International Review of Hydrobiology 2013, 98, 24–33

DOI 10.1002/iroh.201201473

RESEARCH ARTICLE

Drought disturbances increase temporal variability of zooplankton community structure in floodplains
Nadson R. Simões, Fábio A. Lansac-Tôha and Claudia C. Bonecker
Departamento de Biologia, Universidade Estadual de Maringá, Maringá, PR, Brazil

The present study verified how hydrological regime affects the temporal variability of zooplankton communities in floodplains. Multidimensional methods were employed to characterise community variability, and the temporal trend of the community was also evaluated using a matrices comparison procedure. In connected ponds from the main river, the absence of floods (drought) modified the variability of the zooplankton community by increasing temporal dissimilarity of community. In these environments, the periodic input of water due to floods maintained a lower variability of environmental characteristics, sustaining a lower temporal variability of the community. This observation suggests that, in floodplains, flooding is a component of the system that assists with both the maintenance of ecological processes (temporal variability of the community) and the high biodiversity of these environments. This study therefore suggests that the temporal variability of communities in floodplains is increased by extended droughts, and emphasises the importance of flood dynamics to maintain temporal stability of zooplankton communities in river floodplain systems. Keywords: Connectivity / Dry / Flood / Stability / Temporal trend / Temporal turnover

Received: March 22, 2012 Revised: August 20, 2012 Accepted: October 25, 2012

1

Introduction

Ecological systems are naturally dynamic and constantly reorganising themselves according to environmental variations [1]. Therefore, variability is a natural property of ecological communities [2] that can, at some levels, surpass the tolerance range of organisms, producing an adverse effect on populations [3] and causing changes in ecosystem function due to alterations in community structure, biodiversity loss and shifts in energy flow. Understanding this variability is essential for theoretical and applied studies in ecology as it allows us to: (i) identify the effects of extrinsic factors on ecological processes; (ii) understand the dynamics of ecological systems; (iii) identify the environmental range tolerated by organisms; and (iv) intervene rationally in activities of environmental
Handling Editor: Karsten Rinke Correspondence: Nadson R. Simões, Departamento de Biologia, Universidade Estadual de Maringá, PEA/Nupelia, Av. Colombo 5790, 87020-900, Maringá, PR, Brazil E-mail: nadsonressye@yahoo.com.br Fax: (55) 44 3011 4625

management and assist with the implementation of planning strategies and biodiversity conservation [4, 5]. Recently, the variability of communities has been used as a tool to describe ecosystem stability in order to understand how ecological systems respond to natural and anthropogenic disturbances [6–9]. Disturbances are defined as events in time that disrupt the natural development of the ecosystem, community or population and change the availability of resources and physical conditions [10]. In general, the disturbance either removes individuals or acts within the tolerance limits of organisms by affecting reproduction, growth and survival [11]. Identifying and differentiating the variability produced by natural and anthropogenic situations is a strategy for developing a better understanding of ecological systems. This study was conducted in a region with conspicuous and natural environmental fluctuations (floods) that is also subject to anthropogenic impacts, due to an upstream cascade of reservoirs that has generated several changes in the hydrodynamic, physical, chemical and biological aspects of the water [12–15]. The reservoirs affect the aquatic communities as they reduce the variation in the natural range of water level, modifying the periodicity of 24

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These ponds had a depth ranging 1. one connected (CP) and the other isolated (IP) from the main river. where the Upper Paraná River floodplain is situated 22°300 and 23°000 South latitude. In general. We predicted that the temporal variability of the community would be increased when there are changes in the natural variability of the system. whereas the second period (2005–2006) was characterised by floods typical of the Baia and Paraná rivers but was the driest period for the Ivinheima River. 2). secondary channels. Weinheim . a drought occurred in the Baia and Paraná 2 Methods The hydrographic basin of Paraná River is the second largest in South America in terms of length and drainage area [18].eim sy a ste m IP IP Paraná Sub-system CP IP 0 23 00’ 53 30’ o o Isolated Pond Connected Pond 2. In this way.e. the aquatic landscape is formed by rivers. IS and BS). fluvial connectivity index (i.5km CP 23 00’ o Scale Flow direction Figure 1. Each sub-system has one pond isolated from and one pond connected with the main river. Ivinheima and Baia sub-systems. backwaters and connected. but its ecological integrity has recently been threatened by the operation of reservoirs [15. 98. Samples were collected quarterly during two periods (2000–2001 and 2005–2006) in six ponds associated with South America 53o 30’ 53o 15’ BRAZIL Baia Sub-system IP CP CP 22 45’ o Iv Su inh b. Thus. Drought disturbances increase zooplankton variability three large rivers of the regions (the Paraná. respectively. this floodplain occupies an area exceeding 802 150 km2 and plays an important social and economic role through tourism and fishing activities common to this ecosystem.1–3.International Review of Hydrobiology 2013. the ratio between the number of days under potamophase (high water period) and the number of days of the year) [18] and water level variation graphs (Fig.8 ha (species richness was not correlated with pond area). each pond was sampled 16 times (except IP in the PS. Thus. At its upper stretch. Paraná. eight samples during 2000–2001 and eight during 2005–2006. 19]. collecting a total of 94 samples. flood amplitude.5 5. the ponds showed high variability of abiotic characteristics due to flood temporal dynamics (see summary. Appendix 1). We studied two periods with distinct hydrological features. the present study aimed to verify whether the temporal variability in the zooplankton community in two distinct sets of ponds (connected or unconnected to the main river) responds differently to hydrological variation related to the presence or absence of floods. 24–33 floods and. In Brazilian territory. For each sub-system we selected two ponds. KGaA. 1. This study is part of a long-term ecological research project begun in 2000 [13]. 53°000 and 53°300 West longitude. The hydrological variation was compared using flood intensity. The floodplain is also of environmental importance as a system with high biological diversity.01 to 113.5 m. abbreviated as PS. the ecological dynamics of riverfloodplain systems [16.0 7. in the period 2000–2001. 25 © 2013 WILEY‐VCH Verlag GmbH & Co. Location of the sampling in the Upper Paraná River floodplain. consequently. Ivinheima and Baia Rivers) that form three distinct sub-systems (Fig. temporary and isolated ponds [19]. which was sampled 14 times due to complete drying of the pond). 17]. and an area ranging from 0. The first period (2000–2001) was characterised by a drought that affected the water level of the Baia and Paraná rivers but did not affect the Ivinheima River.

divergence or no pattern of directional change. maximum level. 2). Weinheim 2. in an effort to define a geometric order in the relative abundance among species (for details. R. 98. sub-systems (both influenced by floods of the Paraná River). The material was preserved in a formaldehyde solution (4%) buffered with calcium carbonate. Water level has been highlighted because is responsible for drive expansion and contraction of environments. and the distances between the sampling units and their respective centroids were evaluated. we performed factorial analyses of variance. Here. Data were transformed into log2(x) þ 1. PA. The species (rotifers. CI. the drought event was our main categorical variable. cladocerans and copepods) were identified using specialised literature (see [13]). The temporal trend of the community was assessed using time lag analysis [25] in order to assess whether each community had convergence. Data were log transformed to achieve the assumptions of normality and homoscedasticity. while the Ivinheima sub-system was drier in the period 2005–2006 (Fig. Simões et al. For the PCoA. a centroid for each group (drought and flooded periods) was calculated in a space of principal coordinates.6 for Ivinheima River [20.5 for Paraná River and 2. In order to test if the temporal variability of the zooplankton community in each pond differed between drought and flooded periods. Thus. The difference between groups was estimated using a permutation test. At least 80 individuals were counted in three subsequent subsamples [23] obtained with a Hensen-Stempell pipette (2. KGaA. Zooplankton organisms were quantified using a Sedgewick-Rafter chamber under an optical microscope. The assumptions of normality and homoscedasticity were previously tested using Shapiro–Wilk and Levene tests. Species that had one occurrence in each period were removed from the analysis to minimise identification errors and to improve the quality of the multivariate analyses. International Review of Hydrobiology 2013. and biotic interactions (see [22]). Daily variation of water level of the Paraná and Ivinheima rivers (2000–2008). This method tests the variability between groups by calculating a multivariate dispersion measure using a PCoA (Principal Coordinate Analysis).5 mL). see [24]). This design allowed us to test the community variability in distinct hydrological situations independent of the periods studied. Groups occurring at greater distance from the centroids suggest greater variability in relation to the group found at lower distances. 21]. We ran a factorial analysis of variance to test the difference in environmental variability between the types of ponds and periods. potamophase amplitude. The water level of reference used to indicate the threshold between potamophase and limnophase (low water period) [18] to characterise flood pulses was the level at which river water overflowed into the isolated ponds. Rectangles define the sampling periods. this value was 3.1 Data analysis In order to verify the existence of differences in the richness and abundance of the zooplankton community between the connected and isolated ponds in the two 26 . and the Bray–Curtis distance of dissimilarity was used. analysed periods (drought and flooded). Arrows show the sampling date. fluvial connectivity index. 24–33 Figure 2. The vertical dotted line indicates overflow level. Highest coefficient of variation suggest highest environmental variability. convergence means decreasing © 2013 WILEY‐VCH Verlag GmbH & Co. we used the procedure proposed by Anderson et al. The environmental variability of each pond was estimated by calculating the coefficient of variation for each limnological feature in each period (drought and flooded). respectively. MI. Zooplankton communities were sampled under the water subsurface of the pelagic region at each pond in the morning using a pump to filter 600 L of water per sample through a plankton net (68 µm).N. [24].

a positive relationship was observed between the matrix of the dissimilarity coefficient and the matrix of time lag (Mantel. Total alkalinity and chlorophyll a were more variable in the isolated ponds in both periods (F1.05).International Review of Hydrobiology 2013. Table 1). p ¼ 0. Bosmina hagmanni. the temporal variability of community structure was more similar between the two hydrological periods. 3d).64. pH. For © 2013 WILEY‐VCH Verlag GmbH & Co.1 Environmental variability There was no difference in water temperature. That means the hydrological variation did not affect equally the types of ponds (Fig. with higher values in the connected ponds (Table 1). A significant positive association between the Simpson dissimilarity matrix and the matrix time lag indicates an increase in community dissimilarity over time. 3a and c). using the packages ‘vegan’ [30] and ‘simba’ [31]. although the area formed in the drought period by graphic representation was relatively smaller than that formed in the flooded period. 3. a community dissimilarity matrix is regressed with increasing time lags to yield a measure of the rate and nature of community change over time (for details. (a) Firstly. dissolved oxygen. the zooplankton community in connected ponds diverged temporally. Ceriodaphnia cornuta (cladocers). suggesting divergence of the community from its initial configuration. Notodiaptomus amazonicus and Thermocyclops minutus (copepods). while a significant negative correlation indicates a community trend to reverse the dominance pattern among species. This approach is a community-level extension of autocorrelation analysis [25]. while in the flood period the composition did not demonstrate a trend of temporal modification. 3. the maintenance of species rank during each sampling period was measured using the non-parametric Kendall rank correlation coefficient [28]. during drought periods.2 Zooplankton community attributes The accumulated species richness ranged from 65 taxa in PS (isolated pond) to 104 taxa in BS (connected pond.05.78. KGaA. The reverse shows an increase in similarity in the community over time. Moina minuta. 24–33 dissimilarity with time. in these locations.05). using the Simpson dissimilarity [27] because it is less dependent on the species richness.013. with lower variability in 2005–2006 for ponds in PS and BS and in 2000–2001 at IS. BS tended to increase in dissimilarity only during 2005–2006. while divergence suggests an increasing of dissimilarity with time [26]. p > 0. with values near zero indicating the highest similarity and values near one indicating lowest similarity. The analyses were performed with the software R version 2. 1 in [25]). This observation suggests that. there was no difference in the temporal variability of the zooplankton community between the periods (p > 0. Table 2) during drier periods (2000–2001 for BS and PS. F1. This index ranges from zero to one. Fig. changing species composition. p ¼ 0. Secchi disc and total phosphorus showed significant interaction (p < 0. Fig. 3. Hexarthra mira (rotifers). Of the species pool. High coefficients with positive values indicate that the species keep their ranks in a distribution of abundance.007. Abundance varied between 1 Â 103 and 8504 Â 103 ind mÀ3. Values near zero indicate that the distribution of abundance among species has changed unpredictably. In the ponds from PS. suggesting the predominance of similar ecological relationships over time because the patterns of species’ dominance and rarity are maintained. as PS had no trend of community variation over time in the two analysed periods. 27 3 Results 3.90 ¼ 22. see Fig. electrical conductivity and total nitrogen coefficient of variation between the types of ponds or periods (Anova. whereas negative values indicate a reversal in the pattern of abundance distribution among species. the multivariate test did not detect significant differences (possibly as in the drought period the number of samples was lower due to complete drying of the pond). 98.8 ¼ 12. showing that. In isolated ponds.4 Temporal trend of species composition In the connected ponds. and 2005–2006 in IS ponds). Drought and flooded periods showed no difference in richness. suggesting ecological changes that modify the community structure. with differences in the range between the periods only in connected ponds (Table 1).05) between types of ponds and periods. we evaluated the presence and absence of species.1 [29]. Species richness differed only between the types of ponds (F1. A significant positive correlation between the Kendall dissimilarity matrix and time lag suggests that ranks of species abundance tend to become more similar over time.001). Weinheim . and IS tended to increase in dissimilarity during both sampling periods. (b) Secondly. 3b and d). Drought disturbances increase zooplankton variability instance. p<0. eight were more abundant of each group in both periods: Keratella cochlearis. Significance was estimated using the Mantel test to compare the relationship between dissimilarity matrices and the time lag matrix.13.8. respectively. Lecane proiecta. There was no pattern of temporal dissimilarity for isolated ponds (Table 2). showing lower community variability in flooded periods.8 ¼ 10. the drought period increased the variability of the total phosphorus in the connected ponds (Fig. In this procedure.3 Zooplankton community variability The temporal variability of the zooplankton community in connected ponds differed between study periods (p < 0. 4).

Attributes of the zooplankton community in the studied ponds during the period 2000–2001 and 2005–2006 in the Upper Paraná River floodplain: S total. International Review of Hydrobiology 2013.N. Table 1. mean. species richness. Table 3). Coefficient of variation of water features between periods (Drought and Flooded) and types of ponds (Isolated and connected ponds). a negative relationship was observed between the Kendall matrix of similarity and the matrix of time lag during the drier period (2000–2001 for ponds in PS and BS. KGaA. under greater amplitudes of flooding. On the other hand. 24–33 Total Alkalinity a 80 70 Coefficient of variation 60 50 40 30 20 10 Drought b 80 Isolated ponds Connected ponds Coefficient of variation 70 60 50 40 30 20 10 Flooded Drought Secchi disc Flooded Period Period c 130 120 110 Coefficient of variation 100 90 80 70 60 50 40 30 Drought Chlorophyll a d 140 120 Coefficient of variation 100 80 60 40 20 F looded Drought Total phosphorus F looded Period Period Figure 3. Thus. standard error. Total alkalinity (a). R. . 3. 28 © 2013 WILEY‐VCH Verlag GmbH & Co. Chlorophyll a (c) and total phosphorus (d). no temporal trend was recorded in communities from connected ponds during periods with typical floods (Table 3) indicating that. Simões et al. and 2005–2006 for the pond in IS.5 Temporal trend of relative abundance In connected ponds. Weinheim . average species richness and standard deviation 2000–2001 Type of pond Connected ponds Sub-systems Paraná Baia Ivinheima Paraná Baia Ivinheima S total 86 104 90 65 89 70 S (sd) 30(6) 38(9) 30(7) 25(8) 32(6) 25(5) Variation of abundance* 7–8504 14–1808 38–369 9–93 19–401 29–245 S total 94 89 91 79 83 79 2005–2006 S (sd) 29(9) 34(7) 34(6) 21(7) 29(5) 21(6) Variation of abundance* 1–24 1–93 3–49 1–276 6–151 1–575 Isolated ponds * values in ind mÀ3 Â 103. S (sd). the absence of flooding produced a temporal shift in the community dominance. 98. the distribution of the ranks of species abundance is indifferent to time lag. &. Secchi disc (b). reversing the distribution of species abundance over time in connected ponds.

The scores represent different sampling months between analysed periods. © 2013 WILEY‐VCH Verlag GmbH & Co. KGaA. p-values show differences between periods. BS presented a negative trend during the period 2005–2006. there was no association between the time lag of samplings and the matrix of Kendall correlation. The isolated ponds demonstrated no differentiated results for inversion of species ranks during the analysed periods (Table 3). As indicated by Mantel tests.International Review of Hydrobiology 2013. 4).e. In PS. 24–33 Drought disturbances increase zooplankton variability Figure 4. 29 . and IS demonstrated a trend of reversal of species ranks during both sampling periods. Two-dimensional representation of PCoA of the structure of the zooplankton community in two periods (drought and flooded) in the Upper Paraná River floodplain. Weinheim 4 Discussion The temporal variability of the zooplankton community structure differed between the analysed periods in connected ponds that demonstrated greater variability during the drought period (i. higher dispersion between samplings in time. 98. see Fig.

394 p-Value 0.068 0. Result of the Mantel test between the matrix of time lag and the matrix of Simpson dissimilarity in the different types of ponds (connected or isolated) from the Upper Paraná River floodplain in different hydrological periods Connected ponds r-Mantel Baia sub-system 2000–2001 2005–2006 Paraná sub-system 2000–2001 2005–2006 Ivinheima sub-system 2000–2001 2005–2006 0.381 0.013 0. Consequently.393 0. resulting in a lower variation in the niche amplitude of species and thus a lower rate of temporal turnover. the zooplankton community diverges with the prolongation of drought due to change in species composition and the pattern of relative abundance. International Review of Hydrobiology 2013.290 0. Result of Mantel test between the matrix of time lag and matrix of Kendall correlation in the different types of ponds (connected or isolated) from the Upper Paraná River floodplain in different hydrological periods Connected ponds r-Mantel Baia sub-system 2000–2001 2005–2006 Paraná sub-system 2000–2001 2005–2006 Ivinheima sub-system 2000–2001 2005–2006 À0. and in 2005–2006 for the Ivinheima sub-system (IS). Thus. with six samplings as the pond dried up).079 À0.463 p-Value 0. Nevertheless. we observed different temporal trends of the community between the periods. as suggested by Bengtsson et al.620 À0.028 Number of samplings is equal to eight in each study period (except for the isolated pond from the Paraná sub-system (PS) in 2000–2001. R.001 0.566 0. in connected ponds.567 À0. in the absence of floods. 33]. Simões et al.045 À0.N.066 0. favouring the lower variability of the community [32–34].065 0. 24–33 Table 2.095 0. Weinheim . and promoted a distribution reversal of species abundances. [35].454 0.050 0.528 p-Value 0.721 À0.150 À0.122 0.038 0.335 0.344 0. 3c and d). Table 3. as evidenced in 2000–2001 for the Paraná and Baia subsystems (PS and BS).024 2000–2001 2005–2006 2000–2001 2005–2006 2000–2001 2005–2006 Isolated ponds r-Mantel 0. autochthonous processes of productivity overcome allochthonous processes of energy input [33].683 0. This means that. droughts produce a disturbing effect because they increase community variability.002 2000–2001 2005–2006 2000–2001 2005–2006 2000–2001 2005–2006 Isolated ponds r-Mantel 0. 30 © 2013 WILEY‐VCH Verlag GmbH & Co.343 À0.935 0.002 0. mainly in connected ponds. It is likely that the recurrence of floods in connected ponds maintains environmental conditions that are less changeable than drought periods (such as low variability of chlorophyll a).037 0. One of the effects of floods in floodplains is to buffer local variability.397 p-Value 0.010 0.551 0. mainly regarding resources (Fig.787 0.343 0.303 0. KGaA. The temporal variability of the zooplankton community in isolated ponds (Fig. 4) did not differ between the analysed periods. communities exhibit lower variation as environmental conditions vary within a constant range. However. with six samplings as the pond dried up). In response. 98. promoting an increase in environmental variation and consequently in community variation [35]. the absence of floods changed the community composition due to an increase in temporal dissimilarity.457 0.001 0.044 0. as the constant input of water maintains the renewal of nutrients [14.102 0.021 Number of samplings is equal to eight in each study period (except for the isolated pond from the Paraná sub-system (PS) in 2000–2001. in BS. flooding makes the environmental variation range narrower and more constant.279 À0.292 0.298 À0.002 0.

Ecological heterogeneity in streams: Why variance matters. 37]. consequently. Oikos 2004. 560. because the connected ponds that showed lesser recourse variability had their temporal variability affected in extended drought periods. F.g. P.. We thank Dr. This work was supported by Conselho Nacional de Desenvolvimento a Pesquisa (CNPq) with financing of the Long Term Ecological Research. J.. Luis Mauricio Bini (Universidade Federal de Goias) by important comments and suggestions. [8] Angeler. C. KGaA. 1999. Weinheim Drought disturbances increase zooplankton variability locations display high variability regardless of the water level. E. M. 1997. Such environmental variability promotes a higher rate of species replacement due to temporal niche partitioning. [7] Brown. Thus. J. whereas communities in environments with recurring variations (isolated ponds) may become most variable when such fluctuations fail to occur. Morgan. Appl. a flood is sometimes considered to be a disturbance. 9. G. 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1 6. Weinheim 33 .9 3. dissolved oxygen. total phosphorus.0 545.0 0. KGaA. Chl.6 7.8 10.6 100. total nitrogen. 98.7 1.International Review of Hydrobiology 2013.6 688. 24–33 Drought disturbances increase zooplankton variability Appendix 1 Summary of the environmental characteristics in the connected and isolated ponds from the Upper Paraná River floodplain during the study periods (2000–2001 and 2005–2006).4 11.4 42.7 4.2 110.9 237.4 0. TA.3 20.3 282. PT.6 0.3 5.9 6.1 0. pH.9 6. water temperature.9 10. electrical conductivity.4 0.2 149. SD.8 5.8 6. NT.5 24.1 0.7 185. DO (mg LÀ1) EC (µS cmÀ1) TA (µeq LÀ1) SD (m) Chl (µg LÀ1) NT (µg LÀ1) PT (µg LÀ1) WT (°C) Connected ponds 2000–2001 Mean Standard deviation 2005–2006 Mean Standard deviation Isolated ponds 2000–2001 Mean Standard deviation 2005–2006 Mean Standard deviation pH 24.1 92.7 12. Secchi disc.9 3.7 0.6 203.0 © 2013 WILEY‐VCH Verlag GmbH & Co.6 254.4 24.0 24. DO.6 0.7 10.9 655.8 547.7 24.7 1047.4 39.7 1.0 6.9 44.5 0.7 6.3 216.4 36.6 4.7 0.3 40.0 145.3 36.7 113.4 341.3 0. EC. chlorophyll a.3 1.6 377. WT.2 94.5 2.7 6.9 75.9 10. total alkalinity.9 11.3 1.8 21.7 13.

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