[PDF] growth and production of the barnacle balanus amphitrite in an

GROWTH AND PRODUCTION OF THE BARNACLE BALANUS AMPHITRITE IN AN INTERTIDAL AREA AFFECTED BY SEWAGE POLLUTION J. A. Calcagno, J. López Gappa, and A. Tablado ABSTRACT

A low-density, intertidal population of the barnacle Balanus amphitrite was studied close to a sewage outfall near Quequén, Argentina. Barnacles were individually followed during 3 consecu- tive years. Growth rates observed in the present study (orifice length 4.9-5.1 mm at the end of the first year) were remarkably lower than values previously reported for this species. A Von Berta- lanffy growth equation was fitted to length-age data (K = 0.4â쀝쀝0.5, Lâ쀝쀝 = 8.5-8.8, T0 = -0.5 to -0.7). Growth and production were higher in summer/autumn than in winter/spring. The produc- tion/biomass ratio fluctuated between 0.3 and 0.4 for the whole population, but was highest (1.8-1.9) during the first year of benthic life. Based on analysis of length-frequency distributions and fol- lowing the fate of marked specimens, we verified the coexistence of 5 annual cohorts and there- fore a maximal longevity of more than 5 years. Possible causes of this extended life history of B. amphitrite in the study area arc discussed. Barnacles of the genus Balanus Da Costa are estuarine or marine, sessile, filter-feed- ing organisms. The life cycle involves six free-swimming nauplius stages and a bivalved cypris larva which settles generally on inter- tidal or subtidal hard substrata, before meta- morphosing to the adult form. Since most barnacles can be easily identi- fied, measured, and counted in the field, both on natural and artificial surfaces, there is am- ple information about their growth and its re- lation to environmental factors (review in Crisp and Bourget, 1985). European and North American species have been exten- sively studied, particularly Semibalanus bal- anoides (L.), whereas the ecology and life history of barnacles from other parts of the world are still poorly known. Balanus amphitrite Darwin, apparently originally a tropical species, has gained a worldwide distribution by fouling ships and harbors (Zullo et al., 1972). Its geographic range and complex synonymy have been ex- tensively discussed by Henry and McLaugh- lin (1975). In Argentina, B. amphitrite is recorded in harbors and estuaries of Buenos Aires Province (Bastida, 1971; Bastida et al., 1974; Bastida and Brankevich, 1980; Branke- vich et al., 1984, 1985, 1986, 1988), but only few ecological observations are available for this area. The intertidal rocky shores of Buenos Aires Province were originally devoid of acorn barnacles (Olivier et al., 1966), but are presently populated by a dense belt of the introduced species Balanus glandula Darwin. The microstructure of the calcareous shell plates of Balanus amphitrite, as well as its growth during the first days of benthic life, were analyzed by Clare et al. (1994) in lab- oratory-reared specimens. Settlement and growth of this species have been studied mainly on artificial surfaces in harbors (Paul, 1942; Mawatari et al., 1954; Moore and Frue, 1959; Crisp and Bourget, 1985; Shalla et al., 1995; Shkedy et al, 1995). An intertidal population of Balanus am- phitrite near a sewage outfall was studied dur- ing three years at Quequen, Argentina. The low density of this barnacle at the study site allowed us to identify and follow individu- als in order to analyze growth and somatic production. Field work was carried out 4 km eastward of Quequen Harbor, Buenos Aires Province, Argentina (38°34'S, 58°38'30"W) (Fig. 1). The intertidal zone consists of loess platforms divided by irregular breaks of 40-60-cm height. The whole area is exposed to heavy wave action. Two unequal tides occur daily, with a mean amplitude of only 1.28 m dur- ing spring tides. The horizontal distance un- covered during low tides ranges from 40-70 m. Approximately 14-20 million 1 of un- treated sewage from the cities of Necochea and Quequen are discharged daily in this area at the level of low water spring tides. Salin- ity is influenced by fresh water from the Que- quen River, and fluctuates from 20-23 ppt around the outfall. The affected area extends over approximately 400 m of shoreline, Downloaded from https://academic.oup.com/jcb/article/17/3/417/2418901 by guest on 25 July 2023

Fig. 1. Location of study area near Quequen, Argentina. where the typical community dominated by the small mytilid bivalve Brachidontes ro- driguezi (d'Orbigny) is disrupted (Lopez Gappa et al., 1990). The population of Balanus amphitrite is sparse and occurs on vertical substrata, along a narrow area between +0.32 and +0.90 m above the level of low water spring tides. Ob- servations were carried out on individuals lo- cated at a distance of 16-67 m from the out- fall. The most frequent algae at this area are Ulva rigida Agardh, Gelidiella cf. nigrescens (Feldm.) Feldm. et Hamel, Ralfsia sp., and Corallina officinalis L. The dominant herbi- vore is the pulmonate limpet Siphonaria lessoni (Blainville), which can reach high densities (Tablado et al., 1994). Isolated in- dividuals of the barnacle Balanus glandula can be found rarely. The benthic community has a very low species richness. Whelks and sea stars are typically absent, even in areas not affected by sewage. A more detailed de- scription of the physical and chemical vari- ables as well as the spatial and temporal changes in the benthic assemblages can be found in Lopez Gappa et al. (1990, 1993). MATERIALS AND METHODS Growth of Balanus arnhhitrite was assessed by cen- susing the population for 3 consecutive years. Twelve censuses were performed, at intervals ranging from 1.8-4.3 months, from December 1990 to August 1993 (dates shown in Table 1 Preliminary observations were made on 11 September 1990. Counts and measurements were carried out during maximal diurnal low tides and were coincident with the end of each season, except in autumn.

The density of B. amphitrite in the study area was al- ways low. Instances of crowding or individuals elongated by vertical growth were never observed. Therefore, in- traspecific competition is presumed to be minimal. Seventeen 40 x 40-cm permanent squares (2.72 m2) were delimited on vertical surfaces in the zone of maxi- mal density of this species in order to follow temporal changes in as many individuals as possible. These were distributed from the vicinity of the sewage outfall up to an area where the characteristic Brachidontes rodriguezi community began to recover. Balanus amphitrite was rare or completely absent in nonpolluted areas dominated by this mytilid (Lopez Gappa et al., 1990). The squares were photographed at each census and barnacles were individually identified and mapped. Dead specimens and new recruits were also recorded. The ros- trocarinal length of the shell orifice of all live specimens was measured in the field to the nearest 0.1 mm with Vernier calipers. This measurement (hereafter referred to as orifice length) is easy to obtain in the field and is also less variable than the basal diameter, which is frequently affected by contact with other individuals or substratum microtopography.

Growth.-Three cohorts recruited during the summers of 1991, 1992, and 1993 were followed until the end of the study. Most barnacles, however, were already pres- ent in the area before the first census. The polymodal length-frequency distribution of these individuals was separated in normal curves using a BASIC program based on the Marquardt's algorithm (Akamine, 1984). Each bar- nacle was then ranked by size, and assigned to a cohort Table 1. Means ± standard errors (SE) of orifice lengths (mm) of Balanus amphitrite in cohorts recruited before or during the study period. The 1988 cohort probably includes a mixture of older individuals. Downloaded from https://academic.oup.com/jcb/article/17/3/417/2418901 by guest on 25 July 2023

Fig. 2. Frequency distribution of orifice length of bar- nacles (Balanus amphitrite) present in the study area in December 1990. Normal curves and number of individ- uals belonging to each cohort were obtained by polymodal analysis using Marquardt's algorithm. The 1988 cohort probably includes a mixture of older individuals. according to the number of individuals calculated by the program for each normal distribution. The growth and fate of these individuals were then followed during the whole study. The parameters of a Von Bertalanffy growth model were estimated by a nonlinear, iterative method, using 2 sets of data: (1) Individual lengths, consisting of 383 pairs of orifice lengths (L,, L[4.,) obtained in late winter cen- suses of 2 consecutive years. To was estimated from 15 individuals (62 length-age data pairs) recruited during this study which had an orifice length less than I mm at their first census. The age of these recruits was estimated as half the period elapsed between the census when they were recorded for the first time and the previous census. (2) Mean cohort lengths, consisting of 33 pairs of mean lengths (L,, L쀝,) of cohorts in 2 consecutive years. To was estimated only from cohorts of known age (1991-1993 recruitments, 19 length-age data pairs). Production.-In order to assess the somatic production of B. amphitrite, the relationship between orifice length and total dry weight (including shell) was analyzed. Sev- enty individuals were randomly sampled, numbered, mea- Fig. 3. Growth of cohorts of Balanus amphitrite at Que- quen (means ± SE). The 1991, 1992, and 1993 cohorts were recruited during the study period. Older cohorts were already present before the start of the observations. The 1988 cohort probably includes a mixture of older individuals. Fig. 4. Von Bertalanffy growth curves calculated from length-age data of individual barnacles (Balanu5' amphitrite) or cohort means. The 1988 cohort has been omitted. sured, and dried at 70°C to a constant weight. A linear equation was fitted after logarithmic transformation of both variables. Since all the barnacles were individually identified, so- matic production was calculated by weight increments of each specimen. In addition, individual values were summed to provide production estimates for each cohort (per m2) and for the whole population in each season. Inasmuch as the time intervals between censuses fluctu- ated between 55 and 129 days, seasonal estimations were standardized for a period of three months. Production es- timates on an individual basis or production/biomass ra- tios (P/B) are in this case more meaningful than estimates per ml, since the squares were not chosen at random, but were in areas of highest density of B. amphitrite. Sizes of individuals not detected during some censuses were calculated using the Von Bertalanffy growth equation. RESULTS

Growth

At the beginning of this study (spring 1990), the permanent squares selected for monitoring growth were populated by 356 in- dividuals (130.9 ind.M-2), 33 of which died before the next census. The length-frequency distribution of the remaining 323 barnacles was strongly skewed to the right (Fig. 2). A Fig. 5. Seasonal changes of individual somatic produc- tion of ealanus amphitrire at Quequen, Argentina. Downloaded from https://academic.oup.com/jcb/article/17/3/417/2418901 by guest on 25 July 2023

Table 2. Parameters of the Von Bertalanffy growth equa- tions [Size = L_ ( l e"1"*8*"1"!)1)] based on orifice lengths of individual barnacles (Balanus amphitrite) or on co- hort mean values. rZ = coefficient of determination. polymodal distribution composed of three normal curves of 166, 98, and 59 individu- als, was fitted to the data (r쀝 = 0.99). Field ob- servations recorded between 1988 and 1990 indicated that the two younger distributions represented cohorts that entered the benthic population during the summers of 1990 and 1989. The older barnacles (1988 cohort in Figs. 2, 3) may represent a mixture of indi- viduals recruited during 1988 or before. Three main recruitments occurred during the summers of 1991, 1992, and 1993 (Fig. 3). The first and last were represented only by 5 individuals each, first detected during the autumn census, when they had orifice lengths between 2 and 3 mm. Recruitment rate was an order of magnitude higher in 1992 (65 individuals) than in 1991 or 1993. Some of these recruits were already recorded dur- ing the summer census, when they had orifice lengths of approximately 1 mm. While the date of recruitment of these cohorts used for age calculations was estimated to be mid- January, a small proportion of recruits (6 in- dividuals, 8%) settled in late summer or early autumn. These individuals were taken into ac- count for production calculations, but were omitted in Fig. 3. Table 1 and Fig. 3 show growth increments in cohorts that recruited before and during the study period. The 1990, 1991, and 1992 co- horts reached mean values of 4.9-5.1 mm at the end of their first year of benthic existence. The 1989, 1990, and 1991 cohorts reached 5.8-6.3 mm after two years of benthic life. As expected, growth rate was highest during the first months of life and then slowed gradually. Growth rate was highest in summer and low- est in winter. Five or more cohorts coexisted at any season and therefore maximal longevity can be estimated to be at least 5.5 years. Similar results were obtained when adjust- ing a Von Bertalanffy growth equation to in- dividual or cohort length-age data (Fig. 4, Table 2). There was good agreement between expected and observed values at intermedi- ate ages. On the other hand, the model yielded poor estimations for the first three months of benthic life. Only eight barnacles (2%) grew larger than infinite length estimates. PRODUCTION

The relationship between total dry weight and orifice length is shown in the following exponential equation: Total dry weight (g) = 0.006349. Orifice length (mm)l 891 (N = 70, r2 = 0.538). Table 3 shows seasonal somatic production estimates. A clear trend can be seen in the Table 3. Seasonal and annual estimates of mean individual and total production, biomass (total dry weight), and production/biomass (P/B) ratio in a population of Balanus amphitrite during the study period. Downloaded from https://academic.oup.com/jcb/article/17/3/417/2418901 by guest on 25 July 2023

Table 4. Production, biomass (total dry weight), and pro- duction/biomass (P/B) ratio in cohorts of Balanu.s am- phitrite in 1991 and 1992 during their first year of life. seasonal change of the whole population. Summer and autumn figures are higher than winter and spring values (Fig. 5). The pro- duction/biomass (P/B) ratio was highest (1.84-1.88) in 1991 and 1992 cohorts dur- ing their first year of life (Table 4). Since the population grew older and new recruitments were negligible, annual production decreased steadily from 1991 to 1993. For the same rea- son, the PIB ratio of the whole population de- creased from 0.419 in 1991 to 0.303 in 1993. Table 5 shows production values for dif- ferent age classes during the study period. It can be seen that the highest production was observed in the juvenile 1993 cohort and the lowest in those barnacles recruited in 1988 or before.

DISCUSSION

The timing of recruitment observed in this study is coincident with data reported by Bastida and Brankevich (1980) and Branke- vich et al. (1984, 1985, 1986, 1988), who found that B. amphitrite settled from Octo- ber to June (peak in February-March) on pan- els submerged within Quequen Harbor. An extended settlement season, ranging from summer to early autumn has also been re- ported for boreal localities (Mawatari et al., 1954; Shalla et al., 1995). Information about growth of B. amphitrite is available mainly for tropical regions of the northern hemisphere (Table 6). Growth of this species in Quequen, expressed as basal di- ameter in order to allow comparisons with other studies (basal diameter = 1.923 orifice length, N = 100), can be estimated to be 8.2- 8.9 mm at the end of the first year. The growth rate then decreased rapidly and growth almost ceased when approaching an infinite basal di- ameter of 16.4-16.9 mm. Growth rates found for this southern hemi- sphere population are remarkably lower than previously published values for this species (Table 6). Differences may be due to many factors, particularly lower water temperature (9-22°C), and the regular emersion periods affecting this intertidal population. Most stud- ies summarized in Table 6 were carried out in warmer waters and under constant sub- mersion in harbor areas. Growth rate com- parisons are also complicated by the fact that barnacles were studied at different ages. Bastida ( 1971) reported that in the summer, B. amphitrite reached a basal diameter of 5 mm during its first month of life on an ex- perimental raft within Mar del Plata Harbor (located -120 km northeast of Quequen). Taking into account that the growth model fit- ted in the present study overestimates size during the first months of benthic life (Fig. 4), the intertidal population of B. amphitrite at Quequen may attain a similar basal diam- eter in at least three months. Most investigations on growth of B. am- phitrite have focused on the postsettlement and juvenile stages (Clare et al., 1994; Shalla et at., 1995). A more extended study on growth and mortality of this barnacle on the Mediterranean coast of Israel, concluded that maximal longevity reached 1.26-1.40 years, and only 2.7% of individuals could reproduce in two successive breeding seasons (Shkedy et al., 1995). An interesting and unexpected result of the present study is that we have found that B. amphitrite can attain a much longer longevity than previously suspected. Following the fate of marked specimens, we were able to verify the coexistence of at least five annual cohorts and therefore a maximal possible longevity of more than five years. The causes of this different life-history may be related to the relatively little importance of intraspecific competition and predation in the study area. The well-known consequences of competition and crowding on intertidal barnacles (Barnes and Powell, 1950; Connell, Table 5. Production in different annual cohorts of Balanus amphitrite. Downloaded from https://academic.oup.com/jcb/article/17/3/417/2418901 by guest on 25 July 2023

Table 6. Growth rates expressed as basal diameter increments of Balanus amphitrite in different regions of the world. [a] After Shalla et al. (1995). 1961) were not observed at Quequen because recruitment rate was low and thus individu- als were commonly isolated on the substra- tum. The influence of sewage pollution on the growth rate of B. amphitrite cannot be as- sessed in the field, since this species is absent in nonpolluted intertidal areas. Mortality due to predation was not directly observed, but is evidently very low, since sea stars and whelks are absent in this commu- nity (Lopez Gappa et al., 1990, 1993; Tablado et al., 1994). This population is also hardly accessible for fishes, for it occurs at relatively high intertidal levels. Seasonal fluctuations in production reflect higher growth rates during the warmer months of the year, a fact already reported by Shalla et al. (1995) for a population of B. amphitrite at the Suez Canal. ACKNOWLEDGEMENTS

We thank the authorities and staff of the Argentine Mu- seum of Natural Sciences "Bernardino Rivadavia" and Puerto Quequen Hydrobiological Station for their sup- port. E. Marschoff kindly provided his FORTRAN pro- gram for fitting the Von Bertalanffy growth model. Ines O'Farrell improved the English style of an earlier draft of this study. Field sampling at Quequen was partly sup- ported by the National Council for Scientific Research and Technology (CONICET). LITERATURE CITED Akamine, T. 1984. The BASIC program to analyse the polymodal frequency distribution into normal distri- butions with Marquardt's method.-Bulletin Japan Sea Regional Fisheries Research Laboratory 34: 53-60. Barnes, H., and H. T. Powell. 1950. The development, general morphology and subsequent elimination of bar- nacle populations, Balanus crenatus and B. balanoides, after a heavy initial settlement.â쀝쀝Journal of Animal Ecology 19: 175-179. Bastida, R. 1971. Las incrustaciones biologicas en el puerto de Mar del Plata. Periodo 1966/67.-Revista del Museo Argentino de Ciencias Naturales "Bernardino Rivadavia," Hidrobiologia 3: 203-285. â쀝쀝â쀝쀝â쀝쀝â쀝쀝, and G. Brankevich. 1980. Estudios ecológicos preliminares sobre las comunidades incrustantes de Puerto Quequen (Argentina).â쀝쀝In: Proceedings of the Fifth International Congress on Marine Corrosion and Fouling. Pp. 113-138. Barcelona, Spain. â쀝쀝â쀝쀝â쀝쀝â쀝쀝, E. Spivak, S. G. L'Hoste, and H. E. Adabbo. 1974. Las incrustaciones biológicas de Puerto Bel- grano. I. Estudio de la fijación sobre paneles mensu- ales, perÃ쀝odo 1971/72.â쀝쀝Lemit Anales, 3-1974: 97-165.

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RECEIVED: 18 October 1996. ACCEPTED: 28 January 1997. Addresses: (JAC) Departamento de Ciencias Biológi- cas, Facultad de Ciencias Exactas y Naturales, Universi- dad de Buenos Aires, Pabellón II, Ciudad Universitaria, (1428) Buenos Aires, Argentina; (JLG, AT) Museo Ar- gentino de Ciencias Naturales "Bernardino Rivadavia," Av. A. Gallardo 470, (1405) Buenos Aires, Argentina. Correspondence to JLG. (e-mail: lgappa@mail.retina.ar) Downloaded from https://academic.oup.com/jcb/article/17/3/417/2418901 by guest on 25 July 2023