Photosynthetic characteristics of the freshwater red alga Batrachospermum delicatulum (Skuja) Necchi & Entwisle

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Phenology of a dioecious population of Batrachospermum delicatulum (Batrachospermales, Rhodophyta) in a stream from southeastern Brazil

The seasonal dynamics of a dioecious population of Batrachospermum delicatulum (Skuja) Necchi and Entwisle was evaluated biweekly during the growth period of the macroscopic gametophyte, from late autumn (May) to early spring (October) in a third-order stream from the northeast region of Sao Paulo State, southeastern Brazil (20°43'S, 49°13'W). The population fluctuated throughout the study period in terms of percentage cover, frequency and chlorophyll content. Percent cover and frequency showed a clear pattern with the lowest values at the initial and final stages of the growth period and the highest in July-August (winter). Gametophyte growth was associated with high illumination and low temperature, which agrees with most observations on Batrachospermales in stream environments. Relatively wide variations in reproductive characteristics were observed during the growth period, which were not correlated with percentage cover, frequency and chlorophyll content. The phenologic pattern observed in this population was characterized by a synchronic development of female/male plant ratio with the number of spermatangia per plant resulting in. (i) a higher proportion of fertilized (carposporophytic) plants associated with more male plants; (ii) higher fertilization rates during the periods with higher production of spermatangia per plant; and (iii) higher production of spermatangia per plant when the population had more male plants. These characteristics were largely associated with water temperature and ion content. In terms of reproductive success, the population studied can be regarded as highly efficient, considering the relatively low proportion of male to female plants and high fertilization rates. These data are consistent with a hypothesis to explain high fertilization rates in dioecious species in lotic habitats consisting of outcrossing among adjacent plants with intermingled male and female branches within an algal cluster. Efficient reproductive strategies have been reported in dioecious, monoecious and even mixed populations of B. delicatulum and can be interpreted as adaptations to successfully colonize streams with different characteristics.

Reproductive ecology of the freshwater red alga Batrachospermum delicatulum (Batrachospermales, Rhodophyta) in three tropical streams

Batrachospermum delicatulum specimens from three stream segments were analyzed from a tropical region in south-eastern Brazil (20°18′- 20°49′S, 49°13′-49°46′W). Physical and chemical parameters and the spatial placement of thalli were investigated along with the reproductive characteristics of the gametophytic phase. Sequence data of the cox 2-3 spacer region was also utilized to evaluate genetic variation in individuals within and among stream segments. Gametophyte occurred under relatively diverse environmental conditions, whereas thalli abundance was weakly or not correlated to environmental variables within the stream segments. All specimens examined were dioecious. The ratio of male/female plants was relatively low (0.5 to 1.3) and male plants tended to occur as clumps (two or three plants together). High reproductive success was observed, as indicated by the occurrence of 100% fertilized (carposporophytic) female plants. This is similar to previous reports for this and other dioecious species, which is remarkable considering the relatively low proportion of male/female plants. Results support the two hypotheses to explain the high reproductive success in dioecious species. The occurrence of male plants in clumps was evidence for a strict spatial relationship (i.e. male plants located in upstream position of female plants in order to release spermatia, which would be carried by eddies through female plants). In contrast, the occurrence of male and female plants adjacent to each other allowed outcrossing among neighboring plants with intermingled male and female branches, which seemed more applicable to some situations (low turbulence habitats). The cox 2-3 spacer region from the 18 individuals sequenced was 376 bp and the DNA sequence was identical with no base pair substitutions. Likewise, a previous study of another Batrachospermum species showed that the same haplotypes were present in all stream segments from the same drainage basin, even though the stream segments were a considerable distance apart. Short distance dispersal either by small birds or waterway connectivity might explain these findings.

Respostas de curto período das características fotossintéticas da alga vermelha Batrachospermum delicatulum a temperatura e irradiância

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Microhabitat and plant structure of Batrachospermum (Batrachospermales, Rhodophyta) populations in four streams of São Paulo State, southeastern Brazil

Microhabitat and plant structure of seven Batrachospermum populations (four of Batrachospermum delicatulum (= Sirodotia delicatula), one of Batrachospermum macrosporum and two of the 'Chantransia' stage), including the influence of physical variables (current velocity, depth, irradiance and substratum), were investigated in four streams of São Paulo State, southeastern Brazil. The populations of B. delicatulum and the 'Chantransia' stage occurred under very diverse microhabitat conditions, which probably contributes to their wide spatial and seasonal distribution in Brazilian streams. Results suggest branch reconfiguration as a probable mechanism of adaptation to current velocity based on the occurrence of: (i) B. macrosporum (a large mucilaginous form with presumably little ability for branch reconfiguration) under lower current velocity than B. delicatulum; (ii) only dense plants in populations with high current velocities (> 60 cm s-1), whereas 53-77% of dense plants were seen in populations exposed to lower currents (< 40 cm s-1); (iii) positive correlations of plant length with internode length in populations under low current velocities and negative correlation in a population with high velocity (132 cm s-1); and (iv) negative correlations of current velocity with plant diameter and internode length in a population under high flow. This study, involving mainly dioecious populations, revealed that B. delicatulum displayed higher fertilization rates than B. macrosporum. A complementary explanation for a dioecious species to increase fertilization success was proposed consisting of outcrossing among intermingled male and female adjacent plants within an algal spot.

Distribution of Rhodophyta in streams from São Paulo State, southeastern Brazil

Distribution of Rhodophyta was investigated in 172 stream segments, which were sampled from May to October in 1992-1993 and 1996-1997 in six natural regions (parts of biomes or geological areas) of São Paulo State, southeastern Brazil. Red algae occurred in 60.5 % of stream segments sampled, a high frequency in comparison with other major surveys in the world (18-65 %). 17 species of freshwater red algae were found, of which the most widespread was Batrachospermum delicatulum occurring in 17 sites of five regions. The proportion of morphological types was as follows: gelatinous filaments (62.5 %), free filaments (19 %), tufts (12.5 %) and crusts (6 %); all but free filaments can be considered as having mechanisms to tolerate stress provoked by current velocity. No significant difference was found between the frequency distributions of variables measured for all streams and for those with red algae. Rhodophyta occurred under the following conditions (means): temperature (19.0 degrees C), current velocity (48 cm s(-1)), specific conductance (74 mu S cm(-1)), turbidity (8 NTU), oxygen (67.3 %) and pH (6.9 +/- 0.7). on the basis of species composition among the regions, the following patterns were evident: 1) the number of red algal species per region ranged from 1 to 10; 2) the highest proportion of sites with red algae (65-73 %) was found in hard water regions and in Atlantic rainforest, whereas the lowest (50 %) was found in tropical rainforest; 3) more than half of the species were exclusive from a single region, whereas the higher proportion of exclusive species was in the subtropical rainforest (50 %). No combination of stream variables was clearly associated with the occurrence of red algae for the regions as a whole. Species composition for streams and rivers of São Paulo State revealed higher similarities with other tropical regions and had few species in common with freshwater red algal floras of other continents.

Short-term successional dynamics of a macroalgal community in a stream from northwestern São Paulo State, Brazil

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Light-related photosynthetic characteristics of freshwater rhodophytes

Photosynthetic characteristics in response to irradiance were analysed in 21 field and culture populations of thirteen freshwater red algal species applying two distinct techniques (chlorophyll fluorescence and oxygen evolution). Photosynthesis-irradiance (PI) curves indicated adaptations to low irradiances in all species analysed, essentially characterized by occurrence of photoinhibition, low values of the saturation parameter (I-k < 225 mu mol m(-2) s(-1)) and compensation irradiance (I-c < 20 mu mol m(-2) s(-1)) and relatively high values of the effective quantum yield of photosystem II (Delta F/F'(m) >= 45). These characteristics have been reported in freshwater red algae and were confirmed from data based on the two techniques, indicating they are typically shade-adapted plants. on the other hand, some species (e.g. Batrachospermum delicatulum) can tolerate high irradiances (up to 2400 mu mol m(-2) s(-1)), suggesting they have mechanisms that enable them to avoid photodarnage of the photosynthetic apparatus. One of these mechanisms is the increase in dissipation of excessive energy captured by reaction centres after exposure to continuous irradiance, as reflected by the non-photochemical quenching fluorescence parameter in dark/light induction curves. Photo-inhibition occurred in all algae tested by both techniques. Light acclimation was evident particularly in field populations, as revealed by lower values of the saturation parameter (Ik) and the compensation irradiance (I-c) and higher values of Delta F/F'(m) in algae under low irradiances (shaded or heavily shaded stream segments), and vice-versa. Forms living within the boundary layer (e.g. crusts), in a region of reduced current velocity, tended to be more shade-adapted than semi-erect plants (e.g. non-mucilaginous or mucilaginous filaments), as indicated by highest values of photosynthetic efficiency (alpha = 0.31) and effective quantum yield (Delta F/F'(m) = 0.88) under natural conditions. Higher photo- synthetic rates (P-max) for the same species or population were observed under culture than field conditions when measured with the oxygen evolution technique, whereas the opposite trend was observed using chlorophyll fluorescence. (c) 2005 Elsevier B.V. All rights reserved.

DISTRIBUTION AND SEASONAL DYNAMICS OF RHODOPHYTA IN THE PRETO RIVER BASIN, SOUTHEASTERN BRAZIL

Distribution and seasonal dynamics of freshwater Rhodophyta were investigated in the Preto River basin, located in northwestern São Paulo State, southeastern Brazil. Twenty-two sites were sampled, six monthly during one year, four bimonthly during two years, and 12 twice (hot-rainy and cool-dry seasons) during the study period (May 1989 through March 1991). Red algal representatives were found in 19 sites (86.4%). Four species occurred in the basin with varying frequencies: Batrachospermum delicatulum (54.5%), Compsopogon coeruleus (36.4%), B. bicudoi (13.6%) and B. virgatum (4.5%). In addition, 'Chantransia' stage of the batrachospermalean species was found in 17 sites (77.3%). B. bicudoi, B. virgatum and C. coeruleus occurred only in large stream segments (greater-than-or-equal-to 3-order), generally in the main river, whereas B. delicatulum was more frequent in small streams (less-than-or-equal-to 3-order). The stream variables most closely related to the species distribution in the basin were specific conductance, pH and oxygen. B. bicudoi and B. delicatulum showed a marked seasonality: gametophytes were observed from late fall to early spring, while the 'Chantransia' stage generally occurred throughout the year. C. coeruleus was observed throughout the year in most sites, but the populations were generally more abundant from late fall to early spring. The combination of lower temperature and reduced turbidity resulting in increased illumination to the benthic algae during the dry winter months promotes the gametophytic growth of the batrachospermalean species, whereas current velocity was found to be the most influential stream variable for C. coeruleus. The persistance of the 'Chantransia' stage throughout the year as well as its tolerance to wider environmental conditions are key factors in the efficiency of the batrachospermalean life history strategy in lotic ecosystems.

Effects of temperature, irradiance and photoperiod on growth and pigment content in some freshwater red algae in culture

The responses of relative growth rate (% day-1) and pigment content (chlorophyll a, phycocyanin and phycoerythrin) to temperature, irradiance and photoperiod were analyzed in culture in seven freshwater red algae: Audouinella hermannii (Roth) Duby, Audouinella pygmaea (Kützing) Weber-van Bosse, Batrachospermum ambiguum Montagne, Batrachospermum delicatulum (Skuja) Necchi et Entwisle, 'Chantransia' stages of B. delicatulum and Batrachospermum macrosporum Montagne and Compsopogon coeruleus (C. Agardh) Montagne. Experimental conditions included temperatures of 10, 15, 20 and 25°C and low and high irradiances (65 and 300 μmol photons m-2 s-1, respectively). Long and short day lengths (16:8 and 8:16 LD cycles) were also applied at the two irradiances. Growth effects of temperature and irradiance were evident in most algae tested, and there were significant interactions among treatments. Most freshwater red algae had the best growth under low irradiance, confirming the preference of freshwater red algae for low light regimens. In general there was highest growth rate in long days and low irradiance. Growth optima in relation to temperature were species-specific and also varied between low and high irradiances for the same alga. The most significant differences in pigment content were related to temperature, whereas few significant differences could be attributed to variation in irradiance and photoperiod or interactions among the three parameters. The responses were species-specific and also differed for pigments in distinct temperatures, irradiances and photoperiods in the same alga. Phycocyanin was generally more concentrated than phycoerythrin and phycobiliproteins were more concentrated than chlorophyll a. The highest total pigment contents were found in two species typical of shaded habitats: A. hermannii and C. coeruleus. The expected inverse relationship of pigment with irradiance was observed only in C. coeruleus. In general, the most favorable conditions for growth were not coincident with those with highest pigment contents.

Respostas fisiológicas de duas espécies de algas vermelhas continentais ao empobrecimento de fósforo e nitrogênio inorgânicos

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Distribution of stream macroalgae in the northwest region of Sao Paulo State, southeastern Brazil

Forty-four stream segments were sampled from May to October in 1992 and 1993 in the northwest region of São Paulo State, southeastern Brazil (19 degrees 45'-21 degrees 25'S, 49 degrees 05'-51 degrees 30'S). Thirty-six macroalgal subgeneric taxa were found and Chlorophyta was the dominant algal group (47% species), followed by Cyanophyta (33.5%), Rhodophyta (14%) and Chrysophyta (5.5%). The most widespread species were Stigeoclonium helveticum (25% sites), Batrachospermum delicatulum and Compsopogon coeruleus (20.5%). Distribution was patchy, with species number per sampling site ranging from 0 to six (3.1 +/- 1.7) and correlated positively with species abundance. Species cover ranged from 0 to 61% of the stream bottom (19.1 +/- 19.7%). Most sites (57%) were dominated by one or two macroalgae species. No significant difference was found between the frequency distribution of variables measured for streams and for total macroalgae, but the most widespread species differed for most parameters and occurred over wider ranges of environmental conditions. Mean species number and abundance were close to values found in distinct regions or biomes of North America. Higher conductance and lower oxygen values, as well as rocky substrata, generally constituted the most favourable combination of conditions for the development of macroalgae in the region. The pattern of strong dominance of few species was considered to be typical for stream macroalgal communities in general.

THE SECTION SIRODOTIA OF BATRACHOSPERMUM (RHODOPHYTA, BATRACHOSPERMACEAE) IN BRAZIL

The taxonomy, distribution and ecology of Section Sirodotia of Batrachospermum in Brazil is studied. Only one species, B. delicatulum (SKUJA) NECCHI & ENTWISLE, was recognized. This species presents a wide range of morphological features, occurs in a number of distinct habitats and environmental conditions and is widely distributed in Brazil. A full account of the species taxonomy is given and the synonyMy of B. ateleium comb. nov. SKUJA is confirmed. Two growth forms (dense and open) were found in the Brazilian specimens, but they were not treated as different taxa because a continuous range was observed between them. Two morphological features were proposed for species delineation: early development of gonimoblast and presence of specialized spermatangial branches. Three distinct groups of Sirodotia species can be recognized on the basis of these criterions: B. delicatulum (gonimoblast initial arises from a semiglobular protuberance of the carpogonium), B. suecicalum KYLIN (gonimoblast initial arises from the non-protuberant side of the carpogonium) and B. segawae KUMANO and B. yutakae KUMANO (with specialized spermatangial branches).

Distribution of stream macroalgae in three tropical drainage basins of southeastern Brazil

Three drainage basins belonging to different drainage systems, but in close proximity, were evaluated to compare the distribution of macroalgal communities in the northwest region of São Paulo State, southeastern Brazil. Monthly samplings were carried out from September 1992 through September 1993 in three sites along the main river of each basin. 10 m length cross segments were evaluated for species per cent cover and richness, on both the population and community levels. Selected stream variables were measured: specific conductance, temperature, turbidity, mean cross-sectional area of the reach, current velocity, pH, and oxygen saturation (%). Principal Coordinate Analysis (PCO), chi-square good-of-fitness, and Pearson Product-Moment correlation coefficient were applied to evaluate the distribution of the macroalgal species. The survey resulted in 36 taxa of macroalgae, of which Cyanophyta was the dominant group (17 taxa or 41.7% of the total), followed by Chlorophyta (15 taxa or 41.7%), Rhodophyta (3 taxa or 8.3%) and Chrysophyta (1 taxon or 2.8%). Stigeoclonium helveticum, 'Chantransia' stage of Batrachospermum spp., and B. delicatulum were the most widespread and frequent macroalgae throughout the basins. The analyses showed that conductance and current velocity were the factors most closely related to the distribution of the macroalgal species. Positive correlation between richness and percent cover was determined, which reinforces the patchiness of stream macroalgal distribution.

Phylogeography of Batrachospermum macrosporum (Batrachospermales, Rhodophyta) from North and South America

Phylogeographic trends in Batrachospermum macrosporum Mont. were investigated using the mitochondrial intergenic spacer between the cytochrome oxidase subunit 2 and 3 genes (cox2-3). A total of 11 stream segments were sampled with seven in the coastal plain of North America and four in tropical areas of South America. Fifteen thalli were sampled from seven streams, 14 thalli from two streams, and eight thalli from two streams. There were 16 haplotypes detected using 149 individuals. of the eight haplotypes from locations in North America, all were 334 base pairs (bp) in length, and of those from South America, five were 344 bp, and three were 348 bp. Two individual networks were produced: one for the haplotypes from North America and another for those from South America, and these could not be joined due to the large number of base pair differences. This split between haplotypes from North and South America was confirmed with sequence data of the rbcL gene. There was very little genetic variation among the haplotypes from the North American locations, leading us to hypothesize that these are fairly recent colonization events along the coastal plain. In contrast, there was high variation among haplotypes from South America, and it would appear that the Amazon serves as a center of diversity. We detected considerable variation in haplotypes among streams, but frequently, a single haplotype in an individual stream segment, which is consistent with data from previous studies of other batrachospermalean taxa, may suggest a single colonization event per stream.