Acessibilidade / Reportar erro

Distribution of periphytic algae in wetlands (Palm swamps, Cerrado), Brazil

Distribuição de algas perifíticas em áreas úmidas (Veredas, Cerrado), Brasil

Abstracts

The distribution of periphytic algae communities depends on various factors such as type of substrate, level of disturbance, nutrient availability and light. According to the prediction that impacts of anthropogenic activity provide changes in environmental characteristics, making impacted Palm swamps related to environmental changes such as deforestation and higher loads of nutrients via allochthonous, the hypothesis tested was: impacted Palm swamps have higher richness, density, biomass and biovolume of epiphytic algae. We evaluated the distribution and structure of epiphytic algae communities in 23 Palm swamps of Goiás State under different environmental impacts. The community structure attributes here analyzed were composition, richness, density, biomass and biovolume. This study revealed the importance of the environment on the distribution and structuration of algal communities, relating the higher values of richness, biomass and biovolume with impacted environments. Acidic waters and high concentration of silica were important factors in this study. Altogether 200 taxa were identified, and the zygnemaphycea was the group most representative in richness and biovolume, whereas the diatoms, in density of studied epiphyton. Impacted Palm swamps in agricultural area presented two indicator species, Gomphonema lagenula Kützing and Oedogonium sp, both related to mesotrophic to eutrophic conditions for total nitrogen concentrations of these environments.

acidic water; anthropogenic activity; ecology; epiphyton


A distribuição de comunidades de algas perifíticas depende de vários fatores, como tipo de substrato, nível de distúrbio, disponibilidade de nutrientes e luz. De acordo com a predição de que impactos de ação antrópica proporcionam alterações nas características ambientais – tornando Veredas impactadas relacionadas a alterações ambientais, como desmatamentos e maiores cargas de nutrientes via alóctone –, a hipótese testada foi: Veredas impactadas apresentam maiores riqueza, densidade, biomassa e biovolume de algas epifíticas. Avaliaram-se a distribuição e a estruturação de comunidades de algas epifíticas em 23 Veredas do Estado de Goiás sob diferentes impactos ambientais. Os atributos da estrutura de comunidade avaliados foram composição, riqueza, densidade, biomassa e biovolume. Este estudo revelou a importância das características ambientais na distribuição e na estruturação das comunidades de algas, relacionando os maiores valores de riqueza, biomassa e biovolume dos organismos aos ambientes impactados. Águas ácidas e altas concentrações de sílica foram fatores importantes no estudo. Ao todo, foram identificados 200 táxons, sendo as zignemafíceas o grupo mais representativo em riqueza e biovolume, enquanto as diatomáceas, as mais representativas em densidade do epifíton estudado. Veredas impactadas em área de agropecuária apresentaram duas espécies indicadoras, Gomphonema lagenula e Oedogonium sp., ambas relacionadas com condições mesotróficas a eutróficas, para concentrações de nitrogênio total desses ambientes.

águas ácidas; ação antrópica; ecologia; epifíton


1. Introduction

The Palm swamps are wetlands, marshy or wet environments of headwaters from the Brazilian Central Plateau, feeding the water courses for local and regional network, and form the three major Brazilian watersheds: Platina, São Francisco and Amazon (Ferreira, 2006FERREIRA, IM., 2006. Modelos geomorfológicos das Veredas em ambiente de Cerrado. Espaço revista Geografia, vol. 7-8, p. 7-11.). They are characterized by presenting “buritizais” (Mauritia vinifera L. and M. flexuosa Mart.) as remarkable phanerogamic flora (Ribeiro and Walter, 1998RIBEIRO, JF. and WALTER, BMT., 1998. Fitofisionomias do bioma Cerrado. In SANO, SM. and ALMEIDA, SP. (Eds.). Cerrado: ambiente e flora. Planaltina: Embrapa-CPAC. p. 89-166.). The importance of this subsystem of the Cerrado is in its contribution to continuity and regularity of its water courses, to protect the headwaters, supply of water, food and shelter for wildlife (Carvalho, 1991CARVALHO, PGS. 1991. As Veredas e sua importância no domínio dos Cerrados. Informe agropecuário, vol. 168, p. 47-54.).

Deforestation for pasture and agricultural purposes (Allan, 2004ALLAN, JD., 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology and Systematics, vol. 35, p. 257-284. http://dx.doi.org/10.1146/annurev.ecolsys.35.120202.110122
http://dx.doi.org/10.1146/annurev.ecolsy...
) along with urbanization and sources of domestic and industrial pollution (Agostinho et al., 2005AGOSTINHO, AA, THOMAZ, SM. and GOMES, LC., 2005. Conservation of the biodiversity of Brazil's Inland waters. Conservation Biology, vol. 19, p. 646-652. http://dx.doi.org/10.1111/j.1523-1739.2005.00701.x
http://dx.doi.org/10.1111/j.1523-1739.20...
) influence the structure and functioning of aquatic ecosystems (Marcarelli et al., 2009MARCARELLI, AM., BECHTOLD, HA., RUGENSKI, AT. and INOUY, RS., 2009. Nutrient limitation of biofilm biomass and metabolism in the Upper Snake River basin, southeast Idaho, USA. Hydrobiologia, vol. 620, p. 63-7. http://dx.doi.org/10.1007/s10750-008-9615-6
http://dx.doi.org/10.1007/s10750-008-961...
) by changing hydrological and hydraulic patterns, modifying the geomorphology, interfering in water quality (Tundisi et al., 2004TUNDISI, JG., MATSUMURA-TUNDISI, T., ARANTES JUNIOR, JD., TUNDISI, JEM., MANZINI, NF. and DUCROT, R., 2004. The response of Carlos Botelho (Lobo, Broa) reservoir to the passage of cold fronts as reflected by physical, chemical and biological variables. Brazilian Journal of Biology, vol. 64, p. 177-186. PMid:15195377. http://dx.doi.org/10.1590/S1519-69842004000100020
http://dx.doi.org/10.1590/S1519-69842004...
), besides initiating negative impacts on the integrity of these ecosystems. These changes may undermine the biodiversity of these environments and, in Palm swamps, may also undermine several watersheds whose headwaters are located in the Cerrado Biome.

Among the aquatic communities, periphytic algae are one of the major primary producers, affecting the growth, development, survival and reproduction of many organisms (Campeau et al., 1994CAMPEAU, S., MURKIN, HR. and TITMAN, RD., 1994. Relative importance of algae and emergent plant litter to freshwater marsh invertebrates. Canadian Journal of Fisheries and Aquatic Sciences, vol. 51, p. 681-692. http://dx.doi.org/10.1139/f94-068
http://dx.doi.org/10.1139/f94-068...
). Establishing the structure of these communities depends on several factors, such as the type of substrate (Cattaneo et al., 1997CATTANEO, A., KERIMIAN, T., ROBERGE, M. and MARTY, J., 1997. Periphyton distribution and abundance on substrata of different size along a gradient of stream trophy. Hydrobiologia, vol. 354, p. 101-110. http://dx.doi.org/10.1023/A:1003027927600
http://dx.doi.org/10.1023/A:100302792760...
), disturbance level (Biggs et al., 1998BIGGS, JF., STEVENSON, RJ. and LOWE, RL., 1998. A habitat matrix conceptual model for stream periphyton. Archiv für Hydrobiologie, vol. 143, p. 21-56.), hydrological regimes (Algarte et al., 2009ALGARTE, VM., SIQUEIRA, NS., MURAMAKI, EA. and RODRIGUES, L., 2009. Effects of hydrological regime and connectivity on the interannual variation in taxonomic similarity of periphytic algae. Brazilian Journal of Biology, vol. 69, p. 609-616. PMid:19738967. http://dx.doi.org/10.1590/S1519-69842009000300015
http://dx.doi.org/10.1590/S1519-69842009...
), availability of nutrients (Elser et al., 2007ELSER, JJ., BRACKEN, MES., CLELAND, EE., GRUNER, DS., HARPOLE, WS., HILLEBRAND, H., NGAI, JT., SEABLOOM, EW., SHURIN, JB. and SMITH, JE., 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters, vol. 10, p.1135-1142. PMid:17922835. http://dx.doi.org/10.1111/j.1461-0248.2007.01113.x
http://dx.doi.org/10.1111/j.1461-0248.20...
; Ferragut and Bicudo, 2010FERRAGUT, C. and BICUDO, DC., 2010. Periphytic algal community adaptive strategies in N and P enriched experiments in a tropical oligotrophic reservoir. Hydrobiologia, vol. 646, p. 295-309. http://dx.doi.org/10.1007/s10750-010-0168-0
http://dx.doi.org/10.1007/s10750-010-016...
; Larson et al., 2012LARSON, CA., PASSY, SI. and LAANBROEK, R., 2012. Taxonomic and functional composition of the algal benthos exhibits similar successional trends in response to nutrient supply and current velocity. Federation of European Microbiological, vol. 80, no. 2, p. 352-62.), light (Hill, 1996HILL, WR., 1996. Effects of light. In STEVENSON, RJ., BOTHWELL, ML. and LOWE, RL. (Eds.). Algal ecology: freshwater bentic ecosystems. New York: Academic Press. p. 121-148.; Tuji, 2000TUJI, A., 2000. The effect of irradiance on the growth of different forms of freshwater diatoms: implications for sucession in attached diatom communities. Journal of Phycology, vol. 36, p. 659-661. http://dx.doi.org/10.1046/j.1529-8817.2000.99212.x
http://dx.doi.org/10.1046/j.1529-8817.20...
), trophy (Biggs, 1996BIGGS, BJF., 1996. Patterns in benthic algal of streams. In STEVENSON, RJ., BOTHWELL, ML. and LOWE, RL. (Eds.). Algal ecology: freshwater benthic ecosystems. New York: Academic Press. p. 31-56.), water quality and system hydrodynamics (Moschini-Carlos et al., 2000MOSCHINI-CARLOS, V., HENRY, R. and POMPÊO, MLM., 2000. Seasonal variation of biomass and productivity of the periphytic community on artificial substrata in the Jurumirim Reservoir (São Paulo, Brazil). Hydrobiologia, vol. 434, p. 35-40. http://dx.doi.org/10.1023/A:1004086623922
http://dx.doi.org/10.1023/A:100408662392...
), temperature (Marcarelli and Wurtsbaugh, 2006MARCARELLI, AM. and WURTSBAUGH, WA., 2006. Temperature and nutrients interact to control nitrogen fixation in oligotrophic streams: an experimental examination. Limnology and Oceanography, vol. 51, p. 2278-2289. http://dx.doi.org/10.4319/lo.2006.51.5.2278
http://dx.doi.org/10.4319/lo.2006.51.5.2...
) and biological control by grazing (Rosemond et al., 1993ROSEMOND, AD., MULHOLLAND, PJ. and ELWOOD, JW., 1993. Top-Down and bottom-up control of stream periphyton: effects of nutrients and herbivores. Ecology, vol. 74, p. 1264-1280. http://dx.doi.org/10.2307/1940495
http://dx.doi.org/10.2307/1940495...
).

Biological indicators (‘bioindicators’) are readily measured components of the biota that are used to provide general information about the complex ecosystems in which they occur (Andersen, 1999ANDERSEN, AN., 1999. My bioindicator or yours? Making the selection. Journal of Insect Conservation, vol. 3, p. 61-64. http://dx.doi.org/10.1023/A:1017202329114
http://dx.doi.org/10.1023/A:101720232911...
). Due to the high abundance, cosmopolitanism, sensitivity to chemical changes, eutrophication and pollution, algae are considered excellent bioindicators (Larson et al., 2012LARSON, CA., PASSY, SI. and LAANBROEK, R., 2012. Taxonomic and functional composition of the algal benthos exhibits similar successional trends in response to nutrient supply and current velocity. Federation of European Microbiological, vol. 80, no. 2, p. 352-62.).

Despite such importance of the Palm swamps as a threatened neotropical ecosystem, studies linked to these environments related communities of algae, focusing on taxonomy, diversity and ecology are incipient, highlighting only Menezes (1986)MENEZES, M., 1986. Ficoflórula da Chapada dos Guimarães e arredores, Mato Grosso, Brasil: Euglenaceae e pigmentadas (Euglenophyceae). Rickia, vol. 13, p. 87-95. for taxonomy of planktonic algae. Considering the high rate of degradation in Palm swamps caused by human activities and the importance of phycoperiphyton to aquatic ecosystems, the present study aimed to evaluate the distribution and structure of periphytic algal community in Palm swamps under different environmental impacts, in Goiás State. The following hypothesis was tested in this study: Palm swamps impacted present higher richness, density, biovolume and biomass of periphytic algae. We can predict that anthropogenic impacts change environmental characteristics, thus urban Palm swamps and in agriculture areas are related to various environment changes such as deforestation and higher allochthonous input of nutrients. Several studies have demonstrated that an increase in nutrients, in particular, increased productivity and periphytic chlorophyll (Dodds et al., 1997DODDS, WK., SMITH, VH. and ZANDER, B., 1997. Developing nutrient targets to control benthic chlorophyll levels in streams: a case study of the Clark Fork River. Water Research, vol. 31, p. 1738-1750. http://dx.doi.org/10.1016/S0043-1354(96)00389-2
http://dx.doi.org/10.1016/S0043-1354(96)...
; Bourassa and Cattaneo, 2000BOURASSA, N. and CATTANEO, A. 2000. Responses of a lake outlet community to light and nutrient manipulation: effects on periphyton and invertebrate biomass and composition. Freshwater Biology, vol. 44, p. 629-639. http://dx.doi.org/10.1046/j.1365-2427.2000.00610.x
http://dx.doi.org/10.1046/j.1365-2427.20...
), are therefore due to the density of periphytic algae of such environments.

2. Material and Methods

The Palm swamps examined in Goiás State are located in the municipalities of Caldas Novas, Catalão, Cidade de Goiás, Goiânia, Ipameri, Morrinhos and Piracanjuba (Figure 1). We sampled 23 Palm swamps: six in conserved areas – with native vegetation in the surroundings wider than 50 m – according to Law n° 7803 from July, 18 1983 (Brasil, 1992Brasil. Ministério do Meio Ambiente, 1992. Resoluções CONAMA de 1984 a 1991. 4. ed. Brasília: SEMAM/IBAMA. 245 p.); nine in areas impacted by agriculture (under the influence of inputs such as fertilizers, herbicides and pesticides) and eight in urban areas (under the influence of domestic sewage and urban drainage). Nevertheless, all studied environments are within regions of low native vegetation cover of Goiás region (Bonnet et al., 2007BONNET, BRP., FERREIRA, NC. and FERREIRA, LG., 2007. Ampliação de ambientes ripários como alternativa ás reservas legais: conciliando política florestal e conservação dos recursos hídricos no Bioma Cerrado. Boletim Goiano de Geografia, vol. 27, p. 97-115.). The characterizations regarding the presence of current flow, geomorphological position (Ferreira, 2006FERREIRA, IM., 2006. Modelos geomorfológicos das Veredas em ambiente de Cerrado. Espaço revista Geografia, vol. 7-8, p. 7-11.), location, date and sampling time, vegetation cover and type of impact of studied environments are listed in Table 1.

Figure 1.
Location of the 23 Palm swamps sampled in Goiás State during the months of August and September 2008.

Table 1.
Location, date and sampling time, vegetation cover, impact, current flow and geomorphological position of the 23 Palm swamps studied in Goiás State during the months of August and September 2008.

Samplings were undertaken in August and September 2008. Morphometrical analyses of Palm swamps (maximum width of the water body, depth of sampling points, marginal vegetation cover) were measured as suggested by Wetzel and Likens (1991)WETZEL, RG. and LIKENS, GE., 1991. Limnological analysis. 2nd ed. New York: Springer-Verlag.. Limnological variables (pH, water temperature, electric conductivity and turbidity) were gauged concurrently to biotic data collection, and were taken using a multi-parameter water analyzer Horiba model U-22.

The nutrients (total nitrogen and total phosphorus expressed in µg L−1) were measured according to standard methods (APHA, 2005America Public Health Association – APHA, 2005. Standard methods for examination of water and wasterwater. 21nd ed. Washington: APHA.), for which we collected 1L of raw water at each sampling point, fixed in situ with 0.5mL of acid sulfuric p.a., and then processed it. For silica, samples were collected of 250mL of water at each sampling point and analyses (expressed in µg L−1 of SiO2) were done according to APHA (2005)AGOSTINHO, AA, THOMAZ, SM. and GOMES, LC., 2005. Conservation of the biodiversity of Brazil's Inland waters. Conservation Biology, vol. 19, p. 646-652. http://dx.doi.org/10.1111/j.1523-1739.2005.00701.x
http://dx.doi.org/10.1111/j.1523-1739.20...
.

In order to evaluate the trophic status of lentic and lotic palm swamps two indices were used: the proposed one by Lamparelli (2004)LAMPARELLI, MC., 2004. Grau de trofia em corpos d'água do estado de São Paulo: avaliação dos métodos de monitoramento. São Paulo: Universidade de São Paulo. 238 p. Tese de Doutorado em Ecologia Aplicada. for a tropical environment using total phosphorus as a parameter and the one proposed by Dodds et al. (1997)DODDS, WK., SMITH, VH. and ZANDER, B., 1997. Developing nutrient targets to control benthic chlorophyll levels in streams: a case study of the Clark Fork River. Water Research, vol. 31, p. 1738-1750. http://dx.doi.org/10.1016/S0043-1354(96)00389-2
http://dx.doi.org/10.1016/S0043-1354(96)...
for temperate environment using nitrogen and total phosphorus as parameters.

Each Palm swamp was sampled once in this study and periphytic material was obtained from grasses (Poaceae) which were partially submerged, predominant in the environments and randomly selected, as suggested by Rodrigues et al. (2004)RODRIGUES, L., LEANDRINE, JA., JATI, S., FONSECA, IA. and SILVA, ELV., 2004. Structure of communities of Periphytic Algae in the Upper Paraná River Floodplain. In AGOSTINHO, AA., RODRIGUES, L., GOMES, LC., THOMAZ, SM. and MIRANDA, LE. (Eds.). Structure and funcioning of the Paraná river and its floodplain. Maringá: Ed. Eduem. p. 43-50., according to criteria as collected from adult and uniform plants, without evident presence of predation. The periphytic material was obtained from replicates from two petioles of different plants at each Palm swamp, with a total of 46 quantitative samples. The part of the submerged petiole was cut and the epiphytic material was scraped with a steel blade wrapped in aluminum foil and jets of distilled water. The scraped areas of the petioles were then calculated.

Chlorophyll-a samples were taken in replicate from two samples of different plants at each Palm swamp and the analyses performed with 90% acetone extraction (results of chlorophyll-a expressed in µg cm−2) according to Golterman et al. (1978)GOLTERMAN, HL., CLYMO, RS. and OHMSTAD, MAM., 1978. Methods for physical and chemical analysis of fresh waters. Oxford: Blackwell Scientific. 214 p.. For quantitative samples, the epiphytic material obtained in replicates was then fixed with acetic Lugol's solution 0.5% (Bicudo and Menezes, 2006BICUDO, CEM. and MENEZES, M., 2006. Gêneros de algas de águas continentais do Brasil (Chave de identificação e descrições). 2nd ed. São Carlos: Rima. 498 p.).

The periphytic algae were quantified by the method of Utermöhl (1958)UTERMÖHL H. 1958. Zur Vervollkommung der quantitativen phytoplancton-methodik. Mitteilungen Internationale Vereinigung für Theoretische und Angewandte Limnologie, vol. 9, p. 1-38. in random fields up to 100 individuals of the most common species (Bicudo, 1990BICUDO, DC., 1990. Considerações sobre metodologias de contagem de algas do perifíton. Acta Limnologica Brasilica, vol. 3, p. 459-475.), using a Zeiss Axiovert 25 inverted microscope with an objective to 400-fold increase. In order to identify the diatom species, the quantitative material was oxidized and cleaned using the technique of Simonsen (1974)SIMONSEN, R., 1974. The diatom plankton of the indian ocean expedition of R/V “Meteor”. Meteor Forschungsergebnisse Reihe D-Biologie, vol. 19, p. 1-66. modified by Moreira-Filho and Valente-Moreira (1981)MOREIRA-FILHO, H. and VALENTE-MOREIRA, IM., 1981. Avaliação taxonômica e ecológica das diatomáceas (Bacillariophyceae) epífitas em algas pluricelulares obtidas nos litorais dos estados dos estados do Paraná, Santa Catarina e São Paulo. Boletim Museu Botânico Municipal, vol. 47, p. 1-17., and permanent slides were prepared using Naphrax resin as embedding medium for diatom frustules. Taxa analysis was performed using a Zeiss Axioscop 40 optical microscope equipped with an image capture system, and was identified based on morphological characteristics, size and shape of stalk organization, using recent and updated literature. The classification system adopted was that proposed by Round (1971)-, 1971. The taxonomy of the Chlorophyta, 2. British Phycological Journal, vol. 6, p. 235-264. http://dx.doi.org/10.1080/00071617100650261
http://dx.doi.org/10.1080/00071617100650...
.

Species density was estimated according to Ros (1979)ROS, J., 1979. Práticas de Ecologia. Barcelona: Ed. Omega. 181 p. and the results were shown in the number of individuals per unit area (ind cm−2). The biovolume estimate followed Hillebrand et al. (1999)HILLEBRAND, H., DÜRSELEN, C., KIRSCHTEL, D., POLLINGHER, U. and ZOHARY, T., 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, vol. 35, p. 403-424. http://dx.doi.org/10.1046/j.1529-8817.1999.3520403.x
http://dx.doi.org/10.1046/j.1529-8817.19...
from the multiplication of the densities of each individual by the average biovolume of organisms of the species, according to the size of analyzed populations, and the final result was given in mm3cm−2. We determined the dominance and abundance of species as proposed by Lobo and Leighton (1986)LOBO, EA. and LEIGHTON, G., 1986. Estruturas de las fitocenosis planctônicas de los sistemas de desembocaduras de rios y esteros de La zona central de Chile. Revista de Biologia Marina, vol. 22, p. 143-170., where dominant species are those with densities higher than 50% of total density of the community, and abundant were those species whose densities exceed the mean density of populations of each sample.

The principal component analysis (PCA) was used to verify the spatial variation of the environments in relation to limnological variables. The criteria used to retain the axes for interpretation was the Broken-Stick. For this analysis, the matrix of limnological data was previously standardized [(Xij-Xi)/Si] (Legendre and Legendre, 1998LEGENDRE, P. and LEGENDRE, L., 1998. Numerical ecology. 2nd ed. Elsevier Science. 853 p.). Analysis of variance (One way ANOVA) was applied to the scores generated by PCA for the axes retained to test the differences between the environments and the limnological variables, and the impact of Palm swamps was used as a factor to analyse.

Detrended correspondence analysis (DCA, Hill and Gauch, 1980HILL, MO. and GAUCH, HG., 1980. Detrend correspondence analysis, an improved ordination technique. Vegetatio, vol. 42, p. 47-58. http://dx.doi.org/10.1007/BF00048870
http://dx.doi.org/10.1007/BF00048870...
) was applied to verify the similarity between the species composition summarized by classes among the environments studied. A non-metric multidimensional scaling (NMDS) was used to investigate the distribution of the algae group with the highest density among environments. This ordination was used with transformed data matrix by log x + 1 (Legendre and Legendre, 1998LEGENDRE, P. and LEGENDRE, L., 1998. Numerical ecology. 2nd ed. Elsevier Science. 853 p.). The Bray-Curtis index was used for calculating the distances and checking the stress level of adjustment of the newly created axes and the ordering of the dissimilarity matrix (Kruskal and Wish, 1978KRUSKAL, JB. and WISH, M., 1978. Multidimensional scaling: Sage university paper series on quantitative applications in the social Sciences. Beverly Hills: Sage publications. 111 p.). Usually stress values below 20 are acceptable for this analysis (Zheng and Stevenson, 2006ZHENG, L. and STEVENSON, RJ., 2006. Algal assemblages in multiple habitats of restored and extant wetlands. Hydrobiologia, vol. 561, p. 221-238. http://dx.doi.org/10.1007/s10750-005-1616-0
http://dx.doi.org/10.1007/s10750-005-161...
).

The indicator species analysis (Indval, Dufrêne and Legendre, 1997DUFRÊNE, M. and LEGENDRE, P., 1997. Species assemblages and indicator species: the need of asymmetrical approach. Ecological Monographs, vol. 67, p. 345-366.) was performed to evaluate possible species indicators of the studied environments, applied to density of all the dominant and abundant taxa (species matrix log transformed, log x + 1). This method is based on the comparison of relative abundance (specificity) and frequency of occurrences (fidelity) of taxa in different set of environments. The indicator value (IV) ranges from 0 to 100, and is maximum when the individuals of a species show high specificity and high fidelity to all environments of a particular group specified a priori. This analysis was tested by Monte Carlo with 999 randomizations with p < 0.05.

The hypothesis of the present study was tested by an ANOVA (One-Way), using the type of impact on the Palm swamps as factor, assessing if there is difference in the attributes richness, density, biovolume and biomass of epiphytic algae among the Palm swamps examined. All multivariate analysis was conducted using the program PC-ORD version 4.01 (McCune and Mefford, 1999McCUNE, B. and MEFFORD, MJ., 1999. PC-ORD. Multivariate Analysis of Ecological Data. version 4. Oregon: MJM Software Design.) and ANOVA for the program STATISTICA version 7.1 (Statsoft, 2005Statsoft Inc., 2005. Statistica (data analysis software system). version 7.1. Available from: www.statsoft.com.
www.statsoft.com...
).

3. Results

3.1.

Limnological characterization

All the studied Palm swamps presented high values of silica (28.675 × 103 to 727.415 × 103 µg.L−1) and acidic pH (4.6 to 6.9). Low values of electric conductivity were observed in Palm swamps located in areas impacted by agriculture (9, 10, 11, 12), while 7, 8, 13, 14, 15 and 16 had higher conductivity. The Palm swamps situated in urban areas (21, 22 and 23) were resembled by presenting pH values closer to 6 and the higher values of total phosphorus in the present study. The maximum concentration of chlorophyll-a registered was 193.24 µg cm−2 (palm swamp 22), whereas in the palm swamps 8, 11 and 21 this parameter was not detected. Limnological variables values are listed in Table 2.

Table 2.
Morphometric, limnological variables and trophic state index of the 23 Palm swamps in Goiás State, during the study period (PROF-depth, LARG-width, COND-electric conductivity, pH, TEMP-water temperature, TURB- turbidity, PT- total phosphorus, NT- total nitrogen, SIL- silica, CLO-chlorophyll-a, TSI- trophic state index, OLIGO-oligotrophic, MESO- mesotrophic, EUT- eutrophic, HIPER-hipereutrophic).

For total phosphorus concentrations, 95.6% of environments were classified as oligotrophic according to both indices used (Table 2). For total nitrogen concentrations, 30.4% were classified as hipereutrophic environments, and among conserved palm swamps, only one was oligotrophic (Table 2).

PCA results represented 63.2% of total data variability in the first two axes. The first axis was most influenced by electric conductivity and turbidity (Figure 2). The second axis was related with total phosphorus (Figure 2). This analysis showed a gradient between the environment, with preserved Palm swamps and that in urban areas at the extremes and Palm swamps in areas of agriculture as intermediaries. The conserved Palm swamps were highlighted since they presented the lowest values of total nitrogen (except palm swamp 3) (Table 2).

Figure 2.
Principal component analysis biplot with ordination of the studied environments in relation to limnological variables.

The results of ANOVA show differences between Palm swamps with different impacts only to scores for PCA 2 (F = 13.49 p < 0.001), and the differences were significant between all impacts (Tukey, p < 0.05). The variables reached the assumptions for analysis.

3.2.

Epiphytic algal community

The community was represented by 200 taxa, distributed into 66 genera and 10 classes (Bacillariophyceae – 43 taxa, Chlorophyceae – 26, Cyanophyceae – 25, Chrysophyceae – 5, Dinophyceae – 4, Euglenophyceae – 8, Oedogoniophyceae – 6, Rhodophyceae – 1, Xanthophyceae – 3 and Zygnemaphyceae – 79). The genera with the highest number of taxa for the classes Zygnemaphyceae and Bacillariophyceae were respectively Cosmarium Corda (21 taxa) and Eunotia Ehrenberg (nine taxa).

Conserved Palm swamps presented lower richness of taxa, mainly represented by Bacillariophyceae and Cyanophyceae (Figure 3). On the other hand, impacted Palm swamps, with a greater number of taxa, presented Zygnemaphyceae as the most expressive class (Figure 3). The Palm swamps with greater richness were the impacted 19 (33 taxa) and 12 (31 taxa) (Figure 3).

Figure 3.
Richness of the epiphytic algae classes in each studied Palm swamp (Zygn - Zygnemaphyceae, Xant - Xanthophyceae, Rhod - Rhodophyceae, Oedo - Oedogoniophyceae, Eugl- Euglenophyceae, Dino - Dinophyceae, Chry - Chrysophyceae, Cyan - Cyanophyceae, Chlo - Chlorophyceae, Baci - Bacillariophyceae).

For density of taxa, the Bacillariophyceae class was the most relevant, followed by Zygnemaphyceae and Cyanophyceae (Figure 4). Among the examined environments, the highest density values were observed in impacted Palm swamps (palm swamp 19, with the highest density 158.734 × 103 ind cm−2); and the lowest in the conserved Palm swamp 5 (634.54 ind.cm−2) (Figure 4).

Figure 4.
Logarithm of the density of the main classes of epiphytic algae registered in the 23 Palm swamps studied in Goiás State (Baci - Bacillariophyceae, Zygn - Zygnemaphyceae, Cyan - Cyanophyceae, Chlo - Chlorophyceae, Other - others classes).

Zygnemaphyceae was the most significant class regarding biovolume, mainly by the occurrence of filamentous taxa. Similarly to density values, the highest biovolume values were also verified in impacted Palm swamps, mainly for the lentic and urban Palm swamps 20 (Spirogyra) and U18 (Mougeotia) (Figure 5).

Figure 5.
Logarithm of the biovolume of the main classes registered in the studied environments in Goiás State, between August and September 2008 (Baci - Bacillariophyceae).

According to criteria of dominance and abundance adopted, six taxa were dominant (Aphanothece chlatrata West & West; Chlorella vulgaris Beyerinck; Eunotia bilunaris (Ehrenberg) Mills; Eunotia mucophila Lange-Bertalot; Spirogyra sp.6; Tapinothrix bornetii Sauvageau) and 54 were abundant (25.9% belonging to class Bacillariophyceae, and 24% to Zygnemaphyceae (Table 3). Among dominant and abundant organisms occurred the predominance of filamentous algae; 83% of Cyanophyceae and 54% of Zygnemaphyceae presented this morphology (Table 3).

Table 3.
List of dominant and abundant taxa recorded in the 23 Palm swamps studied in Goiás State between August and September 2008 (Legend: A- abundant taxa; D- dominant taxa).

Detrended correspondence analysis (DCA) showed 65% of the variability of the data represented in the first two axes, with eigenvalues 0.51 (first axe) and 0.14 (second axe) (Figure 6). The difference in epiphytic algae composition classes between the Palm swamp showed Zygnemaphyceae and Bacillariophyceae with higher richness of taxa, and together with Oedogoniophyceae and Chrysophyceae were related to impacted environments (Figure 6), both in urban and agricultural area.

Figure 6.
Similarity of the studied environments in relation of epiphytic algae classes summarized by DCA. a) Palm swamps, b) epiphytic algae classes (Bacillariophyceae (Baci), Chrysophyceae (Chry), Cyanophyceae (Cyan), Dinophyceae (Dino), Oedogoniophyceae (Oedo), Rodophyceae (Rodo), Xantophyceae (Xant), Zygnemaphyceae (Zygn).

The ordination of the environments in terms of density of diatoms (NMDS) showed that conserved Palm swamps were more distant from others concerning this distribution, while the impacted Palm swamps had higher similarity according the density of diatoms (Figure 7). The stress value for this analysis for the first three axes was 14.8. Thus, there was differences in the distribution of diatoms in environments under different impacts. In general, preserved Palm swamps were related only to the genera Eunotia, Gyrosigma, Navicula and Pinnularia. In impacted Palm swamps, in addition to thementioned above, Encyonema, Fragilaria, Frustulia, Gomphonema, Nitzschia, Stenopterobia, Surirella and Ulnaria were recorded.

Figure 7.
Distances of studied environments according densities of diatoms by non-metric multidimensional scaling (NMDS).

The indicator species analysis revealed that the taxa Gomphonema lagenula Kützing (IV- 37.5; p < 0.05) and Oedogonium sp.4 (IV- 42.2; p < 0.05) had relative abundance and relative frequency statistically associated with Palm swamps impacted by agriculture, defining them as asymmetric indicator species. Gomphonema lagenula presented low indicator values, however presented high specificity (relative abundance of 100%) for this group of Palm swamps, and fidelity (relative frequency) of 38%. Oedogonium sp.4 also showed low indicator values, but with high specificity (84%) and fidelity of 50% for these environments.

The results of One-Way ANOVA showed evidence of differences in the attributes of the epiphytic algal community among the studied Palm swamps to richness (F = 5,19; p = 0,01), with Palm swamps in urban areas different from others; for biomass (F = 5,19; p = 0,01) with Palm swamps in urban area different from others (Tukey, p = 0,01); for biovolume (F = 3,85; p = 0,03) with Palm swamps in agriculture area different from others (Tukey p = 0,04), but for densities the environments did not differ significantly (F = 3,36; p = 0,05). The log-transformed data reached the assumptions of normality and homoscedasticity for the analysis. Thus, the results support the hypothesis of the study for the parameters richness, biomass and biovolume of epiphytic algae communities.

4. Discussion

The soils of the Palm swamps are hapludult type, rich in clay, iron oxide, silica and aluminum, and present a reddish color (Embrapa, 1999Embrapa, 1999. Sistema brasileiro de classificação de solos. Brasília: Embrapa. 412 p., Lima et al., 2008LIMA, JGC., SCHULZE, SMBB., RIBEIRO, MR. and BARRETO, SB., 2008. Mineralogia de um argissolo vermelho-amarelo da zona úmida costeira do estado de Pernambuco. Revista Brasileira de Ciências do Solo, vol. 32, p. 881-892. http://dx.doi.org/10.1590/S0100-06832008000200042
http://dx.doi.org/10.1590/S0100-06832008...
). Such features may explain the low values of pH and the high values of silica recorded in the present study.

High loads of nutrients in aquatic environments, mainly nitrogen and total phosphorus, may be associated to inappropriate farming practices, urban discharges or effluents from waste treatment plants (EPA, 2006Environmental Protection Agency – EPA, 2006. The Wadeable Streams Assessment: A Collaborative Survey of the Nation's Streams. Available from: <http://www.epa.gov/owow/streamsurvey>. Access in: 22 Oct. 2010.
http://www.epa.gov/owow/streamsurvey...
). These environments with low levels of human interference may present concentrations of total phosphorus around 10 µg L−1 (Stevenson et al., 2008STEVENSON, RJ., WILEY, MJ., GAGE, SH., LOUGHEED, VL., RISENG, CM., BONNELL, P., BURTON, TM., HOUGH, RA., HYNDMAN, DW., KOCHES, JK., LONG, DT., PIJANOWSKI, BC., QI, J., STEINMAN, AD. and UZARSKI, DG., 2008. Watershed Science: Essential, Complex, Multidisciplinary and Collaborative. In JI, W. (Ed.). Wetland and Water Resource Modeling and Assessment: A Watershed Perspective. CRC Press.; Roberts and Bilby, 2009ROBERTS, ML. and BILBY, RE., 2009. Urbanization alters litterfall rates and nutrient inputs to small Puget Lowland streams. Journal of the North American Benthological Society, vol. 28, p. 941-954. http://dx.doi.org/10.1899/07-160.1
http://dx.doi.org/10.1899/07-160.1...
). These characteristics were observed in this study, in which low concentrations of these nutrients were observed in conserved Palm swamps, as opposed to those found in impacted Palm swamps in urban and agricultural areas.

On the other hand, for total nitrogen concentrations, only five palm swamps were classified as oligotrophic environments, confirming the impact caused by human activity in increasing concentrations of nutrients. Moreover, only one conserved palm swamps was assorted as oligotrophic for this nutrient. These results indicate that possibly even in environments with riparian vegetation above 50 m, surrounded with activities the monocultures and large pasture areas lead to changes in nutrient concentration (Ribeiro Filho et al., 2011RIBEIRO FILHO, RA., PETRERE JUNIOR, M., BENASSI, SF. and PEREIRA, JMA., 2011. Itaipu Reservoir limnology: eutrophication degree and the horizontal distribution of its limnological variables. Brazilian Journal of Biology, vol 71, p. 889-902.).

Chemical changes in the water along with urbanization process influence the establishment of periphytic algal communities (Baker et al., 2009BAKER, MA., GUZMAN, G. and OSTERMILLER, JD., 2009. Differences in nitrate uptake among benthic algal assemblages in a mountain stream. Journal of the North American Benthological Society, vol. 28, p. 24-33. http://dx.doi.org/10.1899/07-129.1
http://dx.doi.org/10.1899/07-129.1...
; Wu et al., 2009WU, N., TANG, T., ZHOU, S., JIA. X, LI, D., LIU, R. and CAI, Q., 2009. Changes in benthic communities following construction of run-of-river dam. Journal of the North American Benthological Society, vol. 28, p. 69-79. http://dx.doi.org/10.1899/08-047.1
http://dx.doi.org/10.1899/08-047.1...
). This study observed differences in the distribution and structure of epiphytic algae among the studied Palm swamps under different impacts. Urban impacted Palms swamps presented higher richness and biomass of epiphytic algae and Palm swamps in agriculture areas presented a higher biovolume. These results may be assigned to several factors, such as changes in nutrient input and light availability, which may have a strong impact on algal communities (Miller et al., 1992MILLER, MC., DEOLIVEIRA, P. and GIBEAU, GG., 1992. Epilithic diatom community response to years of PO4 fertilization – Kuparuk River, Alaska (68 N Lat.). Hydrobiologia, vol. 240, p. 103-119. http://dx.doi.org/10.1007/BF00013456
http://dx.doi.org/10.1007/BF00013456...
).

Direct rates of sunlight in the water body (Tuji, 2000TUJI, A., 2000. The effect of irradiance on the growth of different forms of freshwater diatoms: implications for sucession in attached diatom communities. Journal of Phycology, vol. 36, p. 659-661. http://dx.doi.org/10.1046/j.1529-8817.2000.99212.x
http://dx.doi.org/10.1046/j.1529-8817.20...
) and greater nutrient loading via allochthonous in water body both caused by the low proportion of riparian forest may favor the high algal development (Bourassa and Cattaneo, 2000BOURASSA, N. and CATTANEO, A. 2000. Responses of a lake outlet community to light and nutrient manipulation: effects on periphyton and invertebrate biomass and composition. Freshwater Biology, vol. 44, p. 629-639. http://dx.doi.org/10.1046/j.1365-2427.2000.00610.x
http://dx.doi.org/10.1046/j.1365-2427.20...
). This possibly explains the more significant epiphyton in the impacted Palm swamps with low riparian vegetation cover, which is located in areas under agricultural and urban impacts, with greater nutrient loading.

Among the epiphytic algae registered, the high taxa richness and biovolume of Zygnemaphyceae is mainly due to the relationship with acidic waters present in all studied Palm swamps. They are species colonizing substrates, at least for reproduction (Coesel, 1996COESEL, PFM., 1996. Biogeography of desmids. Hydrobiologia, vol. 336, p. 41-53 http://dx.doi.org/10.1007/BF00010818
http://dx.doi.org/10.1007/BF00010818...
), mainly found in acidic water, poor in nutrients, with low electric conductivity, and high transparence (Felisberto and Rodrigues, 2005FELISBERTO, SA. and RODRIGUES, L., 2005. Influência do gradiente longitudinal (rio-barragem) na similaridade das comunidades de desmídias perifíticas. Revista Brasileira de Botânica, vol. 28, p. 241-254.). In the meantime, in this study, a greater richness of this class was verified in impacted Palm swamps, with higher turbidity values.

Regarding the biovolume, Zygnemaphyceae was also significant, mainly by the high occurrence of filamentous organisms (Spirogyra (Link) Endlicher and Mougeotia Agardh). The filaments are excellent adaptive forms that grow rapidly in length and may remain with a constant area/volume ratio (Margalef, 1983MARGALEF, R., 1983. Limnologia. Barcelona: Ediciones Omega. 1009 p.), maintaining high biovolumes. The taxa of Spirogyra prefer freshwater with meso to eutrophic conditions (Margalef, 1983MARGALEF, R., 1983. Limnologia. Barcelona: Ediciones Omega. 1009 p.; Simons, 1994SIMONS, J., 1994. Field ecology of freshwater macroalgae in pools and ditches, with special attention to eutrophication. Netherlands Journal of Aquatic Ecology, vol. 28, p. 25-33. http://dx.doi.org/10.1007/BF02334242
http://dx.doi.org/10.1007/BF02334242...
) and environments with absence or low current velocity (Biggs et al., 1998BIGGS, JF., STEVENSON, RJ. and LOWE, RL., 1998. A habitat matrix conceptual model for stream periphyton. Archiv für Hydrobiologie, vol. 143, p. 21-56.), as registered, mainly under higher nutrient concentrations and in lentic waters. The taxa of Mougeotia are always registered in acidic waters in Europe and North America, but can have wide distribution in waters with high light incidence and under conditions eutrophic to oligotrophic (Graham et al., 1996GRAHAM, JÁ., ARANCIBIA-AVILA, P. and GRAHAN, LE., 1996. Physiological ecology of a species of the filamentous green alga Mougeotia under acidic conditions: Light and temperature effects on photosynthesis and respiration. Limnology and Oceanography, vol. 41, p. 253-262. http://dx.doi.org/10.4319/lo.1996.41.2.0253
http://dx.doi.org/10.4319/lo.1996.41.2.0...
).

High silica concentrations are relevant aspects for the expressivity of Bacillariophyceae in density and composition, and are an essential nutrient for the formation of frustules. Morphological and physiological characteristics may also influence the development of this group in the epiphyton, as they have the ability to secrete mucilage to form stalks or mucilaginous matrices, allowing the attachment to substrates (Round, 1991ROUND, FE., 1991. Use of Diatoms for Monitoring Rivers. In WHITTON, BA., ROTT, E. and FRIEDRICH, G. (Eds.). Use of algae for monitoring rivers. Instritute für Botanik: Universität Innsbruck. p. 25-32.). The high richness of the genus Eunotia Ehrenberg is probably due to the fact that they are acid-tolerant organisms (Planas, 1996PLANAS, D., 1996. Acidification effects. In STEVENSON, R.J., BOTHWELL, M.L. and LOWE, R.L. (Eds.). Algal ecology: freshwater bentic ecosystems. New York: Academic Press. p. 497-522. http://dx.doi.org/10.1016/B978-012668450-6/50045-X
http://dx.doi.org/10.1016/B978-012668450...
; De Nicola, 2000DE NICOLA, DM., 2000. A review of diatoms found in highly acidic environments. Hydrobiologia, vol. 433, p. 111-112. http://dx.doi.org/10.1023/A:1004066620172
http://dx.doi.org/10.1023/A:100406662017...
; Wunsam et al., 2002WUNSAM, S., CATTANEO, A. and BOURASSA, N., 2002. Comparing diatom species, genera and size in biomonitoring: a case study from streams in the Laurentians (Quebec, Canada). Freshwater Biology, vol. 47, p. 325-340. http://dx.doi.org/10.1046/j.1365-2427.2002.00809.x
http://dx.doi.org/10.1046/j.1365-2427.20...
; Andrén and Jarlman, 2008ANDRÉN, C. and JARLMAN, A., 2008. Benthic diatoms as indicators of acidity in streams. Fundamental and Applied Limnology. Archiv für Hydrobiologie, vol. 173, p. 237-253. http://dx.doi.org/10.1127/1863-9135/2008/0173-0237
http://dx.doi.org/10.1127/1863-9135/2008...
), which can develop in environments with acidic waters, such as the Palm swamps.

In this study, two asymmetric indicator species were revealed for Palm swamps impacted by agriculture due to the high specificity (relative abundance) to these environments (Gomphonema lagenula Kützing – Bacillariophyceae and Oedogonium sp.4 – Oedogoniophyceae). Asymmetric indicator species are those, whose presence (frequency) was not detected in all environments of the group in which there were indicators. Nevertheless, they contributed to the habitat specificity of this group, with significant relative abundance in these environments (Dufrêne and Legendre, 1997DUFRÊNE, M. and LEGENDRE, P., 1997. Species assemblages and indicator species: the need of asymmetrical approach. Ecological Monographs, vol. 67, p. 345-366.).

Indicator species have a strong relationship with environmental characteristics (Kitching et al., 2000KITCHING, RL, ORR, AG., THALIB, L., MITCHELL, H., HOPKINS, MS. and GRAHAM, AW., 2000. Moth assemblages as indicators of environmental quality in remnants of upland Australian rain forest. Journal of Applied Ecology, vol. 37, p. 284-297. http://dx.doi.org/10.1046/j.1365-2664.2000.00490.x
http://dx.doi.org/10.1046/j.1365-2664.20...
), thus providing information about the complexity of the ecosystem where they occur, and may respond to ecological changes associated to human intervention (McGeoch, 1998McGEOCH, MA., 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews, vol. 73, p. 181-201. http://dx.doi.org/10.1017/S000632319700515X
http://dx.doi.org/10.1017/S0006323197005...
), making them important for conservation and management plans (Andersen, 1999ANDERSEN, AN., 1999. My bioindicator or yours? Making the selection. Journal of Insect Conservation, vol. 3, p. 61-64. http://dx.doi.org/10.1023/A:1017202329114
http://dx.doi.org/10.1023/A:101720232911...
). In this study, among the main environmental characteristics related to these indicator species, there are mesotrophic to eutropic environments to total nitrogen concentrations, high values of turbidity, conductivity, silica and acidic waters.

Gomphonema lagenula, as well as all species of Gomphonema, have the ability to release mucilage by apical pore field and form long mucilaginous stalks (Round, 1991ROUND, FE., 1991. Use of Diatoms for Monitoring Rivers. In WHITTON, BA., ROTT, E. and FRIEDRICH, G. (Eds.). Use of algae for monitoring rivers. Instritute für Botanik: Universität Innsbruck. p. 25-32.), presenting great advantages representative of other genera in environments where the competition for light is high (Tuji, 2000TUJI, A., 2000. The effect of irradiance on the growth of different forms of freshwater diatoms: implications for sucession in attached diatom communities. Journal of Phycology, vol. 36, p. 659-661. http://dx.doi.org/10.1046/j.1529-8817.2000.99212.x
http://dx.doi.org/10.1046/j.1529-8817.20...
), as in the case of environments with high turbidity. Studies point out that this species can be found in environments with high to moderate nutrient loads (Blanco et al., 2004BLANCO, S., ECTOR, L. and BÉCARES, E., 2004. Epiphytic diatoms as water quality indicators in Spanish shallow lakes. Vie Milieu, vol. 54, p. 71-79.; Leelahakriengkrai and Peerapornpisal, 2010LEELAHAKRIENGKRAI, P. and PEERAPORNPISAL, Y., 2010. Diversity of Benthic Diatoms and Water Quality of the Ping River, Northern Thailand. EnvironmentAsia, vol. 3, p. 82-94.), as reported by Reichardt (1999)REICHARDT, E., 1999. Zur Revision der Gattung Gomphonema. Frankfurt: Koeltz Scientific Books. Iconographic Diatomologica, no. 8., which states that this species is tolerant to high nutrient concentrations, proven in this study.

Oedogonium species can be found attached to several types of substrate (Lee, 2008LEE, RE., 2008. Phycology. 4th ed. Cambridge University Press. 547 p.), they are dominant in environments with a good availability of nutrients and there is a presence of currents with slow or inexistent velocity (Simons, 1994SIMONS, J., 1994. Field ecology of freshwater macroalgae in pools and ditches, with special attention to eutrophication. Netherlands Journal of Aquatic Ecology, vol. 28, p. 25-33. http://dx.doi.org/10.1007/BF02334242
http://dx.doi.org/10.1007/BF02334242...
; Biggs, 1996BIGGS, BJF., 1996. Patterns in benthic algal of streams. In STEVENSON, RJ., BOTHWELL, ML. and LOWE, RL. (Eds.). Algal ecology: freshwater benthic ecosystems. New York: Academic Press. p. 31-56.). 66.6% of the environments impacted by agriculture were lentic and mesotrophic to eutrophic for total nitrogen concentrations and high concentrations of silica.

5. Conclusion

The present study revealed the importance of the environmental characteristics and limnological variables concerning the distribution and structuration of epiphytic algal communities in Palm swamps of Goiás State, relating the higher values of richness, biomass and biovolume to impacted environments. These findings are mainly due to the high light rate in the water body, caused by the low proportion of riparian vegetation and to the availability of nutrients in these environments, unlike conserved Palm swamps. We observed the importance of pH mainly for composition of Zygnemaphyceae species and of silica for diatoms density.

We found that few conserved environments had oligotrophic characteristics for total nitrogen, probably because they were surrounded by large pasture areas, leading to changes in nutrient concentration. Still, here we identified Gomphonema lagenula and Oedogonium sp as bioindicators of impacted areas by agriculture, mostly mesotrophic to eutrophic conditions for total nitrogen.

Acknowledgements

The authors wish to express their gratitude to the Coordination for the Improvement of Higher Education Personnel (CAPES), for the scholarship granted to the first author and to the PostGraduate Program in Environmental Sciences from the Federal University of Goiás State (CIAMB-UFG), by funding part of the project (Process CAPES n° 23038.040928/2008-61). To Prof. Dr. Maria Gizelda de Oliveira Tavares and students from the Ecotoxicology laboratory of the Chemical Institute of UFG, and to Prof. Dr. Idelvone Mendes Ferreira (Campus Catalão– UFG) by valuable contributions, and to Msc. Huilquer Francisco Vogel for assistance in preparation of the study map.

References

  • AGOSTINHO, AA, THOMAZ, SM. and GOMES, LC., 2005. Conservation of the biodiversity of Brazil's Inland waters. Conservation Biology, vol. 19, p. 646-652. http://dx.doi.org/10.1111/j.1523-1739.2005.00701.x
    » http://dx.doi.org/10.1111/j.1523-1739.2005.00701.x
  • ALGARTE, VM., SIQUEIRA, NS., MURAMAKI, EA. and RODRIGUES, L., 2009. Effects of hydrological regime and connectivity on the interannual variation in taxonomic similarity of periphytic algae. Brazilian Journal of Biology, vol. 69, p. 609-616. PMid:19738967. http://dx.doi.org/10.1590/S1519-69842009000300015
    » http://dx.doi.org/10.1590/S1519-69842009000300015
  • ALLAN, JD., 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology and Systematics, vol. 35, p. 257-284. http://dx.doi.org/10.1146/annurev.ecolsys.35.120202.110122
    » http://dx.doi.org/10.1146/annurev.ecolsys.35.120202.110122
  • ANDERSEN, AN., 1999. My bioindicator or yours? Making the selection. Journal of Insect Conservation, vol. 3, p. 61-64. http://dx.doi.org/10.1023/A:1017202329114
    » http://dx.doi.org/10.1023/A:1017202329114
  • ANDRÉN, C. and JARLMAN, A., 2008. Benthic diatoms as indicators of acidity in streams. Fundamental and Applied Limnology. Archiv für Hydrobiologie, vol. 173, p. 237-253. http://dx.doi.org/10.1127/1863-9135/2008/0173-0237
    » http://dx.doi.org/10.1127/1863-9135/2008/0173-0237
  • America Public Health Association – APHA, 2005. Standard methods for examination of water and wasterwater. 21nd ed. Washington: APHA.
  • BAKER, MA., GUZMAN, G. and OSTERMILLER, JD., 2009. Differences in nitrate uptake among benthic algal assemblages in a mountain stream. Journal of the North American Benthological Society, vol. 28, p. 24-33. http://dx.doi.org/10.1899/07-129.1
    » http://dx.doi.org/10.1899/07-129.1
  • BICUDO, DC., 1990. Considerações sobre metodologias de contagem de algas do perifíton. Acta Limnologica Brasilica, vol. 3, p. 459-475.
  • BICUDO, CEM. and MENEZES, M., 2006. Gêneros de algas de águas continentais do Brasil (Chave de identificação e descrições). 2nd ed. São Carlos: Rima. 498 p.
  • BIGGS, BJF., 1996. Patterns in benthic algal of streams. In STEVENSON, RJ., BOTHWELL, ML. and LOWE, RL. (Eds.). Algal ecology: freshwater benthic ecosystems. New York: Academic Press. p. 31-56.
  • BIGGS, JF., STEVENSON, RJ. and LOWE, RL., 1998. A habitat matrix conceptual model for stream periphyton. Archiv für Hydrobiologie, vol. 143, p. 21-56.
  • BLANCO, S., ECTOR, L. and BÉCARES, E., 2004. Epiphytic diatoms as water quality indicators in Spanish shallow lakes. Vie Milieu, vol. 54, p. 71-79.
  • BONNET, BRP., FERREIRA, NC. and FERREIRA, LG., 2007. Ampliação de ambientes ripários como alternativa ás reservas legais: conciliando política florestal e conservação dos recursos hídricos no Bioma Cerrado. Boletim Goiano de Geografia, vol. 27, p. 97-115.
  • BOURASSA, N. and CATTANEO, A. 2000. Responses of a lake outlet community to light and nutrient manipulation: effects on periphyton and invertebrate biomass and composition. Freshwater Biology, vol. 44, p. 629-639. http://dx.doi.org/10.1046/j.1365-2427.2000.00610.x
    » http://dx.doi.org/10.1046/j.1365-2427.2000.00610.x
  • Brasil. Ministério do Meio Ambiente, 1992. Resoluções CONAMA de 1984 a 1991. 4. ed. Brasília: SEMAM/IBAMA. 245 p.
  • CAMPEAU, S., MURKIN, HR. and TITMAN, RD., 1994. Relative importance of algae and emergent plant litter to freshwater marsh invertebrates. Canadian Journal of Fisheries and Aquatic Sciences, vol. 51, p. 681-692. http://dx.doi.org/10.1139/f94-068
    » http://dx.doi.org/10.1139/f94-068
  • CARVALHO, PGS. 1991. As Veredas e sua importância no domínio dos Cerrados. Informe agropecuário, vol. 168, p. 47-54.
  • CATTANEO, A., KERIMIAN, T., ROBERGE, M. and MARTY, J., 1997. Periphyton distribution and abundance on substrata of different size along a gradient of stream trophy. Hydrobiologia, vol. 354, p. 101-110. http://dx.doi.org/10.1023/A:1003027927600
    » http://dx.doi.org/10.1023/A:1003027927600
  • COESEL, PFM., 1996. Biogeography of desmids. Hydrobiologia, vol. 336, p. 41-53 http://dx.doi.org/10.1007/BF00010818
    » http://dx.doi.org/10.1007/BF00010818
  • DE NICOLA, DM., 2000. A review of diatoms found in highly acidic environments. Hydrobiologia, vol. 433, p. 111-112. http://dx.doi.org/10.1023/A:1004066620172
    » http://dx.doi.org/10.1023/A:1004066620172
  • DODDS, WK., SMITH, VH. and ZANDER, B., 1997. Developing nutrient targets to control benthic chlorophyll levels in streams: a case study of the Clark Fork River. Water Research, vol. 31, p. 1738-1750. http://dx.doi.org/10.1016/S0043-1354(96)00389-2
    » http://dx.doi.org/10.1016/S0043-1354(96)00389-2
  • DUFRÊNE, M. and LEGENDRE, P., 1997. Species assemblages and indicator species: the need of asymmetrical approach. Ecological Monographs, vol. 67, p. 345-366.
  • ELSER, JJ., BRACKEN, MES., CLELAND, EE., GRUNER, DS., HARPOLE, WS., HILLEBRAND, H., NGAI, JT., SEABLOOM, EW., SHURIN, JB. and SMITH, JE., 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters, vol. 10, p.1135-1142. PMid:17922835. http://dx.doi.org/10.1111/j.1461-0248.2007.01113.x
    » http://dx.doi.org/10.1111/j.1461-0248.2007.01113.x
  • Embrapa, 1999. Sistema brasileiro de classificação de solos. Brasília: Embrapa. 412 p.
  • Environmental Protection Agency – EPA, 2006. The Wadeable Streams Assessment: A Collaborative Survey of the Nation's Streams. Available from: <http://www.epa.gov/owow/streamsurvey>. Access in: 22 Oct. 2010.
    » http://www.epa.gov/owow/streamsurvey
  • FELISBERTO, SA. and RODRIGUES, L., 2005. Influência do gradiente longitudinal (rio-barragem) na similaridade das comunidades de desmídias perifíticas. Revista Brasileira de Botânica, vol. 28, p. 241-254.
  • FERRAGUT, C. and BICUDO, DC., 2010. Periphytic algal community adaptive strategies in N and P enriched experiments in a tropical oligotrophic reservoir. Hydrobiologia, vol. 646, p. 295-309. http://dx.doi.org/10.1007/s10750-010-0168-0
    » http://dx.doi.org/10.1007/s10750-010-0168-0
  • FERREIRA, IM., 2006. Modelos geomorfológicos das Veredas em ambiente de Cerrado. Espaço revista Geografia, vol. 7-8, p. 7-11.
  • GOLTERMAN, HL., CLYMO, RS. and OHMSTAD, MAM., 1978. Methods for physical and chemical analysis of fresh waters. Oxford: Blackwell Scientific. 214 p.
  • GRAHAM, JÁ., ARANCIBIA-AVILA, P. and GRAHAN, LE., 1996. Physiological ecology of a species of the filamentous green alga Mougeotia under acidic conditions: Light and temperature effects on photosynthesis and respiration. Limnology and Oceanography, vol. 41, p. 253-262. http://dx.doi.org/10.4319/lo.1996.41.2.0253
    » http://dx.doi.org/10.4319/lo.1996.41.2.0253
  • HILL, MO. and GAUCH, HG., 1980. Detrend correspondence analysis, an improved ordination technique. Vegetatio, vol. 42, p. 47-58. http://dx.doi.org/10.1007/BF00048870
    » http://dx.doi.org/10.1007/BF00048870
  • HILL, WR., 1996. Effects of light. In STEVENSON, RJ., BOTHWELL, ML. and LOWE, RL. (Eds.). Algal ecology: freshwater bentic ecosystems. New York: Academic Press. p. 121-148.
  • HILLEBRAND, H., DÜRSELEN, C., KIRSCHTEL, D., POLLINGHER, U. and ZOHARY, T., 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, vol. 35, p. 403-424. http://dx.doi.org/10.1046/j.1529-8817.1999.3520403.x
    » http://dx.doi.org/10.1046/j.1529-8817.1999.3520403.x
  • KITCHING, RL, ORR, AG., THALIB, L., MITCHELL, H., HOPKINS, MS. and GRAHAM, AW., 2000. Moth assemblages as indicators of environmental quality in remnants of upland Australian rain forest. Journal of Applied Ecology, vol. 37, p. 284-297. http://dx.doi.org/10.1046/j.1365-2664.2000.00490.x
    » http://dx.doi.org/10.1046/j.1365-2664.2000.00490.x
  • KRUSKAL, JB. and WISH, M., 1978. Multidimensional scaling: Sage university paper series on quantitative applications in the social Sciences. Beverly Hills: Sage publications. 111 p.
  • LAMPARELLI, MC., 2004. Grau de trofia em corpos d'água do estado de São Paulo: avaliação dos métodos de monitoramento. São Paulo: Universidade de São Paulo. 238 p. Tese de Doutorado em Ecologia Aplicada.
  • LARSON, CA., PASSY, SI. and LAANBROEK, R., 2012. Taxonomic and functional composition of the algal benthos exhibits similar successional trends in response to nutrient supply and current velocity. Federation of European Microbiological, vol. 80, no. 2, p. 352-62.
  • LEE, RE., 2008. Phycology. 4th ed. Cambridge University Press. 547 p.
  • LEELAHAKRIENGKRAI, P. and PEERAPORNPISAL, Y., 2010. Diversity of Benthic Diatoms and Water Quality of the Ping River, Northern Thailand. EnvironmentAsia, vol. 3, p. 82-94.
  • LEGENDRE, P. and LEGENDRE, L., 1998. Numerical ecology. 2nd ed. Elsevier Science. 853 p.
  • LIMA, JGC., SCHULZE, SMBB., RIBEIRO, MR. and BARRETO, SB., 2008. Mineralogia de um argissolo vermelho-amarelo da zona úmida costeira do estado de Pernambuco. Revista Brasileira de Ciências do Solo, vol. 32, p. 881-892. http://dx.doi.org/10.1590/S0100-06832008000200042
    » http://dx.doi.org/10.1590/S0100-06832008000200042
  • LOBO, EA. and LEIGHTON, G., 1986. Estruturas de las fitocenosis planctônicas de los sistemas de desembocaduras de rios y esteros de La zona central de Chile. Revista de Biologia Marina, vol. 22, p. 143-170.
  • MARCARELLI, AM. and WURTSBAUGH, WA., 2006. Temperature and nutrients interact to control nitrogen fixation in oligotrophic streams: an experimental examination. Limnology and Oceanography, vol. 51, p. 2278-2289. http://dx.doi.org/10.4319/lo.2006.51.5.2278
    » http://dx.doi.org/10.4319/lo.2006.51.5.2278
  • MARCARELLI, AM., BECHTOLD, HA., RUGENSKI, AT. and INOUY, RS., 2009. Nutrient limitation of biofilm biomass and metabolism in the Upper Snake River basin, southeast Idaho, USA. Hydrobiologia, vol. 620, p. 63-7. http://dx.doi.org/10.1007/s10750-008-9615-6
    » http://dx.doi.org/10.1007/s10750-008-9615-6
  • MARGALEF, R., 1983. Limnologia. Barcelona: Ediciones Omega. 1009 p.
  • McCUNE, B. and MEFFORD, MJ., 1999. PC-ORD. Multivariate Analysis of Ecological Data. version 4. Oregon: MJM Software Design.
  • McGEOCH, MA., 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews, vol. 73, p. 181-201. http://dx.doi.org/10.1017/S000632319700515X
    » http://dx.doi.org/10.1017/S000632319700515X
  • MENEZES, M., 1986. Ficoflórula da Chapada dos Guimarães e arredores, Mato Grosso, Brasil: Euglenaceae e pigmentadas (Euglenophyceae). Rickia, vol. 13, p. 87-95.
  • MILLER, MC., DEOLIVEIRA, P. and GIBEAU, GG., 1992. Epilithic diatom community response to years of PO4 fertilization – Kuparuk River, Alaska (68 N Lat.). Hydrobiologia, vol. 240, p. 103-119. http://dx.doi.org/10.1007/BF00013456
    » http://dx.doi.org/10.1007/BF00013456
  • MOREIRA-FILHO, H. and VALENTE-MOREIRA, IM., 1981. Avaliação taxonômica e ecológica das diatomáceas (Bacillariophyceae) epífitas em algas pluricelulares obtidas nos litorais dos estados dos estados do Paraná, Santa Catarina e São Paulo. Boletim Museu Botânico Municipal, vol. 47, p. 1-17.
  • MOSCHINI-CARLOS, V., HENRY, R. and POMPÊO, MLM., 2000. Seasonal variation of biomass and productivity of the periphytic community on artificial substrata in the Jurumirim Reservoir (São Paulo, Brazil). Hydrobiologia, vol. 434, p. 35-40. http://dx.doi.org/10.1023/A:1004086623922
    » http://dx.doi.org/10.1023/A:1004086623922
  • PLANAS, D., 1996. Acidification effects. In STEVENSON, R.J., BOTHWELL, M.L. and LOWE, R.L. (Eds.). Algal ecology: freshwater bentic ecosystems. New York: Academic Press. p. 497-522. http://dx.doi.org/10.1016/B978-012668450-6/50045-X
    » http://dx.doi.org/10.1016/B978-012668450-6/50045-X
  • REICHARDT, E., 1999. Zur Revision der Gattung Gomphonema. Frankfurt: Koeltz Scientific Books. Iconographic Diatomologica, no. 8.
  • RIBEIRO, JF. and WALTER, BMT., 1998. Fitofisionomias do bioma Cerrado. In SANO, SM. and ALMEIDA, SP. (Eds.). Cerrado: ambiente e flora. Planaltina: Embrapa-CPAC. p. 89-166.
  • RIBEIRO FILHO, RA., PETRERE JUNIOR, M., BENASSI, SF. and PEREIRA, JMA., 2011. Itaipu Reservoir limnology: eutrophication degree and the horizontal distribution of its limnological variables. Brazilian Journal of Biology, vol 71, p. 889-902.
  • ROBERTS, ML. and BILBY, RE., 2009. Urbanization alters litterfall rates and nutrient inputs to small Puget Lowland streams. Journal of the North American Benthological Society, vol. 28, p. 941-954. http://dx.doi.org/10.1899/07-160.1
    » http://dx.doi.org/10.1899/07-160.1
  • RODRIGUES, L., LEANDRINE, JA., JATI, S., FONSECA, IA. and SILVA, ELV., 2004. Structure of communities of Periphytic Algae in the Upper Paraná River Floodplain. In AGOSTINHO, AA., RODRIGUES, L., GOMES, LC., THOMAZ, SM. and MIRANDA, LE. (Eds.). Structure and funcioning of the Paraná river and its floodplain. Maringá: Ed. Eduem. p. 43-50.
  • ROS, J., 1979. Práticas de Ecologia. Barcelona: Ed. Omega. 181 p.
  • ROSEMOND, AD., MULHOLLAND, PJ. and ELWOOD, JW., 1993. Top-Down and bottom-up control of stream periphyton: effects of nutrients and herbivores. Ecology, vol. 74, p. 1264-1280. http://dx.doi.org/10.2307/1940495
    » http://dx.doi.org/10.2307/1940495
  • ROUND, FE., 1991. Use of Diatoms for Monitoring Rivers. In WHITTON, BA., ROTT, E. and FRIEDRICH, G. (Eds.). Use of algae for monitoring rivers. Instritute für Botanik: Universität Innsbruck. p. 25-32.
  • -, 1971. The taxonomy of the Chlorophyta, 2. British Phycological Journal, vol. 6, p. 235-264. http://dx.doi.org/10.1080/00071617100650261
    » http://dx.doi.org/10.1080/00071617100650261
  • SIMONS, J., 1994. Field ecology of freshwater macroalgae in pools and ditches, with special attention to eutrophication. Netherlands Journal of Aquatic Ecology, vol. 28, p. 25-33. http://dx.doi.org/10.1007/BF02334242
    » http://dx.doi.org/10.1007/BF02334242
  • SIMONSEN, R., 1974. The diatom plankton of the indian ocean expedition of R/V “Meteor”. Meteor Forschungsergebnisse Reihe D-Biologie, vol. 19, p. 1-66.
  • Statsoft Inc., 2005. Statistica (data analysis software system). version 7.1. Available from: www.statsoft.com
    » www.statsoft.com
  • STEVENSON, RJ., WILEY, MJ., GAGE, SH., LOUGHEED, VL., RISENG, CM., BONNELL, P., BURTON, TM., HOUGH, RA., HYNDMAN, DW., KOCHES, JK., LONG, DT., PIJANOWSKI, BC., QI, J., STEINMAN, AD. and UZARSKI, DG., 2008. Watershed Science: Essential, Complex, Multidisciplinary and Collaborative. In JI, W. (Ed.). Wetland and Water Resource Modeling and Assessment: A Watershed Perspective. CRC Press.
  • TUJI, A., 2000. The effect of irradiance on the growth of different forms of freshwater diatoms: implications for sucession in attached diatom communities. Journal of Phycology, vol. 36, p. 659-661. http://dx.doi.org/10.1046/j.1529-8817.2000.99212.x
    » http://dx.doi.org/10.1046/j.1529-8817.2000.99212.x
  • TUNDISI, JG., MATSUMURA-TUNDISI, T., ARANTES JUNIOR, JD., TUNDISI, JEM., MANZINI, NF. and DUCROT, R., 2004. The response of Carlos Botelho (Lobo, Broa) reservoir to the passage of cold fronts as reflected by physical, chemical and biological variables. Brazilian Journal of Biology, vol. 64, p. 177-186. PMid:15195377. http://dx.doi.org/10.1590/S1519-69842004000100020
    » http://dx.doi.org/10.1590/S1519-69842004000100020
  • UTERMÖHL H. 1958. Zur Vervollkommung der quantitativen phytoplancton-methodik. Mitteilungen Internationale Vereinigung für Theoretische und Angewandte Limnologie, vol. 9, p. 1-38.
  • WETZEL, RG. and LIKENS, GE., 1991. Limnological analysis. 2nd ed. New York: Springer-Verlag.
  • WU, N., TANG, T., ZHOU, S., JIA. X, LI, D., LIU, R. and CAI, Q., 2009. Changes in benthic communities following construction of run-of-river dam. Journal of the North American Benthological Society, vol. 28, p. 69-79. http://dx.doi.org/10.1899/08-047.1
    » http://dx.doi.org/10.1899/08-047.1
  • WUNSAM, S., CATTANEO, A. and BOURASSA, N., 2002. Comparing diatom species, genera and size in biomonitoring: a case study from streams in the Laurentians (Quebec, Canada). Freshwater Biology, vol. 47, p. 325-340. http://dx.doi.org/10.1046/j.1365-2427.2002.00809.x
    » http://dx.doi.org/10.1046/j.1365-2427.2002.00809.x
  • ZHENG, L. and STEVENSON, RJ., 2006. Algal assemblages in multiple habitats of restored and extant wetlands. Hydrobiologia, vol. 561, p. 221-238. http://dx.doi.org/10.1007/s10750-005-1616-0
    » http://dx.doi.org/10.1007/s10750-005-1616-0

Publication Dates

  • Publication in this collection
    May 2013

History

  • Received
    5 Dec 2011
  • Accepted
    12 Apr 2012
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br