ecologia de n. diversicolor no estuário do mira (aveiro)

8/12/2019 Ecologia de N. diversicolor no esturio do Mira (Aveiro)

1/17

Ecology of the polychaete Nereis diversicolor in the Canal de Mira (Riade 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: [email protected])

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

Abstract The population ofNereis diversicolorO.F. Mller was studied in 1993 and 1994 at three intertidal areas along the estuarine gradientin the Canal de Mira (Ria de Aveiro). The population dynamics, secondary production and growth were followed for the 2-year period, whereasin the second year, a study on the oogenic cycle was also carried out. For the population dynamics and production studies, core samples werecollected 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 ind m2)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 dryweightm2year1 and theP/B ratio from 4.4 to 7.9. The average body growth rate varied between 0.16 and 0.20 mmd1 for worms longer than2 cm. Two recruitment seasons were detected each year. Two spawning periods were also observed, one in the spring and the other in earlyautumn. 1999 ditions scientifiques et mdicales Elsevier SAS

Nereis diversicolor/ population dynamics / production / oogenesis / benthos / estuaries

1. INTRODUCTION

The polychaete Nereis diversicolor is a commoninhabitant of intertidal mudflats of estuaries and shal-low water bodies with a wide geographical distribu-tion [10, 12, 34]. In the NE Atlantic, the species occursfrom northern Europe to Morocco [22]. Several stud-ies on the life history of this worm have shownimportant variations in different places, in response toenvironmental gradients and local conditions, andsome features of its biology and ecology still remainobscure. Although some knowledge already existsregarding meridional populations, most studies havebeen concentrated in northern Europe. This paperdeals with some aspects of the life history of N.diversicoloralong an estuarine gradient in a Europeanwarm-temperate shallow water body, including thepopulation dynamics, secondary production, growthand oogenic cycle.

2. MATERIALS AND METHODS

2.1. Study area

The Ria de Aveiro (NW Portugal) is a shallowlagoon with a surface area of about 45 km2, formed byseveral branches and an intricate system of bays andnarrow channels. The lagoon communicates with theAtlantic through an artificial inlet [16, 42]. The deeperareas near the inlet are characterised by strong marineinfluence (tidal inflow of 25 to 90 million m3), withhigh values of current velocity and tidal range (23 mat spring tides), while in remote shallow areas, thecirculation and the sea water inflow are reduced. Thetidal wave is considerably distorted as it progresses

inside the lagoon, so that with increasing distance fromthe inlet the duration of flood becomes shorter thanthat of the ebb. The two main channels extend from theinlet northwards (Canal de Ovar) and southwards(Canal de Mira) and are separated from the Atlantic bya narrow sand bar (figure 1). The Canal de Mira, whichis second in terms of average width, receives acontinuous freshwater supply through a small systemof lagoons and streams. Three main sections can berecognised: (i) a lower section with salinities ranging

Acta Oecologica20 (4) (1999) 267283 / 1999 Editions scientifiques et mdicales Elsevier SAS. All rights reserved.


2/17

between tides from values higher than 18 to 3035 formost of the year; (ii) a middle section with a highlyvariable regime; (iii) an upper section with salinitiesnot higher than 0.1 all year round [40]. The threeselected sampling stations (#1, #2 and #3) are locatedin intertidal areas at the Canal de Mira, within thesalinity sections (i) and (ii), and apart from each otheralong the estuarine gradient (figure 1).

2.2. Sampling and laboratory procedures

The sampling programme was carried out at the threestations on a monthly basis during 2 years, from January1993 to December 1994. For the population dynamics

and production studies, ten core samples (correspondingto a total area of 0.1 m2) were randomly collected at eachstation, during both years, to a depth of about 30 cm andsieved in the field using a 0.5-mm mesh. Mentholcrystals were added to the collected material to causerelaxation of the animals. On arrival to the laboratory,the samples were fixed with 10 % buffered formalinstained with Rose Bengal and within a few days, theywere washed under running water over a set of threesieves with 2 000, 1 000 and 500-m mesh size. The

material retained in each sieve was sorted separately in awhite tray, using a magnifying glass for the fractioncorresponding to the finer mesh. All complete wormsobtained in 1993 were used for biometrical measure-ments. The total body length was measured to the nearest

mm and the total jaw length, as defined by Olive andGarwood [44], was determined under a dissecting micro-scope using a calibrated eye piece graticule. The indi-viduals were dried to constant weight (72 h at 65 C) andweighed after cooling in a dessicator to 0.1 mg. The ashcontent was estimated as loss of weight on ignition (4 hat 550 C). The ash free dry weight was given by thedifference between the dry weight and the ash content ofeach specimen. All other worms contained in the sampleswere preserved in 70 % ethanol until further processing.In order to measure the jaw length, these specimens werefirst maintained in freshwater for a few days, since it wasfound that this procedure facilitates the dissection of the

jaws from the surrounding tissues in preserved animals.

For the study of the reproductive cycle, qualitativesamples were obtained during the second year. Me-dium size and large animals were collected monthlyfrom the sediment at stations 1 and 2. These animalswere placed in bottles containing local water, to whichmenthol crystals were added. In the laboratory, thespecimens were fixed with formalin and observed inorder to determine the presence of sexual products inthe ceolom. Whenever possible ten oocyte-bearingfemales from stations 1 and 2 were dissected eachmonth. The worms were opened from the anterior tothe posterior end inside a Petri dish under a dissectingmicroscope, and the ceolomic content was gradually

extracted with a Pasteur pipette and transferred to a550-L Sedgewick-Rafter counting chamber. Thespecimens were carefully rinsed with distilled water,and this water was recovered to ensure that no oocyteswere lost. The number of oocytes in each female wascounted under a binocular microscope and wheneverpossible fifty oocytes were measured using a cali-brated eye piece graticule. The longest and the shortestlength of each oocyte was determined, and the averagevalue was used as an estimate of oocyte size. Maleswere recognised by the presence of sperm aggregates,and those animals without sexual products were con-sidered to have undetermined sex. The jaws of all

specimens were removed and measured using thesame procedure as indicated above.

At each sampling occasion, several environmentalparameters were measured. Sediment temperature wasregistered with a thermometer at the sediment subsur-face (2.5 cm depth). Salinity of the water retained intidal pools was measured with a refractometer. Sedi-ment samples were collected using small PVC corers(4 cm diameter) to a depth of 30 cm and frozen untilanalysis. The organic matter content of the sediments

Figure 1. Ria de Aveiro and Canal de Mira, Portugal, showing thelocation of the three sampling stations (#1, #2 and #3).

268 A. Abrantes et al.

Acta Oecologica


3/17

was determined every month by loss of weight onignition (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 fromthe whole core sample and in 1994, two separate layers

were considered (surface layer up to 2 cm and deeperlayer below 2 cm). For the grain size analysis, sedi-ment samples were homogenised and a portion ofabout 200 g was dried to constant weight (72 h at65 C). A set of seven sieves with mesh sizes corre-sponding 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 aRetsch Sieve Shaker and the frequency of each gradewas expressed as a percentage of total weight. Sedi-ments were classified into different types according tothe criteria adopted by Larsonneur [32].

2.3. Data treatment

The analysis of the Gaussian components in the jawsize frequency histograms was based on Bhatta-charyas method of logarithmic differences [7] usingthe Bhatta software developed by Lepetit et al. [33].Each Gaussian component was interpreted as repre-senting a different cohort as described by Gillet [23] ina study on the population dynamics and production of

N. diversicolorin the Loire estuary, France.The biomass was estimated using the regression

equations of log10 ash free dry weight on log10 jawlength determined separately for stations 1 and 2. Toenable comparisons between this study and othersusing body length, the relationship between bodylength and jaw length was also determined.

The following regressions related total jaw length(JL) to ash free dry weight (AFDW) and to bodylength (BL) at station 1:

log10AFDW (g) = 2.213 log10JL (mm) 2.088(n= 44; r= 0.94; P


4/17

organic matter content for the whole samples in 1993was 2.3 (SD = 1.02), 2.3 (SD = 0.59) and 1.8 %(SD = 0.92) at stations 1, 2 and 3, respectively. In1994, 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, and2.0 (SD = 0.90) and 1.5 % (SD = 0.87) at station 3, atthe subsurface and the deeper layers, respectively.

3.2. Population structure and growth

The abundance of N. diversicolorvaried consider-ably during the study period and between stations(figure 5). On the whole, the densities followed similarpatterns in both years, though the general abundancewas slightly higher in the first year. The mean annualdensities were higher at station 2 (718 indm2,SD = 294.8 in 1993; 573 indm2, SD = 130.4 in1994), followed by station 1 (190 indm2, SD = 70 in1993; 275 indm2, SD = 101.9 in 1994) and station 3(43 indm2, SD = 17.4 in 1993; 94 indm2, SD = 47.2in 1994). In both years, densities increased from latewinter throughout spring, were fairly stable in sum-mer, especially in 1993, and declined drastically in theautumn. In 1993, a clear response to an increase in thesubsurface sediment temperature above 13 C wasobserved, while in 1994, the relationship between theincrease in density and the sediment temperature was

rather obscure. A substantial reduction in the densitiesobserved in May 1994 coincided with a decrease insalinity (figure 3).

Figures 6and 7show the evolution of the popula-tion structure at station 1 for the 2-year period. A totalof 559 individuals were collected with jaw lengths inthe range 0.423.27 mm. When the study began inJanuary 1993, the population was formed by twocohorts, C1 and C2, where C1 corresponds to the olderindividuals. Cohort C1 was registered for the last time

in April and cohort C2 in August. Two newly recruited

cohorts were detected in 1993, in February (C3) andApril (C4), and were followed until March and July1994, respectively. In the second year, three newlyrecruited cohorts were detected, the first (C5) and thesecond (C6) in the same months as C3 and C4 in theprevious year and a third one (C7) in September. Forthe five cohorts that were recruited within the studyperiod, the mean jaw length at recruitment variedbetween 0.80 and 1.12 mm (mean body length:1.42.6 cm). With regard to the four cohorts that

Figure 3. Salinity values at the three sampling stations from January1993 to December 1994.

Figure 4. Cumulative curves of grain size frequency of the sedi-ments collected at the three sampling stations with time intervals of6 months.


Acta Oecologica


5/17

became extinct during the same period, the mean jawlength before extinction ranged from 2.79 to 3.15 mm

(mean body length: 9.210.6 cm). The two cohorts thatwere followed from recruitment to extinction grewfrom 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 to9.2 cm (C3) and from 1.4 to 10.6 cm (C4). Accord-ingly, the average annual increment in body length was6.3 cm for cohort C3 and 7.4 cm for cohort C4.

At station 2, a total of 1 548 individuals werecollected with jaw length ranging from 0.54 to3.29 mm.Figures 8and9indicate that the evolution ofthe population structure was, in general, similar to thatobserved at station 1. From the two cohorts detected inJanuary 1994, one (C1) was registered for the last timein April and the other (C2) in August. Two newlyrecruited cohorts were detected in1993, in March (C3)and May (C4), and these cohorts were followed untilApril and August 1994, respectively. In 1994, twonewly recruited cohorts were detected, C5 in Marchand C6 in May. For the four cohorts recruited withinthe study period, the mean jaw length at recruitmentvaried between 0.99 and 1.19 mm (mean body length:2.23.0 cm). Before extinction, the mean jaw lengthvaried between 2.63 and 2.75 mm (mean body length:9.09.4 cm). The two cohorts that were followed fromrecruitment to extinction grew from 1.19 to 2.72 mmmean jaw length in 13 months (C3) and from 0.99 to

2.63 mm in 15 months (C4), corresponding to in-creases in mean body length from 3.0 to 9.3 cm (C3)and from 2.2 to 9.0 cm (C4). The growth rate forcohort C4 was not estimated due to the continuousrecruitment of small individuals into this cohort duringseveral months (figures 8, 9). The results for cohort C3give an average annual increment in body length of5.8 cm.

At station 3, the abundance of N. diversicolorwasvery low and, therefore, it was not possible to analyse

Figure 5. Population density (indm2) of Nereis diversicolor ateach sampling station from January 1993 to December 1994.

Figure 6. Histograms of total jaw length ofNereis diversicolorfromJanuary 1993 to December 1994 at station 1, showing the cohorts (C)obtained using the Bhatta software.

Figure 7. Growth curves of cohorts (C) ofNereis diversicolorfromJanuary 1993 to December 1994 at station 1. Vertical bars arestandard deviation.

Ecology of Nereis diversicolor in the Ria de Aveiro 271

Vol. 20 (4) 1999


6/17

the Gaussian components of the population structure.At this station, a total of 163 individuals were col-lected with jaw length in the range 0.443.39 mm.Figure 10 shows that small specimens were veryscarce, so that the population was mainly composed ofmedium 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 1993and 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 1was 3.6 and 5.2 g AFDWm2, givingP/B ratios of 4.4and 5.2 in 1993 and 1994, respectively. At station 2,the mean annual biomass was 10.2 and 9.4 gAFDWm2, givingP/B ratios of 5.7 and 7.9 in the firstand second year of this study.

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

Figure 9. Growth curves of cohorts (C) ofNereis diversicolorfromJanuary 1993 to December 1994 at station 2. Vertical bars arestandard deviation.

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


Acta Oecologica


7/17

3.4. Oogenic cycle

The number of oocytes per female varied between40 and 15 242 and, in general, there was a significantpositive correlation between the number of oocytes inthe coelomic cavity and the jaw length (table II).

Figures 11and12show the mean and total range ofoocyte diameter for individual females examined

throughout the study period at stations 1 and 2,respectively. The data are presented in a graph formatsimilar to that used by Olive and Garwood [44] andMettam et al. [37]. While for part of the year, there wasa continuous gradation from small to large oocytes, onsome occasions two well-defined groups of femalescould be identified, one bearing small oocytes and the

Table I. Production of cohorts C1, C2, C3 and C4 ofNereis diversicolorestimated by the method of Crisp [14] at station 2 in 1993. All weightvalues are ash free dry weight.

Cohort Samplingdate

Density Mean weight perindividual

Weightincrement

Mean densityduring periodt

Productionincrement

Annualproduction

(month) N (m2) W (g) DW (g) N (m2) NDW (gm2) P (gm2)

C1 Jan 170 0.0594

Feb 190 0.0615 0.0021 180 0.3763

Mar 150 0.0711 0.0096 170 1.6322

Apr 70 0.0833 0.0122 110 1.3432

3.35

C2 Jan 240 0.0152

Feb 200 0.0217 0.0065 220 1.4246

Mar 510 0.0206 0.0011 355 0

Apr 380 0.0461 0.0255 445 11.3333

May 470 0.0594 0.0134 425 5.6815

Jun 560 0.0528 0.0066 515 0

Jul 460 0.0644 0.0116 510 5.9096Aug 320 0.0868 0.0224 390 8.7437

33.09

C3 Mar 290 0.0084

Apr 380 0.0155 0.0070 335 2.3603

May 510 0.0228 0.0073 445 3.2426

Jun 350 0.0271 0.0043 430 1.8664

Jul 470 0.0320 0.0048 410 1.9831

Aug 440 0.0310 0.0009 455 0

Sep 260 0.0594 0.0284 350 9.9434

Oct 170 0.0561 0.0034 215 0

Nov 250 0.0449 0.0111 210 0

Dec 170 0.0389 0.0061 210 019.40

C4 May 170 0.0051

Jun 170 0.0075 0.0024 170 0.4135

Jul 180 0.0084 0.0010 175 0.1663

Aug 340 0.0113 0.0028 260 0.7340

Sep 370 0.0120 0.0007 355 0.2581

Oct 260 0.0120 0.0000 315 0.0000

Nov 150 0.0088 0.0031 205 0

Dec 220 0.0120 0.0031 185 0.5826

2.15

Total 57.99


Vol. 20 (4) 1999


8/17

other bearing large oocytes. At station 1, two distinctgroups were patent in March, one of which had meanoocyte size in the range 161226m. Later, in theperiod from June to September, two groups of femaleswere also present. The group with large oocytesreached a mean oocyte diameter between 185 and236m in September. Females with large oocytes didnot occur in April, while from the second group, onlyone (out of five) was collected in October and none inNovember. At this station, it is also worthy to noticethat the distribution of the oocyte diameter in Decem-ber was very similar to that observed in January of thesame year, with one out of four to five females bearingoocytes with mean diameter over 200m. At station 2,two females with large oocytes (mean size 204 and217m) were registered in April and, later, a largergroup in September (mean oocyte size in the range185238m), while in the subsequent months, fe-males with large oocytes were absent or rare. Thus, inMay, only a group with a mean oocyte diameter in therange 65132m was present, with only one femalebearing some large oocytes (over 200 m), and thesame happened in June. In July, a new group offemales with small oocytes (less than 60m) started toemerge. With regard to the second period, only two

females with large oocytes were found in October andnone in November. Females with small oocytes (lessthan 75m) started to occur in December.

The size frequency histograms in figures 13and 14show the evolution of oocyte size throughout the year.At station 1, both the presence of large oocytesbetween January and March, when a peak was veryconspicuous, and the complete absence of large oo-cytes in April indicate that a spawning occurred priorto 26 April. A second maturation and spawning period

in summer and early autumn is suggested by thepresence of a group of oocytes with increasing sizefrom June to September. From this group, some largeoocytes were still present in October but none inNovember. A similar pattern, indicating two spawningperiods, was observed at station 2, where the majordifferences in relation to station 1 were the following:(i) the first spawning period was extended until April;(ii) the group of large oocytes corresponding to thesecond 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 inthe samples, on some occasions, males were not found.From the total number observed at station 1, 90 werefemales, 17 males and 37 of undetermined sex. Thecorresponding figures for station 2 were 107, 34 and30. These figures indicate a sex ratio (male:female) of1:5.3 at station 1 and 1:3.1 at station 2.

4. DISCUSSION

4.1. Environmental impact

The population ofNereis diversicolorin the Canal

de Mira exhibited important seasonal fluctuations inabundance with high densities in spring and summerand low numbers in winter, as reported for the Ythanestuary, Scotland [11]. Similar fluctuations but withpeaks delayed until summer or early autumn wereobserved in the Thames estuary, England [18], theDievengat, Belgium [29], the Norsminde Fjord, Den-mark [31] and the Stiffkey saltmarshes, England [43].In the Loire estuary, France, Gillet [23] found highdensities in May and December and low numbers in

Table II. Correlation coefficient between number of oocytes per female and jaw size at stations 1 and 2 during 1994.

Month Station 1 Station 2

n r P n r P

Jan 4 0.982 0.05 > P >0.01 8 0.199 P >0.05

Feb 10 0.904 P < 0.01 10 0.498 P >0.05

Mar 10 0.868 P < 0.01 10 0.855 P 0.01 10 0.935 P 0.05 10 0.751 P 0.05 4 0.855 P >0.05

Dec 5 0.854 P > 0.05 8 0.847 P


9/17

Figure 11. Mean and total range of oocyte diameter in individualNereis diversicolorfrom station 1, ranked by mean diameter, from Januaryto December 1994. ([) Mean size; () smallest oocytes; () largest oocytes.


Vol. 20 (4) 1999


10/17

Figure 12. Mean and total range of oocyte diameter in individualNereis diversicolorfrom station 2, ranked by mean diameter, from Januaryto December 1994. ([) Mean size; () smallest oocytes; () largest oocytes.


Acta Oecologica


11/17

Figure 13. Oocyte diameter ofNereis diversicolorfor all females collected at the same date at station 1, from January to December 1994.


Vol. 20 (4) 1999


12/17

Figure 14. Oocyte diameter ofNereis diversicolorfor all females collected at the same date at station 2, from January to December 1994.


Acta Oecologica


13/17

July and August. Two main annual peaks were alsoreported for a shallow lagoon in the Bay of Cdiz,Spain, one in late spring/early summer and the other inlate autumn/early winter [2].

A considerable variation of density was also ob-served between sampling sites. This can be attributedto environmental factors, since the distribution of N.diversicolorat the various tidal levels in estuaries canbe correlated not only with the exposure period butalso with the salinity and the nature of the substra-tum [12]. Salinity at station 3 was generally low and it

frequently decreased below 2 PSU and the sandysediment with low organic matter content may alsorepresent an adverse situation. The fact that mostspecimens collected at this station were medium sizeor large individuals suggests the absence of or lowsuccess in reproduction. Smith [50] describes the tol-erance profiles for developing larvae ofN. diversicolorfrom Kristineberg, Swedish west coast, andTvrminne, Gulf of Finland, and shows a bottle-neckof salinities above and below which cleavage of theeggs and early larval development are blocked. Healso indicates that optimal development is found atdifferent salinities according to the origin of theworms. 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 theeggs, while high salinities (22.830.5 PSU) are favour-able to fertilisation but not to cleavage. Anotherunfavourable condition may result from the highlyasymmetrical tidal wave in the Canal de Mira leadingto dessication of the surface sediments, inhabited bythe young worms, during the prolonged periods ofemersion in the area of station 3, where flood takes atmost 4 h while the ebb is extended to about 8 h [15].

Therefore, it is possible that the population at thisstation is maintained by immigration from lower sites,as was also suggested by Mettam [36] for upstreamsites in the Severn estuary, Wales. Immigration fromoutside a fish pond was observed in the Bay of Cdiz,Spain, only 2 months after the pond was emptied andthe surface sediments were removed.

The salinities at stations 1 and 2 were within therange commonly indicated for this species in Europeanestuaries [45]. On the other hand, the higher abun-dance of fine particles and organic matter content at

stations 1 and 2 may indicate a more favourablesubstrate when compared to station 3. Nevertheless,differences in abundance between stations 1 and 2were not negligible and these may be attributed todifferences in salinity and to biotic factors, since N.diversicoloris highly prone to predation [8, 26, 27, 39,53] and a weak competitor [38]. Smith [47, 48] con-siders that not only the salinity optimum of N. diver-sicolordiffers according to the type of habitat, but alsothat the potential range may be restricted by interspe-cific competition. In the Canal de Mira, the number ofinfaunal macrobenthic species is substantially reducedin the area of station 2 compared to station 1 [40],indicating a lower interspecific competition at station2. On the other hand, fish is more diverse and moreabundant [46] and the predation pressure by birds isalso much more important (A. Luis, pers. comm.) inthe area of station 1.

4.2. Abundance, production and growth

Recent literature provides comparisons of the re-sults regarding densities, biomass and production ofN.diversicolor obtained by several authors along the

Table III. Density, biomass and production of Nereis diversicolor in relation to geographical distribution. When a single value is given, itcorresponds to the mean density or biomass.

Site Density Biomass Production P/B Authors(indm2) (gm2) (gm2)

Gteborg, Sweden 80060 000+

0.31.4** 1.67.0** 3.55.9 [38]Ythan estuary, Scotland 208961 4.2* 12.8* 3 [11]

Norsminde Fjord, Denmark 1 305 10.5** 27.2** 2.6 [31]

Stiffky saltmarshes, England 392 10.3* 17.9* 1.8 [43]

Fenn Creek, England 4591 296 13.1* 12.2* 1.1 [30]

Dievengat, Belgium 5 00017 000+ 1339* 61* 2.5 [29]

Loire estuary, France 8003 200 15.8* 35.5* 1.82.3 [23]

Ria de Aveiro, Portugal++ 190718 3.610.2** 15.974.2** 4.47.9 Present study

Ria Formosa, Portugal 3.79.7** 19.231.7** 3.35.3 [52]

Bay of Cdiz, Spain 6532 626 4.6** 22.7** 4.9 [2]

Bou Regreg estuary, Morocco 585620 13.115.3* 50.866.1* 3.34.6 [25]

+ When juveniles considered; ++ station 3 excluded; * dry weight; ** ash free dry weight.


Vol. 20 (4) 1999


14/17

Atlantic coast from northern Europe to Morocco [23,43].Table IIIsummarises the information for the siteswhere biomass and production were estimated. Takinginto account the observed trends, Gillet [23] suggests alatitudinal gradient of production, with higher values

in warmer waters. In the Ria de Aveiro, the meanannual densities at stations 1 and 2 were similar tothose cited for the Ythan estuary, the Stiffkey salt-marshes and the Bou Regreg estuary, but slightlylower than those reported for the Norsminde Fjord, theFenn Creek, the Loire estuary and the shallow lagoonin the Bay of Cdiz. The estimated annual productionin the Ria de Aveiro agrees with Gillets suggestionthat the production of N. diversicolor is higher inwarmer waters. Moreover, the P/B ratio is similar tothe previously reported values for Morocco, Portugaland Spain, but is considerably higher than the ratiosobserved 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 forshallow-water embayments on the Swedish west coast,but these were observed in populations of juveniles.

The average annual increment in body length ofN.diversicolor in the study area was estimated as6.37.4 cm at station 1 and 5.8 cm at station 2,indicating an average body growth rate of0.160.20 mmd1 for worms with size over ca. 2 cmlength. These growth rates are higher than thosereported for northern areas and only slightly lowerthan the value estimated for SW Spain (table IV). Inthe Ria de Aveiro, the mean jaw size varied between0.80 and 3.15 mm, which is very close to the valuesfound in the Stiffkey saltmarshes, England(0.73.2 mm; [43]). Nevertheless, the jaw size growthrates at the Ria de Aveiro (3.95.2md1) wereconsiderably higher than those found at Stiffkey(2.22.7md1).

4.3. Recruitment and spawning

A large variation in the breeding season of fieldpopulations of N. diversicolor has been reported by

several authors based on direct observations of theoogenic cycle or deduced from indirect evidence(table V). The reported variation includes a singlespawning season (sometimes very short) during springor summer, an extended breeding season with one or

two spawning peaks, or spawning throughout thewhole year. Under laboratory conditions, Bartels-Hardege and Zeeck [6] found that synchronisation ofreproduction inN. diversicolorcollected in Jadebusen,Germany, depends not only on the absolute tempera-ture, but also on the timing of the temperature risingabove 6 C; under constant temperature (16 C), with-out any simulation of winter, no synchronised spawn-ing was observed. The same authors also reportedsimilar effects in the field, where after an unusuallywarm winter, reproduction took place later and wasless synchronised than in previous years.

In this study, two recruitment periods were consis-

tently observed at stations 1 and 2, the first with a peakin February at station 1 and in March at station 2, andthe second with a peak in April at station 1 and in Mayat station 2. In 1994, a third recruitment seemed tooccur at station 1 in September. However, this laterecruitment was not confirmed by the study of theoogenic cycle, which indicated two spawning periodsat both stations, nor by the number of cohorts thatbecame extinct each year always two usually onein May (but April at station 1 in 1994) and the other inSeptember (but August at station 1 in 1994). Theobservations on the oogenic cycle in 1994 showed thepresence of two cohorts of ripe females, i.e. bearingoocytes larger than 200m [17], one in late

winter/early spring and the other in summer/earlyautumn. The first cohort was completely spawned inApril at station 1 and May at station 2, whereas thesecond cohort appeared to spawn mostly betweenSeptember and October, although some females withlarge oocytes were still present in October. The indi-cated dates for the first spawning are consistent withthe observed extinctions of cohort C3, in April atstation 1 and May at station 2. However, with respectto the second spawning season, there is a time-lag ofabout 1 month between the extinction of cohort C4(August at station 1 and September at station 2) andthe suggested spawning peak. Whether this discrep-

ancy should be merely attributed to sampling effects orrather to the presence of non-spawning females withmature oocytes after the spawning season, as describedby Dales [17], Smith [50], Mettam et al. [37] andMller [38], cannot be discerned from our presentdata. The observed sex ratio in this study was clearlyfavourable to females, as appears to be the case inmost populations ofN. diversicolor[17, 37, 44, 51].

An indirect estimate of pre-recruitment growth rateswas obtained, in order to establish a relationship

Table IV. Comparison of estimated body length growth rates ofNereis diversicolorfor worms longer than 2 cm.

Site Growth rate Authors(mmd1)

Ythan estuary, Scotland 0.15 [11]Dievengat, Belgium 0.0440.091+ [29]

Ria de Aveiro, Portugal 0.160.20 Present study

Bay of Cdiz, Spain 0.272 [2]

+ Decreases with body length.


Acta Oecologica


15/17

between the two annual spawning and recruitmentperiods, and to predict the longevity ofN. diversicolorin the Ria de Aveiro. We assumed the following: (i) thefirst recruitment of the year was formed by juvenilesoriginated from the first spawning of the previousyear; and (ii) the second recruitment was formed by

juveniles originated from the second spawning of theprevious year. Heip and Herman [29] and Mller [38]

observed that worms smaller than 12 mm have highergrowth rates with increasing size, and Dales [17]found a geometrical growth rate until the age of10 weeks, when the worms were 4 mm long. Bearingthis in mind, we estimated the average growth rate forindividuals with body size in the range of 4 mm to theobserved mean size at the peaks of recruitment(20.029.6 mm) using the following expression:growth rate = (assumed number of days from spawn-ing to recruitment 70 d) / (mean size at recruit-

ment 4 mm). The estimated growth rates were 0.10and 0.12 mmd1 for individuals resulting from thefirst and the second spawnings, respectively. Thesevalues are close to those found in literature:0.09 mmd1 in the Dievengat, Belgium [29], forworms with length between 0 and 30 mm, and in theGullmarsvik Fjord, Swedish west coast [38] for wormswith length up to 12 mm; 0.090.20 mmd1 for small

juveniles in the Wadden Sea [29]. Since the estimatedpre-recruitment growth rates appear to validate ourassumptions, we predict that the longevity of N.diversicolorin the study area is about 2 years (2122and 2324 months, for cohorts C4 and C3, respec-tively). Although a 1-year life-span was reported forN.diversicolor in the Wadden Sea, in most populations,somatic growth takes between 1.5 to 2 years beforespawning, but a 3-year life cycle has also beenobserved (table VI). Olive and Garwood [44] discuss

Table V. Breeding period ofNereis 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 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Authors

Gteborg, Sweden * O S, L O O O O * O * O * [38]

St. Andrews, Scotland O O O, S O O O [35]Ythan estuary, Scotland O, S S S, J O O, J O, S O, S S O O * O [11]

Oresund, Denmark L L L L L L [12, 17]

Copenhage, Denmark L L L L L L L L [12, 17]

Skallingen, Denmark O O O O O [12, 17]

Norsminde Fjord, Denmark S J S, J S, J S S, J J [31]

Blyth estuary, England O * O, S S O, L * O, J O * O O O [44]

Stiffky saltmarshes, England S S J [43]

Dee estuary, England J J [12]

Thames estuary, England O O, S O, L O, L J J J O O O O [17, 18]

Severn estuary, Wales O O O O O, S O, J O O O O O O [37]

Baltic Sea S S S S [49, 50, 51]

Baltic Sea S [9]Jadebusen, North Sea O O O J [12]

Zuidersee, the Netherlands L L [12, 17]

Ems estuary, the Netherlands S S S J J J J J J [19]

Dievengat, Belgium J J J J S, J S, J S, J S, J S, J S, J S, J S, J [29]

Cherbourg, France S S S S S S S S S S S S [12, 17]

Roscoff, France S S [12, 17]

Portel, France J J J J J J J J J J J J [12]

Loire estuary, France J J [23]

Ria de Plencia, Spain J J J J J J J J J J J J [21]

Ria de Bilbao, Spain J [21]

Bay of Cdiz, Spain J J J J J J J J J [2]

Ria de Aveiro, Portugal O O, J O, S, J O, S, J O, J O, J O, J O, J O, S, J O, S, J O O Present study

Ribeira de Aljezur, Portugal O, J O, J O, J O, J O, J O, J O, J O, J O, J O, J O, J O, J [20]

* information not available


Vol. 20 (4) 1999


16/17

the survival strategy for a semelparous (monotelic)animal, such as a nereid worm, living for more than 1year (3 years in the case of the Blyth estuary popula-tion) before breeding. They point out that a fixedlife-span would result in reproductive and geneticisolation between consecutive year classes and suggestthat this isolation could be prevented if some animalsreached maturity in less (or possibly more) than 3years; a variable age at maturity could arise if thepopulation was polymorphic in terms of their geneti-

cally determined age at maturity, or if age at maturitywas variable and influenced by environmental condi-tions. Several authors have reported high levels ofphysiological and morphological variation inN. diver-sicolorfrom different areas and different environmen-tal conditions in the same general area [1, 4, 5, 13, 22,24, 49]. In the present study, the two observed spawn-ing seasons may indicate a polymorphic populationarising from selection pressure for a long breedingseason in a remarkably variable environment, butwhere temperature remains favourable for reproduc-tion throughout a large part of the year. However, totest this hypothesis, further studies are needed, includ-

ing genetic intraspecific variation.

Acknowledgments

The authors wish to thank Sr Rui Marques for his assistance inthe field, and the helpful comments by an anonymous referee on anearlier version of the paper. This work was carried out while one ofus (F. Pinto) received a research studentship from JNICT (CINCIABM/3553/92).

REFERENCES

[1] Abbiati M., Cognetti-Varriale A.M., Variabilit del numero diparagnati in alcune popolazioni di Nereis diversicolorMller(Annelida, Polychaeta), Oebalia 16 (Suppl.) (1990) 311322.

[2] Arias A.M., Drake P., Distribution and production of thepolychaeteNereis diversicolorin a shallow coastal lagoon inthe Bay of Cdiz (SW Spain), Cah. Biol. Mar. 36 (1995)201210.

[3] Banse K., Mosher S., Adult body mass and annualproduction/biomass relationships of field populations, Ecol.Monogr. 50 (1980) 355379.

[4] Barnes R.S.K., Variation in paragnath number of Nereisdiversicolor in relation to sediment type and salinity regime,Estuar. Coast. Mar. Sci. 6 (1978) 275283.

[5] Barnes R.S.K., Head S.M., Variation in paragnath number insome British populations of the estuarine polychaete Nereisdiversicolor, Estuar. Coast. Mar. Sci. 5 (1977) 771781.

[6] Bartels-Hardege H.D., Zeeck E., Reproductive behaviour ofNereis diversicolor (Annelida: Polychaeta), Mar. Biol. 106

(1990) 409412.[7] Bhattacharya C.G., A simple method of resolution of adistribution into Gaussian components, Biometrics 23 (1967)115135.

[8] Boates J.S., Goss-Custard J.D., Foraging behaviour of oyster-catchers Haematopus ostralegus during a diet switch fromwormsNereis diversicolorto clamsScrobicularia plana, Can.J. Zool. 67 (1989) 22252231.

[9] Bogucki M., Rozrd i rozwj wieloszczeta Nereis diversi-color (O. F. Mller) w Baltyku. (The reproduction anddevelopment of Nereis diversicolor (O. F. Mller) in theBaltic sea), Polskie Archiwum Hydrobiol. 1 (1953) 251270(English summary).

[10] Cabral J.A., Pardal M.A., Lopes R.J., Mrias T., MarquesJ.C., The impact of macroalgal blooms on the use of the

intertidal area and feeding behaviour of waders (Charadrii) inthe Mondego estuary (west Portugal), Acta Oecol. 20 (1999)417427.

[11] Chambers M.R., Milne H., Life cycle and production ofNereis diversicolorO. F. Mller in the Ythan Estuary, Scot-land, Estuar. Coast. Mar. Sci. 3 (1975) 133144.

[12] Clay E., Literature survey of the common fauna of estuaries.1. Nereis diversicolorO. F. Mller, Marine Research Station,Brixham, Devon, UK, 1967, pp. 128.

[13] Cognetti-Varriale A.M., Caractristiques morphologiques etcologiques dune population de Nereis diversicolordes eauxsaumtres de Livourne, Cah. Biol. Mar. 14 (1973) 110.

[14] Crisp D.J., Energy flow measurements, in: Holme N.A.,McIntyre A.D. (Eds.), Methods for the Study of MarineBenthos, Blackwell, Oxford, 1971, pp. 197279.

[15] Cunha M.R., Moreira M.H., Macrobenthos of PotamogetonandMyriophyllumbeds in the upper reaches of Canal de Mira(Ria de Aveiro, NW Portugal): community structure andenvironmental factors, Neth. J. Aquat. Ecol. 29 (1995)377390.

[16] Cunha M.A., Almeida M.A., Alcntara F., Compartments ofoxygen consumption in a tidal mesotrophic estuary (Ria deAveiro, Portugal), Acta Oecol. 20 (1999) 227235.

[17] Dales R.P., The reproduction and larval development ofNereis diversicolorO. F. Mller, J. Mar. Biol. Assoc. UK 29(1950) 321360.

Table VI. Comparison of Nereis diversicolor longevity data re-corded in literature.

Site Life-span Authors(years)

Gteborg, Sweden 23 [38]Ythan estuary, Scotland 12 [11]

Norsminde Fjord, Denmark 11 [31]

Blyth estuary, England 3 [44]

Stiffky saltmarshes, England 12 [43]

Thames estuary, England 1 [18]

Severn estuary, Wales 2 [37]

Ems estuary, the Netherlands 2 [19]

Wadden Sea 1 [28]

Loire estuary, France 1 [23]

Ria de Aveiro, Portugal 2 Present study

Bou Regreg estuary, Morocco 2 [25]


Acta Oecologica


17/17

[18] Dales R.P., An annual history of a population of NereisdiversicolorO. F. Mller, Biol. Bull. 101 (1951) 131137.

[19] Essink K., Kleef H.L., Visser W., Tydeman P., Populationdynamics of the ragworm Nereis diversicolorin the Dollard(Ems Estuary) under changing conditions of stress by organicpollution, in: Gray J.S., Christiansen M.E. (Eds.), Marine

Biology of Polar Regions and Effects of Stress on MarineOrganisms, John Wiley & Sons, Chinchester, 1985, pp.585600.

[20] Fidalgo-e-Costa P., Cancela-da-Fonseca L., First data onHediste diversicolorO. F. Mller, 1776 (Annelida, Polycha-eta) in the small river of Aljezur (Southwest coast of Portu-gal), in: IX Simposio Ibrico de Estudios del Bentos Marino- Libro de Resumenes, Universidad de Alcal de Henares,1996, pp. 260261.

[21] Frances-Zubillaga G., Saiz-Salinas J.I., Ciclo de vida delpoliqueto Nereis diversicolor, in: IX Simposio Ibrico deEstudios del Bentos Marino - Libro de Resmenes, Univer-sidad de Alcal de Henares, 1996, pp. 262263.

[22] Gillet P., Variations de la distribution des paragnathes chezNereis diversicolordans lestuaire du Bou Regreg (Maroc),

Cah. Biol. Mar. 28 (1986) 481490.[23] Gillet P., Biomasse, production et dynamique des populationsdeNereis diversicolor(annlide polychte) de lestuaire de laLoire (France), Oceanol. Acta 13 (1990) 361371.

[24] Gillet P., Variation intraspcifique des paragnathes chezNereisdiversicolor (Annlides, Polychtes) de lAtlantique Nord-Est, Vie Milieu 40 (1990) 297303.

[25] Gillet P., Impact de limplantation dun barrage sur la dy-namique des populations de Nereis diversicolor (Annlidepolychte) de lestuaire du Bou Regreg, Maroc, J. Rech.Oceanogr. 18 (1993) 1518.

[26] Goss-Custard J.D., Jones R.E., Newbery P.E., The ecology ofthe Wash. 1. Distribution and diet of wading birds (Charadrii),J. Appl. Ecol. 14 (1977) 681700.

[27] Goss-Custard J.D., Warwick R.M., Kirby R., McGrorty S.,Clarke R.T., Pearson B., Rispin W.E., Le V. Dit Durell S.E.A.,Rose R.J., Towards predicting wading bird densities frompredicted prey densities in a post-barrage Severn estuary, J.Appl. Ecol. 28 (1991) 10041026.

[28] Hartmann-Schrder G., The ragwormNereis diversicolor, in:Dankers N., Khl H., Wolff W.J. (Eds.), Invertebrates of theWadden Sea, Balkema, Rotterdam, 1981, pp. 113114.

[29] Heip C., Herman R., Production ofNereis diversicolorO. F.Mller (Polychaeta) in a shallow brackish-water pond, Estuar.Coast. Mar. Sci. 8 (1979) 297305.

[30] Humphreys T.J., Production ofNereis diversicolorin an upperestuarine creek, J. Biol. Educ. 19 (1985) 141146.

[31] Kristensen E., Life cycle, growth and production in estuarinepopulations of the polychaetes Nereis virens and N. diversi-color, Holarct. Ecol. 7 (1984) 249256.

[32] Larsonneur C., La cartographie des dpots meubles sur le

plateau continental franais : mthode mise au point et utilisen Manche, J. Rech. Oceanogr. 2 (1977) 3339.

[33] Lepetit M., Loranchet S., Gillet P., Marion J.M., Un logicielde traitement des histogrammes de structure de population parla mthode des diffrences logarithmiques de Bhattacharya,Vie Milieu 41 (1991) 127131.

[34] Masero J.A., Prez-Gonzlez M., Basadre M., Otero-SaavedraM., Food supply for waders (Aves: Charadrii) in an estuarinearea in the Bay of Cdiz (SW Iberian Peninsula), Acta Oecol.20 (1999) 429434.

[35] McIntosh W.C., Notes from the Gatty Marine Laboratory, St.Andrews, No. 28. On the reproduction ofNereis diversicolor,O. F. Mller, Ann. Mag. Nat. Hist. Ser. 7 20 (1907) 176185.

[36] Mettam C., Survival strategies in estuarine nereids, in: JonesN., Wolff W.J. (Eds.), Feeding and Survival Strategies ofEstuarine Organisms, Plenum Press, 1981, pp. 6578.

[37] Mettam C., Santhanam V., Havard M.S.C., The oogenic cycleofNereis diversicolorunder natural conditions, J. Mar. Biol.Assoc. UK 62 (1982) 637645.

[38] Mller P., Production and abundance of juvenile Nereisdiversicolor, and oogenic cycle of adults in shallow waters ofwestern Sweden, J. Mar. Biol. Assoc. UK 65 (1985) 603616.

[39] Moreira F., Diet, prey-size selection and intake rates ofBlack-tailed GodwitsLimosa limosafeeding on mudflats, Ibis136 (1994) 349355.

[40] Moreira M.H., Queiroga H., Machado M.M., Cunha M.R.,Environmental gradients in a southern Europe estuarine sys-tem: Ria de Aveiro, Portugal. Implications for soft bottommacrofauna colonization, Neth. J. Aquat. Ecol. 27 (1993)465482.

[41] Morgans J.F.C., Notes on the analysis of shallow-water soft

substrata, J. Anim. Ecol. 25 (1956) 367387.[42] Mucha A.P., Costa M.H., Macrozoobenthic community struc-

ture in two Portuguese estuaries: Relationship with organicenrichment and nutrient gradients, Acta Oecol. 20 (1999)363376.

[43] Nithart M., Population dynamics and secondary production ofNereis diversicolorin a North Norfolk saltmarsh (UK), J. Mar.Biol. Assoc. UK 78 (1998) 131143.

[44] Olive P.J.W., Garwood P.R., Gametogenic cycle and popula-tion structure of Nereis (Hediste) diversicolor and Nereis(Nereis) pelagica from North-East England, J. Mar. Biol.Assoc. UK 61 (1981) 193213.

[45] Ozoh P.T.E., Jones N.V., Capacity adaptation of Hediste(Nereis) diversicolor embryogenesis to salinity, temperatureand copper, Mar. Environ. Res. 29 (1990) 227243.

[46] Rebelo J.E., The ichthyofauna and abiotic hydrological envi-ronment of the Ria de Aveiro, Portugal, Estuaries 15 (1992)403413.

[47] Smith R.I., Salinity variation in interstitial water of sand atKames Bay, Millport, with reference to the distribution of

Nereis diversicolor, J. Mar. Biol. Assoc. UK 34 (1955) 3346.[48] Smith R.I., On the distribution of Nereis diversicolor in

relation to salinity in the vicinity of Tvrminne, Finland, andthe Isefjord, Denmark, Biol. Bull. 108 (1955) 326345.

[49] Smith R.I., The reproduction ofNereis diversicolor(Polycha-eta) on the south coast of Finland - some observations andproblems, Soc. Sci. Fennica Comment. Biol. 26 (1963) 112.

[50] Smith R.I., On the early development ofNereis diversicolorindifferent salinities, J. Morphol. 114 (1964) 437464.

[51] Smith R.I., Further observations on the reproduction ofNereisdiversicolor (Polychaeta) near Tvrminne, Finland, andKristineberg, Sweden, Ann. Zool. Fennici 13 (1976) 179184.

[52] Sprung M., Macrobenthic secondary production in the inter-tidal zone of the Ria Formosa a lagoon in Southern Portugal,Estuar. Coast. Shelf Sci. 38 (1994) 539558.

[53] Zwarts L., Esselink P., Versatility of male curlewsNumeniusarquatapreying uponNereis diversicolor: deploying contrast-ing capture modes dependent on prey availability, Mar. Ecol.Prog. Ser. 56 (1989) 255269.


Vol. 20 (4) 1999

ecologia de n. diversicolor no estuário do mira (aveiro)

Documents