reproduccion aulacomya
TRANSCRIPT
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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
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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
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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
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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.
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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
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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.
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