team, 2015). Sample-based rarefaction curves were performed using the iNEXT package (Hsieh et al., 2016). PERMANOVA and SIMPER were calculated using the vegan package (Oksanen et al., 2015) and PCoA using vegan and ape packages (Paradis, 2012).

3 Results

3.1 Zooplankton species list and distribution

We recorded 227 zooplankton species, being 137 Rotifera, 65 Cladocera and 25 Copepoda (Cyclopoida = 21; Calanoida = 4) (Tab. 1). According to the frequency of occurrence, only 4% of the zooplankton species were considered “frequent” (FO > 40%), 21% were classified as “accessory” (FO 10–40%), and about 75% as “accidental” (FO < 10%).

The small cladoceran Ceriodaphna cornuta Sars, 1985 was the most common species (FO = 50.7%) of the zooplankton community considering all sampled lakes. C. cornuta was followed in the frequency of occurrence by the rotifers Brachionus havanaensis Rousselet, 1911 (FO = 49%) and Lecane bulla (Gosse, 1851) (FO = 45.1%). Among the copepods, Termocyclops decipiens (Kiefer, 1929) was the most common (FO = 40.9%), occupying the eighth place in the list of most frequent species (Tab. 1).

Table 1

Checklist and frequency of occurrence (%) of freshwater zooplankton (Copepoda, Cladocera, and Rotifera) from 180 Brazilian tropical shallow lakes located in the states of Rio Grande do Norte (n = 99) and Pernambuco (n = 81) by biome (Atlantic Forest n = 29; Caatinga n = 98), lake origin (Natural lake n = 45; Reservoirs n = 82), and lake habitat (Pelagic n = 127; Littoral n = 127) (TN = number of occurrences).

3.2 Zooplankton community by biome, lake origin and habitat type

The five most common zooplankton species in the Atlantic Forest are the rotifers L. bulla (FO = 62%), Anthalona verrucosa (Sars, 1901) (FO = 55%), Keratella americana Carlin, 1943 and Lecane lunares (Ehrenberg, 1832) (both, FO = 54%), and the copepod Microcyclops anceps (Richard, 1987) (FO = 55%) (Tab. 1). While in the Caatinga biome are the cladoceran C. cornuta (FO = 53%), the rotifers Brachionus plicatilis Muller, 1786 (FO = 48%), B. havanaensis (FO = 47%), Brachionus falcatus Zacharias, 1898 (FO = 43,7%), and the copepod T. decipiens (FO = 46%) (Tab. 1).

The rarefaction curves showed that Atlantic Forest and Caatinga biomes had proportionally similar species richness for all zooplanktonic groups (Figs. 2A, 2D and 2G). Whereas, the zooplankton community composition between the biomes were statistically different for rotifers (Fig. 3A), copepods (Fig. 3D) and cladocerans (Fig. 3G) (Tab. 2). The SIMPER analysis for the species composition in Atlantic Forest and Caatinga revealed that 28 Rotifera, 5 Copepoda and 13 Cladocera species accounted for about 70% dissimilarity between the two biomes (Tab. 3). The most important zooplankton species that discriminated between biomes were e.g. the rotifers Lecane lunaris (Ehrenberg, 1832), Keratella americana, Lecane stichaea Harring, 1913, the copepods Microcylops anceps and Notodiaptomus nordestinus (Wright S., 1935), the cladocerans Bosmina hagmanni Stingelin, 1904, Chydorus pubescens Sars, 1901 and Ilyocryptus spinifer Herrick, 1882 (typical for Atlantic Forest). The rotifer Brachionus plicatilis was typical for the Caatinga biome (Tab. 3).

Considering the classification of lakes sampled by their origin, the five most common zooplankton species in the natural lakes are the rotifers Lecane bulla (FO = 63%), Lecane stichaea (FO = 52%), Polyarthra vulgaris Calin, 1943 (FO = 50%), Lecane lunaris (FO = 46%), and the cladoceran Anthalona verrucosa (FO = 53%) (Tab. 1). While in the man-made lakes, the common species are the cladocerans Ceriodaphnia cornuta (FO = 57%) and Diaphanosoma spinulosum Herbst, 1975 (FO = 50%), the copepod Termocyclops decipiens (FO = 55%), the rotifers Brachionus havanensis (FO = 52%) and Brachionus falcatus (FO = 46%) (Tab. 1).

The rarefaction curves showed that natural lakes had proportionally more Cladocera species than man-made lakes (Fig. 2H) and similar species richness for Rotifera (Fig. 2B) and Copepoda (Fig. 2E). Considering the zooplankton community composition, differences between natural and man-made lakes were observed for rotifers (Fig. 3B), copepods (Fig. 3E) and cladocerans (Fig. 3H) (Tab. 2). Similar to biomes results, the SIMPER analysis revealed that 28 Rotifera, 5 Copepoda and 13 Cladocera species accounted for about 70% composition dissimilarity between natural and man-made lakes (Tab. 3). The zooplanktonic species that most contributed to distinguish the lakes by their origin were e.g. the rotifers Lecane bulla, Lecane stichaea, Lecane lunaris, the copepod Notodiaptomus nordestinus, the cladocerans Latonopsis australis Sars, 1888, Chydorus pubescens, Ephemeroporus hybridus (Daday, 1905) (typical for natural lakes). The copepod Thermocyclops decipiens was typical for man-made lakes (Tab. 3).

Analyzing the zooplankton community by habitat type, the five most common zooplankton species in the littoral are the cladoceran C. cornuta (FO = 44%), Anthalona verrucosa (FO = 39%) and Diaphanosoma spinulosum (FO = 36%), the rotifers Lecane bulla (FO = 40%) and Brachionus falcatus (FO = 37%) (Tab. 1). While in the pelagic habitat are the rotifers Brachionus havanaensis and Filinia longiseta (Ehrenberg, 1834) (both, FO = 43%), Brachionus plicatilis (FO = 41%), the copepod Termocyclops decipiens (FO = 38%) and the cladoceran Ceriodaphnia cornuta (FO = 36%) (Tab. 1).

The rarefaction curves showed that littoral habitat had proportionally more Rotifera (Fig. 2C) and Cladocera species (Fig. 2I), with the composition of their communities being different for the littoral and pelagic habitats (rotifers Fig. 3C; cladocerans Figs. 3I) (Tab. 2). These patterns were not observed for Copepoda (Fig. 2F and 3F) (Tab. 2). Among the species that contributed to differentiate communities between habitats, the SIMPER analysis revealed that 27 Rotifera, 4 Copepoda and 12 Cladocera species accounted for about 70% composition dissimilarity between littoral and pelagic habitats (Tab. 3). These species were e.g. the cladocerans Ceriodaphnia cornuta, Diaphanosoma spinulosum and Anthalona verrucosa (typical for littoral habitat). Also, the rotifers Filinia longiseta, Hexarthra intermedia (Wiszniewski, 1929), Polyarthra vulgaris, the cladocerans Moina minuta Hansen, 1899 and Bosmina hagmanni (typical for pelagic habitat) (Tab. 3).

thumbnail Fig. 2

Sample-based rarefaction curves for Rotifera (first line − A, B, C), Copepoda (second line − D, E, F) and Cladocera (third line − G, H, I) by biomes: Atlantic Forest and Caatinga (first column − A, D, G), lake origin: natural lakes and man-made lakes (second column − B, E, H), and habitat type: pelagic and littoral (third column − C, F, I). The curves are showing the average (solid lines) and extrapolation (dashed lines) accumulated zooplankton species richness with their ± 95% confidence intervals (shaded areas).
thumbnail Fig. 3

Ordination diagrams of Principal Coordination Analysis (PCoA) for Rotifera (first line − A, B, C), Copepoda (second line − D, E, F) and Cladocera (third line − G, H, I) by biomes: Atlantic Forest and Caatinga (first column − A, D, G), lake origin: natural lakes and man-made lakes (second column − B, E, H), and habitat type: pelagic and littoral (third column − C, F, I).
Table 2

List of zooplankton species in typifying the lakes groups by SIMPER analysis performed on presence/ absence data (bold p-values = significance p < 0,05). Cut off for low contributions: 70%.

Table 3

PERMANOVA table (summary) of the effect of biome, lake origin and lake habitat on the Rotifera, Copepoda and Cladocera communities.

4 Discussion

We provide here an updated species list of freshwater zooplankton from 180 shallow lakes in northeastern Brazil. Also, we performed the first sampling in a large number of lakes through significant environmental filters: biome, the origin of ecosystems, and habitat type. The patterns of species richness and zooplankton composition varied according to the zooplankton group and the subset of lakes. These responses reinforce that Rotifera, Copepoda and Cladocera respond in different ways to the landscape features that limnological conditions imposed, for example, to the type of biome that the lakes are inserted in, whether these ecosystems have a natural or man-made origin and within a single lake if we consider the differences between pelagic and littoral habitats.

Analyzing the species richness for all lakes, we observed that Rotifera had the highest species richness among the zooplankton taxa, a typical pattern in tropical freshwater ecosystems as lakes, reservoirs, tanks, and rivers, including the Brazilian ones (Maia-Barbosa et al., 2014; Moretto, 2001). The rotifers consume a variety of phytoplankton species, debris and bacteria (Souza-Soares et al., 2011), present high dispersion capacity (Fernández-Rosado and Lucena, 2001; Koste, 1978), have opportunistic life history with parthenogenetic reproduction (Maia-Barbosa et al., 2014), and produce resting eggs that constitute an adaptation against environmental adversities (Gilbert, 1974; Ricci, 2001), such as the frequent drought periods that occur in the Brazilian northeast region (Finan and Nelson, 2001; Lazzaro et al., 2003). Also, many rotifer species are adapted to productive ecosystems (Sampaio et al., 2002; Malveira et al., 2011) and the most freshwater ecosystems sampled in our study presents high nutrient levels (i.e., nitrogen, phosphorus, and chlorophyll-a) associated with the eutrophication process (see details in Cabral et al., 2019). Although Cladocera also produces resting eggs, fewer species of cladocerans are adapted to eutrophic and hypereutrophic conditions (Sendacz et al., 2006; Nogueira et al., 2008; Parra et al., 2009) contributing to the rotifer species dominance.

Although the rotifers showed the highest species richness, the small cladoceran Ceriodaphna cornuta was the most common species of the zooplankton community. This species is recognized for being widely distributed and considered as a “frequent” specie in Brazilian freshwater ecosystems (Elmoor-Loureiro, 2000; Sampaio et al., 2002; Maia-Barbosa and Bozelli, 2006) usually in meso/eutrophic waters (Sampaio et al., 2002). C. cornuta was followed in the frequency of occurrence list by the rotifers Brachionus havanaensis and Lecane bulla. B. havanaensis is described as a common planktonic rotifer in Brazilian lakes (Souza-Soares et al., 2011; Keppeler et al., 2018) and eutrophic ecosystems (Alva-Martínez et al., 2009; Arruda et al., 2017) as most of our sampled lakes (Cabral et al., 2019). Whereas, L. bulla, a cosmopolitan non-planktonic species, is classified as a typical littoral organism with the highest occurrence associated with the macrophyte zone in Brazil (Bonecker et al., 1998; Lucinda et al., 2004), which was present in the littoral habitats sampled in our study. The families Brachionidae and Lecanidae were responsible for about 53% of the rotifers species recorded in our study, which are considered the main ones in South America (Rocha et al., 1995; Segers, 2001).

Among copepods, Termocyclops decipiens was the most common. It is considered a dominant planktonic cyclopoid from the tropics (Lévêque et al., 2005), especially in disturbed and nutrient-enriched environments (Sampaio et al., 2002). However, only T. decipiens was considered “frequent” (FO > 40%), contrasting with 76% of the other Cyclopoids species classified as “accidental” (FO < 10–40%). Our results confirm the current premise that most of the Cyclopoida species have a restricted geographic distribution (Silva and Matsumura-Tundisi, 2005; Silva, 2008), despite the paradigm on Cyclopoida cosmopolitanism. Comparing the copepods orders, we observed that 84% are Cyclopoida, and only 16% are Calanoida, confirming that Cyclopoida is the most abundant Copepoda order in freshwater ecosystems (Huys and Boxshall, 1991; Santos-Wisniewski and Rocha, 2007). Usually, Cyclopoida copepods are associated with small-sized consumers (e.g., rotifers and small cladocerans) characterizing a detrital food-chain in eutrophic systems − as the most lakes sampled in our study (Cabral et al., 2019) − dominated for microphytoplankton, bacteria, and colonial algae (Bays and Crisman, 1983; Sampaio et al., 2002).

In general, we observed that the total of zooplankton species found in our study was lower when compared to other Brazilian regions (Neves et al., 2003, Aoyagui and Bonecker, 2004; Eskinazi-Sant'anna et al., 2005; Souza-Soares et al., 2011). However, the species record per region is generally related to the number of specialists researchers in each area, which makes it difficult, or even impossible, to compare results among regions (Silva 2008; Diniz et al., 2020). We know that there is a traditional discrepancy between knowledge about biodiversity in northeastern Brazil when compared to other Brazilian regions, especially from Caatinga biome and semiarid climate (Silva and Perbiche-Neves, 2017; Barros et al., 2020). The high “accidental” species percentage (75%) shows that a significant subset of the zooplankton community is considered unique for a specific ecosystem (Melo Júnior et al., 2007b), reinforcing the role of these lakes as enriching Brazilian aquatic biodiversity.

When we analyzed the frequency of species, we recorded a variation in the frequency of species according to biome, the origin of ecosystems, and habitat type. However, we observed a relative overlap of the most common species between the sets of biome and lake origin: Caatinga biome with, mainly, man-made lakes, and Atlantic Forest biome with, mainly, natural lakes (Tab. 1). We also observed this pattern of overlap when analyzing the species that contributed to the zooplankton composition dissimilarity between biomes and the origin of the lake (Tab. 3).

Indeed, most of the natural lakes are in the coastal area of northeastern Brazil across the Atlantic Forest biome, a humid climate region. The occurrence of natural lakes in the Caatinga biome (i.e., semiarid climate) is rare, prevailing the man-made lakes incidence (Cabral et al., 2019; Junger et al., 2019; Nobre et al., 2020). Also, the most common species in the Atlantic Forest biome and natural lakes are bioindicators of aquatic vegetation, as the Lecanidae rotifers (Bonecker et al., 1998; Lucinda et al., 2004) and the phytophilous cladoceran Anthalona verrucosa (Elmoor-Loureiro, 2007). The same was observed for the characteristic species (Tab. 3), like Chydorus pubescens and Ilyocryptus spinifer, both commonly found in dense vegetation (Moreira et al., 2016; Paranaguá et al., 2005). Although the abundance and identity of macrophytes were not quantified, our study recorded the presence and absence of aquatic vegetation. We found that 100% of the natural lakes sampled had submerged macrophytes, favoring the frequency of occurrence of zooplankton species commonly associated with vegetation in natural lakes.

Whereas, the most frequent and characteristic species in Caatinga biome and man-made lakes are recognized as bioindicators of eutrophication process (e.g., T. decipiens, Brachionus plicatilis, Brachionus rubens (Muller, 1786), Diaphanosoma spinulosum, Keratella tropica (Apstein, 1907), Filinia longiseta − Eskinazi-Sant'Anna et al., 2007; Sousa et al., 2008; Kostopoulou et al., 2012). The broad species distribution recognized to be tolerant to seasonal droughts, productive ecosystems and cyanobacteria indicate the high trophic state and low water quality of the most man-made lakes from Caatinga (Cabral et al., 2019).

Although the Caatinga has been historically neglected in biodiversity studies − even presenting an erroneous reputation as poor in species richness (Vanzolini et al., 1980; Andrade-Lima, 1982; Whitmore and Prance, 1987; Paiva and Campos, 1995) − we observed here that the Caatinga and Atlantic Forest biomes had similar species richness for Rotifera, Copepoda and Cladocera. In fact, there are fewer biodiversity studies carried out in the Caatinga when compared to other Brazilian biomes (Silva and Perbiche-Neves, 2017; Barros et al., 2020). The majority of the Caatinga biome has never been investigated or remains sub-sampled (Tabarelli and Vicente, 2004; de Albuquerque et al., 2012), especially for invertebrates groups (Silva and Perbiche-Neves 2017; Diniz et al., 2020). It is also important to note that the Rotifera, Copepoda and Cladocera composition differed between the lakes from Caatinga and the Atlantic Forest biome. This shows that, despite being microscopic organisms and easily dispersed, zooplankton groups respond differently to the environmental filter created by both biomes.

We observed that the species richness was higher in natural lakes than in man-made ones for Cladocera. As the majority of man-made lakes sampled here suffered with the impacts of increasing nutrient concentrations causing eutrophication (Cabral et al., 2019; Nobre et al., 2020), which may act as an environmental filter selecting species that are adapted to eutrophic and hypereutrophic conditions, this may have contributed for the decrease of Cladocera richness (Crossetti et al., 2008; Arthaud et al., 2012) since the most of cladocerans are not adapted to eutrophic and hypereutrophic ecosystems (Nogueira et al., 2008; Sendacz et al., 2006; Parra et al., 2009). Also, all natural lakes sampled in our study present submerged macrophytes and most of the 26% of exclusive species recorded for natural lakes are typical of environments dominated by macrophytes, such as the Chydoridae and Macrothricidae families (Debastiani-Júnior et al., 2016; Sousa and Elmoor-Loureiro 2008).

Considering the habitat type, we recorded differences in the composition of rotifer and cladoceran communities between the littoral and pelagic habitats, with higher species richness of these groups in the littoral zone confirming the role of this habitat as an environmental filter of species selection and promoter of local species richness. Littoral habitat is recognized as being more structurally complex than the pelagic ones, mainly due to the macrophytes diversity and abundance (Taniguchi et al., 2003; Thomaz et al., 2008). This characteristic affects the coexistence, competition, and predation among the zooplankton species that live in association with the primary producers (Nogueira et al., 2003; Cabral, 2015). We observed that the cladocerans families Chydoridae, Macrothricidae, and Ilyocriptidae were more frequent at the littoral habitat. Chydoridae and Macrothricidae are typically substrate scraper feeders and usually occur in freshwater ecosystems dominated by submerged macrophytes (Elmoor-Loureiro, 2007), a regular pattern in the littoral habitat sampled in our study. Moreover, cladocerans filter feeders from the planktonic community as Moina minuta and Diaphanosoma spinulosum were also found with high FO% in the littoral habitat (Elmoor-Loureiro, 2007).

In our study, most of the sampled lakes had submerged macrophytes in the littoral habitat. Also, all of our zooplankton samples were obtained during the light photoperiod. It is possible that both factors may have contributed to an increase in species richness in the littoral habitat and an underestimation of species richness in the pelagic ones. Since some zooplanktonic species protect themselves among littoral aquatic vegetation against visual predation of planktivorous fish during diurnal photoperiod (i.e., diel horizontal migration (DHM) − Burks et al., 2002). Although we believe that such aspects do not invalidate our results, we emphasize that the patterns described in our study were generated from data obtained with a time-standardized sampling strategy considering only the daylight hours. Besides, DHM is very associated with the presence of pelagic predators. However, in most tropical lakes, a large number and diversity of small fish − which are predators of zooplankton − also seek refuge from their predators in the vegetation of the littoral habitat (Meerhoff et al., 2007; Arcifa et al., 2013, 2016). Thus, the horizontal migration towards the coastal region during the day in these lakes does not bring the same benefit to the zooplankton described for high latitude lakes. The horizontal distribution pattern and the possible effects of collecting during complete 24-hour cycles may be better clarified in future studies that incorporate nocturnal photoperiod into their sampling strategies.

Finally, the checklist provides essential information on zooplankton biodiversity. In northeastern Brazil, where extensive spatial surveys on the distribution of invertebrate biodiversity in aquatic ecosystems are scarce, local managers and scientific researchers have now a starting point for environmental, ecological and monitoring studies. Additionally, we demonstrated that conservation programs and management plans cannot make generalizations about zooplankton distribution across lakes from different biomes, origins and even within a single lake, between the pelagic and littoral zones.

Conflict of interest

The authors declare no conflicts of interest.

Acknowledgements

This study was supported by grants provided by the Brazilian National Council for Scientific and Technological Development (CNPq—www.cnpq.br) through the Universal Grant (Process 477637/2011-6) to LSC, and by the Foundation of Science and Technology of the State of Pernambuco (FACEPE—www.facepe.br; grants APQ-0664-2.05/10 and APQ-1268-2.05/12) to MMJr. CRC is thankful to Coordination for the Improvement of Higher Education (CAPES—www.capes.gov.br) for the concession of Ph.D. scholarship and LPD (Process 141914/2017-3) and AJS thank CNPq for the concession of Ph.D scholarships. AC gratefully acknowledges continuous funding through Research Productivity Grants provided by CNPq (Process 304621/2015-3).

References

  • Albrecht C, Wilke T. 2008. Ancient Lake Ohrid: biodiversity and evolution. Hydrobiologia 615: 103. [Google Scholar]
  • Alva-Martínez AF, Fernández R, Sarma SSS, Nandini S. 2009. Effect of mixed toxic diets (Microcystis and Chlorella) on the rotifers Brachionus calyciflorus and Brachionus havanaensis cultured alone and together. Limnologica 39: 302–305. [Google Scholar]
  • Anderson MJ. 2001. A new method for non‐parametric multivariate analysis of variance. Austral Ecol 26: 32–46. [Google Scholar]
  • Andrade-Lima D. de. 1982. Present-day forest refuges in northeastern Brazil. In: Prance, G. (Ed.), Biological Diversification in the Tropics. New York: Columbia University Press, p. 251. [Google Scholar]
  • Aoyagui ASM, Bonecker CC. 2004. The art status of rotifer studies in natural environments of South America: floodplains. Acta Sci Biol Sci 26: 385–406. [Google Scholar]
  • Aranguren-Riaño N, Guisande C, Ospina R. 2011. Factors controlling crustacean zooplankton species richness in Neotropical lakes. J Plankton Res 33: 1295–1303. [Google Scholar]
  • Arcifa MS, Bunioto TC, Perticarrari A, Minto WJ. 2013. Diel horizontal distribution of microcrustaceans and predators throughout a year in a shallow neotropical lake. Br J Biol 73: 103–114. [CrossRef] [Google Scholar]
  • Arcifa MS, Perticarrari A, Bunioto TC, Domingos AR, Minto WJ. 2016. Microcrustaceans and predators: diel migration in a tropical lake and comparison with shallow warm lakes. Limnetica 35: 281–296. [Google Scholar]
  • Arruda G de A, Diniz LP, Almeida VL dos S, Neumann-Leitão S, de Melo Júnior M. 2017. Rotifer community structure in fish-farming systems associated with a Neotropical semiarid reservoir in north-eastern Brazil. Aquac Res 48: 4910–4922. [Google Scholar]
  • Arthaud F, Vallod D, Robin J, Bornette G. 2012. Eutrophication and drought disturbance shape functional diversity and life-history traits of aquatic plants in shallow lakes. Aquat Sci 74: 471–481. [Google Scholar]
  • Barbosa JE de L, Medeiros ESF, Brasil J, Cordeiro R da S, Crispim MCB, da Silva GHG. 2012. Aquatic systems in semi-arid Brazil: limnology and management. Acta Limnol Bras 24: 103–118. [CrossRef] [Google Scholar]
  • Bays JS, Crisman TL. 1983. Zooplankton and Trophic State Relationships in Florida Lakes. Can J Fish Aquat Sci 40: 1813–1819. [Google Scholar]
  • Bonecker C, Lansac-Tôha FA, Rossa DC. 1998. Planktonic and non-planktonic rotifers in two environments of the Upper Paraná River floodplain, state of Mato Grosso do Sul, Brazil. Braz Arch Biol Technol 41: 447–456. [CrossRef] [Google Scholar]
  • Brandorff GO. 1976. The geographic distribution of the Diaptomidae in South America (Crustacea, Copepoda). Rev Bras Biol 36: 613–627. [Google Scholar]
  • Buainain AM, Garcia JR. 2013. Pobreza rural e desenvolvimento do semiárido nordestino: resistência, reprodução e transformação. In: M. C and T. B (eds), A nova cara da pobreza rural: desenvolvimento e a questão regional. Brasília: Instituto Interamericano de Cooperação para a Agricultura, 217–305. [Google Scholar]
  • Burks RL, Lodge DM, Jeppensen E, Lauridsen TL. 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshw Biol 47: 343–365. [Google Scholar]
  • Cabral CR. 2015. Padrões de diversidade α (alfa) e β (beta) zooplanctônica em lagos tropicais: a importância da estrutura do habitat e da identidade das espécies. Universidade Federal do Rio Grande do Norte. Phd Thesis, 124 p. [Google Scholar]
  • Cabral CR, Guariento RD, Ferreira FC, Amado AM, Nobre RLG, Carneiro LS, Caliman A. 2019. Are the patterns of zooplankton community structure different between lakes and reservoirs? A local and regional assessment across tropical ecosystems. Aquat Ecol 54: 1–12. [Google Scholar]
  • Chao A, Jost L. 2012. Coverage‐based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93: 2533–2547. [CrossRef] [PubMed] [Google Scholar]
  • Chellappa NT, Costa MAM. 2003. Dominant and co-existing species of Cyanobacteria from a Eutrophicated reservoir of Rio Grande do Norte State, Brazil. Acta Oecolog 24: S3–S10. [CrossRef] [Google Scholar]
  • Clarke KR. 1993. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117–143. [CrossRef] [Google Scholar]
  • Costa IAS, Azevedo SMF, Senna PAC, Bernardo RR, Costa SM, Chellappa NT. 2006. Occurrence of toxin-producing cyanobacteria blooms in a Brazilian semiarid reservoir. Braz J Biol 66: 211–219. [Google Scholar]
  • Crossetti LO, Bicudo D. de C, Bicudo CE de M, Bini LM. 2008. Phytoplankton biodiversity changes in a shallow tropical reservoir during the hypertrophication process. Braz J Biol 68: 1061–1067. [Google Scholar]
  • da Costa MRA, Attayde JL, Becker V. 2016. Effects of water level reduction on the dynamics of phytoplankton functional groups in tropical semi-arid shallow lakes. Hydrobiologia 778: 75–89. [Google Scholar]
  • da Silva JMC, Leal IR, Tabarelli M. 2017. Caatinga: the largest tropical dry forest region in South America. Cham: Springer, 506 p. [Google Scholar]
  • de Albuquerque UP, de Lima Araújo E, El-Deir ACA, de Lima ALA, Souto A, Bezerra BM, Ferraz EMN, Maria Xavier Freire E, Sampaio EV de SB, Las-Casas FMG. 2012. Caatinga revisited: ecology and conservation of an important seasonal dry forest. Sci World J 18. [Google Scholar]
  • Dean W. 2010. A Ferro e Fogo: A História e a Devastação da Mata Atlântica Brasileira. São Paulo: Companhia das Letras, 484 p. [Google Scholar]
  • Debastiani-Júnior JR, Elmoor-Loureiro LMA, Nogueira MG. 2016. Habitat architecture influencing microcrustaceans composition: a case study on freshwater Cladocera (Crustacea Branchiopoda). Br J Biol 76: 93–100. [CrossRef] [Google Scholar]
  • Diniz LP, Morais Júnior CS de, Medeiros ILS, Silva AJ da, Araújo AP, Silva TA, Melo Júnior M de. 2020. Distribution of planktonic microcrustaceans (Cladocera and Copepoda) in lentic and lotic environments from the semiarid region in northeastern Brazil. Iheringia. Série Zoologia 110. [Google Scholar]
  • Diniz MTM, Pereira VHC. 2015. Climatologia do estado do Rio Grande do Norte, Brasil: Sistemas atmosféricos atuantes e mapeamento de tipos de clima. Bol Goiano Geogr 35: 488–506. [Google Scholar]
  • DNOCS. 2015. Departamento Nacional de Obras Contra às Secas [WWW Document]. História do DNOCS. URL http://www.dnocs.gov.br/ (accessed 11.1.15). [Google Scholar]
  • Dodson SI, Everhart WR, Jandl AK, Krauskopf SJ. 2007. Effect of watershed land use and lake age on zooplankton species richness. Hydrobiologia 579: 393–399. [Google Scholar]
  • Elmoor-Loureiro L. 2000. Brazilian cladoceran studies: where do we stand? Nauplius 8: 117–131. [Google Scholar]
  • Elmoor-Loureiro L. 1997. Manual de identificação de cladóceros límnicos do Brasil. Ed. Universitária, Brasília, Distrito Federal, 106 p. [Google Scholar]
  • Elmoor-Loureiro LMA. 2007. Phytophilous cladocerans (Crustacea, Anomopoda and Ctenopoda) from Paraná River Valley, Goiás, Brazil. Rev Bras Zool 24: 344–352. [CrossRef] [Google Scholar]
  • Eskinazi-Sant'anna EM, Maia-Barbosa PM, Brito S, Rietzler AC. 2005. Zooplankton biodiversity of Minas Gerais state: a preliminary synthesis of present knowledge. Acta Limnol Bras 17: 199–218. [Google Scholar]
  • Eskinazi-Sant'Anna EM, Menezes R, Costa IS, Panosso R, Araújo MF, Attayde JL. 2007. Composição da comunidade zooplanctônica em reservatórios eutróficos do semi-árido do Rio Grande do Norte. Oecol Bras 11: 410–421. [CrossRef] [Google Scholar]
  • Esteves F, Caliman A. 2011. Águas Continentais: Características do Meio, Compartimentos e Suas Comunidades, In: Fundamentos de Limnologia. Interciência, Rio de Janeiro, pp. 113– 118. [Google Scholar]
  • Esteves FA, Caliman A, Santangelo JM, Guariento RD, Farjalla VF, Bozelli RL. 2008. Neotropical coastal lagoons: an appraisal of their biodiversity, functioning, threats and conservation management. Br J Biol 68: 967–981. [CrossRef] [PubMed] [Google Scholar]
  • Fernández-Rosado MJ, Lucena J. 2001. Space-time heterogeneities of the zooplankton distribution in La Concepción reservoir (Istán, Málaga; Spain). Hydrobiologia 455: 157–170. [Google Scholar]
  • Finan TJ, Nelson DR. 2001. Making rain, making roads, making do: public and private adaptations to drought in Ceará, Northeast Brazil. Clim Res 19: 97–108. [CrossRef] [Google Scholar]
  • Gariglio MA, Sampaio EV de SB, Cestaro LA, Kageyama PY. 2010. Uso sustentável e conservação dos recursos florestais da caatinga. MMA: Serviço Florestal Brasileiro, Brasília, 369 p. [Google Scholar]
  • Gilbert JJ. 1974. Dormancy in rotifers. Trans Am Microsci Soc 43: 490–513. [CrossRef] [Google Scholar]
  • Gotelli NJ, Colwell RK. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4: 379–391. [Google Scholar]
  • Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M, (Eds.), 2000. ICES zooplankton methodology manual. London; Academic Press, 684 p. [Google Scholar]
  • Havel JE, Lee CE, Vander Zanden MJ. 2005. Do Reservoirs Facilitate Invasions into Landscapes? Bioscience 55: 518–525. [Google Scholar]
  • Hsieh TC, Ma KH, Chao A. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (H ill numbers). Methods Ecol Evol 7: 1451–1456. [Google Scholar]
  • Huys R, Boxshall G. 1991. Copepod evolution. London: The Royal Society, 468 p. [Google Scholar]
  • IBGE − Instituto Brasileiro de Geografia e Estatística, 2004. Mapa de Biomas do Brasil. Escala 1:5.000. Ed. IBGE. Rio de Janeiro. [Google Scholar]
  • INMET. 2015. Instituto Nacional de Meteorologia. Banco de Dados Meteorológicos para Ensino e Pesquisa. [WWW Document]. http://www.inmet.gov.br/portal/%0Aindex.php?r=bdmep/bdmep (accessed 7.1.15). [Google Scholar]
  • Junger PC, Dantas F da CC, Nobre RLG, Kosten S, Venticinque EM, de Carvalho Araújo F, Sarmento H, Angelini R, Terra I, Gaudêncio A, They NH, Becker V, Cabral CR, Quesado LB, Carneiro LS, Caliman A, Amado AM. 2019. Effects of seasonality, trophic state and landscape properties on CO2 saturation in low-latitude lakes and reservoirs. Sci Total Environ 664: 283–295. [Google Scholar]
  • Keppeler EC, Serra AJ, Vieira LJS, de Oliveira JP, da Silva MT, dos Santos MJA, Ferraudo AS. 2018. Seasonal fluctuations of Rotifera in a tropical lake in Amazonia (Acre River floodplain, Brazil). Hidrobiológica 28: 335–347. [CrossRef] [Google Scholar]
  • Koste W. 1978. Rotatoria. Die Rädertiere Mitteleuropas Ein Bestimmungswerk, begründet von Max Voigt Überordnung Monogononta, Verlag Gebrüder Bornträger, Stuttgart, 673 p. [Google Scholar]
  • Kostopoulou V, Carmona MJ, Divanach P. 2012. The rotifer Brachionus plicatilis: an emerging bio-tool for numerous applications. J Biol Res 17: 97–112. [Google Scholar]
  • Lazzaro X, Bouvy M, Ribeiro-Filho RA, Oliviera VS, Sales LT, Vasconcelos ARM, Mata MR. 2003. Do fish regulate phytoplankton in shallow eutrophic Northeast Brazilian reservoirs? Freshw Biol 48: 649–668. [Google Scholar]
  • Leal IR, Silva JMC da, Tabarelli M, Lacher Jr TE. 2005. Mudando o curso da conservação da biodiversidade na Caatinga do Nordeste do Brasil. Megadiversidade 1: 139–146. [Google Scholar]
  • Lévêque C, Balian EV, Martens K. 2005. An assessment of animal species diversity in continental waters. Hydrobiologia 542: 39–67. [Google Scholar]
  • Likens GE. 2010. Plankton of inland waters, 1st ed. San Diego: Academic Press, 412 p. [Google Scholar]
  • Lohbeck M, Bongers F, Martinez-Ramos M, Poorter L. 2016. The importance of biodiversity and dominance for multiple ecosystem functions in a human-modified tropical landscape. Ecology 97: 2772–2779. [CrossRef] [PubMed] [Google Scholar]
  • Lucinda I, Moreno I, Melão M., Matsumura-Tundisi T. 2004. Rotifers in freshwater habitats in the Upper Tietê River Basin, São Paulo State, Brazil. Acta Limnol Bras 16: 203–224. [Google Scholar]
  • Maia-Barbosa P, Bozelli RL. 2006. Community structure and temporal dynamics of cladocerans in an Amazonian lake (lake Batata, PA, Brazil) impacted by bauxite tailings. Acta Limnol Bras 18: 67–75. [Google Scholar]
  • Maia-Barbosa PM, Menendez RM, Pujoni DGF, Brito SL, Aoki A, Barbosa FAR, 2014. Zooplankton (Copepoda, Rotifera, Cladocera and Protozoa: Amoeba Testacea) from natural lakes of the middle Rio Doce basin, Minas Gerais, Brazil. Biota Neotrop 14. [Google Scholar]
  • Malveira VTC, Araújo JC de, Güntner A. 2011. Hydrological impact of a high-density reservoir network in semiarid northeastern, Brazil. J Hydrol Eng 17: 109–117. [Google Scholar]
  • Marengo J. 2008. Vulnerabilidade, impactos e adaptação à mudança do clima no semi-árido do Brasil. Parcerias Estratégicas 13: 149–176. [Google Scholar]
  • Matsumura-Tundisi T. 1986. Latitudinal distribution of Calanoida copepods in freshwater aquatic systems of Brazil. Rev Bras Biol 46: 527–553. [Google Scholar]
  • Medeiros S de S, Pinto TF, Hernan Salcedo I, Cavalcante A de MB, Perez Marin AM, Tinôco LB de M. 2012. Sinopse do censo demográfico para o semiárido brasileiro. Campina Grande: Instituto Nacional de Seminário (INSA), 107 p. [Google Scholar]
  • Meerhoff M, Iglesias C, Melo F, Clemente J, Jensen E, Lauridsen T, Jeppesen E. 2007. Effects of habitat complexity on community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes. Freshw Biol 52: 1009–1021. [Google Scholar]
  • Melo Júnior M de, Santos Almeida VL dos, Neumann-Leitão S, Nogueira Paranaguá M, Nascimento Moura A. do. 2007a. O estado da arte da biodiversidade de rotíferos planctônicos de ecossistemas límnicos de Pernambuco. Biota Neotrop 7: 109–117. [CrossRef] [Google Scholar]
  • Melo Júnior M, dos Santos Almeida VL, Paranaguá MN, dos Nascimento Moura A. 2007b. Crustáceos planctônicos de um reservatório oligotrófico do Nordeste do Brasil. Rev Bras Zoociências 9. [Google Scholar]
  • Merrix-Jones FL, Thackeray SJ, Ormerod SJ. 2013. A global analysis of zooplankton in natural and artificial fresh waters. J Limnol 72: 12. [Google Scholar]
  • Moreira RA, Rocha O, Santos RM dos, Dias ES, Moreira FWA, Sant'Anna EME. 2016. Composition, body-size structure and biomass of zooplankton in a high-elevation temporary pond (Minas Gerais, Brazil). Oecologia Australis 20: 81–93. [CrossRef] [Google Scholar]
  • Moretto EM. 2001. Diversidade zooplanctônica e variáveis limnológicas das regiões limnética e litorânea de cinco lagoas do Vale do Rio Doce-MG, e suas relações com o entorno. Universidade de São Paulo. Phd Thesis, 310 p. [Google Scholar]
  • Moss BR. 2009. Ecology of Fresh Waters: Man and Medium, Past to Future. Oxford: Blackwell Science, 572 p. [Google Scholar]
  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853. [CrossRef] [PubMed] [Google Scholar]
  • Naiman R, Décamps H. 1990. The ecology and management of aquatic-terrestrial ecotones, ed. UNESCO, Paris, 303 p. [Google Scholar]
  • Nobre RLG, Caliman A, Cabral CR, de Carvalho FA, Guérin J, Dantas FC, Quesado LB, Venticinque EM, Guariento RD, Amado AM, Carneiro LS. 2020. Precipitation, landscape properties and land use interactively affect water quality of tropical freshwaters. Sci Total Environ 716: 137044. [PubMed] [Google Scholar]
  • Neves IF, Rocha O, Roche KF, Pinto AA. 2003. Zooplankton community structure of two marginal lakes of the river Cuiabá (Mato Grosso, Brazil) with analysis of Rotifera and Cladocera diversity. Braz J Biol 63: 329–343. [PubMed] [Google Scholar]
  • Nogueira M, George D, Jorcin A. 2003. Estudo do zooplâncton em zonas litorâneas lacustres: um enfoque metodológico, In: Henry, R. (Ed.), Ecótonos Nas Interfaces Dos Ecossistemas Aquáticos. Rima, São Carlos, SP, pp. 83–127. [Google Scholar]
  • Nogueira MG, Reis Oliveira PC, Tenorio de Britto Y. 2008. Zooplankton assemblages (Copepoda and Cladocera) in a cascade of reservoirs of a large tropical river (SE Brazil). Limnetica 27: 151–170. [Google Scholar]
  • Oksanen J, Kindt R, Legendre P, O'Hara B, Stevens MHH, Oksanen MJ, Suggests MASS. 2015. Vegan: community ecology package. [Google Scholar]
  • Paiva MP, Campos E. 1995. Fauna do nordeste do Brasil: conhecimento científico e popular. Banco do Nordeste do Brasil Fortaleza, Fortaleza, 245 p. [Google Scholar]
  • Paradis E. 2012. Analysis of Phylogenetics and Evolution with R. New York: Springer Science & Business Media, 386 p. [Google Scholar]
  • Paranaguá MN, Neumann-Leitão S, Nogueira-Paranhos JD, Silva TA, Matsumura-Tundisi T. 2005. Cladocerans (Branchiopoda) of a tropical estuary in Brazil. Br J Biol 65: 107–115. [CrossRef] [Google Scholar]
  • Paranhos JDN, Almeida VLS, Silva Filho JP, Paranaguá MN, Melo Júnior M. de, Neumann-Leitão S. 2013. The zooplankton biodiversity of some freshwater environments in Parnaíba basin (Piauí, Northeastern Brazil). Br J Biol 73: 125–134. [CrossRef] [Google Scholar]
  • Parra G, Matias NG, Guerrero F, Boavida MJ. 2009. Short term fluctuations of zooplankton abundance during autumn circulation in two reservoirs with contrasting trophic state. Limnetica 28: 175–184. [Google Scholar]
  • Pekel J-F, Cottam A, Gorelick N, Belward AS. 2016. High-resolution mapping of global surface water and its long-term changes. Nature 540: 418. [PubMed] [Google Scholar]
  • Pennington RT, Lavin M, Oliveira-Filho A. 2009. Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annu Rev Ecol Evolut System 40: 437–457. [CrossRef] [Google Scholar]
  • Perbiche-Neves G, Boxshall GA, Previattelli D, Nogueira MG, Da Rocha CEF. 2015. Identification guide to some Diaptomid species (Crustacea, Copepoda, Calanoida, Diaptomidae) of “de la Plata” River Basin (South America). Zookeys 1. [Google Scholar]
  • Pinto-Coelho R, Pinel-Alloul B, Méthot G, Havens KE. 2005. Crustacean zooplankton in lakes and reservoirs of temperate and tropical regions: variation with trophic status. Can J Fish Aquat Sci 62: 348–361. [Google Scholar]
  • Prado DE. 2003. As caatingas da América do Sul. In: I.R. Leal, M. Tabarelli, J. Silva (Eds.), Ecologia e conservação da caatinga. Recife: Universitária da UFPE, 3–73. [Google Scholar]
  • R Core Team, 2015. R: A language and environment for statistical computing. [Google Scholar]
  • Reid JW. 1985. Chave de identificação e lista de referências bibliográficas para as espécies continentais sulamericanas de vida livre da ordem Cyclopoida (Crustacea, Copepoda). Bol Zool 17–143. [CrossRef] [Google Scholar]
  • Ribeiro EMS, Arroyo‐Rodríguez V, Santos BA, Tabarelli M, Leal IR. 2015. Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. J Appl Ecol 52: 611–620. [Google Scholar]
  • Ribeiro MC, Martensen AC, Metzger JP, Tabarelli M, Scarano F, Fortin MJ. 2011. The Brazilian Atlantic Forest: a shrinking biodiversity hotspot. In: Z. F. and H. J. (eds), Biodiversity hotspots, Springer, Berlin, 405–434. [CrossRef] [Google Scholar]
  • Ricci C. 2001. Dormancy patterns in rotifers. Hydrobiologia 446: 1–11. [Google Scholar]
  • Rocha O, Sendacz S, Matsumura-Tundisi T. 1995. Composition, biomass and productivity of zooplankton in natural lakes and reservoirs in Brazil. Limnol Brazil 151–165. [Google Scholar]
  • Rosenberg DM, McCully P, Pringle CM. 2000. Global-Scale Environmental Effects of Hydrological Alterations: Introduction. Bioscience 50: 746–751. [Google Scholar]
  • Sampaio EV, Rocha O, Matsumura-Tundisi T, Tundisi JG. 2002. Composition and abundance of zooplankton in the limnetic zone of seven reservoirs of the Paranapanema River, Brazil. Braz J Biol 62: 525–545. [CrossRef] [PubMed] [Google Scholar]
  • Santos-Silva E dos. 2000. Revisão das espécies do “complexo nordestinus” (Wright, 1935) de Notodiaptomus Kiefer, 1936 (Copepoda: Calanoida: Diaptomidae). Universidade de São Paulo, São Paulo. Phd Thesis, 250 p. [Google Scholar]
  • Santos-Wisniewski MJ, Rocha O. 2007. Spatial distribution and secondary production of Copepoda in a tropical reservoir: Barra Bonita, SP, Brazil. Braz J Biol 67: 223–233. [PubMed] [Google Scholar]
  • Schindler DE, Scheuerell MD. 2002. Habitat coupling in lake ecosystems. Oikos 98: 177–189. [Google Scholar]
  • Segers H. 2001. Zoogeography of the Southeast Asian Rotifera, In: Sanoamuang L, Segers H, Shiel RJ, Gulati RD. (Eds.), Rotifera IX. Netherlands, Dordrecht: Springer, 233–246. [CrossRef] [Google Scholar]
  • Sendacz S, Caleffi S, Santos-Soares J. 2006. Zooplankton biomass of reservoirs in different trophic conditions in the state of São Paulo, Brazil. Braz J Biol 66: 337–350. [CrossRef] [Google Scholar]
  • Silva MJ da, Ramos TPA, Diniz VD, Ramos RT da C, Medeiros ESF. 2014. Ichthyofauna of Seridó/Borborema: a semi-arid region of Brazil. Biota Neotrop 14. [Google Scholar]
  • Silva WM da, Matsumura-Tundisi T. 2011. Checklist dos Copepoda Cyclopoida de vida livre de água doce do Estado de São Paulo, Brasil. Biota Neotrop 11: 1–11. [CrossRef] [Google Scholar]
  • Silva WM. 2008. Diversity and distribution of the free-living freshwater Cyclopoida (Copepoda: Crustacea) in the Neotropics. Braz J Biol 68: 1099–1106. [PubMed] [Google Scholar]
  • Silva WM, Matsumura-Tundisi T. 2005. Taxonomy, ecology, and geographical distribution of the species of the genus Thermocyclops Kiefer, 1927 (Copepoda, Cyclopoida) in São Paulo State, Brazil, with description of a new species. Braz J Biol 65: 521–531. [PubMed] [Google Scholar]
  • Silva WM, Perbiche-Neves G. 2017. Trends in freshwater microcrustaceans studies in Brazil between 1990 and 2014. Braz J Biol 77: 527–534. [PubMed] [Google Scholar]
  • Simões NR, Nunes AH, Dias JD, Lansac-Tôha FA, Velho LFM, Bonecker CC. 2015. Impact of reservoirs on zooplankton diversity and implications for the conservation of natural aquatic environments. Hydrobiologia 758: 3–17. [Google Scholar]
  • Sousa FDR, Elmoor-Loureiro LMA. 2008. Cladóceros fitófilos (Crustacea, Branchiopoda) do Parque Nacional das Emas, estado de Goiás. Biota neotropica 8: 159–166. [CrossRef] [Google Scholar]
  • Sousa W, Attayde JL, Rocha EDS, Eskinazi-Sant'Anna EM. 2008. The response of zooplankton assemblages to variations in the water quality of four man-made lakes in semi-arid northeastern Brazil. J Plankton Res 30: 699–708. [Google Scholar]
  • Souza-Soares F, Galizia Tundisi J, Matsumura-Tundisi T. 2011. Checklist de Rotifera de água doce do Estado de São Paulo, Brasil. Biota Neotrop 11. [Google Scholar]
  • SUDENE. 2017. Superintendência do Desenvolvimento do Nordeste [WWW Document]. MAPAS. [Google Scholar]
  • Suthers IM, Rissik D. 2009. Plankton: A guide to their ecology and monitoring for water quality. Csiro Publishing, Colinwood, 650 p. [Google Scholar]
  • Tabarelli M, Vicente A. 2004. Conhecimento sobre plantas lenhosas da Caatinga: lacunas geográficas e ecológicas, in: Silva J, Tabarelli M, Fonseca M, Lins, L. (Eds.), Biodiversidade Da Caatinga: Áreas e Ações Prioritárias Para a Conservação. Ministério do Meio Ambiente Brasília, Brasília, Distrito Federal, pp. 101– 111. [Google Scholar]
  • Taniguchi H, Nakano S, Tokeshi M. 2003. Influences of habitat complexity on the diversity and abundance of epiphytic invertebrates on plants. Freshw Biol 48: 718–728. [Google Scholar]
  • Thomaz SM, Dibble ED, Evangelista LR, Higuti J, Bini LM. 2008. Influence of aquatic macrophyte habitat complexity on invertebrate abundance and richness in tropical lagoons. Freshw Biol 53: 358–367. [Google Scholar]
  • Vadeboncoeur Y, Zanden M. Vander Lodge D. 2002. Putting the Lake Back Together: Reintegrating Benthie Pathways into Lake Food Web Models. Bioscience 52: 1. [Google Scholar]
  • Vanzolini PE, Ramos-Costa AMM, Vitt LJ. 1980. Répteis das caatingas. Rio de Janeiro: Academia Brasileira de Ciências. [CrossRef] [Google Scholar]
  • Walseng B, Hessen DO, Halvorsen G, Schartau AK. 2006. Major contribution from littoral crustaceans to zooplankton species richness in lakes. Limnol Oceanogr 51: 2600–2606. [Google Scholar]
  • Whitmore TC, Prance GT. 1987. Biogeography and Quaternary history in tropical America. Oxford: Oxford Science Publications. [Google Scholar]
  • Winfree RW, Fox J, Williams NM, Reilly JR, Cariveau DP. 2015. Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol Lett 18: 626–635. [Google Scholar]
  • Yurista P, Kelly JR, Miller S. 2005. Evaluation of optically acquired zooplankton size-spectrum data as a potential tool for assessment of condition in the great lakes. Environ Manag 35: 34–44. [CrossRef] [Google Scholar]

Cite this article as: Cabral CR, Diniz LP, da Silva AJ, Fonseca G, Carneiro LS, de Melo Júnior M, Caliman A. 2020. Zooplankton species distribution, richness and composition across tropical shallow lakes: A large scale assessment by biome, lake origin, and lake habitat. Ann. Limnol. - Int. J. Lim. 56: 25

All Tables

Table 1

Checklist and frequency of occurrence (%) of freshwater zooplankton (Copepoda, Cladocera, and Rotifera) from 180 Brazilian tropical shallow lakes located in the states of Rio Grande do Norte (n = 99) and Pernambuco (n = 81) by biome (Atlantic Forest n = 29; Caatinga n = 98), lake origin (Natural lake n = 45; Reservoirs n = 82), and lake habitat (Pelagic n = 127; Littoral n = 127) (TN = number of occurrences).

In the text
Table 2

List of zooplankton species in typifying the lakes groups by SIMPER analysis performed on presence/ absence data (bold p-values = significance p < 0,05). Cut off for low contributions: 70%.

In the text
Table 3

PERMANOVA table (summary) of the effect of biome, lake origin and lake habitat on the Rotifera, Copepoda and Cladocera communities.

In the text

All Figures

thumbnail Fig. 1

Map of the study area showing the 180 natural and man-made shallow lakes distributed across the states of Rio Grande do Norte and Pernambuco, in northeast Brazil. The grayscale on the map indicates the transition between the Atlantic Forest (on the right) and Caatinga biome (on the left)
In the text
thumbnail Fig. 2

Sample-based rarefaction curves for Rotifera (first line − A, B, C), Copepoda (second line − D, E, F) and Cladocera (third line − G, H, I) by biomes: Atlantic Forest and Caatinga (first column − A, D, G), lake origin: natural lakes and man-made lakes (second column − B, E, H), and habitat type: pelagic and littoral (third column − C, F, I). The curves are showing the average (solid lines) and extrapolation (dashed lines) accumulated zooplankton species richness with their ± 95% confidence intervals (shaded areas).
In the text
thumbnail Fig. 3

Ordination diagrams of Principal Coordination Analysis (PCoA) for Rotifera (first line − A, B, C), Copepoda (second line − D, E, F) and Cladocera (third line − G, H, I) by biomes: Atlantic Forest and Caatinga (first column − A, D, G), lake origin: natural lakes and man-made lakes (second column − B, E, H), and habitat type: pelagic and littoral (third column − C, F, I).
In the text

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