Diatom Research (2006), Volume 21 (1),81-89

CYCLOTELLA ALCHICHICANA SP. NOV.FROM A SALINE MEXICAN LAKE

Ma. Guadalupe Oliva *

Unidad de Morfologia y Función, UMF and Proyecto de Investigación en LimnologiaTropical, UIICSE. FES Iztacala, UNAM Av. de los Barrios No. 1, Los Reyes Iztacala,

54090 Tlalnepantla, Estado de México, México

Alfonso Lugo, Javier Alcocer

Proyecto de Investigación en Limnologia Tropical. UIICSE, FES Iztacala, UNAM Av. de losBarrios No. 1,Los Reyes Iztacala, 54090 Tlalnepantla, Estado de México, México

Enrique A. Cantoral-Uriza

Grupo Ecologia de Algas, Departamento de Ecologia y Recursos Naturales, Facultad deCiencias, UNAM Apdo. Postal 70-620, Circuito Exterior, Ciudad Universitaria,

Coyoacán 04510, México, DF, México

Cyclotella alchichicana sr. nov. is described fram Lake Alchichica, Puebla, Mexico, a salineand alkaline crater-Iake in Central Mexico. The new species is similar to C. quillensis ITomwhich it distinguished by the arrangement of the marginal fultoportulae and by the externalopening of the rimoportula that is elongated slit-like and lacking the external prajection onthe mande. Some habitat and ecological data where C. alchichicana has been observed areprovided.

INTRODUCTION

.f

Diatoms typically form a significant fraction of the biota in saline lakes (Saros & Fritz2000). Such is the case in Lake Alchichica, Puebla, Mexico, where the phytoplanktonassemblage included 10 planktonic diatoms out of a total of 19 species (Oliva et al. 2001).Among saline water diatoms, only eight species of Cyclotella have been recognized (Prasadet al. 1990).

Tl}e taxonomy of Cyclotella Kützing ex Brébisson is hard to unravel because of theconsiderable morphological variation among species (Hi'ikansson & Kling 1994, Meyer &Hi'ikansson1996).

A centric diatom was found in the limnetic water samples from Lake Alchichica, Puebla,Mexico. Light and scanning electron microscopy observations revealed that it hascharacteristic features that allowed us to propase it as a new species. Habitat and ecologicalinformation of the new species is provi&~d. .

,

* e-mail: oliva@servidor.unam.mx

82 MA.G. OLIVA, A. LUGO, J. ALCOCER & EA CANTORAL-URIZA

Description of study site

Alchichica crater-lake (19° 24' N, 97° 24' W) is 2,300 m above sea level (Fig. 1) in theendorheic -closed- Oriental basin, Central Mexico. It is deep (maximum depth 64 m, meandepth 38.6 m), with a 1.81 km2 surface afea (maximum length 1.7 km, maximum widthlA km). Its basin holds 7 x 107m3 of saline (8.3-9.0 g ¡-') and alkaline (pH 8.7-9.2) water,dominated by sodium, magnesium, chloride and bicarbonate ions (Arredondo-Figueroa el al.1983, Vilaclara el al. 1993,Alcocer el al. 1998).

Annual atmospheric temperature fluctuates between -5.5 and 30°C (García 1988). Theclimate is arid, with an annual precipitation <400 mm and an annual evaporation rate of500-600 mili.

Lake Alchichica is oligotrophic and warrn-monomictic. Mixing takes place from lateDecember to early March, during the cold-dry season, and the lake remains stratifiedthroughout the Testof the year (from late March to early December) during the warm-rainyseason (Alcocer el al. 2000). Further information of the thermal stratification regime andphytoplankton and zooplankton composition in this lake is provided elsewhere (Alcocer el al.1998, Lugo el al. 1999, Oliva el al. 2001).

Fig. 1. Location of Lake Alchichica. Upper: The State of Puebla (the small square within the State ofPuebla indicates Lake Alchichica approximate situation). Lower: Aerial photograph ofLake Alchichica.

A NEW CYCLOTELLA SPECIES FROM A SALINE LAKE 83

MATERIAL AND METHODS

Sampling took place at mid-day once each month in the central and deepest part of thelake during a twelve-month period (1998). Profiles in situ of temperature, dissolved oxygen,pH and conductivity (K2s) were obtained with a calibrated Hydrolab@ DS3/SVR3 multi-parameter water-quality data logger and logging system (discrete readings every meter). Fivewater samples (depth 2,5, 10,20 and 50 m) for phytoplankton analysis were obtained with a6-liter Niskin-type water sampler. Two 500 mI sub-samples from each sampling depth werefixed, one with 4% formaldehyde and the other with Lugor s solution (1%). Valves ofC. alchichicana were observed at a magnification of 204.8x. Additional material was cleanedthrough acid oxidation (Rushforth el al. 1984). Aliquots were dried anta cover slips andmounted in Naphrax (Hasle & Fryxell 1970). Slides were examined using a Zeiss phase-contrast microscope. Light micrographs were taken on a Nikon Lobophot-2 photomicroscope.For scanning electron microscopy (SEM), cover slips with the dried material were mounted onaluminum stubs and coated with pure silver. We used a JEOL JSM-5200 microscope(working distance 10 mm, accelerating voltage 25 kV). We followed the terminology inAnonymous (1975), Ross el al. (1979) and Hiikansson (2002).

Morphological traits included for comparison were valve diameter, number andarrangement of the marginal and central fuItoportulae (strutted processes), presence of themarginal rimoportula (labiate process), presence of marginal spines, presence of granules,density of striae, and the structure of the central afea of the valves.

RESULTS

Cyclotella alchichicana Oliva, Lugo, Alcocer & Cantoral, sp. nov. (Figs 2-19).

Cellulae solitariae chloroplastis discoideis numerosis. Frustula tympaniformia aspectucingulari. Cingulum ex valvocopula et copulis pagina laevi sine ornamentis constans. Valvaecirculares, tangentaliter undulatae, 35~63 ¡lm diametro. Valva in microscopio electronico(SEM) extus duabus areis: afea marginali 1/3 radi toti occupanti, et afea centrali. Margoexternus striis radiantibus, interstriis leviter prominentibus tholiformibus. Striae ex 2-6seriebus areolarum limbum versus latae factae constantes, 8-10 in 10 ¡lm. Interstriae duabusspinis ad valvae et limbi adjuncturam, in secunda vel tertia quaeque interstria, aliquandospinis marginalibus etiam in striis. Striae interstriaeque in limbo continuantes, ubi multaeinterstriae indistinctae redigentes. Spinae parvae in limbi pagina dispersae. Area centralisvalvae lineis radialibus in cristis vadosis undulatis dispositis versus strias marginalescurrentibus, granulis parvis obtectis; aperturae externae fultoportularum centralium in aedemafea. Aperturae externae fultoportularum marginalium ad basim spinarum valvae limbi.Aspectus externus rimoportulae unicae est apertura rimiformis in limbo, projectura externacarens. Rimoportula intus pedunculata, in duobus labiis leviter obliquis ad costam terminata.Aspectus internus valvae fultoportulis marginalibus varíe dispositis; in quaeque costa, vel inalterna quaeque costa, vel in secunda aut tertia costa; omnes fultoportulae tribus poribussatellitibus. Alveoli marginales varíe occlusi. Valva in microscopio photonico annuloirregulari punctorum in afea centrali; puncta in microscopio electronico fultoportulaecentrales sunt. Area centralis laevis, 7~19 fultoportulis, unaquaque per tres poros satellitescircumcincta.

Solitary cells with numerous discoid chloroplasts. Frustules drum-shaped in girdle view.Cingulum consists of a valvocopula and copulae with smooth surfaces withoutornamentation (Fig. 4). Valves are circular, tangentially undulate (Figs 2--4), 35~63 ¡lm indiameter (mean 49 ¡lm, n=lOO).In the SEM, the external view ofthe valve shows two afeas,a marginal zone occupying approximately one-third of the total radius, and a central zone(Fig. 3). The external margin has radiating striae, separated by slightly elevated domed

84 MAG. OLIVA, A. LUGO, J. ALCOCER & EA CANTORAL-URIZA

ridges (interstriae). The striae are composed of 2-6 rows of areolae broadening to the mantle,with 8-10 striae in lO /-1m.The interstriae have at the valve face/mantle junction two spines,located on every second or third interstria (Figs 7, 8) but sometimes the marginal spines arealso found on the striae (Fig. 9). Both striae and interstriae continue auto the mantle, wheremany of the interstriae tose their distinctness (Fig. lO). Small spines are scattered on thesurface of the mantle (Fig. 9). The central afea of the valve has radial lines arranged inshallow undulating ridges that mn towards the marginal striae, covered by small granules(Fig. 5); in the same afea are the external openings of the central fultoportulae . The externalopenings ofthe marginal fultoportulae are in the base ofthe spines ofthe valve mantle (Fig.8). The external view of the single rimoportula is a slit-like opening on the mantle lackingthe external projection (Figs lO, 11). Internally, the rimoportula is stalked, and ends in twoslightly oblique lips on the costa (Figs 13, 14, 16). The internal view of the valve hasmarginal fultoportulae showing a variable arrangement, on every, or every other, or everysecond or third costa (Figs 13, 15, 16); each fultoportula has three satellite pares. The degreeof occlusion ofthe marginal alveoli was variable (Figs 13, 16). In LM, the valve presents oneirregular ring of puncta in the central afea, which are shown to be the central fultoportulae inSEM (Fig. 12).The central afea is smooth, with 7-19 fultoportulae, each ofthem surroundedby three satellite pares, which are covered by semicircular siliceous flaps (Fig. 17).

Holotype: here designated: Slide 1544, Izta Herbarium (IZTA) FES- Iztacala, UniversidadNacional Autónoma de México. Collector: J. Alcocer, 1998.

Isotype: Slide 1545, Izta Herbarium (IZTA), FES Iztacala, Universidad Nacional Autónomade México.

Type locality: Lake Alchichica, Puebla, Mexico (19°24' N, 97°24' W).

Etymology: The specific epithet alchichicana refers to Alchichica, the llame where the typelocality is situated.

Habitat and ecological notes

In our study, C. alchichicana was found from the surface (epilimnion) clown to Jeepwater (hypolimnion), and throughout the year. C. alchichicana was abundant during the lakemixing period and distributed throughout the water column. From then on, all during thestratification period, C. alchichicana remained in low numbers and mostly at the metalimnionas part ofthe DCM (deep chlorophyll maximum).

Lake Alchichica waters are alkaline and saline, rich in sodium chloride, large amounts ofcarbonate-bicarbonates, magnesium and sulphates. The range of environmental variableswhere C. alchichicana was found is as follows. Conductivity (K2s) ranged between 13.3 and14.5 mS cm-I and the pH between 8.8 and 10.0. Water temperature fluctuated between14.5 and 20°C. Disso1ved oxygen ranged from anoxic (non detectab1e) up to saturation(7 mg ¡-I). Lake Alchichica is oligotrophic (Oliva et al. 2001, Alcocer & Lugo 2003) with lownutrient (N-NH3 between non detectable (n.d.) and 0.98 mg ¡-I, N-NO2 n.d-0.007 mg 1-1,N-NO3 0.1-1.0 mg 1-1, P-PO4 n.d.-0.54 mg 1-1) and chlorophyll Ha" concentrations(mean < 5 /lg ¡-\

DISCUSSION

Morphology of Cyclotella alchichicana

The valve morphology (i.e. size, density of marginal striae) of Cyclotella alchichicanaresembles that of C. quillensis Bailey (1922) based on the material from Quill Lakes(Table 1). The morphology ofthe central afea ofthe valve face, and the structure and numberof central fultoportulae on the inside valve of material from Alchichica, coincided with the

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86 MA.G. OLIVA, A. LUGO, J. ALCOCER & E.A. CANTORAL-URIZA

('

Figs 2-5. Cyclotella alchichicana, Lake Alchichica. Fig. 2. LM. Figs 3-5. SEM. Fig. 2. Live cell invalve view. Fig. 3. Tangential undulation of the valve face and external view of the valve showing themarginal and central afea. Fig. 4. Cell in girdle view showing the valvocopula and copulae. Fig. 5. Detailof central afea showing radiating ridges. Scale bars = ]O¡..tm(Figs 2--4), 1 ¡..tm(Fig. 5).

.-

Figs 6-9. Cyclotella alchichicana, Lake Alchichica. SEM. Fig. 6. Detail of central afea showing theexternal openings of the valve face fultoportulae (arrowed) and silica granules. Figs 7, 8. Externalmarginal afea showing the spines on the interstriae and the openings of the fultoportulae (arrowed).Fig. 9. Extemalmarginalafea showingthe spineson the striae.Scalebars = 5 ¡..tm(Fig.7), 1 ¡..tm(Figs 6, 8, 9).

A NEW CYCLOTELLA SPECIES FROM A SALINE LAKE 87

Figs 10-13. Cyclotella alchichicana, Lake Alchichica. SEM. Fig. 10. Detail of external marginal afeashowing the external opening of the rimoportula (arrowed) and two or four rows of areolae.Fig. 11. Detail ofthe external opening ofthe rimoportula. Fig. 12. Whole valve, internar view showingthe ring of central fultoportulae. Fig. 13. Internal view of marginal afea showing the fultoportulae (fp)and the rimoportula (rp). Scale bars = 10 ¡.Lm(Fig.12), I ¡.Lm(Figs 10,13),0.5 ¡.Lm(Fig. 11).

Figs 14-17. Cyclotella alchichicana, Lake Alchichica. SEM. Fig. 14. Internal view ofthe marginal afeashowing detail of the rimoportula. Fig. 15. Internal view of the marginal afea showing detail of afultoportula with three satellite pares. Fig. 16. Internal view of marginal afea showing the alveolarocclusion. Fig. 17. Detail of central afea with fultoportulae showing three satellite pares.Scale bars = I ¡.Lm(Fig. 16),0.5 ¡.Lm(Fig. 14),0.1 ¡.Lm(Figs 15, 17).

88 MA.G. OLIVA, A. LUGO, J. ALCOCER & EA CANTORAL-URIZA

description by Battarbee et al. (1984) based on ftustules of C. quillensis from Medicine Lake.That description, as well as mikansson & Kling (1994) and Hilkansson (2002) is similar in thepresence of three satellite pares in the marginal fultoportulae and in the morphology ofinternal rimoportula. Despite these similarities, C. alchichicana differs from C. quillensis inthe following characters: The internal valve of ftustules from Lake Alchichica showedmarginal fultoportulae every, every second or third costa, thereby differing fram thedescriptions by Battarbee et al. (1984) and Hilkansson & Kling (1994) who mentioned afultoportula on every costa. The morphology of the external opening of the rimoportula is anelongated slit-like opening on the mantle, but the Lake Alchichica materiallacks the sleeve-like prajection on the mantle described by those other authors. The position of the spines inthe Lake Alchichica material was variable, on every second to third interstria or stria at thevalve face/mantle junction. Battarbee et al. (1984) and Hilkansson & Kling (1994) indicatedspines at the end of the stria, but Hilkansson (2002) observed the presence of the spines at theend oran interstria (Table 1).

Flower et al. (1990) mentioned that the Cyclotella assemblage is particularly difficult toanalyze because a continuum of morphotypes seems to exist between the individual species.They commented that the taxonomy of the genus is particularly difficult because not onlythere is considerable intraspecific morphological variation but also, interspecific gradients inmorphology. The morphology and position of the rimoportula lately have been given greattaxonomic value within the "cyclostephanoid" genera (Theriot et al. 1987, Hilkansson 2002).The morphological features of Lake Alchichica frustules are more similar to C. quillensisdescribed by Battarbee et al. (1984) and Hilkansson (2002), fram which they differ by havingfewer marginal fultoportulae and by lacking the external prajection of the rimoportula.Considering that specimens in our material exhibit features that have not been recorded for thespecies of the genus, we feel that description of a new species in Cyclotella is justified.

~

ACKNOWLEDGEMENTS

The research on which this paper is based on was supported by Dirección General deAsuntos del Personal Académico, UNAM grant IN204597, and Consejo Nacional de Cienciay Tecnología grant 34893- T. We thank Laura Peralta and Luis A. Oseguera (FES Iztacala,UNAM) for field assistance, Jaqueline Cañetas (Institute of Physics, UNAM) for her skilfulassistance with the SEM. This paper greatly benefited fram the comments and critical revisionofthe manuscript of Sarah J. Davies (University ofWales), Sarah E. Metcalfe (The Universityof Edinburgh), and 1. Platt Bradbury. We are grateful to Fernando Chiang Cabrera (UNAM)who translated into Latin the description of the species. Matthew L. Julius (University St.Cloud State) and other anonymous reviewers are acknowledged for helpful comments of themanuscript. Finally, we thank Ann Grant for her valuable comments and correction of thelanguage.

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