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<I>Scutellastra Flexuosa</I>

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<I>Scutellastra Flexuosa</I> BULLETIN OF MARINE SCIENCE, 81(2): 219–234, 2007 REPRODUCTION, ECOLOGY, AND EVOLUTION OF THE INDO-PACIFIC LIMPET SCUTELLASTRA FLEXUOSA David R. Lindberg ABSTRACT Scutellastra flexuosa (Quoy and Gaimard, 1834) was studied at Temae islet reef on Moorea, Society Islands, French Polynesia between 1998 and 2001 to compare and contrast the respective roles of deep phyletic history with recent adaptations in shaping its current ecological and life history characteristics. Most of the charac- ters examined are consistent with related specialist species and are therefore deter- mined by ancestry. These characteristics include habitat restriction, algal gardening, local distribution, home site fidelity, adult/juvenile differentiation, and protandric hermaphroditism. The only character that appears autapomorphic and a possible adaptation to its proximal setting is its small body size. Large body size is often as- sociated with species that maintain and defend territories. However, the variance in size in clades with and without territorial species presents a more complex picture. The putative size reduction of S. flexuosa has not affected many of the specialized traits shared within its lineage and it remains a classic territorial taxon albeit in miniature. The phyletic pattern that emerges here is one of a clade dominated by specialist species that gave rise to generalist species that in turn gave rise to another group of specialists with identical traits albeit in different habitats. Studies of the evolution of life history characteristics of marine invertebrates have produced a large body of empirical data and theoretical interpretations. Many recent studies of the evolution of life history traits have become grounded in phylogenet- ic analysis (e.g., McHugh and Fong, 2002; Kupriyanova, 2003; Meyer, 2003; Collin, 2004; Kohler et al., 2004; Byrne, 2006; Glenner and Hebsgaard, 2006); a trend that is a welcomed alternative to the former practice of using current taxonomic classi- fications to parse traits. In some cases, the results and interpretations of these more recent studies have corroborated earlier work, while in others they have suggested alternative hypotheses. Patellogastropod limpets (or “true” limpets) have long been studied in a broad ar- ray of biological disciplines. Because of their intertidal occurrence, they were some of the first and remain one of the commonest taxa manipulated in ecological studies (e.g., Jones, 1948; Lodge, 1948; Underwood, 1979; Branch, 1981; Hawkins and Hart- noll, 1983). They have served as physiological “guinea pigs” in studies of desiccation and growth (e.g., Wolcott, 1973; Branch, 1974b, 1975a; Parry, 1978; Creese, 1981; Lowell, 1984; Niu et al., 1998; Gray and Hodgson, 2004). They also have a long and illustrious record as model organisms in life history studies, especially with regard to reproductive cycles and hermaphrodism (e.g., Orton, 1919; Dodd, 1956; Orton et al., 1956; Fritchman, 1961; Rao, 1973; Branch, 1974a; Wright and Lindberg, 1982; Wright, 1988; Creese et al., 1990; Le Quesne and Hawkins, 2006). However, the dis- tributions of these life history characters have seldom been explored except for quick comparisons or corroborations of similarities (and differences) with “other limpets” in another region or genus. Here I report the results of a multi-year study of the patellogastropod limpet Scutel- lastra flexuosa (Quoy and Gaimard, 1834) on Moorea, Society Islands, French Poly- nesia. Scutellastra flexuosa is often a common member of the algal ridge community Bulletin of Marine Science 219 © 2007 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 220 BULLETIN OF MARINE SCIENCE, VOL. 81, NO. 2, 2007 where it experiences the full intensity of reef-crest wave action. Unlike most other patellogastropod faunas found in high-energy environments (Branch, 1976; Lind- berg, 1988), S. flexuosa is the only patellogastropod species to occur there. Therefore, it presents an opportunity to compare the roles of phyletic history and recent adapta- tions in shaping its ecology and life history uncomplicated by the co-occurrence of closely related taxa and interactions. To compare the ecological and life history characteristics S. flexuosa with other patellid species a standardized list of ecological and life history characters was used. This list was developed by George M. Branch (1975b) during his study of intraspecific competition in southern African Patella spp. Branch was especially interested in the role of migration, differentiation, and territorial behavior and when he scored his study taxa he found that they sorted into two distinct categories with few interme- diates. Branch termed these groups “migratory” and “non-migratory”, but they also denote groupings of characters commonly associated with distinguishing generalist (migratory) and specialist (non-migratory) species. Scutellastra flexuosa was scored for these traits and the characters examined on a phylogenetic tree to determine character distribution and to separate shared historical characters (pleisomorphy) from new unique characters (autapomorphy) that might represent more recent and local adaptation (Irschick et al., 2005). Materials and Methods The study site was located on the Temae islet reef along the northeast shore of Moorea, Society Islands, French Polynesia (17°38´S, 149°27´W) (Fig. 1A–C). This location was selected because of the close proximity of the barrier reef to the coast and ease of access to a typically difficult habitat in which to conduct intertidal observations. Mean tidal range is < 0.25 m and low tides occur between 0530 and 0600 daily (NOAA, 2005). Scutellastra flexuosa occurs in patches on the algal ridge that gently slopes towards the ocean side of the reef crest (Fig. 1D). Limpets associated with these patches were observed yearly between 1998 and 2001; except for 1999 when surf conditions prohibited access to the site (Table 1). In addition to general observations, 17 0.25 m2 quadrats were arbitrarily located within patches and the limpets within these quadrats collected, measured, and sexed. Photoquadrats of both before and after removal were also taken and the removed limpets individually located in the quadrat by mapping their position prior to their removal (Table 1). General observations of S. flexuosa were photo-documented and used to score this species in Branch’s (1975b) matrix. Characteristics.—Branch (1975b) categorized nine “behaviors” of 11 patellid taxa from southern Africa. Each behavior was assigned one of four states represent by the symbols , , , or was scored as unknown ? (Table 2). The solid circles represented “migratory” or gen- eralist characteristics while the open squares represented “non-migratory” or specialist char- acteristics. The size of the symbol represented well-developed and poorly developed traits. Scutellastra flexuosa was scored for these behaviors based on observations of the animals at Temae. To quantify Branch’s (1975b) symbolic representation each symbol was assigned a value between −1 and 1: = −1.0, = −0.5, = 1.0, and = 0.5. Data for Scutellastra argenvil- lei (Krauss, 1848), Scutellastra barbara (Linnaeus, 1758), Cymbula miniata (Born, 1758), and Helcion concolor (Krauss, 1848) were updated from Bustamante et al. (1995), Ridgway et al. (1999, 2000), and G. Branch (pers. comm., University of Cape Town, 2007). Median, mean, and standard deviations were then calculated for each species. Phylogeny.—A molecular phylogeny was constructed by reanalyzing 16s rRNA sequence data first presented and analyzed by Koufopanou et al. (1999). AdditionalS. flexuosasequenc - es were provided by C. Meyer, and additional Cellana spp. sequence data were obtained from LINDBERG: REPRODUCTION, ECOLOGY, AND EVOLUTION OF THE INDO-PACIFIC LIMPET 221 Figure 1. Location of study area. (A) Global position of Moorea, Society Islands, French Poly- nesia (17°38´S, 149°27´W). (B) Topographic hi-resolution map of Moorea showing location of Richard B. Gump South Pacific Research Station (diamond) and regional setting of study area along the northeastern coast. Map provided by the Moorea GIS Consortium. (C) Insert from box on (B) showing Temae islet reef area and location of study area. (D) Transect across barrier reef and reef flat at Temae islet reef illustrating geomorphological and biological zonation of the study area and habitat of Scutellastra flexuosa. Redrawn from Galzin and Pointier (1985). Reeb (1995), Simison (2000), and Begovic (2004). The dataset was subjected to maximum parsimony analysis using PAUP* Ver. 4.0b10 (Swofford, 1998). All characters were equally weighted and unordered. The tree-bisection-reconnection (TBR) branch-swapping algorithm was used with a random addition sequence (500 replicates), and one tree was held at each step during stepwise addition. Results Scutellastra flexuosa densities at Temae ranged between 5 and 48 individuals per 0.25 m2 with an average density of 20.4 limpets per 0.25 m2. Sex ratios in the indi- vidual quadrats were highly variable with a mean ratio of approximately 5 males for every 2 females (0.38) (Table 1). There was no correlation between density and sex ratio (r2 = 0.0453). Females were most common in the larger size classes (m = 28.59 mm ± SD = 4.70), while males averaged 23.70 mm in length ± SD = 4.70, and indeterminate individuals averaged 16.36 mm in length (SD = 6.00). The size frequency distribution ofS. flexu- 222 BULLETIN OF MARINE SCIENCE, VOL. 81, NO. 2, 2007 Table 1. Sampling data and summary
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