LIMNOLOGY
AND
I
December 1994
OCEANOGRAPHY
Limnol. Oceanogr., 39(8), 1994, 1783-1789
0 1994, by the American
society of Limnology
and Oceanography,
Volume
39
Number
8
Inc.
Retention of elements absorbed by juvenile fish
(Menidia menidia, Menidia beryllina) from
zooplankton prey
John R. Reinfelder’ and Nicholas S. Fisher
Marine Sciences Research Center, State University of New York, Stony Brook 11794-5000
Abstract
Radiolabeled copepods (Acartia spp.) were fed to juvenile silversides (Menidia menidia and Menidia
to study element absorption in the fish. Copepods were reared from nauplii in the presence of
different radiotracers (i*C, lo9Cd,57Co,32P,35S,‘?Se, or “‘Zn) and were analyzed for relative concentrations
of these elements in their tissue fractions. Copepod exoskeletons contained nearly all of the trace metals
(>97%), 60% of the Se, and less than half of the C, P, and S accumulated by the copepods. Within the
nonexoskeleton tissues of the copepods, nonpolar (CHCl, extractable) material contained 34 and 24% of
the total C and P, but only 8 and 2% of the total S and Se
Absorption efficiencies of trace metals in juvenile silversides (2.7% for Cd, 2.1% for Co, 6.2% for Zn)
were an order of magnitude lower than those for nonmetals (29% for Se, 50% for S and C, 60% for P).
The absorption efficiencies in the juvenile silversides of all seven elements studied were directly related
to the percent of each element in the nonexoskeleton fraction of the copepod prey, indicating that the
fish absorbed the soft tissues of the copepods and egested the chitinous exoskeleton and its associated
elements.
beryllina)
Although trace metal concentrations
and
concentration factors generally decrease from
algae to fish in aquatic food webs, the accumulation of harmful levels of trace metals
through the ingestion of contaminated food is
still a threat to aquatic carnivores and the animals that consume them (Rainbow 1989). In
carnivorous
fish, trace metal accumulation
’ Present address: Department of Geological and Geophysical Sciences, Guyot Hall, Princeton University,
Princeton, New Jersey 08544-1003.
Acknowledgments
We thank J. Hare and three anonymous reviewers for
helpful comments.
This research was supported by National Science Foundation grant OCE 8810657 and by NOAA award
NA90AA-D-SG078 to the Research Foundation of SUNY
for the New York Sea Grant Institute.
Contribution 961 from the Marine Sciences Research
Center.
from food has been reported to be higher than
direct accumulation
from water (Pentreath
1973a,b, 1976; Willis and Sunda 1984; Dallinger and Kautzky 1985). Despite such evidence, the trophic transfer of essential and toxic elements in aquatic organisms has received
little attention from regulatory agencies that
rely on models concerned exclusively with accumulation from the dissolved phase. The digestive processing of elements by pelagic consumers can also influence the geochemical
cycling of trace elements in the ocean because
the animals package ingested elements into fecal pellets that sink rapidly (100-l ,000 m d- ‘)
out of surface waters (Fowler and Knauer
1986). Without quantitative study of the processes involved in the trophic transfer of elements from herbivores to carnivores in marine
ecosystems, however, it is difficult to predict
the fate of elements in marine systems.
The accumulation
of trace metals in sec-
1783
1784
Reinfelder and Fisher
ondary consumers has been studied in predators fed radiolabeled prey, but prey were often
radiolabeled for relatively short periods of time
before presentation to the predator (Fowler and
Benayoun 1976; Pentreath 1973a,b, 1976).
Under these conditions, slowly exchanging tissues may not accumulate sufficient radioactivity for the pathways of elements in such tissues
to be followed. Moreover, tissues synthesized
during larval or juvenile stages of a prey organism’s life may not be radiolabeled if only
adult individuals
are exposed, precluding the
uniform labeling of the prey’s tissues. Metal
accumulation experiments in which consumers are fed prey in which only some tissues are
radiolabeled can only yield information about
the trophic transfer of elements from portions
of the prey.
The quantitative study of the trophic transfer of elements in marine animals requires information about the efficiencies with which
predators absorb elements from ingested prey,
since only absorbed elements are metabolized
by consumer animals or transferred to higher
carnivores. Absorption efficiency, defined here
as the fraction of an ingested substance absorbed across the gut lining, is an essential parameter in contaminant
bioaccumulation
models (Thomann 198 1; Luoma et al. 1992).
We measured the absorption efficiencies of
seven elements in juvenile planktivorous
fish
(Atlantic and inland silversides, Menidia menidia and Menidia beryllina) fed copepods
(Acartia spp.) that had been reared from nauplii in the presence of radiotracers in the phytoplankton food and in the dissolved phase.
Long-term exposures to the radiotracers were
necessary to produce uniformly radiolabeled
copepods (i.e. copepods in which the specific
activity is constant in all fractions).
The seven elements examined (C, Cd, Co,
P, S, Se, and Zn) display a wide range of assimilation
efficiencies in marine herbivores
(Reinfelder and Fisher 199 1, 1994), but relatively little is known about their assimilation
in planktivorous
fish.
Materials and methods
Juvenile Atlantic silversides (M. menidia)
were obtained from a stock of fish reared at
the Flax Pond Laboratory of the State University of New York at Stony Brook,
_- and juvenile inland silversides (M. beryllina) were
obtained from Aquatic Biosystems Inc., Fort
Collins, Colorado. Prior to feeding experiments, the silversides were held at 18°C in aerated glass-fiber-filtered
seawater (27oroo>and
were fed brine shrimp nauplii (Artemia salina)
ad libitum. Assimilation
efficiencies of elements were measured in Menidia spp. fed adult
Calanoid copepods (Acartia spp.) which had
developed from nauplii in the presence of particulate (phytoplankton)
and dissolved radiotracers.
Acartia nauplii (identification confirmed for
adult individuals)
were collected from Stony
Brook Harbor, Long Island, New York, with
a 63-pm-mesh plankton net and were separated from other zooplankton with a Pasteur
pipette. Once isolated, the nauplii were transferred to glass-fiber-filtered seawater (277~) and
fed uniformly radiolabeled diatoms (Thalassiosira pseudonana) or prymnesiophytes
(Zsochrysis galbana). Phytoplankton cells fed to
the developing copepods were exposed to 14C,
109Cd
57Co
32p
35S, 75Se, or 65Zn. Two pairs
of rahioiso;opes,
75Se-65Zn and 109Cd-57Co,
were used to produce double-labeled phytoplankton cells. The peak y emissions of the
two radionuclides in each pair were measured
with a minimum of spillover, which was corrected for in all dual-radiotracer
experiments
(see below). Cells were grown in sterile-filtered
seawater (0.2~pm Nuclepore filters; SFSW) enriched with modified f/2 nutrients (Guillard
and Ryther 1962). T. pseudonana was exposed
to 14C, lo9Cd, 32P, 75Se, and 65Zn; I. galbana
was exposed to lo9Cd, 57Co, and 35S. Diatoms
labeled with lo9Cd and 32Pwere grown in SFSW
enriched with f/2 N, P (f/50 P for 32P), Si, and
vitamins and with f/ 10 trace metals minus Cu,
Zn, and EDTA. For 75Se and 65Zn exposures,
diatom cells were grown in f/2 N, P, Si, and
vitamins and f/50 trace metals minus Cu, Zn,
and EDTA. 14C-radiolabeled diatoms were
grown in SFSW with complete f/2 enrichment.
Radionuclide additions to the diatom cultures
were 100 kBq liter-l of 14C as NaH14C03 in
distilled water, 148 kBq liter-’ (69.7 pM) of
lo9Cd in 0.1 N HCl, 37 kBq liter-l (1 nM) of
32P as NaH232P04 in distilled water, 37 kBq
liter-l (0.14 nM) of 75Se as selenite in 0.5 N
HCl, and 111 kBq liter-’ (67 PM) of 65Zn in
0.1 N HCl (1 Bq = 1 dps).
I. galbana cells labeled with lo9Cd and 57Co
were prepared in the same way as logCd ra-
Element absorption in Jish
diolabeled diatoms, except that trace metal enrichments were f/20 minus Cu, Zn, and EDTA.
35S-labeled I. galbana cells were grown in SFSW
diluted to 160/00to minimize dilution of the
radiotracer by 32S, with complete f/2 enrichment (minus Si). Radionuclide additions to the
I. galbana cultures were 36.9 kBq liter-l (17.4
PM) of lo9Cd in 0.1 N HCl, 6 10 kBq liter-’
(37.5 PM) of 57Co in 0.1 N HCl, and 6.7 MBq
liter-l of 35S as Na235S04 in distilled water.
Radiolabeled phytoplankton
were collected
by filtration (diatoms) or centrifugation (I. galbana) and were resuspended in 500 ml of glassfiber-filtered seawater (27o/oo)to yield a cell density of lo5 cells ml-l (2.2 mg liter-‘, T. pseudonana; 1.6 mg liter-l, I. galbana). Copepod
nauplii were reared on radiolabeled phytoplankton for 2-3 weeks, during which time
they developed into adult copepods. The radiolabeled phytoplankton cell density (1 O5cells
ml-l) was maintained in all copepod feedings
throughout the development period, with additional radiolabeled phytoplankton added periodically to maintain constant cell density.
Copepods were exposed to radiotracers in their
food and dissolved in the ambient seawater.
Assuming equilibrium partitioning between the
phytoplankton
and the water during the copepod feedings, the copepods were exposed to
dissolved concentrations of 100-400 fM lo9Cd,
2 10 fM 57Co, and 3.9 pM (j5Zn, representing
99% of the total lo9Cd and 57Co activity and
76% of the total 65Zn activity (phytoplankton
plus dissolved activity). Developing copepods
were therefore exposed to significant amounts
of dissolved trace metals approximating
natural conditions in which particle concentrations are low. It was assumed that any C, P,
S, or Se lost from the phytoplankton
into the
dissolved phase in the feeding suspensions
would not be accumulated by the copepods in
significant amounts. Higher yields of adult copepods were obtained when nauplii were fed
I. galbana than when they were fed T. pseudonana, possibly because I. galbana has no cell
wall and these cells may be easier to digest.
Absorption eficiency experiments
Radiolabeled copepods were removed from
their feeding suspensions with a Pasteur pipette and gently rinsed with radioisotope-free
glass-fiber-filtered seawater on a submerged 1Ohm Nitex mesh. Twenty to forty of the cope-
1785
pods labeled with y-emitting radiotracers were
assayed for radioactivity
and then transferred
to plastic beakers containing 100 ml of glassfiber-filtered seawater (27%0, 18OC) for feeding
to the silversides. Ten to fifteen of the copepods labeled with P-emitting radiotracers were
killed for scintillation
counting, and the remaining copepods were fed to the silversides.
Three silversides (5-l 0 mg dry wt each) which
had been starved for 12 h just before the experiment were added to each beaker and allowed to ingest all the copepods. M. menidia
was fed copepods labeled with 14C, 32P, 75Se,
or (j5Zn; M. beryllina was fed copepods labeled
with lo9Cd, 57Co, or 35S. No fecal matter was
produced during feeding. After all the copepods had been eaten (l-4 h), the silversides
were transferred to radioisotope-free
glass-fiber-filtered seawater and fed unlabeled Artemia for 20 h to enable them to clear their guts.
In a preliminary study, we found that silversides egested the copepod remains within a few
hours when fed Artemia ad libitum. The radioactivities
retained in the silversides were
measured after gut clearance and pooled for
the three fish in each replicate beaker. Absorption efficiencies were calculated by dividing the amount of retained radiotracer by the
amount ingested.
In addition, 1O-l 5 radiolabeled copepods
from the same pool of animals that were fed
to the silversides were subjected to biochemical fractionation. Copepods were collected on
a 1O-pm polycarbonate filter, rinsed with glassfiber-filtered seawater, and extracted in 1 ml
of 0.2 N NaOH at 45°C for 1 h. The copepod
exoskeletons remaining after this extraction
were collected on a glass-fiber filter (GFK) and
rinsed with 1 ml of 0.2 N NaOH. The soluble
tissue filtrate was collected in a small glass test
tube to which 1 ml CHC13 was added. This
mixture was vigorously shaken, and two phases
were allowed to form (10 min). The polar phase
(containing proteins, polysaccharides, nucleic
acids, and small soluble compounds) was removed with a Pasteur pipette; the lower, nonpolar phase (containing lipids) was washed
twice with 0.5 ml of 0.2 N NaOH, and these
washes were combined with the original upper
phase. Copepods exposed to logCd, 57Co, or
65Zn were washed with 1O-3 M EDTA in seawater for 3 min before the NaOH extraction
to remove surface-bound metal that may have
Reinfelder and Fisher
1786
Table 1. Distribution of radiotracers in different fractions of uniformly radiolabeled copepods (Acartia spp.).
Values are percent of total accumulated radioisotope in
1O-l 5 individuals, depending on isotope.
Radiotracer
14C
‘09Cd
=co
32P
3%
75Se
65Zn
Polar
23.8
2.5
2.48
44.9
58.6
39.0
1.5
Nonpolar
34.2
0.1
0.02
24.3
8.3
1.8
0
Exoskeleton
42.0
97.4
97.5
30.8
33.1
59.2
98.5
been mobilized by NaOH and collected in the
soluble tissue fractions. The radioactivity
removed by the EDTA was included in the exoskelton fraction.
y-emitting isotopes were measured with a
Pharmacia-Wallac
LKB gamma counter
equipped with a well-type NaI(T1) crystal. The
y emissions of 57Co were measured at 122 keV,
of 75Se at 264 keV, and of 65Zn at 1,115 keV..
The radioactivity
of logCd was quantified by
measuring its X-ray emissions at 22 keV. The
p emitters (14C, 32P, and 35S) were measured
with an LKB Rack Beta liquid scintillation
counter. Before measuring the p activity of the
silversides, the fish were incubated in 1 ml of
Solvable Tissue Solubilizer (NEN) at 45°C for
- 3 h. After adding 10 ml of Aquasol (scintillation fluor) to the solubilized silversides, 330
~1 of 3 N HCl was added to quench the chemiluminescence
from the tissue solubilizer.
Quenching of P-emitting samples was corrected by the external standards ratio method.
Counting times were adjusted so that propagated counting errors were I 5%. Background
radioactivity
of the fish was negligible.
Results and discussion
In the radiolabeled adult copepods, nearly
all of the logCd, 57Co, and 65Zn was found in
the exoskeleton (Table 1). In contrast, only 3 l42% of the copepods’ total body burdens of
14C, 32P, and 35S and almost 60% of the 75Se
were associated with the exoskeleton. Within
the soft tissues, logCd, 57Co, 35S 75Se and 65Zn
were predominantly
associated with’ the polar
fraction, while 14C and 32P were more evenly
distributed between the nonpolar and polar
fractions. The even distributions
of C and P
among the polar, nonpolar, and exoskeleton
fractions of copepods are not surprising given
the biochemical roles of these two elements in
living tissues.
Sulfur was mainly associated with soluble,
polar tissues in the copepods and to a lesser
extent with the copepod exoskeleton (Table 1).
Sulfur in the exoskeleton fraction of the copepods was probably in chitin-associated proteins. The distribution
of Se among different
fractions of animal tissues was not similar to
that of S, despite the fact that these two group
6A elements behave similarly in biological systems (Wrench and Campbell 198 1).
The accumulation
of strongly particle-reactive trace metals such as Am, Pb, and Pu in
small planktonic animals is directly related to
the animal’s surface area (Fisher and Fowler
1987; Michaels and Flegal 1990) indicating
the predominance of surface accumulation directly from seawater. Previous studies have
also identified adsorption of dissolved metal
to copepod exoskeletons as an important path. way of trace metal accumulation (Martin 1970;
Sick and Baptist 1979). Although the three trace
metals studied (Cd, Co, and Zn) were found
overwhelmingly
in association with copepod
exoskeleton (Table l), much of this exoskeleton-associated metal may have been accumulated via ingested food. Bertine and Goldberg (1972) found high concentrations of Co
and Zn in the carapaces of pelagic shrimp,
whose large size would be expected to diminish
the importance of uptake via surface adsorption (Michaels and Flegal 1990). Similarly,
Fowler et al. (1970) found 3 5-4 1% of the total
body burdens of 65Zn in the exoskeleton of
euphausiids, prawns, and shrimps when accumulation was from ingested food. These results were attributed to the rapid mobilization
of Zn from crustacean guts to other tissues,
including the inner layers of the exoskeleton
(Fowler et al. 1970). Cd, Co, and Zn are much
less particle reactive than metals such as Am
or Pb (IAEA 1985) and Cd and Zn have higher
assimilation efficiencies than these other metals in planktonic herbivores (Reinfelder and
Fisher 199 1, 1994). Significant proportions of
the body burdens of Cd, Co, and Zn in herbivorous copepods may therefore be accumulated in the gut from ingested food and then
deposited in exoskeleton tissues as a means of
detoxification
or storage.
Absorption
efficiencies in juvenile silver-
Element absorption in jGh
sides fed radiolabeled copepods ranged from
2.1% for 57Co to 60.4% for 32P (Table 2). The
lowest assimilation efficiencies were for the
three trace metals (Table 2). The nonmetals,
14C, 32P, and 35S, were assimilated by the silversides with efficiencies that ranged from 50.2
to 60.4%, but the fish only assimilated 29% of
the metalloid 75Se. As major components of
essential biochemicals, C, P, and S were expected to have high absorption efficiencies in
the silversides. Their absorption efficiencies
were, in fact, the highest in this study but were
somewhat lower than carbon assimilation efficiencies reported for carnivorous fish (Welch
1968) and planktonic carnivores (Alldredge
1984). Absorption efficiencies of the nonmetals may have been lower in our study because
the fish were fed only copepods, whose chitinous carapace is difficult to digest. In addition,
excreted and respired radiotracers,
which
would have contributed to assimilated C, P,
and S pools, were not quantified because dissolved levels in the feeding suspensions were
below detection.
The absorption efficiencies of the three trace
metals in this study compared well with those
measured in different species of marine and
freshwater fish. Silversides absorbed Cd with
an efficiency (2.7%) within the ranges reported
for rainbow trout (Salmo gairdneri) (0.5-5.4%;
Kumada et al. 1980) and guppies (Poecilia reticulata) (1.6-4.1%; Hatakeyama and Yasuno
1982). Low Cd absorption efficiencies in carnivorous fish are consistent with the observations of Macdonald and Sprague (1988), who
found much lower Cd concentrations in arctic
cod than in their prey, which included copepods. Co absorption efficiencies in silversides
fed copepods (2.1%, this study) were similar
to those in plaice fed radiolabeled worms (3.5%,
Pentreath 19733) but were lower than in plaice
fed labeled gelatine (26%) or starch (72%) pellets (Pentreath 19733). Absorption efficiencies
of Zn were also higher in fish fed artificial foods
than in those fed natural prey organisms (Pentreath 1973a). The behavior of radiotracers in
fish fed artificial foods is probably not representative of the behavior of elements in natural
systems because such foods may lack the refractory components (e.g. exoskeleton or insoluble granules) found in natural prey organisms which would likely contribute to lower
absorption efficiencies (Nott and Nicolaidou
1787
Table 2. Silversides (Menldu spp.) fed uniformly radiolabcled copepods (Acartia spp.): radioactivity
ingested
and retained, and radiotracer assimilation efficiencies (AE).
Radiotracer
‘T
‘09Cd
5’C0
‘2P
‘?3
‘3e
h5Zn
* Mean
asslmllatlon
RadioactIvIty
Ingested
Retamed
17.2
9.64
3.13
0.792
0.900
0.282
1.34
0.84 1
0.3 13
3.39
2.06
I .65
I .30
0.612
0.337
6.28
5.15
4.85
6.48
35.2
18.7
172.0
26.5
23.0
14.2
47.4
39.5
21.9
6.36
3.18
2.39
2.39
1.16
0.707
19.7
19.7
96.3
87.6
etlhencles
(Bq)
calculated
in replicate
AE (%)*
50- 1.9
31 1.0
2 to.7
602 7.8
50+ 1.9
29k4.1
6+ 1.7
expenmrnts.
i I \I)
1990). The average absorption efficiency of Zn
in plaice fed worms was about three times
higher (18%; Pentreath 1976) than that measured in silversides fed copepods (6.2%). Based
on these laboratory results and the field study
of Cross et al. (1975), who measured higher
assimilation efficiencies of Zn in three species
ofjuvenile fish than of the other metals studied
(Cu, Fe, and Mn), it would seem that Zn is
generally more bioavailable to fish than these
other trace metals.
The Se absorption efficiency measured in
silversides was 29%. This relatively low efficiency may have been because 59% of the Se
in the copepods was associated with the exoskeleton, similar to the 6 1% found in pelagic
shrimp (Bertine and Goldberg 1972). Fowler
and Benayoun (1976), however, found in shortterm exposure experiments that < 10% of the
total Se was in the exoskeleton of the euphausiid Meganyctiphanes norvegica. Longer exposures may be required to radiolabel euphausiid exoskeleton because euphausiids,
unlike copepods, molt continuously as adults.
Our results suggest that less Se is bioavailable
for crustacean-consuming
carnivores than for
marine herbivores, in which efficiencies are
Reinfelder and Fisher
i
0
0
I
I
I
I
20
40
60
80
1
Percent of element associated with the
nonexoskeleton tissues of ingested copepods
Fig. 1. Absorption efficiencies
sides (Menidia spp.) fed copepods
with the percent of each element
tissues of the ingested copepods.
0.798~ + 1.32, r2 = 0.979. Error
of elements in silver(Acartia spp.) compared
in the nonexoskeleton
Equation of line: y =
bars indicate 1 SD.
> 85% (Fisher and Reinfelder 199 1; Luoma et
al. 1992; Reinfelder and Fisher 1994). Therefore, the trophic transfer of Se to marine carnivores should be greater than that of trace
metals and less than that of bulk organic matter.
The absorption efficiencies of the seven radiotracers in the juvenile silversides were directly related to the compartmentalization
of
each in the nonexoskeleton tissues of the copepod prey (Fig. 1). This relationship was described by the geometric mean regression line
(Ricker 1973) that had a slope of 0.798 kO.059
and an intercept of 1.32* 1.9 (r2 = 0.979, SEs
based on Tukey’s Jacknife procedure described by Sokal and Rohlf 198 1). The slope
of the regression line suggests that almost 80%
of the elements associated with the soft (nonexoskeleton) tissues of crustacean zooplankton
is available to be absorbed by juvenile planktivorous fish (absorption efficiency = 0.8 x
soft-tissue fraction of element). Elements associated with crustacean carapaces and that
fraction (20%) of the soft tissues which is not
retained will be packaged by the fish into fecal
pellets. These pellets can sink rapidly out of
surface waters (Robison and Bailey 198 1) and
contribute significantly to the vertical flux of
the elements packaged therein (Fowler and
Knauer 1986).
The assessment of contaminant accumulation in aquatic food webs has suffered from
the lack of reliable information
about assimilation efficiencies and physiological turnover
rates of individual contaminants in consumer
animals. As more data become available, these
parameters of contaminant bioaccumulation
models can be subjected to more rigorous sensitivity analysis, and the models can be applied
to field conditions with greater authority. For
example, Luoma et al. (1992) considered assimilation
efficiency and turnover rate in
quantifying Se accumulation in the clam Mucoma balthica and showed that Se accumulation in this organism was dominated by uptake
from food. Absorption efficiencies of ingested
elements can be used to calculate concentration factors in fish according to the equation,
modified from Thomann (198 l),
wish
= WE
x I)/@ + G)]CF,,
(g element)(g fish) -I
= (g element)(g water)-’ .
(1)
CFfish and CF,, are the trace-element concentration factors in the fish and the zooplankton
food (g g-l), AE is the trace-element absorption efficiency defined as the proportion of ingested trace element retained by the fish (O/o),
I is the weight-specific ingestion rate (O/otime- I),
k is the first-order rate constant of physiological turnover of assimilated element (timeel),
and G is the first-order growth rate constant
of the fish (time-‘). It is important to note that
there is considerable uncertainty around each
of the parameters in Eq. 1 (which ignores accumulation in fish directly from the dissolved
phase); thus, application of this model to most
elements and marine organisms is currently
difficult. Consequently, studies that provide element-specific data for each of the parameters
in Eq. 1 are needed to develop predictive models of element accumulation
in marine food
chains.
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Submitted: 14 March 1994
Accepted: 21 June 1994
Amended: 14 July 1994