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Species Separation Within the Lessonia Nigrescens Complex (Phaeophyceae, Laminariales) Is Mirrored by Ecophysiological Traits

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Species Separation Within the Lessonia Nigrescens Complex (Phaeophyceae, Laminariales) Is Mirrored by Ecophysiological Traits Botanica Marina 2015; 58(2): 81–92 Kristina Koch*, Martin Thiel, Florence Tellier, Wilhelm Hagen, Martin Graeve, Fadia Tala, Philipp Laeseke and Kai Bischof Species separation within the Lessonia nigrescens complex (Phaeophyceae, Laminariales) is mirrored by ecophysiological traits Abstract: Lessonia nigrescens used to be an abundant including the species overlapping zone). Phlorotannins, kelp species along the Chilean coast, but recent molecular pigments and Chl a fluorescence of PSII were most crucial studies revealed the existence of a L. nigrescens species for species-specific adaptations at the respective growth complex, which includes the two cryptic species Lessonia sites, whereas changes in total lipids and fatty acid com- berteroana and Lessonia spicata. Since these species have positions were negligible. Hence, species differentiation different distributions (16°S–30°S for L. berteroana and within the L. nigrescens complex is also manifested at the 29°S–42°S for L. spicata), they experience differences ecophysiological level. These findings may help to predict in environmental conditions, such as solar irradiance, kelp responses towards future environmental changes. seawater temperature and air exposure during low tide. This study tested to what extent the genetic distinctness Keywords: Chile; fatty acid composition; Lessonia nigres­ of each of the two species [identified by a mitochondrial cens complex; phlorotannins; photosynthetic pigments. marker (atp8/trnS)] is reflected by ecophysiological traits (total lipids, fatty acid composition, phlorotannins, pig- DOI 10.1515/bot-2014-0086 ments and variable chlorophyll a fluorescence of PSII) Received 13 November, 2014; accepted 17 February, 2015 in response to the respective environmental conditions, prevailing along the latitudinal gradient. We studied algal individuals from eight populations (27°S–32°S, Introduction *Corresponding author: Kristina Koch, Department of Marine Botany and Bremen Marine Ecology Center for Research and Education (BreMarE), University of Bremen, Leobener Str. NW2, Members of the kelp genus Lessonia (Bory de Saint-Vin- 28359 Bremen, Germany, e-mail: [email protected] cent, 1825; Lessoniaceae, Laminariales) are distributed Martin Thiel: Facultad de Ciencias del Mar, Universidad Católica del in the Pacific and Atlantic Oceans of the Southern Hemi- Norte and Centro de Estudios Avanzados en Zonas Áridas (CEAZA), sphere. Along the coasts of Chile, Peru, Tasmania, New and Nucleus Ecology and Sustainable Management of Oceanic Zealand and the sub-Antarctic islands (Nelson 2005), Les­ Island (ESMOI), Larrondo 1281, Coquimbo, Chile Florence Tellier: Departamento de Ecología, Facultad de Ciencias, sonia represents an ecosystem engineer (sensu Jones et al. Universidad Católica de la Santísima Concepción, Casilla 297, 1994) and forms extensive kelp beds of significant ecologi- Concepción, Chile cal and economic importance (Steneck et al. 2002). These Wilhelm Hagen: Department of Marine Zoology and Bremen Marine kelp beds exhibit high primary production rates (Tala and Ecology Center for Research and Education (BreMarE), University of Edding 2007), provide three-dimensional habitats, refuge Bremen, Leobener Str. NW2, 28359 Bremen, Germany and shelter, food sources and nursery grounds for associ- Martin Graeve: Ecological Chemistry, Alfred Wegener Institute for Polar and Marine Research (AWI), Am Handelshafen 12, 27570 ated invertebrates and fishes (e.g., Santelices et al. 1980, Bremerhaven, Germany Villouta and Santelices 1984), and modify water motion Fadia Tala: Facultad de Ciencias del Mar, Universidad Católica del (Santelices and Ojeda 1984). Additionally, Lessonia is Norte and Centro de Investigación y Desarrollo Tecnológico en Algas harvested commercially for alginate extraction and high- (CIDTA), Larrondo 1281, Coquimbo, Chile quality feed for abalone cultures (Vásquez 2008). Philipp Laeseke and Kai Bischof: Department of Marine Botany and Bremen Marine Ecology Center for Research and Education Along the Pacific coast of South America, Lessonia (BreMarE), University of Bremen, Leobener Str. NW2, 28359 Bremen, nigrescens used to be one of the major representatives of the Germany genus Lessonia (Searles 1978). Recently, molecular work Brought to you by | Universidad Catolica Del Authenticated Download Date | 11/2/15 4:31 PM 82 K. Koch et al.: Ecophysiology of the Lessonia nigrescens complex by Tellier et al. (2009) revealed that L. nigrescens is actu- (20°C, 25 days of incubation) than those of L. spicata ally a species complex, which includes two cryptic species (Oppliger et al. 2012). In the latter study, further temper- ( Lessonia berteroana Montagne (1842) and Lessonia ature-related differences in life history strategies were spicata (Suhr) Santelices; as renamed by González et al. detected between the species. At increased temperatures, 2012). In their study, Tellier et al. (2009) detected that, L. berteroana displays a shorter haploid phase, whereas among other characteristics, L. berteroana and L. spicata L. spicata shows an extended haploid phase with remark- vary by the size of the intergenic spacer atp8/trnS, a mito- able vegetative growth. The different temperature optima chondrial marker previously used for phylogenetic studies for the two species are apparently related to the species’ (Voisin et al. 2005, Tellier et al. 2009). Since the size of this geographic origin and play an important role in the adapta- marker is unique for each of the two species, species iden- tion to the prevailing local seawater temperatures. Besides tification can be performed easily via nucleotide electro- genetic differences and contrasting tolerance ranges, these phoresis, hence without sequencing (Tellier et al. 2011c). species vary in very few morphological characteristics. Both cryptic species inhabit the middle to low inter- Based on the external morphology, for example, individu- tidal zones of wave-exposed rocky shores (Santelices et al. als of L. spicata are shorter and show more dichotomies 1980), but they show contrasting latitudinal distribution than those of L. berteroana. Internally, blades of L. spicata ranges along the southeast Pacific coast, with L. bertero­ are composed of smaller and higher amounts of cortex cells ana occurring from 16°S to 30°S and L. spicata from 29°S as well as more filaments in the medulla compared to those to 42°S (Tellier et al. 2009). In the zone between 29°S and of L. berteroana (González et al. 2012). However, since those 30°S, the two species spatially overlap in strict parapatry, morphological differences are solely based on relative so that a mosaic of monospecific populations either of L. traits, we suggest that the two species are only completely berteroana or L. spicata can be observed. This strict geo- distinguishable from each other by genetic identification, graphic segregation of the two species is accompanied by especially within the overlapping zone. a complete absence of interspecific gene flow and conse- The objective of this study was to test to what extent quently the lack of hybridization (reproductive isolation; the genetic identity of the two cryptic species within the Tellier et al. 2011a). The location of the overlapping zone L. nigrescens complex is reflected by ecophysiological corresponds to a biogeographic transition zone at 30°S, traits. To check for ecophysiological differences, sporo- which represents a margin for numerous marine organ- phytes of L. berteroana and L. spicata were collected at isms with low dispersal potentials (Camus 2001, Haye eight locations (27°S–32°S) along the coast of northern- et al. 2014) and is characterized by changes in their recruit- central Chile. Thereby, algal individuals were selected ment patterns (e.g., of some Phaeophyceae; Meneses and from within the overlapping zone and from within the Santelices 2000). Nonetheless, the distribution of species monospecific core zone of each species. Ecophysiological with a higher dispersal potential, such as the gastropod differences and potential adaptive traits at their specific Concholepas concholepas, is less affected by the transi- growth sites were addressed by measurements of total tion zone. Those species cross the transition zone without lipids, phlorotannins, pigments and variable chlorophyll any changes in abundance (Broitman et al. 2001, Cárdenas (Chl) a fluorescence of photosystem II (PSII). Further, et al. 2009). Until now the cause for this biogeographic variations in fatty acid composition were studied for the transition zone located at 30°S is not entirely resolved but first time. More specifically, we tackled the question of is presumably the outcome of a combination of ancient and whether observed ecophysiological differences are based present-day oceanographic features (e.g., breaks in eddy on variations in genetics (species differentiation, identi- kinetic energy, equatorward wind stress and upwelling fied by a mitochondrial marker (atp8/trnS)) or whether regimes; Hormazabal et al. 2004, Thiel et al. 2007). they are impacted by environmental conditions prevailing Since the two cryptic species cover contrasting dis- along the latitudinal gradient. tribution ranges, they experience differences in environ- mental conditions, for example, in seawater temperatures. Consequently, the species may differ in their tolerances with respect to temperature (Martínez 1999, Oppliger et al. Materials and methods 2011, 2012). For example, Martínez (1999) found that young sporophytes of the L.
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