P.S.Z.N. I: Marine Ecology, 14 (4): 313-327 (1993) 0 1993 Paul Parey Scientific Publishers, Berlin and Hamburg ISSN 0173-9565

Accepted: May 5 , 1993

Life Cycle, Growth and Secondary Production in a Brackish-Water Population of the Polychaete Notomastus latericeus (Capitellidae) in the Mediterranean Sea ADRIANA GIANGRANDE' & SIMONETTA FRASCHETTI~

1 Dipartimento di Biologia, Universith degli Studi di Lecce, 1-73100 Lecce, Italy. 2 Istituto di Scienze Ambientali Marine, Universith di Genova, 1-16038

S. Margherita Ligure (GE), Italy.

With 8 figures and 1 table

Key words: Notomastus latericeus, life cycle, growth, secondary production, environ- mental variability.

Abstract. Three years of observations on a population of Notomastus latericeus SARS from Acquatina lagoon (Lecce, Italy) are reported. The population dynamics, life cycle, and reproduc- tion were investigated in order to explain periodic density variations of this species. Some physical parameters of the water column were measured and sediment analyses were performed to charac- terize the environment. Secondary production was also estimated as part of a functional study of the benthic system in the Acquatina lagoon. The species is opportunistic; its density is apparently correlated to variation in salinity, but its presence in the lagoon is dependent on recruitment success and competition with other polychaete species.

Problem

During a study of polychaete distribution and community dynamics carried out in the Acquatina lagoon (west coast of the Adriatic Sea, Lecce, Italy), the species Notomastus lutericeus SARS was found to be one of the most common taxa, even though in some periods it was confined to well-defined patches. The opportunity was therefore taken to study the life cycle and reproduction of the species within this area in order to clarify its temporal variation in abundance. Moreover, the estimate of its secondary production provides a quantitative basis for functional studies of the benthic system in the Acquatina lagoon.

Notomastus latericeus is a burrowing polychaete of the family Capitellidae, one of the best known families from the reproductive point of view, especially for the Capitella complex (DAY, 1937; BOOKHOUT, 1957; GRASSLE & GRASSLE, 1974; 1976; ECKELBARGER & GRASSLE, 1982; OYENEKAN, 1983; GEORGE, 1984;

U.S. Copyright Clearance Center Code Statement: 0173-9565/93/1404-0313$02.50/0

314 GIANGRANDE & FRASCHETTI

GRBMARE et ul., 1989). In addition, Capitellidue typically have a fast growth rate and a great ability in colonizing unpredictable environments (GRASSLE & GRASSLE, 1976; GRAY, 1989).

Notomasfus lutericeus is widely distributed in the Mediterranean as well as in extramediterranean areas, mainly on muddy sediments (GRAVINA & SOMA- SCHINI, 1990). Few works on its life cycle are available: larval development and substrate selection have been studied by WILSON (1933; 1937), and reproduction was investigated by GUBRIN & MASSB (1974), but there has been no comprehen- sive study of its autoecology.

Material and Methods

The investigated area is a brackish-water coastal environment, with a mean depth of two meters. It is connected with the sea by a southern channel, while a freshwater in5ow is located in the northern area (Fig. 1). After a previous survey conducted on the whole lagoon, a first station was selected and sampled monthly between February 1989 and February 1992. At this site (A), N . lutericeus was abundant from April 1990 to July 1991. After this period, the species disappeared from site A and sampling was continued at a second site (B) where the species remained abundant until December 1991.

Sampling was performed at water depth of 50cm using a quadrat of 50cm X 50cm and digging the sediment to a depth of lOcm (about 40 1 of sediment). The samples were washed through a 1 mm sieve and the retained material was preserved in an 8 % formalin solution. In addition, in the area surrounding the sites, plankton samples were collected weekly at about 1 metre from the bottom by filtering 2m3 with a net of 7 0 p mesh.

Notomastus lutericeus specimens were carefully sorted in the laboratory. Fragments bearing the prostomium were counted, and the density was expressed as individual .m-2. About ten live specimens were examined on each sampling date to evaluate sexual maturity.

For the population dynamics study, all specimens were measured using a stereomicroscope. Due to the difficulty of collecting specimens having an entire abdomen, size-frequency histograms were constructed on thorax length; this allowed the separation of different classes. All specimens were cut at the junction between thorax and abdomen. Biomass values were estimated separately for thoraces and for abdominal fragments, taking into consideration those parts already present in each sample. reweighed. The ash-free dry weight (AFDW) of each group was ascertained and secondary

500 m

Fig. 1. Study area with the two sampling sites.

Life-history pattern of Notomustus lutericeus 315

production was estimated for the population according to CRISP (1972) for stocks with recognizable recruitment and separable age-classes.

During 1991 a total of 4 additional samples were taken seasonally at both sites (A and B) for granulometric sediment analysis using the dry sieve technique, and for TOM (Total Organic Matter) evaluation; the latter was expressed as percentage and determined by ignition of sediment at 450°C for 2 h.

Results

1. Physical parameters

During three years of observations, the temperature (Fig. 2 a) showed an annual cyclic trend, ranging between 10 and 32°C. Salinity, on the other hand, fluctuated irregularly (Fig.2b), with a clear decrease toward the end of the

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316 GIANGRANDE & F R A S C H E ~

study period to 6 %O because of the obstruction of the connection with the sea. During 1990, strong storms obstructed the freshwater channel, causing a salinity increase up to 40X in July.

The sand content of the sediment was consistently high at both sites; in site A (fraction > 0.21 mm = 50 % ; fraction > 0.13 mm = 40 %), sedimentary condi- tions did not vary appreciably in time, while in site B a local sedimentary instability was present (fraction > 0.21 mm ranging from 23 YO to 52 'YO ; fraction > 0.13 mm ranging from 23 YO to 70 %).

The annual TOM mean was higher in site A than in site B (2.1 'YO vs. 1.7 YO).

2. Reproduction and larval development

Notomastus latericeus is a gonochoric species. In males, gametes are released within the coelom at early stages of development. Oogenesis is intraovaric. The ovaries lie in the abdomen (Fig. 3 a, b).

Mature eggs were about 150pm in diameter and developed into lecitho- trophic larvae. In 1990 and 1991, larvae were present in the water column from late December to February, showing a peak abundance in February. Mean

Fig. 3. a. Notomustus lutericeus: abdomen segments of a ripe female. Lateral view. o = ovary, s = sediment in the gut; b. eggs of N . lutericeus from a female collected in January; c. N . lutericeus: detail of an ovary from a female collected in December showing eggs at different stages of maturity.

Life-history pattern of Notomasm latericeus 317

larval density in plankton samples was higher in 1990 than in 1991 (60 individ- uals . m-3 vs. 30 indiv. . m-”. However, larval abundance was probably underestimated because, in the laboratory, larvae exhibited a demersal behaviour during all the stages. The difficulty in obtaining N . lutericeus larvae from plankton was already pointed out by GUBRIN & MASS& (1974).

Some larvae, collected in the plankton in February 1990 at the trochophora stage (about 2 days old), were reared in the laboratory. Larval developmental phases (Fig. 4a, b) were similar to those described by WILSON (1933) for a population from Plymouth. Metamorphosis occurred after five days, and within two weeks the worms developed eight thoracic chaetigers (Fig. 4c). As in other capitellids, ontogenetic setal changes occurred in thorax segments (FREDEITE, 1982; GEORGE, 1984). At metamorphosis, specimens had three chaetigerous segments bearing capillary setae in the thorax; the final configuration (11

Fig. 4. Developmental stages of Notomastus latericeus. a. three-day stage; b. five-day stage, just before metamorphosis; c. juvenile after 15 days.

318 GIANGRANDE & FRASCHET~

thoracic chaetigers with capillary setae) was reached only after two months of benthic life. The thorax length of individuals reared in the laboratory from February to April 1990 was similar to the length of juveniles collected in the benthos in April 1990 (about 2.5 mm).

3. Abundance and distribution of Notomastus latericeus within the lagoon

Polychaete distribution was assessed from a previous survey conducted in the whole lagoon during the year 1989 (GIANGRANDE, unpubl. data).

In most of the area, N. lutericeus was almost absent and the dominant species was Nuineris luevigutu GRUBE (GIANGRANDE & PETRAROLI, 1991). The site A was chosen as representative of this situation. Here, most of the other polychaete species living in the lagoon were present together with N. 1uten'ce.w.

During 1989, N . lutericeus was confined to some patches together with a few other species, especially Spionidue. One of these patches was site B.

Site A: Notomustus lutericeus was very rare throughout 1989. A great increase in density was observed from April to July 1990, followed by a sharp decrease. A second peak occurred during the summer of 1991 , followed by the disappear- ance of the species in September (Fig. 5, solid line).

Site B: No quantitative data are available for 1989 and 1990. N. lutericeus' presence here was observed only in qualitative samples. The spawning events of 1990, were followed at this site. During this year, recruitment occurred success- fully all over the lagoon.

In 1991, despite its disappearance in site A, the species remained abundant, with a September peak comparable in density to that noted in site A during summer 1990 (Fig. 5, broken line).

In February 1992, all polychaete species disappeared from the whole lagoon. The cause of this phenomenon is still under investigation.

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F M A M J J S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F

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Fig.5. Abundance (number of individuals) of Notomastus latericeus during the three year study period. Broken line refers to site B.

Life-history pattern of Notomustus latericeus

4. Population dynamics

319

Figure 6 shows the size-frequency histograms computed on thorax length. In April 1990, young worms appeared as a result of larval settlement.

Recruitment, as shown in the histograms, is based on the portion of individuals retained on the 1 mm sieve and is no doubt an underestimate.

From April 1990 to March 1991 the growth of a single cohort was easy to follow. In March 1991 a second recruitment was observed. In this month, young

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Fig. 6. Frequency histogram of Notomastus lutericeus population computed on thorax length. They refer to the actual number of collected individuals. Empty histograms of September and December 1991 are relative to site B.

320 GIANCRANDE & FRASCHEITI

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Fig.7. Thorax length increment of Notomasfus lutericeus in time; broken lines refer to site B. Drawing showing the measured part of the animal.

classes (0-age class) were present together with a few surviving adults (1-age class) of the previous year.

In both years, after successful recruitment, rapid growth was observed from spring to summer. During 1990, growth could be followed until December. This was not possible for 1991 due to an earlier mortality in July.

The histograms of the last two months (September and December 1991, Fig. 6) are based on site B, where the N . lutericeus population remained con- fined after July 1991.

The thorax length increment is summarized in Fig. 7. The mean thorax length over the whole period was 6.7 mm.

5. Biomass and production

The biomass trend (AFDW) (Fig. 8 a) of site A followed the pattern described for density (Fig.5) throughout both 1990 and 1991. At this site, biomass increased from April to July 1990, followed by a drastic decrease from Sep- tember 1990 to March 1991. A second biomass increase was observed between March and June 1991, followed by a rapid decrease in July (earlier than in the previous year). As with abundance (Fig. 5) , September and December 1991 samples refer to site B. Here, the abundance peak was less pronounced than the density increase.

Thorax and abdomen weights were highly correlated (r = 0.95, n = 14). The estimate of weight, obtained separately for the abdomens and for the thoraces, showed that the percentage of ash present in these two parts of the animal differed. The thorax organic content was about 90% of the dry weight, while the abdomen organic content was variable, ranging from 36 to 51 % .

Life-history pattern of Notornustus latericeus 321

a

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months - total biomass abdomen biomass _*- thorax biomass

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Fig. 8. Trend of Notornustus lutericeus biomass. a. Total biomass (g AFDW . m-z) for entire worms, thoraces, and abdomens. b. Mean individual weight (total biomass/number of individuals) for entire worms, thoraces, and abdomens. Broken lines refer to site B.

Figure 8 b shows mean biomass values related to total worms, thoraces, and abdomens. In 1990 it was possible to determine the mean growth rate. In the following year, a similar trend was observed only until July. The mean biomass values for site A were 1.09g (AFDW) . m-2 for the period from April 1990 to March 1991, and 1.08g . m-2 from March to July 1991.

Comparing the two winter periods (1990 and 1991), mean growth was apparently higher in site A than in site B (0.007g vs. 0.004g).

Total annual production at site A could only be computed for the period April 1990 to March 1991, corresponding to one cohort growth. The estimated secondary production value was 1.9g . m-2 * a-l. The P : B ratio was 1.7 (Tablel). In 1991, the earlier heavy mortality at this site only allowed the

322 GLANCRANDE & FRASCHETTI

Table 1. Secondary production of N o t o m h u latericeus.

sampling density mean indiv. biomass average weight production date (n . m-z) weight (mg) (g . m-z) value increment (g . m-2)

of density (mg)

04.04.90 159 1.8 0.291 0.290 23.05.90 477 2.3 1.099 318 0.5 0.159 25.06.90 576 4.2 2.397 526.5 1.9 1.OOO 26.07.90 573 4.5 2.557 574.5 0.3 0.172 19.09.90 429 4.1 1.780 501 - 0.4 - 0.200 17.10.90 114 5.8 0.536 271.5 1.7 0.462 18.12.90 114 6.9 0.665 114 1.1 0.125 13.02.91 60 5.4 0.323 87 - 1.5 - 0.131 14.03.91 15 2.2 0.090 37.5 0.6 0.023

total: 2517 9.738 1.900 P:B 1.7

14.03.91 36 2.1 0.077 0.077 20.05.91 261 2.6 0.684 148.5 0.5 0.074 07.06.91 480 5.1 2.438 370.5 2.5 0.926

total: 984 4.152 0.906 26.07.91 207 4.6 0.953 343.5 - 0.5 - 0.172

P:B 0.8

computation of production until July. Comparing the same periods (March- July) the production was higher in 1990 (1.6 vs. 0.9), as was the P : B ratio (1.06 vs. 0.8).

Discussion

In the Acquatina lagoon, N . lutericeus is apparently an annual species exhibiting rapid growth. The population is characterized by a single generation, whose growth was easily followed, and by heavy adult mortality. March 1991 was the only month with overlapping generations.

The heavy adult mortality is probably due to extrinsic causes such as decreas- ing salinity and high competition. In early 1992, the persisting low salinity caused mortality even in other taxa. On the other hand, caging experiment indicated that predation is not a controlling factor in the Acquatina lagoon (GIANGRANDE, unpubl. data). The presence of a monothelious cycle with a natural post-spawning mortality could also be hypothesized.

Observations on reproductive features are consistent with the trend showed by population dynamics: reproduction occurred during winter, and lecitho- trophic larvae with a short pelagic life (five days) were present every year from late December to February.

The present study revealed some differences in reproductive period com- pared with previous studies. WILSON (1933) reported reproduction during April-May, in Plymouth, and THORSON (1946) from January to June, in Den-

Life-history pattern of Notomastus latericeus 323

mark. The same prolonged reproductive period observed by THORSON was found by GUBRIN & MAS& (1974) for a Mediterranean population (Gulf of Marseille). These two last authors hypothesized the existence of sucessive spawnings within the population, together with maturity reached only a few weeks after metamorphosis. Therefore, as observed in other polychaetes with a wide distribution, the reproductive features of N . lutericeus seem to be peculiar to the population rather than species (BHAUD, 1982; GENTIL et ul., 1990).

Differences in the duration of larval life are also apparent: DAUVIN (1984) reported a longer larval period for this species along the Atlantic coast.

Lastly, WILSON (1933) observed metamorphosis after ten days vs. the 5 days of the Mediterranean population. Therefore, growth may be faster in the Acquatina population than in that from Plymouth.

The similarity observed in density and biomass trends, unusual for an annual species, could be due to the underestimation of juvenile abundance through use of a 1 mm mesh sieve.

In this study, the secondary production of N . Zutericeus was estimated to be 1.9g (AFDW) * m-2 . a-l, giving a production : biomass ratio of 1.7. Moreover, production was lower in 1990 than in 1991, at least until July. This production value is not very high when compared with other polychaete species (WARWICK et ul., 1978; CARRASCO & ARCOS, 1980; PRICE & WARWICK, 1980; KRISTENSEN, 1984; VALDERHAUG, 1985; AMBROGI, 1990), especially considering the fast growing of the species and the environment it inhabits. However, comparison is difficult because the species are not all estuarine forms and belong to different families. The only available data for Cupitellidue are those pertaining to Cupitellu cupitutu of OYENEKAN (1986), who reported values similar to those of the present study, and GRBMARE et ul. (1989), who reported higher values, but in a laboratory population.

The obtained P : B ratio seems to be low, especially if compared with that of other annual species (CARRASCO & ARCOS, 1980; PRICE & WARWICK, 1980; OYENEKAN, 1986; 1987; AMBROGI, 1990). Following the equation of ROBERTSON

with a P : B ratio equal to 4.5. Probably, values computed directly from the observed population are affected by the limited period of high density.

A different ash percentage was found in thoraces and abdomens. Most of the abdominal weight was due to large amounts of sediment in the gut, explaining the highly variable percentage among samples (see also Fig. 3 a). Therefore, care must be taken in using the various conversion factors for determining AFDW in polychaetes, especially in limnivore species.

The lower mean individual weight at site B, together with the higher abundance during the periods corresponding to the phase of low density in site A, could indicate a crowding-effect limiting growth. This phenomenon has already been recorded in other polychaete species (ZAJAK, 1986).

During 1989 N . lutericeus was almost absent in most parts of the investigated environment, the population being confined in low density patches with less sediment stability and lower percentage of organic matter. One of these patches was site B, while site A represented the situation existing in most of the lagoon.

The appearance of a first N . lutericeus cohort in April 1990 at site A was coincident with an increasing salinity and corresponded with the first significant

(1979), the expected value for 1990 would be higher (5.48 g [AFDW] - m-2 . a-97

324 GIANGRANDE & F R A S C H E ~

increase in density of this species in the whole lagoon; in 1990 it became the most abundant polychaete species. This success was due to the synchrony between recruitment period and the onset of favourable conditions. In contrast, increasing salinity probably represented a disturbance factor for the other polychaete species, which showed a marked decrease in density. The subse- quent salinity decrease in 1991 was coincident with the disappearance of N . lutericeus from site A as well as from virtually the whole lagoon. During this period the species once again remained confined to patches (site B).

Salinity can play a key role in balancing competitive equilibria among polychaete species (DIAZ, 1984; NICHOLS, 1985). At salinities between 10 and 25 “A, N . luevigutu seems to be competitively superior to N. lutericeus. This last species is confined within patches characterized by sediment instability where N . luevigutu is not very abundant. In this manner, species coexistence should be mediated by environmental heterogeneity (DENSLOW, 1985; SHORROCKS, 1990). When salinity rises, N. lutericeus seems to be favoured and expands into the N. luevigutu areas as well, acting as a typical opportunistic species.

Notomastus lutericeus can respond to short-term, positive environmental changes with a rapid increase in density due to a short pelagic stage and fast growth. The heavy adult mortality is also typical of opportunistic species.

Site B, and probably other similar patches, can act as “refuges” for further recolonizations of the rest of the lagoon. The analysis of site A could have been misleading had it concluded that the species was present only during certain periods, while actually it can always be present in some “refuges”. Moreover, larval recolonization from populations of other biotopes is improbable due to the short pelagic stage and the limited larval exchange of the lagoon with the sea (GIANGRANDE & RUBINO, in press).

The life strategy adopted by N. lutericeus can be very successful during favourable periods if those match with the recruitment period; on the other hand, unfavourable conditions lead to drastic reductions of population size and, perhaps, local extinctions. In the Acquatina population the reproduction of N. lutericeus, with its non-overlapping generations, causes complete dependance of population persistence on juvenile survivorship.

Periodic small population size coupled with frequent local extinctions and recolonizations can also influence evolutionary processes (BARTON & CHARLES- WORTH, 1984; CARSON, 1975; NEI et ul., 1975; CARSON & TEMPLETON, 1984; VRIJENHOEK, 1985). As already hypothesized by GRASSLE & GRASSLE (1977) and GRAY (1989), opportunistic taxa can be considered to be metaspecies in which species are continuously formed and become extinct.

Summary

Between February 1989 and February 1992, a study of the polychaete assem- blage of the Acquatina lagoon (Lace, Italy) was carried out. Reproduction, growth, and secondary production of Notomustus lutericeus SARS, one of the most abundant species, were investigated. Notomustus lutericeus appeared as an annual species, breeding in winter. Larvae were present in the plankton from

Life-history pattern of Notomustus lutericeus 325

late December to February. Pelagic larval life was short (about five days). Recruitment occurred in early spring and was followed by rapid growth, with a density peak in June, followed by heavy adult mortality.

The density of the species was apparently strongly correlated to salinity variations (from 6 to 40 %O abiotic control factor), but its presence in the lagoon was mostly the result of successful recruitment and possible competition with other polychaete species. Biomass varied between 0.07 and 2.5 g (AFDW) . m-2. Annual secondary production was 1.9g (AFDW) * m-2 . a-1, and the annual turnover (P : B) was 1.7.

Notomastus latericeus could be defined as an opportunistic species with a rapid increase in abundance during favourable periods. Some evolutionary consequences of local extinction and recolonization arising from the life history pattern of N . latericeus are discussed.

Acknowledgements

This study was financially supported to 60 % by the University program. The authors wish to thank Prof. F. BOERO (University of Lecce) and Dr. R. WARWICK (Plymouth Laboratory) for critically reading the manuscript.

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