Reproduccion Aulacomya

7/26/2019 Reproduccion Aulacomya

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Reproductive cycle ofAulacomya ater [Bivalvia:

Mytilidae (Molina 1782)] in Punta Arenas Cove(Antofagasta Region, Chile)

Miguel Avendano Marcela Cantillanez

Received: 21 August 2013 / Accepted: 22 December 2013 Springer Science+Business Media Dordrecht 2014

Abstract Changes in the condition of broodstock, presence of larvae, and post-larval

settlement of A. ater in Punta Arenas Cove (Antofagasta Region, Chile) were used to

determine its reproductive cycle. The condition used as a spawning indicator shows that

these events occur in three periods throughout the year (MayJuly, AugustNovember, and

DecemberFebruary). Intense periods recorded in OctoberNovember and December

February coincided with periods in which the water temperature descended to less than

13 C. Simultaneously, plankton samples indicated constant presence ofA. aterlarvae atthis site, with large increases in abundance during August and between October and

January, reaching a maximum of 2,192 larvae m-3 in October. The periods of increase in

larval abundance coincide with spawning periods; however, the greatest abundances were

recorded before the start of the descent of the spawning indicator of the population under

study. Monthly installation and replacement of collectors, after recording the first

spawning, showed the permanent settlement of A. aterpost-larvae over the course of the

study, with a period of greater intensity occurring from the end of August to the end of

January, registering peaks in October and November with 5,667 and 4,183 post-lar-

vae 9 600 cm2 collector-1, months which also coincide with the greatest larval abun-

dance. The presence of larvae and post-larvae of the mytilids Choromytilus chorus andSemimytilus algosuswas also recorded alongside A. aterlarvae and post-larvae. Ch. chorus

presented a cycle very similar to that ofA. aterin both stages, with a maximum abundance

of 4,531 larvae m-3 in November and 13,533 post-larvae 9 600 cm2 collector-1 in

December.

Keywords Aulacomya ater Mytilids Chile Reproductive cycle

Larval cycle

M. Avendano (&) M. Cantillanez

Laboratorio de Cultivo y Manejo de Moluscos, Dpto. de Ciencias Acuatica y Ambientales,

Universidad de Antofagasta, Av. Universidad de Chile S/N, Casilla 170, Antofagasta, Chile

e-mail: [email protected]

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DOI 10.1007/s10499-013-9743-5


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Introduction

Currently, the farming of mytilids in Chile is made up of three species: Mytilus chilensis,

Choromytilus chorus,andAulacomya ater, whose production in 2010 reached 221,522 tons

for M. chilensis, 1,736 tons for A. ater, and 757 tons for Ch. chorus (Sernapesca 2011).This productive activity, 99 % of which is concentrated in the Lakes Region (42S), is

sustained exclusively by pediveliger larvae collection from the natural environment, just as

is done traditionally in other mussel farms around the world, where natural spat collection

is considered the most important segment of this activity. However, despite the importance

of this step to maintain the growth of farms, in Chile, there are few studies focused on

understanding the dynamics of natural banks as a source of larvae, and the temporal

distribution of the banks used as capture places is poorly understood.

Knowledge of the biological and reproductive cycles of species, and their duration, is

not only necessary to create an effective spat collection program, but is also necessary to

provide qualitative information regarding the strength of the recruitments (Avendano and

Cantillanez2008). Hjort (1914) described knowledge of larval availability as indispensable

because it is a determining factor of population abundance, while Bayne (1976) indicated

that the larval abundance pattern of mytilids was related to spawning of the local adult

population.

In northern Chile,A. ater, a species which is distributed along the Pacific Ocean from El

Callao, Peru to the Strait of Magellan in Chile, extending along the Atlantic Ocean from

the south of Argentina to the south of Brazil, and also present along the South African

coast (Avendano and Cantillanez2013), has been, economically, the most important of the

mytilids. Between 1973 and 1981 in the Bay of South Mejillones (23

S), commercialproduction reached over 500 tons annually (Avendano1984). Based on this history, and

with the intention of evaluating the possibilities of restarting A. aterfarming in this area of

the country, the following study was done, which seeks to determine the reproductive cycle

and quantify the abundance and timing of larvae and the settlement of post-larvae, so as to

implement future programs of artificial spat collection which could satisfy commercial

demand for A. ater.

Materials and methods

Study area

This study was done in Punta Arenas Cove (21380S; 70090W), in Antofagasta Region,

Chile (Fig.1). This place has a natural bank ofA. ater, which is distributed from depths of

15 m to more than 30 m. Oceanographically, this area is located in a subtropical transition

zone which, during a normal year, presents a predominance of the sub-Antarctic water

mass (ASA), which dominates the upper 200 m of the northern branch of the cold

Humboldt Current. These waters (ASA) mix with a smaller proportion of subtropical

waters which contain a higher salinity and temperature, and also mix periodically withcolder waters that come from greater depths and correspond to subsurface equatorial

waters, which ascend toward the coast due to upwelling induced by southern and south-

eastern winds that predominate in this zone (Avendano and Cantillanez 2011). As a

response to these irregular upwelling processes, which are present during most of the year,

with intense periods in summer and winter, there are variations of temperature which have

altered seasonal cycles (Escribano et al. 1995,2002).

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Water temperature in the study area

The average daily water temperature in the area where theA. aterpopulation is distributed

was determined using records obtained with data loggers (Tid Bit, onset model), installed

at a depth of 16 m, and programmed to take measurements every hour for the duration of

the study period.

Reproductive cycle

Numerous authors (among them Winter et al.1980; Prieto et al.1999; Oyarzun et al.2010)

have shown that fluctuation of meat weight (condition indexes) is a good indicator for

detecting massive spawnings in mytilid populations. To establish the reproductive cycle of

the study population ofA. ater, the spawning indicator applied by Avendano and Cantil-

lanez (2013) was used. This spawning indicator corresponds to changes of the slope value

(b), obtained from the following potential adjustment function: dry weight (g) = a 9 size

(mm)b

, in which the decrease in the value ofb represents a spawning event. Thus, monthly

sampling between March 2010 and March 2011 was done, extracting 100 specimens each

month from the natural bank, with sizes that varied between 65 and 95 mm along the

anteriorposterior axis. In the laboratory, the specimens were individualized and submitted

to a steam bath to extract the meat, which was dehydrated in an oven at 80 C to obtain a

constant weight.

Fig. 1 Geographic localization of the study site in the Antofagasta Region, Chile. (1) Punta Arenas Cove,

(dark circle) areas of larval sampling

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Larval sampling

Between April 2010 and March 2011, quantitative sampling of larvae was done with a

periodicity of 15 and 30 days at three sampling stations (Fig. 1). A 55-lm mesh HYDRO-

BIOS plankton net was used to perform vertical plankton hauls from a depth of 18 m. Thesamples were then transported to the laboratory where the larvae in each sample were

identified, counted, and measured. Identification ofA. aterlarvae (given their interaction in

the samples with two other mytilids: Chorumytilus chorus and Semimytilus algosus) was

done with a morphological and morphometrical analysis (Le Pennec1978; Ramorino and

Campos1983; Avendano et al.2011). All of the larvae were counted; however, when they

were very abundant, they were homogenized in a plankton sampler with 10 divisions, and

two subsamples of 1/10 of each of these were taken to be counted and measured using

stereomicroscope with ocular micrometer (Avendano et al. 2006, 2007). The number of

total larvae in each sample was calculated using the average obtained in the two subs-

amples multiplied by ten, and the total larvae per m3 were determined using the volume of

water filtered through the plankton net. The average of each sampling period was calcu-

lated from the three samples obtained. The larvae size was measured using the anterior

posterior longitude (Le Pennec 1978).

The size population structure that the larvae of the three mytilids presented in the

samples was later submitted to an analysis of cohort discrimination (Cantillanez et al.

2007; Avendano et al.2011), in order to identify the number of cohorts, mean length, and

proportionality of the cohorts, per species, using the program MIX 3.1a (MacDonald and

Pitcher 1979). The histograms of size frequency were plotted according to a normal

distribution (significance level = 0.05).

Installation and sampling of collectors

Starting on July 29, 2010, after a decrease in the A. aterspawning index and confirmation

of the presence of larvae in the plankton, a collector was installed and replaced monthly.

This collector consists of a 10-cm-wide by 12-m-long strip of net used for anchovy

collection that was in disuse. It was tied to an experimental farming line and installed in a

16-m-deep column of water. The collectors were then ready to start from 1 m depth with

the help of a rope which tied them to the mother line, therefore maintaining themselves

vertically using a weight tied to its lower section (Avendano1984).Each collector was extracted monthly and transported to the laboratory where, after

visually confirming spat settlement on them, 100 cm2 sections were obtained from its

upper, middle, and lower parts, and were then washed separately with a 180-lm sieve,

detaching all of the attached post-larvae (Cantillanez et al. 2007). All the post-larvae

obtained from each section of the collector were homogenized in a plankton separator with

10 divisions, and two subsamples of 1/10 were fixed in 708 alcohol and submitted to an

analysis under a stereoscopic microscope with ocular micrometer, so as to identify,

measure, and count the species (Avendano et al.2007). The average monthly settlement of

post-larvae of each species was obtained from the settlement recorded in the three sections

of the analyzed collectors, permitting the projection of their settlement to 600 cm2 (con-

sidering both faces of the sampled section).

A one-way ANOVA was used to detect differences in the abundance of the post-larvae

per species, with prior transformation of the data (log X? 1) for normalization and

homogenization of the variance. A post hoc Scheffes pair-wise multiple comparison test

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was performed when significant differences were detected. The tests were done in Systat

12, and the significance was determined at a = 0.05.

The demographic structure of the post-larvae of each species of mytilid identified in the

collectors, considering that Ch. chorus and S. algosus attached themselves along with A.

ater, was produced by integrating the measurement obtained in the three sections of the

collector. Later, the number of post-larval cohorts and their median size were estimated

following the same methodology described for the identification of larval groups.

Results

Environmental parameters

The average daily temperatures during the course of the study fluctuated between 12.4 and17.6 C (Fig.2). High temperatures above 16 C were recorded at the start of autumn (the

end of March and middle of April 2010), while decreases in daily averages between 13.6

and 12.9 C occurred between October 25 and November 4 as well as 13.7 and 12.9 C

between December 14 and January 3, 2011.

Reproductive cycle

The spawning indicator used to determine the reproductive cycle of A. ater during the

study period (Fig. 3) shows that this species spawns more than once during the annual

cycle, with variable intensities. A low magnitude evacuation of gametes is recorded in

winter, between the end of May and the last days of July. Afterwards, a marked decrease

occurs starting at the end of August, with a rapid and sustained evacuation of gametes

during the last 15 days of the month of October that reaches its lowest value of 0.5 at the

beginning of November, making it the most important spawning event of this species in the

study area. A second event of lower magnitude occurs in summer, with a sustained

01-Mar-10

01-Apr-10

01-Ma

y-10

01-Ju

n-10

01-Jul-10

01-Au

g-10

01-Se

p-10

01-Oct-10

01-No

v-10

01-De

c-10

01-Ja

n-11

01-Fe

b-11

01-Mar-11

Temperature

C

11

12

13

14

15

16

17

18

19

Fig. 2 Mean daily water temperatures recorded in Punta Arenas Cove at 16 m depth between March 2010

and March 2011

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decrease in the indicator that sets off in the beginning of December, reaching its minimum

value of 0.8 at the start of February.The intense spawning periods occurring between OctoberNovember and December

February coincide with periods in which the water temperature reached the lowest daily

average values in the area where the A. aterpopulation is distributed.

Larval cycle

The presence of A. ater larvae was constant in the study area (Table 1), with a hetero-

geneous temporal abundance pattern. The maximum annual peak of 2,192 larvae m-3

was

produced in the middle of October and beginning of November. Large increases also

occurred at the end of August, beginning of December, and end of January, when thevalues varied between 272 and 453 larvae m-3. These periods of greater larval abundance

coincide with the periods in which decreases in the spawning indicator were recorded;

however, the greatest abundances were recorded in earlier dates, before the decrease in the

indicator.

Between one and four different A. ater, larval cohorts were identified in the obtained

samples, of which their median sizes indicated the presence of post-larval stages, com-

petent larvae, and initial phases of development (Table 1). The post-larval and initial stage

cohorts were present during a large part of the study, presenting the first median sizes that

varied between 278.5 and 371.3 lm, in proportions that represented 8 and 100 % of the

samples, and the second, with median sizes that varied between 117.3 and 137.5 lm,

reaching proportions of 13.7 and 100% of the sample (Table 1). The greatest proportions of

cohorts in initial stages occurred in dates before the decrease in the spawning indicator of

the population ofA. ater in the area.

The results also showed that, along with A. aterlarvae, in all of the samples, Ch. chorus

and S. algosus were found. The larval abundance of this species increased in the same

Fig. 3 Variation of the slope value (b) used as a spawning indicator for A. ater in Punta Arenas Cove,

Antofagasta Region, Chile, between March 2010 and March 2011. The bars represent in the confidence

interval for the slope (a = 0.05)

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Table1

Averagenu

mberoflarvae/m

3

andlarvalcohortsofA.ater,

Ch.chorus,

andS.algosus(C

n),identifiedineachs

amplingdate

Date

Me

anlarvae

perm

3

SD

Cohort1

Proportion

(%)

Cohort2

Proportion

(%)

Cohort3

Proportion

(%)

Cohort4

Proportion

(%)

Length

SD

(lm)

Length

SD

(lm)

Length

SD

(lm)

Length

SD

(lm)

A.ater

04-2

9-2

010

11

2

324.1

18.9

26.4

235.1

18.3

25.9

158.0

8.2

47.7

05-3

1-2

010

9

4

311.0

36.1

48.0

128.2

19.2

52.0

06-2

9-2

010

54

5

328.8

27.2

13.9

196.4

23.1

16.2

120.9

12.3

69.9

07-2

7-2

010

17

6

337.5

53.0

14.3

137.5

22.4

85.7

08-2

6-2

010

2

72

49

332.6

25.0

29.2

210.4

23.5

10.8

117.6

10.0

60.0

09-0

7-2

010

18

10

126.4

3.4

100.0

10-0

1-2

010

49

20

355.0

3.4

75.8

239.2

14.1

8.5

162.7

8.0

15.7

10-1

5-2

010

21

92

514

371.3

6.9

8.0

211.7

8.8

4.1

117.3

1.0

87.9

11-0

4-2

010

9

98

175

330.1

6.0

8.1

207.2

1.4

91.9

11-1

8-2

010

2

26

93

287.7

23.2

21.7

127.2

19.3

78.3

11-2

4-2

010

48

8

228.5

13.0

30.3

157.4

5.1

69.7

12-0

2-2

010

4

53

109

334.8

5.3

25.9

278.5

5.6

23.5

211.3

5.2

13.7

134.2

2.5

36.9

12-1

6-2

010

1

30

64

344.2

3.2

34.0

287.6

7.1

11.9

241.1

1.9

54.1

12-2

9-2

010

91

15

350.1

4.9

45.8

282.7

6.8

25.0

241.6

5.3

29.2

01-2

7-2

011

3

85

156

193.5

2.9

86.3

131.8

8.8

13.7

03-0

3-2

011

55

28

303.7

2.8

100.0

03-3

1-2

011

40

17

328.1

11.2

20.5

214.1

9.3

32.0

142.2

6.2

47.5

Ch.chorus

04-2

9-2

010

5

3

273.6

26.8

27.8

151.3

20.2

73.7

05-3

1-2

010

23

10

128.9

18.0

100.0

06-2

9-2

010

72

17

142.3

45.0

100.0

07-2

7-2

010

25

14

104.4

45.9

100.0

08-2

6-2

010

48

8

249.6

26.4

27.8

147.8

16.6

72.2

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Table1

continued

Date

Me

anlarvae

perm

3

SD

Cohort1

Proportion

(%)

Cohort2

Proportion

(%)

Cohort3

Proportion

(%)

Cohort4

Proportion

(%)

Length

SD

(lm)

Length

SD

(lm)

Length

SD

(lm)

Length

SD

(lm)

09-0

7-2

010

26

1

122.5

27.9

100.0

10-0

1-2

010

88

62

354.5

42.8

21.6

140.5

38.3

78.4

10-1

5-2

010

7

09

192

356.9

30.3

48.7

129.6

25.2

51.3

11-0

4-2

010

2

51

136

356.2

27.8

30.4

237.3

25.1

57.5

137.1

25.1

12.1

11-1

8-2

010

4,5

31

1,7

19

355.8

24.0

55.7

248.0

26.8

14.6

140.2

24.8

29.7

11-2

4-2

010

78

26

363.3

29.9

65.7

264.3

25.5

11.4

150.8

17.7

22.9

12-0

2-2

010

1,6

86

317

223.5

25.5

86.2

110.5

15.8

13.8

12-1

6-2

010

1,5

01

239

341.8

30.0

89.1

204.7

25.0

10.9

12-2

9-2

010

1

87

78

565.5

40.0

15.2

381.2

36.8

57.8

267.1

30.0

15.5

159.4

22.9

11.5

01-2

7-2

011

2

72

57

296.4

39.9

37.0

170.0

27.0

63.0

03-0

3-2

011

19

9

150.4

32.0

100.0

03-3

1-2

011

20

12

257.9

26.5

51.3

178.8

24.0

48.7

S.algosus

04-2

9-2

010

77

5

185.6

16.7

61.2

141.6

11.6

38.8

05-3

1-2

010

24

9

147.2

15.6

100.0

06-2

9-2

010

1

01

22

272.6

32.6

19.7

178.8

20.4

29.6

129.7

19.3

50.7

07-2

7-2

010

41

12

134.3

25.1

100.0

08-2

6-2

010

1,8

71

554

196.5

36.8

30.9

111.8

8.8

69.1

09-0

7-2

010

20

3

183.5

19.6

64.4

134.4

14.5

35.6

10-0

1-2

010

1

06

28

361.3

32.6

34.3

175.1

25.4

65.7

10-1

5-2

010

1,8

86

494

342.3

32.0

11.7

199.2

22.2

30.3

114.5

10.5

58.0

11-0

4-2

010

3

07

108

360.7

35.0

14.7

193.0

17.6

63.1

133.8

10.6

22.2

11-1

8-2

010

5

85

289

309.8

30.3

23.2

129.6

22.1

76.8

11-2

4-2

010

1

49

107

301.0

35.2

49.0

181.0

18.8

39.5

110.4

13.0

11.5

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Table1

continued

Date

Me

anlarvae

perm

3

SD

Cohort1

Proportion

(%)

Cohort2

Proportion

(%)

Cohort3

Proportion

(%)

Cohort4

Proportion

(%)

Length

SD

(lm)

Length

SD

(lm)

Length

SD

(lm)

Length

SD

(lm)

12-0

2-2

010

3

55

57

181.8

20.4

73.9

130.6

14.5

26.1

12-1

6-2

010

1,6

30

349

343.3

28.4

54.6

203.1

16.3

41.4

131.1

12.0

3.9

12-2

9-2

010

1

45

57

339.4

36.4

28.2

208.4

20.5

63.8

116.7

19.0

8.1

01-2

7-2

011

2,1

35

634

283.2

18.4

50.6

177.6

15.0

49.4

03-0

3-2

011

17

6

184.2

17.0

100.0

03-3

1-2

011

21

3

308.8

36.2

43.6

218.4

20.0

34.5

145.6

18.4

21,9

Aquacult Int

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periods in which the A. ater larval density increased (August and from the middle of

October to the end of January), with S. algosus reaching maximum values that varied

between 1,630 and 2,135 larvae m-3 and between 272 and 4,531 larvae m-3 for Ch.

chorus (Table1). Only for the latter species was there no increase in the abundance at the

end of August, as occurred with A. aterand S. algosus.Cohort analysis applied to the larval size structure ofCh. chorusdiscriminated, as with

A. ater, between one and four cohorts at different stages of development in one sampling

period. The post-larval cohorts had average sizes ranging between 273.6 and 565.5 lm in

proportions of 15.2 and 89.1 %, while in initial stages, their median sizes ranged between

104.4 and 137.1 lm in proportions of 13.8 and 100 % (Table1). In S. algosus, it was

possible to discriminate between one and three cohorts in each sampling, integrated as with

the other species by different stages of development, of which the post-larvae showed

median sizes ranging between 272.6 and 361.3 lm in proportions of 11.7 and 54.6 %,

respectively (Table1).

Post-larval collection

Monthly settlements ofA. aterpost-larvae on collectors showed a variation between 6 and

5,667 specimens 9 600 cm2 collector-1 (Table 2). The most intense period of settlement

occurred between late August 2010 and late February 2011, with a peak in October and

November when settlements were 5,667 and 4,183 post-larvae 9 600 cm2 collector-1,

respectively. The fewest settlements of this period occurred during the months of Sep-

tember and February with 880 and 1,753 post-larvae 9 600 cm2 collector-1 (Table 2).

The cohort separation analysis of these post-larvae allowed discrimination between oneand two cohorts with median lengths that fluctuated from 374.6 to 1,242.3 lm; The latter

cohort was recorded in March 2011 and accounted for 6 % of the settlement that occurred

during that month (Table2).

Along with the settlement of A. ater that occurred in the collectors, there was also

settlement ofCh. chorusandS. algosuspost-larvae. The abundance of the three species was

significantly different (p\0.05), with the settlement of S. algosus being the less repre-

sented in the collectors compared toCh. chorus(p\0.05), whose abundance was similar to

that ofA. ater(p[ 0.05). The period of greatest settlement ofCh. choruscoincided with the

period of settlement for A. ater, reaching a maximum settlement between November and

December when 11,400 and 13,533 post-larvae 9 600 cm2 collector-1 were recorded,respectively (Table2). The monthly size structure analysis ofCh. chorus post-larvae dis-

criminated between one and three cohorts with median sizes that ranged between 403.6 lm

and 1,587 lm (Table2). For its part, S. algosus presented a shorter period of greater

settlement which was restricted between the months of December and February 2011,

reaching a peak in December with 3,843 post-larvae 9 600 cm2 collector-1. Monthly, only

one cohort of this species appeared attached to the collection units, whose sizes during the

study period varied between 312.9 and 387.5 lm (Table2).

Discussion

Reproductive cycle

Knowledge of the reproductive cycle of mollusks is a prerequisite to understand recruit-

ment phenomena and to maximize spat collection, which is the base for artificial

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Table2

Averagenu

mberofpost-larvae/600cm

2

ofcollectorandpost-

larvalcohortso

fA.ater,

Ch.chorus,

andS.algo

sussettledonartificialcollectors

Date

Meanpost-larvae

Cohort1

Proportion(%)

Cohort2

Proportio

n(%)

Cohort3

Proportion(%)

Immersionremoval

600cm

2

collector

Length

SD(lm)

Length

SD(lm)

Length

SD(lm)

A.ater

07/29

08/26/2010

6

4

475.3

85.3

100

08/26

10/01/2010

880

1,2

73

818.9

179.6

6

375.3

38.7

94

10/01

11/04/2010

5,6

67

2,4

08

740.7

113.5

74.8

374.6

64.0

25.2

11/04

12/02/2010

4,1

83

1,7

25

985.9

185.6

12.7

457.7

75.1

87.3

12/02

12/29/2010

2,1

41

1,2

43

455.7

107.6

100

12/29

01/27/2011

2,8

98

2,9

59

375.6

54.7

100

01/27

03/03/2011

1,7

53

1,4

34

498.1

141.9

100

03/03

03/31/2011

115

46

1,2

42.3

190.2

6

613.9

140.5

94

Ch.chorus

07/29

08/26/2010

3

2

307.2

160.0

100

08/26

10/01/2010

1,8

00

410

783.8

136.0

31.5

443.5

65.4

68.5

10/01

11/04/2010

2,3

27

1,3

45

1,4

23.6

142.7

25.9

997.1

108.2

57

685.9

94.3

17.1

11/04

12/02/2010

11,4

00

2,6

10

1,3

82.5

181.2

5

758.5

105.8

77.4

403.6

61.2

17.1

12/02

12/29/2010

13,5

33

12,4

82

862.3

174.7

28.1

536.4

113.5

71.9

12/29

01/27/2011

5,6

01

4,4

29

1,5

87.4

206.3

20,5

781.2

147.1

60.8

467.1

94.9

18.7

01/27

03/03/2011

4,1

92

3,4

81

424.6

125.0

100

03/03

03/31/2011

135

125

1,2

27.3

217,5

24.5

704.6

204.4

75.5

S.algosus

07/29

08/26/2010

2

3

387.5

62.7

100

08/26

10/01/2010

170

72

312.9

33.8

100

10/01

11/04/2010

187

243

318.8

75.0

100

11/04

12/02/2010

103

42

335.9

60.5

100

12/02

12/29/2010

3,4

83

1,1

41

326.4

64.7

100

12/29

01/27/2011

920

747

331.8

84.5

100

01/27

03/03/2011

1,7

07

1,5

60

324.4

64.9

100

03/03

03/31/2011

82

66

318.9

87.7

100

Aquacult Int

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cultivation of these organisms. To understand this process and evaluate the reproductive

condition of mollusks, numerous researchers have turned to the use of gonadosomatic

indexes, employing the change in meat weight as a good indicator to detect massive

spawnings (Winter et al. 1980). In mytilids, the decreases in the index values have been

principally related to spawning (Prieto et al. 1999), which has been statistically demon-strated in the case ofPerumitylus purpuratus, for which the largest values of the index used

represent the gametogenic mature state and lower values represent the stages of spawning

and post-spawning (Oyarzun et al.2010). In the present work, the use of the slope obtained

from the relationship between size and dry meat weight (Avendano and Cantillanez2013)

has resulted in a good indicator for the estimation ofA. aterspawning.

On the other hand, knowledge regarding the reproductive cycles of marine bivalves

shows that they differ according to species and populations within the same species, caused

by a group of endogenous as well as exogenous variables which do not permit the existence

of a specific reproductive pattern (Barber and Blake1991). Among the exogenous factors,

temperature and latitude have been associated with reproductive strategy of species,

indicating annual reproductive cycles in circumpolar zones, semiannual cycles in tem-

perate zones, and continuous reproduction in tropical zones (Kinne 1963; Lubet and Le

Gall 1967; Rand1973; Bayne1976; Oyarzun et al. 2010). In mytilids, the importance of

thermal stress in the regulation of reproduction had already been mentioned by Orton

(1920), while Lubet and Le Gall (1967) concluded that thermal stress varied by latitude,

which was corroborated by Calvo et al. (1998) in the case of A. ater.

The results obtained in the present study show thatA. aterpresented gamete evacuations

in the months of winter, spring, and summer, with the most intense occurring in August

November and DecemberFebruary, confirming the long spawning periods that inverte-brates at low latitudes have (Giese1959). Spawnings for this species occur during most of

the year, with significant periods in AugustSeptember and January, which have been

identified in the South Mejillones Bay (Henrquez and Olivares 1980). Intense periods

extending principally between the months of August and February have been reported for

populations in Peru (Gamarra and Cornejo 2002).

The influence of temperature on the reproductive cycle dynamic of this species was

clearly observed during the most important periods of gamete evacuations occurring in this

population ofA. ater, which were coincident with periods in which the water temperature

reached lower daily averages. Spawnings occurring in a critical range of temperature have

been reported for Lamellibranchia by Bayne (1976); however, the results differ from thosereported by Solis and Lozada (1971) for populations of A. ater from the south of the

country (42S), where spawnings occur when the water temperature reaches between 18

and 19 C.

Larval cycle

Although the periods in which A. aterspawnings occurred coincided with the periods in

which there were increases in larval abundance, it was not possible to establish a good

relationship between both processes. The larvae were present all year long in the studyarea, and the greatest abundances occurred before the beginning of the decreases of the

spawning index in this area. The lack of a direct relationship between spawnings and larval

abundance has been shown in various bivalve species, for example M. chilensis, Pecten

maximus (Paulet et al. 1997), Ruditapes phillippinarum (Calvez 2002) and Argopecten

purpuratus(Avendano et al.2008), whose high index values do not necessarily correspond,

after their decrease, to the greater quantities of larvae in these species in plankton and the

Aquacult Int

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weaker values do not necessarily correspond to the absence of reproduction. Thus, for

example inP. maximusfrom the Roadstead of Brest (France), it is possible to find larvae in

the winter, when the index is very low, which would lead one to think that fertilization and

larval development would be impossible (Paugan et al. 2003).

By contrast, the different larval cohorts present during this study, whose mean sizesshowed a predominant presence of post-larval cohorts (considering that A. ater meta-

morphoses to 260 lm (Ramorino and Campos 1983)), as well as significant cohorts of

initial stages in dates prior to those that registered a decrease in the spawning index, are

difficult to explain. The larval stage of mytilids normally lasts for 3 and 4 weeks, and can

be prolonged up to 10 weeks given their capacity to release and resettle themselves on

various occasions, as post-larvae passively dispersed by currents (Alfaro 2006). Conse-

quently, the different cohorts found in this study could come from a larval pool generated

from distinct reproductive populations that spawn non-simultaneously. Their transport

process could occur within a mesoscale distribution range. The consistent presence of A.

aterbanks on rocky substrata characteristic of the subtidal area of the Chilean coastal strip

could be a place for a potential connection between reproductive populations (Pineda et al.

2007). This would allow the hypothesis that the dynamic of these A. aterbanks could be

responding to a meta-population structure under the modern concept (Hanski and Sim-

berloff1997), wherein larval availability of a particular site will depend on the intercon-

nections that exist between different banks that make up the meta-population (Narvarte

et al.2001). Toro et al. (2006) show that for M. chilensislarvae in the south of Chile, their

dispersion capacity over large distances along the coast allows the process of transport and

settling to occur within a meta-population distribution range.

To strengthen the hypothesis, it is necessary to point out that along the Chilean coast,with the predominance of the sub-Antarctic current that flows toward the north, the north of

Chile is subjected to a predominance of southeastern winds which last the whole year

(Escribano et al. 2002; Avendano and Cantillanez 2008), which has been considered the

principal causative force of the circulation of surface waters (020 m) in the coastal ocean,

favoring the advection of larvae from the south, as has been shown for the gastropod

Concholepas Concholepas (Gonzalez et al.2005). Significant distributions ofP. maximus

larvae, in size and density in areas devoid of mature specimens, have been explained by

horizontal transport generated by tides and winds from other spawning sites (Boucher and

Dao1990).

These results also show that the larval cycle ofS. algosus andCh. chorus, the latter ofwhich has reestablished itself in the north of Chile in the last decade (Avendano and

Cantillanez 2011), was similar to that exhibited by A. ater, which demonstrates that in

northern Chile, the reproductive periods of these mytilid species coincide, similar to that

which occurs in populations ofM. chilensis, A. ater, and Ch. chorus in the south of the

country, where the larvae interact during the same time period (Avendano and Cantillanez

2011). The different larval cohorts recorded in both species in each sampling period

strengthen the hypothesis posited earlier for A. aterthat its origin could be generated from

different reproductive populations that make up a meta-population structure in this area of

the country. However, the simultaneous presence of larvae of these three species couldbecome an undesired element in the implementation of spat collection programs. This

creates the necessity of larval identification at the species level, so as to understand aspects

of their larval ecology (Shanks2001), principally the levels of distribution within the water

column, to assure the appropriate installation of collectors. Currently the identification of

mollusk larvae in plankton is one of the main difficulties because of the high cost and effort

that research of this type demands, and the benefits of which are seen over the long term.

Aquacult Int

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However, work done on species such as Placopecten magellanicus, P. maximus, and A.

purpuratus have allowed the understanding of aspects of the larval and settlement level

dynamic (Sinclair et al. 1985; Thouzeau et al. 1991; Cantillanez et al. 2007), creating

optimization of seed attachment like in the case ofA. purpuratus (Cantillanez et al.2007).

Post-larval settlement

The results obtained from the collectors after 1 month of immersion indicate that the most

significant settlements of A. ater post-larvae coincide with the periods with the most

reproductive activity occurring between August and November and December and Feb-

ruary. Also, these results allow the observation of a certain relationship between the larvae

present at installation of the collectors and the settlements obtained 1 month later on them,

as happened during the months of October and November. This relationship becomes more

direct and proportional with the presence at the moment of installation of the collector,

from a larger number of competent larvae and post-larvae in the plankton as was observed

in the months from October to January. A relationship between the presence of competent

larvae and the eventual number of seeds settled on collectors has been demonstrated for the

pectinids A. purpuratus (Cantillanez et al. 2007) and Patinopecten yessoensis (Ventilla

1982). For them, the median size of the settled post-larvae cohorts also has a relationship

with the sizes of the larval cohorts present during the period when the collectors are in the

water; however, the cohort 1 recorded in March 2011 with a mean size of 1,242 lm, which

represented only 6% of the settlement, could be influenced by the transfer of post-larvae

that occurred from the mother line toward the collector, considering their capacity to loose

themselves and resettle, and the existence of attachments that are present on the line duringthe study period.

Similar results were seen with post-larval settlements ofCh. chorus, showing that they

more than doubled the number of settlements recorded for A. ater, reaching maximum

values during November and December, 1 month later than that of A. ater. The median

sizes of the post-larval cohorts of Ch. chorus in the collectors during most of the study

were greater than those of A. aterthe same as the number of attached cohorts. These

results, along with showing the greater effectiveness ofCh. chorussettlement, demonstrate

that this species experiences greater growth than A. ater does. Greater growth ofChor-

omytilus meridionales than A. aterhas been demonstrated for populations in South Africa

by Barkai and Branch (1989).In contrast to the above, S. algosus had fewer post-larvae settled on the collectors, with

a restricted period of settlement between the months of December and February. Their

settlements were also limited to a sole monthly cohort, whose median size varied from 313

to 387 lm, which then leads to the supposition that not all larval groups present during the

period in which the collector was immersed in water attached, considering that its set-

tlements is produced at 230 lm (Ramorino and Campos 1983). The non-existence of a

systematic relationship between cohort larval abundance with the performance of seed

capture has been described by Boucher (1985) for P. maximus. According to this author,

the absence of attachments of many larval cohorts implies the existence of strong mor-tality, independent of larval density. However, keeping in mind the results for Ch. chorus

andA. aterin the present study, it is necessary to consider that S. algosusis a species that is

distributed in the intertidal area, such that the position of collectors far from the coast and

in a 16 m column of water could affect the settlement of all the larval cohorts.

In conclusion, the continual presence over the course of the year of different larval

cohorts of A. aterand Ch. chorus and the continual settlement on collectors in the study

Aquacult Int

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zone, indicate a potential area for the implementation of massive spat supply programs

with the purpose of developing mussel farming in northern Chile, as well as launching

studies on the larval and post-larval dynamic, therefore generating information about the

growth and survival of these stages.

Acknowledgments The present study was developed under the framework of the project INNOVA Cod.07CT91DM-56.

References

Alfaro AC (2006) Population dynamics of the green-lipped mussel,Perna canaliculus, at various spatial and

temporal scales in northern New Zealand. J Exp Mar Biol Ecol 334:294315

Avendano M (1984) Tecnica para captacion de semillas deAulacomya ater(Molina, 1782) en la Baha de

Mejillones Chile. Rev Latinam Acuicult 21:1822

Avendano M, Cantillanez M (2008) Aspectos biologicos y poblacionales de Argopecten purpuratus (La-marck, 1819) en la Reserva Marina la Rinconada: contribucion para su manejo. In: Lovatelli A, Faras

A, Uriarte I (eds) Taller regional de la FAO sobre el estado actual del cultivo y manejo de moluscos

bivalvos y su Proyeccion Futura: Factores que Afectan su Sustentabilidad en America Latina. Actas de

Pesca de la FAO, 12 Roma, pp 249266

Avendano M, Cantillanez M (2011) Reestablecimiento de Choromytilus chorus (Bivalvia: Mytilidae

(Molina 1782)) en el Norte Grande de Chile. Lat Am J Aquat Res 39(2):390396

Avendano M, Cantillanez M (2013) Reproductive cycle, collection and early growth ofAulacomya ater

(Bivalvia:Mytilidae (Molina 1782)) in northern Chile. Aquac Res 44(9):13271338

Avendano M, Cantillanez M, Pena JB (2006) Effect of immersion time of cultch on spatfall of the scallop

Argopecten purpuratus (Lamarck 1819) in the Marine Reserve at La Rinconada, Antofagasta, Chile.

Aquac Int 14:267283

Avendano M, Cantillanez M, Thouzeau G et al (2007) Artificial collection and early growth of spat of thescallopArgopecten purpuratus(Lamarck, 1819), in La Rinconada Marine Reserve, Antofagasta, Chile.

Sci Mar 71:1972005

Avendano M, Cantillanez M, Le Pennec M et al (2008) Reproductive and larval cycle of the scallop

Argopecten purpuratus (Ostreoida: Pectinidae), during El Nino-La Nina events and normal condition

in Antofagasta, Northern Chile. Rev Biol Trop 56:121132

Avendano M, Cantillanez M, Le Pennec M et al (2011) Distribucion temporal de larvas deMytilus chilensis

(Mollusca: Mytilidae (Hupe, 1854)), en el mar interior de la X Region, Sur de Chile. Lat Am J Aquat

Res 39(3):416426

Barber B, Blake N (1991) Reproductive physiology. In: Shumway SE (ed) Scallops: biology, ecology and

aquaculture. Developments in aquaculture and fisheries science, vol 21. Elsevier, New York,

pp 377428

Barkai A, Branch GM (1989) Growth and mortality of the mussels Choromytilus meridionalis (Krauss) and

Aulacomya ater(Molina) as indicators of biotic conditions. J Molluscan Stud 55:329342

Bayne BL (1976) The biology of mussel larvae. In: Bayne BL (ed) Marine mussels: their ecology and

physiology. Cambridge University Press, London, New York, pp 81120

Boucher J (1985) Caracteristiques dynamiques du cycle vital de la coquille Saint-Jacques ( Pecten maximus):

hypotheses sur les stades critiques pour le recrutement. Cons Int Explor Mer, C.M. 1985/K23/Sess.Q.

10 pp

Boucher J, Dao JC (1990) Repeuplement et forcage du recrutement de la coquille Saint-Jaques (Pecten

maximus). In: Troadec JP (ed) Lhomme et les ressource halieutiques. SDP. IFREMER, France,

pp 313357

Calvez I (2002) Approche de la variabilitespatiale des stades larvaires et post-larvaires dune population de

palourdes japonaises, Ruditapes philippinarum. Ph. D. Thesis, Univ. Bretagne Occidentale, Brest

Calvo J, Morriconi E, Orler PM (1998) Estrategias reproductivas de moluscos bivalvos y Equinoideos. En:

Boschi EE (ed) El Mar Argentino y sus recursos pesqueros. Tomo 2. Los moluscos de interes pesquero.

Cultivo y estrategias reproductivas en bivalvos y equinoideos. Publicaciones Especiales. INIDEP, Mar

del Plata, pp 195231

Cantillanez M, Thouzeau G, Avendano M (2007) Improving Argopecten purpuratus culture in northern

Chile: results from the study of larval and post-larval stages in relation to environmental forcing.

Aquaculture 272:423443

Aquacult Int

1 3


16/16

Escribano R, Rodrguez L, Irribaren C (1995) Temporal variability of sea temperature in Bay of Anto-

fagasta, northern Chile (19911995). Estud Oceanol 14:3947

Escribano R, Marn VH, Hidalgo P et al (2002) Physical-biological interactions in the pelagic ecosystem of

the nearshore zone of the northern Humbold Current System. In: Castilla JC, Largier JL (eds) The

oceanography and ecology of the nearshore and bays in Chile. Ediciones Universidad Catolica de

Chile, Santiago, pp 145175Gamarra A, Cornejo O (2002) Study of the musselAulacomya ater, Molina, 1782 (Bivalvia:Mytilidae), near

Santa Rosa Island, Independence bay, Peru, during the El Nino phenomenon 199798. Inv Mar

Valparaso 30 Suppl. Symposium, pp 140

Giese AA (1959) Comparative physiology: annual reproductive cycle of marine invertebrates. Annu Rev

Physiol 21:547576

Gonzalez J, Tapia C, Wilson A, et al (2005) Bases biologicas para la evaluacion y manejo de metapob-

laciones de loco en la III y IV Regiones. Informe Final FIP 200216, Chile

Hanski I, Simberloff D (1997) The metapopulation approach, its history, conceptual domain and application to

conservation. In: Hanski I, Gilpin ME (eds) Metapopulation biology. Academic Press, London, pp 526

Henrquez R, Olivares A (1980) Ciclo estacional de la Cholga Aulacomya ater(Molina 1782) en la Baha de

Mejillones. Arch Biol Med Exp 13:74

Hjort J (1914) Fluctuations in the great fisheries of Northern Europe. Rapp Cons Exp Mer 20:1228Kinne O (1963) The effects of temperature and salinity on marine and brackish water animals: 1. Tem-

perature. Oceanogr Mar Biol Annu Rev 1(1):301340

Le Pennec M (1978) Genese de la coquille larvaire et post larvaire chez divers bivalves marins. These

dEtat, Universite de Bretagne Occidentale, Brest

Lubet P, Le Gall P (1967) Observations sur le cycle sexuel de Mytilus edulis L. a Luc-sur-Mer. Bull Soc

Linn Normandie Ser 10(8):303307

MacDonald PDM, Pitcher TJ (1979) Age-groups from size-frequency data: a versatile and efficient method

of analyzing distribution mixtures. J Fish Res Board Can 36:9871001

Narvarte M, Felix-Pico E, Ysla-Chee L (2001) Asentamiento larvario de pectnidos, en colectores artifi-

ciales. In: Maeda-Martnez AN (ed) Los Moluscos Pectnidos de Iberoamerica: Ciencia y Acuicultura.

Editorial Limusa, Mexico, pp 173192

Orton JH (1920) Sea-temperature, breeding and distribution of marine animals. J Mar Biol Assoc UK12:299366

Oyarzun P, Toro J, Jaramillo R et al (2010) Analisis comparativo del ciclo gametogenico de Perumytilus

purpuratus(Bivalvia: Mytilidae), en las localidades de Taltal y Huasco, norte de Chile. Rev Biol Mar

Oceanogr 45(1):4358

Paugan A, Le Pennec M, Marhic A et al (2003) Immunological in situ determination of Pecten maximus

larvae and their temporal distribution. J Mar Biol Assoc UK 83:10831093

Paulet YM, Bekhadra F, Devauchelle N et al (1997) Cycles saisonniers, reproduction et qualitedes ovocytes

chez Pecten maximus en rade de Brests. Ann Inst Oceanogr 73(1):101112

Pineda J, Hare JA, Sponaugle S (2007) Larval dispersal and transport in the coastal ocean and consequences

for population connectivity. Oceanography 20:2239

Prieto AS, Flores M, Lodeiros C (1999) Sexual maturity and condition index in a population of mussel

Modiolus squamosus (mollusca, bivalvia) in Tocuchare, Gulf of Cariaco, Venezuela. Ecotropicos12:8390

Ramorino L, Campos B (1983) Larvas y postlarvas de Mytilidae de Chile. Rev Biol Mar 19(2):143192

Rand WM (1973) A stochastic model of the temporal aspect of breeding strategies. J Theor Biol 40:337351

Sernapesca (2011) Anuarios Estadsticos de Pesca. Servicio Nacional de Pesca, Chile

Shanks A (2001) An Identification Guide to the Larval Marine Invertebrates of the Pacific Northwest.

Oregon State University Press, Corvallis, p 314

Sinclair M, Mohn RK, Robert RK et al (1985) Considerations for the effective management of Atlantic

scallops. Can Tech Rep Fish Aquat Sci 1382:1113

Solis IF, Lozada E (1971) Algunos aspectos biologicos de la Cholga en Magallanes. Biol Pesq 6:9144

Thouzeau G, Robert G, Smith S (1991) Spatial variability in distribution and growth of juvenile and adult

sea scallops Placopecten magellanicus (Gmelin) in eastern Georges Bank. Mar Ecol Prog Ser

74:205218Toro J, Castro G, Ojeda J et al (2006) Allozymic variation and differentiation in Chilean blue mussel,

Mytilus chilensis, along in natural distribution. Genet Mol Biol 29:174179

Ventilla RF (1982) The scallop industry in Japan. Adv Mar Biol 20:310380

Winter J, Navarro J, Roman C et al (1980) Estudios biologicos en tres Mitiliculturas de Chiloe(Tubildad,

Huildad y Yaldad). Analisis experimental de la alimentacion de Mytilus chilensis. Informe final.

Convenio UACH-CORFO, X Region, Chile

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