versión impresa ISSN 0716-078X
Rev. chil. hist. nat. v.81 n.4 Santiago dic. 2008
Revista Chilena de Historia Natural 81: 575-584,2008
Feeding and nutritional ecology of the edible sea urchin Loxechinus albus in the northern Chilean coast
Ecología nutricional y alimenticia del erizo comestible Loxechinus albus en el norte de Chile
SOLANGE J. GONZÁLEZ2, CRISTIAN W. CÁCERES3 & F. PATRICIO OJEDA1
1 Center for Advanced Studies in Ecology and Biodiversity, Departamento de Ecología, Pontificia Universidad Católica de Chile, CP 6513677, Santiago, Chile * e-mail for correspondence: firstname.lastname@example.org
2 Departamento de Ciencias del Mar, Universidad Arturo Prat, Iquique, Chile.
3 Departamento de Ecología Costera, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Concepción, Chile
The red sea urchin Loxechinus albus, an economically important species oceurring along the Chilean littoral benthic systems, has been heavily exploited by artisanal fisheries in recent decades. However, basic knowledge of its trophic biology is still scarce. Studies of this kind are critical to the successful development of farming techniques as an alternative to the harvest of natural populations. The aims of this study were to quantify the composition of L. albus' natural diet, to determine the assimilation efficieney of the most important dietary components, and to experimentally examine the species' trophic selectivity. Adult and juvenile specimens were sampled in spring 1993 and summer, fall and winter 1994 from the shallow subtidal zone of Iquique, northern Chile. Neither juveniles ñor adults showed significant seasonal differences in dietary composition. The main Ítems in the diet were the green alga Ulva sp. for juveniles and the kelp Lessonia sp. for adults. In adults, assimilation efficieney (as percentage of the total organic matter ingested) was not significantly different among individuals that consumed Lessonia sp. (48.7 %), Ulva sp. (44.6 %) and Macrocystis (38.1 %), whereas in juveniles assimilation efficieney was significantly higher for individuals fed on the chlorophyte Ulva sp. (55.4 %), followed by Lessonia sp. (35.0 %) and Macrocystis (25.5 %). These results suggest that L. albus undergoes an ontogenetic shift in the diet, consisting of a differential foraging strategy between juveniles and adults.
Key words: assimilation efficieney, Loxechinus, natural diet, trophic selectivity.
El erizo Loxechinus albus (Molina, 1782) es un recurso de gran importancia económica en los sistemas bentónicos costeros, y que se encuentra bajo una fuerte presión de explotación. Sin embargo, los antecedentes sobre diversos aspectos básicos de su biología trófica son aún escasos. Estudios de esta naturaleza son importantes en razón a que constituyen la base para el desarrollo de técnicas de cultivo exitosas, alternativa a la explotación de poblaciones naturales. Los objetivos del presente trabajo fueron: determinar cuantitativamente la composición dietaria de L. albus, el grado de selectividad trófica, y las tasas de asimilación de los componentes de su dieta. Especímenes adultos y juveniles fueron muestreados en la primavera de 1993 y el verano, otoño e invierno de 1994 en la zona submareal de Iquique, norte de Chile. No se detectaron diferencias en la composición de la dieta de adultos y juveniles entre las estaciones muestreadas. El principal ítem alimentario de los juveniles y adultos fueron el alga verde Ulva sp. y el alga parda Lessonia sp., respectivamente. En experimentos de selección trófica se observó que los juveniles y adultos prefieren el ítem que es más abundante en su dieta natural. Estos resultados muestran un cambio ontogenético en la dieta de esta especie, sugiriéndose una estrategia de forrajeo diferencial entre juveniles y adultos.
Palabras clave: eficiencia de asimilación, Loxechinus, dieta, selectividad trófica.
The red sea urchin, Loxechinus albus (Molina 1782), is distributed along the South Pacific coast, from northern Perú (6°53'50" S) to Tierra del Fuego (53° 15' S) (Clark 1948, Bernasconi 1953). It is a gregarious, sedentary species inhabiting crevices and ledges in coastal shallow waters (Viviani 1975). It is also a benthic littoral resource of great social and economic importance along the Chilean coast, where it has been intensively exploited over the last decades by artisanal fisheries. Recent studies have shown that exploitation of L. albus has significantly increased, with a total catch of about 300,000 tons between 1984 and 1994 (Vásquez 2001). This amounts to over 20 % of the global sea urchin catch, making it the most heavily exploited echinoderm species in the world (Sernapesca 2006). Its commercial exploitation has virtually led to the extinction of the natural populations along the Chilean coast, where this fishery is currently operating with a closed season and size restriction. Therefore, mass cultivation (hatchery) of L. albus and subsequent repopulation in the wild is a viable alternative to prevent the species extinction and maintain it as an important economic resource. Despite the species' commercial valué, basic biological aspects -from the physiological to the community level-remain poorly known (Vásquez 2001), which poses a constraint on the implementation of management strategies and successful hatchery technology.
In most animáis, feeding and digestión are two interdependent stages of a single process by which most organisms obtain the nutrients and energy necessary to meet their metabolic demands (Penry & Jumars 1986). Accordingly, the mechanisms involved in searching for prey, feeding and digesting are of vital importance because they determine the organisms' nutritional status and reproductive performance (Vadas 1977, Karasov 1990, Penry 1993). Although several factors have been shown to affect the fitness of a predator exploiting a given prey resource, the nutritional valué of the prey and handling cost for the predator are the most important in optimal foraging models (Pyke 1984).
The aim of this study was to describe the feeding behavior and nutritional ecology of juveniles and adults of L. albus in the northern Chilean coast by: (1) determining their natural feeding patterns; (2) exploring relationships between food preferences, nutrient values and assimilation efficiency, and (3) determining their feeding strategies.
MATERIAL AND METHODS
Collection of specimens
Individuals of L. albus were collected from Caleta Los Verdes (20°25' S, 70°08' W), approximately 30 km south of Iquique (northern Chile). Individuals were captured manually by diving in shallow subtidal waters, in spring 1993 and summer, autumn and winter 1994. On each occasion a total of 100 sea urchins were haphazardly collected. They were weighed to the nearest 0.1 g and their test diameter was measured to the nearest 0.01 mm. The urchins were classified into juveniles and adults according to the relationship between sexual maturity and body size, as defined by Bückle et al. (1978).
The gastrointestinal tracts of both juveniles and adults were removed, placed in plástic bags in a solution of 10% formalin with sea water, and transported to the laboratory where the contents were adjusted to a volume of 60 mi. Three 5 mi aliquots were distributed at random on a Petri dish with 30 intersection points and analyzed under a stereoscopic microscope (Castilla & Moreno 1982, Vásquez et al. 1984, Klumpp et al. 1993). Prey Ítems were identified to the lowest taxonomic resolution possible. Kendall's Coefficient of Concordance was used to evaluate seasonal variations in the dietary composition of adults and juveniles (Siegel & Castellan 1988). Ontogenic changes in the diet were evaluated by means of the Spearman's rank correlation coefficient (rs), using frequency of food item in the diet as the dependent variable and body weight as the independent variable.
Prey cholee experiments
Juvenile and adult individuals of L. albus were collected from the study site and transported live to the laboratory in aerated seawater, where they were acclimated in seawater running systems under a natural photoperiod and at an average water temperature of 17 °C.
To evaluate ecologically realistic food selectivity, múltiple prey choice experiments were conducted. Among juveniles, 10 specimens of 35.0 ± 2.4 mm (X ± SE) of test diameter (TD) were offered 10 g of the most abundant Ítems in their diet: the brown algae Lessonia nigrescens (Bory 1826), L. trabeculata (Villouta & Santelices 1986), Glossophora kunthii (C. Agardh; J. Agardh, 1822), Macrocystis integrifolia (Bory, 1826), and the green alga Ulva sp. In adults, a group of 10 specimens of 64.62 ± 3.39 mm (X ± SE) of TD were offered 20 g of the same algal species offered to juveniles. The kelp Macrocystis integrifolia was included in these experiments because it was an abundant algal component in the northern Chilean coast until it was wiped out during a strong ENSO event in 1982-1983 (Soto 1985), and because it has been reported as an important component of L. albus's natural diet in other Chilean sites (Bückle et al. 1980, Vásquez et al. 1984). All these experiments were replicated three times.
Before each experiment, juvenile and adult urchins were starved until no feces were observed in the tanks (72 h) (Larson et al. 1980, Hay et al. 1986). Each experiment lasted 24 h under a natural photoperiod. At the end of the experiments, the remaining algae were removed and weighed to calcúlate total consumption rates. Statistical differences between consumption of the different Ítems were evaluated using Friedman's non-parametric test (Siegel & Castellan 1988, Manly 1993).
Digestibility and nutritional food values
To evaluate the assimilation digestibility efficiency of organic matter of the most important Ítems in the diet of L. albus, four groups composed of 10 juveniles and 10 adults each, were fed with 30 g of each of the algae most frequently consumed in the prey choice experiments. Before each experiment, the urchins were starved for 72 h. After 24 h. the feces produced during each experiment were siphoned out onto Whatman N 1 filter paper and dried. Assimilation efficiency was determined by an indirect method (Montgomery & Gerking 1980, Targett & Targett 1990, Benavides et al 2005), which compares organic and ash content in food and feces, using ash as a non-absorbed reference marker. Assimilation efficiency was calculated using the following formula: [1 - (% ash in food / % ash in feces)] x 100%. The differences between the Ítems assayed were evaluated using a Kruskal-Wallis non-parametric ANOVA, and an a-posteriori test (Siegel & Castellan 1988).
Energy content of each algal item used in the experiments was determined in a Parr 1261 computerized calorimeter. Two replicates were determined to be ash free and reliable when the difference between two measurements was less than 1 %. Protein content was measured by a modification of the method used by Lowry et al. (1951). The percentage of ash content in the algal samples was determined by heating 3 sub-samples at 650 °C for 4 h in a muffle furnace.
Test diameter in both adults and juveniles of L. albus did not show seasonal variation (Kruskal-Wallis ANOVA, H = 3.75, P = 0.29; H = 2.02, P = 0.57 for adults and juveniles, respectively) and ranged between 21.9 and 126.9 mm, 33.2 mm being the average diameter for juveniles and 70.8 mm for adults (Table 1). Body weight, however, showed seasonal variations (Kruskal-Wallis ANOVA, H = 15.42, P < 0.01; H = 23.91, P < 0.01 for juveniles and adults, respectively). The greatest mean body weight for adults and the lowest weight for juveniles were observed in winter (Table 1).
The analysis of the diet of L. albus showed that this is a strictly herbivorous species. Algae comprised 100% of the Ítems found in the guts in all seasons. The most frequent dietary Ítems found in L. albus were: three phaeophytes (Lessonia sp., Halopteris sp., and Glossophora sp.), two chlorophytes (Ulva sp. and Enteromorpha sp.) and three rhodophytes (Gelidium sp., Centroceras sp., and Polysiphonia sp.). Of these algae, Ulva sp., Lessonia sp. and Halopteris sp., comprised over 98 % of the diet of L. albus juveniles and adults. No significant seasonal differences were detected in the diet (Kendall's coefficient of concordance, W = 1, P < 0.01; W = 0.925, P < 0.01 for adults and juveniles, respectively).
In adults, the brown algae Lessonia sp. and Halopteris sp. were the most abundant food items in all seasons sampled, comprising 72.5 and 17.7 % of the average gut contents, respectively, followed by the green alga Ulva sp. with 7.7 % (Table 2). Ulva sp. was the most important food item (49.2 %) in juveniles' diet, followed by Lessonia sp. and Halopteris sp. (26.3 and 21.4 %, respectively; Table 2).
During its ontogeny, L. albus showed marked dietary differences. The relative abundance of Ulva sp. in the diet decreased sharply as L. albus' body size increased. A similar trend was observed for Halopteris sp. In contrast, Lessonia sp., showed a marked increase with L. albus' increasing body size (Sperman's rank correlation, rs = -0.47, P < 0.01 for Ulva sp.; rs = -0.29, P < 0.01 for Halopteris sp.; rs = 0.55, P < 0.01 for Lessonia sp.).
Prey cholee experiments
The results of múltiple prey choice experiments reject the nuil hypothesis of no prey selection in both juvenile and adult urchins (Friedman test, X2 = 14.61, P < 0.05 for juveniles; X2 = 12.43, P < 0.05 for adults). Of the six items offered to juveniles, Ulva sp. was the preferred alga, whereas Halopteris hordacea and Glossophora kunthii were the least consumed items. In contrast, in adults the preferred item was Macrocystis integrifolia, whereas H. hordacea and G. kunthii were less consumed (Fig. 1).
Assimilation efficiency and nutritional food values
The energy content analysis of the five most important food items in L. albus diet (Lessonia nigrescens, Lessonia trabeculata, Halopteris hordacea, Ulva sp., and Glossophora kunthii), and of the kelp M. integrifolia, showed that Ulva sp. exhibits the highest caloric valué (ash free), followed by L. trabeculata, then by L. nigrescens and G. kunthii with similar values. The lowest values corresponded to Macrocystis integrifolia and H. hordacea (Table 3). Lessonia trabeculata and L. nigrescens had the highest protein content values (16.1 and 13.1 %, respectively). Glossophora kunthii, Ulva sp.. and H. hordacea exhibited similar protein levels, and the lowest caloric content (3.6 %) was observed in M. integrifolia (Table 3).
Assimilation efficiency in adults was not significantly different for the different algae assayed, the greater values corresponding to those individuals fed on Lessonia nigrescens (48.7 %). followed by Ulva sp. (44.6 %) and M. integrifolia (38.1 %) (Kuskal-Wallis test, H = 1.77, P = 0.41). On the other hand, assimilation efficiency in juveniles was significantly higher for Ulva sp. (55.4 %), followed by L. nigrescens (35.0 %), and lowest for M. integrifolia (25.5 %) (Kuskal-Wallis test, H = 6.48, P < 0.05) (Table 4).
Seasonal differences in individual biomass observed in Loxechinus albus may be related to seasonal differences in feeding rates. Previous studies on this species in central Chile reported a decrease in ingestión of plant material during the autumn-winter period, probably due to reproductive events and to fluctuations in algal availability (Bückle et al. 1980, Bay-Schmith 1982). Similarly, southern populations of this species show strong seasonal differences in energy allocation as response to food availability and reproduction (Pérez et al. 2008).
The diet of L. albus comprised eight algal taxa, the most important for adults being the brown algae Lessonia sp. and Halopteris sp., which together accounted for over 80% of the total diet between spring 1993 and winter 1994. These Ítems were followed by the green alga Ulva sp., the red algae Centroceras sp.. Polysiphonia sp. and Gelidium sp., representing less than 1 % of the total diet. The prevalence of brown algae in the diet was also observed in others populations of L. albus from the central and southern Chilean coast (Bückle et al. 1980, Castilla & Moreno 1982, Vásquez et al. 1984), suggesting that brown algae are the most palatable components in the diet of adult sea urchins. This pattern can be primarily attributed to changes in digestive performance of adults probably related to the presence of enteric bacteria capable to break down the cell wall of phaeophytes, a characteristic that has been occasionally observed in sea urchins (Eppley & Lasker 1959, Harris 1993). In contrast, in juveniles, the most important item was Ulva sp. The prevalence of this green alga in the diet of L. albus has been reported earlier (Contreras & Castilla 1987, Santelices 1989, Bustos et al. 1991). This preference in juveniles for green algae could be attributed to facilitated digestión of starch over laminarin or a size effect that mechanical limits access to nutrients in a more rigid and leathery brown algae (Cáceres & Ojeda2000).
The absence of seasonal changes in the diet of juveniles and adults may be because most of its trophic components (Lessonia, Halopteris, Ulva, Glossophora) are perennial and annual species that did not exhibit important seasonal fluctuations in the study site (S.J. González, personal observations). This disagrees with observations along the central and southern coast of Chile, where macroalgal communities undergo marked seasonal variations in diversity and abundance (Santelices 1989). For other Chilean species, particularly fish, these regional differences are reflected in the organisms' fitness and reproductive output (Cáceres et al. 1994).
Multiple prey cholee experiments
Our results show that L. albus juveniles preferred Ulva, which was also the most important prey item in their diet during the sampling period. Similar results were obtained in other locations of the Chilean coast (Contreras & Castilla 1987, Santelices 1989, Bustos et al. 1991). Juveniles may prefer green algae because green algal compounds are more digestible than those of brown algae. Furthermore, previous studies reported that juveniles fed on Ulva grew faster than those fed on M. pyrifera (Bustos et al. 1991). Similar results were reported for other echinoid species by Lawrence & Lañe (1982) and Dafni (1992).
Loxechinus albus juveniles assimilated Ulva sp. more efficiently (55.4 %) than adults (44.6 %). The opposite situation was observed with the brown alga L. nigrescens. Such differences in assimilation efficieney may be due to ontogenic changes in the composition of the symbiotic bacterial flora in the digestive tract. These findings suggest that sea urchins have a great capacity to digest food efficiently (Fong & Mann 1980, Yano et al. 1993). Enteric bacteria would play an important role in food digestión, as in other species (Fuji 1967, Lawrence 1975, Fong & Mann 1980, Harris 1993, Yano et al. 1993, Bozinovic & Martínez del Río 1996). Neither juveniles ñor adults showed preference for Glossophora kunthii. This trophic behavior is consistent with the natural diet found in the stomach of L. albus (1.8 % of G. kunthii in juveniles and 1.5 % in adults) and could be due to the presence of secondary metabolites in this alga that would act as a deterrent to herbivores (Arroyo et al. 1991, Martínez 1996).
The brown algae H. hordacea was the third most frequent (26.3 %) trophic item present in the diet of juveniles. These results together with results of múltiple feeding preference experiments show that L. albus juveniles do not prefer H. hordacea, suggesting that its consumption is related to its natural availability. This is consistent with results of Vadas (1977), who showed that Strongylocentrotus spp. consume the alga Agarum in the laboratory in a lower amount than in the natural environment. The study of herbivores' diet is considered complex because of several factors: the prevalence of food Ítems of low nutritional quality, the difficulties in selecting a balanced diet consistent with herbivores' nutritional requirements, and herbivores' need to avoid over-ingestion of the plants' secondary compounds (Lawrence 1975, Webster 1975, Hughes 1980, Krebs et al. 1983, Belovsky 1984, Pyke 1984, Stephens & Krebs 1986, Dearing & Schall 1992, Bozinovic & Martínez del Río 1996). In our study, L. albus clearly preferred food Ítems with the highest protein content and energy values, henee the highest fitness valué. Results of the absorption efficiency experiments may explain the natural dietary composition patterns mentioned above. Thus, juveniles absorbed the green alga Ulva more efficiently than the other algae assayed. Ulva was the most frequently consumed item in múltiple and dichotomic food preference experiments and was also the most abundant food item in the natural diet of L. albus juvenile stages (González 1995). Our findings are not consistent with the results of González et al. (1993), who found that juveniles of L. albus of southern Chile populations did not meet their metabolic requirements with Ulva because of higher losses of metabolic nitrogen as compared to other algae (M. pyrifera and Gracilaria sp.). The reason for such inconsistent results may be related to an effect of temperature on the physiology of this ectothermic invertebrate. For instance, Bückle et al. (1980) demonstrated that individuals of the southern Chilean coast consumed higher amounts of food and showed lower reproductive output and growth rates than those from the central coast, this suggest a lack of compensatory mechanisms against a thermal gradient. This paucity could partially explain the apparent lower incidence of Loxechinus' herbivory in the structure of the southern subtidal algal stand (Dayton 1985).
The metabolic requirements of an average juvenile individual would be met by consuming a lower amount of the green alga Ulva than of Lessonia or Macrocystis. In the study site, Ulva was less abundant than Lessonia or Macrocystis, suggesting that L. albus juveniles would act as energy maximizers (sensu Emlen 1966), Le., they would consume the food that reports a higher energy input and nutrient gain-assuming a constant handling and searching time- thus obtaining a higher scope for growth and maintenance. On the contrary, L. albus adults would have a conformist behavior, foraging on a single patch of brown algae, the most abundant resource, during the necessary amount of time.
In comparison to terrestrial herbivores, specialization and co-evolutionary development of defenses are less common in marine systems (Stimson et al. 2007). This difference allows large marine invertebrates to change their dietary patterns as a plastic response to food availability and metabolic demand, and consequently are suitable models for testing predictions derived from foraging theory.
We thank C. Brieba, R. Pinto, B. Ostojic, N. León, and P. Haye for their laboratory and field assistance. F. Bozinovic and J. Brasca made valuable comments that greatly improved the manuscript. This study was funded by Fondecyt grant 1941205, DIPUC grant 356-96, and FONDAP 1501-0001 (program 5) to F.P.O.
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Associate Editor: Jorge Navarro
Received May 16, 2008; accepted October 20, 2008