Aquaculture 246 (2005) 181 – 195 www.elsevier.com/locate/aqua-online
Reproductive cycle of Argopecten purpuratus (Bivalvia: Pectinidae) in La Rinconada marine reserve (Antofagasta, Chile): Response to environmental effects of El Nin˜o and La Nin˜a Marcela Cantillaneza, Miguel Avendan˜oa, Ge´rard Thouzeaub,T, Marcel Le Pennecb a
Universidad de Antofagasta, Facultad de Recursos del Mar, Av. Universidad de Chile S/N, Casilla 170 Antofagasta, Chile b CNRS, UMR 6539 (LEMAR), IUEM, Technopoˆle Brest-Iroise, Place N. Copernic, 29280 Plouzane´, France Received 29 June 2004; received in revised form 20 December 2004; accepted 23 December 2004
Abstract Gonadosomatic index (GSI) and ovarian histology were used to determine the seasonality, amplitude, and magnitude of spawnings of the Argopecten purpuratus population within the marine reserve at La Rinconada, Chile, between December 1995 and February 2000. In general, spawnings occurred most of the year without prolonged periods of reproductive inactivity. Studies of this population throughout warm and cold oceanographic phenomena such as the El Nin˜o-Southern Oscillation (ENSO) event of 1997–1998 and the La Nin˜a event of 1998–2000 showed that the reproduction of this population occurred mainly between September and April, declining in the winter months from June through August, during which a period of sexual quiescence was observed in some individuals. An intense reproductive activity in the population, following the 1997–1998 warmer period, extended over the whole year. Histological analysis of the female portion of the gonad confirmed the GSI results and demonstrated the presence both of acini which appeared to be mature and other acini with various degrees of atresia and/or oocyte lysis. The study also revealed spawning asynchrony in this species and the presence of various stages of maturity within the same individual. Periods of high reproductive activity were correlated with strong diurnal temperature fluctuations and rises in phaeopigment concentration and phytoplankton cell counts, suggesting that these factors could be triggers for Argopecten spawning. These new insights on the reproductive cycle and conditioning of A. purpuratus would facilitate future management practices on the timing of artificial collectors and spat collection. D 2005 Elsevier B.V. All rights reserved. Keywords: Argopecten purpuratus; Reproductive cycle; Northern Chile; ENSO events; Culture improvement
1. Introduction T Corresponding author. Tel.: +33 2 98 49 86 39; fax: +33 2 98 49 86 45. E-mail address:
[email protected] (G. Thouzeau). 0044-8486/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.12.031
The Chilean scallop Argopecten purpuratus (Lamarck, 1819) is a dbay scallopT found in shallow
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bays from Paita, Peru (58S, 818W) to Valparaiso, Chile (338S, 718W; Bore and Martinez, 1980). Extinct beds have been found as far south as Bahia Vincente, Chile (378S, 738W; Wolff and Mendo, 2000). A. purpuratus would be a relict form of a tropical/subtropical fauna that existed in Chile and Peru in the Miocene (see Wolff, 1987). Life span of this fast-growing species is about 4–5 years and commercial size in north-central Chile (90 mm) is reached in 18 months (Stotz and Gonza´lez, 1997). The Tongoy and Guanaqueros banks (Coquimbo, 30814VS, 71822VW) in addition to the Rinconada (Antofagasta, 23828VS, 70830VW) and Mejillones (23804VS, 70827VW) banks were among the more important scallop banks to be exploited in the 1980s (Avendan˜o and Cantilla´nez, 1997). These last two populations contributed up to 80% of the annual landings at that time. Economic exploitation of A. purpuratus in Chile in recent years has been primarily based on cultured individuals, as the species was banned from harvesting on natural banks in 1988, due to severe overexploitation (Avendan˜ o and Cantilla´ nez, 1997; Stotz and Mendo, 2001). Indeed, the annual landings dropped dramatically from 4997 tons in 1985 to 492 tons in 1987 despite an identical fishing effort (Avendan˜o, 1993). The scallop fishery has been closed for many years, but natural scallop beds are still in jeopardy because illegal harvesting continues (Stotz and Gonza´lez, 1997). Since intensive culture began in the 1980s (see Disalvo et al., 1984), Chile has become the world’s third largest producer of cultured scallops (FAO, 1999), with 16,474 tons produced in 1998 (Stotz, 2000). The wild stock of scallops at that time was estimated to 10–15% of the total stocks of the species in Chile, with most of the individuals being kept in sea farms (Stotz, 2000). The domestication process of cultured species lead to genetic impoverishment (see Meffe and Carroll, 1994); Stotz concluded that it was urgent that selected natural beds be protected in order to preserve Argopecten genetic diversity. As part of management of the species as a renewable resource with conservation of wild reproductive stocks, a protected marine reserve was established by law in 1997 in the Rinconada Bay, north of the City of Antofagasta, Chile. The Rinconada population was selected because previous studies on
biometrics (adductor muscle weight) and enzyme polymorphism suggested that this population would be the most appropriate to be used in future aquaculture attempts (Avendan˜o and Le Pennec, 1997). Scallop management studies have been carried out within the reserve, the objectives of which included development of a program for artificial collection of scallop spat to be used both in repopulation of wild stocks to historic population levels and in support of mass culture activities in Chile. Successful development of a scallop spat collection program requires adequate knowledge of the reproductive cycle of the species, which in turn is critical to the knowledge of the natural history of the species as needed for the management of any commercial fishery (Barber and Blake, 1991). Previous studies carried out on the reproductive cycle of A. purpuratus populations from 238S to 308S have suggested that the species may produce gametes continuously, with partial or complete spawnings throughout the entire year (Brown and Guerra, 1980; Akaboshi and Illanes, 1983; Illanes et al., 1985; Navarro et al., 1991; Avendan˜o, 1993; Avendan˜o and Le Pennec, 1996, 1997). Analyses of spawning intensity done by observing the occurrence and frequency of sharp decreases in the gonadosomatic index (GSI) have allowed identification of periods of major reproductive activity, which vary with regard to months and duration. Barber and Blake (1991) reported that within a scallop population, individuals tend to mature and spawn synchronously, although intra-specific differences may occur in spawning frequency, period, and duration. These differences may be the result of environmental variations between years and localities. The main goals of the present study were to characterize the reproduction cycle of A. purpuratus, in order to later optimize scallop spat collection in La Rinconada Marine Reserve. For this, spawning seasonality as well as the amplitude and the magnitude of gamete release are described in relation to environmental factors such as temperature and food availability. Data were obtained during local non-periodic oceanic phenomena such as the El Nin˜o Southern Oscillation (ENSO), in which unusually warm seawater mass enters the area, and La Nin˜a event when unusually cold
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seawater conditions prevail for periods of several months.
2. Materials and methods 2.1. Geographic location of the study area The study area is known as La Rinconada Marine reserve sector of Antofagasta Bay at 23828V28US and 70830V35UW, about 20 km north of the City of Antofagasta in Chile’s 2nd Region (Fig. 1). A. purpuratus is mainly distributed between 6 and 29 m depth, with a scallop high-density area extending on the western part of the Bay (Cantillanez Silva, 2000). 2.2. Environmental parameters Water temperature was recorded at 16 m depth throughout the duration of this study, from the area from which scallops were collected (see Fig. 1), using a Minilog 8-BIT temperature recorder (Vemco, Model TR). Records were taken once daily at 0800 hrs from
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1st June 1996 to 31 September 1997. From October 1997 to February 2000, the temperature was recorded every 6 h. Water samples were collected from 16 m depth every 15 days between February 1999 and February 2000 using Nisking bottles. Chlorophyll and phaeopigment concentrations were measured after Strickland and Parsons (1972). Phytoplankton counts were made according to Utermo¨hl (1956). Regression analyses between the GSI values and pigment concentrations or phytoplankton cell counts were subsequently calculated for this period. 2.3. Scallop sampling Individuals of A. purpuratus were collected by divers from December 1995 to February 2000, within the scallop high density area in the Rinconada (Fig. 1). Sample depth ranged from 14 to 17 m. Each sample was made of 30 adult scallops measuring from 85 to 105 mm shell height. Scallops were collected monthly from May through October of a given year, and every 15 days from November of this year to April of the following year.
Fig. 1. Location of the study area, the Rinconada Bay (23828V28US, 70830V35UW), 20 km north of the city of Antofagasta (Chile, 2nd Region). (+) Site for bottom-water temperature recording (16 m depth; Minilog 8-BIT Vemco temperature recorder), bottom-water sampling for pigment analysis and phytoplankton cell counts, and sampling of A. purpuratus individuals. The scallops were collected by SCUBA divers every year from December 1995 to February 2000, within the scallop high density area. Sample depth ranged from 14 to 17 m.
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2.4. Gonadosomatic index The gonadosomatic index (GSI) was estimated on each specimen after Mottet (1979), Illanes et al. (1985), Wolff (1987), and Avendan˜o and Le Pennec (1997): GSI ¼ ðGW=WSPÞ 100 where GW=fresh wet weight of the gonad and WSP=fresh wet weight of soft parts. The mean and standard deviation were calculated for each sample and were used to determine the coefficient of variation following Paulet et al. (1997), in order to determine the degree of inter-individual synchrony of the A. purpuratus population for reproduction. The correlation coefficient between the GSI value and the coefficient of variation was estimated in order to detect any degree of association between the two indices. The statistical analyses were carried out following Zar (1984), using a SYSTAT 8.0 for Windows computational package (SPSS Inc., 1998).
determined. The samples were fixed in alcoholic Bouin solution and embedded in paraffin (Gabe, 1968). Sections of 5 Am thickness were then cut, mounted onto slides and stained with Masson trichrome (Gabe, 1968) for microscopic analysis. Qualitative classification of the stages of development of the ovarian tissue of A. purpuratus were adapted from the scale presented by Lucas (1965) for Pecten maximus. Five stages of sexual maturity were defined: (0) quiescent period, (1) initiation of maturation, (2) maturation, (3) advanced maturation and atresia, and (4) gamete release (Table 1 and Fig. 2). Once histological preparations were analysed and GSI values were determined, a frequency table was constructed between the GSI values (one-unit increments) and the percentages of individuals in the different stages of sexual maturity. Correlation analysis was then carried out between the GSI value and (using an angular transformation) the percentage of individuals in stage of advanced maturity and atresia (stage III), in order to estimate the degree of individual synchrony between gonad maturation and spawning events.
2.5. Gonad histology Histological analysis of gonad samples was carried out between December 1995 and September 1998, in order to follow gametogenesis and verify the GSI results. This analysis was done using tissue samples obtained from the middle of the female part of gonads obtained from specimens for which the GSI was
3. Results 3.1. Annual reproductive cycle The variations in the GSI values of A. purpuratus between December 1995 and February 2000 showed
Table 1 Classification scale for ovarian maturity stages in Argopecten purpuratus according to the scale of Lucas (1965) Stage no.
Stage name
Description
0 1
Quiescence Initiation of maturation Maturation
No cellular activity at the acini periphery. Absence of residual oocytes. Gonadal acini small. Germinal line mostly oogonia in proliferation and previtellogenic oocytes of various sizes adhering to the acini wall. Acini lumen large and mostly empty. Gonadal acini enlarging. Germinal line represented by vitellogenic oocytes adhering to the acini wall, and pedunculate oocytes. The lumen may contain free vitellogenic oocytes. Acini large in size, with a preponderance of completely developed free vitellogenic oocytes (polyhedric shape due to compression). Mature oocytes undergoing atresia or complete lysis begin to appear in the gonad. Partially or totally damaged acini may be present only in the distal portion of the section, or all acini may show partial or total lysis of mature oocytes. In some cases, generative activity may be observed in the walls. Also within this stage are included acini with oocytes in advanced vitellogenesis but showing signs of atresia. Initiation of gamete release, evidenced by the decrease in free vitellogenic oocytes in the lumen, some of which showing signs of atresia. Also classified in this stage are ovaries in advanced gametogenesis with the presence of residual oocytes and ovaries with symptoms of total evacuation of gametes characterized by small acini without generative activity in their walls. Residual oocytes may be seen in their lumens.
2 3
Advanced maturity and atresia
4
Gamete release
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Fig. 2. Histological sections of A. purpuratus gonad showing the different ovarian maturity stages (scale: 50 Am). (A) Stage 0: quiescence (no cellular activity at the acini periphery); (B) stage 1: initiation of maturation (O: ovogonia; PO: previtellogenic oocytes); (C) stage 2: maturation (PD: pedunculate oocytes; VO: vitellogenic oocytes); (D) stage 3: advanced maturity and atresia (MO: mature oocytes; AO: atretic oocytes); (E) stage 4: gamete release (EA: empty acini); (F) stage 4: gamete release (RO: residual oocytes). See Table 1 for the description of the different ovarian maturity stages.
gamete release most of the year (Fig. 3), with no prolonged quiescent period in reproductive activity of the population. Reproductive activity was consistently highest between September and April (GSI N10), with sudden declines in the gonadosomatic index followed by rapid recovery. A first minor spawning event was recorded during October, but main spawnings
occurred from November to December overall. In late fall and winter months (June to August), only small variations were noted in the GSI changes, thus highlighting low reproductive activity. Some alterations were observed in the above described pattern during the El Nin˜o event of 199798. A mass spawning event of the majority of the
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25
El Niño 97/98
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Fig. 3. Variations in the gonadosomatic index (GSI) of the A. purpuratus population between December 1995 and February 2000 (dotted line). The GSI was estimated on each specimen after Mottet (1979), Illanes et al. (1985), Wolff (1987), and Avendan˜o and Le Pennec (1997). Mean daily water temperatures at 16 m depth between June 1996 and February 2000 are superimposed (plain line; see Fig. 1 for site location). Records were taken once daily at 08:00 h from June 1996 to September 1997 and every 6 h from October 1997 to February 2000. No data from 01/06 to 30/10/1997, due to battery failure. The El Nino-Southern Oscillation (ENSO) event of 1997–1998 and the La Nin˜a event of 1998–2000 are also mentioned on the figure.
individuals was observed in late 1996 to early 1997, that is at the beginning of the ENSO event. After a sustained decline in the GSI values to a minimum in February 1997, there was a partial re-maturation of the population in March, initiating an unusually long intense (GSI N10) reproductive period from the winter of 1997 until April 1998. The lowest value of the GSI (4) ever recorded during the study, in May 1998, indicated total gamete release for most of the individuals and marked a new period of sexual quiescence. During the La Nin˜a event of 1998–2000, the reproductive activity of the Argopecten population was similar to the pattern observed in 1996 (which was considered a dnormalT year), except for January and February 2000, where the GSI values did not show any pronounced variation. 3.2. Gametogenic cycle Results of the histological analysis showed strong inter-individual variations of gonad maturity stages over the same sampling period (Fig. 4). The annual
gametogenic cycle of the population was characterized by the continuous presence, although in variable proportions, of individuals in stage 3 (advanced maturation and atresia) together with individuals in stage 4 (partial or total gamete release), except for July and August when some individuals showed sexual inactivity (stage 0). The simultaneous presence of mature oocytes, oocytes undergoing atresia and lysed oocytes was noted in all histological observations of gonads in the advanced maturation stage, thus precluding the definition of one intermediate stage (just mature oocytes) between stages 2 and 3 (Figs. 2 and 4). Inter-individual asynchrony in the gametogenic cycle of this population was observed throughout the year (Fig. 4). Reproductive patterns also showed high inter-annual variability linked to environmental forcing, especially the occurrence of the ENSO event. In 1996, the high percentages of individuals in stage 3 were concentrated in months coincident with the highest spawning rates, as indicated by the GSI. A strong decline in the number of individuals in stage 3 during the winter, together with an increasing
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Relative frequency of gonad maturity stages
quiescence
initiation of maturation
maturation
advanced maturity and atresia
187 gametes release
1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 d- j- f- m- a- m- j- j- a- s- o- n- d- j- f- m- a- m- j- j- a- s- o- n- d- j- f- m- a- m- j- j- a- s95 96 96 96 96 96 96 96 96 96 96 96 96 97 97 97 97 97 97 97 97 97 97 97 97 98 98 98 98 98 98 98 98 98
Fig. 4. Relative frequency of gonad maturity stages in the A. purpuratus population between December 1995 and September 1998. Following Lucas (1965), five stages of sexual maturity were defined: (0) quiescent period, (1) initiation of maturation, (2) maturation, (3) advanced maturity and atresia, and (4) gamete release.
proportion of individuals in stage 0 (from 10% to 50%), marked a period of lower gametogenic activity between June and August 1996. Similar trends were observed in 1998 during the La Nin˜a event. Various departures from the pattern typical of 1996 and 1998 were observed in the reproductive activity of the population in 1997: (1) in February, 25% of the individuals showed reproductive inactivity (stage 0), with a progressive decline of individuals in stage 3, the latter disappearing completely in March (100% of individuals in the initial maturation stage); (2) maturation began in April and continued uninterrupted until April 1998, with a gradual increase of individuals in stage of advanced maturation and atresia (stage 3); and (3) the winter months (June and July 1997) exhibited the predominance of individuals in stage 3 (up to 91% in July) and the absence of individuals in sexual quiescence (stage 0). 3.3. Synchrony of the reproductive process Individuals exhibiting different stages of gonad maturity (asynchrony) were observed within a given range of GSI values (Fig. 5). Maximum asynchrony
between individuals occurred for low GSI values (GSI b8), while a significant correlation existed between the GSI classes and the percentage of individuals in the stage of advanced maturity and atresia (r=0.895; df=15; pb0.001). However, only GSI values equal to or above 21 were exclusively associated with stage 3. Synchrony of the reproductive process is expressed by the coefficient of variation of the gonadosomatic index at each sampling period (Paulet et al., 1997). The mean value of the coefficient of variation of the GSI was 23%, which indicated a high degree of synchrony of reproductive events within this population. However, there was no association between the correlation coefficient for the total sample and the coefficient of variation of each GSI (r=0.133; df=106; p=0.17). This result suggests the absence of a regular pattern in the degree of inter-individual synchrony during the reproductive process. In fact, the degree of inter-individual synchrony showed strong and rapid seasonal variations. Asynchrony was generally highest in fall (March to May), followed by rapid synchronization in winter (Fig. 6). Marked interindividual asynchrony was visible at the histological level in fall and winter, particularly from April to
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14-15
22-23
23-24
24-25
27-28
gametes release
21-22
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20-21
advanced maturity and atresia
19-20
maturation
18-19
initiation of maturation
17-18
quiescence
16-17
1.0
15-16
0.9
13-14
0.8
12-13
0.7
11-12
Gonadosomatic index range
10-11
0.6
9-10
0.5
8-9
0.4
7-8
0.3
5-6
0.2
4-5
0.1 0.0 2-3
3-4
6-7
60 56 52 48 44 40 36 32 28 24 20 16 12 8
Fig. 6. Change in the coefficient of variation of the gonadosomatic index (GSI) of the A. purpuratus population between December 1995 and February 2000.
01/12/95 01/01/96 01/02/96 01/03/96 01/04/96 01/05/96 01/06/96 01/07/96 01/08/96 01/09/96 01/10/96 01/11/96 01/12/96 01/01/97 01/02/97 01/03/97 01/04/97 01/05/97 01/06/97 01/07/97 01/08/97 01/09/97 01/10/97 01/11/97 01/12/97 01/01/98 01/02/98 01/03/98 01/04/98 01/05/98 01/06/98 01/07/98 01/08/98 01/09/98 01/10/98 01/11/98 01/12/98 01/01/99 01/02/99 01/03/99 01/04/99 01/05/99 01/06/99 01/07/99 01/08/99 01/09/99 01/10/99 01/11/99 01/12/99 01/01/00 01/02/00
Fig. 5. Percentage of individuals of A. purpuratus in the different stages of gonad maturity, based on the respective values of the gonadosomatic index (GSI). See Fig. 3 legend for the definition of the 5 gonad maturity stages.
Relative frequency of individuals GSI variation coefficient
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irregular oceanic phenomena such as El Nin˜o and La Nin˜a. The ENSO event in 1997–1998 led to maximum bottom-water temperatures of 21.1 8C and 22.7 8C in 1997 and 1998, respectively (Fig. 3), and temperatures near 18 8C during the fall-winter months, which were unusual for this period. On the contrary, temperatures below 16 8C were frequent during the La Nin˜a event, starting in April 1998. Annual temperature patterns in 1998 and 1999 showed no clear temporal trends, except for the initial winter decrease in temperature and significant increases above 17 8C restricted to summer 1999 (March) and late spring 1999 (December). Temperature records at 6-h intervals showed daily variations which at some times of the year were greater than seasonal variations. The daily temperature variability around the mean was significantly different throughout the year (ANOVA; F 5,848=29.42, pb0.001). In particular, the periods of May to August 1998, July–August 1999, and January to late February 2000 exhibited within-day variations of less than 2.2 8C (Fig. 7), which coincided with decreases in
August 1996 and 1998. However, a tendency towards synchronization was observed in the population when the individuals reached the stage of advanced maturity and atresia, and in periods prior to major spawnings (N80% of the individuals in stage 3). Another period of synchrony in the population was observed during the initiation of gametogenesis (stage 1) in March 1997 and in January 1999. In the latter, all the individuals proceeded in gonad development synchronously, reaching 100% maturity in February of that year. On the other hand, the results of this study also suggest low synchrony in spawning events, where, although a high percentage of mature individuals occurs, only a fraction of the latter actually release gametes. 3.4. Environmental fluctuations during the study period 3.4.1. Bottom-water temperature Bottom-water temperature showed high year-toyear variability in the study area, produced by 7
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y = -4E-15x + 8E-10x - 7E-05x + 3.4724x - 94164x + 1E+09x - 8E+12 2
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Fig. 7. Differences between the minimum and maximum temperature (dT in Celsius degrees) recorded daily at 16 m depth between 10 November 1997 and 29 February 2000 in the Rinconada Bay.
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Argopecten reproductive activity. In periods between November 1997 and April 1998, September 1998 and June 1999, and between September and December 1999, there was a greater dispersion of temperature values around the mean; maximum temperature variation for the first two periods was F5.5 8C versus F6.5 8C in the third one (Fig. 7). These periods of high within-day temperature changes coincided with a high degree of reproductive activity in the scallop population.
tration (r=0.48; df=21; p=0.02), and between the GSI and phytoplankton density (r=0.55; df=22; p=0.006). On the other hand, reproductive activity of the A. purpuratus population was not associated with chlorophyll a concentration in bottom-water (r=0.11; df=21; p=0.61).
4. Discussion The results obtained using the GSI values and histological data of the A. purpuratus population support the hypothesis of a continuous, more or less intense, spawning process over the entire year. Under dnormalT oceanographic conditions, reproductive activity is most intense from September to April of the following year; the same pattern was observed during the cold temperature anomaly of bLa Nin˜aQ, which occurred from the end of 1998 to the beginning of 2000. Reproduction intensity declines considerably from May to July, when a portion of the population enters a period of sexual quiescence. Reactivation of the reproductive process occurs in August, with a large number of scallops found in the initial stage of
3.5. Pigment concentrations Periodic rises in chlorophyll a concentrations were recorded in the study area throughout the year, with peak values ranging from 6 to 20 Ag l1 at 16 m depth in 1999 (Fig. 8). These rises coincided with rises in phytoplankton cell counts, the values of which fluctuated between 3 and 207 cells ml1. The phaeopigment concentrations rose in the middle of April, end of July, and beginning of September 1999, with the latter peak being the highest at 4.7 Ag l1. A significant negative relationship was found between the GSI values and phaeopigment concenchlorophyll
pheopigment
phytoplankton density
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20 18
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12 10 8
100
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Pigment concentration ( g l-1)
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Fig. 8. Pigment concentrations (chlorophyll a and phaeopigments; Ag l1) and phytoplankton cell counts (cells ml1) in bottom water at 16 m depth, in the Rinconada Bay (see Fig. 1 for site location).
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gametogenesis (stage 1), and a few individuals in the maturation stage (stage 2). These results confirm previous observations made on populations of A. purpuratus along the northern coast of Chile: in addition to spawning events over most of the year, several studies have mentioned that this species has the ability to replace gametes within periods of about 20 days after spawning (Brown and Guerra, 1980; Illanes et al., 1985; Avendan˜o, 1993; Avendan˜o and Le Pennec, 1996, 1997). The highintensity spawning periods, although typical of the species, may vary greatly from one population to another (both in terms of occurrence and duration), depending on the geographical location of the scallop beds. In Tongoy Bay (30814VS), the reproductive activity is generally highest in spring and summer (Akaboshi and Illanes, 1983). In Mejillones Bay (23804VS), reproduction would last for 150 days, from January–February to June (Avendan˜o and Le Pennec, 1996, 1997). At La Rinconada (23828VS), previous studies (Avendan˜o, 1993; Avendan˜o and Le Pennec, 1996, 1997) suggested that the main spawning period of A. purpuratus extended for 120 days, beginning in December and ending in March, with secondary spawning occurring in August–September. The present study, however, gives a more reliable description of the reproduction patterns occurring over an 8month period from September to April. Further North, in Bahı´a Independencia (Peru, 14810VS), reproduction would occur all year long after ENSO events (Cha´vez and Ishiyama, 1989). Whether the duration of the reproductive period increases from South to North within the A. purpuratus distribution area remains to be determined however, since all the studies did not occur at the same time, i.e., in the same environmental conditions (El Nin˜o vs. La Nin˜a). Extended reproductive periods exhibited by some bivalve populations have been considered as adaptive strategies to variable environmental conditions, particularly bottom-water temperature and food availability (Newell et al., 1982; Paulet et al., 1988; Avendan˜o, 1993). The long reproductive period observed for P. maximus in the Bay of Brest (France) would allow individuals to carry out a series of reproductive trials culminating in major larval settlement when pediveliger larvae encounter favorable environmental conditions (Paulet et al., 1988). This example of the match/mismatch theory once proposed
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by Cushing (1982) for fish populations may not apply for A. purpuratus in the Rinconada Bay. The strong interindividual synchrony found in this study when using the coefficient of variation for the reproductive events in the population contrasts with the histological results, which show individual asynchrony within the same population. This discrepancy may result from the occurrence of different stages of gonad development within a narrow range of GSI values (a low standard deviation within a sample may lead to the erroneous conclusion of the existence of individual synchrony). On the basis of the histological results of this study, one can say that the reproductive process of A. purpuratus in the Rinconada Bay is asynchronous, which has previously been suggested by Avendan˜o and Le Pennec (1996, 1997), and that the tendency towards synchrony only occurs in particular periods, such as those which precede major spawning events. According to Martinez et al. (2000a), gamete release in A. purpuratus would be triggered by the detection of an external stimulus implying intermediation by amines in the gonads, in some way modulated by prostaglandins. Barber and Blake (1991) showed that a population of Argopecten irradians would act in synchrony to reach sexual maturity, in spite of variations in oocyte size due to differences in time of initiation of cytoplasmic growth. The latter in turn may rely on the quantity of energy available to the gonad. Individual internal controlling mechanisms may exist, which may be sensitive to environmental factors capable of initiating the oocyte cytoplasmic growth phase (Barber and Blake, 1991). Paulet et al. (1997) also reported that the period of early gametogenesis in P. maximus (Bay of Brest, France) was characterized by being a highly synchronized process, with maximum intensity during spring (April–May) every year. Thus, an entire population may be stimulated into initiation of gametogenesis at the same time and progress synchronically towards maturity as a response to environmental changes. Then, synchronous spawning may occur when all members of the population are mature and react simultaneously to factors which induce spawning. This functional scheme is based on the hypothesis that spawning synchrony depends on the critical stage of physiological maturity of the population as a whole, and the sensitivity of the population to exogenous spawning inducers.
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By contrast, the asynchrony observed in a large portion of A. purpuratus spawnings in this study, despite early gametogenesis synchrony, supports the hypothesis that successive gamete releases from groups of individuals within the overall population is part of the reproductive strategy of the species, as a response to variable environmental conditions. Thus, the probability that at least some of the larval cohorts produced achieve survival and settlement would be increased, as hypothesized for P. maximus in the Bay of Brest and at the Isle of Man, off England (Paulet, 1990). It has been suggested that high bottom-water temperature may promote greater synchrony of major spawnings by Placopecten magellanicus, but the individuals may adopt a bdrop by dropQ strategy if environmental conditions are not favorable, which increases the probability that at least some larvae will survive (Barber and Blake, 1991). This strategy is supported in the present study by the histological results, where different stages of oocyte maturity could be found within the same individuals of A. purpuratus. Barber and Blake (1991) suggested that for some scallop populations, successive bwavesQ of maturing oocytes might allow pulses in gamete release, which could extend over periods of 8 weeks after the initiation of spawning. Another characteristic of A. purpuratus reproduction in La Rinconada is the co-occurrence of apparently mature and atretic oocytes. Oocyte degeneration, previously mentioned by Avendan˜o and Le Pennec (1996, 1997), has also been observed in other pectinid species, among which are Chlamys varia (Lucas, 1965), Aequipecten opercularis (Allarakh, 1979), Pecten ziczac (Peres, 1981), Mizuhopecten yessoensis (Motavkine and Varaksine, 1983), P. magellanicus (Beninger, 1987), A. irradians (Epp et al., 1988), P. maximus (Dorange and Le Pennec, 1989), and Pecten jacobaeus (Mestre, 1992). In the present study, various degrees of oocyte atresia were observed even when the individuals had GSI index over 21 and were histologically in the final maturation stage. Overmaturity of the oocytes may greatly influence larval development and ultimately larval survival. This pattern has been frequently cited in explanation of certain failures of scallop larval growth and settlement in the wild, as well as in commercial scallop hatcheries. In particular, oocyte atresia may be the cause of some of the difficulties encountered in
artificial production of A. purpuratus spat in Chile (Avendan˜o et al., 2001). Numerous authors have shown or suggested the effects of environmental parameters on the reproductive processes of scallop species. Sastry (1966) suggested that the coincidence of high temperature and food availability induced gonad development in A. irradians. Temperature-dependent transfer of energy from somatic tissues to the gonad was then demonstrated experimentally for this species (Sastry and Blake, 1971). Paulet (1990) and Paulet et al. (1997) showed the strong dependence between gonad weight and water temperature for P. maximus. Illanes et al. (1985) suggested the roles of temperature and food availability on gametogenesis and spawning of A. purpuratus in Tongoy Bay, while Wolff (1988) suggested that rises in temperature occurring during the 1982–1983 ENSO event stimulated gonad maturation and probably intensified the spawning events on the Peruvian scallop beds. On the other hand, Avendan˜o (1993) suggested that scallop mass spawning events observed at Mejillones and La Rinconada occur under temperature conditions below the maximum values recorded in these two bays. In the present study, it was found that: (i) discrete and sustained increase in water temperature occurring during August and September coincided with the initiation of reproductive activity at La Rinconada, (ii) a high percentage of individuals were mature by the end of this period, and (iii) even if a seasonal pattern is not observed for temperature during cold (La Nin˜a) years, the sudden changes in bottom-water temperature which may occur during one day (up to 6.5 8C on December 2, 1999) may induce Argopecten spawning, whatever the oceanographic conditions. The latter result agrees with those of Barber and Blake (1991) and Paulet et al. (1997) showing how either rises or declines in temperature over short time periods can trigger scallop spawning. This pattern is not common in the literature; most of the studies on bivalves refer to temperature increase as the triggering factor for gametogenesis and spawning. The present results suggest that during the ENSOrelated warming of the water column between November 1996 and February 1997, reproductive activity became more intense and sustained than in the absence of the ENSO event in the Rinconada Bay. These conditions led to complete gamete release by A.
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purpuratus, similarly to that reported by Illanes et al. (1985) in Tongoy Bay during the El Nin˜o event of 1982–1983. During the occurrence of the 1996–1997 ENSO event, the scallop population in La Rinconada did not show the typical periods of low reproductive activity, which occur in dnormalT years between May and August. On the contrary, a more intense and continuous reproductive process was observed, which extended from March 1997 to April 1998. These results agree with Wolff (1987, 1988) indicating intensified spawning activity with subsequent recruitment during the 1982-83 El Nin˜o years, leading to a 60-fold increase of the scallop population size (up to 86–129 ind m2) off Pisco in 1983–1984. Stotz (2000) also found a very intense spatfall in Tongoy Bay during the 1996–1997 ENSO event leading to a 13-fold increase of the Argopecten stock in the protected area of Puerto Aldea. According to Wolff (1987), this relict species of a Miocene tropical/ subtropical fauna of the Caribbean and Atlantic would have maintained its warm-water characteristics during evolution in the cold upwelling waters because of periodic post-Miocene El Nin˜o events. Surprisingly, experimental results on the interactive effects of temperature and diet on reproductive conditioning of A. purpuratus breeders showed that gonad recovery was slower for individuals conditioned at 20 8C compared with 16 8C (Martinez et al., 2000b). The percentage of gamete fertilization did not differ between the different treatments but the percentage of larvae D survival was much higher for those issued from scallops conditioned at 16 8C and fed pure microalgae or microalgae mixed with lipids. It is possible however that the higher metabolic requirements the scallops have at 20 8C could not be met in the laboratory. The effects of the 1996–1997 ENSO event on the larval, post-larval and juvenile stages of A. purpuratus in the Rinconada will be discussed later on in a second paper. The present study established a negative correlation between the GSI index and pheopigment concentration or phytoplankton cell counts, which suggested that the decline in the GSI index (that is spawning) might be linked to food availability. This parallels previous results of Avendan˜ o (1993) showing significant correlations between Argopecten spawning periods and months of high pelagic primary production in the bays of Mejillones and La Rinconada. Such a trend
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was also cited by Navarro et al. (1991) who reported the existence of two annual spawning peaks for A. purpuratus in Mejillones Bay, which coincided with phytoplankton and temperature variations occurring in late spring. Whether phytoplankton or resuspended microphytobenthos constitutes the main food source for Argopecten in La Rinconada remains to be determined however. On the other hand, an experimental work (Navarro et al., 2000) suggested that reproductive conditioning in A. purpuratus was mainly affected by the diet and not by temperature. It is likely, however, that experimental conditions in the latter study exceeded the minimum threshold of temperature before food could influence reproductive conditioning. In agreement with Himmelman (1981), A. purpuratus would fit the pattern of evolved marine invertebrates with planktotrophic larvae, which adjust their life cycle to release their gametes at times when food is available in the water column, which may assure the success of larval survival. Further work is required to use the temporal variations of food availability to predict spawning events in the Rinconada Bay.
5. Conclusions This study provides new and useful results on A. purpuratus reproduction in the Rinconada Bay, that is the area designed to permit repopulation of wild scallop beds to historic population levels and to support the mass culture activities undertaken in the Bay and elsewhere in Chile. The results obtained allow to the characterization of scallop response to environmental forcing, with the occurrence of two opposite hydro-climatic regimes, El Nin˜o and La Nin˜a, during the study period. They clearly show the interest of monitoring scallop reproductive processes in the Bay, in order to optimize spat collection on artificial Japanese collectors, which is one of the objectives of the management studies being carried out within the reserve. In particular, intense spatial and possibly trophic competition within the collectors (Cantillanez Silva, 2000), both intra- and inter-specific, requires optimal deployment of the artificial substrates with respect to the occurrence of larval stages, in order to reduce collector immersion. These optimal temporal bwindowsQ can be easily identified from the survey of the GSI index. Spat collection on artificial substrates
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and subsequent seeding of Argopecten juveniles are all the more important to avoid recruitment failure in the Rinconada Bay. Indeed, the only natural substrates available for settlement, which are the benthic red macroalgae Rhodymenia sp., disappear during warm years and their absence may last for several years. The impacts of warm and cold years on the larval, postlarval and juvenile stages of A. purpuratus in the Rinconada, and the way the results obtained can be used to improve further scallop cultivation in the Bay, will be discussed later on in another paper.
Acknowledgments This research was financed through the Regional Development National Fund (FNDR), Antofagasta, Chile No. 20124810-0 and No.20127869-0, and a ECOS-CONICYT (France-Chile) program (Action No. C98B02). The authors greatly acknowledged Dr. L.H. Disalvo for translating an earlier version of the manuscript. Contribution No. 942 of the IUEM, European Institute for Marine Studies (Brest, France).
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