Phenology of Sirodotia Suecica (Batrachospermaceae, Rhodophyta) in a High-Altitude Stream in Central Mexico

Phycological Research 2009; 57: 118–126

Phenology of Sirodotia suecica (Batrachospermaceae,

Rhodophyta) in a high-altitude stream in central Mexicopre_528 118..126

Javier Carmona,* Miriam Bojorge-García, Yenny Beltrán and Rocio Ramírez-Rodríguez Phycology Laboratory, A. P. 70-620, Faculty of Sciences, National Autonomous University of Mexico (UNAM), Ciudad Universitaria, Coyoacán, 04510, México, D.F.

shaped filaments that produce new gametophytes SUMMARY through vegetative meiosis (Necchi 1991; Necchi et al. 1993; Kumano 2002). The studies of Pascoaloto and The morphology and phenology of a monoecious popu- Necchi (1990), Necchi and Branco (1999), Necchi and lation of Sirodotia suecica Kylin was evaluated season- Vis (2005) and Carmona et al. (2006) are the most ally in a central Mexican fifth-order high-altitude comprehensive investigations of the reproductive stream. Abundance of gametophytes is positively cor- success of each phase of the life-history of Sirodotia related with concentrations of total dissolved solids, species. Umezaki (1960) and Necchi (1991) reported specific conductivity and total ionic concentration; monoecious and/or dioecious populations without any being present the whole dry season and disappearing in clear relation with the environmental situation. In dio- the rainy season. The gametophytes grew in eutrophic ecious populations of Sirodotia delicatula Skuja (as circumstances and particular microhabitat conditions: Batrachospermum delicatulum) the presence of game- high current velocity (66–122 cm s-1), low irradiance tophyte is associated with high irradiance and low tem- (75–263 mmol photons m-2 s-1) and shallow depth perature, and synchronous development of female and (7–26 cm). Percent cover of gametophytes ranged from male thalli results in a higher proportion of fertilized 5–90% and significant differences in abundance were thalli (Necchi & Branco 1999). In contrast, dioecious not observed when alga was present. Some morphologi- populations of Sirodotia huillensis Welwitsch ex G.S. cal and reproductive characteristics seem to be adap- West et West are restricted to waters of low irradiance tations to high current velocity: abundant secondary and high temperature, and exhibits a low female: male branches, spermatangia and carpogonia. ‘Chantransia’ thallus ratio and a low number of carposporophytic stage, microscopic creeping filaments associated with thalli (Carmona et al. 2006). Furthermore, the the base of the gametophyte, were not observed in ‘Chantransia’ stage in Sirodotia suecica and S. huillen- natural conditions. In terms of reproductive success, sis are usually conspicuous and occur in different envi- the population studied can be regarded as highly effi- ronmental conditions throughout the year (Necchi cient, considering the high fertilized carpogonia rate, 1997; Carmona et al. 2006). similar to monoecious populations in lotic habitats. Two species of Sirodotia have been reported for However S. suecica was not common in the study region North America, S. suecica and S. huillensis (Necchi because it was restricted to particular microhabitat et al. 1993; Vis & Sheath 1999; Carmona & Vilaclara conditions. 2007). Sirodotia suecica is distinguished by the gonimoblast initial arising from the non-protuberant side of Key words: Batrachospermaceae, ecology, monoecious, the carpogonia (Necchi et al. 1993; Carmona & phenology, Rhodophyta, Sirodotia suecica, stream. Vilaclara 2007) and S. huillensis has the gonimoblast arising from the protuberant side of the carpogonial base (Carmona et al. 2004). Additionally, development and life history are described in S. huillensis (Carmona INTRODUCTION et al. 2006), and are poorly known in S. suecica. One monoecious population identified as S. suecica has The genus Sirodotia Kylin has the typical vegetative been reported from Mexico (Carmona & Vilaclara 2007) morphology of members of the family Batrachosper- maceae: a uniseriate main axis with four to six pericen- tral cells producing repeatedly branched fascicles of limited growth. It has a heteromorphic triphasic life *To whom correspondence should be addressed. history consisting of a gametophyte (monoecious and/or Email: [email protected] dioecious), which produces spermatangia in clusters, Communicating editor: G. Zuccarello. carpogonia with elongated trichogynes and the Received 14 December 2007; accepted 10 September 2008. ‘Chantransia’ stage (sporophyte) consisting of tuft- doi: 10.1111/j.1440-1835.2009.00528.x

© 2009 Japanese Society of Phycology Phenology of Sirodotia suecica in Mexico 119 and corresponds morphologically and ecologically to the influence of variables at the microhabitat level the description of this species. Sirodotia suecica (current velocity, depth and underwater irradiance) on appears to have a global distribution, being more abun- the vegetative and reproductive characteristics of the dant in temperate climates, neutral to alkaline pH, low population. The sampling site consisted of a stream specific conductance waters and in clean to polluted segment of 58 m2. Each sampling unit was a circle of conditions (Necchi et al. 1993; Carmona & Vilaclara 10 cm radius (area = 314 cm2). Type and size of sam- 2007). Sirodotia suecica has been collected in streams pling units were defined from preliminary tests and from Europe (Kylin 1912; Israelson 1942; Kwandrans previous research (Necchi et al. 1995; Carmona et al. et al. 2002), North America (Flint 1948; Necchi et al. 2006). Sampling consisted of 10 quadrats, each sepa- 1993; Carmona et al. 2004; Carmona & Vilaclara rated by 1 m and its location was determined by a table 2007), Asia (Umezaki 1960; Kumano 1982) and of random numbers. On all sampling dates the micro- Oceania (Entwisle & Foard 1999). However, the sea- habitat characteristics were recorded. Microhabitat sonal dynamics and microhabitat requirements for this variables were measured in situ at the center of each species are virtually unknown. The present investigation sampling unit: current velocity and irradiance were was conducted to describe the phenology and environ- measured as close as possible to the algae, using a mental conditions which favored the occurrence of Swoffer 3100 current velocity meter and a Li-Cor gametophytes based on field monitoring of a population LI-1000 quantum meter with a flat subaquatic sensor of S. suecica in a high-altitude stream from central of photosynthetically active radiation (PAR), respec- Mexico. tively. The number of thalli (gametophytes) within each sampling unit was recorded by visual estimation 2 MATERIALS AND METHODS (Necchi 1997), with a 175 cm viewfinder. ‘Chantran- sia’ stage was not observed in natural conditions, it was The material used in the present study was collected found during microscopic observations of the gameto- from the Amanalco river; a fifth-order stream segment phyte. A description of the ‘Chantransia’ stage was in a mountainous (elevation 1890 m) region of central realized. Thirty thalli were randomly selected (three in Mexico (19°13′N, 100°07′W). Field work was con- each sampling unit) and preserved in 3% formaldehyde ducted from May 2006 to June 2007, including the for subsequent analysis in the laboratory. The following most contrasting parts of the seasonal cycle; that is, the morphological and phenological characteristics were rainy and dry seasons. Three samplings were carried out defined from preliminary tests and previous research: early, in the middle and at end of the dry season: thalli height; number of secondary branches; whorl December, February and May, respectively (December diameter; axial cell length; number of carpogonia, sper- being the coldest month) and two more during the matangia and carposporangia; the ratio of carpogonia: initial and middle parts of the rainy season (June and fertilized carpogonia (Necchi et al. 1993; Necchi September). Temperature and specific conductance 1997; Entwisle & Foard 1999; Necchi & Branco 1999; were measured with a Conductronic (Puebla, Mexico) Carmona & Vilaclara 2007). PC-18 conductivity meter. Dissolved nutrients (30 mL Five replicates were measured in 1 cm of thallus for was filtered in situ with 0.45 and 0.22 mm pore diam- the calculation of secondary branches and 20 for whorl eter membranes and preserved with chloroform and diameter and axial cell length. To avoid inclusion of frozen) were measured in the laboratory with a multi- incompletely developed reproductive structures, the channel analyzer, following standard titration. Water apical region (top 1 cm) was removed (Necchi & Branco samples for dissolved inorganic nitrogen (DIN) and 1999). Segments were squashed prior to examination, soluble reactive phosphorous (SRP) were kept in cold and spermatangia and carposporangia were counted in conditions until analyses were completed (APHA- replicates of five in an area of 50 mm using a microme- AWWA-WPCF 1980). Water samples for determination ter. The number of carpogonia and fertilized carpogonia of anions and pH were preserved frozen in the dark, were counted around the filament. In addition, mac- whereas samples for cations were preserved with 40% roalgae, diatoms and aquatic invertebrates were iden- nitric acid (pH 2–3). Determination of carbonates was tified from each thallus to examine species associations carried out with the titration method, chlorides by the (Merrit & Cummins 1996; Wiggins 1996). An Olympus selective electrode method, hardness with the titration BX51 microscope with a DP12 microphotography method of ethylenediaminetetraacetic acid (EDTA), and system was used for microscopic analyses. To assess Na+ and K+ by the spectrophotometric atomic absorp- significant differences in environmental and morpho- tion method (Greenberg et al. 1985). Observations metric measurements between quadrats at each season were made on natural substrata (boulders) directly in Kruskal–Wallis tests were undertaken. Associations the stream bed. Temporal variations were monitored by among morphometric and reproductive data and micro- the quadrat technique (Necchi et al. 1995; Necchi & habitat variables between five seasons were tested Branco 1999; Carmona et al. 2006) which evaluates using the Spearman correlation coefficient (Gotelli &

Table 1. Physical and chemical characteristics of the segment of the Amanalco river under study

Dry season Rainy season Dry season Dry season Rainy season 31.v.06 26.ix.06 19.xii.06 15.ii.07 07.vi.07

Depth (cm) 10–40 (26) 3–30 (18) 2–15 (7) 6–30 (16) 35–59 (50) Temperature (°C) 15 15 14 16 18 Irradiance (mmol photon m-2 s-1) 9–25 (17) 42–712 (156) 31–901 (263) 14–319 (75) 27–43 (35) Current velocity (cm s-1) 50–240 (122) 29–129 (80) 23–193 (74) 11–123 (66) 33–160 (103) Dissolved oxygen (mg l-1) 7.1 7.8 9.9 7 7.5 Speciﬁc conductance (mScm-1) 236 147 209 210 178 pH 6.7 7.4 6.8 7 6.6

Values are minimum–maximum (mean).

Ellison 2004). Statistics were carried out with the high number of secondary branches (24–28 branches SPSS 12 program. cm-1) and axial cell length (317–341 mm) in May and December showed significant differences (H = 8.7; < -1 RESULTS P 0.05) to February (22 branches cm and 281 mm, respectively). The population of S. suecica occurred under particular Morphometric and environmental correlations found environmental conditions (Tables 1,2). During the dry in this study seemed not to have biological relevance. season, chemical characteristics (pH, total alkalinity, One correlation was found between morphological char- total hardness, calcium, magnesium, sodium and potas- acteristics: in May, a negative correlation was found sium) were consistent with a slightly increased concen- between thalli height and number of secondary tration of total dissolved solids (TDS), chloride, sulfate branches (r = 0.69; P < 0.05). Comparison of repro- and SRP during February. The remaining chemical ductive characteristics of S. suecica in different - variables showed a wider variation (Si-SiO2, N-NO3 , seasons revealed opposite responses. During May (end - + N-NO2 , N-NH4 ). Ionic content was high during the of dry season) the thalli exhibited the highest number of dry season (total ionic concentration: 4.1–4.5 meq l-1, carpogonia (X = 39 Ϯ 3cm-1) and the ratio of carpogo- specific conductance: 209–236 mScm-1, TDS: 143– nia: fertilized carpogonia (X = 9 Ϯ 1cm-1) and the 184 mg l-1) and the lowest during the rainy season (total lowest number of carposporangia (X = 9 Ϯ 2 per ionic concentration: 3.8–4.0 meq l-1, specific conduc- 50 mm2), whereas December and February presented tance: 147–178 mScm-1, TDS: 146–151 mg l-1). the lowest number of carpogonia (X = 18–22 Ϯ Sirodotia suecica occurred in particular microhabitat 1cm-1) and the ratio of carpogonia: fertilized carpogo- conditions: high current velocity (66–122 cm s-1), low nia (X = 2–3 Ϯ 0.1 cm-1) and the highest number of irradiance (17–263 mmol photons m-2 s-1), shallow carposporangia (X = 14–24 Ϯ 1.2 per 50 mm2). All depth (7–26 cm) and with boulders as a substratum thalli were carposporophytic throughout the study. (Table 1, Fig. 1). Kruskal–Wallis test revealed signifi- Length of axial cell showed a positive correlation cant differences for current velocity (H = 27.64; between the number of carposporangia (r = 0.76– P < 0.001), depth (H = 32.95; P < 0.001) and irradi- 0.85; P < 0.05–0.001) and the number of fertilized ance (H = 30.72; P < 0.0) between sampling dates. carpogonia (r = 0.66; P < 0.05) in May and December. Gametophytes were present throughout the dry No significant differences were observed in the number season (Figs 2,3). Percent cover of gametophytes of spermatangia throughout the study (16–40 in ranged from 5% to 90% and significant differences in 50 mm2). abundance were not observed when algae were present. ‘Chantransia’ stage, composed of microscopic creep- Thalli height changed significantly throughout the study ing filaments, was associated with the base of the (H = 15.1; P < 0.001) and was negatively correlated gametophyte, blue-green color, Յ1 mm height, with with the number of secondary branches (r =-0.69; erect and scarcely branched filaments, cylindrical cells P < 0.05) in May. The greatest thalli height values were 7.0–14.5 mm in length (X = 9.5 mm) and 2.5–3.5 mm recorded during February (mean (X) Ϯ standard error in diameter (X = 3 mm), monosporangia 3–4 mm (1 SE) = 5.4 Ϯ 0.4 cm) while the lowest values were length (X = 3.2 mm) and 2.0–3.5 mm in diameter recorded in December (X = 2.8 Ϯ 0.4 cm). Significant (X = 2.8 mm). Later stages of juvenile gametophytes differences (H = 8.7; P < 0.001) were observed in showed the typical uniaxial construction of the Batra- whorl diameter between December and February, with chospermaceae. the highest values in December (X = 274.5 Ϯ 4.8 mm) Sirodotia suecica occurred associated with other and the lowest in February (X = 243.9 Ϯ 4.4 mm). A freshwater Rhodophyceae: Paralemanea mexicana

Table 2. Chemical characteristics of the Amanalco river: Values are given in mg L-1, except where indicated

Dry season Rainy season Dry season Dry season Rainy season

31.v.06 26.ix.06 19.xii.06 15.ii.07 07.vi.07 Mexico in

TDS 143 151 176 184 146

Total alkalinity as CaCO3 78 73 83 80 63 - HCO3 95 89 101 97 77 = CO3 00000 Cl- 6 6.2 6.6 11 9.3 = SO4 696910

Si-SiO2 552 514 578 175 293

Total hardness as CaCO3 70 68 74 77 72 ++ Ca hardness as CaCO3 30 32 31 37 32 ++ Mg hardness as CaCO3 40 36 43 40 40 Ca++ 12 13 12 15 13 Mg++ 109101010 Na+ 13 11 15 17 13 K+ 33344 - - = = - = - = - - = = - - = = - = - = Ionic dominance HCO3 > Cl > SO4 > CO3 HCO3 > SO4 > Cl > CO3 HCO3 > Cl > SO4 > CO3 HCO3 > Cl > SO4 > CO3 HCO3 > SO4 > Cl > CO3 Ca++ > Na+ > Mg++ > K+ Ca++ > Na+ > Mg++ > K+ Na+ > Ca++ > Mg++ > K+ Ca++ > Na+ > Mg++ > K+ Ca++ > Na+ > Mg++ > K+ SRP 4.8 3.5 6.5 6.7 2.4 - N-NO3 45 28 38 26 20 - N-NO2 0.19 0.07 0.16 0.16 0.49 + N-NH4 3 2 2.3 0.19 1.5 DIN4830402622 DIN: SRP ratio 76 67 44 9 91 Total ionic concentration (meq L-1) 4.2 4 4.1 4.5 3.8

DIN, dissolved inorganic nitrogen; SRP, soluble reactive phosphorous; TDS, total dissolved solids. 121 122 J. Carmona et al.

Fig. 1. Current velocity, depth and irradiance in quadrats with Sirodotia suecica. Seasons with the same letter do not signiﬁcantly differ (Kruskal–Wallis test, a = 0.05). n = 10 (X Ϯ 1 SE).

(Kützing) Vis et Sheath and Batrachospermum gelati- reported in North America (10–99 mScm-1) contrast nosum (Linnaeus) De Candolle and several epiphytic with the high values reported in this study (209– and metaphytic diatoms: Achnanthes inflata (Kützing) 236 mScm-1). Grunow in Cleve et Grunow, Amphipleura lindheimeri The relative stability (non-seasonality) of current Grunow, Gomphonema angustum Agardh and Navicula velocity and temperature seems to have an effect on the shroeterii Meister. As well, epiphytic aquatic inverte- high reproductive success of S. suecica, indicated brates of the orders Simulidae (Simulium sp.) and by the occurrence of 100% carposporophytic thalli. Chironomidae were found. Hydropsichidae, Hydrobio- Narrow seasonal variation of water temperature sidae (Atopsyche sp.) and Glossomatidae build cases in observed in this study typically occurs in high-altitude the gametophyte and there was no evidence of damage streams from tropical and subtropical regions (Carmona by them (Fig. 3). A positive correlation was observed et al. 2004). between the number of refugees associated with the On the other hand the absence of gametophytes gametophyte and the percent cover of gametophytes in during the rainy season is associated with the lower December and February (r = 0.66–0.69; P < 0.05). TDS, specific conductivity and total ionic concentration and the increase in temperature. This result is com- DISCUSSION patible with other species of Batrachospermales from temperate climates: B. boryanum Sirodot (Hambrook Sirodotia suecica was collected in similar conditions to & Sheath 1991), B. turfosum Bory (Müller et al. 1997) the previous records in North America: low to moderate and Paralemanea annulata (Kützing) Vis et Sheath temperature (8–18°C), slightly acid pH (5.9–6.8) and (Filkin & Vis 2004). low to fast current velocity (19–106 cm s-1) (Necchi The stream segment presented eutrophic conditions: et al. 1993). However, the low specific conductance SRP, 2.4–6.7 mg l-1; DIN, 22–48 mg l-1 (Dodds

Fig. 2. Percent cover and morphometric values (X Ϯ 1 SE) for seasonal samples of Sirodotia suecica. Seasons with the same letter do not signiﬁcantly differ (Kruskal–Wallis test, a = 0.05). For percent cover n = 10, height thalli n = 30, number of secondary branches n = 150, whorl diameter and axial cell length n = 600.

Fig. 3. Reproductive characteristics and number of insect refugees (X Ϯ 1 SE) for seasonal samples of Sirodotia suecica. Seasons with the same letter do not signiﬁcantly differ (Kruskal–Wallis test, a = 0.05). For all reproductive variables n = 30.

2003). In Mexico, S. suecica has been collected with ing with Sheath and Hambrook (1990) abundance of other red algae, Paralemanea mexicana, in similar con- branches (dense growth forms) can reduce drag force ditions (Carmona & Vilaclara 2007). at high current. In addition the abundance of sper- Some characteristics of S. suecica seem to be matangia and carpogonia it’s a probable alternative adaptations to high current velocity: abundant second- strategy to increase fertilization success (Necchi ary branches, spermatangia and carpogonia. Accord- 1997).

The monoecious condition favors self-fertilization N.E. Ceniceros B. and O. Cruz R. (IGeof-UNAM) for (Necchi & Vis 2005) and individuals tend to be major ion analyses; to M. Cartagena and J. Ramírez homozygous at most loci, nevertheless this type of Lynn for fieldwork help, to David Adams for English breeding system confers a reproductive advantage and review and to the Posgrado en Ciencias Biológicas, often leads to a large number of morphologically dis- Universidad Nacional Autónoma de México. JCJ tinguishable microspecies (Hawkes 1990; Müller et al. received financial support by Research Grant PAPIIT 1997; Vis & Sheath 1997, 1999). The character of (209107) and CONACyT (52386). monoecious versus dioecious thalli does not distinguish between taxa because mixed monoecious and dioecious REFERENCES populations of S. delicatula (Necchi 1991; Vis & Sheath 1999) and S. suecica (Flint 1948; Entwisle & APHA-AWWA-WPCF. 1980. Métodos normalizados para el Foard 1999) have been reported in the same or differ- análisis de aguas potables y residuales. Ediciones Días de ent environments. Santos, Madrid, 1816 pp. In our field study, the ‘Chantransia’ stage of S. Cantoral, U. E., Carmona, J. and Montejano, G. 1996. suecica was microscopic in contrast to S. delicatula Diatoms of calcareous tropical springs in the central region and S. huillensis that has a macroscopic ‘Chantransia’ of Mexico. Crypt. Algol. 18: 19–46. stage (0.1–1.5, 0.4–1.0 cm, respectively) (Necchi Carmona, J. and Vilaclara, F. G. 2007. Survey and distribution 1991; Necchi & Carmona 2002; Carmona et al. 2006). of Batrachospermaceae (Rhodophyta) in tropical high- The juvenile gametophyte in S. suecica may form a altitude streams from central Mexico. Crypt. Algol. 28: system of rhizoidal filaments or a cluster of cells, which 271–82. produce new gametophytes (i.e. clonal reproduction) Carmona, J., Montejano, G. and Necchi, O. Jr. 2006. Ecology similar to what is observed in S. delicatula in culture and morphological characterization of gametophyte and (Necchi & Carmona 2002). In contrast the ‘Chantran- ‘Chantransia’ stages of Sirodotia huillensis (Batrachosper- sia’ stage in S. huillensis originates haploid dome- males, Rhodophyta) from a stream in central Mexico. shaped structures that precede the development of new Phycol. Res. 54: 108–15. gametophytes (Carmona et al. 2006). Carmona, J. J., Montejano, G. and Cantoral, U. E. 2004. The In terms of associated species, the occurrence of S. distribution of Rhodophyta in streams of Central Mexico. suecica in this study corresponded with the presence Arch. Hydrobiol. Algol. Stud. Suppl. 114: 39–52. of Paralemanea mexicana and B. gelatinosum, a group Dodds, W. K. 2003. Misuse of inorganic N and soluble reac- of temperate species (Kwandrans et al. 2002) and tive P concentrations to indicate nutrient status of surface diatoms typical for alkaline waters (Cantoral et al. waters. J. N. Am. Benthol. Soc. 22: 171–81. 1996). Sirodotia suecica was frequently colonized by Entwisle, T. J. and Foard, H. J. 1999. Sirodotia (Batrachos- Simulidae and Chironomidae, similar to previous permales, Rhodophyta) in Australia and New Zealand. records from North America (Sheath et al. 1996). Aust. Syst. Bot. 12: 604–13. However in the present study, we have found no evi- Filkin, N. R. and Vis, M. L. 2004. Phenology of Paralemanea dence of damage in the gametophyte, only the forma- annulata (Lemaneaceae, Rhodophyta) in a Ohio woodland tion of refugees in the surface. Apparently these larvae stream. Hydrobiologia 518: 159–68. of Diptera use the red algae for case making and as a Flint, L. H. 1948. Studies of fresh-water red algae. Am. J. refugium in fast current velocities during its final larvae Bot. 35: 428–33. stage, similar to other species of invertebrates (Sheath Gotelli, N. J. and Ellison, A. M. 2004. A Primer of Ecological & Hambrook 1990). Statistics. Sinauer Associates, Inc., Massachusetts, 492 Efficient reproductive strategies of S. suecica found pp. in this study can be interpreted as adaptations to suc- Greenberg, A. E., Trussell, R. R. and Clesceri, L. S. 1985. cessfully colonize streams, covering up to 90% of the Standard Methods for the Examination of Water and Waste Amanalco stream segment in the period from early Water, 16th edn. American Public Health Association winter to early summer, in concordance with several (APHA), Washington DC, 1269 pp. freshwater red algae in streams of North America Hambrook, J. A. and Sheath, R. G. 1991. Reproductive (Sheath & Burkholder 1985; Hambrook & Sheath ecology of the freshwater red alga Batrachospermum bory- 1991; Filkin & Vis 2004). However, it is not common in anum Sirodot in a temperate headwater stream. Hydrobio- the study region because it is restricted to particular logia 218: 233–46. microhabitat conditions. Hawkes, M. W. 1990. Reproductive strategies. In Cole, K. M. and Sheath, R. G. (Eds) Biology of the Red Algae. Cam- ACKNOWLEDGMENTS bridge University Press, Cambridge, pp. 455–76. Israelson, G. 1942. The freshwater Florideae of Sweden: The authors are indebted to S. Castillo and J. Ramírez studies on their taxonomy, ecology and distribution. Symb. (ICMyL-UNAM) for nutrient analyses; to A. Aguayo Ríos, Bot. Upsal. 6: 1–135.

Kumano, S. 1982. Development of carpogonium and taxonomy Necchi, O. Jr., Sheath, R. G. and Cole, K. M. 1993. Distri- of six species of the genus Sirodotia, Rhodophyta from bution and systematics of the freshwater genus Sirodotia Japan and West Malaysia. Bot. Mag. Tokyo 95: 125–37. (Batrachospermales, Rhodophyta) in North America. J. Kumano, S. 2002. Freshwater Red Algae of the World. Bio- Phycol. 29: 236–43. press Limited, Bristol, UK, 375 pp. Necchi, O. Jr., Branco, L. H. Z. and Branco, C. C. Z. 1995. Kwandrans, J., Eloranta, P. and Bengtsson, R. 2002. Sötvat- Comparison of three techniques for estimating periphyton tensensrödalger I Sverige – en översikt och ett nyfynd. abundance in bedrock streams. Arch. Hydrobiol. 134: Svensk Bot. Tidsk. 96: 274–80. 393–402. Kylin, H. 1912. Studien über die schwedischen Arten der Pascoaloto, D. and Necchi, O. Jr. 1990. Seasonal variation of Gattungen Batrachospermum Roth und Sirodotia nov. gen. Sirodotia delicatula Skuja (Rhodophyta, Batrachosper- Nova Acta Regiae Soc. Sci. Upsal. Ser. 4 (3), 1–40. maceae) in a small stream from São Paulo State, south- Merrit, R. and Cummins, K. 1996. An Introduction to the eastern Brazil. Rev. Bras. Biol. 50: 37–44. Aquatic Insects of North America, 3rd edn. Kendall/Hunt, Sheath, R. G. and Burkholder, J. M. 1985. Characteristics of Iowa, 862 pp. soft-water streams in Rhode Island. 2. Composition and Müller, K. M., Vis, M. L., Chiasson, W. B., Whittick, A. and seasonal dynamics of macroalgal communities. Hydrobio- Sheath, R. G. 1997. Phenology of a Batrachospermum logia 128: 109–18. population in a boreal pond and its implications for the Sheath, R. G. and Hambrook, J. A. 1990. Freshwater ecology. systematics of section Turfosa (Batrachospermales, Rhodo- In Cole, K. M. and Sheath, R. G. (Eds) Biology of the Red phyta). Phycologia 36: 68–75. Algae. Cambridge University Press, Cambridge, pp. 423– Necchi, O. Jr. 1991. The section Sirodotia of Batrachosper- 53. mum (Rhodophyta, Batrachospermales) in Brazil. Arch. Sheath, R. G., Müller, K. M., Colbo, M. H. and Cole, K. M. Hydrobiol. Algol. Stud. Suppl. 62: 17–30. 1996. Incorporation of freshwater Rhodophyta into the Necchi, O. Jr. 1997. Microhabitat and plant structure of cases of chironomid larvae (Chironomidae, Diptera) from Batrachospermum (Batrachospermales, Rhodophyta) North America. J. Phycol. 32: 949–52. populations in four streams of São Paulo State, southeast- Umezaki, I. 1960. On Sirodotia delicatula Skuja from Japan. ern Brazil. Phycol. Res. 45: 39–45. Acta Phytotax. et Geobot. 18: 208–14. Necchi, O. Jr. and Branco, C. C. Z. 1999. Phenology of a Vis, M. L. and Sheath, R. G. 1997. Biogeography of Batra- dioecious population of Batrachospermum delicatulum chospermum gelatinosum (Batrachospermales, Rhodo- (Batrachospermales, Rhodophyta) in a stream from south- phyta) in North America based on molecular and eastern Brazil. Phycol. Res. 47: 251–6. morphological data. J. Phycol. 33: 520–6. Necchi, O., Jr. and Carmona, J. J. 2002. Somatic meiosis and Vis, M. L. and Sheath, R. G. 1999. A molecular investigation development of the gametophyte in Batrachospermales of the systematic relationships of Sirodotia species (Batra- sensu lato. Phycologia 41: 340–7. chospermales, Rhodophyta) in North America. Phycologia Necchi, O., Jr. and Vis, M. L. 2005. Reproductive ecology of 38: 261–6. freshwater red alga Batrachospermum delicatulum (Batra- Wiggins, G. 1996. Larvae of the North America Caddisﬂy chospermales, Rhodophyta) in three tropical streams. Genera (Trichoptera). University of Toronto Press, Toronto, Phycol. Res. 53: 194–200. 457 pp.