Journal of Experimental Marine Biology and Ecology
313 (2004) 63 – 73
www.elsevier.com/locate/jembe
Effects of temperature on growth rate and body size
in the Mediterranean Sea anemone Actinia equina
O. Chomskya,*, Y. Kamenira, M. Hyamsa, Z. Dubinskya,
N.E. Chadwick-Furmana,b
a
Faculty of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel
Interuniversity Institute for Marine Science, P.O. Box 469, Eilat, Israel
b
Received 2 May 2004; received in revised form 31 May 2004; accepted 31 July 2004
Abstract
Actinia equina is the most common sea anemone in the rocky intertidal zone of the Mediterranean
coast of Israel, yet little is known about its biology in this habitat. We examined variation in polyp
growth at several temperatures within the local range. Under laboratory conditions, only polyps at low
temperatures (15 and 20 8C) grew, whereas those at higher temperatures (25 and 30 8C) lost body
mass. Seasonal monitoring of pedal disk diameter over 18 months at field sites showed that polyps
shrank significantly during the summer when temperatures were high. We conclude that at summer
seawater temperatures along the coast of Israel (28.7–29.5 8C), polyps of A. equina are unable to
balance their metabolic requirements with energy input, resulting in a seasonal reduction in biomass.
Polyps appear able to acclimate to high temperatures, but not sufficiently to avoid shrinkage of tissues.
D 2004 Elsevier B.V. All rights reserved.
Keywords: Acclimation; Metabolism; Actiniaria; Respiration; Geographical limits; Distribution; Population size
structure
1. Introduction
Occupation of the intertidal zone by sessile invertebrates imposes a restriction on
energy input by limiting the time available for feeding, and also subjects them to
* Corresponding author. Tel: +972 3 531 8283; fax: +972 3 535 1824.
E-mail address: [email protected] (O. Chomsky).
0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2004.07.017
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O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
desiccation and to more extreme temperatures than those prevailing in the subtidal area.
Many intertidal animals have developed biochemical, physiological, and behavioral
adaptations to maintain a positive energy balance despite these short-term perturbations
(reviewed by Newell and Bayne, 1973; Newell, 1980). Only a positive energy budget over
time allows growth, whereas an excess of metabolic expenditure over energy obtained
from ingested food inevitably leads to biomass loss and shrinkage. Along the
Mediterranean coast of Israel, populations of the sea anemone Actinia equina live at the
upper isotherm of distribution of this species, so the question arises as to how temperature
affects polyp growth rates in this habitat.
The main sources of cyclic temperature fluctuation in the littoral zone are latitude,
season, time of day, and tidal rhythm. Effects of temperature on the metabolism of some
intertidal invertebrates have been examined extensively (Newell, 1969; Newell and Bayne,
1973), but little is known about thermal acclimation in intertidal sea anemones. The
problem of temperature response is of particular interest in A. equina, which is a
cosmopolitan littoral sea anemone subject to a wide range of climatic conditions
throughout its distribution. Individuals of A. equina occur in rocky intertidal areas ranging
from the northeastern Atlantic and Mediterranean, to northern and southern Africa and
Japan (Sole-Cava and Thorpem, 1992; Monteiro et al., 1997; Allcock et al., 1998; Yanagi
et al., 1999). The most extensive database regarding growth and temperature in A. equina
is that of Ivleva (1964), who found that the optimal temperature for growth in this species
is 18.7–19.9 8C. Growth declines at temperatures above and below this range, possibly due
in part to inefficient food ingestion at extreme temperatures (Ivleva, 1964).
Respiration is the main energy sink in non-reproducing sea anemones, and respiration
rate depends on temperature (reviewed by Shick, 1991). Thus, it is likely that the annual
growth cycle of the local sea anemone A. equina relates to the temperature cycle in the
Eastern Mediterranean Sea through the effects of temperature on respiration rate.
In some populations of Actinia spp., individuals have been shown to acclimate to
seasonal temperature changes occurring in their natural surroundings, thereby reducing the
temperature dependence of respiration. During the summer, these polyps show a lateral
displacement of the respiration rate–temperature curve to the right, in comparison with
conspecifics in winter, suggesting acclimation of the respiratory enzyme system (Griffiths,
1977a). The same pattern is seen when comparing populations from different regions,
apparently due to local adaptation to the ambient temperature range within each habitat
(Griffiths, 1977a). Individuals of the intertidal sea anemone Metridium senile also vary in
their response to temperature according to their latitude of origin (Sassaman and Mangum,
1970; Walsh and Somero, 1981). Southern California polyps differ in their oxygen
consumption patterns from northern ones, in response to both gradual and acute changes in
temperature. Northern anemones show a pronounced increase in Q10 at temperatures just
above the normal environmental range, but southern anemones do not. In contrast, this
pattern was not observed in a population of M. senile examined in Massachusetts
(Sassaman and Mangum, 1970). Populations of M. senile also adjust their extent of
metabolic compensation to temperature following several weeks of acclimation. Temperature acclimation involves changes in the activity of several enzymes of intermediary
metabolism, but the extent and direction of these changes are not consistent between
temperatures or populations.
O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
65
In contrast to some populations of both Actinia spp. and M. senile, temperature
acclimation does not appear to occur in the sea anemones Haliplanella luciae and
Diadumene leucolena (Sassaman and Mangum, 1970). In the latter two species, after
natural ambient temperature boundaries are exceeded, respiration is affected by temperature. Also in at least one population of A. equina, no temperature acclimation has been
observed. Navarro et al. (1981) studied a population of A. equina along the northern coast
of Spain, where the mean summer temperature of coastal waters is 20 8C. They found that
the rate of oxygen consumption in submerged polyps increased with temperature over the
10–30 8C range. Navarro et al. (1981) view this temperature dependence of respiration as
the absence of temperature acclimation, however, this result may be interpreted as
acclimation by a shift of the whole respiration rate–temperature curve.
In summary, high temperature always increases respiratory rates. Thermal acclimation
can only mitigate its severity, but never totally eliminate that dependence.
Thus, conflicting reports exist in the literature regarding the extent of temperature
acclimation in sea anemones in general, and in A. equina in particular. There is a lack of
long-term, integrated field and laboratory data on the effects of temperature in A. equina.
We report here on impacts of temperature on the growth rate of A. equina polyps under
laboratory conditions, and on seasonal variation in the size structure of populations at field
sites along the Mediterranean coast of Israel.
2. Materials and methods
2.1. Laboratory experiment
Polyps of A. equina were collected at low tide during February 2001 from three
intertidal sites along the Mediterranean coast of Israel (32828VN; 30853VE): Akhziv,
Newe-Yam, and Bat-Yam. Individuals were removed from intertidal rocks using a small
metal spatula and transferred to temperature- and light-controlled rooms at Bar Ilan
University (after Chomsky et al., 2004). Due to the technical constraints of maintaining a
large number of aquaria at different temperatures in the laboratory, four large aquaria were
set up, each at a different experimental temperature. This lack of replication of aquaria
within each temperature treatment is standard for laboratory growth experiments, and is
based on studies which have demonstrated the validity of growth results using this method
(Navarro et al., 1981; Ortega et al., 1984; Tsuchida and Potts, 1994). Polyps from the three
field sites were distributed randomly among the four experimental aquaria (N=22 polyps
per each aquarium of 707025 cm). All aquaria were supplied with aerated
Mediterranean seawater and maintained at ambient seawater temperature at the time of
collection (17 8C). The temperature in each aquarium gradually was altered to one of four
experimental temperatures: 15, 20, 25, or 30 8C. During acclimation, the temperature of
each aquarium was changed by 1–2 8C each day, until the target temperature was reached.
This technique of gradual change was used to simulate the naturally slow rate of
temperature change in nature (after Griffiths, 1977a). During acclimation, the polyps were
not fed, in order to allow residual food and detritus from the collection sites to be
eliminated. The experimental temperatures were selected to include the annual range in the
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O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
local environment (range=17.1–29.5 8C mean monthly seawater temperature at Haifa,
Israel during 1992–1999 at 1 km distance from the shoreline, at 0.5 m depth).
Only adult polyps were used (basal disk diameter N15 mm), since juvenile A. equina
are known to differ from adults in their metabolism (Ivleva, 1964). Experimental polyps
ranged in size from 3.51 to 68.17 g wet mass (X̄FSD=24.03F13.52 g), and from 18.9 to
68.7 mm pedal disk diameter (45.42F10.01 mm). The light regime was a 12 h:12 h
light/dark cycle, controlled by a timer. Light intensity was 200 Amol quanta m 2 s 1 at
the water surface, similar to the daytime light intensity in typical habitats for this sea
anemone in Israel (after Chomsky et al., 2004). The polyps in all four aquaria were fed
to repletion with brine shrimp (Artemia) once each week (after Chomsky et al., 2004).
Since they were provided with as many brine shrimp as their oral disks could hold,
larger anemones received more food than did smaller ones, but the amount of food was
proportional to body size. All anemones engulfed the Artemia quickly and completely.
On the day after feeding each week, egested boluses produced by each anemone were
removed from the aquaria, and the aquaria were cleaned. Individual anemones were
placed in labeled glass Petri dishes (10 cm diameter, 1.5 cm height), which were
submerged 15 cm below the water surface. The positions of the dishes in the aquaria
were rotated each week, and anemones were weighed fortnightly for 110 days. Repeated
measurements were made on the same individuals, so a technique of live wet mass
assessment was used: we weighed each animal in a Petri dish after blotting off excess
water with tissue paper. Pedal disk diameter was measured with calipers to the nearest
0.5 mm. If the disk was markedly elliptical, size was calculated as the mean of the
minimum and maximum diameters (after Brace and Quicke, 1986). These parameters
were considered good indicators of polyp size, since polyp dry mass correlates with wet
mass, and both increase exponentially with the diameter of the pedal disk (Chomsky et
al., 2004).
2.2. Field observations on population size structure
We examined a natural population of A. equina over 18 months (March 2001 to July
2002), at three sites along the Israeli coast (Habonim, Shikmona, and Mikhmoret), to
assess seasonal changes in anemone size. Every few months, approximately 40–60 marked
polyps were measured for column diameter at each site. All monitored polyps were
recognized individually, based on their locations relative to small stainless steel markers
and to each other. Polyps appeared to move little if at all during the study period.
To minimize effects of daily fluctuations in column diameter, due to a tide-related
semidiurnal expansion cycle (Ottaway, 1979a,b), anemones always were measured at low
tide when their tentacles were fully contracted.
2.3. Statistical analysis
The computer program SPSS version 11.0 (Norusis, 1999) was used for all statistical
analyses. Analyses of variance (ANOVA) were applied to test for variation in body mass
and diameter among temperature treatments in the laboratory, and among seasons in the
field. A Bonferroni correction was applied to all multiple comparison tests, except in the
O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
67
case of heteroscedastic data (i.e.: population size structure at the Habonim site), where a
Tamhane correction was applied.
3. Results
The four experimental groups initially did not vary significantly in either wet mass or
pedal disk diameter (ANOVA, F=0.240 and p=0.868 for mass, F=0.955 and p=0.418 for
diameter). During the laboratory experiment, only anemones in the low temperature
groups (15 and 20 8C) increased in body mass and diameter over 110 days, whereas
individuals in the high temperature groups (25 and 30 8C) shrank (Fig. 1). Anemones at
Fig. 1. Variation in the growth rate of polyps of the sea anemone A. equina from the Mediterranean coast of Israel,
among four experimental temperature regimes under laboratory conditions. (A) Change in percent body mass.
The dashed lines indicate linear approximations for body mass decline in the early (0–38 days) versus late (39–
110 days) stages of the experiment at 30 8C. See text for details. (B) Change in percent pedal disk diameter.
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O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
low experimental temperatures increased in mass by approximately 64% (at 15 8C) and
38% (at 20 8C) (Fig. 1A), and in mean diameter by approximately 10% (Fig. 1B). In
contrast, anemones at both of the higher temperatures (25 and 308) lost about 63% of
body mass (Fig. 1A), and 30% of mean diameter (Fig. 1B). Percent changes in body
mass and pedal disk diameter did not depend on initial body size in any of the four
experimental groups (Regression analysis, pN0.05 for all temperatures and body size
parameters).
After 110 days, there was a significant effect of temperature on percentage change in
both polyp mass and diameter (ANOVA, F=29.52 and pb0.001 for mass, F=44.78 and
pb0.001 for diameter). The polyps at low temperature (15 and 20 8C) formed a
subgroup that differed significantly in both mass and diameter from those at high
temperature (25 and 30 8C), which formed a separate subgroup (Bonferroni multiple
comparisons post-test, pb0.001 for subgroups, Fig. 1). For polyps at the two high
temperatures (25 and 30 8C), there appeared to be a faster rate of mass change during
the first third (days 1–38) than the second two-thirds of the experiment (days 39–110,
Fig. 1A). For example, at 25 8C the polyps lost a total of 63% of their initial body mass
over the entire experiment, but more than half of this loss (37.5%) occurred during the
first third of the experiment (days 1–38). To assess this pattern statistically, the daily
percent change in body mass was calculated for each polyp as a linear approximation of
Table 1
Seasonal changes in the column diameter of polyps of the sea anemone A. equina, and in seawater temperature, at
three sites along the Mediterranean coast of Israel during March 2001–July 2002
Winter (January–March)
Spring (April–June)
Summer (July–September)
Site
MeanFS.D.
diameter (mm)
Temperature
(8C)
MeanFS.D.
diameter (mm)
Temperature
(8C)
MeanFS.D.
diameter (mm)
Temperature
(8C)
Habonim
n=41
Shikmona
n=36
Mikhmoret
31.6F7.5
(17–55)
30.7F7.0
(16–48)
20.4F10.3
(3–39)
n=66
26.5F6.8
(16–39)
n=43
17.4
27.8F4.7
(18–40)
30.8F7.2
(16–46)
27.7F10.6
(3–50)
n=39
30.4F8.2
(16–50)
n=34
22
27.6F6.7
(15–40)
25.6F5.1
(13–32)
14.6F10.0
(3–39)
n=69
25.2F4.9
(16–36)
n=30
28.7
Mikhmoret
Diameter
N15 mma
(N=30–43)
Mikhmoret
Diameter
V15 mma
(N=5–39)
9.1F4.2
(3–15)
n=23
17.1
17.4
17.4
17.4
9.6F6.1
(3–15)
n=5
19
19
19
19
6.5F2.4
(3–15)
n=39
28.7
29.5
29.5
29.5
The size ranges of anemones observed at each site are given in parentheses. Data were not collected during fall
(October–December) due to high wave conditions that prevented intertidal fieldwork.
a
Only in the Mikhmoret site did the number of individuals vary over the course of the study, and the only site
where we found young polyps.
O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
69
change for the first versus the second period. At 25 8C, this linear slope was
0.93F0.33% loss in body mass per day (X̄FSE, N=9 polyps) for first third versus
0.36F0.16% loss in mass per day for the second two-thirds of the experiment. A paired
t-test of the early versus late slopes for each polyp revealed a significantly faster rate of
change during the initial 38 days than later, at both of the high temperatures (25 and 30
8C, t=4.32, p=0.003, and t=4.05, p=0.001 respectively), but not at low temperatures (15
and 20 8C, t=1.16, p=0.264, and t=0.99, p=0.334 respectively, Fig. 1A). A repeated
measures ANOVA (Huynh-Feldt test with degrees of freedom correction for the withinsubjects factors and interaction terms) on differences among the four temperature groups,
with time as a factor, also revealed a significant effect of time for the high temperature
groups (25 and at 30 8C) ( F=28.43, df=1,25, pb0.001), but not for the groups at 15 and
20 8C ( F=2.10, df=1,35, p=0.135).
At all three field sites along the Mediterranean coast of Israel, polyps of A. equina were
significantly smaller during summer (July–September) than during winter (January–
March): Habonim (ANOVA, F=5.19; df=2,120; p=0.007); Mikhmoret ( F=20.61;
df=2,171; pb0.001); Shikmona ( F=8.41; df=2,105; pb0.001, Table 1).
4. Discussion
Our observation that weight changes are positive (40–70%) for A. equina polyps at low
temperatures, while at high temperatures they are negative ( 60%), may be explained on
the basis of the universal temperature dependence of animal metabolism in terms of
oxygen consumption rate (Griffiths, 1977b). Food intake apparently exceeds polyp
metabolic requirements under low winter temperatures and allows significant growth, but
is inadequate for meeting the demands of high respiratory metabolism at elevated
summertime temperatures of 25–30 8C. In the laboratory, the optimum temperature for
growth in A. equina appears to be 18.7–19.9 8C, as both growth rate and the amount of
food that anemones ingest decline above and below this range (Ivleva, 1964). We also
observed that changes in body weight were greater (40–70%) than those in pedal disk
diameter (10–30%, Fig. 1), which is expected because body mass is approximately
proportional to the cube of polyp radius.
Since growth rate did not vary significantly between the two lowest temperatures (15–
20 8C) or between the two highest (25–30 8C), it appears that the impact of temperature is
small over the 15–20 and 25–30 8C ranges, but strong for the 20–25 8C interval (Fig.
1A,B). There was no effect of initial adult size on temperature-related growth rates, similar
to our previous observations on feeding-related growth in this species (Chomsky et al.,
2004). These findings are compatible with existing information on sea anemones, which
shows that juveniles differ in their metabolism from adults, while adults of different sizes
are likely to have similar metabolic patterns and growth rates (Ivleva, 1964).
During the first 38 days of our experiment, the anemones may have adjusted to the
elevated temperatures of 25 and 30 8C, resulting in a decline in the rate of mass and
diameter loss during the following days (Fig. 1). This pattern may represent thermal
acclimation, involving the activation of appropriate respiratory isozymes, and the
denaturing of temperature inappropriate ones. Hochachka and Somero (1984) suggested
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O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
that evolutionary adjustment to local thermal regimes in latitudinally separated populations
also may involve the selection of enzymes appropriate to each locality. We observed a
decrease in mass loss during the second experimental period, of polyps collected in winter
and exposed to summertime temperatures (Fig. 1A). This rate of loss was almost equal
(0.39% day 1) to that of polyps collected in a separate experiment during summer (0.33%
day 1), when sea temperature was 29.5 8C (Chomsky et al., 2004). This pattern indicates
that since temperature increase in nature is quite gradual (for example: June 26.1 8C, July
28.7 8C and August 29.5 8C), animals in the summer study may have been acclimated
already to high ambient temperature. Our results are similar to those of Griffiths (1977a),
who derived rate–temperature curves of adult A. equina collected during summer and
winter, and found that summer animals acclimated to higher environmental temperatures
than did winter ones. Sassaman and Mangum (1970) also reported a trend of greater
metabolic adaptation in individuals from higher environmental temperatures, in three
species of sublittoral actinians.
During summer, the anemones at our field sites lost diameter at a rate of 0.1–0.2%
day 1, even though conditions apart from temperature appeared to be optimal for the
anemones in the eastern Mediterranean during this season. At these sites, the anemones
are submerged much of the time during summer, since the tidal range is 5 to +45 cm
relative to the ILSD (Israel Land Survey Datum), while in spring it is 20 to +20 (Israel
Oceanographic and Limnological Research, National Oceanographic Data Center, Report
H01/2000). Because sea anemones are sit-and-wait predators that feed only when
immersed, energy intake depends in part on immersion time, which is considerably
longer in summer than in spring. Also during the summer (June–September),
zooplankton abundance in most parts of the Mediterranean Sea is at its annual peak
(Rodriguez, 1983; Fernandez de Puelles and Jansa, 1992; Fonda-Umani, 1992; SiokouFrangou, 1996). Thus, it seems likely that the main factor contributing to polyp shrinkage
during summer is high sea temperature, which at our study sites is at the upper limit of
tolerance for this species.
In a population of the sea anemone Anthopleura elegantissima, body size also
decreases with increasing temperature, likely due to thermal effects on respiration (Sebens,
1980). Individuals at a single intertidal height (with the same immersion/feeding time), but
in tidepools of different sizes (with different maximum water temperatures at low tide)
vary in body size. In A. elegantissima, a seasonal increase in mean individual size also
coincides with an increase in zooplankton abundance (Sebens, 1983).
One of the problems with assessing temperature effects on growth in sea anemones is
that temperature also affects asexual reproduction. For example, in the intertidal sea
anemone Haliplanella luciae, as temperature rises, the size of individual anemones
decreases due to an accelerated rate of fission (Johnson and Shick, 1977; Minasian, 1982).
The sea anemone A. equina does not fission and thus is a good model for examining
effects of temperature on polyp growth rate. Another problem with temperature
experiments on sea anemones under laboratory conditions is that technical constraints
often lead to pseudoreplication. It is not possible to intersperse temperature treatments
within each aquarium, and so groups of anemones within each treatment often are cultured
separately. However, these physically segregated replicates have been used to test
temperature impacts on sea anemones in several studies and the results have not indicated
O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
71
inconsistencies due to aquarium effects alone (Navarro et al., 1981; Ortega et al., 1984;
Tsuchida and Potts, 1994). Our results in the present study (Fig. 1) also are as expected
based on past physiological work on this species (Ivleva, 1964), and do not indicate
random aquarium effects.
In some sea anemones (Actinia tenebrosa, A. elegantissima, A. xanthogrammica),
mean size fluctuations in the adult population also relate in part to the sexual reproductive
cycle (Ottaway, 1979a,b, 1980; Sebens, 1983). Adults reach maximum mean size at about
the time that gonads are fully developed, and revert to minimum mean size several months
later, after spawning. In A. equina, late fall and spring are characterized by reserve
accumulation. These periods coincide with peaks of gonadal development, which involve
high rates of glycogen and lipid synthesis (Rostron and Rostron, 1978; Gashout and
Ormond, 1979). We also observed an increase in polyp size during spring at the
Mikhmoret site prior to brooding. The mean size of large polyps (column diameterN15
mm) increased from 26.5 mm in winter to 30.4 mm in spring, and decreased to 25.2 mm in
summer. During this period, the number of small anemones increased from 5 to 39 (Table
1), so it appears that the brooding process may have caused the observed spring increase in
body size. In addition to providing the resources needed for sexual reproduction, energy
reserves accumulated during fall to spring also allow sufficient stores to survive the
summertime energy imbalance. Low metabolic rates during winter may reflect in part
depressed nutrient conditions, in which reduced metabolism operates as an energy
conserving mechanism (Ortega et al., 1988). These physiological processes contribute to
the ability of A. equina to overcome the high metabolic demands imposed by hot summers
in the eastern Mediterranean Sea.
Temperature is an important factor limiting the geographical distribution of sea
anemones. In the eastern Mediterranean Sea, polyps of A. equina do not extend southward
from Israel to the coast of Egypt, possibly due to high seawater temperatures that exceed
their physiological tolerance limits. Individuals of this species appear able to acclimate
successfully to low water temperatures, but not to those higher than maximal sea
temperatures in their local habitat (Griffiths, 1977a). In spite of the mitigating factors of
long submersion time and peak zooplankton supply during the summer in Israel, these
anemones appear unable to maintain their biomass at high summertime seawater
temperatures. We speculate that the prevalence of zooxanthellae in sea anemones, and
in coelenterates in general, in the year-round warm waters of tropical seas is due partly to
the inability of these animals to balance their increased metabolic requirements via
predation alone on the relatively sparse zooplankton usually occurring in tropical seas. The
photosynthate of algal endosymbionts thus provides the energy needed to balance the
energy budget of cnidarian hosts in the high-temperature tropics, where polyp metabolic
rates are high year-round (Falkowski et al., 1984).
Acknowledgements
This study was completed in partial fulfillment of the requirements for a doctoral
degree in Life Sciences at Bar Ilan University, awarded to O. Chomsky. Funding was
provided by a research grant from Bar Ilan University to N.E. Chadwick-Furman. [SS]
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O. Chomsky et al. / J. Exp. Mar. Biol. Ecol. 313 (2004) 63–73
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