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Invertebrate Biology 132(2): 133–144. © 2013, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12021 Demography and feeding behavior of the kelp crab Taliepus marginatus in subtidal habitats dominated by the kelps Macrocystis pyrifera or Lessonia trabeculata David Jofre Madariaga,1,2 Marco Ortiz,2 and Martin Thiel1,3,a 1 2 Facultad de Ciencias del Mar, Universidad Cat olica del Norte, Coquimbo, Chile Instituto Antofagasta de Recursos Naturales Renovables (IARnR), Instituto de Investigaciones Oceanol ogicas, Facultad de Recursos del Mar, Universidad de Antofagasta, Antofagasta, Chile 3 Centro de Estudios Avanzados en Zonas Aridas, Coquimbo, Chile Abstract. We studied the population and feeding ecology of the kelp crab Taliepus marginatus in subtidal kelp forests dominated by either of two morphologically different kelp species (Macrocystis pyrifera or Lessonia trabeculata) in northern Chile. The sizes and abundances of T. marginatus differed between the two kelp habitats. Kelp crabs were more abundant in the M. pyrifera forest than in the L. trabeculata forest. Size-frequency distributions showed that juvenile and immature crabs were more common in the M. pyrifera forest than in the L. trabeculata forest, where reproductive adults predominated. The smaller crabs in the M. pyrifera habitat also consumed a higher proportion of kelp tissues than the larger crabs in the L. trabeculata habitat, which had a higher proportion of animal food in their diet. In both kelp forests, individuals of T. marginatus showed a similar pattern of nocturnal feeding over a 24-h period, consuming more food at night than during the day. The more complex and dense forests of M. pyrifera appear to present better nursery habitats for juvenile kelp crabs than the more open and less dense forests dominated by L. trabeculata. These results suggest that the role of the two kelp habitats for T. marginatus varies during the life cycle of the kelp crabs, with M. pyrifera tending to have nursery function and L. trabeculata being more suitable as a reproductive habitat. Additional key words: habitat use, nursery habitat, reproductive habitat, diet Habitats differ in their availability of food items, predation pressure, and physical disturbance (e.g., habitat-specific environmental factors), resulting in specific costs and benefits for individuals (Amaral et al. 2008). For example, habitats with higher structural complexity offer more shelter and resources, thereby supporting high densities of individuals. On the other hand, high densities may result in interference competition for resources and space, leading to emigration and occupation of less favorable habitats by some individuals, allowing for more feeding time, albeit possibly on less preferred food items (Amaral et al. 2008). Kelp beds are highly productive benthic ecosystems (V asquez 1992; Steneck et al. 2002; Ortiz 2008), which provide shelter for a wide variety of species (e.g., fishes, seastars, crabs, and snails) with different feeding behaviors (Smith et al. 1996). Majid crabs living on kelps act as both consumers and a Author for correspondence. E-mail: [email protected] prey, and thus represent an important trophic link (Hines 1982). As consumers, they obtain most of their nutrition from algal material (Hines 1982; Kilar & Lou 1986; Daly & Konar 2010). The nutritional value and abundance of this algal material are factors that determine its consumption (Wolcott & O′Connor 1992), and multiple structural and chemical adaptations have evolved that might reduce the palatability of seaweeds (Duffy & Hay 1990). Despite this, some herbivores from temperate kelp beds consume large amounts of algal biomass (Leighton 1966; Vasquez & Buschmann 1997). Some algal consumers, primarily the smaller, less mobile ones, commonly specialize in one type of food (e.g., the habitat-forming macroalgae) and live directly on it, using it as both food and shelter (Hines 1982; Woods 1993; Stachowicz & Hay 1999; Gutow et al. 2012). In contrast, larger individuals that roam farther also incorporate other food items in their diet. This may lead to spatial segregation between different ontogenetic groups. 134 In many habitats, crab consumers have special feeding rhythms to avoid interspecific competition for food and predation risk (Jesse 2001; KronfeldSchor & Dayan 2003). For example, members of many brachyuran species feed mainly during the night, with no or low foraging activity during the day (Aris et al. 1982; Jesse 2001; Novak 2004; Almeida et al. 2008). By limiting their activity period to times of low predation pressure, these crabs reduce the amount of time available for foraging (Aris et al. 1982). Taliepus marginatus (BELL 1835) (Superfamily Majoidea) is a decapod crab widely distributed along the Chilean coast, but little is known about its life cycle. Recently settled juveniles of its congener T. dentatus (MILNE EDWARDS 1834) are commonly found in shallow subtidal habitats, often dominated by turf algae, and while the habitats of growing juveniles and subadults are not known, the reproductive adults generally occur in subtidal kelp forests (Pardo et al. 2007; Palma et al. 2011). Taliepus marginatus has been reported from deeper subtidal waters (Antezana et al. 1965) in subtidal kelp systems dominated by either Macrocystis pyrifera (LINNAEUS) C. AGARDH 1820 or by Lessonia trabeculata VILLOUTA & SANTELICES 1986 (Villegas et al. 2008). These two kelp species show important differences; they develop in different environmental conditions, have contrasting morphological structures (Ortiz 2008; Villegas et al. 2008), and likely differ substantially in their tissue consistency and attractivity for grazers (for differences between M. pyrifera and Lessonia spp. see for example Pansch et al. 2008). Based on these ecological differences, we expected that the natural diet, density, size distribution, and foraging activity of T. marginatus might differ between these two kelp habitats. Specifically, we hypothesized that smaller crabs would be more common in the shallow and dense kelp beds of M. pyrifera, while larger crabs would dominate in the deeper and more open beds of L. trabeculata. We also expected to find differences in the feeding ecology of crabs between the two kelp systems. This study thus aims to contribute to knowledge of the demography and feeding ecology of T. marginatus in two subtidal kelp habitats. The objectives were to compare the (i) size structure, (ii) density, (iii) natural diet, and (iv) daily feeding cycle of T. marginatus inhabiting beds dominated by either M. pyrifera or L. trabeculata. This work is part of an extensive study examining the properties of the kelp forest ecosystems formed by M. pyrifera and L. trabeculata (Ortiz 2008, 2010). Invertebrate Biology vol. 132, no. 2, June 2013 Jofre, Ortiz, & Thiel Methods Study area This study was carried out in austral fall during the months of April 2006 and April 2007 near Isla Santa Marıa at the southern tip of the Mejillones Peninsula (SE Pacific coast, Antofagasta, Chile: 23°27′S–70°36′W). The study area is close to an important upwelling center that supplies nutrients to the coastal ecosystem (Escribano et al. 2004). These nutrient-rich coastal areas are dominated by subtidal kelp forests of Macrocystis pyrifera and Lessonia trabeculata, which develop in different environmental conditions (Ortiz 2008). Macrocystis pyrifera forms extensive and complex patches in coastal areas mostly protected from direct wave exposure, where they often grow on boulders extending over depths of 2–10 m (Vega et al. 2005; Villegas et al. 2008). Blades of M. pyrifera grow along the entire stipe, forming a dense mesh of algal canopy from the bottom to the sea surface (Villegas et al. 2008). In contrast, L. trabeculata grows mostly on more exposed coasts on bedrock ranging in depth from 8 to 14 m (Vega et al. 2005; Villegas et al. 2008). The blades of older kelp stands usually originate from the stipes at some distance above the bottom, but the individual kelp plants rarely exceed 1.5 m in height and thus do not reach the sea surface. Given their different bathymetric distribution, at the study site the kelp forests composed of M. pyrifera are closer to the shore, growing over a gentle slope down to ~6 m depth, while stands of L. trabeculata start at the seaward edge of the M. pyrifera patches, extending in depth from ~5 m down to ~12 m (Fig. 1). Both kelp forests have a high standing biomass, but system throughput (a measure of ecosystem metabolism) in M. pyrifera kelp beds is higher than in L. trabeculata (Ortiz 2008, 2010). A wide diversity of different invertebrates is found in the kelp forests around Isla Santa Marıa; among these, sea urchins and their seastar predators dominate in biomass (Vasquez et al. 2006; Gaymer et al. 2010). Fish predators are also important in these kelp forests (Ortiz 2008), which offer more refuge and food than surrounding barren grounds (e.g., Vasquez et al. 2006; Villegas et al. 2008; Perez-Matus et al. 2012). In these kelp systems, Taliepus marginatus is one of the most abundant brachyuran crabs. Settlement occurs primarily during austral spring (personal observations), and growing juveniles and subadults were expected to be most abundant during late Demography and feeding behavior of a kelp crab 135 Fig. 1. Location of the study area on the Mejillones Peninsula close to Santa Marıa Island, SE Pacific coast (northern Chile), showing Macrocystis pyrifera (dark shading) and Lessonia trabeculata (light shading) kelp forests. Sampling plots in each kelp habitat are shown. summer and fall, as had also been reported for other kelp inhabitants (Gaymer et al. 2010) and for kelp crabs in California (Hines 1982). Consequently, sampling of crabs was conducted during early austral fall (April). Crabs collected during the fall of two subsequent years (2006 and 2007) were pooled herein. Sampling procedure To estimate abundance and size structure of the crabs in the two kelp habitats, we collected samples of T. marginatus from three rectangular plots of 20 m2 (592 m) in each kelp forest (Fig. 1). The positions of these sampling plots were selected from the areas with the highest kelp density, covering the main depth range of each kelp. In the M. pyrifera forest one of the three rectangular plots was placed close to the shore (~3 m deep) and the other two were oriented away from shore (~5–6 m deep), and in the L. trabeculata forest the plots were placed between 8 and 12 m depth. All rectangular plots were linked and fixed by an anchor in the middle (Fig. 1). Each plot was carefully sampled by two scuba divers using semiautonomous (hookah) diving systems. The scuba divers collected crabs on the bottom and in the kelp canopy by carefully surveying the entire fronds (e.g., searching on both sides of the blades). This was done to collect all crabs >10 mm carapace width (CW), including those that were still camouflaged against the canopy background. Crabs were collected by hand and placed into thick-walled plastic bags with handles. These plastic bags were used because kelp crabs quickly entangle in the mesh of regular dive bags. At the end of each sampling, all crabs were transported to the shore for further processing. To preserve the stomach contents, each crab was injected with a solution of 10% formalin in the oral and abdominal regions. This method was used to rapidly stop digestion and degradation processes. All samples were frozen (20°C) for subsequent analysis. Sample analysis In the laboratory, all crabs were identified as T. marginatus according to Retamal (1977). Sex was determined through visual observation of the abdomen. Females were distinguished by a wide abdomen, and all mature females were examined for Invertebrate Biology vol. 132, no. 2, June 2013 136 brooded embryos. The total wet weight of each crab was measured with a semianalytical balance (precision0.1 g). Carapace width (CW) was measured with a digital caliper (precision0.1 mm). In this study, we distinguish two size groups of crabs, juveniles and subadults (10.0–40.0 mm CW), and adult crabs (>40.0 mm CW). The smallest ovigerous female had a CW of 44.8 mm, suggesting that T. marginatus reaches sexual maturity at ~40 mm CW. The cardiac stomachs were extracted from each specimen and the wet weights of the full (before removing stomach contents) and empty stomachs were measured after absorbing excess water with paper tissues. Stomach contents were diluted in distilled water and 10% ethanol and analyzed visually with the aid of a binocular microscope. The contents of each stomach were classified to the lowest possible taxonomic level. Finally, the importance of each food item in the diet of T. marginatus was described in two ways: (i) frequency of occurrence, and (ii) the wet weight of each food item. The frequency of occurrence was estimated based on the presence of a particular item in the stomach using equation (1), ni Fi ¼ N where ni is the number of occurrences (number of stomachs in which the prey i is present) and N is the total number of stomachs containing food. Then, each frequency was multiplied by 100 and expressed as percentage of occurrence (%). A total of 361 crabs were examined in the two kelp habitats (258 in M. pyrifera and 103 in L. trabeculata) for frequency of occurrence. For the wet weight proportions, a total of 181 stomachs (97 from M. pyrifera and 84 from L. trabeculata) were randomly selected from the 361 examined stomachs (Table 1). For this analysis, all food items (by category) were weighed on an analytical balance (precision0.0001 g), and the abundance of each item in each gut expressed as a percentage of total stomach content weight. The combination of the two methods was used to (i) determine whether food items were present in the diet of crabs, and (ii) estimate the proportional wet weight (importance) of each food item in the stomachs. Daily feeding cycle To determine the daily feeding cycle over 24 h, we collected specimens of T. marginatus (n=20) at regular intervals of 6 h (16:00, 22:00, 04:00, 10:00). Each sampling was conducted by two scuba divers. Invertebrate Biology vol. 132, no. 2, June 2013 Jofre, Ortiz, & Thiel The crabs were collected by hand and placed in thick-walled plastic bags with a handle. The divers rapidly collected all visible crabs >40 mm CW, because crabs had to be collected quickly at the defined sampling hours. During the nocturnal samplings it was necessary to use a lantern, and the restricted field of view limited the search efficiency of divers. For this reason it was decided to focus on larger crabs for both the day and the night samples of the daily feeding cycle. These samples were preserved and analyzed as described above. The feeding periodicity of T. marginatus in each kelp forest was assessed by calculating the relative stomach content (SC%) over a 24-h cycle by equation (2): SCð%Þ ¼ gut content (g) 100 body weight (g) This index describes the stomach fullness for each sampling hour (Jesse 2001; Baumann & Kwak 2011). Statistical analyses Prior to analyses, all data were tested for normality using Kolmogorov–Smirnov and Shapiro–Wilk’s tests. Homogeneity of variances was tested with Ftests or with Fligner–Killeen tests. If assumptions were not met, data were transformed or a nonparametric test was applied (Zar 1996). To examine the differences in the median size distribution between kelp habitats, a nonparametric Mann–Whitney U-test was performed. Density data were log-transformed and a t-test was used to examine the differences in crab densities between habitats. To determine whether the proportion of ovigerous females differed between kelp habitats, a chi-squared test (v2) was used. Sizes of ovigerous females from the two kelp habitats were compared with a Student’s t-test. A two-way ANOVA was used to test for significant differences in the daily feeding cycle, with the two factors being time (hour) and site (habitat). When the ANOVAs revealed significant differences, a post hoc Tukey HDS was applied. The analyses were carried out using R (R Development Core Team 2010). Nonmetric multidimensional scaling (nMDS) was performed to assess similarity/dissimilarity in diet (species/taxa: using the proportion of wet weight per food item) between habitats (Macrocystis/Lessonia) and size groups of the crabs (10.0–40.0 mm/ >40.0 mm CW) based on the Bray–Curtis similarity index. Prior to the analysis, the data were square- Demography and feeding behavior of a kelp crab Table 1. Volume proportions (%, meanSD) of each food category (wet weight in g) in the stomach contents of Taliepus marginatus from the two kelp habitats. Dashes indicate absence of the respective food type in the analyzed stomachs. Habitats Stomachs analyzed Food category Macrocystis Lessonia Rhodophyta Hydrozoa Detritus Crustacea Mollusca Bryozoa Gastropod egg capsules a Macrocystis (n=97) % Lessonia (n=84) % 96.35.9 — 2.43.6 0.10.4 0.10.7 0.63.7 0.10.8 a 0.1 0.11.0 — 93.913.3 5.012.2 a 0.1 0.72.0 — 0.11.3 a 0.1 a 0.1 0.1=Weight < 0.1 g. root transformed. Three separate one-way analyses of similarity (ANOSIM) were performed to test the following hypotheses: (A) there are no differences in diet composition of T. marginatus from M. pyrifera and L. trabeculata habitats, and (B-i & B-ii) within each kelp habitat (i & ii) there are no differences in diet composition between immature and adult crabs. In addition, the SIMPER routine was used to establish which species/taxa contributed most to either the similarity or dissimilarity between habitats and habitat per size (Clarke 1993). The multivariate analysis was carried out using PRIMER v.6 (Clarke & Gorley 2006). 137 Results Size distribution and abundance The size distribution of crabs differed significantly between the two kelp habitats (U=28185.5; df=1; p<0.001), even though the range of crab sizes was similar in the two habitats (Fig. 2). The size distribution of females and males in Macrocystis pyrifera varied from 14.0 to 63.9 mm CW (49.716.2 mm; meanSD) and 10.9–91.3 mm (48.39.2 mm), respectively (Fig. 2). In contrast, in Lessonia trabeculata, females ranged 20.9–72.2 mm CW (53.48.4 mm) and males ranged 10.7–97.6 mm (70.618.4 mm) (Fig. 2). The total crab densities were 3.11.6 ind. m2 in M. pyrifera, and 0.70.6 ind. m2 in L. trabeculata; these densities differed significantly between the two kelp habitats (t=4.38; df=12; p<0.001). The proportion of females and males was 49.7% and 50.3%, respectively, in the M. pyrifera habitat, and 28% of all females found in M. pyrifera were ovigerous. In the L. trabeculata habitat, the proportion of females and males was 38.3% and 61.7%, respectively, and 66% of the females were ovigerous. The sizes of ovigerous females did not differ significantly between the two kelp habitats (Macrocystis, n=52; Lessonia, n=27) (t=2.027; df=77; p=0.05). The proportion of ovigerous females was significantly higher in L. trabeculata than in M. pyrifera (v2=21.263; df=1; p<0.001). Diet composition In general, crabs from both habitats had similar diets, but they differed in the proportional occurrence Fig. 2. Size-frequency distribution of Taliepus marginatus in both kelp habitats. Open bars show the total frequency of males and females in both habitats. Black bars show the frequencies of ovigerous females. Data from both study years (April 2006 and April 2007) were pooled. Invertebrate Biology vol. 132, no. 2, June 2013 138 Jofre, Ortiz, & Thiel Fig. 3. Diet composition expressed as frequency of occurrence (as % of individuals) for Taliepus marginatus of two different size ranges (carapace width in mm) in each kelp habitat. n, number of stomachs examined per size range. of kelp tissues and other types of food (Fig. 3). Kelp remains (either M. pyrifera or L. trabeculata) were found in the stomachs of all crabs. Tissues of red algae were also common (~70% of all samples) in crab stomachs, except for the small crabs in L. trabeculata. The most common red algal genera occurring in stomach contents were Chondrus, Chondria, Polysiphonia, Callophyllis, Pterosiphonia, Cryptopleura, and Gastroclonium. Remains of a wide range of other taxa were also detected, particularly Hydrozoa, Mollusca (small pieces of gastropod shells and bivalves, including occasionally complete individuals of Brachidontes granulatus (HANLEY 1843), Bryozoa, Polychaeta, Crustacea (parts of carapaces, pleopods, small shrimps, and amphipods), and egg capsules of neogastropods (Mitrella unifasciata (SOWERBY 1832), Nassarius sp., and Crassilabrum crassilabrum (SOWERBY 1834)) (Fig. 3). Kelp tissues (M. pyrifera and L. trabeculata) were highest in proportional volume (96.35.9 and 93.913.3) of the stomach contents for crabs from both kelp habitats, followed by red algae and other items (Table 1). In both kelp habitats, all individuals of the two crab size categories (10.0–40.0 mm and >40.0 mm) had kelp tissues in their stomachs (Table 2). The small crabs (10.0–40.0 mm) from L. trabeculata had no animal tissues in their stomachs, while all other crabs, including the small crabs from M. pyrifera, also had ingested animal food. Diet composition significantly differed between crabs from both kelp habitats (ANOSIM, R Global=0.93; p<0.001) (Fig. 4). Within each habitat, the diet composition of small crabs (10.0–40.0 mm) also differed from that of the larger crabs (>40.0 mm); this difference was highly significant both in M. pyrifera (ANOSIM, R Global=0.68; p<0.001) and in L. trabeculata (ANOSIM, R Global=0.66; p<0.001) (Fig. 4). The SIMPER routine showed that the two kelp species contribute most to the dissimilarity in diets between habitats and size categories (Table 3A,B). Daily feeding cycle Taliepus marginatus showed a mostly nocturnal daily feeding cycle in both habitats (Fig. 5). There were no significant differences in feeding patterns Table 2. Percentage of individuals of Taliepus marginatus per size class with algal tissues and other kinds of food (animal tissue and detritus) in the stomach contents, in both kelp habitats. Habitats Macrocystis Size range in mm (sample size) Percentage of crabs with algal tissue Percentage of crabs with other tissue Invertebrate Biology vol. 132, no. 2, June 2013 Lessonia 10.0–40.0 (n=67) >40.0–92.0 (n=191) 10.0–40.0 (n=14) >40.0–92.0 (n=89) 100% 31% 100% 46% 100% 0% 100% 58% Demography and feeding behavior of a kelp crab 139 Fig. 4. Nonmetric multidimensional scaling (nMDS) plot, resulting from classification analysis (Bray–Curtis similarities) based on the wet weight (g) of item food (taxa/species) of Taliepus marginatus collected from Macrocystis pyrifera (circles) and Lessonia trabeculata (triangles). Data were square-root transformed for analysis. Open dots and triangles represent immature crabs, filled dots and triangles represent mature crabs. Number of crabs analyzed per habitat: M. pyrifera, n=97, and L. trabeculata, n=84. For SIMPER details see Table 3. between the two kelp habitats (Fig. 5, Table 4). In M. pyrifera, the peak stomach fullness was reached at 22:00, remained high until 4:00, and then decreased until 10:00. In L. trabeculata the feeding pattern was similar, but the peak stomach fullness was reached at 4:00, after which it decreased sharply Table 3. Results of SIMPER analysis of (dis)similarity in diet composition (A) within and between habitats, and (B) between immature and adult crabs (size ranges in mm, CW) from each kelp habitat (i & ii). Based on wet weight of food items (g wet weight per food item) from the stomach contents of Taliepus marginatus. Av. Biomass=mean biomass, Contribution %=contribution percentage of each taxon, Av. Diss.=average of dissimilarity, and Av. Sim.=average of similarity. Av. Biomass (g ww) A. Habitats Between habitats (Av. Diss.=95.75) M. pyrifera L. trabeculata Rhodophyta Within habitats Macrocystis (Av. Sim.=76.07) Lessonia (Av. Sim.=68.77) B. Crab sizes (range mm) ii-a. Macrocystis (Av. Diss.=43.40) M. pyrifera Rhodophyta Crustacea ii-b. Lessonia (Av. Diss.=59.63) L. trabeculta Rhodophyta Contribution % Macrocystis Lessonia n=97 n=84 1.15 0 0.12 0 1.13 0.18 95.14 42.91 6.96 1.13 93.84 93.38 1.15 10.0–40.0 n=14 0.54 0.06 0.05 n=12 0.37 0 >40.0–92.0 n=83 1.25 0.13 0.01 n=72 1.25 0.22 74.15 11.92 5.93 77.96 15.54 Invertebrate Biology vol. 132, no. 2, June 2013 140 Jofre, Ortiz, & Thiel observed in adult crab stomachs may provide energy for reproductive purposes. Overall, these results suggest that the role of the two kelp habitats for T. marginatus varies during the life cycle of the kelp crabs, with M. pyrifera tending to have nursery function and L. trabeculata being more suitable as reproductive habitat. Habitat use Fig. 5. Relative stomach contents (in % body wet weight) of Taliepus marginatus over a 24 h cycle in each kelp habitat. Means and standard deviation (vertical bars) calculated from 20 crab samples at each sampling hour. Different letters indicate significant differences (p<0.001) between sampling hours. For ANOVA details see Table 4. Table 4. Results from the statistical analysis of relative stomach content volume (SC%) using two-factor analysis of variance (ANOVA), with the factors Time (hour: 16:00, 22:00, 4:00, and 10:00) and Site (habitat: Macrocystis and Lessonia). Source df MS F value p-value Hour Habitat Hour: Habitat Residuals 3 1 3 152 11.262 1.886 1.448 0.493 22.808 3.820 2.934 <0.001 0.052 <0.05 until the morning (10:00). In both kelp habitats, the two night samplings differed significantly from the day samplings (Fig. 5, Table 4). Discussion The size distribution of the kelp crab Taliepus marginatus differed between kelp forests dominated by Macrocystis pyrifera and Lessonia trabeculata. While the higher abundance, especially of smaller crabs, in M. pyrifera forests suggests that this kelp could favor the survival and growth of juvenile and subadult crabs, the higher proportion of large males and of ovigerous females in L. trabeculata indicates that this kelp species has an important reproductive function for T. marginatus. In both kelp habitats, kelp tissues were the most abundant food item of T. marginatus, but adult crabs (and small crabs in M. pyrifera) also ingested other food items. The larger proportion of animal food Invertebrate Biology vol. 132, no. 2, June 2013 Many decapod crustaceans have changing habitat requirements during their life cycle. Our field data showed differences in the size distribution and density of T. marginatus between the two kelp habitats, which can be attributed to two possible causes. First, the two kelp species differ in habitat structure (Vega et al. 2005; Villegas et al. 2008), and second, the M. pyrifera kelp forests, due to their density, complexity, and proximity to the coast, could play an important role as nursery habitat for smaller crab individuals. In a field study on the most conspicuous and abundant brachyuran species inhabiting the shallow rocky subtidal zone in central Chile, Pardo et al. (2007) found that settlement and recruitment of T. dentatus (the congener of T. marginatus) occurred mainly on shallow subtidal algal turfs. Furthermore, they could not find larger juveniles in any of the habitats surveyed (e.g., algal turf, cobbles, and shell hash). This might be due to an ontogenetic habitat shift from turf algae to adjacent kelp forests. Small recruits find shelter and protection in shallow subtidal seaweeds (Pardo et al. 2007), which even may offer chemical defenses against fish predators (Palma et al. 2011). Rockfishes are presumed the major predators of settlers and juveniles of most invertebrates in these kelp habitats (Fari~ na et al. 2008). Given the complex structure of M. pyrifera forests, juvenile crabs might escape predation in this habitat, enhancing their recruitment, as also reported for other invertebrate species inhabiting this kelp (Almanza et al. 2012). The presence of the largest (and mostly reproductive) individuals of T. marginatus in the deeper (seaward) L. trabeculata kelp forests has also been reported by Palma et al. (2011), supporting our interpretation that this kelp has an important reproductive function for kelp crabs. Similar observations have also been reported for Pugettia producta (RANDALL 1840) from California kelp forests (Hines 1982; Hultgren & Stachowicz 2010). The size distribution of P. producta varies from the low intertidal zone (Mastro 1981) to the deeper sections of the kelp forest (Hines 1982). Individuals of this Demography and feeding behavior of a kelp crab species are apparently recruiting into intertidal Phyllospadix zones, and subsequently migrate into the subtidal kelp forests (Hines 1982). Several studies on P. producta point out that adult crabs (52– 72 mm CW) prefer kelps as reproductive habitat (Hines 1982; Wicksten & Bostick 1983; Hultgren & Stachowicz 2010). Therefore, the predominance of small recruits in nearshore habitats (turf algae, seagrass, cobble) and of reproductive individuals in the seaward, deeper kelp habitats might be a general pattern for kelp crabs (Hines 1982; Hultgren & Stachowicz 2010; Palma et al. 2011; this study). The ultimate causes (e.g., food availability, shelter, lower competition, larval dispersal) for this apparent habitat shift during ontogeny need to be investigated in future studies. Feeding ecology Individuals of T. marginatus from both habitats consumed large amounts of kelp tissues (M. pyrifera or L. trabeculata), but they differed in the proportion of other food items. High prevalence of the habitat-forming algal species in stomachs has also been observed for other majid species (Leighton 1966; Aracena 1971; Hines 1982; Woods 1993), and for other species associated with kelp habitats, such as echinoids, gastropods, and fishes (PerezMatus et al. 2012). Species that feed on habitatforming kelps obtain certain benefits, which include a large biomass and a predictable availability of resources (Leighton 1966; Wolcott & O′Connor 1992; Daly & Konar 2010; Hultgren & Stachowicz 2010). Examination of the natural diet of T. marginatus showed that in general it can be considered an herbivorous species, but that some individuals (especially adults) also include animal material in their diet. Other majid crabs, such as Loxorhynchus crispatus STIMPSON 1857, Pugettia richii DANA 1851, Notomithrax ursus (HERBST 1788), Taliepus dentatus, and Eurynolambrus australis H. MILNE EDWARDS & LUCAS 1841 also consumed some animal material together with the algae dominating their diets (Hines 1982; Manriquez & Cancino 1991; Woods 1993; Woods & McLay 1996; Cumillaf 2010). Animal food may play a role as a critical nutrient supplement (Wolcott & O′Connor 1992) for growth and reproduction. Algal tissues are poor sources of essential amino acids, vitamins, and sterols, compared with animal material. Nitrogen is considered a limiting nutrient for herbivorous crabs (Wolcott & O′Connor 1992). For instance, nitrogen assimilation efficiencies from an 141 algal diet may be 30% lower than those from an animal diet (Wolcott & Wolcott 1984). Therefore, a supplement of animal protein in the diet might benefit growth and possibly also the reproductive output of kelp crabs. Our results showed differences in the diet of T. marginatus with respect to crab size, similar to results reported for many other crab species (Hines 1982; Stevens et al. 1982; Choy 1986; Woods 1993; Woods & McLay 1996). In majid crabs, body size is a limiting factor during resource utilization (Hines 1982). Different sizes at sexual maturity are also a reflection of species-specific abilities to use microhabitats (e.g., crevices) as refuges from predators (Hines 1982). In our study, the analysis of diet composition within each habitat suggested that immature crabs differ from adults in the use of the kelps. As members of the genus Taliepus live on the stipes and blades of large kelps (Santelices 1989), kelp architecture may constrain their foraging behavior, especially of juvenile and subadult individuals. While there are extensive open spaces under the arborescent L. trabeculata, the closely spaced blades of M. pyrifera offer visual protection along the stipes all the way down to the holdfasts (Villegas et al. 2008), allowing crabs to move up and down within the protective cover of the canopy. As the majority of nonkelp food is found in the kelp holdfasts and on the surrounding seafloor (Santelices 1989; Thiel & Vasquez 2000; Ortiz 2008; Villegas et al. 2008), it is likely that in M. pyrifera all crab sizes descend to the bottom to obtain these food items, while the blade-less stipes of L. trabeculata restrict the movement of juvenile and subadult crabs. This interpretation is also supported by the fact that small kelp crabs have a substantially smaller activity range than adult crabs (Hultgren & Stachowicz 2010). As kelp forest systems have high trophic complexity (e.g., multiple connections between a wide diversity of consumers and resources), development of adaptive foraging behaviors is important. Most organisms exhibit specific feeding rhythms (Hines 1982; Jesse 2001; Kronfeld-Schor & Dayan 2003; Hultgren & Stachowicz 2010). Despite the differences in kelp forest structures, members of T. marginatus showed a similar daily feeding cycle in both kelp habitats, with a mostly nocturnal feeding behavior. The tendency of T. marginatus to feed more at night than during the day may also help mitigate predation risks, very similar to what has been suggested for other species of kelp crabs (Aris et al. 1982; Hultgren & Stachowicz 2010). Invertebrate Biology vol. 132, no. 2, June 2013 142 Jofre, Ortiz, & Thiel Fig. 6. Hypothetical model of the life cycle of kelp crabs Taliepus spp., highlighting the importance of different species of macroalgae. Based on results from the present study and from Pardo et al. (2007) and Palma et al. (2011). Conclusions and outlook Kelp serves as both an important foundation species and a significant energy source for much of the nearshore food web (Dayton 1985; Graham 2004), both at the community and ecosystem level (Ortiz 2008, 2010). The present results on habitat use and feeding behavior demonstrate that T. marginatus uses the macroalgae as food and possibly as refuges during most part of its benthic life cycle (Fig. 6). The results confirm that T. marginatus is an omnivore in both types of kelp habitat, maintaining a strong dependence on kelp tissues throughout their lives, albeit adding other food items as they grow. Both M. pyrifera and L. trabeculata are subject to intensive exploitation (>70,000 tons in 2010) along the Chilean coast (SERNAPESCA 2010). This has led to a notable reduction in the density and coverage of kelp beds. In addition, the effects from El Ni~ no Southern Oscillation (ENSO) also alter the extent of kelp beds (Vega et al. 2005; Gaymer et al. 2010), even causing local kelp extinctions. Because these kelp forests are habitats for the reproductively active populations of T. marginatus, the continued persistence of both kelps is likely to be important for the population dynamics of this kelp consumer. Acknowledgments. We thank Paula Ruz, Rosita Chavez, Manuel Rojo, Luis Rojas, Claudio Silva, Rodrigo Saavedra, Leonardo Campos, and Carlos Alvarez for their help in the fieldwork. In particular, we are grateful Invertebrate Biology vol. 132, no. 2, June 2013 to several anonymous reviewers and to Lucas Eastman for their constructive comments, which were of great help in improving the manuscript. During the preparation of this manuscript, David Jofre Madariaga was partially supported by the CONICYT fellowship program (Becas para Estudios de Magister). This study was financed by FONDECYT 1040293. References Almanza V, Buschmann AH, Hernandez-Gonzalez MC, & Henrıquez LA 2012. Can giant kelp (Macrocystis pyrifera) forests enhance invertebrate recruitment in southern Chile? Mar. Biol. Res. 8: 855–864. Almeida MJ, Flores A, & Queiroga H 2008. Effect of crab size and habitat type on the locomotory activity of juvenile shore crabs, Carcinus maenas. Estuar. Coast. Shelf Sci. 80: 509–516. Amaral V, Cabral HN, & Paula J 2008. Implications of habitat-specific growth and physiological condition on juvenile crab population structure. Mar. Freshw. Res. 59: 726–734. Antezana T, Fagetti E, & L opez MT 1965. Observaciones bioecol ogicas en decapodos comunes de Valparaıso. Rev. Biol. Mar. 12: 1–60. Aracena O 1971. Algunos aspectos de la biologıa de la poblaci on de Taliepus dentatus (Milne Edwards) 1834, en Caleta Leandro, Talcahuano. Tesis para optar al tıtulo de licenciado en Biologıa, Universidad de Concepci on, Chile. 145 pp. Aris JP, Eisemann AD, & Moulton L 1982. The occurrence of Pugettia richii (Crustacea: Decapoda) on Cystoseira osmundacea follows a diel pattern. Bull. Mar. Sci. 32: 243–249. Demography and feeding behavior of a kelp crab Baumann JR & Kwak TJ 2011. Trophic relations of introduced flathead catfish in an Atlantic river. Trans. Am. Fish. Soc. 140: 1120–1134. Choy SC 1986. Natural diet and feeding habits of the crabs Liocarcinus puber and L. holsatus (Decapoda: Brachyura: Portunidae). Mar. Ecol. Prog. Ser. 31: 87– 99. Clarke KR 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18: 117–43. Clarke KR & Gorley RN 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth. 187 pp. Cumillaf JP 2010. Respuestas fisiol ogicas a la carnivorıa y herbivorıa durante el desarrollo bent onico del cangrejo Taliepus dentatus (Milne Edwards, 1834) (Decapoda, Majidae), una aproximaci on bioenergetica. Tesis para optar al tıtulo de ingeniero en Acuicultura, Universidad Austral de Chile, Puerto Montt, Chile. 61 pp. Daly B & Konar B 2010. Temporal trends of two spider crabs (Brachyura: Majoidea) in nearshore kelp habitats in Alaska, USA. Crustaceana 83: 659–669. Dayton PK 1985. Ecology of kelp communities. Annu. Rev. Ecol. Syst. 16: 215–45. Duffy JE & Hay ME 1990. Seaweed adaptations to herbivory. Bioscience 40: 368–376. Escribano R, Rosales SA, & Blanco JL 2004. Understanding upwelling circulation off Antofagasta (northern Chile): a three-dimensional numerical-modeling approach. Cont. Shelf Res. 24: 37–53. Fari~ na JM, Palma AT, & Ojeda FP 2008. Subtidal kelp communities off the temperate Chilean coast. In: Food Webs and the Dynamics of Marine Reefs, Chapter 4. McClanahan TR & Branch GM, eds., pp. 79–102. Oxford University Press, NewYork. Gaymer CF, Palma AT, Vega JMA, Monaco CJ, & Henrıquez LA 2010. Effects of La Ni~ na on recruitment and abundance of juveniles and adults of benthic community-structuring species in northern Chile. Mar. Freshw. Res. 61: 1185–1196. Graham MH 2004. Effects of local deforestation on the diversity and structure of southern California giant kelp forest food webs. Ecosystems 7: 341–357. Gutow L, Long JD, Cerda O, Hinojosa IA, Roth€ausler E, Tala F, & Thiel M 2012. Herbivorous amphipods inhabit protective microhabitats within thalli of giant kelp Macrocystis pyrifera. Mar. Biol. 159: 141–149. Hines AH 1982. Coexistence in a kelp forest: size, population dynamics, and resource partitioning in a guild of spider crabs (Brachyura, Majidae). Ecol. Monogr. 52: 179–198. Hultgren KM & Stachowicz JJ 2010. Size-related habitat shifts facilitated by positive preference induction in a marine kelp crab. Behav. Ecol. 21: 329–336. Jesse S 2001. Comparative ecology of sympatric brachyuran crab species in the shallow subtidal of the Pacific coast of north Chile and their importance for the artisanal fishery Puerto Aldea. PhD Dissertation, University of Bremen, Germany. 125 pp. 143 Kilar JA & Lou RM 1986. The subtleties of camouflage and dietary preference of the decorator crab, Microphrys bicornutus Latreille (Decapoda: Brachyura). J. Exp. Mar. Biol. Ecol. 101: 143–160. Kronfeld-Schor N & Dayan T 2003. Partitioning of time as an ecological resource. Annu. Rev. Ecol. Evol. Syst. 34: 153–181. Leighton DL 1966. Studies of food preference in algivorous invertebrates of southern California kelp beds. Pac. Sci. 20: 104–113. Manriquez PHR & Cancino JM 1991. Depredaci on de Membranipora isabelleana (Bryozoa) por Taliepus dentatus (Crustacea: Decapoda). Rev. Biol. Mar. 26: 309–323. Mastro E 1981. Algal preferences for decoration by the Californian kelp crab, Pugettia producta (Randall) (Decapoda; Majidae). Crustaceana 41: 64–70. Novak M 2004. Diurnal activity in a group of Gulf of Maine decapods. Crustaceana 77: 603–620. Ortiz M 2008. Mass balanced and dynamical simulations of trophic models of kelp ecosystems near the Mejillones Peninsula of northern Chile (SE Pacific): comparative network structure and assessment of harvest strategies. Ecol. Model. 216: 31–46. ———— 2010. Dynamic and spatial model of kelp forest of Macrocystis integrifolia and Lessonia trabeculata (SE Pacific) for assessment harvest scenarios: short-term responses. Aquat. Conserv.: Mar. Freshw. Ecosyst. 20: 494–506. Palma AT, Soto-Gamboa M, & Ojeda FP 2011. Ontogenetic habitat shift of an herbivorous crab: a chemically mediated defense mechanism? Rev. Biol. Mar. Oceanogr. 46: 329–338. Pansch C, G omez I, Roth€ausler E, Veliz K, & Thiel M 2008. Species-specific defense strategies of vegetative versus reproductive blades of the Pacific kelps Lessonia nigrescens and Macrocystis integrifolia. Mar. Biol. 155: 51–62. Pardo LM, Palma AT, Prieto C, Sep ulveda P, Valdivia I, & Ojeda FP 2007. Processes regulating early postsettlement habitat use in a subtidal assemblage of brachyuran decapods. J. Exp. Mar. Biol. Ecol. 344: 10–22. Perez-Matus A, Pledger S, Dıaz FJ, Ferry LA, & V asquez JA 2012. Plasticity in feeding selectivity and trophic structure of kelp forest associated fishes from northern Chile. Rev. Chil. Hist. Nat. 85: 29–48. R Development Core Team 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3900051-07-0, URL http://www.R-project.org/. Retamal MA 1977. Los crustaceos decapodos chilenos de importancia econ omica. Gayana Zool, 39: 1–49. Santelices B 1989. “Algas Marinas de Chile.” Distribuci on, Ecologıa, Utilizaci on y Diversidad. Ediciones Universidad Cat olica de Chile, Santiago, Chile. 399 pp. SERNAPESCA 2010. Anuario Estadıstico de Pesca. Servicio Nacional de Pesca, Santiago, Chile. Invertebrate Biology vol. 132, no. 2, June 2013 144 Smith SDA, Simpson RD, & Cairns SC 1996. The macrofaunal community of Ecklonia radiata holdfasts: description of the faunal assemblage and variation associated with differences in holdfast volume. Aust. J. Ecol. 21: 81–95. Stachowicz JJ & Hay M 1999. Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivores. Ecology 80: 495–509. Steneck R, Graham M, Bourque B, Corbett D, Erlandson J, Estes J, & Tegner M 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29: 436–459. Stevens BG, Armstrong DA, & Cusimano R 1982. Feeding habits of the Dungeness crab Cancer magister as determined by the index of relative importance. Mar. Biol. 72: 135–145. Thiel M & V asquez JA 2000. Are kelp holdfasts island on the ocean floor?- indication for temporarily closed aggregations of peracarid crustaceans. Hydrobiologia 440: 45–54. Vasquez JA 1992. Lessonia trabeculata, a subtidal bottom kelp in northern Chile: a case study for a structural and geographical comparison. In: Coastal Plant Communities of Latin America. Seeliger U, ed. 392 pp. Academic, New York. Vasquez JA & Buschmann AH 1997. Herbivore-kelp interactions in Chilean subtidal communities: a review. Rev. Chil. Hist. Nat. 70: 41–52. Vasquez JA, Vega JMA, & Buschmann AH 2006. Long term variability in the structure of kelp communities in Invertebrate Biology vol. 132, no. 2, June 2013 Jofre, Ortiz, & Thiel northern Chile and the 1997–98 ENSO. J. Appl. Phycol. 18: 505–519. Vega JMA, Vasquez JA, & Buschmann AH 2005. Population biology of the subtidal kelps Macrocystis integrifolia and Lessonia trabeculata (Laminariales, Phaeophyceae) in an upwelling ecosystem of northern Chile: interannual variability and El Ni~ no 1997–1998. Rev. Chil. Hist. Nat. 78: 33–50. Villegas MJ, Laudien J, Sielfeld W, & Arntz WE 2008. Macrocystis integrifolia and Lessonia trabeculata (Laminariales; Phaeophyceae) kelp habitat structures and associated macrobenthic community off northern Chile. Helgol. Mar. Res. 62: 33–43. Wicksten MK & Bostick CR 1983. Migration of kelp crabs (Pugettia producta) at San Pedro, California. J. Crust. Biol. 3: 364–366. Wolcott DL & O′Connor NJ 1992. Herbivory in crabs: adaptations and ecological considerations. Am. Zool. 32: 370–381. Wolcott DL & Wolcott TG 1984. Food quality and cannibalism in the red land crab, Gecarcinus lateralis. Physiol. Zool. 57: 318–324. Woods CMC 1993. Natural diet of the crab Notomithrax ursus (Brachyura, Majidae) at Oaro, South Island, New Zealand. N. Z. J. Mar. Freshw. Res. 27: 309–315. Woods CMC & McLay CL 1996. Diet and cryptic colouration of the crab Eurynolambrus australis (Brachyura: Majidae) at Kaikoura. Crustac. Res. 25: 34–43. Zar JH 1996. Biostatistical Analysis, 3rd ed. Prentice Hall, Upper Saddle River, New Jersey. 662 pp.