Reproduction, Population Dynamics and Production of Nereis Falsa (Nereididae: Polychaeta) on the Rocky Coast of El Kala National Park, Algeria

Helgol Mar Res (2011) 65:165–173 DOI 10.1007/s10152-010-0212-5

ORIGINAL ARTICLE

Reproduction, population dynamics and production of Nereis falsa (Nereididae: Polychaeta) on the rocky coast of El Kala National Park, Algeria

Tarek Daas • Mourad Younsi • Ouided Daas-Maamcha • Patrick Gillet • Patrick Scaps

Received: 8 January 2010 / Revised: 1 July 2010 / Accepted: 2 July 2010 / Published online: 18 July 2010 Ó Springer-Verlag and AWI 2010

Abstract The polychaete Nereis falsa Quatrefages, 1866 N. falsa was 1.45 g m-2 year-1, and the production/bio- is present in the area of El Kala National Park on the East mass ratio was 1.07 year-1. coast of Algeria. Field investigations were carried out from January to December 2007 to characterize the populations’ Keywords Nereididae Á Population dynamics Á reproductive cycle, secondary production and dynamics. Production Á Reproduction Reproduction followed the atokous type, and spawning occured from mid-June to the end of August/early September when sea temperature was highest (20–23°C). Introduction The diameter of mature oocytes was approximately 180 lm. Mean lifespan was estimated to about one year. In The polychaete Nereis falsa Quatrefages, 1866 has a wide 2007, the mean density was 11.27 ind. m-2 with a mini- geographical distribution. This species has been recorded mum of 7.83 ind. m-2 in April and a maximum of 14.5 ind. along the coast of the Atlantic Ocean [Atlantic coast of m-2 in February. The mean annual biomass was Morocco (Fadlaoui and Retie`re 1995), Namibia (Glassom 1.36 g m-2 (fresh weight) with a minimum of 0.86 g m-2 and Branch 1997) and South Africa (Day 1967), North in December and a maximum of 2.00 g m-2 in June. The American Atlantic coast (Posey et al. 2002, 2006), Florida population consisted of two cohorts distinguishable from Bay (Vittor 1997a, 1998), north coast of the Gulf of size frequency distributions. One cohort corresponded to Mexico (Vittor 1984), Galveston Bay in the Gulf of Texas the recruitment of 2006 and the other appeared during the (Vittor 1997b), north-east coast of Venezuela (Arana and study period in September 2007. The annual production of Diaz 2006), Colombian Caribbean coast (Baez and Ardila 2003)] and the Mediterranean Sea [Alge´siras Bay in Spain (Sanchez-Moyano et al. 2001), Cueta harbour in Morocco Communicated by H.-D. Franke. (Guerra-Garcia et al. 2003; Guerra-Garcia and Garcia- Gomez 2004), Circeo National Park on the Italian Adriatic T. Daas Á M. Younsi Á O. Daas-Maamcha coast (Andrea and Giancarlo 2003), Izmir Bay/Turkey Laboratoire de Biologie Animale Appliqueé, (Ertan Ç inar et al. 2008), on floating debris in the Liguran De´partement de Biologie, Faculte´ des Sciences, Universite´ Badji Mokhtar, 23 000 Annaba, Algeria Sea (Alliani and Meloni 1999) and on current metre moorings deployed in the Corsica Channel (Alliani and P. Gillet Meloni 1999)]. Moreover, this species lives as epibiont on Centre d’Etude et de Recherche sur les Ecosyste`mes Aquatiques, loggerhead turtles (Caretta caretta) nesting on the coast of Institut de Biologie et d’Ecologie Appliqueé, UCO, 44, rue Rabelais, Angers, France Georgia, USA (Pfaller et al. 2006), and on mussels Mytilus galloprovincialis in Izmir Bay, eastern Mediterranean P. Scaps (&) (Ertan Ç inar et al. 2008). The species is a facultative rafter; Laboratoire de Biologie Animale, i.e. it typically lives in benthic habitats but may become Universite´ des Sciences et Technologies de Lille, 59655 Villeneuve d’Ascq Ce´dex, France dispersed while being associated with floating items (Thiel e-mail: [email protected] and Gutow 2005). 123 166 Helgol Mar Res (2011) 65:165–173

level, using the diagnostic patterns of paragnaths on the proboscis, worms were made to evert their proboscis by generating pressure some distance behind the head. The number of collected specimens varied between 47 in April and 87 in February. A total of 812 worms were collected and examined. At each sampling date, air and sea water temperature were recorded.

Reproduction

For the study of the reproductive cycle, the individuals were fixed in the laboratory with 8% neutral formalin and Fig. 1 Study area and location of sampling station examined for the presence sexual products in the coelom. A short incision was made in the body wall at about the twentieth chaetigerous segment and a drop (*1 ml) of the A preliminary study of the species’ distribution on the coelomic fluid was taken out with a Pasteur pipette and Algerian east coast (between Skikda and El Kala, (Fig. 1) examined under a binocular microscope. If possible, forty revealed its presence only in the area of El Kala National oocytes each were measured using a calibrated eye piece Park. The reproductive biology and population dynamics of graticule. The longest and the shortest diameter of oocytes this species are poorly documented. So, this study was were determined, and the average value was used as an conducted to obtain information on the cycle of repro- estimate of oocyte size. duction, secondary production and dynamics of a population of N. falsa on a rocky shore on the Algerian east coast (Mediterranean Sea). This work is part of a research pro- gramme dedicated to the identification of indicator species Population dynamics of pollution on the Algerian east coast (Abdenour et al. 2000, 2004; Bouzeraa et al. 2004; Beldi et al. 2006; Sifi After species identification, the fresh weight of each indi- et al. 2007). vidual was measured. Weight frequency histograms were treated by FISAT II FAO software, which is used for the identification of parameters of a mixture of distributions Materials and methods (Gayanilo et al. 2005) and replaces the methods based on the analysis of modes of histograms (Gayanilo et al. 1988; Study site and collection of material Gayanilo and Pauly 1989). The secondary production (P) was estimated by the method of Crisp (1971) using the Individuals were collected in the area of El Kala National equation P = (Nt1 ? Nt2)/2(Wt2 - Wt1) with Nt1 and Nt2 Park, Algerian east coast. Worms were found among red representing numbers of individuals in a cohort at times t1 algae covering hard bottoms. Rocks are metamorphic and and t2 and Wt1 and Wt2 representing the mean fresh are composed of gneiss and quartzite. The maximum tide is weights of a cohort at times t1 and t2. The secondary pro- small (0.9 m). duction and the production/biomass ratio (P/B) were cal- Individuals were collected monthly from January to culated for the year 2007. December 2007. The region sampled corresponded with the area of greatest density of individuals. The individuals occur in the lower intertidal zone and extend down into the Results subtidal. We used bleaching liquid (10% in sea water) to force individuals out of their algal mats in order to obtain Temperature at the study site (Fig. 2) undamaged whole individuals. Approximately 6 m2 of hard bottom has been monitored each month in order to collect During the study period from January to December 2007, enough individuals for the population dynamics study. air temperature varied between 10°C in December and In our study site, N. falsa coexists with two other species 34°C in August (average: 21.08 ± 9.40°C). Sea water of nereidid polychaetes, Perinereis cultrifera and Platy- temperature measured during low tide ranged between 8°C nereis dumerilii. For a correct identification to species in January and 23°C in August (average: 16.08 ± 5.01°C).

123 Helgol Mar Res (2011) 65:165–173 167

40 Reproductive biology 35

30 Cœlomic punctures of each female showed a homogeneous C) ° aspect with oocyte diameters being appreciably equal. 25 Thus, ovogenesis was considered to be synchronous. The 20 mean oocyte diameter frequency histograms of individuals 15 collected from January to December 2007 are shown in

Temperature ( 10 air Fig. 3. Most of the histograms are unimodal and can be 5 sea-water considered to show a single cohort. 0 The study of the changes in average oocyte diameters (Fig. 4) allowed us to reveal the female sexual cycle. The July June May April March

August mean oocyte diameter varied between 42.44 ± 11.19 lm January October February December November September in September and 166.27 ± 16.06 lm in August. From Months January to May, the mean oocyte diameter ranged between 80 and 100 lm. We recorded a steady increase of the mean Fig. 2 Monthly sea water and air temperature in the studied area oocyte diameter from May to July, with maximal mean

100 100 100 100 April January February March 80 80 80 80

60 60 60 60

40 40 40 40

20 20 20 20

0 0 0 0 0-20 0-20 0-20 0-20 20-40 40-60 60-80 20-40 40-60 60-80 20-40 40-60 60-80 20-40 40-60 60-80 80-100 80-100 80-100 80-100 100-120 120-140 140-160 160-180 180-200 200-220 100-120 120-140 140-160 160-180 180-200 200-220 100-120 120-140 140-160 160-180 180-200 200-220 100-120 120-140 140-160 160-180 180-200 200-220

100 100 100 100 May June July August

80 80 80 80

60 60 60 60

40 40 40 40 Percentage 20 20 20 20

100 100 100 100 September October November December 80 80 80 80

60 60 60 60

40 40 40 40

20 20 20 20

Fig. 3 Size distribution frequency of oocytes between January and December 2007 123 168 Helgol Mar Res (2011) 65:165–173 values of 155 lm. The first mature oocytes (diameter autumn and winter (October to February) (Fig. 6), reflect- greater than 160 lm) occurred in the cœlomic fluid of ing the mortality of adults and recruitment of juveniles. females collected in mid-June. From July to August, oocyte The temporal variation in biomass is largely explained by growth was weak and the mean oocyte diameter became the variation in mean individual fresh weight. maximal (166.27 lm). The coelomic fluid of females collected in early August contained a majority of large oocytes A 15 (diameter between 120 and 200 lm) (Fig. 3), while the coelomic fluid of females collected in September contained ) -2 only small oocytes indicating that the spawning period was 10 finished. So, the spawning season begins in mid-June and spreads out until the end of August or early September. From September to December, the mean oocyte diameter 5 ranged between 40 and 60 lm and remained relatively Density (ind. m constant. Oocytes took less than one year to develop fully (Fig. 4). 0 During the whole study period, we did not find large July June May April March August

mature males or females showing morphological modiﬁ- January October February December November cations characteristic of epitoky. In consequence, individ- September uals seem to reproduce exclusively in the atokous state and Months neither of sex appears to survive spawning. A comparison B 2,5 of Figs. 2 and 4 shows that spawning occurs when sea

water surface temperature is highest (20–23°C). ) 2,0 −2

Population dynamics 1,5

The mean density and biomass of N. falsa, at the study site 1,0 between January and December 2007, were 11.27 ± 2.09 Biomass (g. m 0,5 ind. m-2 and 1.36 ± 0.38 g m-2, respectively. From one month to another, N. falsa density and biomass varied 0,0 considerably (Fig. 5a, b). Nevertheless, the biomass tended July May June April March to be higher in summer than in winter (Fig. 5b), with the August January October -2 February December November highest value recorded in June (B = 2gm ) and the September lowest in December (B = 0.86 g m-2). Months The mean individual fresh weight was maximal during Fig. 5 Temporal variations in the density (ind. m-2)(a) and in the spring and summer (March to August). It decreased at the biomass (fresh weight g m-2)(b) of the studied population of Nereis end of summer (September) and was minimal during falsa at El Kala, Algeria

0,20 200

175 0,15 150

125 0,10 100

Body weight (g) 0,05 50

Oocyte diameter (µm) 25 0,00 0 July May June April March August January July October June May April February March December November September August January October February December November September Months Months Fig. 6 Changes in the mean individual fresh weight from January to Fig. 4 Changes in oocyte size from January to December 2007. Each December 2007. Each data point represents mean ± standard error of data point represents mean ± SD of the mean the mean 123 Helgol Mar Res (2011) 65:165–173 169

Recruitment pattern and the appearance of another cohort (C2). This cohort could be followed for the rest of the sampling period The weight frequency histograms of N. falsa collected into December. It corresponded to a new generation of from January to December 2007 are shown in Fig. 7. individuals (0-group; i.e. individuals hatched during Two cohorts (C1,C2) can be distinguished. One cohort the sampling year) which had just settled in the study (C1) could be followed over eight months from January area. This cohort was represented by females with to August 2007. This cohort represents the older (I-group) small oocytes ranging from 30 to 70 lm in diameter in individuals. Its members showed a progressive increase September. All frequency histograms showed a unimodal in mean individual weight from January to August distribution (Fig. 7). (Fig. 6). During summer, this cohort was well repre- Growth curves (Fig. 8) have been constructed using the sented by large females with large oocytes ranging from means of fresh weight for each cohort shown in Fig. 7. 140 to 190 lm in diameter in August. In September, the The mean lifespan was estimated to be one year using the mean individual weight decreased, related to the disap- appearance and disappearance of modes in the cohort pearance of the large individuals after reproduction (C1) analysis.

80 80 80 80 January February March April 70 N = 63 70 N = 87 70 N = 58 70 N = 47 60 60 60 60 50 50 50 50 40 40 40 40 30 30 30 30 20 20 20 20 10 10 10 10 0 0 0 0 0-0.05 0-0.05 0-0.05 0-0.05 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35

80 May 80 80 80 June July August 70 N = 61 70 N = 82 70 N = 70 70 N = 72 60 60 60 60 50 50 50 50 40 40 40 40 30 30 30 30 20 20 20 20 10 10 10 10 Number of individuals 0 0 0 0 0-0.05 0-0.05 0-0.05 0-0.05 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35

80 80 80 80 September October November December 70 N = 82 70 N = 62 70 N = 76 70 N = 52 60 60 60 60 50 50 50 50 40 40 40 40 30 30 30 30 20 20 20 20 10 10 10 10 0 0 0 0 0-0.05 0-0.05 0-0.05 0-0.05 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 0.05-0.10 0.10-0.15 0.15-0.20 0.20-0.25 0.25-0.30 0.30-0.35 Weight (g) Weight (g) Weight (g) Weight (g)

Fig. 7 Weight frequency histograms of Nereis falsa at El Kala between January and December 2007 123 170 Helgol Mar Res (2011) 65:165–173

0,18 Data on the species’ mode of reproduction are very scarce 0,16 and based on old and incomplete observations. To our 0,14 knowledge, the present study is the ﬁrst providing on the 0,12 life cycle of N. falsa. Fauvel (1923) stated that the species 0,10 reproduces in an epitokous state. However, ecological 0,08 plasticity in the mode of reproduction has been observed

Weight (g) 0,06 for several species of polychaetes and particularly for 0,04 nereidid polychaetes (see review by Giangrande 1997). For C1 0,02 C2 example, individuals of Perinereis cultrifera reproduce 0,00 with or without the morphological modiﬁcations which are July June May characteristic of epitoky depending on geographical origin. April March August January October

February This species is particularly interesting since it occupies the December November September Months same habitat as N. falsa (rocky shores) and is present in our study site. The reproduction of P. cultrifera in the English Fig. 8 Growth curves of the cohorts of Nereis falsa at El Kala Channel and the French Atlantic coast is of an epitokous between January and December 2007 type and has been observed from May to June and some- times July (Fauvel 1916; Herpin 1925; Fage and Legendre Production estimates 1927; Durchon 1951; Cazaux 1965; Scaps et al. 1992). In the Arcachon Basin (Cazaux 1965) and on the north coast Estimates for the production by the two cohorts of N. falsa of Brittany, P. cultrifera (Scaps et al. 1992) has a 3-year during the study period are shown in Table 1. The annual lifespan. Along the Atlantic coast of El Jadida (Morocco), secondary production in 2007 was P = 1.45 g m-2 year-1 the reproduction of P. cultrifera is of an atokous type and at a mean annual biomass of B = 1.36 g m-2. Thus, the spawning occurs from April until the end of May (Rouhi ratio P/B amounted to 1.07 year-1. et al. 2008). In the Mediterranean Sea, mature specimens are atokous in Marseille (Peres and Rancurel 1948) and on the west coast of Algerian in the Bay of Algiers (Durchon Discussion 1957; Marcel 1962; Rouabah et al. 2008). In the Bay of Algiers, the lifespan of the species probably does not The reproduction of N. falsa in the El Kala National Park exceed two years and the reproductive period spans most of (Mediterranean, eastern Algeria) follows the atokous type. the year, but reproduction is most intense in spring from Table 1 Secondary production of the cohorts of the population March to May (Rouabah et al. 2008). Reproduction of P. cultrifera is of an epitokous type in the Venice lagoon in Cohort Wt Wt2 - Wt1 Nt Nt1 ? Nt2/2 Production Italy (Ansaloni et al. 1986), at Salammboˆ near Tunis (g for 6 m2) (Zghal and Ben Amor 1989) and at Annaba on the east January 0.095 – 63 – – coast of Algeria near the Tunisian border (Rouabah and February 0.108 0.013 87 75 0.975 Scaps 2003a). At Annaba, P. cultrifera has a 3-year life- March 0.135 0.027 58 72.5 1.957 span and spawning occurs in late April/early May (Roua- April 0.130 -0.005 47 52.5 -0.262 bah and Scaps 2003a, b). The existence of two modes of May 0.132 0.002 61 54 0.108 reproduction in this species (atoky and epitoky) led Marcel June 0.147 0.015 82 71.5 1.072 (1962) and Zghal and Ben Amor (1989) to split the species July 0.165 0.018 70 76 1.368 into two physiologically different subspecies (‘‘races’’), August 0.149 -0.016 72 71 -1.152 while the observations of Scaps et al. (2000), Roubah and Total C1 4.066 Scaps (2003b) and Roubah et al. (2009) indicated that September 0.083 0.083 82 41 3.403 ‘‘P. cultrifera’’ may represent a complex of species. October 0.100 0.017 62 72 1.224 Our study showed that N. falsa from the coast of El Kala November 0.105 0.005 74 68 0.340 has a synchronous oogenesis. Similar results have been December 0.100 -0.005 52 63 -0.315 obtained for other species of nereidid polychaetes such as Total C2 4.652 P. cultrifera (Rouabah and Scaps 2003a) and Platynereis Total 8.718 dumerilii (Fischer and Dorresteijn 2004). In contrast, Zribi et al. (2007) showed that Perinereis macropus from the Wt mean weight variation of a cohort between t and t , Wt and Wt 1 2 1 2 Gulf of Gabes (Tunisia) has an asynchronous oogenesis, mean fresh weights of a cohort at times t1 and t2, Nt number of individuals in a cohort at times t, Nt1 and Nt2 numbers of individuals with the female individual bearing oocytes of quite dif- in a cohort at times t1 and t2 ferent diameters. 123 Helgol Mar Res (2011) 65:165–173 171

Table 2 Comparison of the production/biomass ratio (P/B) in some species of polychaetous annelids Family Species P/B Site Authors

Arenicolidae Arenicola marina 1.14 Grevelingen estuary, North Sea Wolff and Wolff (1977) Nephthyidae Nephthys hombergii 1.9 Lynher estuary, English Channel Warwick and Price (1975) Nereididae Nereis diversicolor 3.9–4.6 Bou Regreg, Morocco Gillet (1993) Nereis diversicolor 1.7–1.9 Oued Souss, Morocco Aı¨t Alla et al. (2006) Nereis falsa 1.07 El Kala, Algeria Present work Perinereis cultrifera 2.3 El Jadida, Morocco Rouhi et al. (2008) Owenidae Owenia fusiformis 0.89 English channel Me´nard et al. (1989) Spionidae Scolelepis squamata 2.0 Morocco Bayed et al. (2006)

Data on the reproductive biology of nereidid polychae- for Owenia fusiformis in the English Channel (0.89 year-1) tes from the east coast of Algeria and the coast of Tunisia and Arenicola marina in the North Sea (1.14 year-1) but is are very scarce. Nevertheless, Rouabah and Scaps (2003a) lower than those for polychaete worms from North Africa studied the life cycle and population dynamics of P. cul- (e.g. P/B = 2.3 year-1 for P. cultrifera on the Atlantic trifera in the area of Annaba, about 30 km west to our coast of El Jadida, Morocco; Rouhi et al. 2008). study site. It should be noticed that we did not find individuals of N. falsa in the site studied by Roubah and Scaps in (2003a, b), while these two species co-occur on the coast References of El Kala. Nereis falsa has smaller mature oocytes (diameter of Abdenour C, Smith BD, Boulakoud MS, Samraoui B, Rainbow PS 160–210 lm, mean 165 lm) than P. cultrifera (diameter (2000) Trace metals in marine, brackish and freshwater prawns from 220 to, mean 250 lm). The reproductive period of from north-east Algeria. Hydrobiologia 432:217–227 P. cultrifera is short and spawning occurs from the end of Aı¨t Alla A, Gillet P, Deutsch B, Bergayou H, Moukrim A (2006) April to early May; that of N. falsa is longer with spawning Respones of Nereis diversicolor (Polychaeta, Nereididae) populations to reduced wastewater discharge in the polluted estuary occurring from the end of July to early September. of oued Souss, bay of Agadir, Morocco. Estuar Coast Shelf Sci Oogenesis in P. cultrifera takes 16 months, while that in 70:633–642 N. falsa takes less than one year. So, these two co-occur- Alliani S, Meloni R (1999) Dispersal strategies of benthic species and ring nereids show clear differences in reproductive traits. water current variability in the Corsica Channel. Scientia Marina 63:137–145 The reproductive season of P. macropus stretches from Andrea P, Giancarlo MJ (2003) La Fauna del Parco Nazionale del March to June in the Gulf of Gabes in Tunisia, and mature Circeo. Progetto ‘‘Parchi in qualita`’’ ovvero ‘‘applicazione pilota oocytes range between 220 and 300 lm in diameter with del Sistema di Gestione Ambientale nelle aree naturali protette’’. a mean of 250 lm (Zribi et al. 2007). In contrast to ENEA, pp 1–81 Ansaloni L, Pellizzato M, Zunarelli-Vandini R (1986) Policheti di P. cultrifera and P. macropus, which reproduce in spring interessse economiconella laguna di Venezia. Nova Thalassia at rising sea water temperature, N. falsa reproduces in 8:641–642 summer when sea water temperature is at its maximum. Arana IL, Diaz OD (2006) Polychaeta (Annelida) associated with In our study site, there are three species of nereids Thalassia testudinum in the northeastern coastal waters of Venezuela. Rev Biol Trop Int J Trop Biol Conserv 54:971–978 co-occurring in the same habitat (N. falsa, P. cultrifera and Baez D, Ardila NE (2003) Polychaetes (Annelida: Polychaeta) of the P. dumerilii) but only the life cycles of N. falsa and Colombian Caribbean. Biota Colomb 4:89–109 P. cultrifera have been investigated in this area. The life Bayed A, Cherkaoui F, Gle´marec M (2006) Population dynamics of cycle of P. dumerilii, well known from some other geo- Scolelepis squamata (Annelida: Polychaeta) from a Northwest African beach. Cah Biol Mar 47:143–155 graphical locations, remains to be studied for the coast of Beldi H, Gimbert F, Maas S, Scheiffer R, Soltani N (2006) Seasonal El Kala in order to compare all three species with respect variations of Cd, Cu, Pb and Zn in the edible mollusc Donax to their reproductive characteristics. trunculus (Mollusca, Bivalvia) from the gulf of Annaba, Algeria. The values of the mean annual biomass (B = 1.36 g Afr J Agr Res 1:85–90 -2 -1 Bouzeraa N, Abbes A, Soltani N (2004) Analyse des proteínes chez m year ) and the secondary production (P = 1.45 g trois espe`ces de bivalves vivant dans des milieux diffe´rents, la m-2)ofN. falsa at El Kala National Park are among the lagune El Mellah et le golfe d’Annaba. Bull INSTM 9:97–100 lowest recorded for polychaetes. The known P/B ratios of Cazaux C (1965) Evolution de Perinereis cultrifera (Grube) au cours polychaete worms range between 0.89 and 4.6 year-1 d’un cycle annuel a` Arcachon. Soc Linn Bord 101:1–18 -1 Crisp D (1971) Energy flow measurements. In: Holme NA, Mc Intyre (Table 2). The P/B ratio value of 1.07 year for the AD (eds) Methods for the study of marine benthos. Blackwell, N. falsa population of El Kala is similar to those reported Oxford, pp 197–279

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