Zooplankton diversity in a dammed river basin is maintained by preserved tributaries in a tropical floodplain

Zooplankton diversity in a dammed river basin ismaintained by preserved tributaries in a tropical floodplain

Louizi S. M. Braghin . Bruno R. S. Figueiredo . Thamis Meurer .

Thaisa S. Michelan . Nadson R. Simoes . Claudia C. Bonecker

Received: 17 November 2014 / Accepted: 6 April 2015 / Published online: 18 April 2015

� Springer Science+Business Media Dordrecht 2015

Abstract In this study, we tested the hypothesis

that in floodplain lakes connected to a primary river

with regulated flow, the zooplankton composition is

maintained by the species found in lakes connected

to preserved tributaries. Zooplankton were sampled

from 23 lakes connected to the Parana, Ivinhema

and Baıa Rivers on the floodplain of the Upper

Parana River. For this purpose, we evaluated

zooplankton a, b and c diversity and applied

dispersal analysis to identify the dispersal of species

among lakes. In addition, we investigated whether

the Baıa and Ivinhema Rivers could disperse species

to the Parana River Basin through an analysis of

source environments. A total of 150 species were

observed, and the greatest number of species (115

species) occurred in environments associated with

the flow-regulated Parana River. Dispersal of

species among all lakes was identified. The highest

a-diversity values were found in the environments

connected to the tributaries, the Ivinhema and Baıa

Rivers, which also contributed with more than 50 %

of the composition of the lakes associated with the

Parana River. There was also greater b-diversity in

these environments, where the composition was

significantly correlated with turbidity, chlorophyll-a

and conductivity. The results supported our hy-

pothesis and showed that when the main river is

regulated by a dam, the tributaries take on the role

of maintaining c-diversity in the floodplain, favour-

ing the maintenance of the natural characteristics of

the system. We propose that preserving the integrity

of natural floodplain environments assists in main-

taining the regional diversity of the ecosystem as a

whole.

Keywords Zooplankton � Species composition �a-Diversity � b-Diversity � Dispersal

Introduction

Since the pioneering study by Forbes in 1887 (The lake

as a microcosm), ecological studies have sought to

understand patterns and mechanisms that explain the

structure of communities in various environments. In

Handling Editor: Piet Spaak.

L. S. M. Braghin (&) � B. R. S. Figueiredo �T. Meurer � T. S. Michelan � C. C. BoneckerUniversidade Estadual de Maringa – Programa de Pos-

graduacao em Ecologia de Ambientes Aquaticos

Continentais, Avenida Colombo, 5790, Bloco G-90,

Maringa, PR CEP 87020-900, Brazil

e-mail: [email protected]

N. R. Simoes

Universidade Federal do Sul da Bahia– Centro de

Ciencias Ambientais, Rodovia BA001 Porto Seguro–

Eunapolis, Porto Seguro, BA CEP 45810-000, Brazil

123

Aquat Ecol (2015) 49:175–187

DOI 10.1007/s10452-015-9514-7

general, these studies measure biodiversity using the

species richness (a-diversity), which is the simplest

method; however, accurate assessments of changes in

species along a gradient (b-diversity) are also impor-

tant (Magurran 2011). Measuring and analysing the b-diversity of an ecosystem can contribute to a better

understanding of ecosystem functioning and manage-

ment and of biodiversity conservation (Legendre et al.

2005) because such analyses reflect the variation in the

species composition in a geographical area.

In aquatic ecosystems, species diversity is deter-

mined by (1) local factors, such as resource avail-

ability, habitat structure, and the physical and

chemical properties of the water (Hutchinson 1957),

and/or (2) regional factors, such as the distance

between environments, which affects the capacity

for dispersal and the chance of colonisation by

individuals (Hubbell 2001). The relative importance

of each of these factors in structuring communities has

been the topic of numerous studies (Leibold et al.

2004). In studies on floodplains, these factors have

shown different degrees of influence because of the

hydrodynamics of the systems, including periodic

flooding and drought (Junk et al. 1989; Neiff 1990;

Simoes et al. 2013a).

In floodplains, floods are known to increase the

biotic similarity between environments (Thomaz et al.

2007) because they favour the dispersal of organisms

(Havel and Shurin 2004; Bonecker et al. 2009). Faunal

exchange among environments can decrease the

probability of stochastic or induced local extinctions

(Ward et al. 1999; Thomaz et al. 2007). A corollary is

that species extend their regional range, increasing the

similarity among environments, and b-diversity is

therefore diminished (Havel et al. 2000; Agostinho

et al. 2009; Lansac-Toha et al. 2009; Simoes et al.

2013a).

In contrast, during droughts, both biotic relation-

ships (e.g. predation) and environmental conditions

(e.g. physical and chemical properties of the water)

appear to be more important for maintaining the

populations in biotopes and can lead organisms to seek

new delimitations of their niches (Connell 1961;

Simoes et al. 2012). Therefore, the response of

organisms to all these local factors leads to changes

in species diversity in the ecosystem and reduces the

similarity of the species composition between envi-

ronments, increasing b-diversity during drought

events compared with diversity during flood events.

Changes in the natural dynamics of rivers can be

considered a major threat to floodplain ecosystems

(Agostinho et al. 2005). The damming of main

rivers, allowing significant collection of biological

information for the watershed (Green 1963, 1975),

alters the hydrological regime and reduces the

seasonally flooded area and duration of floods

(Ward and Stanford 1995; Souza Filho 2009). As

a result, the physical and chemical conditions of the

water in different environments of floodplain

ecosystems are altered, causing increased environ-

mental heterogeneity as a result of the reduced

connectivity among these environments (Agostinho

et al. 2007, 2008; Bovo-Scoparin et al. 2013), which

may influence the dispersal and survival of some

species (Bunn and Arthington 2002; Simoes et al.

2013b).

Zooplankton are one of the various aquatic com-

munities found in floodplains, and they are charac-

terised by high species diversity. Because zooplankton

consist of ecologically distinct groups with different

niche requirements, for example, regarding food

quality, habitat structure, current velocity and tur-

bidity (Allan 1976; Bozelli 2000; Bonecker et al.

2009), this community is appropriate for investigating

the influence of local and regional factors on the

structure of floodplain communities.

Thus, the objectives of this study were to (1) assess

whether the composition of zooplankton species in

lakes associated with two preserved tributaries (the

Ivinhema and Baıa Rivers) is similar to the compo-

sition found in lakes connected to the Parana River (a

dam-regulated river) and determine the relative con-

tributions of species from the tributaries to lakes of the

Parana; (2) evaluate the mean a-diversity among the

set of lakes associated with different rivers (dammed

and preserved) in the floodplain of the Upper Parana

River; (3) evaluate the variability of the zooplankton

community composition (b-diversity) between the set

of lakes associated with different rivers (dammed and

preserved) in the floodplain of the Upper Parana River;

and (4) evaluate whether the regional distribution of

zooplankton is associated with the geographical

distance between the lakes and/or the environmental

conditions of each lake. With these objectives, we

tested the hypothesis that preserved environments

(tributaries) contribute to the maintenance of species

composition in environments under the influence of

damming.

176 Aquat Ecol (2015) 49:175–187

123

Materials and methods

Study area

This study was conducted on the floodplain of the

Upper Parana River (22�400–22�500 S; 53�100–53�240W), which is characterised by high biodiversity

(Agostinho et al. 2004), including high zooplankton

diversity (testate amoebae, rotifers, cladocerans and

copepods), with 541 described species (Lansac-Toha

et al. 2009). The study area is an extensive alluvial

plain (802,150 km2) located in Brazil and consists of

various aquatic environments with different degrees of

connectivity, including three rivers that form a com-

plex river-floodplain ecosystem. The Parana River is

the main river of this ecosystem and is largely

regulated by a series of upstream reservoirs; therefore,

it is not regarded as a preserved river because of the

influence of damming. The Ivinhema and Baıa Rivers

are the major tributaries of the Parana River, connect-

ing just downstream of the Porto Primavera Dam

(Fig. 1). This reservoir was filled in 1998 and is the

latest in a chain of reservoirs distributed along the

Parana, Tiete, Rio Grande and Parnaıba Rivers in the

states of Sao Paulo and Minas Gerais. The Ivinhema

and Baıa Rivers are located in the floodplain of Mato

Grosso do Sul State and are considered preserved

rivers in this study because they lack dams along their

courses. In addition, the lower stretch of the Ivinhema

River is located in a legally protected area belonging

to Ivinhema State Park.

Sampling design

Samples were collected in the morning from 23 lakes

permanently connected to the dam-regulated and

preserved rivers, including nine lakes associated with

the Parana River, seven associated with the Ivinhema

River and seven associated with the Baıa River.

Sampling was carried out in October 2012, in the

interim period between droughts and floods on the

plain, which are observed during a major portion of the

year (see Simoes et al. 2013b).

The littoral and pelagic regions of the lakes are

colonised by different morphological types of

aquatic macrophytes. In lakes associated with the

Parana River, these types include emergent, free-

floating, rooted with floating leaves, epiphytes, free

submerged and immersed, whereas in lakes associ-

ated with the Ivinhema and Baıa Rivers, there is a

predominance of rooted plants with floating leaves.

Zooplankton were sampled at 20 random points in

the pelagic region of each lake through 20 vertical

hauls, performed at each point using a 68-lmplankton net, trawling from the bottom to the

surface, providing composite samples for each lake.

The samples were preserved in a 4 % formaldehyde

solution buffered with calcium carbonate, and

species of rotifers, cladocerans and copepods were

identified based on specialised literature (see

Lansac-Toha et al. 2009). The zooplankton were

identified using a Sedgewick-Rafter chamber under

an optical microscope. For each sample, the iden-

tification effort continued until the species accumu-

lation curve had reached stabilisation and no new

species were found. To analyse the community

data, the lakes were grouped into three sets of data:

lakes connected to the Ivinhema River, lakes

connected to the Baıa River (both preserved rivers)

and lakes connected to the Parana River (regulated

river).

The environmental conditions of each lake were

measured during zooplankton community sampling

from the subsurface at three random points located in

the pelagic region [depth between 10 and 20 cm

(Roberto et al. 2009)] and included the following

Fig. 1 Map of the sampling area, showing the lakes connected

to the Parana (dammed river), Ivinhema and Baıa (preserved

rivers) Rivers. The black points indicate sampling sites in the

Upper Parana River floodplain

Aquat Ecol (2015) 49:175–187 177

123

environmental variables: pH (Digimed portable digital

potentiometer), electrical conductivity (lS cm-1;

Digimed portable digital potentiometer), turbidity

(NTU; LaMotte 2008� portable digital turbidimeter),

dissolved oxygen (mg L-1; YSI portable digital

oximeter), depth (m) and water temperature (�C). Inaddition, water samples from the subsurface were

collected at the same points with a Van Dorn bottle

(5 L), and the chlorophyll-a concentration (mg L-1)

was analysed and processed according to the method-

ology of Golterman and Clymo (1969). For the data

analyses, the mean of all the results for the environ-

mental variables was calculated per lake.

Data analysis

A permutational analysis of variance (PERMA-

NOVA; Anderson 2001) based on a binary matrix

(presence and absence of species) was performed to

test the similarity of the species composition between

the sets of lakes connected to the rivers, and a post hoc

Tukey’s test was performed to determine whether the

species composition varied significantly (P\ 0.05)

between the lakes. The contribution of species in the

lakes associated with the Ivinhema and Baıa Rivers

relative to the species composition found in lakes

associated with the Parana River was analysed based

on the total number of species occurring in the lakes

connected to each river and species similarity (pres-

ence and absence) between the sets (objective 1). The

hypothesis that the contribution of species in lakes

connected to preserved tributaries maintains the

species composition in the lakes connected to the

regulated river was supported if the number of similar

species between the two sets of lakes (Parana and

Ivinhema and Parana and Baıa) exceeded 50 % and

based on the following two analyses:

1. Dispersal analysis The indicator of dispersal

through spatial autocorrelation was obtained by

analysing the relationship between the similarity

of communities and the geographical distance

between the studied lakes. If dispersal is an active

process in the regional pool of species in the

floodplain, the nearest lakes should show more

similarity between their communities than those

separated by a greater distance (Borcard et al.

2011). Mantel tests between community dis-

similarity and the geographical distance matrix

(among lakes) were employed. The community

dissimilarity (1-similarity of Bray–Curtis) was

obtained using the density of the species subjected

to square-root transformation.

2. Source environment analysis Once the spatial

limitations on the dispersal of species among lakes

were identified, we sought the source systems.

According to Gonzalez (2009), source environ-

ments are where species grow rapidly and produce

significant numbers of emigrants, which can

sustain populations of the species in the colonised

environment (sink). Thus, we postulate that

preserved lakes will show more common species

than regulated lakes. Common species were

considered as those with a frequency of occur-

rence higher than 50 % (Dajoz 2005). Further-

more, source environments should show younger

individuals than sink environments. Due to

methodological difficulties in identifying young

cladocerans and rotifers, only young individuals

of calanoid copepods and cyclopoids (nauplii and

copepodites) were tested.

A one-way ANOVA (Zar 1996) was performed to

test significant (P\ 0.05) differences between the

mean a-diversity, number of common species and

density of young among the systems. A post hoc

Tukey’s test was conducted to assess the sets (Parana,

Ivinhema and Baıa) that were significantly (P\ 0.05)

different. The assumptions of normality and ho-

moscedasticity were tested. When appropriate, data

were log-transformed to meet these assumptions.

A dispersion homogeneity test (PERMDISP; An-

derson et al. 2006) was performed to test the

variability of the zooplankton communities (b-diver-sity) between each set of lakes (objective 3). A

centroid was computed for each group, and the

distances between each lake and the centroid were

considered the b-diversity of the Parana, Ivinhema and

Baıa River lakes. The significance (P\ 0.05) of the

differences in b-diversity between each set of lakes

was tested using a permutation test with 999

permutations.

Three matrices were calculated for each group of

lakes: geographical distance (latitude and longitude of

the lakes), environmental conditions (physical and

chemical characteristics of the water) and zooplankton

composition (presence and absence of species). These

matrices were correlated using the Mantel test

178 Aquat Ecol (2015) 49:175–187

123

(Legendre and Legendre 1998) to investigate whether

the geographical distance matrix (Euclidean distance

matrix) or environmental condition matrix (Euclidean

distance matrix) influenced the diversity of the commu-

nity (Jaccard dissimilarity matrix with the presence and

absence of species) (objective 4). The significance of the

results (P\ 0.05) was determined using 999 permuta-

tions. One-way ANOVA (Zar 1996) was performed

with each environmental variable to determine the

variables that differed significantly between the sets of

lakes. The assumptions of this analysis were also tested.

All the analyses were performed using the software

R version 3.0 (R Development Core Team 2012) with

the ‘‘vegan’’ package (Oksanen et al. 2011).

Results

The zooplankton community was represented by 150

species (c-diversity; Table 1) in the floodplain, with

115, 105 and 96 species being found in lakes

connected to the Parana, Ivinhema and Baıa Rivers,

respectively. There was a significant difference in the

species composition between the three sets of lakes

(pseudo-F = 1.55; P\ 0.01). The post hoc test

showed that the species composition in the set of

lakes associated with the Parana River was similar to

the composition found in lakes connected to the

Ivinhema River and different from the composition

found in the lakes associated with the Baıa River.

Eighty-one species (70.4 % of the total number of

Parana species) were shared between the lakes con-

nected to the Ivinhema and Parana; 77 species (66.9 %

of the total number of the Parana species) were shared

between the lakes connected to the Baıa and Parana;

and 75 species (72 % of the total number of Baıa

species) were shared between the lakes connected to

the Ivinhema and Baıa (Fig. 2).

Regarding the a-diversity in the three sets of lakes,

the highest values were recorded in the Ivinhema and

Baıa lakes, whereas the Parana lakes exhibited the

lowest mean, which was significantly different from

the other two means (F = 2.69; P\ 0.05) (Fig. 3).

Additionally, the greatest variability in the compo-

sition of the zooplankton community was observed for

the lakes connected to the Parana River; these lakes

showed the highest b-diversity values (distance from

centroid = 0.48), which differed significantly from

the values recorded for the sets of lakes associated

with the Ivinhema (distance from the centroid = 0.44)

and Baıa (distance from the centroid = 0.38) Rivers

(P\ 0.01) (Fig. 4).

There was no relationship between the composition

of the zooplankton community and the geographical

distance between lakes (Mantel test; r\ 0.08;

P[ 0.1) for any set of lakes analysed (Parana,

Ivinhema and Baıa). However, when the density of

individuals was analysed considering all lakes, we

detected a significant relationship between community

structure and geographical distance (Mantel = 0.182;

P = 0.021), indicating spatial autocorrelation and

dispersal limitation.

We found evidence that the Baıa and Ivinhema

Rivers disperse species to the Parana system. Thirty-

one species were common, showing a wide distribu-

tion among the studied lakes. However, the diversity

of common species differed between the systems

(F2,17 = 16.10; P = 0.001) (Fig. 5a). The Baıa River

exhibited the highest average diversity of common

species (26.8 ± 14.2), while the Parana River showed

the lowest diversity of common species (18.9 ± 2.85).

Furthermore, the density of young zooplankton was

significantly different between the three rivers

(F2,17 = 3.50; P = 0.05; Fig. 5b), and the average

number of young individuals was highest in the Baıa

River Basin (16,586 ind.m-3) and lowest in the

Parana River Basin (4,956 ind.m-3).

A significant influence of environmental conditions

on the composition of zooplankton species was only

observed in the lakes connected to the Parana River

(r = 0.32; P\ 0.01). In addition, ANOVA revealed

that the values for turbidity (F = 43.32; P\ 0.01),

chlorophyll-a (F = 15.25; P\ 0.01) and conductivity

(F = 77.24; P\ 0.01) differed significantly between

the lakes associated with the Parana River, with low

values of turbidity and chlorophyll-a and high values

of conductivity being observed for these lakes,

suggesting a possible influence on the composition

of the community. For more details about the

evaluated environmental variables, see Table 2.

Discussion

The characteristics of zooplankton biodiversity (com-

position, a-diversity and b-diversity) differed betweenthe preserved tributaries and the regulated system,

with lower a-diversity and higher b-diversity being

Aquat Ecol (2015) 49:175–187 179

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Table 1 List of species in

the lakes connected to the

Parana, Ivinhema and Baıa

Rivers—floodplain lakes of

the Parana River, Brazil, in

October 2012

ROTIFERA

Asplanchnidae

Asplanchna sieboldii (Leydig, 1854)

Brachionidae

Brachionus budapestinensis Daday, 1885 Kellicottia bostoniensis (Rousselet, 1908)

B. calyciflorus (Pallas, 1766) Keratella americana Carlin, 1943

B. caudatus Barrois and Daday, 1894 K.cochlearis (Gosse, 1851)

B. dolabratus Harring, 1914 K. tropica (Apstein, 1907)

B. falcatus Zacharias, 1898 Plationus patulus (Muller,1786)

B. mirus Daday, 1905 Platyias leloupi Gillard, 1967

B. quadridentatus Hermann, 1783 P. quadricornis (Ehrenberg, 1832)

Collothecidae

Collotheca ambigua (Hudson, 1883)

Conochilidae

Conochilus coenobasis (Skorikov, 1914) C. unicornis Rousselet, 1892

C. dossuaris Hudson, 1885 C. natans (Seligo, 1900)

Dicranophoridae

Dicranophoroides caudatus (Ehrenberg, 1834) Trichotria tetractis Ehrenberg (1830)

Epiphanidae

Epiphanes clavulata (Ehrenberg, 1832) E. macrourus Barrois and Daday, 1894

Euchlanidae

Beuchampiella eudactylota (Gosse, 1886) Euchlanis dilatata Ehrenberg, 1832

Dipleuchlanis propatula (Gosse, 1886) E. incisa Carlin, 1939

Filinidae

Filinia longiseta (Ehrenberg, 1834) F. terminalis (Plate, 1886)

F. opoliensis Zacharias, 1891

Flosculariidae

Floscularia sp. Ptygura sp.

Gastropodidae

Ascomorpha ecaudis Perty, 1850 Gastropus hyptopus (Ehrenberg, 1938)

A. saltans Bartsch, 1870 G. stylifer (Imhof, 1891)

Hexarthridae

Hexarthra intermedia (Wiszniewski, 1929) H. mira (Hudson, 1871)

Ituridae

Itura deridderae Segers, 1993

Lecanidae

Lecane bulla (Gosse, 1886) L. luna (Muller, 1776)

L. cornuta (Muller, 1786) L. lunaris (Ehrenberg, 1832)

L. curvicornis (Murray, 1913) L. papuana (Murray, 1913)

L. decipiens (Murray, 1913) L. proiecta Hauer, 1956

L. elsa Hauer, 1931 L. quadridentata (Ehrenberg, 1832)

L. leontina (Turner, 1892) L. signifera (Jennings, 1896)

L. ludwigii (Eckstein, 1883) L. stichaea Harring, 1913

Lepadellidae

Colurella obtusa (Gosse, 1886) L. (L.) patella (Muller, 1773)

Lepadella ovalis (Muller, 1786)

180 Aquat Ecol (2015) 49:175–187

123

Table 1 continued ROTIFERA

Mytilinidae

Mytilina macroceca (Jennings, 1894) M.ventralis (Ehrenberg, 1830)

Notommatidae

Cephalodella gibba (Ehrenberg, 1832) Notommata copeus Ehrenger, 1834

Eothinia elongata (Ehrenberg, 1832) N. pachyura (Gosse, 1886)

Monommata dentata Wulfert, 1940

Synchaetidae

Polyarthra dolichoptera Idelson, 1925 Synchaeta oblonga Ehrenberg, 1831

Ploesoma truncatum (Levander, 1894) S. pectinata Ehrenberg 1832

Testudinellidae

Pompholyx complanata Gosse, 1951 T. patina (Hermann, 1783)

Testudinella ohlei Koste, 1972 T. tridentata Smirnov, 1931

Trichocercidae

Trichocerca bicristata (Gosse, 1887) T. iernis (Gosse, 1887)

T. bidens (Lucks, 1912) T. myersi Hauer, 1931

T. brachyura (Gosse, 1851) T. scipio (Gosse, 1886)

T. elongata (Gosse, 1886) T. similis (Wierzejski, 1893)

T. gracillis (Tessin, 1890)

Trichotriidae

Trichotria tetractis Ehrenberg, (1830)

Bdelloidea

Philodinidae

Proalidae

Proales sp.

CLADOCERA

Bosminidae

Bosmina hagmanni Stingelin, 1904 B. tubicen Brehm, 1939

B. freyi De Melo and Hebert, 1994 Bosminopsis deitersi Richard, 1895

Chydoridae

Acroperus tupinamba Sinev and Elmoor-

Loureiro, 2010

Dunhevedia odontoplax Sars, 1901

Alona dentifera Sars, 1901 E. barroisi (Richard, 1894)

A. guttata Sars, 1862 Ephemeroporus hybridus (Daday, 1905)

A. ossiani Sinev, 1998 E. tridentatus (Bergamin, 1931)

A. verrucosa Sars, 1901 E. orientalis (Daday, 1898)

Alonella clathratula Sars, 1896 Chydorus pubescens Sars, 1901

A. dadayi Birge, 1910 C. sphaericus O. F. Muller, 1776

Coronatella poppei (Richard, 1897) Kurzia longirostris Daday, 1898

Camptocercus australis Sars, 1896 Leberis davidi (Richard, 1895)

Chydorus eurynotus Sars, 1901 Nicsmirnovius incredibilis (Smirnov,

1984)

C. parvireticulatus Frey, 1897 Notoalona sculpta (Sars, 1901)

Daphniidae

Ceriodaphnia cornuta Sars, 1886 D. lumholtzi G. O. Sars, 1885

Daphnia gessneri (Herbst, 1967) Simocephalus latirostris Stingelin, 1906

Aquat Ecol (2015) 49:175–187 181

123

found in the lakes of the regulated system. The

damming of floodplain rivers alters the dynamics of

the entire ecosystem and affects the structure of the

associated communities because the main river ceases

to contribute as a source of propagule dispersal (for

species) between the existing environments on the

Table 1 continued CLADOCERA

Ilyocryptidae

Ilyocryptus spinifer Herrich, 1882

Macrothricidae

Macrothrix elegans (Sars, 1901) M. squamosa Sars, 1901

Moinidae

Moina micrura Kurz, 1874 Moina minuta Hansen, 1899

Sididae

Diaphanosoma birgei Korineck, 1981 D. fluviatile Hansen, 1899

D. brevireme Sars, 1901 D. spinulosum Herbst, 1967

COPEPODA

Cyclopidae

Eucyclops ensifer Kiefer, 1936 M. longisetus (Thiebaud, 1912)

E. serrulatus (Fischer, 1851) Microcyclops finitimus Dussart, 1984

E. solitarius Herbst, 1959 M. meridianus (Kiefer, 1926)

Eucyclops sp. Paracyclops chiltoni (Thomson, 1882)

Ectocyclops rubescens Brady, 1904 P. pilosus Dussart, 1984

Macrocyclops albidus (Jurine, 1920) Thermocyclops decipiens (Kiefer, 1929)

Mesocyclops actices Myers, 1930 T. minutus (Lowndes, 1934)

M. anceps (Richard, 1897)

Diaptomidae

Argyrodiaptomus azevedoi (Wright,

1935)

N. iheringi (Wright, 1935)

Notodiaptomus cearensis (Wright, 1936) N. isabelae (Wright, 1936)

N. henseni (Dahl, 1894) N. spinuliferus Dussart and Matsumura-Tundisi,

1986

Fig. 2 Venn diagram showing zooplankton c-diversity in the

Upper Parana River floodplain. The values represent the number

of species found in each subset of lakes connected to the studied

rivers

Fig. 3 Mean and standard error of zooplankton a-diversityvalues in lakes connected to the Parana (dammed river),

Ivinhema and Baıa (preserved rivers) Rivers

182 Aquat Ecol (2015) 49:175–187

123

floodplain. This exchange between rivers and flood-

plains can be altered by factors such as flow control

performed by upstream reservoirs, which causes

decreases in the intensity and magnitude of floods

and interferes with connectivity among environments,

even permanently connected environments (e.g.

Thomaz et al. 2007). Thus, the similarity of the

species composition and environmental conditions

between environments is reduced (Ward and Stanford

1983; Junk et al. 1989; Agostinho et al. 2009; Simoes

et al. 2012), resulting from an absence or degraded

effect of homogenisation (Thomaz et al. 2007).

Moreover, a-diversity is expected to increase during

inundation because each lake receives species from

others, which increases biotic similarity and decreases

b-diversity.In the absence of floods, regulated river basins are

compromised because their connections are dimin-

ished, but adjacent river basins, such as tributaries and

lakes distributed along the floodplain (preserved

environments), play a crucial role in minimising the

effects of anthropogenic activity on ecosystem dy-

namics and can help to restructure environmental

conditions and aquatic communities. We found

evidence that preserved tributaries can serve as source

environments for regulated systems: first, the observed

dispersal limitation suggests a gradient of communi-

ties among the lakes; second, the number of common

species diminished in the regulated system; and third,

there was a greater density of young individuals in the

preserved systems. These results highlighted the large

contribution of zooplankton species from lakes con-

nected to preserved tributaries to the zooplankton

community composition of the lakes influenced by

damming. Furthermore, the higher a-diversity found

in the first set of lakes shows that preserved lakes,

particularly lakes that are located in legally protected

plain areas (Ivinhema State Park), play a particular

role in the maintenance of zooplankton biodiversity.

Only the Parana River Basin showed a relationship

between b-diversity and environmental heterogeneity.

The construction of dams causes a variety of changes

Fig. 4 Graphic representation of the compositional variability of

the zooplankton community in lakes connected to the Parana

(dammed river), Ivinhema and Baıa (preserved rivers) Rivers

Basin. The scores represent the different sampled lakes of the

systems: Parana River Basin (clear triangles), Ivinhema River

Basin (clear squares) and Baıa River Basin (clear triangles)

Fig. 5 Graphic

representation of the

zooplankton common

species diversity (a) and the

density of zooplankton

(b) in lakes connected to theParana (dammed river),

Ivinhema and Baıa

(preserved rivers) Rivers

Aquat Ecol (2015) 49:175–187 183

123

in the physical and chemical characteristics of down-

stream water bodies, such as greater water transparen-

cy and lower concentrations of nutrients, especially in

environments directly influenced by the regulated

river (Agostinho et al. 2004; Rodrigues et al. 2015). A

study by Roberto et al. (2009) on the floodplain of the

Upper Parana River (the floodplain under study)

illustrated the consequences of damming the Parana

River on the limnological characteristics of environ-

ments downstream of the Porto Primavera Dam, with

the authors reporting that there was a decrease in

nutrients and an increase in water transparency in

these biotopes after damming. In addition, the shift of

connectivity between environments also explained the

high zooplankton b-diversity among the lakes associ-

ated with the Parana River because it causes environ-

mental heterogeneity and unfavourable conditions for

food resources such as phytoplankton (Agostinho et al.

2009; Rodrigues et al. 2009, 2015; Bovo-Scoparin

et al. 2013).

It is noteworthy that the lakes connected to the

Parana River were characterised by low values of

chlorophyll-a and turbidity and high values of con-

ductivity. These variables are important for structuring

zooplankton communities because they affect the

availability of food resources (Dodson et al. 2000;

Barnett and Beisner 2007; Simoes et al. 2013a) and

intensify predator–prey relationships (Simoes et al.

2012; Figueiredo et al. 2015). Thus, local factors (the

physical and chemical conditions of the lakes and the

availability of food resources) determine the compo-

sition of the zooplankton community in the lakes

associated with the Parana River because such factors

promote or limit the occurrence of certain species,

which has been discussed in other studies (Hutchinson

1957; Simoes et al. 2013b). Thus, the b-diversity of thezooplankton in the regulated river is a response to the

variability of environmental conditions and to the

different degrees of connectivity between environ-

ments (Bonecker et al. 2013).

Another factor that may have caused the decreased

similarity of the species composition between the

lakes associated with the Parana River was the

presence of different morphological types of aquatic

macrophytes (emergent, floating, rooted with floating

leaves and submerged) in the environments. The

greater transparency of the water in the Parana River

may also have facilitated the diversity macrophytes in

the lakes, especially the occurrence of submergedTable

2Mean,maxim

um

andminim

um

values

forspeciesdiversity

(S);littoralspecies(LPK);planktonic

species(PK);depth

(m);Secchidepth

(m);pH;dissolved

oxygen

(D.O.,mg/L

and%);temperature

(Tem

p,C�);turbidity(N

TU);chlorophyll-a

(lg/L);electricalconductivity(E.C.,lS

/cm);andfiltratedvolume(F.V.,L)forthreegroupsoflakes

connectedto

theParana(PR),Ivinhem

a(IV)andBaıa(BA)Riversin

October

2012

SLPK

PK

Depth

(m)

Secchi(m

)pH

D.O.(m

g/L)

PR

35(24–50)

16(9–32)

12(12–30)

1.73(1.25–2.27)

1.36(0.87–2.20)

5.72(5.13–6.29)

6.66(5.39–8.31)

IV42(33–54)

18(6–33)

25(10–32)

1.99(1.02–3.13)

0.55(0.32–1.10)

5.56(5.11–5.90)

7.34(5.43–8.55)

BA

44(38–50)

18(12–26)

26(21–30)

2.04(1.68–2.43)

0.63(0.60–0.67)

5.76(5.37–6.42)

7.15(6.00–8.37)

D.O.(%

)Tem

p(�C)

Chlorophyll-a

(ug/L)

Turbidity(N

TU)

E.C.(lS/cm)

F.V.(L)

PR

80.12(65.40–97.83)

24.64(23.60–26.20)

4.23(1.26–8.19)

5.65(1.34–11.36)

54.83(49.40–59.10)

2983.5

(2044.61–4198.73)

IV88.04(63.10–103.17)

24.46(22.80–26.30)

15.03(0.82–29.35)

31.32(13.11–38.00)

31.32(13.11–38.00)

2701.95(2097.60–4176.12)

BA

85.59(71.37–100.80)

24.24(23.63–25.00)

28.94(16.93–54.61)

13.88(12.57–15.16)

21.5

(16.24–27.25)

2397.05(2283.54–2549.76)

184 Aquat Ecol (2015) 49:175–187

123

plants (Thomaz et al. 2009); such communities are

responsible for structuring the habitats of species and

making these habitats heterogeneous.). The greater

number of littoral species in the lakes connected to the

Parana River compared to the lakes connected to the

preserved tributaries could be an aftermath of this

macrophyte dependence of the zooplankton species

richness (Table 2). In contrast, the lakes connected to

preserved tributaries showed dominance of only one

morphological type of macrophyte (rooted with float-

ing leaves), which appears to have contributed to the

formation of more similar zooplankton communities.

Thus, the presence of aquatic macrophytes can

determine the composition of zooplankton by adding

a set of microhabitats and surfaces for colonisation by

various types of organisms and providing a greater

amount of resources and refuges from predators

(Lansac-Toha et al. 2003; Declerck et al. 2007;

Colwell 2009).

This study showed that when the main river is

regulated, the tributaries assume the role of maintain-

ing the c-diversity of the floodplain, thus highlighting

the importance of the river-floodplain relationship and

spatial connectivity between environments. Such

relationships favour the maintenance of the system’s

natural characteristics because even when changes in

environmental characteristics are sufficient to affect

the local diversity of certain lakes (a-diversity),regional diversity may remain unchanged because

the lakes contribute species that may have been lost as

a result of damming, which supports the proposed

hypothesis.

Therefore, the natural integrity of floodplain envi-

ronments may be preserved even when the main river

is strongly influenced by anthropogenic activities,

such as the construction of dams. This management

proposal can assist in maintaining the regional diver-

sity of the ecosystem as a whole.

Conceptual framework for the structure

of zooplankton communities in floodplains (see

Fig. 6)

The composition of zooplankton species in impacted

environments (lakes connected to the Parana River) is

maintained by preserved tributaries [lakes connected

to the Ivinhema (A) and Baıa (B) Rivers]. The

preserved tributaries are considered source environ-

ments because the Ivinhema and Baıa Rivers exhibit

species showing a frequency of occurrence higher than

50 % and greater numbers of younger individuals than

sink environments (Dajoz 2005). The dotted circles

represent the b-diversity observed in each basin, and

their sizes are proportional to the size of the variability

in the composition of the zooplankton community in

each basin. The main environmental variables influ-

encing the distribution of zooplankton species in the

Parana Basin are turbidity, chlorophyll-a and electrical

conductivity. This model may be valid for other

aquatic species; however, the variables and the

proportion of shared species are dependent on the

group studied.

Acknowledgments We thank two anonymous reviewers for

comments made on our first draft. We also thank Ana P.

C. Fernandes and Diogo C. Amaral, for support during the

fieldwork and the sampling period. The authors are grateful to

Coordination of Improvement of Higher Level Personnel

(CAPES) and National Council for Scientific and

Fig. 6 Conceptual model of zooplankton diversity in flood-

plain lakes connected to the main river, based on our findings in

the Upper Parana River floodplain. The composition of

zooplankton species in impacted environments (lakes connected

to the Parana River) is maintained by preserved tributaries [lakes

connected to Ivinhema (A) and Baıa (B) Rivers]. The preserved

tributaries are considered source environments because the

Ivinhema and Baıa Rivers exhibit species showed a frequency of

occurrence higher than 50 % and greater numbers of younger

individuals than sink environments. The dotted circles represent

the b-diversity observed in each basin, and their sizes are

proportional to the size of the variability in the composition of

the zooplankton community in each basin. The main environ-

mental variables influencing the distribution of zooplankton

species in the Parana Basin are turbidity, chlorophyll-a and

electrical conductivity

Aquat Ecol (2015) 49:175–187 185

123

Technological Development (CNPq), for scholarship. Claudia

C. Bonecker also thank to CNPq for providing the research

productivity grant. Finally, we thank Juliana D. Dias for

critically reading this manuscript and Limnology Laboratory

of Nupelia/UEM for providing the abiotic data used.

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