The Temporal Asynchrony of Planktonic Cladocerans Population at Different Environments of the Upper Paraná River Floodplain

© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/08/612-0679

Internat. Rev. Hydrobiol. 93 2008 6 679–689

DOI: 10.1002/iroh.200711032

ERICA MAYUMI TAKAHASHI*, FÁBIO AMODÊO LANSAC-TÔHA,LUIZ FELIPE MACHADO VELHO and LUIS MAURICIO BINI

Nupélia, Postgraduate Course in Ecology of Continental Aquatic Environments, Universidade Estadual de Maringá. Av. Colombo, 5790, Maringá-PR, 87020–900, Brazil;

e-mail: [email protected]

Research Paper

The Temporal Asynchrony of Planktonic Cladocerans Population at Different Environments of the Upper Paraná River Floodplain

key words: Cladocera, abundance, spatial synchrony, spatial and temporal heterogeneity, Brazil

Abstract

The aim of this study was to investigate the existence of synchronic fluctuation patterns in cladoceran populations of the Upper Paraná River floodplain. The following hypothesis were tested: (i) the popula-tions of a given species present the same fluctuation pattern in abundance for different environments and (ii) synchrony is higher when we consider subsets of neighboring environments or those belonging to the same category (e.g., lagoons, rivers). Samplings were performed every three months from Febru-ary 2000 to November 2002 at 11 sites. To evaluate spatial synchrony, the intraclass correlation coef-ficient was used. The results showed no significant correlation for the most abundant species, meaning that fluctuation patterns of planktonic cladocerans were asynchronous. Asynchrony indicated that the influence of floods and regional climatic factors was not strong enough to synchronize the populations, suggesting that local factors were more important than regional effects in determining zooplankton abundance patterns. The implications of these results are that the observations from a single environment cannot be extrapolated to other environments in a manner that would allow its use as a sentinel site. This means that a monitoring program for floodplain systems, or at least for the Paraná River floodplain, has to comprise greater spatial extents.

1. Introduction

Temporal and spatial fluctuations of abundance are notable features of all animal popu-lations (HEINO et al., 1997). Ecologists have had a special interest in spatial synchrony since MORAN demonstrated it in quantitative terms (MORAN, 1953). ROYAMA, after analyzing this paper, restated “if two regional populations have the same intrinsic structure (density-dependent), they will be correlated under influences of density-independent factors (i.e., climatic factors), if the factors are correlated between the regions” (ROYAMA, 1992). In this way, there is a common extrinsic factor guiding fluctuations of distinct populations; there-fore, synchrony exists between them. ROYAMA (1992) calls this phenomenon the “Moran effect” and affirms that the importance of this theorem is that the cause of spatial synchrony can be completely independent of the cause of population cycles.

KRATZ et al. (1987) interpreted similar regional patterns of population variability as evi-dence that the population densities were determined by density-independent factors (i.e.,

* Corresponding author

680 E. M. TAKAHASHI et al.

© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com

climate) operating on regional scales. The absence of synchrony suggests that local scale regulators are more important in determining population fluctuations. MAGNUSON (1990), studying synchrony in limnological variables in a suite of American lakes, defined temporal coherence as the degree in which different environments behave similarly over time. The degree of temporal coherence can indicate whether the populations within a region are influ-enced more by local (intrinsic) or regional (extrinsic) factors, a central question in population ecology (NICHOLSON, 1933; ANDREWARTHA and BIRCH, 1954).

One of the most important aspects in spatial synchrony studies is the fact that increases in spatial synchrony decreases metapopulation life expectancy (PARADIS et al., 1999). Altera-tion in a regional factor, strong enough to cause the extinction of a local population, leads all populations that fluctuate synchronously to the same risk. Moreover, if this synchrony is high, several population models are invalidated because they assume complete asynchrony, which is the most adequate setting for metapopulation persistence (HANSKI and WOIWOD, 1993).

The practical importance of studying this phenomenon is the possibility of predicting environmental changes (HUDSON and CATTADORI, 1999). BURROWS et al. (2002) stated that populations presenting no correlated dynamics (asynchrony) need to be monitored in more environments. Population with synchronized dynamics could be monitored in a few environ-ments in order to detect changes, giving rise to a decrease in sampling effort. In addition, spatial synchrony favours the extrapolation of the results from an environment or set of environments and the application of adjacent environments as a reference to evaluate the effects of different treatments in entire ecosystem experiments (ANNEVILLE et al., 2004).

Regarding the zooplankton community, some studies have observed evidences that local conditions prevail in structuring plankton communities, in other words, the importance of intrinsic factors controlling population fluctuations (LANSAC-TÔHA et al., 1997, 2004; COT-TENIE et al., 2001; ALVES et al., 2008).

Among zooplankton groups, cladocerans have a great ecological importance in freshwater ecosystems since they act as a link in the food chain: most of them are herbivorous, feed on phytoplankton and, in turn, are preyed upon by certain invertebrate and fish predators. Due to their high filtering feeding rate are capable to maintain water clearance and they can be used in monitoring and conservation programs aiming to improve water quality (DODSON and FREY, 2001; DUMONT and NEGREA, 2002; SARMA et al., 2005).

If extrinsic factors like flood (JUNK et al., 1989; NEIFF et al., 2000; THOMAZ et al., 2007) and climatic factors like temperature and precipitation (ROCHA, 2003) exert regional influ-ence on the entire floodplain, driving populations dynamics, the following expectation must be refuted: the populations of a given species present distinct fluctuation pattern (temporal coherence) in different environments, i.e., they present spatial asynchrony. Here, this predic-tion was tested by studying the fluctuations in cladocerans densities in the Upper Paraná River floodplain.

2. Methods

2.1. Study Area

This study was carried out in different environments of the Upper Paraná River floodplain (22°40´–22°50´ S and 53°10´–53°40´ W) in the States of Mato Grosso do Sul and Paraná, Brazil. This ecosystem presents a braided channel, low declivity and an extended floodplain (SOUZA FILHO et al., 2004) (Fig. 1).

For this study, 11 sampling sites were established, encompassing three rivers (Paraná, Baía and Ivin-heima), two channels, three connected lagoons (those directly connected to the rivers all year round) and three isolated lagoons (those with no direct connection to the rivers) (Table 1). These rivers present different current velocity and limnological characteristics. The lagoons analyzed are shallow and have limnological features similar to the rivers to which they are associated (THOMAZ et al., 2004).

Temporal Asynchrony of Planktonic Cladocerans 681


Figure 1. Study area and sampling stations. 1. Paraná River; 2. Baía River; 3. Ivinheima River; 4. Ipoitã Channel; 5. Curutuba Channel; 6. Garças Lagoon; 7. Patos Lagoon; 8. Fechada Lagoon;

9. Guaraná Lagoon; 10. Ventura Lagoon and 11. Osmar Lagoon.

Table 1. Environments studied from the Upper Paraná River floodplain and categories of aquatic ecosystems that were used in this study (r = river, c = channels, cl = connected

lagoons and il = isolated lagoons), area and mean depth.

Environments Categories Area (ha) Mean depth (m)

Paraná r 4.00Ivinheima r 3.90Baía r 3.20Ipoitã c 3.20Curutuba c 2.70Garças cl 14.10 2.00Patos cl 113.80 3.50Guaraná cl 4.20 2.10Fechada il 7.50 2.46Ventura il 89.80 2.16Osmar il 0.006 1.10



2.2. Sampling and Data Groups

Sampling was performed every three months from February 2000 to November 2002 by filtering 600 L of water per sample from the subsurface of the pelagic region of the environments using a motor-ized pump and a plankton net (68 μm mesh). The samples were fixed in 4% buffered formalin. Osmar Lagoon (isolated lagoon) was dried up in August and October 2001, thus precluding sampling.

Although the temporal sampling resolution could be considered too long for a group of organisms which present low turnover rate, much of environmental availability inherent to high dynamics flood-plains could be lost, the main concern in population synchrony studies is exactly the opposite, that is, it is necessary to minimize the overlap between consecutive measurements to minimize temporal autocorrelation. Thus, we think that the increasing of sample size by interpolation could generate the opposite effect: pseudoreplication and increase possibility of concluding that a correlation is statistically significant when, in fact, it is not (PYPER and PETERMAN, 1998). For example, RUSAK et al. (1999) used annual average of zooplankton abundance to evaluate temporal coherence.

Quantitative analyses were undertaken from subsamples obtained using a Hensen-Stempell pipette (2.5ml). At least 100 individuals per subsample were counted using a Sedgewick-Rafter counting cell and an optical microscope. The counting procedure was based on methodology proposed by BOTT-RELL et al. (1976), where three subsequent subsamples were established for each sample. Samples with few individuals were counted integrally. Density was expressed in individuals · m–3.

Fluviometric level data were furnished by Agência Nacional de Águas (ANA).

2.3 Data Analysis

To evaluate the existence of temporal coherence among the populations of each species among the environments, we used the intraclass correlation coefficient, ri, which quantifies the degree of synchrony in the abundance between two or more populations over time. In a comparison between n environments, the intraclass correlation coefficient (ri) was estimated as:

ri = MSM – MSE / MSM + (n – 1) MSE ,

where MSM and MSE are the mean squares for months and error (also from the factor “months”) from a two-way ANOVA (environments and months) without replication. When synchrony increases, MSE approaches 0 and ri approaches 1. When fluctuations are asynchronous, MSE increases until it is greater than MSM (there is more variability within months than among months) and ri becomes negative.

Detailed information about this correlation coefficient can be found elsewhere (RUSAK et al., 1999). For this analysis, abundance data were previously log transformed (log x + 1).

To analyze spatial synchrony in subsets, ri was also calculated among different environments associ-ated with the rivers (Paraná, Baía and Ivinheima) and among different types of environments (rivers, channels, connected and isolated lagoons).

More detailed analyses were made to verify whether the environments present any significant correla-tion. We used Spearman’s correlation for the abundance of a given species in different environments. All analyses were performed using Statistica (STATSOFT, 1996).

3. Results

3.1. Fluviometric Level

During 2000, the Paraná River presented no floods and the dry seasons were clearly dif-ferentiated (Fig. 2). There were short-term fluctuations related to the flow control exerted by upstream dams, mainly Porto Primavera Reservoir. In the next year, no expressive flood period was recorded, but we did observe two distinct periods: January to June, with a dry period in March, and July to November, with prevailing values below 170 cm. On the other hand, between January and March 2002, predominate high fluviometric levels, character-izing a flood period, and afterwards, short fluctuation periods were observed (Fig. 2).



3.2. Cladoceran Assemblage

We recorded a total of 57 cladoceran species. The most frequent and abundant cladocerans were Bosmina hagmanni (29%), Ceriodaphnia cornuta (24.7%), Moina minuta (15%), Bos-minopsis deitersi (10.9%), Diaphanosoma spinulosum (7.9%) and Daphnia gessneri (4.4%). Patterns of spatial synchrony in population dynamics were analyzed only for these species.

3.3. Temporal Fluctuation and Spatial Synchrony

Considering that temporal coherence estimates the “parallel” nature of patterns among environments (RUSAK et al., 1999), it is useful to observe the number of times that the graph lines cross. As abundance fluctuations of these species were not synchronized (see results below), it was possible to note several crossed lines (Fig. 3).

Analyses considering different subsets (environments associated with different rivers and belonging to the same type) were also performed. However, as can be seen through intraclass correlation coefficient results, none of them were significant (P > 0.05) (Table 2).

We can also observe that all coefficients were negative, except for the coefficient calculat-ed for B. hagmanni in environments associated with the Paraná River (Table 2 and Fig. 4).

The calculated coefficients were placed in the coherence plane (RUSAK et al., 1999), inside of the area that delimitates the predominance of local factors. In other words, there was no regional spatial synchrony. The intrinsic factors acting in each environment are the main responsibles for temporal fluctuations in species abundances (Fig. 4). However, due to small sample size (months were analyzed for each sampling site) and large sampling interval (higher than the species’ generation times) all synchrony analyses carried out in this study should be considered conservative.

Spearman’s correlation results indicate some significant and isolated correlations (Table 3). These correlations ranged from 0.58 to 0.87. D. spinulosum and C. cornuta presented the highest number of pair of sites with significant correlations. In most comparisons, significant

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Figure 2. Paraná River fluviometric level measured daily in Porto São José. The arrows indicate sampling periods.



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M. minuta

Figure 3. Time series of dominant Cladocera population densities at the Upper Paraná River floodplain.

Table 2. Intraclass correlation coefficients (ri) for abundance data (log x + 1) of cladoceran species.

Species all envi-ronments

Paraná Baía Ivinheima rivers isolated lagoons

connected lagoons

channels

ri ri ri ri ri ri ri ri

B. hagmanni –0.07 0.07 –0.22 –0.16 –0.50 –0.16 –0.48 –0.98B. deitersi –0.10 –0.50 –0.21 –0.33 –0.50 –0.50 –0.50 –1.00C. cornuta –0.09 –0.21 –0.26 –0.33 –0.46 –0.50 –0.44 –1.00D. gessneri –0.10 –0.21 –0.21 –0.33 –0.50 –0.50 –0.50 –0.60D. spinulosum –0.08 –0.50 –0.24 –0.33 –0.40 –0.40 –0.38 –0.75M. minuta –0.10 –0.50 –0.19 –0.33 –0.50 –0.50 –0.27 –1.00



correlations were detected for only one or two species. In the Paraná River and Ipoitã Chan-nel and in the Baía River and Curutuba Channel comparisons, significant correlations were detected for three species, respectively.

4. Discussion

The most abundant species recorded in this study were Bosmina hagmanni, Bosminopsis deitersi, Ceriodaphnia cornuta, Daphnia gessneri, Diaphanosoma spinulosum and Moina minuta, representative of typically planktonic families. These species have been frequently recorded as the most abundant in plankton from several Brazilian inland aquatic ecosystems (NOGUEIRA, 2001; SAMPAIO et al., 2002; NEVES et al., 2003; LANSAC-TÔHA et al., 2004).

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Figure 4. Temporal coherence of cladoceran species in every environment and in different subsets. Species inside of area (A) have their abundances determined by intrinsic factors, while species to the right of the dotted curve (area B) are predominately extrinsically regulated. Values to the left of the

solid curve are not possible (area C).



The results of intraclass correlation analyses indicate the absence of spatial synchrony among populations of the same species in different environments. Regarding the predic-tion of the negative relationship between spatial distance among environments and spatial synchrony (HANSKI and WOIWOD, 1993; RUSAK et al., 1999), a new intraclass correlation analysis was performed considering neighboring environments associated with the same river which indicated absence of spatial synchrony. According to COTTENIE et al. (2001), neighboring and even interconnected environments may be different in relation to zoo-plankton community dynamics, and these differences are strongly related to the differences in trophic structure and biotic interactions in these environments. RUSAK et al. (2002) also found greater influence of spatial variability on the zooplankton dynamics in studies under-taken in American temperate lakes.

VELHO et al. (2003), studying the distribution of testate amoebae abundance on this floodplain, suggest that spatial heterogeneity is more important than temporal variability in determining the patterns of abundance distribution. It is necessary to consider, however, the effects of upstream damming (e.g., Porto Primavera Reservoir), which decreases the amplitude and duration of the floods (SOUZA FILHO et al., 2004). This may be decreasing the influence of these events on the regional dynamics of aquatic communities in the Upper Paraná River floodplain as a whole. WEBSTER et al. (2000), analyzing temporal dynamics of

Table 3. Significant Spearman’s correlations (rS; P < 0.05) among species abundances in different environments.

B. hag-manni

B. deitersi C. cornuta D. gessneri D. spinulo-sum

M. minuta

Paraná R. × Garças L. 0.59Paraná R. × Osmar L. 0.70 0.77Paraná R. × Ipoitã C. 0.65 0.73 0.64Paraná R. × Fechada L. 0.62Paraná R. × Ivinheima R. 0.84Baía R. × Guaraná L. 0.76Baía R. × Osmar L. 0.68 0.64Baía R. × Curutuba C. 0.72 0.63 0.66Ivinheima R. × Fechada L. 0.61 0.71 0.81Ivinheima R. × Osmar L. 0.71 0.70Ivinheima R. × Guaraná L. 0.61Ivinheima R.× Curutuba C. 0.67 0.67Ivinheima R. × Ipoitã C. 0.83Garças L. × Patos L. 0.68 0.66Garças L. × Curutuba C. 0.65Osmar L. × Ipoitã C. 0.87Osmar L. × Guaraná L. 0.70 0.72Guaraná L. × Ipoitã C. 0.65Guaraná L. × Patos L. 0.77Fechada L. × Curutuba C. 0.70Fechada L. × Ipoitã C. 0.64Patos L. × Ipoitã C. 0.58Ventura L. × Curutuba C. 0.84

R. = riverL. = lagoonC. = channel



limnological variables, concluded that synchrony tends to be higher in lakes with relatively simple hydrology.

Since environments belonging to the same category (e.g., lagoons) could present similar limnological characteristics (independent of spatial distance among environments), leading populations to fluctuate similarly, we also estimated intraclass correlations considering these subsets. However, synchronous patterns were not observed.

The results from the Spearman’s correlation analysis showed some significant correlations that could suggest synchrony. The abundances of B. hagmanni were correlated between Baía River and Guaraná Lagoon, adjacent and permanently interconnected environments. Other significant correlations were observed for B. hagmanni and C. cornuta among environments associated with the same river. These correlations suggest synchrony, determined, however, by the proximity and connectivity of these environments and were probably independent of the influence of regional factors.

Significant correlations were also recorded among populations from environments belonging to different categories and associated with different rivers (e.g., the significant correlation observed for M. minuta between Ivinheima River and Fechada Lagoon). These correlations were considered to be determined by chance given the large number of correla-tions that were calculated.

Thus, the results obtained from Spearman’s correlation suggest that, in the Paraná River floodplain, population dynamics would not be determined by regional factors, as proposed by the Moran effect. The central idea of the Moran effect is that locally regulated populations would be synchronized if environmental events were regional (BJØRNSTAD et al., 1999). In this study, floods and climatic factors (e.g., temperature and precipitation) are the probable events that could exert regional effects on cladoceran assemblages. Our results do not show that these regional factors were not acting. However, they indicate that these events were not preponderant in determining the temporal fluctuation of populations. In other words, regional events can influence communities from distinct environments on a floodplain; however, in different ways, depending on local features.

The absence of synchrony is likely to be generated predominantly by environmental heterogeneity and its interaction with wide-scale temporal and environmental variability (SUTCLIFFE et al., 1996). In addition, local environmental constraints can be strong enough to structure local communities (COTTENIE et al., 2003)

Thus, the absence of spatial synchrony among planktonic cladoceran populations from distinct environments of the Upper Paraná River floodplain suggests that spatial heterogene-ity is more important than regional effects in determining zooplankton abundance patterns.

Even considering a possible limitation of this study regarding temporal resolution to evaluate the importance of regional and local factors, the implications of our study are that the results obtained from a single environment cannot be extrapolated to other environments in a way that would allow its use as a sentinel site. This means that a monitoring program for floodplain systems, or at least for the Upper Paraná River floodplain, has to comprise greater spatial extents.

5. Acknowledgements

This study was supported by Science Governmental Agency (CNPq/LTER Program) and Nupélia/PEA-UEM. The authors wish to express their gratitude to CLAUDIA COSTA BONECKER for suggestions and criticism and JOHN JERVIS STANLEY JR. and DAVID HOEINGHAUS for English review.



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Manuscript received November 2nd, 2007; revised February 29th, 2008; accepted May 19th, 2008

Documents

The Temporal Asynchrony of Planktonic Cladocerans Population at Different Environments of the Upper Paraná River Floodplain