Marie-Noële Croteau,
Catherine Munger, Isabelle Roy, Landis Hare and André Tessier.
INRS-Eau, Université du
Québec, C.P. 7500, Sainte-Foy, QC, Canada, G1V 4C7
Corresponding author: landis@inrs-eau.uquebec.ca
We conducted laboratory and field experiments to
determine if predatory insects take up Cd from their food or from water. In the
laboratory, we showed that both planktonic Chaoborus
larvae and benthic Sialis larvae take
up the majority of their Cd from prey. Because laboratory experiments can be
subject to artifacts, we tested our conclusions in nature by transferring Chaoborus larvae from a low-Cd lake to
mesh enclosures in a high-Cd lake where they were exposed to Cd in water and in
various concentrations of prey from the high-Cd lake. Once again, food was
confirmed to be the major Cd source for this animal. Given the importance of
food as a source of Cd, we measured the dependence of predator Cd
concentrations on prey ingestion rate and Cd assimilation efficiency.
Information on metal sources for animals is important for understanding metal
distributions in aquatic communities.
Animals can be used as biomonitors to estimate
pollution levels in ecosystems provided that an appropriate model is available
to relate pollutant concentrations in animals to those in their surroundings.
Such a model, grounded in biological and chemical theory, has been developed to
relate Cd concentrations in lakewater to those in the predatory insect Chaoborus (Croteau et al. 1998, Hare
& Tessier 1996, 1998). This relationship between animal and aqueous Cd
could be taken to infer that the animal’s Cd comes directly from water.
However, such a relationship could also be observed if the predator took up its
Cd from prey, that in turn took up their Cd from water. Information on routes
of metal uptake is lacking for most animals but is important for the
elaboration of reliable theoretically-based biomonitoring models. To fill this
knowledge gap, we determined the relative importance of food and water as Cd
uptake routes for two types of predatory aquatic insects: the phantom midge Chaoborus (Diptera), which feeds on
planktonic organisms, and the alderfly Sialis
(Megaloptera), which feeds on benthic animals. We also determined the
dependence of predator Cd on prey type, ingestion rate, and assimilation
efficiency.
To determine the relative importance of water and
food as Cd sources for larvae of Chaoborus
punctipennis (Say) and Sialis velata Ross in the laboratory, we created an experimental food chain
for each of these predators. Final instar larvae of C. punctipennis were exposed for 14 d to 109Cd in either
food alone or in both food and water (10 nM Cd). Food for this predator was the
cladoceran Ceriodaphnia dubia that
had been exposed for 1 d to 109Cd in both water (10 nM Cd) and their
food, the green alga Selenastrum
capricornutum (Munger & Hare 1997). Sialis
velata larvae were offered the chironomid Cryptochironomus that had in turn been fed a mixture of meiobenthic
organisms at one of 3 Cd concentrations (exposure to 3, 10 or 30 nM dissolved
Cd for 16 d; Roy & Hare 1999). Larvae of S. velata were fed daily for 4 d either one 109Cd-rich
prey (exposed at 1 of 3 109Cd concentrations) in 109Cd-free
water or one 109Cd-free prey in 109Cd-rich water (3, 10,
or 30 nM Cd). For both predators, Cd exposures were conducted in artificial
lake water of known composition to better control aqueous Cd speciation; we
estimate that >95% of the Cd in the predator exposure water was present as the free
metal ion, Cd2+. Detailed experimental and analytical methods for
our experiments with Chaoborus and Sialis are given in Munger & Hare
(1997) and Roy & Hare (1999), respectively.
We transferred final instar Chaoborus punctipennis larvae from a low- to a high-Cd lake where
they were held in mesh mesocosms (64-µm-mesh aperture) that allowed the free
passage of lake water but restricted the movement of planktonic crustaceans
that are the major food source for late instars of this insect. We offered C. punctipennis larvae in mesocosms
various quantities of a mixture of micro-crustacean prey (from 0 prey / larva
to 675 prey / larva) taken from the high-Cd lake and measured changes in their
Cd content over 16 d. Detailed experimental and analytical methods are given in
Munger et al. (1999).
We compared Cd uptake from prey by four Chaoborus species widespread in North
America, that is, C. albatus (Johnson), C. americanus (Johannsen),
C. flavicans (Meigen) and C. punctipennis. Twenty-five final-instar larvae of each of these Chaoborus species were collected from low-Cd lakes and placed
individually in 30-mL bottles filled with filtered (64-µm) water from a high-Cd
lake. Chaoborus larvae were held in
the dark at 5°C and fed ad libidum
Cd-rich calanoid copepods (Skistodiaptomus
oregonensis Lilljeborg)
collected from the high-Cd lake using a 64-µm plankton net. Both filtered lake
water and prey were renewed every 24 h by transferring each larva to a new
bottle filled with freshly collected filtered lake-water and copepods. Formalin
was added to the previous 24-h exposure bottles to preserve uneaten copepods
for later counting. On the basis of these samples we calculated daily ingestion
rates for each Chaoborus larva.
Larvae of each Chaoborus species were
sampled for measurement of mass and Cd content at days 0, 2, 4, 7, 10 and 14.
Detailed experimental and analytical methods are given in Croteau et al.
(2000).
In our laboratory experiment with Chaoborus punctipennis, no significant
difference was observed between either the slopes (p>0.05) or the y-intercepts
(p>0.05) of the regression lines for the “food + water” and the “food only”
treatments (Fig. 1), indicating that Cd bioaccumulation from water was
negligible.
Likewise, Sialis
velata larvae exposed to Cd via prey accumulated much more Cd than did
larvae exposed to Cd via water (Fig. 2). The Cd accumulated by S. velata larvae from food represented
approximately 85 % of the estimated total Cd
that this predator would have accumulated if it had been exposed to Cd in prey
and water simultaneously (assuming that Cd accumulated from food and water is
additive).
In our field experiment with Chaoborus, larvae exposed to Cd simultaneously in prey and water
showed a significant increase (P <
0.05) in their Cd content over time, whereas the Cd content of larvae exposed
to Cd in water only (Fig. 3, open squares) remained constant. There was little
difference in larval Cd content among treatment levels at high prey densities
(Fig. 3), likely because Chaoborus
larvae assimilate Cd less efficiency when they consume larger numbers of prey
(Munger & Hare 2000).
Figure 1. Accumulation over
time, in the laboratory, of Cd (means ± 95% CI) by the predator Chaoborus punctipennis from either “food
only” or from both “food + water”. Food for the predator was the cladoceran Ceriodaphnia dubia that had been exposed
to Cd in both water and its algal food (Selenastrum
capricornutum). Redrawn from Munger & Hare (1997).
Figure 2. Variation in the rate at which Sialis velata larvae accumulated Cd
(means ± SD) as a function of
aqueous Cd concentrations in the exposure media of this predator and its prey (Cryptochironomus). Larvae were exposed
to Cd for 4 d in either water or prey. Redrawn from Roy & Hare (1999).
Figure 3. Increases above initial values (means ±
SE, n = 3) in the Cd content of Chaoborus
punctipennis larvae exposed in mesocosms to water and crustacean prey from
a Cd-rich lake at nominal prey : predator ratios from 0 to 675. Lines are model
predictions and experimental data are represented by symbols. The slope of the
line for the nominal ratio of 0 prey per predator (open squares) is
not significantly different from zero (P >
0.05). Redrawn from Munger et al. (1999).
Our finding that food is the major Cd source for C. punctipennis and S. velata agrees with those obtained for several other freshwater animals (e.g., Timmermans et al. 1992, Stephenson & Turner 1993). The results of other studies suggesting that food is a negligible Cd source for freshwater invertebrates are questionable due to flaws in their experimental designs (Munger et al. 1999). In more general terms, our experimental results indicate that models designed to trace the dynamics and fate of metals in communities of aquatic animals should not be based solely on metal uptake from water, but are likely to be improved by including metal transfer along trophic pathways. Our results also suggest that food should not be excluded a priori as a Cd source for animals in laboratory experiments and toxicity tests, since doing so would likely result in the under-estimation of Cd accumulation and toxicity with a concomitant risk for the environment.
Larvae of the four Chaoborus species increased in weight and Cd content during our 14
d feeding experiment (Croteau et al. 2000). Increases were greater for the
large-bodied species (C. flavicans, C. americanus) than for the small-bodied
ones (C. albatus, C. punctipennis). However, the rates at
which these four species ingested
prey differed little, suggesting that differences in ingestion rates among
species cannot explain their differences in weight or Cd content. The
explanation for these differences among species appears to reside in the
efficiency with which they assimilate Cd and essential nutrients. We estimated Cd assimilation
efficiencies (AE`s) for the four Chaoborus
species using a bioaccumulation model (Croteau et al. 2000). Cadmium AE`s were
low (» 6-7 %) for the small-bodied species C. albatus and C. punctipennis; similar Cd
accumulation by these species suggests that they could be treated as a unit for
Cd monitoring purposes. In contrast, larvae of the large-bodied
species C. flavicans and C. americanus had much higher Cd AE`s (» 40 %), which likely explains their higher Cd
concentrations both in our experiment and in nature (Croteau et al. 2000).
Grouping small and large-bodied species would likely result in some loss of
predictive power for a generic-level biomonitoring model (Croteau et al. 1998).
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