Printer Friendly

The effect of seasonality on gonad fatty acids of the sea urchins Paracentrotus lividus and Arbacia lixula (Echinodermata: Echinoidea).

ABSTRACT The sea urchins Paracentrotus lividus and Arbacia lixula were collected monthly for 1 y in the southern coast of Spain and their gonad fatty acids were analyzed to evaluate seasonal variations. The gonad fatty acids of A. lixula significantly differed from those of P. lividus, probably because of substantial differences in diet. In both sea urchins, seasonal changes were mainly characterized by the marked decrease of the major polyunsaturated fatty acid 20:5n-3 in summer and early autumn, and the opposite increase of 20:1n-11, 18: 1n-9 and the principal nonmethylene-interrupted diene 20:2[DELTA]5,11. Arachidonic acid showed the lowest levels in winter, increasing in April through May, and remaining at relatively high levels until the end of the year. Saturated fatty acids were less affected by seasonality, although they tended to decrease with advancing maturity of the gonad and to increase after spawning.

These seasonal changes are discussed in relation to the annual reproductive cycle and to fluctuations in seawater temperature.

KEY WORDS: sea urchin, fatty acid, gonad, Paracentrotus, Arbacia, seasonal changes

INTRODUCTION

The sea urchins Paracentrotus lividus (Lamarck, 1816) and Arbacia lixula (Linnaeus, 1758) are 2 species common in shallow subtidal habitats of the Mediterranean and Atlantic coasts of Spain. P. lividus is an opportunistic generalist species able to exploit a number of food sources, although brown macroalgae and seagrasses constitute the main feeding resource (Boudouresque & Verlaque 2007, Privitera et al. 2008). A. lixula, however, shows a strong preference for encrusting corallines (Frantzis et al. 1988, Privitera et al. 2008). The gonads of both species are suitable for human consumption and in Spain constitute a valuable product for the fisheries industry. Indeed, its capture is strictly regulated because the populations have been intensely exploited. However, P. lividus is usually more appreciated because of the higher size of its gonads and, thus, aquaculture investigation has been mainly focused on P. lividus rather than in A. lixula. In fact, a research national project supported by the Spanish government is being carried out (since 2006) with the aim of developing the culture and management of P. lividus. With this project, the natural populations are being genetically studied, and juveniles obtained in a hatchery are moving to their natural field for restocking the populations. Studies in a controlled, offshore marine system are also carried out to optimize the growth and survival providing different diets.

Sea urchins have a reproductive cycle mainly characterized by a growing stage, during which nutrients accumulate in the gonad nutritive phagocytes; a maturation stage, during which these nutrients are transferred to germ cells for gametogenesis; and finally a spawning stage, when mature spermatozoa and ova are released from the gonad (Walker et al. 2007). This reproductive cycle is linked to seasonal changes of temperature and photoperiod (Walker et al. 2007), although the quantity and quality of food can also influence gonad growth (Marsh & Watts 2007). The biochemical composition of the sea urchin gonads has been studied in different species, and its seasonal changes and possible relationship with the reproductive cycle investigated. Proteins usually increase during growing and maturation stages, decreasing with spawning, whereas glycogen accumulates in nutritive phagocytes but declines when gametogenesis initiates (Marsh & Watts 2007). Changes in lipid content are less clear but tend to be similar to that of glycogen, with higher levels during the growing phase and a decrease before spawning (Fenaux et al. 1977, Fernandez 1998, Montero-Torreiro & Garcia-Martinez 2003). However, little information is available about the seasonal changes of fatty acids and their possible relation to reproduction and/or environmental factors. Fatty acids are an important energy source and, in addition to their possible use during gametogenesis, they are needed by spermatozoa for swimming (Mita & Nakamura 2001); in ova, they can be important for larval development and survival (Khozina et al. 1978, Yasumasu et al. 1984, Sewell 2005). In addition, polyunsaturated fatty acids have important structural roles in membranes and are needed for the synthesis of eicosanoids (active biological compounds that are known to be implicated in reproduction) (Stanley-Samuelson 1994). Therefore, to have detailed information about changes in fatty acids during an annual cycle could be important for better management of sea urchins in aquaculture.

The current study focuses on gonad fatty acids of the sea urchins A. lixula and P. lividus, which were sampled monthly during 1 y at 2 different locations along the southern coast of Spain. We analyze the seasonal changes of gonad fatty acids and discuss their possible relation to the annual reproductive cycle and/or seawater temperature fluctuations. We also compare the gonad fatty acid profile of A. lixula with that of P. lividus in relation to differences in diet and endogenous synthesis.

MATERIALS AND METHODS

Sample Collection

The study was conducted at 2 locations on the south shore of Spain: La Herradura on the southeastern coast (3[degrees]45'29"W, 36[degrees]44'14"N) and Torregorda on the southwestern side (6[degrees]15'0"W, 36028 1"N; Fig. 1). Specimens of P. lividus were collected at Torregorda and those of A. lixula were collected at La Herradura. The sampling station of La Herradura, located at depths between 3 m and 7 m, has vertical walls and large rocks lying on a soft bottom with sandy and pebbly patches. It is a sheltered area, exposed to low hydrodynamics. The studied assemblages are dominated by seaweed, mainly the articulated red algae Corallina elongata, some encrusting coralline algae such as those of the genera Lithophyllum and Mesophyllum, and some frondose brown and red algae such as Cystoseira sp., Halopteris scoparia, Padina pavonica, Sphacelaria sp., Colpomenia sinuosa, and Asparagopsis armata. Torregorda is an intertidal area where the bottom is a horizontal rocky platform with many pools. It is exposed to high hydrodynamics. With respect to the seaweed structure, there is a community of red turf algae such as those of the genera Gelidium, Caulacanthus, and Corallina; some brown algae such as Dyctiota dichotoma and Dilophusfasciola; and some species of the green algae Enteromorpha and Ulva. The sea urchins were found on the walls of the pools. Although La Herradura is located in the Mediterranean Sea and Torregorda along the coast of the Atlantic Ocean, differences in water temperature between both locations are usually small. Table 1 shows the values for sampling seawater temperatures obtained during the year 2003, when the specimens of both sea urchin species were collected. The data were taken with a probe (Oxiguard delta model, Oxiguard, Birkerod, Denmark).

[FIGURE 1 OMITTED]

A. lixula and P. lividus were sampled monthly for 1 year (January through December 2003). Each month, 20 individuals of both sea urchin species were collected and brought to the laboratory, where they were weighed, and their gonads removed and weighed for gonad index (GI) calculation. In addition, 6 gonads were stored at -30[degrees]C for fatty acid analysis. The GI was calculated as GI = 100 x Wet weight of gonads/Wet weight of the whole animal.

Fatty Acid Analysis

For each individual, 1 gonad was weighed and homogenized in 0.9% NaCl (1:2 w/v). The fatty acid methyl esters were prepared by a direct transesterification reaction according to Lepage and Roy (1987). Briefly, 2 mL methanol-benzene--4:1 (v/v) was added to 0.2 mL homogenate and then, while stirring, 0.2 mL acetyl chloride was slowly added. Nonadecanoic acid was added to act as an internal standard. Tubes were tightly closed and maintained at 100[degrees]C for 1 h. After cooling, 5 mL 6% [K.sub.2][C[O.sub.3] solution was added. The tubes were then shaken and centrifuged, and the benzene upper phase was recovered for fatty acid analysis.

Fatty acid methyl esters were separated by gas--liquid chromatography using a Hewlett-Packard 5890 gas chromatograph equipped with a fused silica capillary column (30 m x 0.25 mm internal diameter) coated with TR-WAX and supplied by Teknokroma (Barcelona, Spain). The initial column temperature was 190[degrees]C, with an initial hold time of 10 min, and was programmed to 240[degrees]C at a rate of 2[degrees]C/min and a final hold time of 10 min. The temperature of the injector was 250[degrees]C and that of the detector was 275[degrees]C. Peaks were identified by comparison with known standards (FAME mix C4-C24, Supelco/Sigma-Aldrich) and with a well-characterized profile of menhaden fish oil (Supelco-Sigma-Aldrich). The identification of nonmethylene-interrupted dienoic (NMID) fatty acids was based upon the work of Takagi et al. (1986), because these compounds do not appear either in the FAME mix or in menhaden oil. The results were reported as area percentages.

Statistical Analysis

One-way analysis of variance (ANOVA), followed by the Student-Newman-Keuls test, was used to determine differences in fatty acids between P. lividus and A. lixula and to evaluate seasonal significant differences of gonad fatty acids. Prior to performing parametric tests, the normality of the data and homogeneity of variances were checked. Sygmastat 3.5 software was used for the statistical analyses.

RESULTS

Gonad fatty acid composition of the sea urchin P. lividus collected at Torregorda, in the Atlantic Ocean, and of A. lixula collected at La Herradura, in the Mediterranean Sea, is shown in Table 2. Data are the average of samples collected for 1 y. Significant higher percentages of total saturated fatty acids (SFAs) and monounsaturated fatty acids (MUFAs), and lower levels of total polyunsaturated fatty acids of the n-6 series (n-6 PUFA) and n-3 series (n-3 PUFA) were found in P. lividus compared with A. lixula. The increase in SFA was mainly the result of myristic acid (14:0), with a percentage that was more than 3 times higher in P. lividus than in A. lixula. Palmitic acid (16:0), the major SFA, was also significantly higher, but stearic acid (18:0) and other minor saturates (15:0, 17:0, and 20:0) were more elevated in the gonads of A. lixula. The three n-9 MUFAs, 18:1n-9 (oleic acid), 20:1n-9, and 22:1n-9, were found in higher percentages in the gonads of P. lividus than in A. lixula, whereas the levels of 18:1n-7, 20:1n-7, and 20:1n-11 were lower. The 2 essential fatty acids linoleic (18:2n-6) and [alpha]-linolenic (18:3n-3) acids were found in higher proportions in the gonads of P. lividus than in A. lixula. However, most of their long-chain derivatives (20:4n-6, 20:5n-3, 22:5n-3, 22:6n-3) were higher in A. lixula. The 2 NMIDs 20:2[DELTA]5,11 and 20:2[DELTA]5,13 showed higher percentages in P. lividus than in A. lixula.

To investigate the annual reproductive cycle of A. lixula and P. lividus, the GI was calculated monthly from January to December. As shown in Figure 2, the GI reached its maximum values in April for P. lividus and in May for A. lixula, indicating the end of the maturing period and the beginning of spawning. In addition, in both sea urchin species, GI showed a second minor peak, observed in February for A. lixula and in July for P. lividus, which suggests the existence of a secondary and less important spawn.

Significant seasonal variations were found when the gonad fatty acids of A. lixula and P. lividus were analyzed monthly from January to December. The most interesting data are shown in Figures 3 through 10, and results of the ANOVA are shown in Table 3. Annual changes of PUFA were mainly characterized by the marked decrease of n-3 PUFA in summer and early autumn (Fig. 3A) and the opposite increase of n-6 PUFA, which remained at high values from April/May to November (Fig. 3B). The two major PUFAs, 20:5n-3 and 20:4n-6, were principally responsible for these temporal variations (Fig. 4), although some other minor long-chain PUFAs such as 22:5n-3 and 22:5n-6 also contributed to some extent (data not shown); 22:6n-3 did not vary during the year (Fig. 4).

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Figure 5 shows seasonal changes of the 2 essentials fatty acids 18:2n-6 and 18:3n-3, as well as 18:4n-Y In P. lividus, the 3 fatty acids showed similar variations characterized by a significant drop in April and May, and a subsequent recovery of the values, more pronounced in 18:3-n3 and 18:4n-3, and slower in 18:2n-6 (Fig. 5A). In the gonads of A. lixula, these fatty acids did not show significant seasonal variations but their annual profile clearly paralleled. As shown in Figure 5B, their levels remained constant throughout the year, with the exception of

a decrease in February and a clear increase in August.

The annual variations of the principal NMID, 20:2[DELTA]5,11, for A. lixula and P. lividus are shown in Figure 6. The most interesting finding was the significant increase observed in both sea urchin species from July/August to October. The rest of the year, this fatty acid showed only minor changes.

Total MUFA significantly increased during summer and early autumn in the 2 sea urchin species (Fig. 7), but although in P. lividus MUFA declined from January to April and then began to increase, in A. lixula this index remained rather constant during the first half of the year. However, as shown in Figure 8, not all the MU FAs followed this annual cycle. Oleic acid and 20:1n-11 also showed their highest values in summer. However, 18:1n-7 and, in P. lividus, 16:1n-7 decreased, too, during the warmer months.

SFAs showed only minor changes. As seen in Figure 9, SEA did not vary significantly during the year in A. lixula, whereas in P. lividus it showed a significant decrease from March to May, an increase in June, and then remained rather constant during the second half of the year. In P. lividus, 14:0 and 16:0 showed a similar annual profile that clearly paralleled that of total SFA (Fig. 10A). In A. lixula, 16:0 was the only SFA with seasonal variations, with a significant decrease in July (Fig. 10B). Dimethyl acetal 18:0 (DMA 18) acid also varied significantly during the year, showing the highest levels from July to October in A. lixula (Fig. 10B) and from April to October in P. lividus (Fig. 10A).

DISCUSSION

In this study, gonad fatty acid composition of A. lixula was found to be clearly distinct from that of P. lividus, with lower levels of SFAs and MUFAs, and higher percentages of n-6 and n-3 polyunsaturates, probably because of substantial differences in diet. It is well known that tissue fatty acid composition is influenced by the source of dietary lipids and, indeed, in marine ecosystems, some fatty acids have been used as indicators to characterize specific food webs (Kharlamenko et al. 1995, Reuss & Poulsen 2002). In sea urchins, Serrazanetti et al. (1995) found low levels of 20:4n-6 in the soft tissues of P. lividus from the Adriatic Sea that they justified by the almost total absence of this fatty acid in UIva lactuca, the main algae consumed by the sea urchin in this location. Similarly, Cook et al. (2000) found higher levels of 20:4n-6 in the gonads of Psammechinus miliaris fed with Laminaria saccharina, a macroalgae enriched in this fatty acid, than in those fed a salmon diet containing less than 1% of 20:4n-6. Castell et al. (2004), using different mixtures of corn, linseed, and menhaden oil, also investigated the influence of the dietary lipid source in Strongylocentrotus droebachiensis fatty acid composition and found that the tissue levels of 18:1n-9, 18:2n-6, 18:3n-3, 20:4n-6, and 20:5n-3 strongly reflected the levels of these fatty acids in the diet.

[FIGURE 4 OMITTED]

It has been reported that P. lividus usually feeds on brown algae and less frequently on green algae (Boudouresque & Verlaque 2007, Privitera et al. 2008), whereas A. lixula is a main grazer of encrusting coralline algae (Frantzis et al. 1988, Privitera et al. 2008). Although we did not analyze the fatty acids of the algae found at the sampling sites, it has been reported that brown algae usually have higher proportions of 14:0, 18:1n-9, and C18 PUFAs (18:2n-6, 18:3n-3, 18:4n-3) than red algae and lower amounts of 20:4n-6 and 20:5n-3 (Dembitsky et al. 1990, Dembitsky et al. 1991, Khotimchenko 1998, Khotimchenko et al. 2002, Li et al. 2002). Therefore, the higher levels of 14:0, 18:1n-9, 18:2n-6, and 18:3n-3, and the lower percentages of 20:4n-6 and 20:5n-3 found in the gonads of P. lividus compared with A. lixula possibly reflect differences in the fatty acid content of brown and red algae.

Nevertheless, as recently reported in S. droebachiensis (Kelly et al. 2008), the composition of gonad fatty acids is also dependent on endogenous synthesis, and therefore their presence in the tissue lipids may also be related to the ability of the sea urchin species to synthesize them. For example, the higher level of 18:0 and 20:0 found in the gonads of A. lixula with respect to P. lividus suggests that A. lixula has an enhanced ability to elongate 16:0. Similarly, elongation of 18:1n-9 seems to be favored in P. lividus as its 2 long-chain derivatives 20:1n-9 and 22:1n-9 were higher than in A. lixula.

[FIGURE 5 OMITTED]

The presence of 20 and 22 carbon NMID has been previously reported in the soft tissues ofP. lividus (Serrazanetti et al. 1995) as well as in other sea urchin species (Takagi et al. 1986, Cook et al. 2000, Liyana-Pathirana et al. 2002, Castell et al. 2004, Hughes et al. 2005). These fatty acids are not usually found in algae, and thus their presence in the gonads of both sea urchins suggests that they have been formed endogenously from 20:1n-9 and 20:1n-7, following the same metabolic pathway described by Zhukova (1986, 1991) in molluscs. The higher level of the N MID 20:2[DELTA]5, 11 in the gonads of P. lividus might also be related to the higher percentage of 20:1n-9, its immediate precursor. However, although 20:1n-7 was higher in the gonads of A. lixula than in P. lividus, the NMID 20:2[DELTA]5,13 was significantly lower. This suggests that the synthesis of NMID can depend on the availability of their precursors, but could also be species specific.

Some previous studies have described seasonal variations of the principal biochemical components of the gonads of A. lixula (Fenaux et al. 1977) and P. lividus (Fernandez 1998, Montero-Torreiro & Garcia-Martinez 2003, Dincer & Cakli 2007), but information about the annual variations of fatty acids is scarce. In this study we found that gonad fatty acids vary significantly during the year, and that these variations are similar in P. lividus and A. lixula despite the marked differences in their fatty acid composition and their different feeding habits. Two main factors could be responsible for these seasonal variations: fluctuations in seawater temperature and the annual gametogenic cycle.

[FIGURE 6 OMITTED]

It is well known that sea urchins show an annual reproductive cycle that is influenced by photoperiod, temperature, and food quality and quantity (Walker et al. 2007). In our study, in agreement with previous studies (Fenaux et al. 1977, Byrne 1990, Montero-Torreiro & Garcia-Martinez 2003, Sanchez-Espana et al. 2004, Bayed et al. 2005), both sea urchin species showed 1 main spawning period that, in P. lividus, started in May and, in A. lixula, started in June. Seasonal variations of gonad biochemical components have been related to the gametogenic cycle. Although proteins increase during the growing and maturation stages, and then decrease with spawning, glycogen accumulates in nutritive phagocytes as they develop, but decline after gametogenesis is initiated (Marsh & Watts 2007). The behavior of lipids is less clear, but in P. lividus (Fernandez 1998, Montero-Torreiro & Garcia-Martinez 2003) as well as in A. lixula (Fenaux et al. 1977), it has been shown that they tended to be higher during the growing phase but decreased before spawning, suggesting that lipids are being used as an energy source for gametogenesis. In the gonads of P. lividus, changes of the fatty acids 14:0, 16:0, 16:1n-7, and 18:1n-7 also appear to indicate that they are being used as energy for gametogenesis because they clearly decreased when the GI was reaching its maximum values and during spawning. After spawning, when gonads initiate a new gametogenic cycle and nutritive phagocytes are being refilled with triglycerides (Marsh & Watts 2007), these fatty acids showed an increase. In the gonads of A. lixula, these seasonal changes were less marked but could also be observed for 16:0 and 18:1n-7.

[FIGURE 7 OMITTED]

[FIGURE 8 OMITTED]

Annual variations of 20:5n-3 clearly paralleled those of GI values in both P. lividus and A. lixula. This fatty acid increased during the first months of the year, coinciding with the increase of GI, and remained at low levels in summer and early autumn, the months in which the gonads are mainly in the spent stage, when there are virtually no gametes inside (Byrne 1990, Sanchez-Espana et al. 2004, Walker et al. 2007). This fatty acid is found in high proportions in both ova and spermatozoa (Khozina et al. 1978, Metzman et al. 1978, Mita et al. 1994), and therefore this loss of 20:5n-3 could be related, at least in part, to the absence of gametes in the gonads during this period of the reproductive cycle. Although sea urchin larvae were reported to be able to synthesize 20:5n-3 (Schiopu et al. 2006, Liu et al. 2007a, Liu et al. 2007b), the supply of adequate amounts of this fatty acid could be important during the first stages of development, prior larvae are able to feed by themselves. The annual profile of arachidonic acid differed from that of 20:5n-3 and began to increase in April/May, when GI reached its maximum values, and remained elevated until the end of the year. This increase could be related to a higher demand of 20:4n-6 for eicosanoid synthesis in stressful situations such as spawning, or during higher ambient temperatures or activation of immune function as suggested previously by Sanina and Kostetsky (2002) in different species of marine invertebrates and by Pernet et al. (2007) in the bivalves Mytilus edulis and Crassostrea virginica. In P. lividus, seasonal changes of 18:2n-6, 18:3n-3, and 18:4n-3 suggest an enhanced utilization of these fatty acids for long-chain PUFA synthesis, because the lowest levels of these fatty acids in April/May coincided with the highest levels of n-3 and n-6 PUFA. However, in the gonads of A. lixula, variations were not statistically significant and could not be associated with the seasonal fluctuations of PUFA.

[FIGURE 9 OMITTED]

It is well known that one of the mechanisms used by poikilotherms to counteract the effect of temperature on membrane fluidity is to modify acyl-chain composition of phospholipids. In marine invertebrates, as in other aquatic animals, it has been reported that when temperature increases SFAs are increased, whereas at low temperatures these fatty acids are partially replaced by more unsaturated components, mainly 20:5n-3 and 22:6n-3 (Gillis & Ballantyne 1999, Pernet et al. 2006, Sanina & Kostetsky 2002). In the gonads of A. lixula and P. lividus, the seasonal variations of palmitic acid did not appear to be related to thermal adaptation, because in both sea urchins this fatty acid was elevated in winter. On the other hand, although 22:6n-3 did not vary during the year, 20:5n-3 showed a marked decreased as temperature increased, which suggests a possible use of 20:5n-3 to counteract the disordering effect of high temperatures on membrane lipids. Interestingly, MUFA (mainly 20:1n-11) and n-3 PUFA showed an opposite behavior, with a marked increased during summer. The increase of MUFA during thermal acclimation, also reported in other marine invertebrates (Sanina & Kostetsky 2002) and in trout (Guderley et al. 1997, Kraffe et al. 2007), is not easy to explain, because the effect of these fatty acids in membrane fluidity is similar to that exert by PUFA (Hazel & Williams 1990). One possibility is that these MUFAs increase to compensate a possible diminution of membrane fluidity that could originate by the marked decrease of the highly unsaturated n-3 PUFA. On the other hand, as suggested by Hazel and Williams (1990), the primary aim of these monounsaturated acyl chain modifications during thermal acclimation might not be to regulate fluidity, but to modify the lipid environment and thereby modulate membrane function.

[FIGURE 10 OMITTED]

In different aquatic ectothermal animals, it has also been reported that plasmalogens increase in response to an elevation of temperature (Yeo et al. 1997, Lahdes et al. 2000, Sanina & Kostetsky 2002, Kraffe et al. 2007, Kake1a et al. 2008). Plasmalogens have been shown to favor the formation of nonlamellar structures, reducing membrane fluidity (Brites et al. 2004). In addition, it has been proposed that they may act as antioxidants, protecting other membrane lipids from the oxidative stress induced, among other factors, by high temperatures (Brites et al. 2004). In our study, plasmalogens were not analyzed, but we identified 2 dimethylacetals, DMA 16 and DMA 18, that are indicative of the presence of this kind of phosphoglyceride in the gonad. In both sea urchins, the level of DMA 18, the major dimethylacetal, was higher during the warmer months. On the other hand, 20:1n-11, a fatty acid that was reported to be located primarily in plasmalogens (Kraffe et al. 2004), was also significantly increased during the summer, showing an annual profile very similar to that of DMA 18. Thus, it appears that in the gonads of both sea urchins plasmalogens might also be involved in membrane adaptation to temperature fluctuations.

Other fatty acids that could be implicated in membrane lipid remodeling during thermal adaptation are NMID, because the flexibility of their acyl chains was reported to be usually less than that of the corresponding acyl chains with methylene-interrupted double bonds (Rabinovich & Ripatti 1991). However, according to the available data, a clear involvement of NMID in thermal adaptation in marine invertebrates cannot be established because either an increase of these fatty acids with cold (Pernet et al. 2006) or, as in our study, at higher ambient temperatures (Sanina & Kostetsky 2002) has been reported. More likely, the increase of the NMID 20:2[DELTA]5,11 in the gonads of A. lixula and P. lividus from July/August to October appears to be related to the marked decreased of 20:5n-3 during the same months, as it has been suggested that NMID could be used to compensate a diminution of n-3 PUFA (Klingensmith 1982, Ojea et al. 2004).

CONCLUSIONS

The gonad fatty acids of A. lixula and P. lividus showed similar annual variations despite their clearly distinct fatty acid profiles. Some of these changes appear to be related to the reproductive cycle, either because certain fatty acids could be used as an energy source for gametogenesis (i.e., some SFAs and MUFAs) or because they are important for future larvae and could be specifically transferred to gametes (i.e., 20:5n-3). On the other hand, the need for cell membranes to adapt their fluidity to seawater temperature fluctuations could also justify variations of the highly unsaturated 20:5n-3 or those of 20:1n-11 and DMA 18. This study provides new data about the significance of fatty acids in the gonad during an annual cycle than can be useful for aquaculture research, because both sea urchin species are appreciated as seafood and are a good source of n-3 PUFAs, the health benefits of which are well known.

ACKNOWLEDGMENTS

The authors express their gratitude to Ana Sanchez-Espana, who helped collect the samples and extract the gonads in the laboratory.

LITERATURE CITED

Bayed, A., F. Quiniou, A. Benrha & M. Guillou. 2005. The Paracentrotus lividus populations from the northern Moroccan Atlantic coast: growth, reproduction and health condition. J. Mar. Biol. Assoc. U. K. 85:999-1007.

Boudouresque, C. F. & M. Verlaque. 2007. Ecology of Paracentrotus lividus. In J. M. Lawrence, editor. Developments in aquaculture and fisheries science, vol. 37. Edible sea urchins: biology and Ecology. Amsterdam: Elsevier. pp. 243-283.

Brites, P., H. R. Waterham & R. J. A. Wanders. 2004. Functions and biosynthesis of plasmalogens in health and disease. Biochim. Biophys. Acta 1636:219-231.

Byrne, M. 1990. Annual reproductive cycles of the commercial sea urchin Paracentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar. Biol. 104:275-289.

Castell, J. D., E. J. Kennedy, S. M. C. Robinson, G. J. Parsons, T. J. Blair & E. Gonzalez-Duran. 2004. Effect of dietary lipids on fatty acid composition and metabolism in juvenile green sea urchins (Strongylocenlrotus droebachiensis). Aquaculture 242:417-435.

Cook, E. J., M. V. Bell, K. D. Black & M. S. Kelly. 2000. Fatty acid compositions of gonadal material and diets of the sea urchin Psamntechinus miliaris: trophic and nutritional implications. J. Exp. Mar. Biol. Ecol. 255:261-274.

Dembitsky, V. M., E. E. Pechenkina-Shubina & O. A. Rozentsvet. 1991. Glycolipids and fatty acids of some seaweeds and marine grasses from the black sea. Phytochemistry 30:2279-2283.

Dembitsky, V. M., O. A. Rozentsvet & E. E. Pechenkina. 1990. Glycolipids, phospholipids and fatty acids of brown algae species. Phytochemistry 29:3417-3421.

Dincer, T. & S. Cakli. 2007. Chemical composition and biometrical measurements of the Turkish sea urchin (Paracentrotus lividudus, Lamarck, 1816). Crit. Rev. Food Sci. Nutr.. 47:2126.

Fenaux, L., G. Malara, C. Cellario, R. Charra & I. Palazzoli. 1977. Evolution des constituants biochimiques des principaux compartiments de l'oursin Arbacia lixula (L.) an tours d'un cycle sexuel el effets d'un jefine de courte duree cours de la maturation sexuelle. J. Evp. Mar. Biol. Ecol. 28:17-30.

Fernandez, C. 1998. Seasonal changes in the biochemical composition of the edible sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar. Ecol. (Berl.) 19:1-11.

Erantzis, A., J. F. Berthon & F. Maggiore. 1988. Relation trophique entre les oursins Arbacia lixula et Paracentrotus lividus (Echinoidea regularia) et le phytobenthos infralittoral superficiel de la bate de Port-Cross (Var, France). Sci. Rep. Port-Cros Natl. Park 14:81-140.

Grillis, T. W. & S. Ballantyne. 1999. Influences of subzero thermal acclimation on mitochondrial membrane composition of temperate zone marine bivalve mollusks. Lipids 34:59-66.

Guderley, H., J. St. Pierre, P. Couture & A. J. Hulbert. 1997. Plasticity of the properties of mitochondria from rainbow trout red muscle with seasonal acclimatization. Fish Physiol. Biochem. 16:531-541.

Hazel, J. R. & E. E. Williams. 1990. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog. Lipid Res. 29:167-227.

Hughes, A. D., A. 1. Catarino, M. S. Kelly, D. K. A. Barnes & K. D. Black. 2005. Gonad fatty acids and trophic interactions of the echinoid Psammechinus miliaris. Mar. Ecol. Prog. Set. 305:101-111.

Kakela, R., M. Mattila, M. Hermansson, P. Haimi, A. Uphoff, V. Paajanen, P. Somerharju & M. Vornanen. 2008. Seasonal acclimatization of brain lipidome m a eurythermal fish (Carassius carassius) is mainly determined by temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294:R1716-R1728.

Kelly, J. R., R. E. Sheibling, S. J. Iverson & P. Gagnon. 2008. Fatty acid profiles in the gonads of the sea urchin Strongylocentrotus droebachiensis on natural algal diets. Mar. Ecol. Prog. Ser. 973:1-9.

Kharlamenko, V. I., N. V. Zhukova, S. V. Khotimchenko, V. I. Svetashev & G. M. Kamenev. 1995. Fatty acids as markers of food sources in a shallow water hydrothermal ecosystem (Kraternaya Bight, Yankich Island, Kurile Islands). Mar. Ecol. Prog. Ser. 120: 231-241.

Khotimchenko, S. V. 1998. Fatty acids of brown algae from the Russian Far East. Phytochemistry 49:2362-2369.

Khotimchenko, S. V., V. E. Vaskovsky & T. V. Titlyanova. 2002. Fatty acids of marine algae from the Pacific coast of North California. Bot. Mar. 45:17-22.

Khozina, V. P., T. A. Terekhova & V. I. Svetashev. 1978. Lipid composition of gametes and embryos of the sea urchin Strongylocentrotus intermedius at early stages of development. Dev. Biol. 62:512-517.

Klingensmith, J. S. 1982. Distribution of methylene and nonmethylene-interrupted dienoic fatty acids in polar lipids and triacylglycerols of selected tissues of the hardshell clam (Mercenaria mercenaria). Lipids 17:976-981.

Kraffe, E., Y. Marty & H. Guderley. 2007. Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mydiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J. Exp. Biol. 210:149-165.

Kraffe, E., P. Soudant & Y. Marty. 2004. Fatty acids of serine, ethanolamine, and choline plasmalogens in some marine bivalves. Lipids 39:59-66.

Lahdes, E., G. Balogh, E. Fodor & T. Farkas. 2000. Adaptation of composition and biophysical properties of phospholipids to temperature by the crustacean, Gammarus spp. Lipids 35:1093-1098.

Lepage, G. & C. C. Roy. 1987. Direct transesterification of all classes of lipids in a one-step reaction. J. Lipid Res. 27:114-120.

Li, X., X. Fan, L. Han & Q. Lou. 2002. Fatty acids of some algae from the Bohai Sea. Phytochemistry, 59:157-161.

Liu, H., M. S. Kelly, E. J. Cook, K. Black, H. Orr, J. X. Zhu & S. L. Dong. 2007a. The effect of diet type on growth and fatty-acid composition of sea urchin larvae, i. Paracentrotus lividus (Lamarck, 1816) (Echinodermata). Aquaculture 264:247-262. Liu, H., M. S. Kelly, E. J. Cook, K. Black, H. Orr, J. X. Zhu & S. L.

Dong. 2007b. The effect of diet type on growth and fatty-acid composition of sea urchin larvae, I1. Psammechinus miliaris (Gmelin). Aquaculture 264:263-278.

Liyana-Pathirana, C., F. Shahidi, A. Whittick & R. Hooper. 2002. Lipid and lipid soluble components of gonads of green sea urchin (Strongylocentrotus droebachiensis). J. Food Lipids 9:105-126.

Marsh, A. G. & S. A. Watts. 2007. Biochemical and energy requirements of gonad development. In: J. M. Lawrence, editor. Developments in aquaculture and fisheries science, vol. 32. Edible sea urchins: biology and ecology. Amsterdam: Elsevier. pp. 35-53.

Metzman, M. S., A. Mastroianni & J. F. Strauss. 1978. Fatty acid composition of unfertilized and fertilized eggs of the sea urchin, Arbacia punctulata. Lipids 13:823-824.

Mira, M. & M. Nakamura. 2001. Energy metabolism of sea urchin spermatozoa: the endogenous substrate and ultrastructural correlates. In: M. Jangoux & J. M. Lawrence, editors. Echinoderm studies, vol. 6. Lisse: A. A. Balkema. pp. 85-110.

Mita, M., A. Oguchi, S. Kikuyama, H. Namiki, I. Yasumasu & M. Nakamura. 1994. Comparison of sperm lipid components among four species of sea-urchin based on echinoid phylogeny. Comp. Biochem. Physiol. B 108:417-422.

Montero-Torreiro, M. F. & P. Garcia-Martinez. 2003. Seasonal changes in the biochemical composition of body components of the sea urchin, Paracentrotus lividus, in Lorbe (Galicia, northwestern Spain). J. Mar. Biol. Assoc. U. K. 83:575- 581.

Ojea, J., A. J. Pazos, D. Martinez, S. Novoa, J. L. Sanchez & M. Abad. 2004. Seasonal variation in weight and biochemical composition of the tissues of Ruditapes decussatus in relation to the gametogenic cycle. Aquaculture 238:451-468.

Pernet, F., R. Tremblay, L. Comeau & H. Guderley. 2007. Temperature adaptation in two bivalve species from different thermal habitats: energetics and remodelling of membrane lipids. J. Exp. Biol. 210: 2999-3014.

Pernet, F., R. Tramblay, C. Gionet & T. Landry. 2006. Lipid remodelling in wild and selectively bred hard clams at low temperatures in relation to genetic and physiological parameters. J. Exp. Biol. 209:4663-4675.

Privitera, D., M. Chiantore, L. Mangialajo, N. Glavic, W. Kozul & R. Cattaneo-Vietti. 2008. Inter- and intra-specific competition between Paracentrotus lividus and Arbacia lixula in resource-limited barren areas. J. Sea Res. 60:184-192.

Rabinovich, A. L. & P. O. Ripatti. 1991. The flexibility of natural hydrocarbon chains with non-methylene-interrupted double bonds. Chem. Phys. Lipids 58:185-192.

Reuss, N. & L. K. Poulsen. 2002. Evaluation of fatty acids as biomarkers for a natural plankton community: a field study of a spring bloom and a post-bloom period offWest Greenland. Mar. Biol. 141: 423-434.

Sanchez-Espana, A., I. Martinez-Pita & F. J. Garcia. 2004. Gonadal growth and reproduction in the commercial sea urchin Paracentrotus lividus (Lamarck, 18163 (Echinodermata: Echinoidea) from southern Spain. Hyvdrobiologia 519:61-72.

Sanina, N. M. & E. Y. Kostetsky. 2002. Thermotropic behaviour of major phospholipids from marine invertebrates: changes with warm acclimation and seasonal acclimatization. Comp. Biochem. Physiol. B 133:143-153.

Schiopu, D., S. B. George & J. Castell. 2006. Ingestion rates and dietary lipids affect growth and fatty acid composition of Dendraster excentricus larvae. J. Exp. Mar. Biol. Ecol. 378:47-75.

Serrazanetti, G. P., C. Pagnucco, L. S. Conte & O. Cattani. 1995. Hydrocarbons, sterols and fatty acids in sea urchin (Paracentrotus lividus) of the Adriatic Sea. Chemosphere 30:1453-1461.

Sewell, M. A. 2005. Utilization oflipids during early development of the sea urchin Evechinus chloroticus. Mar. Ecol. Prog. Set. 304:133-142.

Stanley-Samuelson, D. W. 1994. The biological significance of prostaglandins and related eicosanoids in invertebrates. Am. Zool. 34:589-598.

Takagi, T., M. Kaneniwa, Y. Itabashi & R. G. Ackman. 1986. Fatty acids in echinoidea: unusual cis-5-olefinic acids as distinctive lipid components in sea urchins. Lipids' 21:558-565.

Walker, C. W., T. Unuma & M. P. Lesser. 2007. Gametogenesis and reproduction of sea urchins. In: J. M. Lawrence, editor. Edible sea urchins: biology and ecology, vol. 37. Developments in aquaculture and fisheries science. Amsterdam: Elsevier. pp. 11-33.

Yasumasu, I., A. Hino, A. Suzuki & M. Mita. 1984. Change in the triglyceride level in sea urchin eggs and embryos during early development. Dev. Growth Differ. 26:525-532.

Yeo, Y. K., E. J. Park, C. W. Lee, H. T. Joo & T. Farkas. 1997. Ether lipid composition and molecular species alterations in carp brain (Cyprinus carpio L.) during normoxic temperature acclimation. Neurochem. Res. 22:1257-1264.

Zhukova, N. V. 1986. Biosynthesis of non-methylene-interrupted dienoic fatty acids from 14-C-acetate in molluscs. Biochim. Biophys. Acta 878:131-133.

Zhukova, N. V. 1991. The pathway of the biosynthesis of nonmethylene-interrupted dienoic fatty acids in molluscs. Biochem. Physiol. B 100:801-804.

INES MARTINEZ-PITA, (1) * FRANCISCO J. GARCIA (2) AND MARIA-LUISA PITA (3)

(1) I.F.A.P.A. Centro "Agua del Pino," Consejeria de Innovacidn, Ciencia y Empresa, Carretera Punta Umbria-Cartaya Km 3.8, C.P. 21450, Huelva, Spain; (2) Departamento de Sistemas Fisicos, Quimicos y Naturales, Facultad de Ciencias Experimentales, Universidad Pablo de Olavide, Carretera de Utrera, Km 1., Sevilla, Spain; (3) Departamento de Bioquimica Mddica y Biologia Molecular, Universidad de Sevilla, Avda . Sanchez Pizjuan, 7, 41009 Sevilla, Spain

* Corresponding author. E-mail: ines.martinez@juntadeandalucia.cs
TABLE 1.
Sampling seawater temperatures recorded at La Herradura
and Torregorda during the year 2003

             La Herradura ([degrees]C)   Torregorda ([degrees]C)

January                 12                         15
February                14                         15
March                   16                         17
April                   18                         19
May                     22                         22
June                    23                         23
July                    23                         22
August                  24                         22
September               22                         21
October                 20                         20
November                17                         15
December                12                         13

TABLE 2.
Gonad fatty acid composition of Paracentrotus lividus
harvested at Torregorda and Arbacia lixula harvested
at La Herradura

Fatty acids              P. lividus (n = 71)        A. lixula (n = 69)

14:00                8.3 [+ or -] 0.2 *              2.5 [+ or -] 0.1
15:00                1.0 [+ or -] 0.0 *              1.4 [+ or -] 0.0
16:00               17.5 [+ or -] 0.3 *             16.0 [+ or -] 0.3
16:1n-7              2.2 [+ or -] 0.1                2.1 [+ or -] 0.2
17:00                0.4 [+ or -] 0.0 *              0.8 [+ or -] 0.0
18:0 DMA             4.0 [+ or -] 0.2                3.9 [+ or -] 0.1
18:00                3.6 [+ or -] 0.1 *              5.8 [+ or -] 0.3
18:1n-9              1.5 [+ or -] 0.1 *              1.2 [+ or -] 0.1
18:1n-7              3.0 [+ or -] 0.1 ([dagger])     3.3 [+ or -] 0.1
18:2n-6              1.0 [+ or -] 0.0 *              0.7 [+ or -] 0.0
18:3n-3              1.4 [+ or -] 0.1 *              0.8 [+ or -] 0.1
18:4n-3              1.5 [+ or -] 0.1                1.5 [+ or -] 0.1
20:00                0.6 [+ or -] 0.0 *              1.5 [+ or -] 0.1
20:1n-11             5.0 [+ or -] 0.2 *              6.9 [+ or -] 0.3
20:1n-9              4.9 [+ or -] 0.1 *              1.3 [+ or -] 0.0
20:1n-7              1.0 [+ or -] 0.0 *              1.3 [+ or -] 0.0
20:2 [DELTA]
  5,11 NMID          4.2 [+ or -] 0.1 *              2.9 [+ or -] 0.1
20:2 [DELTA]
  5,13 NMID          0.7 [+ or -] 0.0 *              0.5 [+ or -] 0.0
20:4n-6             11.9 [+ or -] 0.2 *             15.5 [+ or -] 0.4
20:5n-3             14.1 [+ or -] 0.5 (#)           15.7 [+ or -] 0.6
22:1n-9              4.0 [+ or -] 0.1                3.6 [+ or -] 0.2
22:4n-6              2.0 [+ or -] 0.0 *              1.7 [+ or -] 0.0
22:5n-6              0.0 [+ or -] 0.0 *              0.8 [+ or -] 0.0
22:5n-3              0.5 [+ or -] 0.0 *              0.8 [+ or -] 0.0
22:6n-3              0.8 [+ or -] 0.0 *              1.9 [+ or -] 0.1
[SIGMA] SAF         31.3 [+ or -] 0.4 *             27.9 [+ or -] 0.3
[SIGMA] MU FA       21.6 [+ or -] 0.2 *             19.6 [+ or -] 0.3
[SIGMA] PU FA n-6   18.1 [+ or -] 0.3 *             20.4 [+ or -] 0.4
[SIGMA] PU FA n-3   19.9 [+ or -] 0.4 ([dagger])    22.2 [+ or -] 0.6

Values are mean percentages [+ or -] S.E. n = number of samples.
DMA: dimethyl acetat. NMID: non-methylene interrupted dienoic.
SAF: sum of saturated fatty acids. MUFA: sum of monounsaturated
fatty acids. PUFA: sum of polyunsaturated fatty acids. Other
minor fatty acids not included in the Table: 18:3n-6, 20:2n-6,
20:3n-6, 20:3n-3, 20:4n-3, and 16:0 dimethylacetal. Significant
difference with respect to A. lixula (Student t-test):
(#) P < 0.05 ; ([dagger]) P < 0.01; * P < 0.001.

TABLE 3.
ANOVA statistical analysis of the annual variations of gonad
fatty acids of Paracentrotus liridus and Arbacia lixula

                              P. lividus           A. lixula

Fatty acid                F-ratio   P-Value    F-ratio   P-Value

14:0                        3.034     0.003      0.865    0.578
16:0                        3.020     0.003      2.264    0.023
16:1n-7                     3.722    <0.001      1.090    0.386
DMA 18                      3.286     0.001     12.672   <0.001
18:1n-9                     2.300     0.020      7.091   <0.001
18:1n-7                     5.729    <0.001      8.447   <0.001
18:2n-6                     5.259    <0.001      1.130    0.356
18:3n-3                     9.260    <0.001      1.030    0.433
18:4n-3                     5.335    <0.001      0.999    0.458
20:1n-11                    6.263    <0.001     19.869   <0.001
20:2 [DELTA] 5,11 NMID      6.304    <0.001      3.729   <0.001
20:4n-6                     2.833     0.005      4.198   <0.001
20:5n-3                    23.403    <0.001     11.338   <0.001
22:6n-3                     2.124     0.032      1.152    0.340
[SIGMA]-SAF                 3.142     0.002      0.958    0.494
[SIGMA]-MUFA                4.433    <0.001      6.705   <0.001
[SIGMA]-PUFA n-6            2.695     0.007      4.403   <0.001
[SIGMA]-PUFA n-3           15.468    <0.001      8.814   <0.001

DMA: dimethyl acctal; NMID: non-methylene interrupted diene; SAF:
sum of saturated fatty acids; MUFA: sum of monounsaturated fatty
acids; PUFA: sum of polyunsaturated fatty acids.
COPYRIGHT 2010 National Shellfisheries Association, Inc.
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2010 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Martinez-Pita, Ines; Garcia, Francisco J.; Pita, Maria-Luisa
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:4EUSP
Date:Aug 1, 2010
Words:7108
Previous Article:Stocking density and captive sea urchin Paracentrotus lividus (Lamarck, 1816) gamete production and fertilization.
Next Article:Identification of genes potentially involved in pearl formation by expressed sequence tag analysis of mantle from freshwater pearl mussel (Hyriopsis...
Topics:

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters |