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

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