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GROWTH AND PRODUCTION OF THE BARNACLE BALANUS AMPHITRITE IN AN INTERTIDAL AREA AFFECTED BY SEWAGE POLLUTION J. A. Calcagno, J. López Gappa, a n d A. Tablado A B S T R A C T 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 consecutive years. Growth rates observed in the present study (orifice length 4.9-5.1 m m at the end of the first year) were remarkably lower than values previously reported for this species. A Von Bertalanffy growth equation was fitted to length-age data (K = 0.4â홢홢0.5, L홢 â 홢 = 8 . 5 - 8 . 8 , T0 = - 0 . 5 to - 0 . 7 ) . Growth and production were higher in summer/autumn than in winter/spring. The production/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 following the fate of marked specimens, we verified the coexistence of 5 annual cohorts and therefore 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-feeding organisms. The life cycle involves six free-swimming nauplius stages and a bivalved cypris larva which settles generally on intertidal or subtidal hard substrata, before metamorphosing to the adult form. Since most barnacles can be easily identified, measured, and counted in the field, both on natural and artificial surfaces, there is ample information about their growth and its relation to environmental factors (review in Crisp and Bourget, 1985). European and North American species have been extensively studied, particularly Semibalanus balanoides (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 extensively discussed by Henry and McLaughlin (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; Brankevich 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 laboratory-reared specimens. Settlement and growth o f 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 a l , 1995). An intertidal population o f Balanus amphitrite near a sewage outfall was studied during three years at Quequen, Argentina. The low density of this barnacle at the study site allowed us to identify and follow individuals 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 4 0 - 6 0 - c m height. The whole area is exposed to heavy wave action. Two unequal tides occur daily, with a mean amplitude of only 1.28 m during spring tides. The horizontal distance uncovered during low tides ranges from 4 0 - 7 0 m. Approximately 1 4 - 2 0 million 1 of untreated sewage from the cities of Necochea and Quequen are discharged daily in this area at the level of low water spring tides. Salinity is influenced by fresh water from the Quequen River, and fluctuates from 2 0 - 2 3 ppt around the outfall. The affected area extends over approximately 4 0 0 m of shoreline, scription of the physical and c h e m i c a l variables as w e l l as the spatial a n d t e m p o r a l c h a n g e s in the b e n t h i c a s s e m b l a g e s c a n b e f o u n d in Lopez Gappa et al. (1990, 1993). MATERIALS AND M E T H O D S Growth of Balanus arnhhitrite was assessed by censusing the population for 3 consecutive years. Twelve c e n s u s e s were p e r f o r m e d , at intervals r a n g i n g 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. Fig. 1. Location of study area near Quequen, Argentina. where the typical community dominated by the small mytilid bivalve Brachidontes rodriguezi (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. Observations were carried out on individuals located at a distance of 1 6 - 6 7 m from the outfall. 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 herbivore is the pulmonate limpet Siphonaria lessoni (Blainville), which can reach high densities (Tablado et al., 1994). Isolated individuals 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- The density of B. amphitrite in the study area was always low. Instances of crowding or individuals elongated by vertical growth were never observed. Therefore, intraspecific 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 maximal 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 rostrocarinal length of the shell orifice of all live specimens was measured in the field to the nearest 0.1 m m 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. G r o w t h . - T h r e e cohorts recruited during the summers of 1991, 1992, and 1993 were followed until the end of the study. Most barnacles, however, were already present in the area before the first census. The polymodal length-frequency distribution o f these individuals was separated in normal curves using a BASIC program based on the Marquardt's algorithm (Akamine, 1984). Each barnacle 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. Fig. 2. Frequency distribution of orifice length of barnacles (Balanus amphitrite) present in the study area in December 1990. Normal curves and number of individuals 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 censuses 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 w h e n they were recorded for the first time and the previous census. (2) Mean cohort lengths, consisting of 33 pairs of mean lengths (L,, L홢,) of cohorts in 2 consecutive years. To was estimated only from cohorts of known age (1991-1993 recruitments, 19 length-age data pairs). P r o d u c t i o n . - I n order to assess the somatic production of B. amphitrite, the relationship between orifice length and total dry weight (including shell) was analyzed. Seventy individuals were randomly sampled, numbered, mea- 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, somatic 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 fluctuated between 55 and 129 days, seasonal estimations were standardized for a period of three months. Production estimates on an individual basis or production/biomass ratios (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 1990), the beginning the permanent of this squares study (spring selected for m o n i t o r i n g g r o w t h w e r e p o p u l a t e d b y 3 5 6 individuals (130.9 ind.M-2), 33 o f w h i c h died before the next census. T h e length-frequency distribution of the remaining 323 barnacles w a s s t r o n g l y s k e w e d to the r i g h t (Fig. 2). A Fig. 3. Growth of cohorts of Balanus amphitrite at Quequen (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. 5. Seasonal changes of individual somatic production of e a l a n u s amphitrire at Quequen, Argentina. Table 2. Parameters of the Von Bertalanffy growth equations [Size = L_ ( l e"1"*8*"1"!)1)] based on orifice lengths of individual barnacles (Balanus amphitrite) or on cohort mean values. rZ = coefficient of determination. polymodal distribution composed o f three normal curves of 166, 98, and 59 individuals, was fitted to the data (r홢 = 0.99). Field observations 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 individuals 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 during 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 midJanuary, a small proportion of recruits (6 in- dividuals, 8%) settled in late summer or early autumn. These individuals were taken into account 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 cohorts 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 lowest 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 adjusting a Von Bertalanffy growth equation to individual or cohort length-age data (Fig. 4, Table 2). There was good agreement between expected and observed values at intermediate 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. Table 4. Production, biomass (total dry weight), and production/biomass (P/B) ratio in cohorts of Balanu.s amphitrite 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 production/biomass (P/B) ratio was highest (1.84-1.88) in 1991 and 1992 cohorts during 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 reason, the PIB ratio of the whole population decreased from 0.419 in 1991 to 0.303 in 1993. Table 5 shows production values for different 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 Brankevich et al. (1984, 1985, 1986, 1988), who found that B. amphitrite settled from October to June (peak in February-March) on panels submerged within Quequen Harbor. An extended settlement season, ranging from summer to early autumn has also been reported 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 diameter in order to allow comparisons with other studies (basal diameter = 1.923 orifice length, N = 100), can be estimated to be 8.28.9 mm at the end of the first year. The growth rate then decreased rapidly and growth almost ceased when approaching an infinite basal diameter of 16.4-16.9 mm. Growth rates found for this southern hemisphere 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 studies summarized in Table 6 were carried out in warmer waters and under constant submersion in harbor areas. Growth rate comparisons 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 m m during its first month of life on an experimental raft within Mar del Plata Harbor (located - 1 2 0 km northeast o f Quequen). Taking into account that the growth model fitted 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 diameter in at least three months. Most investigations on growth of B. amphitrite 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. 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 individuals were commonly isolated on the substratum. The influence of sewage pollution on the growth rate of B. amphitrite cannot be assessed 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 community (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 Museum of Natural Sciences "Bernardino Rivadavia" and Puerto Quequen Hydrobiological Station for their support. E. Marschoff kindly provided his FORTRAN program 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 supported by the National Council for Scientific Research and Technology (CONICET). LITERATURE C I T E D Akamine, T. 1984. The BASIC program to analyse the polymodal frequency distribution into normal distributions with Marquardt's m e t h o d . - B u l l e t i n Japan Sea Regional Fisheries Research Laboratory 34: 5 3 - 6 0 . Barnes, H., and H. T. Powell. 1950. The development, general morphology and subsequent elimination of barnacle populations, Balanus crenatus and B. balanoides, after a heavy initial settlement.â홢홢Journal of Animal Ecology 19: 175-179. Bastida, R. 1971. Las incrustaciones biologicas en el puerto de Mar del Plata. Periodo 1 9 6 6 / 6 7 . - R e v i s t a del Museo Argentino de Ciencias Naturales "Bernardino Rivadavia," Hidrobiologia 3: 2 0 3 - 2 8 5 . 홢 â홢 홢 â홢 홢 â홢 홢 â 홢, and G. Brankevich. 1980. Estudios ecológicos preliminares sobre las comunidades incrustantes de Puerto Quequen (Argentina).â홢홢In: Proceedings of the Fifth International Congress on Marine Corrosion and Fouling. Pp. 113-138. Barcelona, Spain. 홢 â홢 홢 â홢 홢 â홢 홢 â 홢, E. Spivak, S. G. L'Hoste, and H. E. Adabbo. 1974. Las incrustaciones biológicas de Puerto Belgrano. I. Estudio de la fijación sobre paneles mensuales, perÃ홢odo 1971/72.â홢홢Lemit Anales, 3 - 1 9 7 4 : 97-165. Brankevich, G., R. Bastida, and C. Lemmi. 1988. A comparative study of biofouling settlements in different sections of Necochea power plant (Quequen Port, Argentina). Biofouling 1: 113-135. 홢 â홢 홢 â홢 홢 â홢 홢 â 홢,홢 â홢 홢 â홢 홢 â홢 홢 â 홢,and D. Martinez. 1984. Ecological aspects of marine fouling at the Necochea power plant (Puerto Quequen, Argentina).â홢홢In: Proceedings of the Sixth International Congress on Marine Corrosion and Fouling. Pp. 567-583, Athens, Greece. 홢 â홢 홢 â홢 홢 â홢 홢 â 홢,홢 â홢 홢 â홢 홢 â홢 홢 â 홢,and 홢 â홢 홢 â홢 홢 â홢 홢 â 홢. 1985. Estudios ecológicos sobre las comunidades incrustantes de la central electrica Necochea (Puerto Quequén, Argentina).â홢홢Cidepint Anales 1985: 173-239. 홢 â홢 홢 â홢 홢 â홢 홢 â 홢,J. L. Flaminio, and R. Bastida. 1986. Estudios ecológicos sobre las comunidades incrustantes de la toma de agua de la central electrica Necochea (Puerto Quequen, Argentina), perÃ홢odo 1 9 8 1 - 8 2 . - C i d e p i n t Anales 2-1986: 4 1 - 9 9 . Clare, A. S., S. C. Ward, D. Rittschof, and K. M. Wilbur. 1994. Growth increments of the barnacle Balanus amphitrite amphitrite Darwin ( C i r r i p e d i a ) . - J o u r n a l of Crustacean Biology 14: 27-35. Connel, J. H. 1961. Effects of competition, predation by Thais lapillus, and other factors on natural populations of the barnacle Balanus balanoides.â홢홢Ecological Monographs 31: 61-104. Crisp, D. J., and E. Bourget. 1985. Growth in barnacles.â홢홢Advances in Marine Biology 22: 1 9 9 - 2 4 4 . Henry, D. P., and P. A. McLaughlin. 1975. The barnacles of the Balanus amphitrite complex (Cirripedia, T h o r a c i c a ) . - Z o o l o g i s c h e Verhandelingen 141: 1-254. Lopez Gappa, J. J., A. Tablado, and N. H. Magaldi. 1990. Influence of sewage pollution on a rocky intertidal community dominated by the mytilid Brachidontes rodriguezi.â홢홢Marine Ecology Progress Series 63: 163-175. 홢 â홢 홢 â홢 홢 â홢 홢 â 홢,홢 â홢 홢 â홢 홢 â홢 홢 â 홢,and 홢 â홢 홢 â홢 홢 â홢 홢 â홢. 1993. Seasonal changes in an intertidal community affected by sewage pollut i o n . - E n v i r o n m e n t a l Pollution 82: 157-165. Mawatari, S., Y. Hirosaki, and S. Kobayashi. 1954. Settlement and growth of acorn barnacle, B a l a n u s am- phitrite communis Darwin. II.â홢홢Miscellaneous Reports Research Institute for Natural Resources (Tokyo) 34: 48-57. Moore, H. B., and A. C. Frue. 1959. The settlement and growth of Balanus improvisus, B. eburneus and B. amphitrite in the Miami a r e a . - B u l l e t i n of Marine Science of the Gulf and Caribbean 9: 4 2 1 - 4 4 0 . Olivier, S. R., A. Escofet, J. M. Orensanz, S. E. Pezzani, A. M. Turró, and M. E. Turro. 1966. Contribucion al conocimiento de las comunidades benticas de Mar del Plata. I. El litoral rocoso entre Playa Grande y Playa C h i c a . - A n a l e s de la Comisión de Investigaciones CientÃ홢ficas de la Provincia de Buenos Aires 7: 185-206. Paul, M. D. 1942. Study on the growth and breeding of certain sedentary organisms in the Madras harbour.â홢홢Proceedings of the Indian Academy of Sciences 15: 1-42. Shalla, S. H. A., A. F. A. Ghobashy, and R. G. Hartnoll. 1995. Studies on the barnacle Balanus amphitrite Darwin, 1854 (Cirripedia) from lake Timsah in the Suez Canal.â홢홢Crustaceana 68: 5 0 3 - 5 1 7 . Shkedy, Y., U. N. Safriel, and T. Keasar. 1995. Life-his- tory of B a l a n u s amphitrite and Chthamalus stellatus recruited to settlement panels in the Mediterranean coast of Israel.â홢홢Israel Journal of Zoology 41: 147-161. Tablado, A., J. J. Lopez Gappa, and N. H. Magaldi. 1994. Growth of the pulmonate limpet Siphonaria lessoni (Blainville) in a rocky intertidal area affected by sewage pollution.â홢홢Journal of Experimental Marine Biology and Ecology 175: 211-226. Zullo, V. A., D. B. Beach, and J. T. Carlton. 1972. New barnacle records (Cirripedia, Thoracica).â홢홢Proceedings of the California Academy of Sciences, series 4, 39: 65-74. RECEIVED: 18 October 1996. ACCEPTED: 28 January 1997. Addresses: (JAC) Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria, (1428) Buenos Aires, Argentina; (JLG, AT) Museo Argentino de Ciencias Naturales "Bernardino Rivadavia," Av. A. Gallardo 470, (1405) Buenos Aires, Argentina. Correspondence to JLG. (e-mail: [email protected])