Colonization potential of the genus Ulva (Chlorophyta, Ulvales) in Comodoro Rivadavia Harbor (Chubut, Argentina)

El potencial de colonización del género Ulva (Chlorophyta, Ulvales) en el puerto de Comodoro Rivadavia (Chubut, Argentina)

Alicia Rico^1*, Paola Lanas¹ and Juan López-Gappa²

¹ Departamento de Biología General Facultad de Ciencias Naturales. Universidad Nacional de la Patagonia Ciudad Universitaria, Km 4 9000 Comodoro Rivadavia, Chubut, Argentina. * E-mail: arico@unpata.edu.ar

Recibido en julio de 2004;
aceptado en junio de 2005.

Abstract

Temporal and spatial changes in the coverage of five Ulva L. species (U. prolifera O.F. Müller, U. intestinalis L., U. hookeriana (Kützing) Hayden et al., U. compressa L. and U. linza L.) were analyzed on rocky substrata experimentally immersed in Comodoro Rivadavia Harbor (Argentina). Colonization was studied during an annual period at three levels: upper intertidal, middle intertidal and subtidal. Coverage was significantly higher in the middle intertidal and subtidal levels than in the upper intertidal level, where all species of Ulva were absent. Seasonal changes were also significant: coverage in summer and spring was significantly higher than in autumn and winter. Most species showed high spatial variability among replicates from the same level and season. Zonation patterns within the harbor differed from those observed in natural areas, probably due to low wave exposure and its interaction with herbivory and desiccation stress. Colonization patterns observed in this study indicate niche segregation in closely related species of the genus Ulva.

Key words: Ulva, Chlorophyta, Comodoro Rivadavia Harbor, Patagonia, Argentina.

Resumen

Palabras clave: Ulva, Chlorophyta, puerto de Comodoro Rivadavia, Patagonia, Argentina.

Introduction

Green macroalgae of the genus Ulva L. (including Enteromorpha Link) are widely distributed throughout the world (Hayden et al., 2003), sometimes forming dense algal mats in eutrophicated coastal areas and estuaries (Dolbeth et al., 2003; Cardoso et al., 2004; Cummins et al., 2004).

A recent revision based on molecular data concluded that the genera Enteromorpha and Ulva are not distinct evolutionary entities. Since the latter is the older name, Enteromorpha should be regarded as a synonym of Ulva (Hayden et al., 2003).

In Patagonia (Argentina), Rico et al. (1993) recorded six Ulva species for the Comodoro Rivadavia area: U. intestinalis L., U. compressa L., U. linza L., U. prolifera O.F. Müller, U. flexuosa Wulfen and U. hookeriana (Kützing) Hayden et al. [formerly E. bulbosa (Suhr) Montagne].

The genus Ulva is one of the most important members of fouling communities in harbors because of its strong resistance to toxic chemicals frequently employed in antifouling paints (Rascio and Bastida, 1973) and its high growth rate at salinities higher than 10 psu (Martins et al., 1999). Since the increase of green macroalgae may enhance sediment deposition (Romano et al., 2003) and significantly alter the structure of macrobenthic assemblages (Cardoso et al., 2004; Cummins et al., 2004), the aim of the present study was to analyze spatial and temporal changes in the coverage of the Ulva species colonizing experimental substrata immersed at different levels in Comodoro Rivadavia Harbor.

Materials and methods

Comodoro Rivadavia Harbor is located at 45°52' S and 67°28' W (fig. 1). It is composed of two structures: an older section of vertical walls, and a new breakwater that was built using natural rocks and man-made concrete blocks. Tidal amplitude during spring and neap tides is 6.21 and 4.34 m, respectively (Servicio de Hidrografía Naval, 1998). Salinity varies between 33.4 and 33.8 psu. Mean monthly temperatures of coastal waters near Comodoro Rivadavia vary between 9°C (August-September) and 16°C (February-March) (W. Maza, Climate Prediction Center, pers. comm.).

Sampling and data analysis

All sampling units consisted of the same granitic stones used to build the breakwater. They were originally extracted from Cerro Diagón, Chubut Province (45°35' S, 69°04' W). All the experimental substrata used in this study were devoid of marine life since they had not been submerged. At the beginning of each season, roughly square-shaped stones (ca. 20 x 20 cm) were collected from the breakwater and glued to the substratum with epoxy putty. They were distributed along four transects perpendicular to the breakwater, separated by around 20 m, at three levels: upper intertidal, middle intertidal and subtidal. Upper intertidal stones were immersed at approximately 4.50 m above mean low water level (MLWL). This is the most elevated zone where macroscopic marine organisms can be found and it is dominated by a belt of green algae. Middle intertidal stones were immersed at around 2.60 m above MLWL, in an area characterized by the presence of several invertebrates, such as the non-indigenous barnacle Balanus glandula. Stones could not be sampled in the lower intertidal level because of logistical problems. Subtidal stones were immersed at around 4 m below MLWL. The stones remained between 84 and 100 days in the harbor, during the following intervals: 19/12/97 to 29/03/98 (summer), 29/03/98 to 28/06/98 (autumn), 28/06/98 to 20/09/98 (winter) and 20/09/98 to 20/12/98 (spring). A total of 48 samples (four seasons x three levels x four replicates) were analyzed. Two additional stones were glued at each level, anticipating possible losses, but only one replicate had to be replaced (spring, subtidal) throughout the study period. Samples were fixed in 4% formalin in seawater.

Coverage of the whole benthic community was assessed within an area of 100 cm² in the center of each stone by means of a grid of points.

Since coverage values were not normally distributed and variances were frequently heterogeneous owing to a high proportion of replicates without any Ulva species, the non-parametric Kruskal-Wallis test was used instead of ANOVA to test for differences in coverage among different levels and seasons (Sokal and Rohlf, 1981). Once significant variation was indicated, multiple Mann-Whitney tests were used for pairwise comparisons.

Results

The genus as a whole showed significant changes at different levels: coverage was significantly higher in the middle intertidal (three species) and subtidal (four species) levels than in the upper intertidal level, where all species were absent. As expected, seasonal changes were also significant: coverage in summer (three species) and spring (three species) was higher than in autumn (one species) and winter (zero species).

Ulva prolifera showed significant changes at different levels: coverage was maximum in the middle intertidal level, even though it showed high spatial variability among replicates, and intermediate in the subtidal and absent in the upper intertidal levels. Seasonal changes were also significant, since this species showed highest coverage values in summer but was absent in winter and spring.

Ulva intestinalis showed significant seasonal changes, occurring only in spring.

Changes in coverage of U. hookeriana at different levels were highly significant, since this species occurred only on subtidal substrata.

Ulva compressa was recorded only in spring in the middle intertidal level, with very high spatial variability among replicates.

Ulva linza appeared just as traces on subtidal substrata during summer.

The most abundant species of the genus Ulva in Comodoro Rivadavia Harbor were U. intestinalis and U. prolifera. The former is one of the most conspicuous and frequent algal foulers in all harbors studied to date in Argentina (e.g., Bastida et al., 1974; Brankevich et al., 1986), whereas the latter has only been recorded as a rare component of the fouling assemblages at Puerto Belgrano (Bastida et al., 1974) and the port of Mar del Plata (Bastida et al., 1980).

Ulva intestinalis and U. compressa are widespread in the upper intertidal zone of Buenos Aires Province (Sar et al., 1984). The latter forms a conspicuous belt at high intertidal levels of San José Gulf (Boraso de Zaixso, 1996) and is also abundant at sites impacted by eutrophication due to sewage discharges in Buenos Aires Province (López-Gappa et al., 1993) and in Chubut Province, Argentina (Díaz et al., 2002).

The vertical zonation of some of the species found in this study differs from patterns described previously. Ulva hookeriana has been found in the upper and middle intertidal zones and in tide-pools of the Comodoro Rivadavia area (Rico et al., 1993), but only appeared on subtidal substrata within the harbor. Ulva intestinalis colonized almost exclusively the uppermost panels attached to experimental rafts moored in harbors of Buenos Aires Province (Bastida et al., 1974); however, the stones immersed in the upper intertidal level of Comodoro Rivadavia Harbor lacked all species of Ulva. According to Sar et al. (1984), U. intestinalis and U. compressa may dominate the upper levels of rocky and siltstone substrata in Buenos Aires Province, and their vertical distribution encompasses both the upper and middle intertidal zones.

Much of the variation along a gradient of wave exposure can be explained by the complex interactions between the activities of grazers and the effects of variations in the physical environment that influence the recruitment, survival and growth of algae (Underwood and Jernakoff, 1984). The present results suggest that these interactions are the most likely factors explaining differences in vertical distribution between exposed intertidal areas and habitats located within a harbor.

Seasonal changes in the coverage of Ulva in Comodoro Rivadavia Harbor were significant and matched those observed previously in other harbors of Argentina, where Ulva spp. colonized artificial panels during most of the year, but showed a minimum or were completely absent during winter (Bastida et al., 1974, 1980). As in the present study, U. intestinalis appeared only during spring in an intertidal community affected by a sewage outfall at Quequén (López-Gappa et al., 1993).

One of the most remarkable results of this study is the high degree of spatial variability in coverage at a scale of a few tens of meters, i.e., among replicates from the same level and season. Underwood and Chapman (1998) also found considerable small-scale patchiness among replicate quadrats within sites in intertidal assemblages from sheltered rocky shores of New South Wales, Australia.

Several life-history features of Ulva, such as high reproductive output (Boraso, 1979), high growth rates (Martins et al. , 1999), significant seasonal variation in coverage and small-scale patchiness (this study), are characteristic of the well-known opportunistc strategy displayed by species of this genus, which can usually be found as discrete and ephemeral algal patches on natural and man-made hard substrata. Spatial and temporal patterns of colonization observed in this study suggest a relatively high degree of niche segregation in closely related species of the genus Ulva.

Other algae growing on the same experimental substrata showed different patterns of coverage in time and space. The stones immersed in the upper intertidal level lacked all species of Ulva, and were mainly colonized by the green algae Ulothrix flacca, Urospora penicilliformis and Blidingia minima. Coverage of Ulothrix and Urospora was highest during spring, but Blidingia reached maximum development during winter (Rico et al., 2003).

Since the presence of different Ulva species was patchy and highly seasonal, this genus does not seem to play a major role in structuring the fouling community at this harbor.

Acknowledgements

We are indebted to Horacio It for his help during the field work. Financial support from CONICET (PIP N° 02126) to J. López-Gappa is gratefully acknowledged.

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