Intra and inter-annual structure of zooplankton communities in floodplain lakes: a long-term ecological research study
Nadson R. Simões1*, Fábio A. Lansac-Tôha1, Luiz F. M. Velho1 & Claudia C. Bonecker1
*Dirección para correspondencia Abstract ]]>
Water flow management has significantly changed the natural dynamic of floods, which are responsible for the structure and dynamic of aquatic communities in river-floodplain systems. With the aim to elaborate a conceptual framework that describes the main ecological factors associated with zooplankton community structure in the Upper Paraná River, we investigated the mechanisms that regulate the communities structure and their response to inter-annual and hydro-sedimentological ]]>
El manejo del régimen de inundación ha cambiado de manera significativa la dinámica natural de las inundaciones, que son responsables ]]>
Palabras clave: diversidad, estructura de la comunidad, manejo ambiental, procedimientos Bayesianos, modelo conceptual, humedales. Diversity of zooplankton in river-floodplains system is frequently ascribed to interactions between habitat diversity and flood pulse (Robertson & Hardy 1984, Vásquez & Rey 1989, Rodrigo et al. 2003, De Paggi & Paggi 2007, Lansac-Tôha et ]]>
2009). Such interactions are caused by the dynamics of flooding, which is the driving force for variation in communities and their responses to spatial and temporal variations in river-floodplain systems (Junk et al. 1989, Neiff 1990). These community variations depend on the frequency, intensity (water volume), amplitude, and seasonality (period of occurrence) of the phases of the hydro-sedimentological pulse, which fluctuates between limnophase (low water) and potamophase (high water) (Neiff ]]>
Modifications of ]]>
et al. 2006). This occurs because reservoirs reduce the natural amplitude of water levels variation, consequently changing the dynamics of aquatic communities (Ward & Stanford 1995). The resulting ecological damage may have economic and social impacts in human communities, since recent studies ]]>
An extensive literature exists showing the associations between local environmental variations and the structure of zooplankton communities (Dodson 1992, Schell et al. ]]>
et al. 2002) and the influence of human activities on these communities (e.g. Beaver et al. 1998, Dodson & Lillie 2001, Dodson et al. 2005, Angeler & Moreno 2007, Dodson et al. 2007). However, there is a paucity of information about zooplanktonic indicator species (such as those developed for phytoplankton by Reynolds et al. ]]>
et al. 2001, Cardoso & Marques 2004, Aoyagui & Bonecker 2004, Trevisan & Forsberg 2007).
The development of experimental approaches, and the capacity to control variables, have ]]>
et al. 2000, ]]>
et al. 2004).
The present study evaluates the temporal variability in the structure of zooplankton communities in lakes influenced by both natural flood pulse and anthropogenic operation of reservoirs. We tested the following hypotheses: (i) attributes of the zooplanktonic community are influenced by hydro-sedimentological phases; (ii) these attributes show ]]>
Sampling of zooplankton and environmental variables: Samplings were conducted every six months (potamophase in March and limnophase in September) between 2000 and ]]>
a concentration (µg/L) (Golterman et al. 1978), organic and inorganic suspended solids (mg/L), ]]>
et al. 1978, ammonia Mackereth et al. 1978, total phosphorus Golterman et al. 1978), and density of fish (catch per unit effort, CPUE) with standard lengths <7cm. The fish sample represents small species and young individuals from medium and large species; although this size group includes non-planktivorous species, the young individuals of larger species are potential consumers of zooplankton. These fishes were captured using ]]>
et al. (2009); further information on methods of water analysis and their spatio-temporal dynamics can be found in Roberto et al. (2009).
Zooplankton was sampled in the ]]>
et al. 2009). The samples were preserved in formaldehyde (4%) buffered with calcium carbonate. Individuals were identified to the lowest taxonomic level possible using taxonspecific literature (Vucetich 1973, Koste 1978, Reid 1985, Matsumura-Tundisi 1986, Segers 1995, Velho & Lansac-Tôha ]]>
3. At least 80 individuals were counted (Bottrell et al. 1976) in each of three sequential samples, obtained with a Hensen-Stempell pipette (2.5mL).
The zooplankton ]]>
Uni-dimensional dependent variables (species richness, abundance, Shannon diversity index, and evenness) ]]>
et al. 2009).
Local and hydro-sedimentological effects on community attributes (species richness, abundance, Shannon diversity index, and evenness) were evaluated with a Bayesian model analogous to factorial ANOVA, aiming to verify how hydro-sedimentological variations influence the attributes of the zooplankton community in the studied lakes. Hydro-sedimentological effects consisted of two levels (potamophase and limnophase), while ]]>
ab (community attributes of phase a and locality b), were normally distributed (μab, σ2) with ε~N(0, σ2), where E(Yab)=µ0+αa+βb +αβab+ε. In this model, µ0 is the mean of the data, α is the effect of the ]]>
a and b are phases and locality levels, respectively. We assumed a priori non-informative, approximately normal distribution (0, 103; mean and standard deviation, respectively) for the parameters of this equation. The Bayesian credibility interval for the hydro-sedimentological and local effects was simulated using Markov chain Monte Carlo methods with 20 000 iterations and a burn-in of 1 000 iterations. All the chains ]]>
We used the Pearson correlation to determine how attributes covariate within communities; and if they were associated with water levels (mean of the 30 days before samplings; because it represent a temporal dynamic of the water level that can contribute to temporal ]]>
Variations in the structure of the zooplankton community were summarised using NMDS, searching the best solution for representation in two dimensions. NMDS does not require assumptions about the distribution patterns of species abundance and is suitable for ecological data structures inflated by zeros (McCune & Grace 2002). Differences between limnophase and ]]>
et al. 1985) with 10 000 randomizations. This is a non-parametric permutation procedure applied to a previously defined similarity or dissimilarity matrix. We used the Bray-Curtis dissimilarity method, conducting the analysis with transformed data to reduce discrepancies amongst the abundances of different species [log2 (x+1), where x represents the abundance of individuals (m3)]. Rare species, defined as ]]>
Associations of environmental variables with community structure were determined by Envfit. Envfit is an function of the Vegan package (R programming language) that determines the environmental vectors that best represent the ]]>
et al. 2008). To avoid collinearity, we removed some environmental variables that were highly correlated (r>0.70). Following this criterion, water temperature and pH were eliminated owing to their high correlations with dissolved oxygen.
Once we verified ]]>
a concentration, as an indicator of food resource availability, and fish density (standard length<7cm), as an indicator of predation pressure. We considered ]]>
2) with ε~N(0, σ2), where E(Yi)=β0+β1xi+β2xi+ε. We also considered that the parameter β1 (fish den-sity) presented a priori a non-informative nor-mal distribution, β1~N(0, 103). Moreover, the parameters β0 (intercept) and β2 (chlorophyll a concentration) were normally distributed with positive values N ]]>
3); because, the food availability β2 always has a positive effect on zooplankton abundance. The Bayesian credibility interval for the regression coefficients was simulated using a Markov chain Monte Carlo method with 100 000 iterations, a burn-in of 1 000 iterations, and a thinning interval of 15 to minimise autocorrelation. All the analysed chains reached convergence.
The analyses were ]]>
et al. 2008) for the multivariate analyses and BRugs for the Bayesian analyses.
Results ]]>
Zooplankton composition and diversity: The zooplankton community was represented by 342 species, including 196 rotifers, 76 testate protozoans, 50 cladocerans, and 20 copepods. Guaraná Lake contained 267 species; Garças Lake, 242 species; and Patos Lake, 189 species. Seventy species were restricted to Garças Lake, 42 species to Guaraná Lake, and 13 species to Patos Lake. A total of 143 species were common to all ]]>
The mean species richness was highest in Patos Lake (mean=40, SD=12), followed by Guaraná Lake (35; 14) and Garças Lake (29; 12). The a posteriori credibility interval pointed to differences in the effects of locality on species number (Fig. 3a), mainly between Garças Lake, which had the lowest ]]>
Fig. 3b). The a posteriori credibility interval of the hydro-sedimentological phase effects indicated a positive effect of the limnophase on community abundance. Rotifers were the most abundant group, and Testate amoebae was the least abundant one (Fig. 4). In ]]>
Species diversity and evenness presented patterns of variation similar to species richness, with a strong effect for the interaction between locality and seasonality (Fig. 5a and b); this interaction was characterized by lower values of evenness (mean=0.48) and Shannon diversity (mean=2.7bits/ind) during limnophase in Garças Lake, suggesting a negative effect of the limnophase in this locality. On the other hand, the same period showed a positive effect on species diversity (3.2bits/ind) and evenness (0.69) in Patos Lake. No hydrosedimentological phase effects were detected in Guaraná Lake.
Relationship between community attributes and water level: Community attributes presented significant correlations with each other (Table 3). Increased species abundance was associated with decreased Shannon diversity index and evenness. Thus, at lower abundances, the species were distributed more uniformly, and, consequently, diversity was higher. Therefore, the most frequent association observed was between evenness and Shannon diversity index; i.e. homogeneous distributions amongst organisms favoured an increase in the Shannon diversity index. Elevation of water levels was associated with decreased zooplankton abundance, thereby increasing the Shannon diversity index and evenness in these communities.
Structure of the zooplankton community: The hydro-sedimentological phases (potamophase and limnophase) were characterized by different structures of the zooplankton communities in the three lakes (Fig. 6; MRPP<0.01). IndVal results (Table 4) showed that 48 of 342 species significantly distinguish the hydrosedimentological phases, with 20 species characteristic of the limnophase and 28 species characteristic of the potamophase.
In Patos and Guaraná Lakes, the limnological features most associated with community structure were dissolved oxygen and inorganic suspended solids in the limnophase, and electrical conductivity in the potamophase. Lower values of dissolved ]]>
A large number of variables were ]]>
]]>
Intra-annual variability of trophic relationships in the zooplankton community: Biological factors likely responsible for variation in abundance were analysed with a Bayesian multiple regression model that suggested positive associations between zooplankton abundance and chlorophyll a concentration during limnophase (Fig. 7a). It is likely that an increase in resource availability during this phase favours an increase in total abundance. During potamophase, in ]]>
Fig. 7b), suggesting an effect of predation.
Bayesian a posteriori probabilities (0.99, 0.98, and 1.00; Patos, ]]>
Discussion
Zooplankton composition and diversity: Lansac-Tôha et al. (2009) recorded about 540 ]]>
et al. 1999, Aoyagui & Bonecker 2004, Alves et al. 2005). In general, ]]>
et al. 2004). Ward & Tockner ]]>
]]>
The high accumulated species richness values in Guaraná Lake (267 species) and Garças Lake (242 species) are likely due to temporal replacements of local fauna in these lakes; species frequently observed at the beginning of the study gradually disappeared, and other species started to appear during the time frame of the study. An increase in the frequency of hydrodynamic disturbances in the Paraná River (many short flood pulses) might have negatively influenced the occurrence of common species, and favoured species resistant to ]]>
et al. 1999), which also affects the downstream lakes.
Interestingly, high values of accumulated richness did not result in greater mean diversities. ]]>
et al. 2009) contributed to qualitative impoverishment and replacement of aquatic biota in ]]>
Some studies have suggested that floods lose substantial characteristics in localities where ]]>
et al. 2006, Steinberg et al. 2009); the controlled floods that occur in these managed localities do not produce the same effects as observed under natural conditions. Under regulated conditions, flood characteristics are modified by, for example, reductions in sediment load, large variations in the frequency of the ]]>
Relationship between community attributes and water level: The associations of community attributes identified in this study (species richness, Shannon diversity index, evenness, and abundance) ]]>
et al. (2007) and Lindholm et al. (2007). These relationships characterize the behaviour of the zooplankton community according to two main scenarios: (i) at low abundances, fauna uniformly distributed, evenness increases, an increase in the diversity index is favoured, and species coexistence is promoted by minimizing competitive exclusion (Paidere et al. ]]>
Structure of the zooplankton community: Hydro-sedimentological phases were distinguished by the ]]>
et al. 1993, Lima et al. 1998, Rossa & Bonecker 2003, De Paggi & Paggi 2007; Henry et al. 2011), when the ]]>
et al. 2002). In contrast, during potamophase, we observed a dilution effect in which organisms were more dispersed in the water column (Bozelli 2000, Lansac-Tôha et al. 2009). Furthermore, the environmental conditions were disadvantageous for the development of ]]>
Seasonal patterns in the structure of zooplankton communities were strongly correlated with environmental variables: dissolved oxygen, inorganic suspended solids, and electrical conductivity. These variables were indicative of processes that ]]>
Community structure in Garças Lake was characterised by inter-annual variations related to variations system productivity. The upstream reservoir reduced sediment transport and promoted increase in water transparency and a ]]>
et al. 2009). In this lake, there was an increase in the number of environmental variables associated with the structure of the zooplankton community, indicating that this local community is more susceptible to sources of variation. This effect is attenuated in Guaraná Lake, because the particular biogeochemical composition of this site sustains nutrient levels higher than those present in the influx waters from the Paraná River.
]]>
Species that characterize limnophase occur at higher abundances and frequencies in this period. Amongst them, Keratella cochlearis has shown high abundances during dry periods in both natural and affected environments (Beaver et al. 1998, Rossa & Bonecker 2003, Cardoso & Marques 2004). The reproductive effort this species is highest in productive habitats in controlled experiments (Nagae unpublished data). The increased ]]>
et al. 1997, Lima et al. 1998, Branco et al. 2000, Rejas et al. 2005).
In potamophase, ]]>
Lecanidae, Epiphanes clavatula, and Dipleuchlanis propatula propatula (littoral rotifers), Chydoridae species (littoral cladocerans) and Moina reticulata (a pelagic cladoceran) were frequently observed during potamophase in other studies conducted in this same floodplain (Lima et al. ]]>
et al. 2005).
Intra-annual variability of trophic relationships in the zooplankton community: Data on chlorophyll a concentrations support the hypothesis that food availability increases community abundance during limnophase periods, reflecting a positive ]]>
et al. 1998, Azevedo & Bonecker 2003, Trevisan & Forsberg 2007). A negative association of zooplanktonic abundance with fish density was observed in Guaraná and Patos Lakes, suggesting an effect of zooplanktivorous fishes. Zooplankton organisms are important components of the diets of small fish in lakes of the Upper Paraná River floodplain, mainly during potamophase (Russo & Hahn 2006, Crippa
et al. 2009, Hahn & Crippa 2006). The evaluation of these biotic interactions is complex because relationships can be concealed by the ways data are presented, or due the association correlates with others variables (Bonecker et al. 2012)”. For example, zooplanktivorous predation may be significant only on large-size individuals (size-efficiency hypothesis, Brooks & Dodson 1965); variables can have confounded each other, e.g. an increase in water transparency may ]]>
et al. 2001).
Thus, it is provable that trophic interactions, represented by the associations between zooplankton populations and resource availability, and zooplankton populations and predation, were evidently different in the two phases, showing a distinct trophic dynamic between limnophase and potamophase, as ]]>
et al. (2000). As suggested by Neiff (1996) and Thomaz et al. (2007), factors inherent to the hydro-sedimentological phases have different influences on aquatic communities. In potamophase, floods, which are regional-scale processes, result in dilution of the populations and homogenization of environments, whereas in limnophase, local processes, such as productivity, separately influence the succession of isolated communities. ]]>
Conceptual framework for variability in the structure of zooplankton communities in floodplains: The main variation sources of zooplankton communities in connected lakes, that are influenced by the flood dynamic in the Upper Paraná River floodplain, were summarized as follows (Fig. 8): ]]>
a) Flood dynamic processes, which influence the zooplankton community structure physically and biologically: Physically, flood dynamic processes are responsible for the expansion and contraction of environments because they define the size and conditions of the habitat, as well as the quantity and quality of resources. Biologically, the floods change the structure and dynamic of the ]]>
b) Variations in limnological ]]>
During potamophase, an increase in water transparency and electrical conductivity and a decrease in dissolved oxygen and chlorophyll a were associated with increased abundance of some species. During limnophase, a reduction in the size of water bodies increases available food resources, because productivity in each locality is enhanced by increased concentrations of nutrients and chlorophyll a. These conditions support the growth of opportunistic taxa that were able to exploit habitat conditions, resulting in increased species dominance and decreased species richness.
c) Factors intrinsic to each phase, which are related to resource availability and predation, which, in turn, influence the total abundance of zooplanktonic organisms: In limnophase, the greater availability of food resources supported high zooplankton abundances. In potamophase, however, despite the dilution effect due to the greater volume of ]]>
These findings emphasise the complexity of interactions between physical, chemical, and biological factors in floodplain environments, as noted by other authors, and highlight the important contribution of the hydro-sedimentological phases to the seasonal dynamic of the community. ]]>
The conceptual model presented above encompasses the interactions between diverse environmental ]]>
Acknowledgments
This work was supported by Conselho Nacional de Desenvolvimento a Pesquisa (CNPq) with financing of the Long Term Ecological Research; and Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior (CAPES). We thank the Nupélia’s laboratories of Limnology and ichthyology for their assistance with the physical and chemical variables of water and ]]>
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*Correspondencia: Nadson R. Simões: Universidade Estadual de Maringá-Nupélia/ Laboratory of zooplankton DBI-PEA, Av. Colombo, 5790, 87020-900, Paraná, Brazil; nadsonressye@yahoo.com.br Fábio A. Lansac-Tôha: Universidade Estadual de Maringá-Nupélia/ Laboratory of zooplankton DBI-PEA, Av. Colombo, 5790, 87020-900, Paraná, Brazil; fabio@nupelia.uem.br Luiz F. M. Velho: Universidade Estadual de Maringá-Nupélia/ Laboratory of zooplankton DBI-PEA, Av. Colombo, 5790, 87020-900, Paraná, Brazil; felipe@nupelia.uem.br Claudia C. Bonecker: Universidade Estadual de Maringá-Nupélia/ Laboratory of zooplankton DBI-PEA, Av. Colombo, 5790, 87020-900, Paraná, Brazil; bonecker@nupelia.uem.br 1. Universidade Estadual de Maringá-Nupélia/ Laboratory of zooplankton DBI-PEA, Av. Colombo, 5790, 87020-900, Paraná, Brazil; nadsonressye@yahoo.com.br, fabio@nupelia.uem.br, felipe@nupelia.uem.br, bonecker@nupelia.uem.br
Received 25-X-2011. Corrected 25-III-2012.Accepted 30-IV-2012.