Hydrobiologia 505: 119–128, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
119
Species richness and beta diversity of aquatic macrophytes in a large subtropical reservoir (Itaipu Reservoir, Brazil): the influence of limnology and morphometry Sidinei Magela Thomaz1 , D´ebora C. Souza2 & Luis Mauricio Bini3 1 Universidade
Estadual de Maring´a, CCB, NUPELIA, PEA. Av. Colombo, n. 5790, 87020-900, Maring´a, PR, Brazil E-mail:
[email protected]. 2 CEFET-UEM-PEA 3 Universidade Federal de Goi´ as, ICB, DBG, Goiânia, GO, 74001-970, Brazil E-mail:
[email protected] Received 25 June 2002; in revised form 11 June 2003; accepted 20 June 2003
Key words: biodiversity, non-traditional regression, aquatic macrophytes
Abstract Assessment of the environmental factors that control species richness (S) is a central issue in ecology. In this study, aquatic macrophyte S was estimated in 235 sampling sites distributed in 8 arms of a large (1350 km2 ) subtropical reservoir (Itaipu Reservoir, Brazil). Morphometric variables (area, shoreline development and length of shoreline, all measured for each arm; n = 8) and environmental variables measured at each sampling site (extinction coefficient of light (k), electrical conductivity, fetch, distance from the main reservoir body; n = 235) were used to predict aquatic macrophyte S at two spatial scales. At arm scale, linear regression analysis indicated that length of shoreline was a better predictor of S than area. At sampling site scale, multiple regression analysis indicated that S was significantly predicted by electrical conductivity, fetch and distance from the main body. However, other relationships with predictive interest was demonstrated by using non-traditional regression approaches. This analysis started by the visual inspection of scatter plots. The bivariate relationship between S and fetch, for example, showed an envelope or a ‘left triangle’ pattern. The relationship between the number of submerged species and k showed an asymmetrical left triangle pattern. Using randomization procedures, it was demonstrated that these patterns were not generated by chance alone. Beta diversity (estimated within the arms) was significantly and positively correlated with spatial environmental variability. Overall, these results indicate that the prediction of aquatic macrophytes assemblage variables in large waterbodies, specially S, is more complex than previous studies have suggested.
Introduction Understanding the patterns and processes related to biodiversity represents one of the greatest challenges to theoretical and applied ecology. Research programs trying to describe patterns in biodiversity and the mechanisms that explain such patterns are growing rapidly and their importance was attested and increased, by the International Biodiversity Observation Year in 2001 (Wall et al., 2001). This research program
has relevance to aquatic plant ecology, and several articles about biodiversity and aquatic macrophytes have been published (Rørslett, 1991; Robach et al., 1997; Bini et al., 2001; Bornette et al., 2001; Engelhardt & Ritchie, 2001). The determinants of aquatic macrophyte richness include some well-known factors such as area (Rørslett, 1991; Vestergaard & Sand-Jensen, 2001a), water chemistry and trophic state (Murphy et al., 1990; Bornette et al., 2001; Lougheed et al., 2001; Vester-
120 gaard & Sand-Jensen, 2001a, b), lake morphometry (Duarte et al., 1986), degree of exposure to wind (Chambers, 1987; Hudon et al., 2000) and degree of connectivity with rivers (Amoros & Bornette, 1999; Tockner et al., 1999). Most knowledge about freshwater ecosystem biodiversity is restricted to natural systems, such as lakes, rivers and floodplains, and artificial small ecosystems (e.g. artificial waterways; see Willby et al., 2001). Large reservoirs became important waterbodies in the Brazilian landscape, especially after the 1970s (Agostinho et al., 1995). As they age these ecosystems exhibit similar ecological succession to that observed in lakes, although on a shorter timescale (Thornton, 1990; Thomaz & Bini, 1999). At some stage of their aging (usually quite early), aquatic plants usually colonize reservoirs (Agostinho et al., 1999; Thomaz & Bini, 1999). Although considered ‘weeds’ when their colonization interferes with multiple uses, this vegetation is very important for functioning and biodiversity conservation in reservoirs (Smart et al., 1996; Agostinho & Gomes, 1997; Martínez et al., 2000). In this study, we first evaluated the number of aquatic macrophytes species in a large subtropical reservoir (Itaipu Reservoir, Brazil). Secondly, we tested the importance of some environmental factors as predictors of macrophyte diversity (S). We used a non-traditional regression approach to analyze the relationships between S and the environmental factors. We demonstrate that the prediction of S in large aquatic environments is not so easily achieved as formerly acknowledged.
selected limnological variables for the larger arms are shown in Table 1. A detailed map and limnological description can be found in Bini et al. (1999) and Thomaz et al. (1999).
Materials and methods Species richness In April 1999 eight arms located along the Brazilian shore (east bank) were extensively surveyed (Arroio Guaçu, São Francisco Verdadeiro, São Francisco Falso, São João, São Vicente, Ocoí, Pinto and Passo Cuê). A total of 235 stands (approximately 30 per arm) was examined from a boat, at low and constant velocity. In each stand, three independent observers spent 5–10 min recording or collecting aquatic macrophytes for subsequent identification. In the Itaipu Reservoir, the maximum depth colonized by aquatic macrophytes is approximately 2 m and they exceptionally reach 4 m (Thomaz et al., 1998). Three meter long rakes, with curved prongs, were also used to collect submerged vegetation. Thus, the risk of underestimating submerged species richness (Ssubm) was minimized. Only euhydrophytes were included in this study. An euhydrophyte was defined as any plant having functional photosynthetic structures and/or rooting structures in or on the surface of the hydrosoil, or water column overlying the hydrosoil, for at least 50% of the time (K. J. Murphy, pers. comm.; Bini et al., 2001). The use of such criterion circumvents problems caused by dubious ways to distinguish aquatic from non-aquatic species (see also Rørslett, 1991).
Study area Abiotic and morphometric data This investigation was carried out in the Itaipu Reservoir, a large (1,350 km2 ) and deep (mean depth = 22.5 m) reservoir located in the Paraná River, between Brazil-Paraguay border (24◦ 05 S and 25◦ 33 S; 54◦ 00 W and 54◦ 37 W). The mean theoretical residence time is 40 days but it reaches ca. 29 days in the main water body, being longer in the sidearms of the reservoir (which are the drowned valleys of influent streams). Water levels are relatively stable, fluctuating less than 1.0 m per year. Aquatic plants colonize mainly the shallow and sheltered areas of the arms (Thomaz et al., 1999). The eight arms surveyed can be classified from meso to eutrophic, according to phosphorus and nitrogen concentrations (Bini et al., 1999). Results of
In each sampling site, measurements of photosynthetic active radiation (PAR; µmol s−1 m−2 ; LiCor underwater quantum sensor), nephelometric turbidity (NTU; Lamote turbidimeter), water transparency (m; Secchi disk) and electrical conductivity (µS.cm−1 ; Digimed) were made at unvegetated depths. The extinction coefficient of light (k) was estimated as k = [ln (I0 ) – ln (Iz )]/z where I0 = irradiance at the subsurface, Iz = irradiance at the depth z. Universal Transverse Mercator (UTM) coordinates of each stand were measured at 2.0 m−1 ). Despite the limited time-window encompassed by our study and the short-term variations in transparency, it seems that high turbidity has negative effect upon Ssubm in Itaipu Reservoir, as shown by previous long-term scale investigations (Thomaz et al., 1998). This fact, found among-sites of a single ecosystem, is considered important in explaining differences in Ssubm among-sites of the same region (Lougheed et al., 2001; Willby et al., 2001) and among systems of different latitudes (Jacobsen & Terneus, 2001). Thus, it seems that light penetration is an important factor in determining Ssubm at different spatial scales. The inspection of our data showed that stands in highly transparent waters (k < 1.0), where only one
species of submerged macrophyte was found, were colonized by one of the following species: Egeria densa Planchon, E. najas, Myriophyllum brasiliense Cambess., Chara guairensis R. Bicudo or Nitella acuminata C. A. Braun ex. Wallman. The architecture of the first three species (‘canopy forming’), which may exclude other submerged species, probably explains their exclusive presence in such sites. Differently, the presence of charophytes in high transparent sites are associated with their dependence on high light availability (Coops & Doef, 1996) and may indicate the beginning of colonization of such places, given that charophytes are early succession plants (Moore, 1986). The maximum Ssubm at intermediate levels of water transparency may be explained considering the simultaneous effect of fetch. In Itaipu Reservoir, each arm may be considered a smaller reservoir, and longitudinal gradients in environmental factors, described by Kimmel et al. (1990), are similarly observed within each one. Indeed, water transparency and fetch were positively correlated (r = 0.32; P < 0.001; n = 235) and both increased along the longitudinal arm axes, from the headwaters to reservoir main body. Thus, although water transparency conditions, near to the reservoir main body are adequate for submerged vegetation growth, the high values of fetch restrict, as described above, the occurrence of most species. Beta diversity indices measure how the species composition changes along environmental gradients (Whittaker, 1972; Wilson & Shmida, 1984; Harrison et al., 1992; Blackburn & Gaston, 1996; Bini et al., 2001). Our data showed that turnover is higher among arms than among stands of the same arm. Such results may be accounted for by peculiarities of the limnological and morphometric features of each arm. In addition, arm isolation may be efficient in increasing species turnover among arms. Beta diversity was also positively correlated with environmental variability. This result may be considered a general expectation and it was corroborated by other studies using different taxonomic groups (Harrison et al., 1992). Considering the low predictive power of our regression model and the observed relationships between S and environmental factors, not described by simple linear or nonlinear functions (Duarte, 1990), the general conclusion of this study can be stated as follows: although aquatic macrophytes species richness in large aquatic environments is lower (Gasith & Hoyer, 1998) than the expected by general speciesarea relationships, the processes that determine the
127 variation of S in such environments can be as complex as in small environments.
Acknowledgements We wish to thank Dr Kevin Joseph Murphy (Glasgow University) for English corrections and comments, and Maria do Carmo Roberto, Raul Ribeiro and Sandro Alves Heil for help during field work. This study was funded by the Itaipu Binacional.
References Agostinho, A. A., A. E. A. Vazzoler & S. M. Thomaz, 1995. The High Paraná River Paraná basin: limnological and ichthyological aspects. In Tundisi, J. G. C. E. M. Bicudo & T. MatsumuraTundisi (eds), Limnology in Brazil. Brazilian Academy of Science/Brazilian Society of Limnology, Rio de Janeiro: 59–104. Agostinho, A. A., L. E. Miranda, L. M. Bini, L. C. Gomes, S. M. Thomaz & H. I. Suzuki, 1999. Patterns of colonization in neotropical reservoirs, and prognosis on aging. In Tundisi J. G. & M. Stra˘skraba (eds), Theoretical Reservoir Ecology and its Applications. International Institute of Ecology/Brazilian Academy of Sciences/Backhuys Publishers, São Carlos: 227–265. Agostinho, A. A. & L. C. Gomes, 1997. Manejo e monitoramento de recursos pesqueiros: perspectivas para o reservatório de Segredo. In Agostinho A. A. & L. C. Gomes (eds), Reservatório de Segredo: Bases Ecológicas Para o Manejo. Eduem, Maringá: 319–264. Amoros, C. & G. Bornette, 1999. Antagonistic and cumulative effects of connectivity: a predictive model based on aquatic vegetation in riverine wetlands. Arch. Hydrobiol. 3: 311–327. Bini, L. M., S. M. Thomaz, K. J. Murphy & A. F. M. Camargo, 1999. Aquatic macrophyte distribution in relation to water and sediment conditions in the Itaipu Reservoir, Brazil. Hydrobiologia 415: 147–154. Bini, L. M., S. M. Thomaz & D. C. Souza, 2001. Species richness and β-diversity of aquatic macrophytes in the Upper Paraná River floodplain. Arch. Hydrobiol. 151: 511–525. Blackburn, T. M. & K. J. Gaston, 1996. The distribution of bird species in the New World: patterns in species turnover. Oikos 77: 146–152. Bornette, G., H. Piegay, A. Citterio, C. Amoros & V. Godreau, 2001. Aquatic plant diversity in four river floodplains: a comparison at two hierarchical levels. Biodivers. Conserv. 10: 1683–1701. Brown, J. H, 1995. Macroecology. University of Chicago Press, Chicago, pp. Chambers, P. A., 1987. Nearshore occurrence of submersed aquatic macrophytes in relation to wave action. Can. J. Fish. aquat. Sci 44: 1666–1669. Coops, H., R. Boeters & H. Smit, 1991. Direct and indirect effects of wave attack on helophytes. Aquat. Bot. 41: 333–352. Coops, H. & R.W. Doef, 1996. Submerged vegetation development in two shallow, eutrophic lakes. Hydrobiologia 340: 115–120. Duarte, C. M. & J. Kalff, 1986. Littoral slope as a predictor of the maximum biomass of submerged macrophyte communities. Limnol. Oceanogr. 31: 1072–1080.
Duarte, C. E., 1990. Variance and the description of nature. In Cole J. J., G. Lovet & S. Findlay (eds), Comparative Analyses of Ecosystems: Patterns, Mechanisms, and Theories. Springer Verlag, New York: 301–318. Duarte, C. M., J. Kalff & R. H. Peters, 1986. Patterns in biomass and cover of aquatic macrophytes in lakes. Can. J. Fish. aquat. Sci. 43: 1900–1908. Esteves, F. A. & R. Barbieri, 1983. Dry weight and chemical changes during decomposition of tropical macrophytes in Lobo Reservoir – Sáo Paulo, Brazil. Aquat. Bot. 16: 285–295. Engelhardt, K. A. M. & M. E. Ritchie, 2001. Effects of macrophyte species richness on wetland ecosystem functioning and services. Nature 411: 687–689. Gasith, A. & M. V. Hoyer, 1998. Structuring role of macrophytes in lakes: changing influence along lake size and depth gradients. In Jeppesen E., M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Ecological Studies, vol. 131. Springer, New York: 381–392. Goldberg, D. E. & S. M. Scheiner, 1993. ANOVA and ANCOVA: Field competition experiments. In Scheiner S. M. & J. Gurevitch (eds), The Design and Analysis of Ecological Experiments. Chapman & Hall, New York: 69–93. Gotelli, N. J. & G. L. Entsminger, 2000. EcoSim: Null models software for ecology. Version 5.0. Acquired Intelligence Inc. & Kesey-Bear. http://homepages.together.net/gentsmi n/ecosim.htm. Håkanson, L. & M. Jansson, 1983. Principles of lake sedimentology. Springer-Verlag, Berlin. 316 pp. Harrison, S., S. J. Ross & J. H. Lawton, 1992. Beta diversity on geographic gradients in Britain. J. anim. Ecol. 61: 151–158. Heegaard, E., H. H. Birks, C. E. Gibson, S. J. Smith & S. WolfeMurphy, 2001. Species-environmental relationships of aquatic macrophytes in Northern Ireland. Aquat. Bot. 70: 175–223. Henderson, H. V. & P. F. Velleman., 1981. Building multipleregression models interactively. Biometrics 37: 391–411. Hudon, C., S. Lalonde & P. Gagnon, 2000. Ranking the effects of site exposure, plant growth form, water depth, and transparency on aquatic plant biomass. Can. J. Fish. aquat. Sci. 57: 31–42. Jacobsen, D. & E. Terneus, 2001. Aquatic macrophytes in cool aseasonal and seasonal streams: a comparison between Ecuadorian highland and Danish lowland streams. Aquat. Bot. 71: 281–295. Jackson, S. T. & D. F. Charles, 1988. Aquatic macrophytes in Adirondack (New York) lakes: patterns of species composition in relation to environment. Can. J. Bot. 66: 1449–1460. Kimmel, B. L., O. T. Lind & L. J. Paulson, 1990. Reservoir Primary Production. In Thornton K. W., B. L. Kimmel & F. E. Payne (eds), Reservoir Limnology: Ecological Perspectives. John Wiley & Sons, New York: 133–194. Lougheed, V. L., B. Crosbie & P. Chow-Fraser, 2001. Primary determinants of macrophyte community structure in 62 marshes across the Great Lakes basin: latitude, land use, and water quality effects. Can. J. Fish. aquat. Sci. 58: 1603–1612. Manly, B. F. J., 1991. Randomization and Monte Carlo Methods in Biology. Chapman and Hall, London. 281 pp. Martínez, J. C. C., A. Canesin & C. C. Bonecker, 2000. Species composition of rotifers in different habitats of an artificial lake, Mato Grosso do Sul State, Brazil. Acta Scientiarum 22: 343–346. Moore, J. A., 1986. Charophytes of Great Britain and Ireland. Botanical Society of the British Islands, London. 141 pp. Murphy, K. J., B. Rørslett & I. Springuel, 1990. Strategy analysis of submerged lake macrophyte communities: an international example. Aquat. Bot. 36: 303–323.
128 Nilsson, C. & P. A. Keddy, 1988. Predictability of change in shoreline vegetation in a hydroelectric reservoir, Northern Sweden. Can. J. Fish. aquat. Sci. 45: 1896–1904. Rea, T. E., D. J. Karapatakis, K. K. Guy, J. E. Pinder III & H. E. Mackey Jr., 1998. The relative effects of water depth, fetch and other physical factors on the southeastern U.S. pond. Aquat. Bot. 61: 289–299. Robach, F., I. Eglin & M. Tremolieres, 1997. Species richness of aquatic macrophytes in former channels connected to a river: a comparison between two fluvial hydrosystems differing in their regime and regulation. Global Ecol. Biogeogr. 6: 267–274. Rørslett, B., 1991. Principal determinants of aquatic macrophyte richness in Northern European lakes. Aquat. Bot. 39: 173–193. Smart, R. M., R. D. Doyle & J. D. Madsen, 1996. Establishing native submersed aquatic plant communities for fish habitat. Am. Fish. Soc. Symp. 16: 347–356. Sand-Jensen, K., T. Riis, O. Vestergaard & S. E. Larsen, 2000. Macrophyte decline in Danish lakes and streams over the past 100 years. J. Ecol. 88: 1030–1040. Scheffer, M., M. R. Redelijkheid & F. Noppert, 1992. Distribution and dynamics of submerged vegetation in a chain of shallow eutrophic lakes. Aquat. Bot. 42: 199–216. Sokal, R. R. & F. J. Rohlf, 1981. Biometry. 2nd. Ed. W. H. Freeman and Company, New York. 859 pp. Thomaz, S. M., L. M. Bini & D. C. Souza, 1998. Biomass and maximum colonization depth of Egeria najas Planchon (Hydrocharitaceae) at Itaipu Reservoir, Brazil. In Monteiro A., T. Vasconcelos & L. Catarino (eds), Management and Ecology of Aquatic Plants. Proceedings of the 10th EWRS International Symposium on Aquatic Weeds. EWRS/APRH, Lisbon: 223–226. Thomaz, S. M. & L. M. Bini, 1999. A expansão das macrófitas aquáticas e implicações para o manejo de reservatórios: um estudo na represa de Itaipu. In Henry R. (ed), Ecologia de Reservatórios: Estrutura, Função e Aspectos Sociais. Fundibio, Botucatu: 599–625.
Thomaz, S. M., L. M. Bini, M. C. Souza, K. K. Kita & A. F. M. Camargo, 1999. Aquatic macrophytes of Itaipu Reservoir, Brazil: Survey of species and ecological considerations. Brazil. archiv. biol. technol. 42: 15–22. Thornton, K. W., 1990. Sedimentary processes. In Thornton K. W., B. L. Kimmel & F. E. Payne (eds), Reservoir Limnology: Ecological Perspectives. John Wiley & Sons, New York: 43–69. Tockner, K., F. Schiemer, C. Baumgartner, G. Kum, E. Weigand, I. Zweimuller & J. V. Ward, 1999. The Danube restoration project: Species diversity patterns across connectivity gradients in the floodplain system. Regul. Riv. 15: 245–258. Vestergaard, O. & K. Sand-Jensen, 2000a. Aquatic macrophyte richness in Danish lakes in relation to alkalinity, transparency, and lake area. Can. J. Fish. aquat. Sci. 57: 2022–2031. Vestergaard, O. & K. Sand-Jensen, 2000b. Alkalinity and trophic state regulate aquatic plant distribution in Danish lakes. Aquat. Bot. 67: 85–107. Wall, D., H. Mooney, G. Adams, G. Boxshall, A. Dobson, T. Nakashizuka, J. Seyani, C. Samper & J. Sarukhan, 2001. An International Biodiversity Observation Year. Trends Ecol. Evol. 16: 52–54. Whittaker, R. H., 1972. Evolution and measurement of species diversity. Taxon 21: 213–251. Willby, N. J., J. R. Pygott, & J. W. Eaton, 2001. Inter-relationship between standing crop, biodiversity and trait attributes of hydrophytic vegetation in artificial waterways. Freshwat. Biol. 46: 883–902. Wilson, M. V. & A. Shmida, 1984. Measuring beta diversity with presence-absence data. J. Ecol. 72: 1055–1064.
