Download GROWTH AND PRODUCTION OF THE BARNACLE BALANUS

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])