Temporal variation of Nitella furcata subsp. mucronata var. mucronata f. oligospira (Charophyceae) in the Ninféias pond, São Paulo State, southeast Brazil

Variação temporal de Nitella furcata subsp. mucronata var. mucronata f. oligospira (Charophyceae) no Lago das Ninféias, São Paulo, sudeste do Brasil

Temporal variation of Nitella furcata subsp. mucronata var. mucronata f. oligospira (Charophyceae) in the Ninféias pond, São Paulo State, southeast Brazil

Variação temporal de Nitella furcata subsp. mucronata var. mucronata f. oligospira (Charophyceae) no Lago das Ninféias, São Paulo, sudeste do Brasil

Norma Catarina BuenoI, ¹; Carlos Eduardo de Mattos Bicudo^II

^IUNIOESTE, C. Postal 711, CEP 85814-110, Cascavel, PR, Brasil

^IIInstituto de Botânica, Secção de Ecologia, C. Postal 4005, CEP 01061-970, São Paulo, SP, Brasil ([e-mail])

ABSTRACT

Temporal and spatial variation of Nitella furcata (Roxburgh ex Bruzelius) C. Agardh emend. R.D. Wood subsp. mucronata (A. Braun) R.D. Wood var. mucronata f. oligospira (A. Braun) R.D. Wood were studied at the Ninféias pond (23°38'18.9"S, 46°37'16.3"W), a tropical, shallow, mesotrophic reservoir located in the Parque Estadual das Fontes do Ipiranga Biological Reserve, Municipality of São Paulo, southeast Brazil. Water samples were collected monthly from October/1996 to October/1997 for turbidity, electric conductivity, pH, alkalinity, dissolved oxygen, nutrients, biomass, and algal phenology analysis. Spatial distribution pattern of algal biomass showed that all four sampling stations were similar among themselves during the whole study period. Regarding the temporal variation, greatest algal total biomass values (98.35-266.06 g.m^-2) were measured during the rainy period whereas the smallest ones (48.86-170.56 g.m^-2) were detected during the dry period. Algal population density peaked at all four sampling stations from October/1996 to April/1997 (rainy period) when the greatest values of air and water temperature, precipitation, solar radiation, turbidity, total nitrogen, and ammonium were measured allowing favorable conditions for the algal growth. Period from May/1997 (late fall) to October/1997 (early spring) was favorable to the development of reproductive structures (nucules and globules) with consequent decrease of algal biomass and population density, clearly suggesting the greatest energy allocation towards the development of sexual reproductive structures. This fact was confirmed by the canonic correspondence analysis that indicated strong correlation between nucules length and width, number of nucules per plant, and oospores length and width with the low values of pH and high ones of dissolved inorganic matter detected during the dry period. Consequently, environmental factors such as increasing of water temperature and nutrients availability at the Ninféias pond acted decisively towards growth and accumulation of algal biomass.

Key words: Charophyceae, biomass, phenology, aquatic macrophyte, Nitella

RESUMO

Dinâmica temporal de uma população de Nitella furcata (Roxburgh ex Bruzelius) C. Agardh emend. R.D. Wood subsp. mucronata (A. Braun) R.D. Wood var. mucronata f. oligospira (A. Braun) R.D. Wood foi estudada no Lago das Ninféias (23°38'18,9"S, 46°37'16,3"W), um reservatório tropical, raso, mesotrófico situado na Reserva Biológica do Parque Estadual das Fontes do Ipiranga, Município de São Paulo, sudeste do Brasil. Amostras de água foram coletadas mensalmente de outubro/1996 a outubro/1997 para análise de turbidez, condutividade elétrica, pH, alcalinidade, oxigênio dissolvido, nutrientes, biomassa e fenologia da alga. Os maiores valores médios de biomassa total da carácea (98,35-266,06 g.m^-2) foram registrados no período de chuvas e os menores (48,86-170,56 g.m^-2) no seco. A densidade populacional apresentou picos de outubro/1996 a abril/1997, isto é, durante a estação chuvosa, época em que foram registrados os maiores valores de temperatura do ar e da água, de precipitação pluvial, radiação solar, turbidez, nitrogênio total e de amônio, constituindo condições favoráveis para o crescimento das plantas. O período entre maio/1997 (final do outono) e outubro/1997 (início da primavera) mostrou-se favorável ao desenvolvimento de estruturas reprodutivas (núculas e glóbulos), com diminuição de biomassa e densidade populacional da carácea, sugerindo maior alocação de energia para a formação de estruturas reprodutivas. Este fato foi confirmado pela análise de correspondência canônica, que registrou fortes correlações entre comprimento e diâmetro das núculas, número total de núculas por planta e comprimento e diâmetro dos oósporos, com os baixos valores de pH e altos de matéria orgânica verificados no período de seca. Concluindo, fatores ambientais, como aumento de temperatura da água e disponibilidade de nutrientes, parecem exercer influência decisiva sobre o crescimento e acúmulo de biomassa da alga no Lago das Ninféias.

Palavras-chave: Charophyceae, biomassa, fenologia, macrófita aquática, Nitella

Introduction

Charophyceae is a very typical algal class due to the macroscopic size of its constituents and the extreme morphological complexity of both their thallus organization and the gametangia structure (van-den-Hoek et al. 1996). Despite of the Charophyceae being relatively frequent in ponds, rivers, creeks, etc., research aiming at their ecology, phenology, and geographic distribution are still very scarce worldwide, Brazil being not an exception.

Early papers referring to the seasonal variation of macroalgal communities (including the Charophyceae) or to aspects of their spatial distribution in lotic environments are the ones by Necchi Jr. et al. (1994; 1997), Branco & Necchi Jr. (1996a; 1996b; 1998), Vieira Jr. et al. (2002; 2003), and Vieira Jr. & Necchi Jr. (2002; 2003).

Dealing with material from lentic systems, there are the papers by Carneiro et al. (1994), Palma-Silva (1998), and Palma-Silva et al. (2000; 2002) that studied some ecological aspects of the charophyte community at Imboassica and Piratininga lagoons in the state of Rio de Janeiro.

Present research aimed at determining which environmental variables are responsible for the greatest variability in the distribution of the biological features (reproduction, algal density and biomass) of Nitella furcata (Roxburgh ex Bruzelius) C. Agardh emend. R.D. Wood subsp. mucronata (A. Braun) var. mucronata f. oligospira (A. Braun) R.D. Wood at the Ninféias pond, Municipality of São Paulo, southeast Brazil.

Material and methods

Ninféias pond (23°38'18.9"S, 46°37'16.3"W) is a shallow mesotrophic reservoir located at the Parque Estadual das Fontes do Ipiranga Biological Reserve (Bicudo et al. 2002), Municipality of São Paulo, southeast Brazil. The climate in the area is, according to Conti & Furlan (2003), tropical of altitude based on the local altitude (800 m), average of monthly maximum and minimum temperatures not surpassing 6-8 ºC, and the average precipitation in two months of the year < 60 mm.

Three sampling sites were defined according to the presence of stands of the submersed attached macrophyte N. furcata subsp. mucronata var. mucronata f. oligospira. Size of area covered by the alga at the sampling sites varied among sites and in the same site depending on the time of the year. Samplings within each sampling station were aleatory (n = 6). A total of 216 sample units were obtained. Other macrophytes present in the stands were: Bacopa sp., Cyperus papirus L., Echinodorus grandiflorus (Cham. & Schltdl.) Mich., Eleocharis sp., Hydrocleis nymphoides (Willd.) Buch., Mayaca fluviatilis Aubl., Nymphaea ampla (Salisb.) DC, Nitella leptostachys (A. Braun) R.D. Wood var. leptostachys, Ricciocarpus natans (L.) Corda, Salvinia auriculata Aubl., Utricularia foliosa L., Utricularia gibba L., and Valisneria spiralis L.

Charophyte specimens' identification followed Picelli-Vicentim et al. (2004).

Samplings were carried monthly from October/1996 to October/1997 to include the rainy (October/1996 to February/1997; September/1997October/1997) and the dry period (March/1997 to August/1997) of that year. All specimens collected are deposited in the "Herbário Científico do Estado Maria Eneyda P. Kauffmann Fidalgo" (SP). Air temperature (daily maximum, minimum, and average) and rain precipitation (daily total) data measured during the five consecutive days that preceded the sampling ones and at the sampling days were provided by the meteorological station of the Astronomy, Geophysics and Atmospheric Sciences Institute of the University of São Paulo located about 800 m from the Ninféias pond.

Since reservoir depth at the sampling stations varied from 11 to 60 cm, water samples for physical and chemical variables determination were gathered only at the subsurface (30 cm below surface) of the water column (Tab. 1).

Algal biomass and phenology data were collected using a 25 cm² PVC square frame according to Westlake (1965, 1971). Inside the square frame, a 5 cm in diam. PVC tube (area 19.7 cm²) was used. For biomass determination, material was dried in a drier with forced air circulation at 70 ºC until constant weight (Hunter 1976). The aboveground biomass was estimated as dry weight per surface unit.

Material collected for phenological studies was fixed and preserved in 4% formalin solution. From each individual specimen, at least five nodes were selected at random for the study of reproductive stages taking into account their maturation stage. Morphological characteristics selected were the following: (1) number of plants collected, (2) plant height (cm), (3) diameter (µm) of cauloid, (4) number and dimensions of sterile branchlets per whorl, and (5) number and dimensions of fertile branchlets per whorl.

The following reproductive characteristics were studied: (1) number and dimensions of nucules present in at least five whorls of each individual specimen, (2) number and dimensions of oospores per individual specimen, and (3) number and diameter (µm) of mature globules per individual specimen.

Canonic Correspondence Analysis (Hall & Smool 1992) was used to correlate environment variables and morphometric data taking into consideration the weight-average and the unimodal response model (Ter-Braak & Prentice 1988) to get a more detailed response from the samplings profile. To perform the Canonic Correspondence Analysis (CCA), the following seven environment variables were used: turbidity, pH, HCO₃, electric conductivity, dissolved oxygen, dissolved inorganic nitrogen, and total phosphorus. Also, 16 biological variables (plant height, biomass, density, diameter of cauloid, length and diameter of sterile branchlets, length and diameter of fertile branchlets, total number of nucules, length and diameter of nucules, diameter of globules, total number of globules, length and diameter of oospores, and total number of oospores).

Monte Carlo test (99 permutations; p < 0.05) was used to inform the probability of the axes eigenvalues be distributed at random. Both analyses were performed by using the PC-ORD version 4.0 for Windows software. Data were standardized according to their variation amplitude ("ranging") using the WinMat software (Shepherd 1996).

Results

Air temperature varied from 5.6 (July/1997) to 34.2 ºC (September-October/1997). In June/1997, air temperature maximum values measured during the five days prior to sampling day varied from 15.8 to 20.3 ºC, and in February/1997 from 26.7 to 31.5 ºC. Rain precipitation monthly average varied from 7.1 (July/1997) to 54.5 mm (October/1996).

Environment physical and chemical variables considered important for the present study (Tab. 2) showed that water temperature, pH, turbidity, and dissolved inorganic nitrogen presented their greatest values during the rainy period (summer). As expected, water temperature presented its lowest values during the dry period (winter). Water turbidity presented its greatest values in February, March, and October/1997.

Greatest values of the charophyte total biomass (113-300 g.m^-2) were measured during the rainy period, whereas the lowest ones (80-217 g.PS.m^-2) occurred during the dry period (Fig. 1).

Population density peaked from October/1996 to April/1997 (5,057-8,121 ind.m^-2), i.e. during the rainy period when the greatest water temperature, rain precipitation, solar radiation, turbidity, total nitrogen, and ammonium values were measured, thus constituting favorable conditions to the growth of plants. The greatest average values for the plant height were measured in March/1997 (21 cm) and the smallest in September/1997 (13 cm). In April/1997 (end of the rainy period), the smallest values of plants density and cauloid diameter were detected.

Sterile branchlets of Nitella furcata subsp. mucronata var. mucronata f. oligospira were ca. 3 cm long and 96.1 to 158.3 µm in diameter, whereas length of fertile branchlets varied from 3 to 5 cm and diameter from 116 to 226 µm (Fig. 2).

From July/1997 on (dry period = winter), it was observed a gradual increase in the length of fertile branchlets. Length of fertile branchlets average values varied between 3.08 in May/1997 to 5 cm in September/1997, and their variation coefficient from nihil to 40.2%. It was also observed a relative increase in the diameter of fertile branchlets in February and March/1997 (rainy period = summer), but a strong decrease from April/1997 on (winter).

Reproductive features suggested some synchronism in the production and maturation of male and female gametangia, the period of greatest occurrence of these structures being May (end of fall) to October/1997 (beginning of spring). Total nucule length, including the coronule, varied from 169 (October/1996) to 448 µm (July/1997) and diameter from 89 µm (February/1997) to 284 µm (October/1997), average globule diameter values varied from 98 µm (October/1996) to 228 µm (October/1997), oospore length varied from 167 µm (October/1996) to 282 µm (May/1997), and oospore diameter from 153 µm (during the first 6 sampling months) to 230 µm (September and October/1997) (Fig. 3-4).

CCA analysis indicated the association of the environmental variables with the climatic periods, i.e. the dry and the rainy period (Fig. 5, Tab. 3-4).

Monte Carlo test was significant (p < 0.05), what indicates that events were not at random, but did represent the relationship existing among environment variables and biological information.

Eigenvalues for axes 1 (l = 0.194) and 2 (l = 0.065) explained 59% of biological data variance. Correlation morphometry-environment for axes 1 (0.977) and 2 (0.888) was high indicating some relationship between distribution of biological and abiotic data used for ordination (Tab. 4). Canonic coefficients and intra-set correlations for axis 1 (Tab. 5) showed that electric conductivity contributes significantly towards ordination of data like turbidity and dissolved inorganic nitrogen. CCA intra-set correlations showed just some moderate contribution towards ordination of biological-environment data.

CCA pointed out that the abiotic variables most related to axis 1 were: turbidity (r = 0.916), electric conductivity (r = 0.974), dissolved oxygen (r = 0.700), total phosphorus (r = 0.885), and dissolved inorganic nitrogen (r = -0.937), all together reflecting the best growth conditions for the alga (Fig. 5, Tab. 5), and which were favored by the greatest nutrients availability during the rainy period (summer).

At the positive side of axis 1 they were located almost all biological structures (vegetative, biomass, and algal density), i.e. (alt) plant heigth (r = 0.499), (bio) plant biomass (r = 0.414), and (d) plant density (r = 0.519), and at the negative side the reproductive structures: (nc) length of nucule (r = -0,911), (nd) diameter of nucule (r = -0,926), (nt) total number of nucules (r = -0.754), (oc) length of oospore (r = -0.914), (od) diameter of oospore (r = -0.942), and (nt) total number of oospores (r = -0.807) related to the greatest dissolved inorganic nitrogen values (r = -0.937).

Sampling months were segregated in two periods at the opposite sides of axis 1. At the negative side they were May, June, July, September, and October/1997, whereas at the positive side were October and December/1996, i.e. months of high rain precipitation. February and March/1997 showed the greatest values of dissolved inorganic nitrogen (DIN) characterizing the end of the rainy period (summer) and the best one for algal growth. As the rain precipitation values increased (October, November, and December/1996) there was an increase in the nutrient values. Following the decrease of rain precipitation, there was an increase of nutrient and electric conductivity values, which could have interfered on the development of the alga morphological structures.

Axis 2 is strongly influenced by the pH (r = 0.983), dissolved oxygen (r = 0.960), and dissolved inorganic nitrogen (r = 0.918) (Tab. 5). One can note that reproductive structures (male and female gametangia) are weakly related with axis 2 indicating that the latter axis seems to discretely suggest a gradient related to the physical environmental conditions that dominated the dry period (winter).

Discussion

Morphological features of the charophyte showed the typical seasonal pattern of temperature region (Fernández-Aláez et al. 2002). Thus, period between May (end of fall) and October/1997 (beginning of spring) was favorable to the development of reproductive structures (nucules and globules), with the respective decrease of biomass and algal density, thus suggesting allocation of energetic resources towards the development of reproductive structures according to Wood & Imahori (1965), Casanova (1994), and Vieira Jr. & Necchi Jr. (2002).

During the dry period, as the reproductive structures (nucules, globules, and oospores) started to appear, the vegetative ones showed, in average, metric values lesser than the ones obtained during the rainy period, thus calling for some seasonality in regard to fertility of the population of Nitella furcata subsp. mucronata var. mucronata f. oligospira at the Ninféias pond.

Species temporal variation in relation to fertility showed the following two distinct periods: one between October/1996 (spring) and March/1997 (summer) with sterile plants (rainy period), and the other one between May/1997 (fall) and September/1997 (winter) with fertile plants, in accordance to data in Jair Vieira Jr. (unpublished). For the latter author, environment variables that influenced most the phenological pattern of the charophyte species in tropical lotic systems were current speed, air temperature, and to a lesser degree the ammonium concentration.

Both monoiceous (N. furcata subsp. mucronata var. mucronata f. oligospira) and dioiceous species (N. cernua) seems to have presented some synchrony in the production and maturation of gametangia (Vieira Jr. & Necchi Jr. 2002).

The relatively low number of oospores (39) found during this study was much probably due to the fact that such structures fall from the plant as soon as they ripe to germinate in the system's sediments. Oospores were usually found loose among the verticelate branchlets that, besides sustaining gametangia and oospores, also guarantee protection and habitat for different autotrophic organisms.

Oospores occurred in the Ninféias pond during a similar period to that in Hussain et al. (1996) for six charophyte species (Chara globularis, C. cf. contraria, C. vulgaris var. gymnophylla, C. vulgaris var. longibracteata, C. zeylanica, and C. zeylanica var. diaphana f. oerstediana) in Saudi Arabia, i.e. with oospores production peaks from October/1996 to March/1997 (local winter). Identical behavior was verified by Sokol & Stross (1986) in N. furcata subsp. megacarpa kept in experimental conditions. Latter authors observed that light may affect production of oospores and, consequently, determines distribution of plants in nature.

During the present study, best environment conditions for the growth of and colonization by the charophyte would be greater temperatures and nutrient availability in the reservoir (rainy period). During this period, increase of plant biomass and density, of cauloid diameter, and in the sterile branchlets dimensions were detected leading to larger and more robust plants. During the dry period, however, charophytes population started to produce reproductive structures (nucules, globules, and oospores) suggesting that reproductive activity was more concentrate in this period, and followed by a decrease in size of vegetative structures.

Observations above were confirmed by multivariate analyses (CCA), which allowed a global interpretation of all abiotic and biological information and showed strong correlation between length and diameter of nucules, total number of nucules per plant, and length and diameter of oospores associated with the lowest values of nutrients, water temperature, electric conductivity, HCO₃, and turbidity measured during the dry period.

Population density peaked from October/1996 to April/1997 (rainy period), a period in which they were detected the greatest values of air and water temperature, rain precipitation, and of dissolved inorganic nitrogen, a set of conditions that favored growth of plants. The greatest average values of biomass of N. furcata subsp. mucronata var. mucronata f. oligospira during the rainy period (summer) were five times greater than those of the dry period (winter) due to the greatest nutrient availability (total nitrogen, total phosphorus, and ammonium), and greatest values of turbidity and electric conductivity during the rainy period. Similar observations were documented for the mid portion of the Paraná river by Del-Viso et al. (1968).

Jair Vieira Jr. (unpublished) observed, however, a different pattern that is typical for macroalgae of tropical lotic systems, i.e. greater abundance during the dry period and lesser biomass during the rainy one, that agreed with data in Necchi Jr. & Pascoaloto (1993), Branco & Necchi Jr. (1997), and Necchi Jr. & Branco (1999). Similar conclusion was reached by Carneiro et al. (1994) after studying a community of Chara hornemanii that presented an expansion phase during the winter and a phase in which biomass values decreased during the fall, when the height of the water column increased due to the increase of rain precipitation.

According to Fernández-Aláez et al. (2002), however, the temperate zone macrophyte's biomass usually increases during the spring and peaks during the summer due to the hydrological regimen and the water temperature. Still according to the latter authors, biomass of charophytes studied decreased considerably during the winter due to the increase of the water level in the studied lakes.

Analysis of the seasonal variation of the morphological characteristics of specimens presently studied showed variation along the sampling period, in accordance to Casanova (1994). Morphological modifications in plant height, cauloid diameter, and number and length of verticilate branchlets seems to be related to the environmental variables studied for each period of the year, thus agreeing with the annual life history of the species studied for the Brazilian territory.

Acknowledgements

Senior author (NCB) is indebted to CNPq, Conselho Nacional de Desenvolvimento Científico e Tecnológico, for financial support represented by a Doctoral Fellowship during four consecutive years (Proc. 141492/95-3).

Received: February 02, 2004. Accepted: June 14, 2005.

• Bicudo, C.E.M.; Carmo, C.F.; Bicudo, D.C.; Henry, R.; Pião, A.C.S.; Santos, C.M.S. & Lopes, M.R.M. 2002. Morfologia e morfometria de três reservatórios do PEFI. In: D.C. Bicudo; M.C. Forti & C.E.M. Bicudo (eds.). Parque Estadual das Fontes do Ipiranga (PEFI): unidade de conservação que resiste à urbanização de São Paulo São Paulo, Secretaria do Meio Ambiente do Estado de São Paulo.
• Branco, C.C.Z. & Necchi Jr., O. 1996a. Survey of stream macroalgae of eastern Atlantic rainforest of São Paulo State, southeastern Brazil. Archiv für Hydrobiologie 112(80): 35-57.
• Branco, C.C.Z. & Necchi Jr., O. 1996b. Distribution of stream macroalgae in the eastern Atlantic rainforest of São Paulo State, southeastern Brazil. Hydrobiologia 333: 139-150.
• Branco, L.H.Z. & Necchi Jr., O. 1997. Seasonality of macroalgae in three tropical drainage basins in Sao Paulo State, southeastern Brazil. Archiv fur Hydrobiologie 141: 75-91.
• Branco, L.H.Z. & Necchi Jr., O. 1998. Distribution of stream macroalgae in three tropical drainage basins of southeastern Brazil. Archiv für Hydrobiologie 142(2): 241-256.
• Carneiro, M.E.R.; Azevedo, C.; Ramalho, N.M. & Knoppers, B. 1994. A biomassa de Chara hornemannii em relação ao comportamento físico-químico da lagoa de Piratininga (RJ). Anais da Academia Brasileira de Ciências 66(2): 213-222.
• Casanova, M.T. 1994. Vegetative and reproductive responses of Charophytes to water-level fluctuations in permanent and temporary wetlands in Australia. Australia Journal of Marine and Freshwater Research 45: 1409-1419.
• Conti, J.B. & Furlan, S.A. 2003. Geoecologia: o clima, os solos e a biota. In: J.L. Ross (org.). Geografia do Brasil São Paulo, Editora da Universidade de São Paulo.
• Del-Viso, R.P.; Tur, N.M. & Mantovani, V. 1968. Estimación de la biomassa de hidrófitos en cuencas isleñas del Paraná Médio. Physis 28(76): 219-226.
• Fernández-Aláez, M.; Fernández-Aláez, C. & Rodriguez, S. 2002. Seasonal changes in biomass of charophytes in shallow lakes in the northwest of Spain. Aquatic Botany 72: 335-348.
• Golterman, H.L.; Clymo, R.S. & Ohmstad, M.A.M. 1978. Methods for chemical physical and chemical analysis of freshwaters Oxford, Blackwell Scientific Publications.
• Hall, R.I. & Smool, J.P. 1992. A weight-averaging regression and calibration model for inferring total concentration diatoms in British Columbia (Canada) lakes. Freshwater Biology 27: 417-434.
• Hunter, R.D. 1976. Changes in carbon and nitrogen content during decomposition of three macrophytes in freshwater and marine environments. Hydrobiologia 51(2): 119-128.
• Hussain, M.I.; Khoja, T.M. & Guerlesquin, M. 1996. Chemistry, ecology and seasonal succession of charophytes in the Al-Kharaj Irrigation Canal, Saudi Arabia. Hydrobiologia 333: 127-137.
• Mackereth, F.J.H.; Heron, J. & Talling, J.F. 1978. Water analysis: some revised methods for limnologists Cumbria, Freshwater Biological Association.
• Necchi Jr., O. & Branco, C.C.Z. 1999. Phenology of a dioecious population of Bratrachospermum delicatulum (Batrachospermales, Rhodophyta) in a stream from southeastern Brazil. Phycological Research 47: 251-256.
• Necchi Jr., O. & Pascoaloto, D. 1993. Seasonal dynamics of macroalgal communites in the Preto River basin, São Paulo, southeastern Brazil. Archiv für Hydrobiologie 129(4): 231-252.
• Necchi Jr., O.; Pascoaloto, D.; Branco, C.C.Z. & Branco, L.H.Z. 1997. Stream macroalgal flora from the northwest region of São Paulo, southeastern Brazil. Archiv für Hydrobiologie 118(84): 91-112, 1997.
• Necchi Jr., O.; Pascoaloto, D. & Branco, L.H.Z. 1994. Distribution of macroalgae in a tropical river basin from southeastern Brazil. Archiv für Hydrobiologie 129(4): 459-471.
• Palma-Silva, C. 1998. Crescimento e produção de Typha dominguensis Persoon na lagoa Imboassica. In: F.A. Esteves (ed.). Ecologia das lagoas Costeiras do Parque Nacional da Restinga de Jurubatiba e do município de Macaé (RJ) Rio de Janeiro, NUPEM/UFRJ.
• Palma-Silva, C.; Albertoni, E.F. & Esteves, F.A. 2000. Eleocharis mutata (L.) Roem. et Schult. subject to drawdowns in a tropical coastal lagoon, state of Rio de Janeiro, Brazil. Plant Ecology 148: 157-164.
• Palma-Silva, C.; Albertoni, E.F. & Esteves, F.A. 2002. The role of charophyte primary production in a coastal lagoon subjected to human impacts (RJ, Brazil). Acta Limnologica Brasiliensia 14(1): 59-69.
• Picelli-Vicentim, M.M.; Bicudo, C.E.M. & Bueno, N.C. 2004. Flora ficológica do estado de São Paulo, 5: Charophyceae São Carlos, RiMa Editora.
• Shepherd, G.J. 1996. Fitopac 1: manual de usuário Campinas, Universidade Estadual de Campinas.
• Sokol, R.C. & Stross, R.G. 1986. Annual germination window in oospores of Nitella furcata (Charophyceae). Journal of Phycology 22: 403-406.
• Solorzano, L. 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnology and Oceanography 14(5): 799-801.
• Ter-Braak, C.J.F. & Prentice, I.C. 1988. The theory of gradient analysis. Advances in Ecology Research 18: 271-313.
• Valderrama, J.C. 1981. The simmultaneous analysis of total nitrogen and phosphorus in natural waters. Marine Chemistry 10: 109-122.
• Van-den-Hoek, C.; Mann, D.G. & Jahns, H.M. 1996. Algae: an introduction to phycology Cambridge, Cambridge University Press.
• Vieira Jr., J. & Necchi Jr., O. 2002. Microhabitat and plant structure of characean populations in streams of São Paulo State, southeastern Brazil. Cryptogamie, Algologie 23: 51-63.
• Vieira Jr., J. & Necchi Jr., O. 2003. Photosynthetic characteristic of charophytes from tropical lotic ecosystems. Phycological Research 51: 51-60.
• Vieira Jr., J.; Necchi Jr., O.; Branco, C.C.Z. & Branco, L.H.Z. 2002. Characeae (Chlorophyta) de ecossistemas lóticos do estado de São Paulo, Brasil, 1: gênero Nitella Hoehnea 29: 249-266.
• Vieira Jr., J.; Necchi Jr., O.; Branco, C.C.Z. & Branco, L.H.Z. 2003. Characeae (Chlorophyta) de ecossistemas lóticos do estado de São Paulo, Brasil, 2: gênero Chara e distribuição geográfica. Hoehnea 30: 53-70.
• Westlake, D.F. 1965. Some basic data for investigations of the productivity of aquatic macrophytes. Memorie dell'Istituto Italiano di Idrobiologia Dott. Marco de Marchi 18: 229-248.
• Westlake, D.F. 1971. Macrophytes. In: R.A. Vollenveider (ed.). A manual of methods for measuring primary production in aquatic environments Oxford, Blackwell Scientific Publications.
• Wood, R.D. & Imahori, K. 1965. A revision of the Characeae 1: monograph of the Characeae Weinheim, J. Cramer.

Publication Dates

• Publication in this collection
  28 Aug 2006
• Date of issue
  Mar 2006

History

• Accepted
  14 June 2005
• Received
  02 Feb 2004