Phenology of Paralemanea Mexicana (Batrachospermales, Rhodophyta) in a High-Altitude Stream in Central Mexico

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Phycological Research 2014; 62: 86–93

Phenology of Paralemanea mexicana (Batrachospermales, Rhodophyta) in a high-altitude stream in central Mexico

Javier Carmona Jiménez,* Miriam Guadalupe Bojorge García and Rocío Ramírez Rodríguez Ecology and Natural Sources, Faculty of Sciences, National Autonomous University of Mexico (UNAM), Ciudad Universitaria, Coyoacan, CP 04510, Mexico

that could be linked to unidirectional current velocity SUMMARY For example, morphological adaptation related with the formation of rhizoidal filaments, or aggregation of The morphology and phenology of Paralemanea filaments, from which an efficient attachment system mexicana (Kützing) Vis et Sheath was evaluated sea- is produced (Carmona et al. 2009); abundance of sonally in a fifth order high-altitude stream in central branches or dense growth forms can reduce drag force Mexico. The gametophytes grew during oligotrophic (Sheath & Hambrook 1990); and presence of large and eutrophic conditions, and during particular amounts of mucilage surrounding the thallus (Carmona microhabitat conditions: high current velocity (40– et al. 2006). As reproductive adaptations are somatic 240 cm s−1), low to medium irradiance (5–973 μmol meiosis, clonal multiplication in the ‘Chantransia’ stage photons m−2 s−1), and shallow depth (1–30 cm). The (Sheath 1984; Necchi & Carmona 2002) and abun- abundance of gametophytes was positively correlated dant spermatangia and carposporangia small in size with low temperature, high current velocity and concen- (Carmona et al. 2009). Therefore, in the lotic ecosys- trations of soluble reactive phosphorus. Interestingly, tems, water flow can be considered the environmental monoecious gametophytes formed two types of parameter that is most important to the development of branches, true branches with sympodial pattern origi- the gametophyte, reproduction, and evolutionary adap- nating from meristematic cells in variable number, and tations of these algae. abundant false branches produced during the develop- Traditionally, the genus Paralemanea was placed in ment of the ‘Chantransia’ stage in the surface of the the family Lemaneaceae (Vis & Sheath 1992); however, gametophyte or by uniseriate filaments arising within using molecular data, Entwisle et al. (2009) proposed a the thallus lumen. These filaments generally produce major revision of Batrachospermales and amended the gametophytes and suggest that they could support the circumscriptions of the family Batrachospermaceae to germination of carpospores. The frequently whorled include Lemaneaceae and Psilosiphonaceae. The genus branches are the result of a false branching pattern Paralemanea genera was retained pending further and are exclusive to P. mexicana. These morpholo- investigation, noting the possibility that Paralemanea is gical and reproductive characteristics appear to be paraphyletic in relation to Lemanea (Vis et al. 1998; biomechanical adaptations to avoid detachment and Kapraun et al. 2007; Entwisle et al. 2009). increase reproductive success. Efficient reproductive Paralemanea has a pseudoparenchymatous tube strategies of P. mexicana observed in this study can be construction, with interwoven medullary filaments interpreted as adaptations to successfully colonize absent (Sheath et al. 1996a). Three species of streams; however, these features may not have been Paralemanea have been recognized for North America, common in the study region due to restricted P. annulata (Kützing) M.L. Vis et Sheath, P. catenata microhabitat conditions and geographic isolation. (Kützing) M.L. Vis et Sheath and P. mexicana (Kützing) M.L.Vis et Sheath (Vis et al. 1992). Species delineation Key words: Batrachospermales, ecology, Paralemanea is based on the thallus length and frequency of mexicana, phenology, Rhodophyta, stream. branches, and P. mexicana is characterized by a whorled branch and rebranching pattern. This species is localized in high mountain streams in central Mexico, INTRODUCTION The red algal orders Batrachospermales is a conspicu- ous group of freshwater Rhodophyta that occurs widely *To whom correspondence should be addressed. in lotic ecosystems throughout the world (Sheath & Email: [email protected] Hambrook 1990) and appear to be highly specialized Communicating editor: J. H. Kim. to these ecosystems. Batrachospermalean taxa have Received 5 July 2012; accepted 14 September 2013. several morphological and reproductive adaptations doi: 10.1111/pre.12042

© 2013 Japanese Society of Phycology Phenology of Paralemanea mexicana 87 geographically isolated from the other species of the (Puebla, Mexico) PC-18 conductivity meter. Temporal genus (Vis et al. 1992). Some studies of the reproduc- variations were monitored by the quadrat technique tive success and life-history of Paralemanea species (Necchi et al.1995),whichevaluatestheinfluenceof have been conducted in North America (Filkin & Vis variables at the microhabitat level (current velocity, depth 2004) and the Iberian Peninsula (Carmona et al. and underwater irradiance) on the vegetative and repro- 2011). Paralemanea annulata gametophytes start to ductive characteristics of the population. Each sampling grow in winter, reproduce in spring, and release date consisted of a stream segment of 10 m long. The carpospores in early summer. The gametophytes disap- sampling size consisted of five quadrats, each separated pear during low water and increased temperature con- by 2 m. Each sampling quadrat was a circle of 10 cm ditions; environmental parameters that influence the radius; random numbers between 0 and 180° determined phenological characteristics include current velocity, their locations. The individuals were collected from the water depth, light intensity, water temperature and the middle of the sampling unit. presence of epiphytic Audouinella sp. (Filkin & Vis 2004). The gametophyte of P. catenata is present Chemical analyses throughout the year, with the highest population cover in winter and the release of carpospores in the spring Dissolved nutrients were sampled by filtering 30 mL of and summer (Carmona et al. 2011). Similar ecological stream water through 0.45 and 0.22 μm pore diameter requirements, such as water temperature and current membranes (in situ). Samples were preserved with velocity, were noted for both populations and seemed to chloroform and frozen until measured in the laboratory, play a role in the phenology of these Paralemanea with a multichannel analyzer following standard titra- populations; however, no one environmental parameter tion. Samples for dissolved inorganic nitrogen (DIN) was observed to be most influential (Carmona et al. and soluble reactive phosphorous (SRP) were kept in 2011; Filkin & Vis 2004). Several factors were hypoth- cold conditions until analyses were completed (APHA esized to interact during the trigger events of the et al. 1980). Water samples for determination of anions phenology of P. annulata (Filkin & Vis 2004). and pH were preserved frozen in the dark; samples for Paralemanea mexicana has been collected in several cations were preserved with 40% nitric acid (pH 2–3). streams from high mountain and temperate waters from Determination of carbonates was performed using central Mexico (Carmona & Necchi 2002; Bojorge et al. the titration method, chlorides by the selective 2010). However, the ecology is poorly known and there electrode method, hardness by the titration method + + has been no characterization of gametophytes season- with ethylenediaminetetraacetic acid, and Na and K ally. The present investigation, based on seasonal by the spectrophotometric atomic absorption method observations of a population of P. mexicana in a high (Greenberg et al. 1985). altitude stream from central Mexico, was conducted to describe morphological and reproductive characteris- Microhabitat characterization tics, as well as the environmental conditions that influ- Microhabitat characteristics were recorded on all sam- ence gametophytes occurrence. pling dates. Microhabitat variables were measured in situ at the center of five replicate quadrats of each MATERIALS AND METHODS sampling unit: current velocity and irradiance were measured as close as possible to the algae using a Sample collection Swoffer 3100 current velocity meter (Swoffer Instru- ments, Inc., Seattle, WA) and a Li-Cor LI-1000 The material used in the present study was collected quantum meter (LI-COR Corporate, Lincoln, NE) with a from the Amanalco river; a fifth-order stream segment flat subaquatic sensor of photosynthetically active in a mountainous region of central Mexico (elevation radiation, respectively. The coefficient of variation 1890 m; 19°13′N, 100°07′W). Field work was con- (VC = SE/a·100, where SE = standard error and ducted from October 2007 to November 2008, includ- a = average) was used to evaluate the variability of ing the contrasting rainy and dry seasons. Three environmental parameters. A VC value < 10% indicated samplings were conducted during the early (December), relatively stable parameters; a value >10% indicated middle (February) and end of the dry season (May; those that changed over time and space, usually a termed ‘dry’); December and February were the coldest result of dilution/evaporation processes and biological months (termed; ‘cool dry’). Three more samplings were activity (sensu Margalef 1983). conducted during the middle of the rainy season (Sep- tember, October and November; termed ‘rainy’). Gametophyte characterization Observations were made on natural substrata (boulders) directly in the stream bed. Water temperature and The number of thalli (gametophytes) within each sam- specific conductance were measured with a Conductronic pling unit was recorded by visual estimation using a

175 cm2 viewfinder. The ‘Chantransia’ stage was not observed in natural conditions. Twenty-five thalli were randomly selected (five in each sampling unit) and preserved in 3% formaldehyde for subsequent analysis in the laboratory. The following morphological and phenological characteristics were defined during pre- liminary tests and previous research: thallus height; number of true and false branches; number of nodes with spermatangia; number of visible carposporophytes; number of gametophytes with open tips; and number of ‘Chantransia’ stages associated with the gametophyte surface (Vis et al. 1992; Sheath et al. 1996b; Carmona & Necchi 2002; Filkin & Vis 2004). In addition, epiphytic and aquatic invertebrates were identified from each thallus to examine species associations (Merrit & Cummins 1996; Wiggins 1996). Olympus BX51 and SZX7 microscopes with a DP12 and E-330 microphotography system were used for microscopic analyses.

Statistics Kruskal–Wallis test were performed to assess significant differences in environmental and morphometric meas- urements among six samplings dates. When tests were significant, the Mann–Whitney test was conducted among all dates to detect which differed significantly. Associations among morphometric, reproductive data, and microhabitat variables during the six sampling dates were assessed using the Spearman correlation coefficient (Gotelli & Ellison 2004). The analyses were conducted using SPSS 18 software (Levesque 2006). Fig. 1. Current velocity, irradiance, depth and percentage cover in quadrats with Paralemanea mexicana. Sampling dates indi- RESULTS cated with the same letter do not significantly differ (Mann– During the six collection periods of the year, the river Whitney test, α=0.05). n = 25 (average ± 1 SE). water exhibited relatively low ionic content (143– 210 mg L−1 of total dissolved solids; specific conductance 165–248 μS cm–1), with a near neutral pH (6.7– 8), mild temperature (14–18°C), high dissolved oxygen Kruskal–Wallis test revealed significant differences for saturation (91–100%), low total alkalinity (74–86 mg current velocity (H = 12; P = 0.04) and irradiance −1 CaCO3 L ) and a dominance of sodium and bicarbonate (H = 24; P < 0.00) among sampling dates. (Table 1). The physical characteristics were consistent Based on taxonomic characteristics, the specimens during the six sampling periods (VC < 10%). The were ascribed to P. mexicana (Fig 2a–m). The thalli remaining physical and chemical variables (discharge, were generally branched, and branches of first and specific conductance, total dissolved solids, sodium, second order were usually whorled (Fig. 2a). Two types potassium, chloride, sulfate, nitrate, nitrite, ammo- of branches were identified. The first type, true nium, dissolved silica and SRP) exhibited larger vari- branches, originated from meristematic cells that ations (VC 15–110%), with increased values during divide in the apical region of thallus in variable number cool dry and dry seasons. Changes in DIN were great, (Fig. 2b,c). The meristematic cells produce several probably by the contribution of upstream agricultural apical or intercalary branches along the thallus activities. Gametophytes occurred predominantly in (Fig. 2d,e). The second type, false branches, were pro- microhabitat conditions that exhibited fast current duced by: (i) the development of the ‘Chantransia’ velocity (40–240 cm s−1), low to medium irradiance stage at the surface of the gametophyte and the origin (5–973 μmol photons m−2 s−1), shallow depth of abundant new gametophytes (Fig. 2f–h), and (ii) (1–30 cm), and boulders as a substratum (Fig. 1). The uniseriate filaments arising from the supposed

Table 1. Physical and chemical characteristics of the Amanalco River

Rainy Cool dry Cool dry Dry Rainy Rainy Variation 27.x.2007 05.xii.2007 08.ii.2008 08.v.2008 03.ix.2008 20.xi.2008 (%)†

Temperature, °C 16 14 15 18 17 14 10 pH 6.8 7.5 8 7 6.7 7.3 6 -1 K25 (μs cm ) 175 197 248 244 165 168 19 Q (m3 s-1) 3.5 2.9 2.3 2.6 2.9 2.3 16 Dissolved oxygen 100 97 94 91 92 93 4 saturation (%) Total dissolved solids 170 190 210 199 143 168 15

Total alkalinity as CaCO3 69 81 85 86 74 82 9 - HCO3 84 98 104 105 90 100 9 Cl- 7 7 11 12 4 5 42 = SO4 6 7 14 13 6 6 43

Si-SiO2 52 57 27 56 51 56 23

Total Hardness as CaCO3 65 73 82 77 67 76 9

Ca Hardness as CaCO3 31 34 39 37 32 33 9

Mg Hardness as CaCO3 33 40 42 40 36 43 10 Ca++ 12 13 16 15 13 13 10 Mg++ 8 10 10 10 9 10 9 Na+ 13 15 19 20 11 15 22 K+ 3 4 5 4 3 3 23 SRP 0.82 0.84 0.58 0.66 0.1 0.1 65 - N-NO3 2.0 0.5 2.6 1.0 1.2 1.7 50 - N-NO2 0.071 0.011 0.006 0.01 0.006 0.009 110 + N-NH4 0.044 0.027 0.05 0.006 0.04 0.02 52 DIN 2.10 0.53 2.76 1.0 1.27 1.7 51 - - - - - = - = - = - = Ionic dominance HCO3 > Cl HCO3 > Cl HCO3 > SO4 HCO3 > SO4 HCO3 > SO4 HCO3 > SO4 = = - - - - > SO4 = SO4 > Cl > Cl > Cl ≥ Cl Na+ > Ca++ > Na+ > Ca++ > Na+ > Ca++ > Na+ > Ca++ > Ca++ > Na+ > Na+ > Ca++ > Mg++ > K+ Mg++ > K+ Mg++ > K+ Mg++ > K+ Mg++ > K+ Mg++ > K+

†Margalef (1983): coefﬁcient of variation VC, conservative value (VC < 10%) and not conservative value (VC > 10%) variables. Values −1 are given in mg L except where indicated. K25, speciﬁc conductance standardized at 25°C; Q, discharge; SRP, soluble reactive phosphorous; DIN, dissolved inorganic nitrogen.

carpospores germination within the thallus lumen The number of first order branches and true branches (Fig. 2i,j). The new gametophytes developed and were significantly higher during two of the three rainy created open tips or open sections of the thallus season samplings than during the dry season (U = 146– (Fig. 2k,m). 203; P = 0.001-0.028), while the dry season exhibited Gametophytes were present throughout the seasons a higher number of false branches compared to the and covered 1–60% of thallus; significant difference rainy and cool dry season (U = 122–198; P = 0.000– in abundance were observed (H = 15; P = 0.01) and 0.021). Some significant correlations were found were positively correlated with the cool dry season between morphometric and environmental condi- (ρ = 0.89; P = 0.05). Highest percentage coverage of tions. Negative correlations were obtained for the gametophytes on the boulders occurred in the cool dry current velocity and false branches and ephiphytic season (20–60%) and the lowest was observed in the ‘Chantransia’ stage in the rainy season (ρ =−0.94–1.0; rainy season (2–10%, Fig. 1). There were significant P = 0.01-0.05) and positive correlation was found in differences among sampling dates for all evaluated current velocity and open tips in the rainy season morphological and reproductive characters (Figs 3,4). (ρ = 0.97; P = 0.01). Negative correlation was Thallus height changed significantly throughout the obtained for the morphometric variables thalli height study (U = 92–210; P = 0.000–0.045). The greatest and false branches in the rainy season (ρ =−0.94; thallus heights were recorded during the cool dry P = 0.05). The positive correlation was for false season (2.3–15 cm), the lowest were in the rainy branches and ephiphytic ‘Chantransia’ stages in the season (1.5–9.0 cm). Significant differences were cool dry season (ρ = 0.94; P = 0.05). observed in the true branches and false branches The population collected throughout the study was between seasons (U = 122–202; P = 0.001–0.024). monoecious and carposporophytic (Fig. 4). The number

Fig. 2. Morphological and reproductive features of Paralemanea mexicana. (a) General habit and branches usually whorled. (b) Meristematic cells (arrows) in the apical region. (c) Meristematic cells (arrows) along the apical region. (d) True branches in the apical region of thallus. (e) True branches in the apical and intercalar region of thallus. (f) ‘Chantransia’ stage and rhizoidal system with the origin of abundant new gametophytes (arrow). (g) Epiphytic ‘Chantransia’ stage in apical region of the gametophyte. (h) Cross section of the cortex showing ‘Chantransia’ stage and new gametophytes (arrows). (i) Uniseriate filaments arising from the carpospores within the thallus lumen. (j) Detail of the uniseriate filament arising from a carpospore. (k) Open tip section of thallus with new gametophytes. (l) Open lateral section of thallus with new gametophytes. (m) Damaged section of thallus with new gametophytes (arrow). Scale bar: 1 cm for Figs. a–h, k–m; 30 μm for Figs. i, j. of spermatangial rings, number of carposporophytes and ber (warmer months, U = 19–196; P = 0.0–0.019). The open tips exhibited significant differences between greatest number of open tips (U = 140–210; P = sampling dates (U = 43–212; P = 0.000–0.04). The 0.001–0.04) and the number of epiphytic ‘Chantransia’ spermatangial rings and carposporohytes were signifi- stage (U = 53–207; P = 0.000–0.03) were observed cantly higher during November, December and February during the warm dry season. One correlation was found (cooler months) than during May, October and Septem- between the thallus height and the highest number of

carposphorophytes and spermatangial rings (ρ = 0.90; P = 0.05) during the cool dry season. Paralemanea mexicana occurrence was associated with other freshwater Rhodophyceae: Batrachosper- mum gelatinosum (Linnaeus) De Candolle and Sirodotia suecica Kylin and several epiphytic and metaphytic cyanobacteria: Blennothrix heterotricha (Gomont ex Gomont) Anagnostidis et Komarek, Phormodium inter- ruptum Kützing ex Gomont and Placoma regulare Broady et Ingerﬁeld. Epiphytic aquatic larvae and pupae invertebrates of the orders Simuliidae (Simulium sp.), Chironomidae (Rheotanytarsus sp.) and Hydroptilidae (Hydroptila sp. and Atopsyche sp.) built cases on the gametophyte. A positive correlation was observed between the numbers of epiphytic ‘Chantransia’ stages, the number of insect cases, and the number of associated species in May (dry season, ρ = 0.90–0.97; P = 0.05–0.01).

Fig. 3. Morphometric characteristics measured for Paralemanea DISCUSSION mexicana. Sampling dates indicated with the same letter do not The stream conditions observed during the current significantly differ (Mann–Whitney test, α=0.05). n = 25 study were similar to previous records in high mountain (average ± 1 SE). streams in central Mexico (Carmona & Necchi 2002; Bojorge et al. 2010): mild temperature (12–16°C), slightly acid to neutral pH (5.5–7.6), moderate specific conductance (169–248 μS cm−1), rocky substrata, and medium to fast current velocity (>35 cm s−1). The stream segment showed both oligotrophic to eutrophic conditions during the year: DIN 0.02–2 mg L−1 and SRP 0.2–0.8 mg L−1 (Dodds 2003). According to Bowman et al. (2005), enrichment of the limiting nutrient in mountain streams can increase the abundance of benthic algae, which could contribute to the increased percent cover recorded during the cold dry season at this site. The highest cover percent of gametophytes was observed during the cool season and indicates their association with low temperature, and conversely, with low cover percent during the rainy season with high discharge. This result is comparable with other populations of Paralemanea species from high-altitude streams from tropical climates in Central and South America; e.g. Paralemanea annulata (Necchi & Zucchi 1995) and P. mexicana (Carmona et al. 2004; Bojorge et al. 2010). The preference for cool temperatures (<20°C) seems to be a common feature among species of Batrachospermales collected in temperate regions; for example, Lemanea fluviatilis (Thirb & Benson-Evans 1984, 1985; Carmona et al. 2011), P. annulata (Filkin & Vis 2004), P. catenata (Kucˇera & Marvan 2004; Carmona et al. 2011), as well as populations analyzed Fig. 4. Reproductive characteristics measured for Paralemanea under culture conditions: P. catenata and Paralemanea mexicana. Sampling dates indicated with the same letter do not sp. (Necchi & Carmona 2002). significantly differ (Mann–Whitney test, α=0.05). n = 25 The gametophytes of the P. mexicana population in (average ± 1 SE). central Mexico exhibited several peculiar characteris-

© 2013 Japanese Society of Phycology 92 J. C. Jiménez et al. tics. They contained true branches with a sympodial Efficient reproductive strategies of P. mexicana branching pattern. This branching pattern is important observed in this study can be interpreted as adaptations to taxonomically differentiate specimens of P. mexicana for successful colonization in streams; however, this (with branches) and P. catanata and P. annulata adaptation may not have been common in the study (without branches; Vis et al. 1992). The frequently region because it is restricted to an isolated geographic whorled branches are the result of a false branched region with particular microhabitat conditions. This fact pattern and are apparently exclusive to P. mexicana. suggests that special morphological and reproductive Considering that true and false branches are distin- adaptations promote successful competition with other guishing taxonomic features, we concluded that the species in similar hydrological systems in mountain number and branching pattern are variable and corre- streams. lated with environmental changes, especially with changes in current velocity. The correlation between the number of open tips ACKNOWLEDGMENTS (i.e. greater number of carpospores released) and the number of epiphytic ‘Chantransia’ stages can result in We thank S. Castillo (ICMyL-UNAM) for nutrient analy- the highest number of false branches in the dry season. ses, A. Aguayo Ríos, N.E. Ceniceros B., and O. Cruz R. In P. annulata, the increase of open tips is thought to (IGeof-UNAM) for major ion analyses, M. Cartagena and occur earlier in the areas with higher current velocity, J. Ramírez-Lynn for fieldwork assistance, Professor due to abrasion from sand and detritus (Filkin & Vis Narcís Prat for macroinvertebrate determination and 2004). ScienceDocs, Inc. for English review. JCJ received Gametophytic thalli of P. mexicana populations financial support from Research Grant PAPIIT-UNAM appeared to prefer specific microhabitat conditions, (IN209107) and CONACyT (52386). such low irradiance (average 235 μmol photons m−2 s−1), boulder substrate and particularly high current −1 velocity (average 70 cm s ). Several characteristics REFERENCES seem to provide adaptations to high current velocity: (i) abundant spermatangial rings increase fertilization APHA, AWWA and WPCF. 1980. Métodos normalizados para el success, a feature that can be related to the presence of análisis de aguas potables y residuales. Ediciones Días de carposporophytes in all seasons; (ii) aggregations of Santos, Madrid. gametophytes and abundant whorled branches along Bojorge, M., Carmona, J., Cartajena, M. and Beltrán, Y. 2010. the surface of the substrate provide anchorage for new Temporal and spatial distribution of macroalgal commu- gametophytes. In our field study, the ‘Chantransia’ nities of mountain streams in Valle de Bravo Basin, central stages of P. mexicana were microscopic and formed a México. Hydrobiologia 641: 159–69. system of rhizoidal filaments, or a cluster of cells, Bowman, M. F., Chambers, P. A. and Schindler, D. W. 2005. which produced new gametophytes (clonal reproduc- Epilithic algal abundance in relation to anthropogenic tion), similar to what has been observed in several changes in phosphorus bioavailability and limitation in Batrachospermales species in culture (Necchi & mountain rivers. Can. J. Fish. Aquat. Sci. 62: 174–84. Carmona 2002); (iii) germination of carpospores in the Carmona, J. and Necchi, O. Jr. 2002. Taxonomy and distri- thalli lumen gives the gametophytes the possibility of bution of Paralemanea (Lemaneaceae, Rhodophyta) in developing protected by the cortex of their parental Central Mexico. Cryptogam., Algol. 23: 39–49. thalli. Carmona, J., Montejano, G. and Cantoral, E. 2004. The dis- The occurrence of P. mexicana in this study corre- tribution of Rhodophyta in streams of Central Mexico. sponded with associated species of Sirodotia suecica Arch. Hydrobiol. Suppl. Algol. Stud. 114: 39–52. and Batrachospermum gelatinosum, a group of temper- Carmona, J., Montejano, G. and Necchi, O. Jr. 2006. Ecology ate species (Kwandrans et al. 2002). The presence of and morphological characterization of gametophyte and the epiphytic ‘Chantransia’ stage and gametophytes of ‘Chantransia’ stages of Sirodotia huillensis (Batrachos- these species on the Paralemanea surface suggested permales, Rhodophyta) from a stream in central Mexico. that the thallus serves as a refuge from the high current Phycol. Res. 54: 108–15. velocity. Similarly, P. mexicana was frequently colo- Carmona, J., Bojorge, M., Beltrán, Y. and Ramírez, R. 2009. nized by Simuliidae, Chironomidae and Hydroptilidae; Phenology of Sirodotia suecica (Batrachospermaceae, this has also been observed in previous studies in North Rhodophyta) in a high altitude stream in central Mexico. America (Sheath et al. 1996a). However, in the present Phycol. Res. 57: 118–26. study, we found no evidence of damage to the gameto- Carmona, J., Perona, E., Sánchez-Díaz, E. and Loza, V. phyte; these insect larvae appear to use the red algae as 2011. Morphological and ecological characterization of refuge from fast current velocities during its final larvae Batrachospermales (Rhodophyta) in the Jarama Basin stage (Sheath & Hambrook 1990). (Iberian Peninsula). Limnetica 30: 117–28.

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