Polar Biol DOI 10.1007/s00300-009-0702-6
ORIGINAL PAPER
Reproductive cycle and reproductive output of the sea urchin Loxechinus albus (Echinodermata: Echinoidea) from Beagle Channel, Tierra del Fuego, Argentina Analía Fernada Pérez · Claudia Boy · Elba Morriconi · Jorge Calvo
Received: 13 November 2008 / Revised: 21 July 2009 / Accepted: 23 July 2009 © Springer-Verlag 2009
Abstract Reproductive cycle, frequency and duration of spawning, energetic content of gonads, and reproductive output of the common green sea urchin Loxechinus albus were analyzed in the Beagle Channel (Tierra del Fuego) between May 2004 and May 2005. Gonad indices (GI, percentages of gonad mass in total body mass) were signiWcantly higher in March, April, July, and August than in November and May, thus showing a negative correlation with the photoperiod. Highest GI values of mature individuals were observed in August, and spawning occurred from September to December. In females, the mass-speciWc energy content of gonads (ECG) was highest in spawned gonads and lowest in mature ones, while in males ECG values were higher in immature stage and lower in premature and mature stages. High ECG values can be explained by the abundance of nutritive phagocytes. Both ECG and total gonad energy content (TECG) were higher in females than in males. Mean reproductive output was 7.28% for females and 6.15% for males (expressed as the diVerence between mean GI of mature and spawned gonads) and 25.02 kJ for females and 19.26 kJ for males (expressed as the diVerence between mean TECG of mature and spawned gonads).
A. F. Pérez · C. Boy · E. Morriconi · J. Calvo Centro Austral de Investigaciones CientíWcas (CADIC-CONICET), Bernardo Houssay 200 (V9410BFD) Ushuaia, Tierra del Fuego, Argentina A. F. Pérez (&) Departamento de Ecología Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Universitaria, (C1428EGA), Ciudad Autónoma de Buenos Aires, Buenos Aires, Argentina e-mail:
[email protected]
Keywords Reproductive cycle · Photoperiod · Energetic content of gonads · Reproductive output · Sea urchins
Introduction The common green sea urchin Loxechinus albus (Molina, 1782) is an edible species with a wide geographic distribution along the PaciWc coast, ranging from Ecuador (6°S) to Tierra del Fuego (54°S), including the Magellan Strait and Beagle Channel (Bernasconi 1947, 1953; Dayton 1985). The natural populations on the Chilean coasts were reduced or depleted due to overWshing for commercial purposes (Olave et al. 2001; Stotz 2004), while the Beagle Channel populations were only occasionally exploited. These populations represent the southernmost point of species distribution and are subjected to large seasonal variations in temperature and day length, as well as pronounced Xuctuations in primary productivity (Hernando 2006). Population density (Wahle and Peckham 1999) and seasonal changes of environmental factors like photoperiod (Bay-Schmith and Pearse 1987; Dumont et al. 2006; Pearse et al.1986; Shpigel et al. 2004; Walker and Lesser 1998), water temperature (Pearse and Cameron 1991; Yamamoto et al. 1988), and food availability (Lamare et al. 2002; Lawrence 1987a) have strong inXuence on the reproductive cycles of sea urchin populations. The methodology used to study reproductive cycles and spawning periods is based on analyses of variations in the gonadal index and morphological changes in the histology of gonads (Lamare et al. 2002; MacCord and Ventura 2004; Meidel and Scheibling 1998; Williamson and Steinberg 2002). The knowledge of sea urchin gametogenesis, reproductive cycle, and spawning periods is used to establish Wshery regulations and improve
123
Polar Biol
echinoculture (Dumont et al. 2006; Shpigel et al. 2004; Walker and Lesser 1998). Previous studies on reproductive aspects of L. albus populations were performed on the Chilean PaciWc coast (Gutiérrez and Otsu 1975; Zamora and Stotz 1992), in the Magellan region (Bay-Schmith et al. 1981; Oyarzún et al. 1999), and in the Beagle Channel (Orler 1992). Zamora and Stotz (1992) proposed a delayed spawning pattern along the Chilean PaciWc coast as latitude increases. For example, the spawning period at 30°S occurs between June and August (Zamora and Stotz 1992) and in the Chiloe and Guaitecas Islands (42–45°S) between November and December (Bay-Schmith et al. 1981). In invertebrates the empirical estimation of reproductive inversion was established as: reduction of gonad mass in relation with body mass; decrease of gonadal energetic content after spawning respect of total body energetic value and the energy invested in total eggs production. DiVerent authors denominate these estimations as reproductive eVort and/or reproductive output (Chow 1987; GriYths and King 1979; Liu 1994; Lucas 1982; MacDonald and Bourne 1987; McClintock and Pearse 1986; McClintock 1989; Parry 1982; Raymond et al. 2007; Urrutia et al. 1999) and apply them to compare sexes, diVerent populations or species. The energetic value determination of diVerent gonadal stages provides a complementary approach at the histological Fig. 1 Sampling area in Bridges Islands, Beagle Channel, Tierra del Fuego, Argentina
123
description of reproductive cycle. The monthly variation in energetic content of gonads, gut and celomic Xuid were analyzed previously (Pérez et al. 2008) in the L. albus population object of the present study. The knowledge of both reproductive cycle and temporal variation of roe quantity of L. albus in the Beagle Channel is valuable information for the management of sea urchin populations in order to establish the better time to harvest this species. The aim of this study was to describe the annual reproductive cycle, including the frequency and duration of spawning, of Loxechinus albus using histological analysis of gonads and to estimate the reproductive output of this species by comparing the energetic content of diVerent gonadal stages.
Materials and methods Study site and sampling During the study period from May 2004 to May 2005, once each month a sample of 30 adult specimens of Loxechinus albus were collected by SCUBA diving oV the Bridges Islands, Beagle Channel (54°52⬘S, 68°11⬘W; Fig. 1).
Polar Biol
In addition, seawater temperature was measured at 0.1°C. The monthly day length average was provided by the Servicio de Hidrografía Naval http://www.hidro.gov.ar/observatorio/sol/asp (Fig. 2). Specimens from 65 to 85 mm test diameter were selected to minimize the variation in reproductive parameters due to diVerences in body size (Gonor 1972). Sea urchins were transported to the Ecophysiology Laboratory of CADIC and kept in sea water at 7°C for 24 h. Each sea urchin was drained, weighed (0.01 g), and maximum diameter (through the madreporic plate) and height were measured using a electronic calliper (0.1 mm). The Gonad index (GI) was calculated as the ratio of gonad wet mass (g) to total body wet mass (g) multiplied by 100. Histological determinations A total of 189 females and 191 males sampled during 2004 and 2005 were examined microscopically. One gonad of each specimen was Wxed in Bouin’s solution over 12 h, water washed and transferred to 70% alcohol. A cross-section block was dehydrated in alcohol series, cleared in benzene, embedded in Paraplast, sectioned at 5 m and stained with Groat’s hematoxylin and eosin. Sections were examined microscopically and each individual was assigned to one of six male and female gametogenic stages: (a) immature, (b) growth, (c) premature I, (d) premature II, (e) mature, and (f) spawned. These stages were deWned according to the gonadal scales for other echinoids (Lamare et al. 2002; Williamson and Steinberg 2002) and Loxechinus albus (Orler 1992; Zamora and Stotz 1992). Histological pictures were taken with a Zeiss Image 25
GI (%) Photoperiod (day length, hs) Temperature (°C)
20
15
10
5
0 M
J
J
A
S
O
N
D
J
F
M
A
M
Month Fig. 2 Gonad index (GI) for L. albus from Bridges Islands (May 2004–May 2005). Median, quartiles and data outside 5th and 95th percentiles are indicated (n = 380). Monthly means of seawater temperature and day length in the Bridges Islands (54°50⬘S, 68°15⬘WO), Beagle Channel
Z1-AX10 microscope by a video camera (Zeiss, AxioCam HRc) and viewed using the Axiovision v 4.4 software. Calorimetric determination One gonad of each sea urchin was dried in an air circulating oven at 70°C to constant weight. The dry mass of a gonad was extrapoled to gonadal wet mass (one gonad dry mass £ total gonad wet mass/one gonad wet mass). After obtaining the dry mass, samples were ground and pellets were made with a press (Parr model 2812). The caloric contents of gonads of approximately 20 individuals (10 females and 10 males) per month were obtained by burning pellets (50–200 mg) in a micro-bomb calorimeter (Parr, model 1425) as described by Lucas (1996). The mass-speciWc energy content of gonads (ECG) was calculated as kJ/g ash-free dry mass (AFDM) of the gonads. The total energy content of gonads (TECG) was calculated by multiplying ECG values with the total AFDM (g) of the gonad. The values obtained were corrected for ash and acid content. Benzoic acid calibrations were done periodically. Reproductive output The reproductive output for each sex was determined using two approaches: as the diVerence between (a) the gonadal mass before and after the spawning, expressed as a percentage of total body mass (GI), and (b) the total energy content (TECG) of mature and spawned gonads. Statistical analysis The sex ratio was determined by examining histological slides in all individuals collected across all sample periods. Its departure from unity (1:1) was tested with a Chi-square test (Zar 1984). Monthly diVerences in the GI were analyzed using a non-parametric test (Kruskal–Wallis), pairwise diVerences were analyzed using unplanned Dunn’s multiple comparisons test (Sokal and Rohlf 1995; Zar 1984). DiVerences in GI between sexes were tested using paired t test (Sokal and Rohlf 1995; Zar 1984). Pearson correlation was used to test for relationships among variables (gonad index, photoperiod, and water temperature). The statistical signiWcance of diVerences in GI, ECG, and TECG among gonad stages and sex were Wrst analyzed using two-factor analysis of covariance (ANCOVA) with body size as covariate. However, the regressions between the variables and the covariate were not signiWcant for each factor level, indicating that GI, ECG, and TECG did not signiWcantly vary with body size within the range of sizes of specimens (65–85-mm test diameter) used for our study. Therefore, the eVect of size on the reproductive variables
123
Polar Biol
can be neglected here. Consequently we applied two-way analysis of variance (ANOVA) to test for diVerences among sexes and stages. The assumptions of normality (Kolmogorov–Smirnov test) and homogeneity of variances (Levene’s test) were veriWed prior to ANOVA. Pairwise diVerences between gonad stages were analyzed by unplanned Tukey–Kramer multiple comparisons tests (Sokal and Rohlf 1995). Statistical analyses were performed with Statistica 6.0 and GraphPad Instat packages.
Results Sex ratio During our study, the sex ratio of the Beagle Channel population did not diVer signiWcantly from unity (P > 0.05, Chi-squared = 0.011). Gonad index, photoperiod, and temperature Day lengths varied between 7.3 h in June and 17.4 h in December (Fig. 2). The increase in day length was followed by an increase in water temperature. Monthly mean temperatures were lowest in June (4°C) and highest in February (10.5°C; Fig. 2). Gonad index values were not diVerent between females (n = 189) and males (n = 190) (Student’s t = 0.9911, P > 0.05). In contrast, diVerences between monthly GI values were highly signiWcant (Kruskal–Wallis; H = 177.2625, P < 0.001) (Fig. 2); highest values were found in March, April, July, and August and lowest values in November and May (P < 0.05). Statistical analyses showed a negative correlation between GI and day length (r = 0.748, P < 0.05). However, the correlation between GI and water temperature was not signiWcant (P > 0.05) (Fig. 2).
3. Premature I The number and size of vitellogenic oocytes (>90 m) increases, associated with a marked reduction in the abundance of both nutritive phagocytes and glycoproteic (PAS+) material (Fig. 3c). The acini contain oocytes in all stages of development, but the number of mature ova is very low. The cytoplasm of vitellogenic oocytes is acidophilic, pear-shaped and is projected into the lumen. 4. Premature II In this stage an increase in the number and size of oocytes was observed conserving the staining characteristics (Fig. 3d). A small number of mature ova with a Wnely granular cytoplasm and without visible nucleus are found centrally in the lumen of the acini. 5. Mature The acini contain numerous mature ova, densely packed into the lumen (Fig. 3e). A small number of nutritive phagocytes and primary oocytes are located along the acinous wall. 6. Spawned The ovary appears empty, containing only a small number of relict ova (Fig. 3f). The acinar walls are thin, lining them there are both, an increasing number of nutritive phagocytes and small number of primary oocytes. Male gonadal stages 1.
2.
3.
Female gonadal stages 1. Immature The acinar lumen is occupied by a meshwork of pale-stained nutritive phagocytes, with large darkstained vesicles in the cytoplasm (Fig. 3a). There are few previtellogenic oocytes with basophilic cytoplasm less than 25 m diameter attached to the acinar wall. 2. Growing The beginning of vitellogenesis is indicated by the presence of early vitellogenic oocytes (25–90 m), attached to the acinar wall (Fig. 3b). The cytoplasm of these oocytes are stained light purple showing a decreasing basophily. Distributed in the center of acinar lumen there are nutritive phagocytes containing vacuoles, empties or with granular material.
123
4.
5.
Immature In this stage the acinar lumen is dominated by a lax meshwork of pale-stained nutritive phagocytes containing small dark-stained granules and vesicles (Fig. 4a). There are some spermatogonia lining the acinar walls. Growing A layer of spermatogonia and primary spermatocytes (100-m width) are along the acinar wall; columns of spermatocytes almost regularly disposed are projected to the center of each acinus (Fig. 4b). Nutritive phagocytes remain dominant in the center of the lumen, although the quantity of nutritive material has diminished. Premature I In this stage conspicuous columns of spermatocytes are projected into the lumen (100–120-m length) (Fig. 4c). The spermatozoa begin to accumulate in the center of the acini. Nutritive phagocytes decrease in abundance and are displaced from the center toward the periphery. Premature II This stage has a similar structure to Premature I stage, but the acini contain more abundant number of spermatozoa free in the central lumen (Fig. 4d). The columns of spermatocytes are still abundant. Mature The acini lumina are Wlled with spermatozoa densely packed (Fig. 4e). The spermatogenic layer becomes narrow or absent, decreasing in thickness (70–100-m width). There are nutritive phagocytes located toward the acini periphery, along the germinal epithelium.
Polar Biol Fig. 3 Photomicrographs of females gonadal stages of L. albus: a immature, b growing, c premature I, d premature II, e mature: free oocytes in the alveolar lumen, f spawned: immature oocytes attached to the alveolar wall and few free oocytes in the lumen. Scale bar 50 m
6. Spawned The lumina of acini are almost empty, although small clusters of spermatozoa and nutritive phagocytes may be found (Fig. 4f). The acinar walls are very thin (55%). The immature stage maintained a percentage between 20 and 70% from November to March. The maximum percentage of individuals in growing stage (63%) was found in April. Between April and August premature I and premature II stages are found in percentages from 10 to 80% (Fig. 6). Gonad index and gonadal stages Mean GI values varied signiWcantly among gonadal stages but not between sexes. The interaction between gonadal
123
Polar Biol Fig. 4 Photomicrographs of males gonadal stages of L. albus: a immature, b growing, c premature I, d premature II, e mature, f spawned. Scale bar 50 m
I G PI P II M S
80
60
40
20
0
100
Male gonadal stages (%)
Female gonadal stages (%)
100
I G PI P II M S
80
60
40
20
0
M
J
J
A
S
O
N
D
J
F
M
A
M
M
J
J
A
S
O
N
D
J
F
M
A
M
Months
Months
Fig. 5 Monthy changes in the percentage of females L. albus in each of the six gametogenic stages between May 2004 and May 2005
Fig. 6 Monthy changes in the percentage of males L. albus in each of the six gametogenic stages between May 2004 and May 2005
stage and sex was not signiWcant (two-way ANOVA, F = 0.73, P > 0.05). As the mean GI for each gonadal stage was not diVerent between sexes (F = 0.0002, P > 0.05),
they were analyzed together. Mean GI values were 8.90, 12.74, 12.22, 15.05, 15.18, and 8.06 for immature, growing, premature I, premature II, mature, and spawned stages,
123
Polar Biol
Means of mass-speciWc energy contents of gonads (ECG) varied signiWcantly among gametogenic stages (Fig. 8). The interaction between stages and sex was not signiWcant (two-way ANOVA, F = 0.23, P > 0.05). DiVerences in ECG were signiWcant among stages (F = 3.90, P < 0.001) and between sexes (F = 54.17, P < 0.05). The ECG for females reached the maximum for spawned stage (P < 0.05) and the minimum for mature stage, while in males these values were higher for immature stage and lower for premature II and mature stages (P < 0.05). For females mean values of prematures, mature and spawned stages were higher than males (t test, P < 0.05). Growth and immature stages were not diVerent (P > 0.05) between sexes. Means of total energy contents of gonads (TECG) did not vary signiWcantly between sexes and among gonadal stages. The interaction between stage and sex was also not signiWcant (two-way ANOVA, F = 0.82, P > 0.05) (Fig. 9).
Female Male 30
ECG (kJ/g AFDW)
Gonad energy content and gametogenic stages
32
28
26
24
22
20 I
G
PI
P II
M
S
Gonadal stages
Fig. 8 Mass-speciWc energy content of gonads [ECG (kJ/g AFDM), means § SD] of Loxechinus albus for each gonadal stage (I immature, G growing, P I premature I, P II premature II, M mature, S spawned). Females (n = 128) and males (n = 117)
200
150
TECG (kJ AFDW)
respectively. GI diVerences among stages were signiWcant (F = 42.12, P < 0.001). Values were highest in premature II and mature stages (P < 0.05), and no signiWcant diVerences were found between them (P > 0.05). The minimum values were obtained for spawned and immature stages (P < 0.05), and no signiWcant diVerences were found between them (P > 0.05) (Fig. 7).
100
50
Reproductive output The reproductive output expressed as the diVerence between the GI of mature and spawned gonads was 7.28% for females and 6.15% for males, while the reproductive
0 I
G
PI
P II
M
S
Gonadal stages
Fig. 9 Total energy content of gonads [TECG (kJ AFDM), means § SD, n = 245] of Loxechinus albus for each gonadal stage (I immature, G growing, P I premature I, P II premature II, M mature, S spawned)
25
IG (%)
20
output expressed as the diVerence between the total energy content (TECG) of mature and spawned gonads was 25.02 kJ for females and 19.26 kJ for males.
15
10
Discussion 5
0 I
G
PI
P II
M
S
Gonadal stages
Fig. 7 Mean gonad index (GI § SD, n = 380) of Loxechinus albus for each gonadal stage (I immature, G growing, P I premature I, P II premature II, M mature, S spawned)
The studied population of Loxechinus albus has a sex ratio non-diVerent of 1:1, agreeing with the statement that gonochoric species of echinoderm typically shows a similar proportion of sexes (Lawrence 1987b). Gonadal maturation of L. albus occurs throughout the year synchronically in both sexes as was described in other echinoids (Brewin et al. 2000).
123
Polar Biol
Gonad index has traditionally been used to assess gametogenesis in sea urchins, but this index is not enough to describe the reproductive cycle of echinoderms because the monthly changes in GI values are produced by the presence of variable quantities of both nutritive phagocytes and gametes in diVerent stages of development (Walker and Lesser 1998). In order to obtain a better understanding of the reproductive cycles, a periodic histological analysis of gonads is necessary. In the studied population of L. albus, a major peak of GI was observed in July and August, followed by a spawning period in spring (September–December). Nevertheless, the presence of a minor GI peak in autumn (March–April) did not indicate a second sexual maturation because the gonads were in non-mature stages. This peak can be explained by the high percentage of the growing stage containing a great number of nutritive phagocytes and reserve substances. Similar results were reported in Walker et al. (2001). On the contrary the fall of GI values in September is coincident with the occurrence of high percentage of spawning stage characterized by a signiWcantly low GI. These observations show a strong diVerence with the gametogenic cycle of some Antarctic sea urchins (e.g., S. neumayeri), whose oocytes develop fully over a 2-year period (Pearse and Giese 1966). A similar spawning period is described in L. albus populations of the Magellan region (53–54°S) (Arana et al. 1996; Bay-Schmith et al. 1981; Oyarzun et al. 1999). These results do not follow the general pattern showed along the Chilean PaciWc coast where the spawning is delayed as latitude increases (Vásquez 2007; Zamora and Stotz 1992). This discordance may be explained because the southern populations of L. albus are inXuenced by the Cape Horn Current (Dayton 1985; Strub et al. 1998), while the northern populations are inXuenced by the Humboldt Current (Zamora and Stotz 1992). The diVerent oceanographic characteristics of both water masses could explain this lack of congruity. The environmental conditions, especially temperature and photoperiod, and the food availability inXuence the gamete maturation and spawning of marine invertebrates (Brockington et al. 2001; Giese 1959; Pearse and Cameron 1991). In the Beagle Channel population, the reproductive cycle of L. albus could be inXuenced by photoperiod Xuctuation because the initiation of gametogenesis occurs during autumn, when light period is shortening. The gonadal maximum development (July–September) is found in coincidence with the increase of photoperiod. In September the light period overcomes 12 h, the gamete releasing starts and the 50% of individuals are found in the spawned stage. When the day length is near the maximum, October– December, the spawned stage is found in more than 70% of samples. A similar inXuence of photoperiod is described in
123
Centrostephanus rodgersii (Byrne et al. 1998) and several populations of Strongylocentrotus purpuratus (Bay-Schmith and Pearse 1987; Pearse et al. 1986). Pearse et al. (1986) conWrmed Giese’s (1959) predictions regarding photoperiodic control of gametogenesis in echinoids and other echinoderms. These results suggested that gametogenesis is either stimulated by short days or suppressed by long days. Bay-Schmith and Pearse (1987) conWrmed this suggestion. Other environmental factor regulating gametogenesis development in several sea urchins species is the seasonal change in sea temperature (Pearse and Cameron 1991; Sakairi et al. 1989). However, there is not a signiWcant correlation between gonadal maturation and monthly water temperature in L. albus from Beagle Channel, as many other sea urchins species (Himmelman 1978; Pearse 1974). Several species of marine invertebrates with planktotrophic larvae spawn when the phytoplankton concentration is higher (Himmelman 1981), in a similar way the spawning of L. albus of Beagle Channel populations happened simultaneously with the spring increase in primary production (Hernando 2006). The dual function of the sea urchins gonads in generating germ cells and storing nutrients in the nutritive phagocytes (Giese 1966) give a special interest to study the energetic content variation of gonads. The analysis of the relationship between the reproductive cycle, the energy storage and its utilization, allows understanding the internal energy transfer process for a given species (Lucas 1996; Pérez et al. 2008). ECG values of L. albus, analyzed separately for each gonadal stage, ranged between 24 and 28 kJ/g AFDM. These values are higher than the energetic value of proteins established by Ansell (1974) and Brody (1945), suggesting the presence of lipids in the gonads. The minimum value of ECG in L. albus was recorded in premature II and mature stages when the nutritive phagocytes are scant. In spawned and immature stages, after spawning, gametes were strongly reduced in relation to nutritive phagocytes. These cells contain vacuoles with proteins, neutral mucopolysaccharides, and lipids (Walker et al. 2001), explaining the higher energetic values found in the spawned gonads of L. albus (Pérez et al. 2008). ECG values were higher in ovaries than testes. Similar diVerences were found in Antarctic echinoderms (McClintock and Pearse 1987) and were explained by the higher lipid content in ovaries. The reproductive output of L. albus is higher in females than males, indicating that spawning is energetically more expensive in females. A similar result was found in other broadcasting echinoderms, such as the asteroid Asterias vulgaris from Eastern Canada (Raymond et al. 2007). This study allows to suggest that autumn is the best period to harvest this species since the gonads are in premature stages, reaching the quality (color, texture, and Xavor) required by the market (Pérez et al., submitted).
Polar Biol Acknowledgments This research was supported by P.I.P. 02944 (CONICET), and Subproyecto A-B-21 (PNUDARG/02/018). The authors are grateful to D. Aureliano, M. Gutierrez and S. Rimbau for technical assistance, to M. Brögger for facilitating the microscope and Pedro Francisco Cárcamo for his generous advice.
References Ansell AD (1974) Seasonal changes in biochemical composition of the bivalve Abra alba from the Clyde sea area. Mar Biol 25:13–20 Arana P, Palma S, Bay-Schmith E, Monardes M, Galvez M (1996) Aspectos biológicos y pesqueros del erizo (Loxechinus albus) en la Región de Magallanes. Univ Católica Valparaíso Chile Informe Final 23:83–139 Bay-Schmith E, Pearse JS (1987) EVect of Wxed lengths on the fotoperiod regulations of gametogenesis in the sea urchin Strongylocentrotus purpuratus. Invert Reprod Develop 11:287–294 Bay-Schmith E, Werlinger C, Silva J (1981) Ciclo anual de reproducción del recurso erizo Loxechinus albus entre la X y XII Región, Subsecretaria de Pesca, Univ. Concepción, Chile, Informe Wnal, pp 1–66 Bernasconi I (1947) Distribución geográWca de los equinoideos argentinos. An Soc Arg Est Geogr 6:97–114 Bernasconi I (1953) Monografía de los Equinoideos argentinos. An Mus Hist Nat Montevideo 6:23–25 Brewin PE, Lamare MD, Keogh JA, Mladenov PV (2000) Reproductive variability over a four period in the sea urchin Evechinus chloroticus (Echinoidea: Echinodermata) from diVering habitats in New Zeland. Mar Biol 137:543–557 Brockington S, Clarke A, Chapman ALG (2001) Seasonality of feeding and nutritional status during the austral winter in the Antarctic sea urchin Sterechinus neumayeri. Mar Biol 139:127–138 Brody S (1945) Bioenergetics and growth. Reinhold Publishing, New York Byrne M, Andrew NL, Worthington DG, Brett PA (1998) Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Mar Biol 132:305–318 Chow V (1987) Patterns of growth and energy allocation in northern California populations of Littorina (Gastropoda: Prosobranchia). J Exp Mar Biol Ecol 110:69–89 Dayton PK (1985) The structure and regulation of some South American kelp communities. Ecol Monogr 55:447–468 Dumont C, Pearce CE, Stazicker C, An YX, Keddy L (2006) Can photoperiod manipulation aVect gonad development of a boreoarctic echinoid (Strongylocentrotus droebachiensis) following exposure in the wild after the autumnal equinox? Mar Biol 149:365–378 Giese AC (1959) Reproductive cycle of some west coast invertebrates. In: Withrow RB (ed) Photoperiodism and related phenomena in plants and animals. American Association for the Advancement of Science, Washington, DC, pp 625–638 Giese AC (1966) On the biochemical constitution of some echinoderms. In: Boolootian RA (ed) Physiology of echinodermata. Wiley, New York, pp 757–796 Gonor JJ (1972) Gonad growth in the sea urchin Strongylocentrotus purpuratus (Stimpson) (Echinodermata: Echinoidea) and the assumptions of gonad index methods. J Exp Mar Biol Ecol 10:89– 103 GriYths CL, King JA (1979) Energy expended on growth and gonad output in the ribbed mussel Aulacomya ater. Mar Biol 53:217– 222 Gutiérrez J, Otsu I (1975) Periodicidad en las variaciones biométricas de Loxechinus albus Molina. Rev Biol Marina 15:179–199
Hernando MP (2006) Efectos de la radiación solar sobre el Wtoplancton de aguas Antárticas y sub-Antárticas. PhD Thesis, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Buenos Aires, Argentina Himmelman JH (1978) Reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis. Can J Zool 56:1828–1836 Himmelman JH (1981) Synchronization of spawning in marine invertebrates by phytoplankton. In: Clark WH, Adams TS (eds) Advances in invertebrate reproduction. Elsevier, Amsterdam, pp 3–19 Lamare MD, Brewin PE, Barker MF, Wing SR (2002) Reproduction of the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zeland Word. N Z J Mar Freshw Res 36:719–732 Lawrence JM (1987a) Bioenergetics of echinoderms. In: Keegan BF, O’Connor DS (eds) Echinodermata. Balkema, Rotterdam, pp 47–67 Lawrence JM (1987b) A functional biology of echinoderms. Croom Helm, London Liu JH (1994) The ecology of the Hong-Kong Limpets Cellana grata (Gould 1859) and Patelloida pygmaea (Dunker 1860), reproductive biology. J Moll Stud 2(60):97–111 Lucas A (1982) Evaluation of reproductive eVort in bivalve molluscs. Malacologia 22:183–187 Lucas A (1996) Energetics of aquatic animals. Taylor and Francis, London MacCord FS, Ventura CRR (2004) Reproductive cycle of the endemic cassiduloid Cassidulus mitis (Echinoidea: Cassiduloida) on the Brazilian coast. Mar Biol 145:603–612 MacDonald BA, Bourne NF (1987) Growth, reproductive output, and energy partitioning in weathervane scallops, Pactinopecten caurinus, from British Columbia. Can J Fish Aquat Sci 44:152–160 McClintock JB (1989) Energetic composition, reproductive output and resource allocation of Antarctic Asteroids. Polar Biol 9:147–153 McClintock JB, Pearse JS (1986) Organic and energetic content of eggs and juveniles of antarctic echinoids and asteroids with lecithotrophic development. Comp Biochem Physiol 85A:341–345 McClintock JB, Pearse JS (1987) Biochemical composition of antartic echinoderms. Comp Biochem Physiol 86B:683–687 Meidel SK, Scheibling RE (1998) Annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis, in diVering habitats in Nova Scotia, Canada. Mar Biol 131:461–478 Olave S, Bustos E, Lawrence JM, Cárcamo P (2001) The eVect of size and diet on gonad production by the Chilean sea urchin Loxechinus albus. J World Aquac Soc 32:210–214 Orler PM (1992) Biología reproductiva comparada de Pseudechinus magellanicus y Loxechinus albus, equinoideos del Canal Beagle, PhD Thesis, Universidad Nacional de La Plata, Facultad de Ciencias Naturales y Museo, Buenos Aires, Argentina Oyarzún ST, Marín SL, Valladares C, Iriarte JL (1999) Reproductive cycle of Loxechinus albus (Echinodermata: Echinoidea) in two areas of the Magellan region (53°S, 70–72°W), Chile. Sci Mar 63:439–449 Parry GD (1982) Reproductive eVort in four species of intertidal limpets. Mar Biol 67:262–282 Pearse JS (1974) Reproductive patterns of tropical reef animals: three species of sea urchins. In: Proceedings of 2nd international coral reef symposium, vol 1, pp 235–240 Pearse JS, Cameron RA (1991) Echinodermata: Echinoidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates Volume VI Echinoderms and Lophophorates. The Boxwood Press, California, pp 513–662 Pearse JS, Giese AC (1966) Food, reproduction, and organic constitution of the common antarctic echinoid Sterechinus neumayeri. Biol Bull 130:387–401 Pearse JS, Pearse VB, Davis KK (1986) Photoperiod regulation of gametogenesis and growth in the sea urchin Strongylocentrus purpuratus. J Exp Zool 237:107–118
123
Polar Biol Pérez AF, Morriconi E, Boy C, Calvo J (2008) Energetic variation of the sea urchin Loxechinus albus at the southernmost limit of their distribution range (Beagle Channel, Tierra del Fuego). Polar Biol 31:443–449 Raymond JF, Himmelman JH, Guderley HE (2007) Biochemical content, energy composition and reproductive eVort in the broadcasting sea star Asterias vulgaris over the spawning period. J Exp Mar Biol Ecol 341:32–44 Sakairi M, Yamamoto K, Ohtsu, Yoshida M (1989) Environmental control of gonadal maturation in laboratory-reared sea urchins, Anthocidaris crassispina and Hemicentrotus pulcherrimus. Zool Sci 6:721–730 Shpigel M, McBride SC, Marciano S, Lupatsch I (2004) The eVect of photoperiod and temperature on the reproduction of European sea urchin Paracentrotus lividus. Aquaculture 232:343–355 Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. Freeman, New York Stotz WB (2004) Sea urchin Wsheries: a Chilean perspective. In: Lawrence JM, Guzmán O (eds) Sea urchins: Wsheries and ecology. DEStech Publications, Lancaster, pp 3–17 Strub PT, Mesias JM, Montecinos V, Rutlant J, Salinas S (1998) Coastal ocean circulation oV western South America. In: Brink KH, Robinson AR (eds) The global coastal ocean. The sea, vol 11. Wiley, New York, pp 273–313 Urrutia MB, Ibarrola I, Iglesias JIP, Navarro E (1999) Energetics of growth and reproduction in a high-tidal population of the clam
123
Ruditapes decussatus from Urdaibai Estuary (Basque Country, N. Spain). J Sea Res 42:35–48 Vásquez JA (2007) Ecology of Loxechinus albus. In: Lawrence JM (ed) Edible sea urchins: biology and ecology, 2nd edn. Elsevier, Amsterdam, pp 227–241 Wahle RA, Peckham H (1999) Density-related reproductive trade-oVs in the green sea urchin, Strongylocentrotus droebachiensis. Mar Biol 134:127–137 Walker CW, Lesser MP (1998) Manipulation of food and photoperiod promotes out-of-season gametogenesis in the green sea urchin, Strongylocentrotus droebachiensis: implications for aquaculture. Mar Biol 132:663–676 Walker CW, Unuma T, McGinn NA, Harrington LM, Lesser MP (2001) Reproduction in sea urchins. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 5–26 Williamson JE, Steinberg PD (2002) Reproductive cycle of the sea urchin Holopneustes purpurascens (Temnopleuridae: Echinodermata). Mar Biol 140:519–532 Yamamoto M, Ishine M, Yoshida M (1988) Gonadal maduration independent of photic conditions in laboratory-reared sea urchins, Pseudocentrotus depressus and Hemicentrotus pulcherrimus. Zool Sci 5:979–988 Zamora S, Stotz W (1992) Ciclo reproductivo de Loxechinus albus (Molina 1782) (Echinodermata: Echinoidea) en Punta Lagunillas, IV Región, Coquimbo, Chile. Rev Chil Hist Nat 65:121–133 Zar JH (1984) Biostatistical analysis. Prentice-Hall, New Jersey
