ditions scientiques et mdicales Elsevier SAS. All rights reserved.

Acta Oecologica 20 (4) (1999) 267283 / 1999 E

Ecology of the polychaete Nereis diversicolor in the Canal de Mira (Ria de Aveiro, Portugal): Population dynamics, production and oogenic cycle
Antnio Abrantes, Ftima Pinto, Maria Helena Moreira *
Departamento de Biologia - Universidade de Aveiro, Campus de Santiago, 3810 Aveiro, Portugal. * Corresponding author (fax: +351 34 426408; e-mail: hmoreira@bio.ua.pt)

Received February 26, 1998; revised December 30, 1998; accepted February 26, 1999

Abstract The population of Nereis diversicolor O.F. Mller was studied in 1993 and 1994 at three intertidal areas along the estuarine gradient in the Canal de Mira (Ria de Aveiro). The population dynamics, secondary production and growth were followed for the 2-year period, whereas in the second year, a study on the oogenic cycle was also carried out. For the population dynamics and production studies, core samples were collected monthly at each site, and for the study of the oogenic cycle, medium size and large individuals were sampled from the sediment. Mean annual densities were higher (573718 indm2) at a station located in the middle zone of the channel, followed by the outer (190275 indm2) and the innermost (4394 indm2) stations. A cohort analysis by Bhatta software enabled the separation of the cohorts present at each date, and two cohorts were followed from recruitment to extinction. The secondary production ranged from 15.9 to 74.2 g ash free dry ratio from 4.4 to 7.9. The average body growth rate varied between 0.16 and 0.20 mmd1 for worms longer than weightm2year1 and the P/B 2 cm. Two recruitment seasons were detected each year. Two spawning periods were also observed, one in the spring and the other in early autumn. 1999 ditions scientiques et mdicales Elsevier SAS Nereis diversicolor / population dynamics / production / oogenesis / benthos / estuaries

1. INTRODUCTION

2. MATERIALS AND METHODS 2.1. Study area The Ria de Aveiro (NW Portugal) is a shallow lagoon with a surface area of about 45 km2, formed by several branches and an intricate system of bays and narrow channels. The lagoon communicates with the Atlantic through an articial inlet [16, 42]. The deeper areas near the inlet are characterised by strong marine inuence (tidal inow of 25 to 90 million m3), with high values of current velocity and tidal range (23 m at spring tides), while in remote shallow areas, the circulation and the sea water inow are reduced. The tidal wave is considerably distorted as it progresses inside the lagoon, so that with increasing distance from the inlet the duration of ood becomes shorter than that of the ebb. The two main channels extend from the inlet northwards (Canal de Ovar) and southwards (Canal de Mira) and are separated from the Atlantic by a narrow sand bar (gure 1). The Canal de Mira, which is second in terms of average width, receives a continuous freshwater supply through a small system of lagoons and streams. Three main sections can be recognised: (i) a lower section with salinities ranging

The polychaete Nereis diversicolor is a common inhabitant of intertidal mudats of estuaries and shallow water bodies with a wide geographical distribution [10, 12, 34]. In the NE Atlantic, the species occurs from northern Europe to Morocco [22]. Several studies on the life history of this worm have shown important variations in different places, in response to environmental gradients and local conditions, and some features of its biology and ecology still remain obscure. Although some knowledge already exists regarding meridional populations, most studies have been concentrated in northern Europe. This paper deals with some aspects of the life history of N. diversicolor along an estuarine gradient in a European warm-temperate shallow water body, including the population dynamics, secondary production, growth and oogenic cycle.

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material retained in each sieve was sorted separately in a white tray, using a magnifying glass for the fraction corresponding to the ner mesh. All complete worms obtained in 1993 were used for biometrical measurements. The total body length was measured to the nearest mm and the total jaw length, as dened by Olive and Garwood [44], was determined under a dissecting microscope using a calibrated eye piece graticule. The individuals were dried to constant weight (72 h at 65 C) and weighed after cooling in a dessicator to 0.1 mg. The ash content was estimated as loss of weight on ignition (4 h at 550 C). The ash free dry weight was given by the difference between the dry weight and the ash content of each specimen. All other worms contained in the samples were preserved in 70 % ethanol until further processing. In order to measure the jaw length, these specimens were rst maintained in freshwater for a few days, since it was found that this procedure facilitates the dissection of the jaws from the surrounding tissues in preserved animals. For the study of the reproductive cycle, qualitative samples were obtained during the second year. Medium size and large animals were collected monthly from the sediment at stations 1 and 2. These animals were placed in bottles containing local water, to which menthol crystals were added. In the laboratory, the specimens were xed with formalin and observed in order to determine the presence of sexual products in the ceolom. Whenever possible ten oocyte-bearing females from stations 1 and 2 were dissected each month. The worms were opened from the anterior to the posterior end inside a Petri dish under a dissecting microscope, and the ceolomic content was gradually extracted with a Pasteur pipette and transferred to a 550-L Sedgewick-Rafter counting chamber. The specimens were carefully rinsed with distilled water, and this water was recovered to ensure that no oocytes were lost. The number of oocytes in each female was counted under a binocular microscope and whenever possible fty oocytes were measured using a calibrated eye piece graticule. The longest and the shortest length of each oocyte was determined, and the average value was used as an estimate of oocyte size. Males were recognised by the presence of sperm aggregates, and those animals without sexual products were considered to have undetermined sex. The jaws of all specimens were removed and measured using the same procedure as indicated above. At each sampling occasion, several environmental parameters were measured. Sediment temperature was registered with a thermometer at the sediment subsurface (2.5 cm depth). Salinity of the water retained in tidal pools was measured with a refractometer. Sediment samples were collected using small PVC corers (4 cm diameter) to a depth of 30 cm and frozen until analysis. The organic matter content of the sediments
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Figure 1. Ria de Aveiro and Canal de Mira, Portugal, showing the location of the three sampling stations (#1, #2 and #3).

between tides from values higher than 18 to 3035 for most of the year; (ii) a middle section with a highly variable regime; (iii) an upper section with salinities not higher than 0.1 all year round [40]. The three selected sampling stations (#1, #2 and #3) are located in intertidal areas at the Canal de Mira, within the salinity sections (i) and (ii), and apart from each other along the estuarine gradient (gure 1). 2.2. Sampling and laboratory procedures The sampling programme was carried out at the three stations on a monthly basis during 2 years, from January 1993 to December 1994. For the population dynamics and production studies, ten core samples (corresponding to a total area of 0.1 m2) were randomly collected at each station, during both years, to a depth of about 30 cm and sieved in the eld using a 0.5-mm mesh. Menthol crystals were added to the collected material to cause relaxation of the animals. On arrival to the laboratory, the samples were xed with 10 % buffered formalin stained with Rose Bengal and within a few days, they were washed under running water over a set of three sieves with 2 000, 1 000 and 500-m mesh size. The

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i=m j=n i=1 j=1

was determined every month by loss of weight on ignition (4 h at 550 C) after drying to constant weight (72 h at 65 C) a homogenised portion of about 100 g. In 1993, the sediment homogenates were taken from the whole core sample and in 1994, two separate layers were considered (surface layer up to 2 cm and deeper layer below 2 cm). For the grain size analysis, sediment samples were homogenised and a portion of about 200 g was dried to constant weight (72 h at 65 C). A set of seven sieves with mesh sizes corresponding to integer values of the Wentworth scale [41] in the range 2 to 4 U (4 000 to 63 m) was used. Mechanical agitation was provided for 50 min using a Retsch Sieve Shaker and the frequency of each grade was expressed as a percentage of total weight. Sediments were classied into different types according to the criteria adopted by Larsonneur [32]. 2.3. Data treatment The analysis of the Gaussian components in the jaw size frequency histograms was based on Bhattacharyas method of logarithmic differences [7] using the Bhatta software developed by Lepetit et al. [33]. Each Gaussian component was interpreted as representing a different cohort as described by Gillet [23] in a study on the population dynamics and production of N. diversicolor in the Loire estuary, France. The biomass was estimated using the regression equations of log10 ash free dry weight on log10 jaw length determined separately for stations 1 and 2. To enable comparisons between this study and others using body length, the relationship between body length and jaw length was also determined. The following regressions related total jaw length (JL) to ash free dry weight (AFDW) and to body length (BL) at station 1: log10AFDW (g) = 2.213 log10JL (mm) 2.088 (n = 44; r = 0.94; P < 0.001) BL (cm) = 3.932 JL (mm) 1.776 (N = 44; r = 0.61; P < 0.001) The equations for station 2 were: log10AFDW (g) = 2.782 log10JL (mm) 2.284 (n = 60; r = 0.94; P < 0.001) BL (cm) = 4.132 JL (mm) 1.915 (n = 60; r = 0.94; P < 0.001) The annual production (P) was calculated as the sum for all cohorts of the product of the mean density ) of each cohort at times t and t+1 and the (N corresponding individual mean weight increments (DW ) between successive samplings, as described by Crisp [14]:
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P=

i, j

DW i, j

where m is the number of cohorts in the population and n the number of time intervals from the starting time (tk = 1) to 1 year later (tk = n). Weight losses (negative increments) were not subtracted, since production is dened as the addition of somatic and gonadal tissue to the population regardless of whether or not it accumulates and survives to the end of the period under consideration [3]. ), calculated as the The mean annual biomass (B average sum of the monthly mean biomass for all ratios. sampling dates, was used to determine the P/B 3. RESULTS 3.1. Environmental conditions The temperature at the sediments subsurface (gure 2) ranged from 9.1 to 27.8 C. There was a clear temperature increase from station 1 to station 3 in the summer and a reverse trend during a short period in the winter. Salinity varied largely between stations and with seasons, but the seasonal variation was much more pronounced at station 2 (gure 3). The highest salinity values (PSU) were recorded at station 1 in March 1993 (33.9) and October 1994 (32.0), whereas at the same station, low values were observed in March 1994 (20.0) and October 1993 (21.4). These observations, together with the abnormally low values for the season, registered at all stations in May 1994, show the inuence of rainfall on the salinity in the channel. At station 2, salinity ranged from 4.8 to 30.0, and at station 3 from 0.0 to 7.0. Sediment type (gure 4) was muddy sand at stations 1 and 2 and medium sand at station 3. The mean

Figure 2. Subsurface (2.5 cm) sediment temperature at the three sampling stations from January 1993 to December 1994.

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Figure 3. Salinity values at the three sampling stations from January 1993 to December 1994.

organic matter content for the whole samples in 1993 was 2.3 (SD = 1.02), 2.3 (SD = 0.59) and 1.8 % (SD = 0.92) at stations 1, 2 and 3, respectively. In 1994, the mean organic matter content was 2.4 (SD = 0.99) and 2.1 % (SD = 0.98) at station 1, 2.3 (SD = 0.54) and 2.1 % (SD = 0.56) at station 2, and 2.0 (SD = 0.90) and 1.5 % (SD = 0.87) at station 3, at the subsurface and the deeper layers, respectively. 3.2. Population structure and growth The abundance of N. diversicolor varied considerably during the study period and between stations (gure 5). On the whole, the densities followed similar patterns in both years, though the general abundance was slightly higher in the rst year. The mean annual densities were higher at station 2 (718 indm2, SD = 294.8 in 1993; 573 indm2, SD = 130.4 in 1994), followed by station 1 (190 indm2, SD = 70 in 1993; 275 indm2, SD = 101.9 in 1994) and station 3 (43 indm2, SD = 17.4 in 1993; 94 indm2, SD = 47.2 in 1994). In both years, densities increased from late winter throughout spring, were fairly stable in summer, especially in 1993, and declined drastically in the autumn. In 1993, a clear response to an increase in the subsurface sediment temperature above 13 C was observed, while in 1994, the relationship between the increase in density and the sediment temperature was rather obscure. A substantial reduction in the densities observed in May 1994 coincided with a decrease in salinity (gure 3). Figures 6 and 7 show the evolution of the population structure at station 1 for the 2-year period. A total of 559 individuals were collected with jaw lengths in the range 0.423.27 mm. When the study began in January 1993, the population was formed by two cohorts, C1 and C2, where C1 corresponds to the older individuals. Cohort C1 was registered for the last time

Figure 4. Cumulative curves of grain size frequency of the sediments collected at the three sampling stations with time intervals of 6 months.

in April and cohort C2 in August. Two newly recruited cohorts were detected in 1993, in February (C3) and April (C4), and were followed until March and July 1994, respectively. In the second year, three newly recruited cohorts were detected, the rst (C5) and the second (C6) in the same months as C3 and C4 in the previous year and a third one (C7) in September. For the ve cohorts that were recruited within the study period, the mean jaw length at recruitment varied between 0.80 and 1.12 mm (mean body length: 1.42.6 cm). With regard to the four cohorts that
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Figure 7. Growth curves of cohorts (C) of Nereis diversicolor from January 1993 to December 1994 at station 1. Vertical bars are standard deviation. Figure 5. Population density (indm2) of Nereis diversicolor at each sampling station from January 1993 to December 1994.

Figure 6. Histograms of total jaw length of Nereis diversicolor from January 1993 to December 1994 at station 1, showing the cohorts (C) obtained using the Bhatta software. Vol. 20 (4) 1999

became extinct during the same period, the mean jaw length before extinction ranged from 2.79 to 3.15 mm (mean body length: 9.210.6 cm). The two cohorts that were followed from recruitment to extinction grew from 1.06 to 2.80 mm mean jaw length in 13 months (C3) and from 0.80 to 3.15 mm in 15 months (C4), which gives increases in mean body length from 2.4 to 9.2 cm (C3) and from 1.4 to 10.6 cm (C4). Accordingly, the average annual increment in body length was 6.3 cm for cohort C3 and 7.4 cm for cohort C4. At station 2, a total of 1 548 individuals were collected with jaw length ranging from 0.54 to 3.29 mm. Figures 8 and 9 indicate that the evolution of the population structure was, in general, similar to that observed at station 1. From the two cohorts detected in January 1994, one (C1) was registered for the last time in April and the other (C2) in August. Two newly recruited cohorts were detected in1993, in March (C3) and May (C4), and these cohorts were followed until April and August 1994, respectively. In 1994, two newly recruited cohorts were detected, C5 in March and C6 in May. For the four cohorts recruited within the study period, the mean jaw length at recruitment varied between 0.99 and 1.19 mm (mean body length: 2.23.0 cm). Before extinction, the mean jaw length varied between 2.63 and 2.75 mm (mean body length: 9.09.4 cm). The two cohorts that were followed from recruitment to extinction grew from 1.19 to 2.72 mm mean jaw length in 13 months (C3) and from 0.99 to 2.63 mm in 15 months (C4), corresponding to increases in mean body length from 3.0 to 9.3 cm (C3) and from 2.2 to 9.0 cm (C4). The growth rate for cohort C4 was not estimated due to the continuous recruitment of small individuals into this cohort during several months (gures 8, 9). The results for cohort C3 give an average annual increment in body length of 5.8 cm. At station 3, the abundance of N. diversicolor was very low and, therefore, it was not possible to analyse

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Figure 8. Histograms of total jaw length of Nereis diversicolor from January 1993 to December 1994 at station 2, showing the cohorts (C) obtained using the Bhatta software.

Figure 10. Histograms of total jaw length of Nereis diversicolor from January 1993 to December 1994 at station 3.

the Gaussian components of the population structure. At this station, a total of 163 individuals were collected with jaw length in the range 0.443.39 mm. Figure 10 shows that small specimens were very scarce, so that the population was mainly composed of medium and large size individuals. 3.3. Secondary production The computation of the secondary production using Crisps method is illustrated in table I for station 2 (1993). At station 1, the production was 15.9 in 1993 and 26.8 g AFDWm2year1 in 1994, and at station 2, 58.0 and 74.2 g AFDWm2year1 for 1993 and 1994, respectively. The mean annual biomass at station 1 ratios of 4.4 was 3.6 and 5.2 g AFDWm2, giving P/B and 5.2 in 1993 and 1994, respectively. At station 2, the mean annual biomass was 10.2 and 9.4 g ratios of 5.7 and 7.9 in the rst AFDWm2, giving P/B and second year of this study.
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Figure 9. Growth curves of cohorts (C) of Nereis diversicolor from January 1993 to December 1994 at station 2. Vertical bars are standard deviation.

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Table I. Production of cohorts C1, C2, C3 and C4 of Nereis diversicolor estimated by the method of Crisp [14] at station 2 in 1993. All weight values are ash free dry weight. Cohort Sampling date (month) Jan Feb Mar Apr Jan Feb Mar Apr May Jun Jul Aug Mar Apr May Jun Jul Aug Sep Oct Nov Dec May Jun Jul Aug Sep Oct Nov Dec Density N (m2) 170 190 150 70 240 200 510 380 470 560 460 320 290 380 510 350 470 440 260 170 250 170 170 170 180 340 370 260 150 220 Mean weight per individual W (g) 0.0594 0.0615 0.0711 0.0833 0.0152 0.0217 0.0206 0.0461 0.0594 0.0528 0.0644 0.0868 0.0084 0.0155 0.0228 0.0271 0.0320 0.0310 0.0594 0.0561 0.0449 0.0389 0.0051 0.0075 0.0084 0.0113 0.0120 0.0120 0.0088 0.0120 Weight increment DW (g) 0.0021 0.0096 0.0122 Mean density during period t N (m2) 180 170 110 Production increment N DW (gm2) 0.3763 1.6322 1.3432 3.35 C2 0.0065 0.0011 0.0255 0.0134 0.0066 0.0116 0.0224 220 355 445 425 515 510 390 1.4246 0 11.3333 5.6815 0 5.9096 8.7437 33.09 C3 0.0070 0.0073 0.0043 0.0048 0.0009 0.0284 0.0034 0.0111 0.0061 335 445 430 410 455 350 215 210 210 2.3603 3.2426 1.8664 1.9831 0 9.9434 0 0 0 19.40 C4 0.0024 0.0010 0.0028 0.0007 0.0000 0.0031 0.0031 170 175 260 355 315 205 185 0.4135 0.1663 0.7340 0.2581 0.0000 0 0.5826 2.15 Total 57.99 Annual production P (gm2)

C1

3.4. Oogenic cycle The number of oocytes per female varied between 40 and 15 242 and, in general, there was a signicant positive correlation between the number of oocytes in the coelomic cavity and the jaw length (table II). Figures 11 and 12 show the mean and total range of oocyte diameter for individual females examined
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throughout the study period at stations 1 and 2, respectively. The data are presented in a graph format similar to that used by Olive and Garwood [44] and Mettam et al. [37]. While for part of the year, there was a continuous gradation from small to large oocytes, on some occasions two well-dened groups of females could be identied, one bearing small oocytes and the

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Table II. Correlation coefficient between number of oocytes per female and jaw size at stations 1 and 2 during 1994. Month n Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec 4 10 10 10 5 9 10 9 10 5 3 5 Station 1 r 0.982 0.904 0.868 0.910 0.635 0.975 0.393 0.951 0.804 0.579 0.945 0.854 P 0.05 > P > 0.01 P < 0.01 P < 0.01 P < 0.01 P > 0.05 0.05 > P > 0.01 P > 0.05 P < 0.01 P < 0.01 P > 0.05 P > 0.05 P > 0.05 n 8 10 10 10 10 10 10 10 10 7 4 8 Station 2 r 0.199 0.498 0.855 0.952 0.881 0.935 0.751 0.867 0.918 0.592 0.855 0.847

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P P > 0.05 P > 0.05 P < 0.01 P < 0.01 P < 0.01 P < 0.01 P < 0.01 P < 0.01 P < 0.01 P > 0.05 P > 0.05 P < 0.01

other bearing large oocytes. At station 1, two distinct groups were patent in March, one of which had mean oocyte size in the range 161226 m. Later, in the period from June to September, two groups of females were also present. The group with large oocytes reached a mean oocyte diameter between 185 and 236 m in September. Females with large oocytes did not occur in April, while from the second group, only one (out of ve) was collected in October and none in November. At this station, it is also worthy to notice that the distribution of the oocyte diameter in December was very similar to that observed in January of the same year, with one out of four to ve females bearing oocytes with mean diameter over 200 m. At station 2, two females with large oocytes (mean size 204 and 217 m) were registered in April and, later, a larger group in September (mean oocyte size in the range 185238 m), while in the subsequent months, females with large oocytes were absent or rare. Thus, in May, only a group with a mean oocyte diameter in the range 65132 m was present, with only one female bearing some large oocytes (over 200 m), and the same happened in June. In July, a new group of females with small oocytes (less than 60 m) started to emerge. With regard to the second period, only two females with large oocytes were found in October and none in November. Females with small oocytes (less than 75 m) started to occur in December. The size frequency histograms in gures 13 and 14 show the evolution of oocyte size throughout the year. At station 1, both the presence of large oocytes between January and March, when a peak was very conspicuous, and the complete absence of large oocytes in April indicate that a spawning occurred prior to 26 April. A second maturation and spawning period

in summer and early autumn is suggested by the presence of a group of oocytes with increasing size from June to September. From this group, some large oocytes were still present in October but none in November. A similar pattern, indicating two spawning periods, was observed at station 2, where the major differences in relation to station 1 were the following: (i) the rst spawning period was extended until April; (ii) the group of large oocytes corresponding to the second maturation period did not occur before July. The total number of specimens observed for sex determination was 144 at station 1 and 171 at station 2. While oocyte bearing females were always present in the samples, on some occasions, males were not found. From the total number observed at station 1, 90 were females, 17 males and 37 of undetermined sex. The corresponding gures for station 2 were 107, 34 and 30. These gures indicate a sex ratio (male:female) of 1:5.3 at station 1 and 1:3.1 at station 2. 4. DISCUSSION 4.1. Environmental impact The population of Nereis diversicolor in the Canal de Mira exhibited important seasonal uctuations in abundance with high densities in spring and summer and low numbers in winter, as reported for the Ythan estuary, Scotland [11]. Similar uctuations but with peaks delayed until summer or early autumn were observed in the Thames estuary, England [18], the Dievengat, Belgium [29], the Norsminde Fjord, Denmark [31] and the Stiffkey saltmarshes, England [43]. In the Loire estuary, France, Gillet [23] found high densities in May and December and low numbers in
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Figure 11. Mean and total range of oocyte diameter in individual Nereis diversicolor from station 1, ranked by mean diameter, from January to December 1994. ([) Mean size; () smallest oocytes; (N) largest oocytes. Vol. 20 (4) 1999

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Figure 12. Mean and total range of oocyte diameter in individual Nereis diversicolor from station 2, ranked by mean diameter, from January to December 1994. ([) Mean size; () smallest oocytes; (N) largest oocytes.

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Figure 13. Oocyte diameter of Nereis diversicolor for all females collected at the same date at station 1, from January to December 1994. Vol. 20 (4) 1999

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Figure 14. Oocyte diameter of Nereis diversicolor for all females collected at the same date at station 2, from January to December 1994. Acta Oecologica

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Table III. Density, biomass and production of Nereis diversicolor in relation to geographical distribution. When a single value is given, it corresponds to the mean density or biomass. Site Gteborg, Sweden Ythan estuary, Scotland Norsminde Fjord, Denmark Stiffky saltmarshes, England Fenn Creek, England Dievengat, Belgium Loire estuary, France Ria de Aveiro, Portugal++ Ria Formosa, Portugal Bay of Cdiz, Spain Bou Regreg estuary, Morocco
+

Density (indm2) 80060 000+ 208961 1 305 392 4591 296 5 00017 000+ 8003 200 190718 6532 626 585620
++

Biomass (gm2) 0.31.4** 4.2* 10.5** 10.3* 13.1* 1339* 15.8* 3.610.2** 3.79.7** 4.6** 13.115.3*

Production (gm2) 1.67.0** 12.8* 27.2** 17.9* 12.2* 61* 35.5* 15.974.2** 19.231.7** 22.7** 50.866.1*

P/B
3.55.9 3 2.6 1.8 1.1 2.5 1.82.3 4.47.9 3.35.3 4.9 3.34.6

Authors [38] [11] [31] [43] [30] [29] [23] Present study [52] [2] [25]

When juveniles considered;

station 3 excluded; * dry weight; ** ash free dry weight.

July and August. Two main annual peaks were also reported for a shallow lagoon in the Bay of Cdiz, Spain, one in late spring/early summer and the other in late autumn/early winter [2]. A considerable variation of density was also observed between sampling sites. This can be attributed to environmental factors, since the distribution of N. diversicolor at the various tidal levels in estuaries can be correlated not only with the exposure period but also with the salinity and the nature of the substratum [12]. Salinity at station 3 was generally low and it frequently decreased below 2 PSU and the sandy sediment with low organic matter content may also represent an adverse situation. The fact that most specimens collected at this station were medium size or large individuals suggests the absence of or low success in reproduction. Smith [50] describes the tolerance proles for developing larvae of N. diversicolor from Kristineberg, Swedish west coast, and Tvrminne, Gulf of Finland, and shows a bottle-neck of salinities above and below which cleavage of the eggs and early larval development are blocked. He also indicates that optimal development is found at different salinities according to the origin of the worms. For the Humber estuary, England, Ozoh and Jones [45] found that low salinities (12.23.86 PSU) are not favourable to fertilisation nor to cleavage of the eggs, while high salinities (22.830.5 PSU) are favourable to fertilisation but not to cleavage. Another unfavourable condition may result from the highly asymmetrical tidal wave in the Canal de Mira leading to dessication of the surface sediments, inhabited by the young worms, during the prolonged periods of emersion in the area of station 3, where ood takes at most 4 h while the ebb is extended to about 8 h [15].
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Therefore, it is possible that the population at this station is maintained by immigration from lower sites, as was also suggested by Mettam [36] for upstream sites in the Severn estuary, Wales. Immigration from outside a sh pond was observed in the Bay of Cdiz, Spain, only 2 months after the pond was emptied and the surface sediments were removed. The salinities at stations 1 and 2 were within the range commonly indicated for this species in European estuaries [45]. On the other hand, the higher abundance of ne particles and organic matter content at stations 1 and 2 may indicate a more favourable substrate when compared to station 3. Nevertheless, differences in abundance between stations 1 and 2 were not negligible and these may be attributed to differences in salinity and to biotic factors, since N. diversicolor is highly prone to predation [8, 26, 27, 39, 53] and a weak competitor [38]. Smith [47, 48] considers that not only the salinity optimum of N. diversicolor differs according to the type of habitat, but also that the potential range may be restricted by interspecic competition. In the Canal de Mira, the number of infaunal macrobenthic species is substantially reduced in the area of station 2 compared to station 1 [40], indicating a lower interspecic competition at station 2. On the other hand, sh is more diverse and more abundant [46] and the predation pressure by birds is also much more important (A. Luis, pers. comm.) in the area of station 1. 4.2. Abundance, production and growth Recent literature provides comparisons of the results regarding densities, biomass and production of N. diversicolor obtained by several authors along the

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Table IV. Comparison of estimated body length growth rates of Nereis diversicolor for worms longer than 2 cm. Site Ythan estuary, Scotland Dievengat, Belgium Ria de Aveiro, Portugal Bay of Cdiz, Spain
+

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Growth rate (mmd1) 0.15 0.0440.091+ 0.160.20 0.272

Authors [11] [29] Present study [2]

Decreases with body length.

Atlantic coast from northern Europe to Morocco [23, 43]. Table III summarises the information for the sites where biomass and production were estimated. Taking into account the observed trends, Gillet [23] suggests a latitudinal gradient of production, with higher values in warmer waters. In the Ria de Aveiro, the mean annual densities at stations 1 and 2 were similar to those cited for the Ythan estuary, the Stiffkey saltmarshes and the Bou Regreg estuary, but slightly lower than those reported for the Norsminde Fjord, the Fenn Creek, the Loire estuary and the shallow lagoon in the Bay of Cdiz. The estimated annual production in the Ria de Aveiro agrees with Gillets suggestion that the production of N. diversicolor is higher in ratio is similar to warmer waters. Moreover, the P/B the previously reported values for Morocco, Portugal and Spain, but is considerably higher than the ratios observed in northern areas (ranging from 3 down to 1.1), indicating lower turnover rates at higher latitudes. The only exception is the P/B ratios of 3.55.9 for shallow-water embayments on the Swedish west coast, but these were observed in populations of juveniles. The average annual increment in body length of N. diversicolor in the study area was estimated as 6.37.4 cm at station 1 and 5.8 cm at station 2, indicating an average body growth rate of 0.160.20 mmd1 for worms with size over ca. 2 cm length. These growth rates are higher than those reported for northern areas and only slightly lower than the value estimated for SW Spain (table IV). In the Ria de Aveiro, the mean jaw size varied between 0.80 and 3.15 mm, which is very close to the values found in the Stiffkey saltmarshes, England (0.73.2 mm; [43]). Nevertheless, the jaw size growth rates at the Ria de Aveiro (3.95.2 md1) were considerably higher than those found at Stiffkey (2.22.7 md1). 4.3. Recruitment and spawning A large variation in the breeding season of eld populations of N. diversicolor has been reported by

several authors based on direct observations of the oogenic cycle or deduced from indirect evidence (table V). The reported variation includes a single spawning season (sometimes very short) during spring or summer, an extended breeding season with one or two spawning peaks, or spawning throughout the whole year. Under laboratory conditions, BartelsHardege and Zeeck [6] found that synchronisation of reproduction in N. diversicolor collected in Jadebusen, Germany, depends not only on the absolute temperature, but also on the timing of the temperature rising above 6 C; under constant temperature (16 C), without any simulation of winter, no synchronised spawning was observed. The same authors also reported similar effects in the eld, where after an unusually warm winter, reproduction took place later and was less synchronised than in previous years. In this study, two recruitment periods were consistently observed at stations 1 and 2, the rst with a peak in February at station 1 and in March at station 2, and the second with a peak in April at station 1 and in May at station 2. In 1994, a third recruitment seemed to occur at station 1 in September. However, this late recruitment was not conrmed by the study of the oogenic cycle, which indicated two spawning periods at both stations, nor by the number of cohorts that became extinct each year always two usually one in May (but April at station 1 in 1994) and the other in September (but August at station 1 in 1994). The observations on the oogenic cycle in 1994 showed the presence of two cohorts of ripe females, i.e. bearing oocytes larger than 200 m [17], one in late winter/early spring and the other in summer/early autumn. The rst cohort was completely spawned in April at station 1 and May at station 2, whereas the second cohort appeared to spawn mostly between September and October, although some females with large oocytes were still present in October. The indicated dates for the rst spawning are consistent with the observed extinctions of cohort C3, in April at station 1 and May at station 2. However, with respect to the second spawning season, there is a time-lag of about 1 month between the extinction of cohort C4 (August at station 1 and September at station 2) and the suggested spawning peak. Whether this discrepancy should be merely attributed to sampling effects or rather to the presence of non-spawning females with mature oocytes after the spawning season, as described by Dales [17], Smith [50], Mettam et al. [37] and Mller [38], cannot be discerned from our present data. The observed sex ratio in this study was clearly favourable to females, as appears to be the case in most populations of N. diversicolor [17, 37, 44, 51]. An indirect estimate of pre-recruitment growth rates was obtained, in order to establish a relationship
Acta Oecologica

Ecology of Nereis diversicolor in the Ria de Aveiro

281

Table V. Breeding period of Nereis diversicolor in relation to geographical distribution, according to Dales, [17], Clay, [12] and updated. (O) Oocytes in coelom; (S) spawning; (L) occurrence of larvae; (J) occurrence of juveniles. Site Gteborg, Sweden St. Andrews, Scotland Ythan estuary, Scotland Oresund, Denmark Copenhage, Denmark Skallingen, Denmark Norsminde Fjord, Denmark Blyth estuary, England Stiffky saltmarshes, England Dee estuary, England Thames estuary, England Severn estuary, Wales Baltic Sea Baltic Sea Jadebusen, North Sea Zuidersee, the Netherlands Ems estuary, the Netherlands Dievengat, Belgium Cherbourg, France Roscoff, France Portel, France Loire estuary, France Ria de Plencia, Spain Ria de Bilbao, Spain Bay of Cdiz, Spain Ria de Aveiro, Portugal Ribeira de Aljezur, Portugal * information not available Jan * O O, S Feb O O S Mar S, L O, S S, J L O J O, S Apr O O L L O S, J S May O O, J L L O S, J O, L S J O, S S O S S, J S J J J J O, J O, J Jun O O, S L L O S * S J J O, J Jul O O, S L L O S, J O, J J J J O Aug * S L L J O Sep O O L Oct * O O L Nov O O * L Dec * O O Authors [38] [35] [11] [12, 17] [12, 17] [12, 17] [31] [44] [43] [12] [17, 18] [37] [49, 50, 51] [9] [12] [12, 17] [19] [29] [12, 17] [12, 17] [12] [23] [21] [21] [2] Present study [20]

S *

O O

O, S O

O, L O

O, L O S S O S J S J J

O O S

O O S

O O

O O

J S S, J S J J J O, J O, J L J S, J S J J J O, J O, J L J S, J S J J J S, J S J J J J S, J S J J J S, J S J J J O O, J J S, J S J J J J O O, J

J S S J J J O O, J

J S S J J J O, J O, J

J S J J

J J O, S, J O, S, J O, J O, J

O, J O, J

O, S, J O, S, J O, J O, J

between the two annual spawning and recruitment periods, and to predict the longevity of N. diversicolor in the Ria de Aveiro. We assumed the following: (i) the rst recruitment of the year was formed by juveniles originated from the rst spawning of the previous year; and (ii) the second recruitment was formed by juveniles originated from the second spawning of the previous year. Heip and Herman [29] and Mller [38] observed that worms smaller than 12 mm have higher growth rates with increasing size, and Dales [17] found a geometrical growth rate until the age of 10 weeks, when the worms were 4 mm long. Bearing this in mind, we estimated the average growth rate for individuals with body size in the range of 4 mm to the observed mean size at the peaks of recruitment (20.029.6 mm) using the following expression: growth rate = (assumed number of days from spawning to recruitment 70 d) / (mean size at recruitVol. 20 (4) 1999

ment 4 mm). The estimated growth rates were 0.10 and 0.12 mmd1 for individuals resulting from the rst and the second spawnings, respectively. These values are close to those found in literature: 0.09 mmd1 in the Dievengat, Belgium [29], for worms with length between 0 and 30 mm, and in the Gullmarsvik Fjord, Swedish west coast [38] for worms with length up to 12 mm; 0.090.20 mmd1 for small juveniles in the Wadden Sea [29]. Since the estimated pre-recruitment growth rates appear to validate our assumptions, we predict that the longevity of N. diversicolor in the study area is about 2 years (2122 and 2324 months, for cohorts C4 and C3, respectively). Although a 1-year life-span was reported for N. diversicolor in the Wadden Sea, in most populations, somatic growth takes between 1.5 to 2 years before spawning, but a 3-year life cycle has also been observed (table VI). Olive and Garwood [44] discuss

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Table VI. Comparison of Nereis diversicolor longevity data recorded in literature. Site Gteborg, Sweden Ythan estuary, Scotland Norsminde Fjord, Denmark Blyth estuary, England Stiffky saltmarshes, England Thames estuary, England Severn estuary, Wales Ems estuary, the Netherlands Wadden Sea Loire estuary, France Ria de Aveiro, Portugal Bou Regreg estuary, Morocco Life-span (years) 23 12 11 3 12 1 2 2 1 1 2 2 Authors [38] [11] [31] [44] [43] [18] [37] [19] [28] [23] Present study [25]

A. Abrantes et al.

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Acta Oecologica

the survival strategy for a semelparous (monotelic) animal, such as a nereid worm, living for more than 1 year (3 years in the case of the Blyth estuary population) before breeding. They point out that a xed life-span would result in reproductive and genetic isolation between consecutive year classes and suggest that this isolation could be prevented if some animals reached maturity in less (or possibly more) than 3 years; a variable age at maturity could arise if the population was polymorphic in terms of their genetically determined age at maturity, or if age at maturity was variable and inuenced by environmental conditions. Several authors have reported high levels of physiological and morphological variation in N. diversicolor from different areas and different environmental conditions in the same general area [1, 4, 5, 13, 22, 24, 49]. In the present study, the two observed spawning seasons may indicate a polymorphic population arising from selection pressure for a long breeding season in a remarkably variable environment, but where temperature remains favourable for reproduction throughout a large part of the year. However, to test this hypothesis, further studies are needed, including genetic intraspecic variation.

Acknowledgments
The authors wish to thank Sr Rui Marques for his assistance in the eld, and the helpful comments by an anonymous referee on an earlier version of the paper. This work was carried out while one of us (F. Pinto) received a research studentship from JNICT (CINCIA BM/3553/92).

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