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Positive Associations Between Macroalgal Species in a Rocky Intertidal Zone and Their Effects on the Physiological Performance of Ulva Lactuca

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Positive Associations Between Macroalgal Species in a Rocky Intertidal Zone and Their Effects on the Physiological Performance of Ulva Lactuca MARINE ECOLOGY PROGRESS SERIES Vol. 292: 173–180, 2005 Published May 12 Mar Ecol Prog Ser Positive associations between macroalgal species in a rocky intertidal zone and their effects on the physiological performance of Ulva lactuca Marco A. Molina-Montenegro1,*, Alejandro A. Muñoz1, Ernesto I. Badano1, Billy W. Morales2, Katia M. Fuentes3, Lohengrin A. Cavieres1 1Grupo de investigación en Ecología, Biogeografía y Sistemática (ECOBIOSIS), Departamento de Botánica, 2Centro de Investigaciones Oceanográficas del Pacifico Suroriental (COPAS), and 3Programa Regional de Oceanografía Física y Clima (PROFC), Universidad de Concepción, Casilla 160-C, Concepción, Chile ABSTRACT: Positive interactions become more important as physical stress increases. Rocky inter- tidal habitats display marked desiccation and heat stress gradients, increasing from low- to high-tidal levels. The presence of some macroalgae has been shown to facilitate several intertidal organisms by ameliorating stressful conditions. However, few studies have reported positive interactions among 2 or more macroalgal species, and none has addressed how seaweed canopies could modify the phys- iological performance of other associated algae along intertidal gradients. Here we report on spatial association patterns of 2 macroalgae (the kelp Macrocystis pyrifera and the green alga Ulva lactuca) occurring along a rocky intertidal vertical gradient in southern Chile. We conducted an evaporative water loss experiment and compared temperature and photosynthetic active radiation beneath the canopy of M. pyrifera and on exposed substrates. We compared maximum quantum-yield (Fv/Fm ratio = (Fm–F0)/Fm, where F0 and Fm are the minimum and maximum chlorophyll fluorescence yields, respectively) and photochemical efficiency in Photosystem II (ΦPSII) of U. lactuca beneath and away from kelp canopies along the intertidal gradient. Positive association patterns between M. pyrifera and U. lactuca were detected at high-tidal areas, while neutral patterns were evident at low-tidal heights. Evaporation, temperature, and PAR were lower beneath kelp canopies. The photosynthetic performance of U. lactuca was lower in individuals on exposed substrates compared to those associ- ated with M. pyrifera, with this effect being more pronounced in the upper intertidal zone. Our results support the prediction that the importance of positive interactions increases with stress. We suggest that M. pyrifera could be acting as a ‘nurse species’ for U. lactuca, possibly extending the vertical distribution of this green alga to high intertidal zones. KEY WORDS: Positive interactions · Facilitation · Physical stress · Desiccation gradient · Macroalgae · Photosynthetic performance · Chlorophyll fluorescence · PAR Resale or republication not permitted without written consent of the publisher INTRODUCTION interactions that benefit at least 1 of the participants without negatively affecting the organisms involved Spatial pattern analyses have been widely used to (Bertness & Callaway 1994, Bruno & Bertness 2000, infer on the nature of interactions among organisms, Bruno et al. 2003). These positive interactions fre- with positive spatial associations having been consid- quently have been reported in stressful habitats, such ered a manifestation of facilitation (Callaway 1995, as deserts (e.g. Franco & Nobel 1988, Valiente-Banuet Hasse 2001, Schenk et al. 2003, Tirado & Pugnaire et al. 1991, Tirado & Pugnaire 2003), high-mountain 2003). Facilitation has been defined as nontrophic ecosystems (e.g. Callaway et al. 2002, Cavieres et al. *Email: [email protected] © Inter-Research 2005 · www.int-res.com 174 Mar Ecol Prog Ser 292: 173–180, 2005 2002), and salt-marsh environments (e.g. Hacker & the green macroalga Ulva lactuca, occurring along a Bertness 1995, Callaway & Pennings 2000). Bertness & rocky intertidal vertical gradient in southern Chile. Callaway (1994) and Brooker & Callaghan (1998) pro- The latter alga is a small thin-fronded foliose species posed that both the frequency and the intensity of (Hoffmann & Santelices 1997), and hence can be facilitation increases along environmental stress gradi- considered to be highly susceptible to desiccation. ents, with this having been demonstrated in several Indeed, it usually grows in the lower and mid- ecosystems (e.g. Bertness & Leonard 1997, Bertness et portions of rocky intertidal areas, as well as shallow al. 1999, Callaway et al. 2002). subtidal habitats along the Chilean coast (Hoffmann Rocky intertidal zones are stressful habitats due to & Santelices 1997). We propose that the presence of the high substrate temperatures, strong desiccation, M. pyrifera individuals ameliorates physical stress and high levels of solar radiation they experience beneath their canopies, resulting in positive spatial during periods of low tide (Lively & Raimondi 1987, associations between this kelp and U. lactuca in the Raffaelli & Hawkins 1996, Bertness & Leonard 1997). high intertidal zone. We also hypothesize that micro- Therefore, any species able to ameliorate these condi- climatic improvement by M. pyrifera would result in tions could be expected to enhance the performance of a greater physiological performance of U. lactuca, other species (Bertness et al. 1999). During low-tide expressed as an increase in its photosynthetic effi- periods, some macroalgae have been shown to greatly ciency of Photosystem II. improve water retention of rocky substrates beneath their canopies (Hay 1981, Bertness & Grosholz 1985). The presence of these macroalgae facilitates the estab- MATERIALS AND METHODS lishment and survival of several other species such as snails, mussels, crabs, as well as other macroalgae Study site and species. We carried out this study in (Brawley & Johnson 1991, Bertness et al. 1999). How- February 2003 at Coliumo Bay (36° 35’ S, 72° 58’ W), ever, despite the many reported cases of facilitation in 40 km north of the city of Concepción, southern Chile. algae, seagrasses, and invertebrates in rocky shores, This is a wave-protected bay in which the horizontal the large majority of these studies have focused on distance between low and high tide points is typically positive intraspecific grouping effects (e.g. Hay 1981, ca. 25 m. Substrata along the intertidal range consist Holbrook et al. 1991, Bertness & Leonard 1997). In con- mostly of rocky platforms and boulders, intermixed trast, few studies have demonstrated facilitative inter- with sand (Ruiz & Giampoli 1981). actions among 2 or more macroalgal species (but see The most conspicuous macroalgae occurring in this Brawley & Johnson 1991), and none has indicated how bay are 2 brown kelp species, Macrocystis pyrifera and seaweed canopies could modify the physiological Lessonia nigrescens, the green foliose species Ulva performance of other associated algae. lactuca, and the red foliose species Mastocarpus papil- Desiccation due to the exposure to high ambient latus. Invertebrates such as the bivalve Perumytilus temperatures during periods of low tide has been purpuratus, the gastropods Tegula atra and Fissurella shown to result in reduced physiological performance spp., and cirripedians Jehlius cirratus are also abun- and growth in several macroalgal species (Bewley & dant inhabitants commonly found among these ma- Krochko 1982, Dudgeon et al. 1995, Rico & Fredrik- croalgae (Ruiz & Giampoli 1981). M. pyrifera forms sen 1996). Since high-tidal habitats are exposed to dense and extensive stands consisting of individuals high temperatures and desiccant winds for longer forming large canopies (>1 m diameter). This species periods than lower tidal levels (Lively & Raimondi mainly grows on rocky platforms, occasionally occur- 1987, Bertness & Leonard 1997), mitigation of desic- ring on bulky sand. U. lactuca grows to 20–30 cm in cation by seaweed canopies would be expected to be height, growing both beneath the canopy of individu- more important at the former habitats. Hence, micro- als of M. pyrifera as well as on exposed rocky sub- climatic improvement by seaweed canopies should strates. In Chile, both species are widely distributed produce positive patterns of species associations at from Antofagasta (20° 56’ S, 67° 00’ W) to Tierra del high-tidal zones. In contrast, more benign abiotic Fuego (53° 08’ S, 70° 55’ W) (Hoffmann & Santelices conditions at low-tidal areas should lead to neutral or 1997). negative patterns of species co-occurrence. Further, it Patterns of association between Macrocystis pyri- could also be suggested that amelioration of stressful fera and Ulva lactuca. At each of 4 equally distant abiotic conditions at high-tidal habitats should im- points along the intertidal gradient (5, 10, 15 and 20 m prove the physiological status of associated macro- away from the low intertidal limit), we randomly algal species. selected 10 M. pyrifera individuals, having canopies Here we report on spatial association patterns of 2 between 40 and 60 cm in diameter, and registered the macroalgae, the giant kelp Macrocystis pyrifera and occurrence of U. lactuca beneath them. For each of Molina-Montenegro et al.: Macroalgal species associations along intertidal gradients 175 the studied M. pyrifera individuals, we also located a at 2 and 4 h after commencing the experiment. Weight 50 cm diameter metallic hoop on exposed open sub- differences were used to calculate mean percentage strates ca. 30 to 40 cm away from the kelp canopy, water loss per microsite. Differences in percentage and registered the occurrence of U. lactuca.
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