Printer Friendly

Periphytic diatoms as bioindicators in a tropical stream: from urban to rural environments/Diatomaceas perifiticas como bioindicadores em um corrego tropical: do ambiente urbano para o rural.


Lotic environments are among the systems that suffer most the impact of human activities (BONA et al., 2008). According to Vannote et al. (1980) and Mulholland (1996), sections of headwater streams represent greater interaction with the landscape and therefore are predominantly accumulators, processors and transporters of material from the terrestrial environment.

With the intense population growth, the urbanization process is accelerated (MEYER et al., 2005) as well as the agricultural practices. This raises concerns about the physical and chemical characteristics of rivers and streams (ALLAN; CASTILLO, 2007), negatively affecting the biota of these ecosystems (JUTTNER et al. 2003).The current rate of destruction, alteration and fragmentation of natural habitats resulting from increasing impacts of human activities has led to an alarming loss of global biodiversity. Owing to this, an important objective of ecological studies is to understand spatial and seasonal changes in size and distribution of populations, as well as the mechanisms and processes behind these changes.

Benthic algae show high turnover rates and opportunistic life-history strategies that have enabled them to successfully exploit stream habitats; many are harsh and polluted environments (BIGGS, 1996). In many countries, the monitoring of aquatic environments using biological communities is applied routinely (GROWNS, 1999; FORE; GRAFE, 2002), in which mainly the diatoms are being used in monitoring of rivers (KELLY et al., 1998; JUTTNER et al., 2003; DELA-CRUZ et al., 2006). Their utilization as indicators is advantageous, since the diatoms have peculiar attributes, as for instance: they are found throughout the river, have a short life cycle, responding quickly to environmental changes, are commonly related to specific environmental conditions in different geographic regions (GROWNS, 1999; STEVENSON; PAN, 1999; LOBO et al., 2002; SOININEN, 2002), presenting responses in spatial and seasonal scales, according to the climate, land use, and water chemistry (STEVENSON; PAN, 1999).

Although several indices had been developed to evaluate the water quality by means of diatoms (DESCY; COSTE, 1991; VAN DAM et al., 1994; KELLY; WHITTON, 1995; STEVENSON; PAN, 1999), few studies have been done to evaluate the responses from diatoms over drainage basins influenced by urbanization and by agricultural practices (LOBO et al., 1996; GOMEZ; LICURSI, 2001; JUTTNER et al., 2003; MORESCO; RODRIGUES, 2014), especially in tropical regions.

Therefore, this study evaluated the spatial and seasonal variations in the composition and structure of the periphytic diatom assemblage, according to the urban-rural gradient, relating them to physical and chemical variables, and selected diatom species as bioindicators of urban and rural stretches, in the Guaiapo Stream, Pirapo River basin. Thus, it is expected that the different environmental characteristics found along the stream have influence on the composition and structure of the periphytic diatom assemblage over a seasonal period.

Material and methods

Study area

The Pirapo River basin is in the Northwestern region of Parana State, in the physiographic region called Third Plateau (latitudes 22[degrees]30' and 23[degrees]30' South, and longitudes 51[degrees]15' and 52[degrees]15' West), with a drainage area of approximately 5,076 [km.sup.2]. The predominant climate in the region is subtropical, with abundant rainfall in summer (months: October, November, December, January, February and March), and dry winter (April, May, June, July, August and September) (MAACK, 2012), with annual mean temperatures higher than 20[degrees]C. The municipality of Maringa is within the boundaries of the basins of Pirapo and Ivai rivers, with sources of several streams in the urban area, including the Guaiapo Stream, of low order, located in the Pirapo River basin (Figure 1).

The source of this stream is within the urban area, with residential and industrial occupation. This stretch presents steep banks and riparian vegetation, with low incidence of light (Figure 1). The headwaters receive storm sewers, domestic sewer and superficial runoff. The middle stretch is located on the border between the urban and rural areas, presenting steep banks and scarce riparian vegetation, with high incidence of light. In turn, the mouth is situated in the rural area with crop rotation (corn, soybean and wheat), without arboreal riparian vegetation, and with intense incidence of light. The middle and mouth stretches are subjected to the discharge of agricultural and domestic effluents.

Abiotic variables

Samplings for determination of abiotic variables were conducted simultaneously to the samplings of biotic variables. Data relative to physical and chemical water conditions, like pH (Digimed DM2), electrical conductivity (Digimed DM3, [micro]S [cm.sup.-1]), dissolved oxygen ([O.sub.2]) and water temperature (YSI 55 12 F[T.sup.-1], mL [L.sup.-1] and [degrees]C, respectively), flow velocity (Flo-Mate 2000--Marsh McBirdey, m [s.sup.-1]) were measured in the field with portable analytical equipments. For the analysis of concentrations of total nitrogen (TN), orthophosphate (P[O.sub.4]), and biochemical oxygen demand ([BOD.sub.5]), water samples were collected and analyzed by the laboratories of Sanitation and Agrochemistry of the State University of Maringa, following the methodology used by CETESB (Technology and Environmental Sanitation Company of Sao Paulo), L5.120 biochemical oxygen demand, dilution and incubation method (20[degrees]C, 5 days) (CETESB, 1991). Total nitrogen and orthophosphate were determined according to Silva and Oliveira (2001).

Three sampling sites were established along the longitudinal gradient of the Guaiapo Stream (headwaters, middle and mouth). For analytical purposes, the sampling sites were grouped into urban (headwater) and rural (middle and mouth) sites. The samplings were performed every two months, from August 2007 to June 2008, which were grouped into dry (April, June, August) and rainy season (October, December, February).

For the qualitative and quantitative analyses of periphytic diatoms, at each sampling site, the samples were taken in replica. Each sample consisted of three pebbles (composite sample). This substrate was chosen for being the most abundant and present throughout the stream.

The side opposite to the flow direction was scraped with the aid of brush and blade, and the material was fixed with formalin solution. We also measured the area of the scraped surface, using a caliper. The material was oxidized with potassium permanganate and hydrochloric acid (MOREIRA-FILHO; VALENTE-MOREIRA, 1981). Permanent mounts were made using Hyrax resin. The slides were deposited in the Herbarium of the State University of Maringa (HUEM 16544-16561).

Identification and counting of diatom species were performed in an optical microscope Olympus CX31. The individuals were identified and counted to a minimum of 600 valves were recorded, as recommended by Kobayasi and Mayama (1982), added up to an efficiency of counting of 90%, determined according to Pappas and Stormer (1996). The concentration of cells [cm.sup.-2] was estimated by multiplying the number of valves of each taxon by the conversion factor, according to Hermany et al. (2006). The classification system followed that proposed by Round et al. (1990).

Data analysis

To determine significant differences from the expected proportion in the density of diatoms in each sampling sites and periods, the chi-square test ([chi square]) at a significance level of 5% was applied. In order to summarize the composition and structure of the periphytic algae assemblage, it was applied a Nonmetric Multidimensional Scaling (NMDS) (KRUSKAL, 1964a, b). Sorensen distances were calculated and the general procedure of the NMDS was followed according to McCune and Grace (2002). A hundred permutations were performed and the stability criterion used was the standard deviation ([less than or equal to] 0.005, stress above 100 iterations). This analysis was carried out with the matrix of abundance data (square root transformed to remove the effect of high values) in different sampling sites and periods grouped.

To test significant differences in the composition and structure of the periphytic algae assemblage, summarized by the NMDS, a two-way mixed model PERMANOVA (maximum permutations = 9999) was used to test each data set, with sampling site (urban and rural) and period (dry and rainy season) provided as factors. For this analysis, data were log transformed.

For the determination of indicator species (IndVal), the procedures used was those recommended by Dufrene and Legendre (1997), the input data were the abundance and frequency of occurrence of species in each group, calculating indicator values for each species (McCUNE; GRACE, 2002). The species were considered as indicators when presented the results of Monte Carlo Test with p < 0.05 (based on 1,000 permutations).

Abiotic variables were summarized by a Principal Component Analysis (PCA). To determine which principal components should be retained for interpretation, the Broken-Stick criterion was used. According to this, only the axes with eigenvalues higher than those generated by random should be interpreted (McCUNE; GRACE, 2002). Abiotic data, except pH, were log transformed for PCA.

The association of multivariate analysis (abiotic variables and composition and structure of the periphytic diatom assemblage) was examined by means of the Procrustes analysis (PERES-NETO; JACKSON, 2001). In this analysis, the two matrices are compared using an algorithm that minimizes the sum of squared residuals between the matrices (ROHLF; SLICE, 1990). The resulting value of [m.sup.2] is the best fit, as it describes the degree of association between the matrices.

NMDS, PERMANOVA, IndVal and PCA were run using the software PC-Ord[R] 5.0 (McCUNE; MEFFORD, 2006). The Procrustes statistics was calculated by means of the software PROTEST[R] (JACKSON, 1995). The level of statistical significance adopted was p < 0.05.


Abiotic analysis

Principal components analysis summarized the matrix of abiotic variables. Two axes were retained for interpretation (Figure 2; cumulative explained variance = 55.06; Table 1). The axis 1 (%variance: 33.84%) only distinguished the sampling sites. Flow velocity and pH, positively correlated with the axis 1 (Table 1; Figure 2), showed higher values in rural sites. On the other hand, orthophosphate (P[O.sub.4]), negatively correlated with the axis 1 (Table 1; Figure 2), showed higher values in urban sites. These variables were responsible for the separation of the sampling sites. In the axis 2 (%variance: 21.22%), there was the differentiation of the sampling sites. Electric conductivity, positively correlated with axis 2 (Table 1; Figure 2), showed higher values in rural sites. In turn, total nitrogen, negatively correlated with the axis 2 (Table 1; Figure 2), showed higher values in urban sites.

Periphytic diatom assemblage

In this study, we identified 96 species belonging to 35 genera. Seventy-one specific taxa occurred in the headwaters, 72 in the middle stretch, and 53 in the mouth. Forty-three species were common to the three stretches. Considering the species exclusive to each stretch, we recorded 19, 16 and 4, for the headwaters, middle and mouth stretches, respectively.

Analyzing the distribution of genera, Navicula had the highest number of taxa, followed by Nitzschia and Pinnularia. The genera Diadesmis, Diploneis and Neidium occurred only in the urban area. The genera Adlafia, Caloneis and Kobayasiella occurred only in the rural region.

Considering the total density, higher mean values were observed in rural stretches (Chi-square test [chi square] = 59.64, p < 0.05, Figure 3a), in the dry period (Chi-square test [chi square] = 4.88, p < 0.05, Figure 3b).

The structure of the periphytic diatom assemblage, summarized by a NMDS, showed a separation only between sites studied (Figure 4a). After 47 iterations, the stability criterion was achieved with a final stress of 9.19 (Monte Carlo test, p < 0.01), and two axes were retained for interpretation. The variance represented by each axis, based on the distance between the [r.sup.2] on the ordination space and distances in the original space was 0.32 for the axis 1; and 0.60 for the axis 2, adding up a total of 0.92.

By plotting the axis 1 and 2 (Figure 4a), the spatial scale was identified as the main pattern for the structure of the periphytic diatom assemblage. The urban sites were set apart from the rural sites.

Regarding time, no pattern was found for composition and structure (Figure 4b). PERMANOVA detected significant differences between sites for the composition and structure of the periphytic diatom assemblage (p < 0.05; Table 2).

The result of the Indicator Species Analysis (IndVal) evidenced 23 species of periphytic diatoms, whose abundances and frequencies were significantly associated with some of the studied regions (p < 0.05; Table 3). Eleven species were indicators of urban areas and 12 of rural areas (Table 3).

Relationship between biotic and abiotic variables

A Procrustes test (matrices correlation) was run to investigate the relationship between abiotic variables and the assemblage of periphytic diatoms. In this test, the two first PCA axes were compared with the two first ordination axes of the NMDS, which summarized the structure of the periphytic diatom assemblage.

The value adjusted for the sampling sites and periods distribution was [m.sup.2] = 0.52 and p < 0.01, corroborating the influence of abiotic variables (Table 1), mainly on the spatial distribution of the assemblage of periphytic diatoms of the Guaiapo Stream, once significant temporal changes have not been verified.


Our findings pointed out that the assemblage of periphytic diatoms of the Guaiapo stream presented only spatial heterogeneity. As the geology of the microbasin herein studied is the same for the three sampling sites, it is supposed that the land use has influenced the abiotic variables of the stream, which generated similar responses from the assemblage of periphytic diatoms. In the absence of human influence, the nutrient concentration in the water of a certain stream is determined by geology, atmospheric deposition and vegetation (BIGGS, 1996). Also, variations in biotic and abiotic characteristics take place naturally along the longitudinal axis of a river (VANNOTE et al., 1980).

Periphytic diatoms are affected by anthropogenic or natural factors (PAN et al., 1996; RIMET; BOUCHEZ, 2012). In the Guaiapo Stream, the assemblage structure in the urban area was distinct from that found in rural area (middle stretch and mouth). The urban area presented the higher values of P[O.sub.4] and TN. Aquatic environments in urban centers exhibit increased concentration of nutrients, especially nitrogen, caused by poor sewage treatment and illegal discharge of effluents into these environments (PAUL; MEYER, 2008). Nitrogen and phosphorus are considered the main limiting nutrients for algal growth. Under increased concentrations of nitrogen and phosphorus, McCormick et al. (1996) registered the replacement of diatoms typical of oligotrophic environments with species indicators of eutrophication. In the Guaiapo Stream, even though the higher values of nitrogen found in the urban sites, the values of this nutrient were also high in the rural stretches. High concentrations of TN in these regions can be associated with the use of fertilizers in adjacent areas. In agreement with Lavoie et al. (2004) and Smucker and Vis (2011), the intensive agriculture is responsible for increased concentrations of nutrients in streams and also for chemical and physical changes in these environments.

High conductivity values are also considered one of the main effects of agriculture activity on streams (LELAND et al., 2001). The influence of this variable on periphytic diatoms has been previously reported in other studies (SONNEMAN et al., 2001; WALKER; PAN, 2006). Another factor that should be taken into account is the increase in flow velocity observed in downstream regions, favoring species with effective mechanisms of attachment to the substrate, like those with prostrate habit or attached to the substrate by mucilage tubes (STEVENSON, 1996; HERMANY et al., 2006). The presence of riparian vegetation was also important for the differentiation between urban and rural zones. Hill (1996) highlights the effect of light on the architecture of the periphytic algal assemblage, which influences its composition and growth, but the individual light requirements of periphytic algal species are barely known. Furthermore, the limitation of light is negative to the development of diatoms.

In this study, most indicator taxa of the urban region have a widespread distribution, but previous studies associated their occurrence with specific environments. Achnanthes exigua Grunow, for example, tolerates high nitrogen concentrations, being found in oligo- to eutrophic environments (LOBO et al., 2002; 2004a). Achnanthes rupestoides Hohn was also referred by Van Dam et al. (1994) as a species typical of meso-eutrophic waters. However, according to Hermany et al. (2006), this species has preference for eutrophic environments under strong human impact. Cyclotella pseudoestelligera Hustedt and Amphora copulata (Kutzing) Schoeman & Archibald also are taxa typical of environments with high nitrogen concentrations and eutrophic environments (VAN DAM et al., 1994).

According to the scarce literature on the ecology of Nupela, species belonging to this genus have been recorded in environments with moderate to high concentrations of TN (POTAPOVA et al., 2003), or in rivers severely polluted by organic matter (RUMRICH et al., 2000). In the Guaiapo Stream, Nupela praecipua (Reichardt) Reichardt and Nupela sp. were indicators of the urban region, containing higher concentrations of nitrogen and phosphorus. Similarly, ecological information concerning the species of Placoneis is lacking. Cox (2003) asserted that species belonging to this genus are mainly found in mesotrophic waters. Nevertheless, Taylor et al. (2007) registered species of this genus in mesotrophic to eutrophic environments. With regard to Navicula lohmannii Lange-Bert. & Rumrich there are no ecological data in the literature. In this research, N. lohmannii was indicator of the urban environment, that is, this species tolerates high concentrations of nitrogen and phosphorus.

Among the 12 species indicators of the rural region, the most cited in the literature are Cyclotella meneghiniana Kutzing and Cocconeis placentula var. euglypta (Ehrenberg) Grunow. They are typical of eutrophic environments, requiring high concentrations of nitrogen periodically (VAN DAM et al., 1994). In lotic systems from Southern Brazil, Cyclotella meneghiniana had already been registered as indicator of intermediate levels of eutrophication (LOBO et al., 2004c) and tolerant to heavily impacted environments (LOBO et al., 2004a). In addition to the preference for eutrophic environments, Cocconeis placentula and Cymbella kolbei Hustedt should get advantages from the growth form, strongly attached to the substrate, being resistant to higher flow velocity, verified in rural areas in this study. Soininen (2004) registered high abundance of Cocconeis placentula in environments with high current flow. Also, this species has been associated with agricultural areas (JUTTNER et al., 2003; LAVOIE et al., 2004). Amphora montana Krasske and Nitzschia palea (Kutz.) Smith also indicated eutrophic to hypereutrophic environments (VAN DAM et al., 1994; LOBO et al., 2002; DELGADO et al., 2012). On the species Navicula erifuga Lange-Bert., Navicula schroeteri Meister, Navicula viridula var. rostellata (Kutz.) Cleve and Nitzschia frustulum (Kutz.) Grunow, little ecological information is available, although, according to Van Dam et al. (1994), these taxa are characteristic of eutrophic environments. Nevertheless, in the Guaiapo Stream, this species was indicator of rural stretches, in which were recorded higher pH, flow and conductivity. Furthermore, Mayamaea atomus (Kutz.) Lange-Bert., which is indicator of the rural section, has been reported in strongly polluted environments (LOBO et al., 2002). On the other hand, Geissleria aikenensis (Patr.) Torg. & Oliv. is characteristic of environments with low mineral and organic content as well as high oxygen levels (HERMANY et al., 2006), and has low tolerance to eutrophication (LOBO et al., 2004b). We did not find ecological data on Gomphonema lagenula Kutz. In the Guaiapo Stream, this taxon was indicator of rural stretches, where lower phosphorus and nitrogen concentrations were verified, as well higher pH, flow and conductivity.


The structure of the periphytic diatom assemblage demonstrated the spatial gradient of the stream, reinforcing its role as an excellent environmental indicator. Eleven species characterized the urban sites, where it was found greater values of nitrogen and phosphorus. In rural environments, where the species were strongly influenced by nutrient concentrations, was observed preference for the registered values of pH and conductivity.

Our results evidenced changes in composition and abundance of periphytic diatoms, probably caused by limnological variations along the stream gradient. There are indicator species in each stretch of the stream, which can be used to assess the water quality.

Doi: 10.4025/actascibiolsci.v37i4.27426


To Priscila Izabel Tremarin and Thelma Alvim da Veiga Ludwig for help in the identification of diatoms. To CNPq, for the financial support to the project, 'Identification of possible bioindicators in urban aquatic ecosystems: the response of the groups of organisms to stress gradients', and grants given to LR and EAG. To UEM, Graduate Course in Ecology of Inland Aquatic Ecosystems -PEA and Nupelia, for logistical support.


ALLAN, J. D.; CASTILLO, M. M. Stream ecology: structure and function of running waters. New York: Chapman and Hall, 2007.

BIGGS, B. J. F. Patterns in benthic algae of streams. In: STEVENSON, R. J.; BOTHWELL, M. L.; LOWE, R. L. (Eds.). Algal ecology: freshwater benthic ecosystems. San Diego: Academic Press, 1996. p. 31-56.

BONA, F.; FALASCO, E.; FENOGLIO, S.; IORIO, L.; BADINO, G. Response of macroinvertebrate and diatom communities to human-induced physical alteration in mountain streams. River Research and Applications, v. 24, n. 8, p. 1068-1081, 2008.

CETESB-Companhia Ambiental do Estado de Sao Paulo. Demanda bioquimica de oxigenio (DBO), metodo da diluicao e incubacao 20 graus centigrados 5 dias. Sao Paulo: Cetesb, 1991. (Norma Tecnica L5.120).

COX, E. J. Placoneis Mereschkowsky (Bacillariophyta) revisited: resolution of several typification and nomenclatural problems, including the generitype. Botanical Journal of the Linnean Society, v. 141, n. 141, p. 53-83, 2003.

DELA-CRUZ, J.; PRITCHARD, T.; GORDON, G.; AJANI, P. The use of periphytic diatoms as a means of assessing impacts of point source inorganic nutrient pollution in south-eastern Australia. Freshwater Biology, v. 51, n. 51, p. 951-972, 2006.

DELGADO, C.; PARDO, I.; GARCIA, L. Diatom communities as indicators of ecological status in Mediterranean temporary streams (Balearic Islands, Spain). Ecological Indicators, v. 15, n. 15, p. 131-139, 2012.

DESCY, J. P.; COSTE, M. A set of methods for assessing water quality based on diatoms. Verhandlungen des Internationalen Verein Limnologie, v. 24, n. 24, p. 2112-2116, 1991.

DUFRENE, M.; LEGENDRE, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, v. 67, n. 3, p. 345-366, 1997.

FORE, L. S.; GRAFE, C. Using diatoms to assess the biological condition of large rivers in Idaho (U.S.A.). Freshwater Biology, v. 47, n. 10, p. 2015-2037, 2002.

GOMEZ, N.; LICURSI, M. The Pampean Diatom Index (IDP) for assessment of rivers and streams in Argentina. Aquatic Ecology, v. 35, n. 2, p. 173-181, 2001. GROWNS, I. Is genus or species identification of periphytic diatoms required to determine the impacts of river regulation? Journal of Applied Phycology, v. 11, n. 11, p. 273-283, 1999.

HERMANY, G.; SCHWARZBOLD, A.; LOBO, E. A.; OLIVEIRA, M. A. Ecology of the epilithic diatom community in a low-order stream system of the Guaiba hydrographical region: subsidies to the environmental monitoring of southern Brazilian aquatic systems. Acta Limnologica Brasiliensia, v. 18, n. 1, p. 9-27, 2006.

HILL, W. R. Effects of light. In: STEVENSON, R. J.; BOTHWELL, M. L.; LOWE, R. L. (Ed.). Algal ecology: freshwater benthic ecosystems. San Diego: Academic Press, 1996. p. 121-148.

JACKSON, D. A. Protest: a procrustean randomization test of community environment concordance. Ecoscience, v. 2, n. 3, p. 297-303, 1995.

JUTTNER, I.; SHARMA, S.; DAHAL, B. M.; ORMEROD, S. J.; CHIMONIDES, P. J.; COX, E. J. Diatoms as indicators of stream quality in the Kathmandu Valley and Middle Hills of Nepal and India. Freshwater Biology, v. 48, n. 11, p. 2065-2084, 2003.

KELLY, M. G.; WHITTON, B. A. The trophic diatom index: a new index for monitoring eutrophication in rivers. Journal of Applied Phycology, v. 7, n. 7, p. 433-444, 1995.

KELLY, M. G.; CAZAUBON, A.; CORING, E.; DELL'UOMO, A.; ECTOR, L.; GOLDSMITH, B.; GUASH, H.; HURLIMANN, J.; JARLMAN, A.; KAWECKA, B.; KWANDRANS, J.; LAUGASTE, R.; LINDSTROM, E. A.; LEITAO, M.; MARVAN, P.; PADISAK, J.; PIPP, E.; PRYGIEL, J.; ROTT, E.; SABATER, S.; VAN DAM, H.; VIZINET, J. Recommendations for the routine sampling of diatoms for water quality assessments in Europe. Journal of Applied Phycology, v. 10, n. 2, p. 215-224, 1998.

KOBAYASI, H.; MAYAMA, S. Most pollution tolerant diatoms of severely polluted rivers in the vicinity of Tokyo. Japanese Journal of Phycology, v. 30, n. 3, p. 188-196, 1982.

KRUSKAL, J. B. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypotheses. Psychometrika, v. 29, n. 1, p. 1-27, 1964a.

KRUSKAL, J. B. Nonmetric multidimensional scaling: a numerical method. Psychometrika, v. 29, n. 2, p. 115-129, 1964b.

LAVOIE, I.; VINCENT, W. F.; PIENITZ, R.; PAINCHAUD, J. Benthic algae as bioindicators of agricultural pollution in the streams and rivers of southern Quebec (Canada). Aquatic Ecosystem Health & Management, v. 7, n. 1, p. 43-58, 2004.

LELAND H. V.; BROWN L. R.; MUELLER D. K. Distribution of algae in the San Joaquin River, California, in relation to nutrient supply, salinity, and other environmental factors. Freshwater Biology, v. 46, n. 9, p. 1139-1167, 2001.

LOBO, E. A.; BES, D.; TUSDEQUE, L.; ECTOR, L. Water quality assessment of the Pardinho river, RS, Brazil, using epilithic diatom assemblages and faecal coliforms as biological indicators. Vie et Milieu, v. 54, n. 2-3, p. 115-125, 2004a.

LOBO, E. A.; CALLEGARO, V. L. M.; BENDER, E. P. Utilizacao de algas diatomaceas epiliticas como indicadoras da qualidade da agua em rios e arroios da Regiao Hidrografica do Guaiba, RS, Brasil. Santa Cruz do Sul: Edunisc, 2002.

LOBO, E. A.; CALLEGARO, V. L. M.; HERMANY, G.; BES, D.; WETZEL, C. E.; OLIVEIRA, M. A. Use of epilithic diatoms as bioindicators from lotic systems in southern Brazil, with special emphasis on eutrophication. Acta Limnologica Brasiliensia, v. 16, n. 1, p. 25-40, 2004b.

LOBO, E.A.; CALLEGARO,V. L. M.; WETZEL, C. E.; HERMANY, G.; BES, D. Water quality evaluation of Condor and Capivara Streams, Municipal District of Porto Alegre, RS, Brazil, using epilithic diatom communities as bioindicators. Oceanological and Hydrobiological Studies, v. 33, n. 2, p. 77-93, 2004c.

LOBO, E. A.; CALLEGARO, V. L. M.; OLIVEIRA, M. A.; SALOMONI, S. F.; SCHULE, N. S.; ASAI, K. Pollution tolerant diatoms from lotic systems in the Jacui Basin, Rio Grande do Sul, Brazil. Iheringia. Serie Botanica, v. 47, n. 1, p. 45-72, 1996.

MAACK, R. Geografia fisica do estado do Parana. 4. ed. Ponta Grossa: UEPG, 2012.

McCORMICK, P. V.; RAWLIK, P. S.; LURDING, K.; SMITH, E. P.; SKLAR F. H. Periphyton--water quality relationship along a nutrient gradient in the northern Florida Everglades. Journal of North American Benthological Society, v. 15, n. 4, p. 433-449, 1996.

McCUNE, B.; GRACE, J. B. Analysis of ecological communities. Oregon: Gleneden Beach, 2002.

McCUNE, B.; MEFFORD, M. J. PC-ORD: multivariate analysis of ecological data (Version 5), MJM software design. Oregon: Gleneden Beach, 2006.

MEYER, J. L.; PAUL, M. J.; TAULBEE, W. K. Stream ecosystem function in urbanizing landscapes. Journal of North American Benthological Society, v. 24, n. 3, p. 602-612, 2005.

MOREIRA-FILHO, H.; VALENTE-MOREIRA, I. M. Avaliacao taxonomica e ecologica das diatomaceas (Bacillariophyceae) epifitas em algas pluricelulares obtidas nos litorais dos Estados do Parana, Santa Catarina e Sao Paulo. Boletim do Museu Botanico Municipal, v. 47, n. 1-2, p. 1-17, 1981.

MORESCO, C.; RODRIGUES, L. Periphytic diatom as bioindicators in urban and rural streams. Acta Scientiarum. Biological Sciences, v. 36, n. 1, p. 67-78, 2014. MULHOLLAND, P. J. Role in nutrient cycling in streams. In: STEVENSON, R. J.; BOTHWELL, M. L.; LOWE, R. L. (Ed.). Algal ecology: freshwater benthic ecosystems. San Diego: Academic Press, 1996. p. 609-639.

PAN, Y.; STEVENSON, R. J.; HILL, B. H.; HERLIHY, A. T.; COLLINS, G. B. Using diatoms as indicators of ecological conditions in lotic systems: a regional assessment. Journal of North American Benthological Society, v.15, n. 4, p. 481-495, 1996.

PAPPAS, J. L.; STORMER, E. F. Quantitative method for determining a representative algal sample count. Journal ofPhycology, v.32, n. 4, p. 693-696, 1996.

PERES-NETO, P. R.; JACKSON, D. A. How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia, v. 129, n. 2, p. 169-178, 2001.

PAUL, M. J.; MEYER, J. L. Streams in the urban landscape. In: MARZLUFF, J. M.; HULENBERGER, E.; ENDLICHER, W.; ALBERTI, M.; BRADLEY, G.; RYAN, C.; SIMON, U.; ZUMBRUNNEN, C. (Ed.). Urban Ecology: an international perspective on the interaction between humans and nature. New York: Springer, 2008. p. 207-231.

POTAPOVA, M. G.; PONADER, K. C.; LOWE, R. L.; CLASON, T. A.; BAHLS, L. L. Small-celled Nupela species from North America. Diatom Research, v. 18, n. 2, p. 293-306, 2003.

RIMET, F.; BOUCHEZ, A. Biomonitoring river diatoms: Implications of taxonomic resolution. Ecological Indicators, v. 15, n. 1, p. 92-99, 2012.

ROHLF, F. J.; SLICE, D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology, v. 39, n. 1, p. 40-59, 1990. ROUND, F. E.; CRAWFORD, R. M.; MANN, D.G.

The diatoms. Biology and morphology of the genera. Cambridge: Cambridge University Press, 1990.

RUMRICH, U.; LANGE-BERTALOT, H.; RUMRICH, M. Diatoms of the Andes from Venezuela to Patagonia/Tierra del Fuego and two additional contributions. In: LANGE-BERTALOT, H. (Ed.). Iconographia Diatomologica: annotated diatom micrographs. Ruggell: A.R.G. Gantner Verlag K.G., 2000. p. 1-673. v.9.

SILVA, S. A.; OLIVEIRA, R. Manual de analises fisico-quimicas de aguas de abastecimento e residuarias. Campina Grande: DEC/CCT/UFPG, 2001.

SMUCKER, N. J.; VIS, M. L. Spatial factors contribute to benthic diatom structure in streams across spatial scales: Considerations for biomonitoring. Ecological Indicators, v. 11, n. 5, p.1191-1203, 2011.

SOININEN, J. Responses of epilithic diatom communities to environmental gradients in some finnish rivers. International Review of Hydrobiology, v. 87, n. 1, p. 11-24, 2002.

SOININEN, J. Assessing the current related heterogeneity and diversity patterns of benthic diatom communities in a turbid and a clear water river. Aquatic Ecology, v. 38, n. 4, p. 495-501, 2004.

SONNEMAN, J. A.; WALSH, C. J.; BREEN, P. F.; SHARPE, A. K. Effects of urbanization on streams of the Melbourne region, Victoria, Australia. II. Benthic diatom communities. Freshwater Biology, v. 46, n. 4, p. 553-565, 2001.

STEVENSON, R. J. An introduction to algal ecology in freshwater benthic habitats. In: STEVENSON, R. J.; BOTHWELL, M. L.; LOWE, R. L. (Ed.). Algal ecology: freshwater benthic ecosystems. San Diego: Academic Press, 1996. p. 3-30.

STEVENSON, R. J.; PAN, Y. Assessing environmental conditions in rivers and streams with diatoms. In:

STORMER, E. F.; SMOL, J. P. (Ed.).The diatoms: applications for the environmental and earth sciences. Cambridge: Cambridge University Press, 1999. p. 11-40.

TAYLOR, J. C.; ARCHIBALD, C. G. M.; HARDING, W. R. An illustrated guide to some common diatom species from South Africa. Pretoria: WRC Report, 2007.

VAN DAM, H.; MERTENS, A.; SKINDELAM, J. A coded checklist and ecological indicator values of freshwaters diatoms from Netherlands. Netherlands Journal of Aquatic Ecology, v. 28, n. 1, p. 117-133, 1994.

VANNOTE, R. L.; MINSHALL, G. W.; CUMMINS, K. W.; SEDELL, K. R.; CUSHING, C. E. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, v. 37, n. 1, p.130-137, 1980.

WALKER, C. E.; PAN, Y. Using diatom assemblages to assess urban stream conditions. Hydrobiologia, v. 561, n. 1, p. 179-189, 2006.

Received on April 15, 2015.

Accepted on August 20, 2015.

Carina Moresco (1) *, Eder Andre Gubiani (2) and Liliana Rodrigues (3)

(1) Faculdade Integrado de Campo Mourao, BR-158, km 207, 87300-970, Campo Mourao, Parana, Brazil. (2) Grupo de Pesquisas em Recursos Pesqueiros e Limnologia, Universidade Estadual do Oeste do Parana, Toledo, Parana, Brazil. (3) Programa de Pos-graduacao em Ecologia de Ambientes Aquaticos Continentais, Nucleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringa, Maringa, Parana, Brazil. * Author for correspondence. E-mail:

Table 1. Results of principal component analysis (PCA)
and summary of abiotic variables (mean [+ or -] standard
deviation) measured in the Guaiapo Stream, municipality
of Maringa, Parana State, sampled from August 2007 to
June 2008. Sampling sites were grouped into urban
(headwater) and rural (middle and mouth) sites and
periods were grouped into dry (April, June, August)
and rainy seasons (October, December, February).
It is presented, for each axis, the eigenvalues,
the percent of variance explained and the broken
-stick eigenvalues. For each variable, it is listed
the eigenvector (loading or correlation). T = water
temperature, pH = hydrogenic potential,
Cond. = electrical conductivity, [O.sub.2] = dissolved
oxygen, P[O.sub.4] = orthophosphate, TN = total nitrogen,
BO[D.sub.5] = biochemical oxygen demand, Flow = flow

                       Sampling sites

                       Axis 1   Axis 2

Eigenvalue              2.71     1.70
Broken-Stick            2.72     1.72
Explained              33.84    21.22
  Variance (%)
Accumulated            33.84    55.06
  Variance (%)
T ([degrees]C)         -0.27     0.05
pH                      0.53     0.04
Cond ([micro].S         0.23     0.56
[O.sub.2]               0.31    -0.29
  (mg [L.sup.-1])
P[O.sub.4]             -0.34    -0.30
  (mg [L.sup.-1])
TN (mg [L.sup.-1])      0.32    -0.51
BO[D.sub.5]            -0.25     0.43
  (mg [L.sup.-1])
Flow (m [s.sup.-1])     0.47     0.26

                                     Sampling sites

                              Urban                   Rural

  Variance (%)
  Variance (%)
T ([degrees]C)         22.90 [+ or -] 0.91     22.58 [+ or -] 1.64
pH                      7.00 [+ or -] 0.50     7.55 [+ or -] 0.37
Cond ([micro].S        128.70 [+ or -] 4.82   177.23 [+ or -] 16.07
[O.sub.2]               8.62 [+ or -] 0.56     8.78 [+ or -] 0.68
  (mg [L.sup.-1])
P[O.sub.4]              1.08 [+ or -] 0.07     1.04 [+ or -] 0.05
  (mg [L.sup.-1])
TN (mg [L.sup.-1])      6.75 [+ or -] 1.47     5.99 [+ or -] 3.63
BO[D.sub.5]             1.95 [+ or -] 0.75     1.88 [+ or -] 0.88
  (mg [L.sup.-1])
Flow (m [s.sup.-1])     1.17 [+ or -] 0.03     1.30 [+ or -] 0.10


                                Dry                    Rainy

  Variance (%)
  Variance (%)
T ([degrees]C)          22.11 [+ or -] 1.13     23.38 [+ or -] 1.20
pH                      7.43 [+ or -] 0.53      7.11 [+ or -] 0.46
Cond ([micro].S        157.03 [+ or -] 28.46   148.89 [+ or -] 26.83
[O.sub.2]               8.49 [+ or -] 0.81      8.91 [+ or -] 0.19
  (mg [L.sup.-1])
P[O.sub.4]              1.04 [+ or -] 0.05      1.07 [+ or -] 0.08
  (mg [L.sup.-1])
TN (mg [L.sup.-1])      7.78 [+ or -] 3.26      4.96 [+ or -] 0.82
BO[D.sub.5]             1.63 [+ or -] 0.58      2.19 [+ or -] 0.91
  (mg [L.sup.-1])
Flow (m [s.sup.-1])     1.23 [+ or -] 0.11      1.24 [+ or -] 0.09

Table 2. Results of PERMANOVA main test for periphytic
diatom assemblage in the sites (urban and rural) and periods
(dry and rainy season) of the Guaiapo Stream, municipality of
Maringa, Parana State, sampled from August 2007 to June

Source             df     SS        MS     Pseudo-F   P(perm)

Sites              1    801286    801286     4.17      0.02
Periods            1    153547    153547     0.80      0.43
Sites x Periods    1    191246    191246     0.99      0.38
Residual           20   3841105   192055
Total              23   4987184

Table 3. Summary of the indicator species analysis (IndVal)
showing the relative abundance (RA), relative frequency (RF)
and indicator value (IV) for the periphytic diatom species
in the sites (U = urban and R = rural) of the Guaiapo Stream,
municipality of Maringa, Parana State, sampled from
August 2007 to June 2008. Bold values indicates
significant indicator results (p < 0.05,
Monte Carlo permutation test).

                                  RA          RF         IV

                                U     R     U     R    U    R

Achnanthes exigua Grun.        76    24    100   50    76   12
Achnanthes rupestoides Hohn    99     1    75     8    74   0
Amphora copulata (Kutz.)       87    13    67    17    58   2
Schoe. & Archib.
Aulacoseira sp.                93     7    67     8    62   1
Cycloteua pseudostelligera     89    11    58    17    52   2
Eunotia sp.                    96     4    42     8    40   0
Navicula lohmannii             100    0    50     0    50   0
Lange-Bert. & Rumrich
Nupela praecipua (Reich.)      99     1    100   17    99   0
Nupela sp.                     96     4    83    42    80   2
Placoneis constans var.        90    10    92    25    83   2
symmetrica (Hust.) Kobay.
Placoneis porifera var.        100    0    42     0    42   0
opportuna (Hust.)
Amphora montana Krass.          4    96    83    92    3    88
Cocconeisplacentula var.        0    100    8    75    0    75
euglypta (Ehr.) Cleve
Cychteua meneghiniana Kutz.     2    98    50    92    1    90
Cymbella kolbei Hustedt.        0    100    0    75    0    75
Gomphonema lagenula Kutz.       9    91    100   100   9    92
Mayamaea atomus (Kutz.)         2    98    50    92    1    90
Geissleria aikenensis           1    99    75    100   1    99
(Patr.) Torg. & Oliv.
Navicula erifuga Lange-Bert.    1    99    33    92    0    91
Navicula schroeteri Meister    11    89    75    100   9    89
Navicula viridula var.         17    83    50    83    9    69
rostellata (Kutz.) Cleve
Nitzschiafrustulum (Kutz.)     13    87    17    58    2    51
Nitzschia palea (Kutz.)         4    96    100   100   4    96
COPYRIGHT 2015 Universidade Estadual de Maringa
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2015 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:texto en ingles
Author:Moresco, Carina; Gubiani, Eder Andre; Rodrigues, Liliana
Publication:Acta Scientiarum. Biological Sciences (UEM)
Date:Oct 1, 2015
Previous Article:Assessment of mint (Mentha spp.) species for large-scale production of plantlets by micropropagation/Avaliacao de especies de menta (Mentha spp.)...
Next Article:Composition, structure and floristic diversity in dense rain forest in the Eastern Amazon, Amapa, Brazil/Composicao, estrutura e diversidade...

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters