DIVERSITY AND STABILITY OF AQUATIC MACROPHYTE COMMUNITY IN THREE SHALLOW LAKES ASSOCIATED TO A FLOODPLAIN SYSTEM IN THE SOUTH OF BRAZIL

Leonardo Maltchik, Gislaine Roberto de Oliveira, Ana Silvia Rolon and Cristina Stenert

Leonardo Maltchik. Ph.D. in Ecology, Universidad Autónoma de Madrid, Spain. Professor, Universidade do Vale do Rio do Sinos (UNISINOS), Brazil. Address: Laboratory of Ecology and Conservation of Aquatic Ecosystems, UNISINOS. São Leopoldo, Rio Grande do Sul, Brazil, 93022-000. e-mail: maltchik@bios.unisinos.br

Gislaine Roberto de Oliveira. Master in Biology, UNISINOS, Brazil.

Ana Silvia Rolon. Graduate Student, UNISINOS, Brazil.

Cristina Stenert. Graduate Student, Universidade Federal de São Carlos, Brazil. Researcher, Laboratory of Ecology and Conservation of Aquatic Ecosystems, UNISINOS.

Resumen

Las llanuras de inundación son importantes tipos de humedales en el sur de Brasil, pero estudios que analizan los efectos de las inundaciones en la biota aún son muy escasos. El objetivo del trabajo era analizar y comparar los efectos de las inundaciones en la riqueza, biomasa y diversidad de macrofitos acuáticos en tres lagunas en un ciclo anual (2001-2002) bajo distintos regimenes de inundaciones. El número de inundaciones era diferente en las tres lagunas estudiadas. La menor resistencia de macrofitos frente las inundaciones y la ausencia de dominancia ha sido observada en la laguna con mayor numero de inundaciones. La estabilidad de macrofitos no estuvo relacionada con su diversidad. Estos resultados indicaran la importancia del régimen de inundación (numero de inundaciones, incluyendo los eventos de rápida duración) en la estabilidad y composición de macrófitos en lagunas del sur de Brasil.

Summary

The floodplain systems are important wetland classes in southern Brazil, but studies about the effects of flood pulses on the biota are still scarce. The purpose of this study was to analyze and compare the effects of floods on the richness, biomass and diversity of macrophytes in three shallow lakes over an annual cycle (2001-2002) under different flooding regimes. The number of flood events was different among the three studied shallow lakes. The lowest resistance to disturbance by flood and the absence of dominance were observed in the lake with the highest number of flood events. Macrophyte stability and diversity were not related. The results indicate the importance of the flooding regime (number of flood events, even short duration ones) on the macrophyte stability and composition in shallow lakes of southern Brazil.

Resumo

As planícies de inundação são importantes classes de áreas úmidas no sul do Brasil, entretanto estudos sobre os efeitos do pulso de inundação nas comunidades biológicas ainda são escassos. O objetivo desse estudo foi analisar e comparar os efeitos das inundações na riqueza, biomassa e diversidade de macrófitas aquáticas em três lagoas de diferentes rasas de um ciclo anual (2001-2002) sujeitos a diferentes regimes de inundação. O número de inundações foi diferente nas três lagoas estudadas. A menor resistência de macrófitas aquáticas frente às perturbações hidrológicas e a ausência de espécies dominantes foram observadas na lagoa com maior número de inundações. A estabilidade de macrófitas não esteve relacionada com a diversidade de macrófitas. Estes resultados indicaram a importância do regime de inundação (número de eventos, inclusive os de curta duração) na estabilidade e composição de macrófitas em lagoas rasas do sul do Brasil.

Keywords / Disturbance / Floods / Aquatic Macrophyte / Shallow Lakes / Wetlands /

Received: 05/12/2004. Modified: 02/17/2005. Accepted: 02/19/2005.

Introduction

Hydrologic disturbance has received substantial attention from ecologists, mainly because it is a major organizer in many aquatic ecosystems (Souza, 1984). The concept of disturbance in aquatic ecosystems may be defined in terms of the physical attributes, such as intensity, frequency, duration and predictability (Lake, 1990; Poff, 1992) or in terms of the biotic response (White and Pickett, 1985). In this sense, the definition of perturbation proposed by Bender et al. (1984) and by Glasby and Underwood (1996) is useful because it describes the combination of cause (disturbance) and effects (response).

The flood pulse concept suggests that this is the principal driving force responsible for the existence, productivity and interactions of the major biota in river floodplain systems (Junk et al., 1989). Benke et al. (2000) suggested that the ecological importance of the flood events is far broader than a simple exchange of organic matter between the main channel and the floodplain system. Floods provide a temporary habitat for fishes and other aquatic organisms that is several times larger than the area of the river channel (Ross and Baker, 1983). The water level fluctuation provided by the flood events in floodplain systems is a complex variable, encompassing several attributes (duration, frequency, timing) that can affect the biota in different ways. Studies related to disturbance ecology in aquatic ecosystems have concentrated efforts on understanding the effects of floods on communities, considering mainly events of high duration. However, information on the response of communities to disturbance by floods of low duration is scarce (Lake, 2000).

Several studies have examined the effects of floods on aquatic macrophytes (Howard-Willis, 1975; Bilby, 1977; Bornette et al., 1994; Hill et al., 1998; Casanova and Brock, 2000; Jansson et al., 2000; Maltchik and Pedro, 2001; Crosslé and Brock, 2002; Riis and Hawes, 2002). Variation in macrophyte species composition after flooding events can be related with habitat enlargement, species traits or flood attributes (Junk et al., 1989; Brock, 1991; Henry et al., 1994; Barrat-Segretain and Amoros, 1995; Brock and Casanova, 1997; Fernández-Aláez et al., 1999; Engelhardt and Kadlec, 2001). The macrophyte richness in wetland systems is related to the flood frequency, duration and timing (Brinson, 1990; Robertson et al., 2001).

The floodplain systems are important wetland classes in southern Brazil. However, studies about the effects of flood pulses on the biota are still scarce (Stenert et al., 2003; Avila et al., 2004; Maltchik et al., 2004). In Brazil, most of the functional studies in floodplain systems were developed in the Amazon basin, where the annual thermal amplitude is low (Piedade, 1985; Piedade et al., 1994; Nessimian et al., 1998) and in the Paraná River basin, where the flooding was damaged by the extreme regulation of the Paraná River (Thomaz et al., 1991; Agostinho et al., 2001).

The purpose of this study was to analyze and to compare the effects of floods in the macrophyte richness, biomass and diversity, in three shallow lakes over an annual cycle (2000-2001) under different flooding regimes. The working hypothesis is that the response of the macrophyte community to disturbance by floods is different among shallow lakes under different disturbance attributes.

Study site

The study was carried out in the Sinos River basin (~4000km²), located in southern Brazil (Rio Grande do Sul). The Sinos River is a 7^th order permanent river (Strahler, 1952) of the Jacuí/Guaiba catchment. It is 190km long from its origin at 900m above sea level, to its confluence with the Jacuí River at an elevation of 10m. The annual rainfall in the Sinos River basin ranges from 1200 to 2000mm·y^-1 and is well distributed throughout the year. The increase in the discharge due to high precipitation originates a series of flood events resulting in the temporary inundation of the floodplain.

The studied floodplain has approximately 30ha and presents several permanent and intermittent shallow lakes, scattered within two different types of vegetation, native woodland and grasslands. During the flooding event, the water penetrates into the floodplain system along different streams. The surface water velocity in the floodplain systems during the flooding period is very low. The discharge of the Sinos River near the studied floodplain varies between 2.9 and 71m³·s^-1 (COMITESINOS, 2000).

The three studied shallow lakes are approximately 20m away from each other and some 300m from the Sinos River. They are shallow (mean depth ~30cm), permanent, irregular, and are fed by water from rainfall, and by runoff and flooding from the Sinos River. The permanent presence of surface water contributes to the strong development of aquatic macrophytes. The three lakes studied had different inundation areas, namely 9432m² (lake A), 4026m² (B) and 737m² (lake C). The substrate was composed basically of silt and sand. Following Tiner’s classification (Tiner, 1999), the flood events of the Sinos River basin are frequent (>50 floods in 100 years).

Materials and Methods

A total of 19 macrophyte samples was collected during an annual cycle (from May 2001 to April 2002) in the three shallow lakes. Species richness per collection was recorded as the number of macrophyte species found, and the biomass was measured using the quadrat method (Downing and Anderson, 1985). In each lake, six quadrats (30×30cm) were sampled at random along the selected transect. In each collection, macrophytes were removed close to the substratum with scissors (roots were not collected). The sampled material was placed in plastic bags for subsequent analysis in the laboratory, where they were washed to remove the periphyton and deposited organic and inorganic materials. Afterwards, they were separated by species and dried in an oven at 60ºC up to constant weight (ca. 72h). Macrophyte biomass in each square was expressed as grams of dry weight per m² and the species were identified following Irgang and Gastal (1996).

Water temperature was measured in situ using digital equipment (Water Test model 90). The water depth was measured with a PVC tube graduated in centimeters. The dominance was classified (McCullought and Jackson, 1985) as dominant (100-50%), abundant (49-30%), common (29-10%), occasional (9-1%) and rare (<1%).

To examine resistance, displacements of macrophyte richness and biomass before and after floods were compared. Resistance of the macrophyte community was estimated for each sequence by comparing mean richness and biomass before and after each flood using a t-test. If these differences were not significant (P>0.1), the macrophyte community was considered resistant to the floods (Grimm and Fisher, 1989). The duration of flooding was measured in days and classified (Tiner, 1999) as long (7-30d) and short (2-7d). The flooding regime was computed as the number and the duration of flood events. The variation of richness, biomass and Shannon-Weiner diversity index along the annual cycle was measured using Analysis of Variance (ANOVA One-Way). The macrophyte richness, biomass and diversity were separated in two groups: periods with (from 5/15 to 10/18) and without floods (10/25 to 4/12) and they were compared through a General Linear Model (GLM). The direct analysis of the environmental parameters on the ordination of the species and the collections were carried out according to the Canonical Correspondence Analysis (CCA). The significance of the axis generated in the CCA was validated by the Monte Carlo test (using 1000 unrestricted permutations).

Results

The number of flood events was different among the three studied shallow lakes (Table I). While lakes A and C experienced two floods of different duration, one long (14d) and one short (5d), lake B experienced four floods, one of long duration (14d) and three of short duration (3-5d).

A total of ten macrophyte species was found in the three shallow lakes over the annual cycle (Table II). Nine macrophyte species were registered in lake A and eight species were registered in lakes B and C (Table II). Based on species-environmental data from the CCA ordination method, the eigenvalues of the axis 1 and 2 were 0.478 and 0.234, respectively, and the cumulative percentage of total variation in the data accounted for 35.4% (P<0.001). The first axis (explaining 23.8% of total data variation) separated the collections of the three lakes along a gradient related with the area, focusing mainly the difference between the macrophyte composition of the lake A than lakes B and C (Figure 1). The second axis (explaining 11.7% of total data variation) differentiated the collections of the period with floods from the period without floods (Figure 1). The composition of aquatic macrophytes varied among the three lakes and between the periods with or without flooding events (Figure 1). A Monte-Carlo simulation test showed that the variance in composition of macrophyte community among the three lakes was related with the area (r=0.992, axis 1).

The richness (F=24.674, P<0.001), biomass (F=36.044, P<0.001) and diversity (F=16.553, P<0.001) of macrophytes varied between the three lakes studied. Macrophyte richness, biomass and diversity were higher in lake A (Tukey, P=0.004; P<0.001 and P=0.003, respectively) and lake B (Tukey, P<0.001; P<0.001 and P<0.001, respectively) than Lake C (Figure 2).

Richness and biomass of macrophytes were resistant to all floods in lakes A and C (Table III). In lake B, only one flood (5d) diminished the richness of macrophytes, and it was not related with the flood of highest duration (Table III). The floods in lake B influenced the macrophyte biomass differently; whereas the short floods (3 and 5d) reduced the biomass, the 14d flood increased it (Table III).

Species dominance was different in the three lakes. Whereas E. azurea was the dominant species in lake A, M. aquaticum was dominant in lake C. None of the macrophyte species was dominant in lake B (Table II).

The richness, biomass and diversity of macrophytes were similar between the periods with and without floods in lakes A (F=0.736, P=0.675; F=1.319, P=0.236 and F=0.501, P=0.489, respectively) and C (F=0.689; P=0.718; F=0.925; P=0.527 and F=4.2557; P=0.055,

respectively). In lake B the richness, biomass and diversity were higher in the period without floods (F=2.093; P=0.037, F=2.728; P=0.007, F=14.303; P<0.001, respectively) compared to the flood period.

Discussion

The duration of the floods is an important attribute when evaluating the patterns of community responses to flood disturbance (Romme et al., 1998). Grimm and Fisher (1989) considered that the biota resistance was negatively related to the flood magnitude. In this study, macrophyte resistance to disturbance by floods was different between the three lakes studied. Only in lake B, the macrophyte community was not resistant to the flood events. The higher number of floods experienced in lake B led to a lower stability of resistance in the aquatic macrophyte community. The floods were concentrated on the first half of the annual cycle and during this period the macrophyte composition was different in the three lakes. These results showed the importance of the number of flood events, besides events of short duration, in the stability of macrophytes in the studied wetlands and the importance of the flood frequency in the macrophyte composition.

The increase in the spatial variability after the flood events facilitates species coexistence and avoids the establishment of dominant species in intermittent aquatic ecosystems (Maltchik and Medeiros, 2001; Medeiros and Maltchik, 2001). In this study, the lake that experienced the higher number of flood events (lake B) was the only one that did not have dominant species. This result indicates that floods, even of short duration, influenced the dominance of aquatic macrophytes in shallow wetland systems.

The relationship between the diversity and the stability of communities is controversial, and is of practical and theoretical interest. MacArthur (1955) and Elton (1958) argued that the functional stability of an ecosystem is facilitated by its diversity, whereas other authors concluded the opposite (May, 1974; Pimm, 1979). In this study the highest diversity of macrophytes found in lake B did not provide a higher resistance to disturbance by flood. This result is similar to the one obtained by Engelhardt and Kadlec (2001), suggesting that the highest richness of macrophytes did not provide a higher stability to the community in the face of the flood pulse events.

The community of aquatic macrophytes presented a high resistance to the flood events. The macrophyte stability was not related with diversity and the macrophyte resistance diminished as the number of events increased. The highest variation in macrophyte richness and biomass, and the absence of dominance was observed only in the lake with the highest number of flood events. These results indicate the importance of the flooding regime (number of flood events, besides the ones of short duration) on the macrophyte stability and composition in shallow lakes of Southern Brazil. However, ecological studies of long duration and studies that involve other floodplain systems are necessary for a good understanding of the functional processes in floodplain systems in the area.

REFERENCES

1. Agostinho AA, Gomes LC, Zalewski M (2001) The importance of floodplains for the dynamics of fish communities of the upper Paraná river. Ecohydrol Hydrobiol. 1: 209-217.        [ Links ]

2. Ávila IR, Matsubara CP, Schott P, Maltchik L (2004) Diversity and stability of phytoplankton in a shallow lake associated to a floodplain system in the south of Brazil. Pesquisas: Botânica 55: 201-215.        [ Links ]

3. Barrat-Segretain MH, Amoros C (1995) Influence of flood timing on the recovery of macrophytes in a former river channel. Hydrobiologia 316: 91-101.        [ Links ]

4. Bender EA, Case TJ, Gilpin ME (1984) Perturbation experiments in community ecology: theory and practice. Ecology 65: 1-13.        [ Links ]

5. Benke AC, Chaubey I, Ward GM, Dunn EL (2000) Flood pulse dynamics of an unregulated river floodplain in the southeastern U.S. Coastal Plain. Ecology 81: 2730-2741.        [ Links ]

6. Bilby R (1977) Effects of a spate on the macrophyte vegetation of a stream pool. Hydrobiologia 56: 109-112.        [ Links ]

7. Bornette G, Amoros C, Castella C, Beffy JL (1994) Succession and fluctuation in the aquatic vegetation of two former Rhône River channels. Vegetatio 110: 171-184.        [ Links ]

8. Brinson MM (1990) Riverine forests In Lugo AE, Brinson MM, Brown SL (Eds.) Forested Wetlands. Ecosystems of the World. Elsevier. Amsterdam, Netherlands. pp 87-142.        [ Links ]

9. Brock MA (1991) Mechanisms for maintaining persistent population of Myriophyllum variifolium J. Hooker in a fluctuating shallow Australian lake. Aquat. Bot. 39: 211-219.        [ Links ]

10. Brock MA, Casanova MT (1997) Plant life at the edges of wetlands: ecological responses to wetting and drying patterns. In Klomp N, Lunt I (Eds.) Frontiers of Ecology. Elsevier. Oxford, UK. pp 181-192.        [ Links ]

11. Casanova MT, Brock MA (2000) How do depth, duration and frequency of flooding influence the establishment of wetland plant communities? Plant Ecol. 147: 237-250.        [ Links ]

12. COMITESINOS (2000) Enquadramento das águas da Bacia Hidrográfica do Rio dos Sinos. Impresul. São Leopoldo, Brazil. 16 pp.        [ Links ]

13. Crosslé K, Brock MA (2002) How do water regime and clipping influence wetland plant establishment from seed banks and subsequent reproduction? Aquat. Bot. 74: 43-56.        [ Links ]

14. Dowling JA, Anderson MR (1985) Estimating the standard biomass of aquatic macrophytes. Can. J. Fish. Aquat. Sci. 42: 1660-1669.        [ Links ]

15. Elton CS (1958) The Ecology of Invasions by Animals and Plants. Chapman Hall. London, UK. 181 pp.        [ Links ]

16. Engelhardt KAM, Kadlec JA (2001) Species traits, species richness and the resilience of wetlands after disturbance. J. Aquat. Plant Mgmnt. 39: 36-39.        [ Links ]

17. Fernández-Aláez C, Fernández-Aláez M, Bécares E (1999) Influence of water level fluctuation on the structure and composition of the macrophyte vegetation in two small temporary lakes in the northwest of Spain. Hydrobiologia 415: 155-162.        [ Links ]

18. Glasby TM, Underwood AJ (1996) Sampling to differentiate between pulse and press perturbations. Envir. Monit. Assess. 42: 241-252.        [ Links ]

19. Grimm NB, Fisher SG (1989) Stability of periphyton and macroinvertebrates to disturbance by flash floods in a desert stream. J. North Am. Benthol. Soc. 8: 293-307.        [ Links ]

20. Henry CP, Bornette G, Amoros C (1994) Differential effects of floods on the aquatic vegetation of braided channels of the Rhone River. J. North Am. Benthol. Soc. 13: 439-467.        [ Links ]

21. Hill NM, Keddy PA, Wisheu IC (1998) A hydrological model for predicting the effects of dams on the shoreline vegetation of lakes and reservoirs. Envir. Mgmnt 22: 723-736.        [ Links ]

22. Howard-Willis C (1975) Seasonal and spatial changes in the composition of the aquatic and semiaquatic vegetation of Lake Chilwa, Malawi. Vegetatio 30: 33-39.        [ Links ]

23. Irgang BE, Gastal Jr CVS (1996) Macrófitas aquáticas da planície costeira do RS. Porto Alegre, Brazil. 290 pp.        [ Links ]

24. Jansson R, Nilsson C, Dynesius M, Andersson E (2000) Effects of river regulation on river-margin vegetation: a comparison of eight boreal rivers. Ecol. Applic. 10: 203-224.        [ Links ]

25. Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems. In Dodge DP (Ed.) Proc. Int. Large River Symp. Canadian Special Publication of Fisheries and Aquatic Sciences 106. pp 110-127.        [ Links ]

26. Lake PS (1990) Disturbing hard and soft bottom communities: a comparison of marine and freshwater environments. Austral J. Ecol. 15: 477-488.        [ Links ]

27. Lake PS (2000) Disturbance, patchiness, and diversity in streams. J. North Am. Benthol. Soc. 19: 573-592.        [ Links ]

28. MacArthur RH (1955) Fluctuations of animal populations and a measure of community stability. Ecology 36: 533-536.        [ Links ]

29. Maltchik L, Medeiros ES (2001) Does hydrological stability influence biodiversity and community stability? A theoretical model for lotic ecosystems from the Brazilian semiarid region. Ciência e Cultura. 53: 44-48.        [ Links ]

30. Maltchik L, Pedro F (2001) Responses of aquatic macrophytes to disturbance by flash floods in a Brazilian semiarid intermittent stream. Biotropica 33: 566-572.        [ Links ]

31. Maltchik L, Rolon AS, Groth C (2004) The Effects of Flood Pulse on the Macrophyte Community in a Shallow Lake of Southern Brazil. Acta Limnol. Bras. 16: 103-113.        [ Links ]

32. May RM (1974) Ecosystem patterns in randomly fluctuating environments. Progr. Theor. Biol. 3: 1-50.        [ Links ]

33. McCullought JD, Jackson DW (1985) Composition and productivity of the benthic macroinvertebrate community of subtropical reservoir. Int. Rev. Ges. Hydrobiol. 70: 221-235.        [ Links ]

34. Medeiros ESF, Maltchik L (2001) Fish assemblage stability in an intermittently flowing stream from the Brazilian semiarid region. Austral Ecol. 26: 156-164.        [ Links ]

35. Nessimian JL, Dorvillé LFM, Sanseverino AM, Baptista DF (1998) Relation between flood pulse and functional composition of the macroinvertebrates benthic fauna in the lower Rio Negro, Amazonas, Brazil. Amazoniana 15: 35-50.        [ Links ]

36. Piedade MTF (1985) Ecologia e biologia reprodutiva de Astrocaryum jauari Mart. (Palmae) como exemplo de população adaptada às áreas inundáveis do Rio Negro (igapó). Thesis. Instituto Nacional de Pesquisas do Amazonas, Manaus, AM, Brazil. 184 pp.        [ Links ]

37. Piedade MTF, Long SP, Junk WJ (1994) Leaf and canopy photosynthetic CO₂ uptake of a stand of Eichinochloa polystachya on the Central Amazon floodplain. Oecologia 97: 193-201.        [ Links ]

38. Pimm SL (1979) Complexity and stability: another look at MacArthur’s original hypothesis. Oikos 33: 351-357        [ Links ]

39. Poff NL (1992) Why disturbances can be predictable: a perspective on the definition of disturbance in streams. J. North Am. Benthol. Soc. 11: 86-92.        [ Links ]

40. Riis T, Hawes I (2002) Relationships between water level fluctuations and vegetation diversity in shallow water of New Zealand lakes. Aquat. Bot. 74: 133-148.        [ Links ]

41. Robertson AI, Bacon P, Heagney G (2001) The response of floodplain primary production to flood frequency and timing. J. Appl. Ecol. 38: 126-136.        [ Links ]

42. Romme WH, Everham EH, Frelich LE, Moritz MA, Sparks RE (1998) Are large, infrequent disturbances qualitatively different from small, frequent disturbance? Ecosystems 1: 524-534.        [ Links ]

43. Ross ST, Baker JA (1983) The response of fishes to periodic spring floods in a southeastern stream. Am. Midland Naturalist 109: 1-14.        [ Links ]

44. Souza WP (1984) The role of disturbance in natural communities. Annu. Rev. Ecol. Syst. 15: 353-391.        [ Links ]

45. Stenert C, Santos EM, Maltchik L (2003) Os efeitos do pulso de inundação na comunidade de macroinvertebrados em uma lagoa associada a uma planície de inundação do Sul do Brasil. In Henry R (Ed.) Ecótonos nas interfaces dos ecossistemas aquáticos. RIMA. São Carlos, Brazil. pp. 47-60.        [ Links ]

46. Strahler AN (1952) Dynamics basis of geomorphology. Geol. Soc. Am. Bull. 63: 923-928.        [ Links ]

47. Thomaz SM, Roberto MCM, Lansactôha FA, Esteves FA, Lima AF (1991) Dinâmica temporal dos principais fatores limnológicos do rio Baía-planície de inundação do alto rio Paraná-MS, Brazil. Revista Unimar. 13: 299-312.        [ Links ]

48. Tiner RW (1999) Wetland indicators: a guide to wetland identification, delineation, classification, and mapping. Lewis. New York, USA. 392 pp.        [ Links ]

49. White PS, Pickett STA (1985) Natural disturbance and patch dynamics: an introduction. In Pickett STA, White PS (Eds.) The Ecology of Natural Disturbance and Patch Dynamics. Academic Press. New York, USA. pp 3-9.        [ Links ]