Environmental Health Perspectives Volume
103, Supplement 4, May 1995
[Citation
in PubMed] [Related
Articles]
Commentary on Effects of Anthropogenic and Natural Organic Chemicals
on Development, Swimming Behavior, and Reproduction of Daphnia, a
Key Member of Aquatic Ecosystems
Stanley I. Dodson1 and Takayuki Hanazato2
1Department of Zoology, University of Wisconsin, Madison,
Wisconsin; 2National Institute for Environmental Studies, Onogawa,
Tsukuba, Japan
Abstract
Because of their trophodynamic role, small invertebrates are often critical
components of ecosystems. An especially important group of freshwater invertebrates
is the water fleas of the genus Daphnia. These animals are often
the dominant herbivores in lakes and ponds. They play a key role in determining
water clarity (by grazing on algae) and they are an important part of the
diet of fish. Natural chemical signals (kairomones) produced by predators
affect the development, life history strategy, and behavior of zooplankton.
Laboratory studies of anthropogenic chemicals that have biological activity
(xenobiotics), such as the insecticide carbaryl, have demonstrated effects
of concentrations in the 1 to 5 ppb range on Daphnia development,
growth rate, and swimming behavior in our laboratory experiments. Low concentrations
of carbaryl inhibit growth and reproduction and delay maturation, whereas
survivorship was not effected. These sublethal exposures to carbaryl reduced
Daphnia population growth rate (productivity) by about 15% (at 5
ppb), enough to have significant ecological effects on the rest of the lake
community. The insecticide carbaryl showed synergistic interactions with
natural chemicals associated with predators (kairomones) that modify Daphnia
development and life history characteristics. In addition, there were complex
synergisms between carbaryl, the predator odors, and oxygen concentration
(low oxygen concentration can be either a natural environmental stress or
an anthropogenic stress). Daphnia produce males facultatively, usually
in late fall; at other times, reproduction is asexual. There is some evidence
from long-term field studies that the maximum frequency of males has declined
since the 1940s, when estrogen-mimicking xenobiotics first appeared in lakes.
A decrease in sexual recombination will result in maladapted Daphnia
relative to their constantly changing environment. -- Environ Health
Perspect 103(Suppl 4):00-00 (1995)
Key words: Daphnia, Chaoborus, carbaryl, kairomone, development,
life history, swimming behavior, estrogenic, sex ratio, fitness
This paper was presented at the Conference on Environmentally
Induced Alterations in Development: A Focus on Wildlife held 10-12 December
1993 in Racine, Wisconsin.
We thank Piotr Dawidowicz, Matt Brewer, and Pat Gorski
for reading drafts of this manuscript and for their helpful comments. Bill
Feeny produced the beautiful food web, and Terry Mika helped grow the algae
to feed the Daphnia cultures for many of the experiments. Thanks
to Theo Colborn for inspiration and to Drs. Iwakuma and Yasuno for their
continuing support. T Hanazato was supported by a Fellowship from the Science
and Technology Agency, Government of Japan, and by a Guyer Fellowship,
Department of Zoology, University of Wisconsin-Madison.
Address correspondence to Dr. Stanley Dodson, Department
of Zoology, Birge Hall, University of Wisconsin, 430 Lincoln Drive, Madison,
WI 53706. Telephone (608) 262-6395. Fax (608) 262-9083.
Introduction
The larger species of wildlife, such as eagles, alligators, and pumas,
interact with and depend on an ecological support structure in which the
major players are invertebrates. Although individually small and inconspicuous,
invertebrates play major roles in the transfer of energy from autotrophs
to the tips of the food web.
The long-term goal of our research is to understand how planktonic communities
work in terms of population dynamics of the individual member species, energy
flow among species, and patterns of species diversity and phenology. A current
and fundamental question concerns the influence of natural and anthropogenic
chemicals in inducing changes in the development, life history strategy,
and behavior of zooplankton (1-4).
Results of studies of zooplankton have shown that many species depend
on chemical signals, in natural situations, for optimal development. For
example, the phenomenon of cyclomorphosis (an annual change in morphology
seen from generation to generation, in which some species have long spines
and helmets during the summer) is cued by a combination of physical conditions
and natural chemical signals (kairomones) produced by predacious fish and
invertebrates (5). Zooplankton also modify their life history and
reproductive strategies (e.g., rate of maturation, size
and number of eggs) in response to kairomones. Similarly, zooplankton swimming
behavior, especially diel vertical migration (during which zooplankton populations
move deeper in the lake during the day, and rise at night), depends on the
presence of kairomones (6,7).
Anthropogenic chemicals can induce changes that mimic the effects of
natural kairomones (8-10). For example, xenobiotics and natural chemical
signals show both direct and synergistic effects on zooplankton development
(11,12). The purpose of our current research is to understand how
natural and anthropogenic chemicals interact in lakes to induce changes
in the development, behavior, and ultimately the community ecology of zooplankton.
To study zooplankton development and behavior, we have focused on laboratory
cultures of the cladoceran (water flea) Daphnia. Daphnia are
ideal representatives of the zooplankton partly because of the ease with
which they are cultured in the laboratory and partly because of their key
position in aquatic food webs (Figure 1). Daphnia species (along
with their smaller cousins Ceriodaphnia) are often used in laboratory
bioassays of kairomones (13) or potentially toxic chemicals (14-16).
Daphnia occupy a key position in aquatic food webs because they are
often the most significant herbivore (17) by determining water quality
through their selective consumption of algae (18) and providing a
major dietary component for several fish species (19), and because
of their large size, high rate of reproduction, and lack of an effective
escape response.
Figure 1. An idealized
food web for a freshwater lake showing the position of Daphnia as
an herbivore that affects both algae and fish abundances.
Daphnia in lakes, like other zooplankton and unlike larger animals
higher in the food web, typically contain (bioaccumulate) only low levels
of toxic xenobiotics. For example, Daphnia in Lake Ontario contained
only about 1 ppb PCB and 10 ppb DDT in the 1980s (20). These levels
do not even approach levels of acute toxicity (14,21). However, Daphnia
ecology can be modified significantly by low to moderate sublethal concentrations
of toxic xenobiotics (22,23). The nonlethal effects we have studied
can be divided into three general categories: a) development and
life history, b) swimming behavior, and c) reproductive effects.
Developmental and Life History Effects
Daphnia morphology determines much of their life history strategy
(2). For example, smaller body size tends to reduce feeding rate,
reduce mortality from fish, and increase the chance of being eaten by invertebrate
predators such as Chaoborus. The typical Daphnia response
to either kairomone or the insecticide carbaryl (Table 1) is a reduction
in body length, longer developmental time to maturity, and at high levels
of pesticides, induction of morphological defenses such as higher
helmets, longer tail spines, or neck teeth.
We have found several synergistic interactions between carbaryl and the
Chaoborus kairomone. Carbaryl and kairomone typically interact to
further reduce adult body size and juvenile growth rate (Table 2). When
oxygen stress is combined with carbaryl and kairomone (Table 3), there are
further synergistic reductions in body size and growth rate (12).
Another stress factor, pH, may have a similar synergistic interaction with
the natural and anthropogenic chemicals (24).
Swimming Behavior
Zooplankton (especially copepods, but including cladocerans such as Daphnia)
show complex swimming behavior that is necessary for proper nutrition and
to avoid predators. On a small scale, many zooplankton have a fast swimming
escape response used to avoid predators (25), and zooplankton may
have the ability to maintain their position in food patches (26).
At a large scale, zooplankton often show diel vertical migration, in which
they sink lower in the lake during the day to avoid fish and rise at night
to take advantage of the warmer water near the surface (2). Results
from laboratory studies of individual swimming behavior show that swimming
behaviors can be modified by exposing the zooplankton to various predators
or by exposure to toxic xenobiotics.
Our lab uses a video system to record and digitize the three-dimensional
swimming track of individual zooplanktonic animals (4,27). This system
can be used to study behavior of zooplankton from field populations or in
laboratory experiments and behavioral bioassays. For example, Dodson et
al. (4) report at least three different swimming behaviors as responses
to Chaoborus kairomone or carbaryl. Using different recording techniques,
Dawidowicz et al. (6) and Loose et al. (7) have shown that
diel vertical migration of Daphnia is a response to fish smell (kairomone),
and therefore this large-scale behavior is also potentially modified by
xenobiotics. Also, Daphnia spatial orientation (28) is changed,
and phototactic response (29,30) appears abnormal in sublethal concentrations
of toxic xenobiotics.
Reproductive Effects
Many pesticides, other toxic xenobiotics (such as PCBs and dioxins),
and common industrial chemicals (such as nonylphenol and phthalates) are
estrogen mimics (31,32). These mimics are implicated as agents that
interfere with male development in wildlife populations, including Florida
alligators (33), turtles (34), and panthers (35); Texas
turtles (36); southern California sea gulls (37); Great Lakes
salmon (38); and English trout (39). This interference is
of interest because of the potentially devastating effects on both wildlife
and human reproductive
biology (40,41).
Many zooplankton (cladocerans and rotifers) have a reproductive strategy
based on facultative parthenogenesis (virgin birth) (42). Females
produce daughters during most of the summer growing season. When environmental
conditions deteriorate (crowding, cooler temperatures, low food), females
produce males and haploid eggs. The number of males produced in a population
depends on the genetics of the population and the intensity of the environmental
signals. The sex ratio is not set at 50%, but usually is some smaller
percent of males.
Growth and molting in crustaceans is regulated by a variety of hormones,
including juvenile hormone and ecdysteroids (43). It is probable
that development of cladoceran males (genetically identical to their mothers)
is also under hormonal control, as in vertebrates. Thus, it is possible
that cladoceran sex ratio may be influenced by some of the same xenobiotics
that interfere with vertebrate sexual maturation.
We hypothesize that the flexible cladoceran sex ratio might be more easily
influenced by hormonelike xenobiotics, than would obligate sexual species
(such as copepods) that typically are genetically locked into a 1:1 sex
ratio. We predict that the maximum Daphnia sex ratio observed during
a year will be higher before 1945 than after. A test of this hypothesis
would be to examine historical records of Daphnia sex ratios in lakes
from before and after the advent of anthropogenic toxic organics in the
middle 1940s. Surprisingly few historical zooplankton samples or reports
of cladoceran sex ratios exist. The only example currently known to us is
for Lake Mendota, Wisconsin (Table 4), for which we have estimates of the
maximum sex ratio observed in 1895, 1975, and 1991. The data for Lake Mendota
show a dramatic decrease in the maximum frequency of males for two Daphnia
species and no change in the already low frequency for the third species.
These data are consistent with the hypothesis that anthropogenic compounds
are affecting Daphnia reproductive strategy in a lake, but more data
(e.g., from European lakes for which there are long series of historical
samples) is needed before we can conclude that the lower sex ratio in Daphnia
is a general phenomenon.
Ecological Consequences
Morphology and Life History
In natural predator-prey systems, the induction of morphological predator
defenses (such as high helmets or long tail spines) by kairomones is often
(although not always) associated with a reduction in biological fitness,
measured as the population growth rate of a clone (1,18,44-47). The
reduction in fitness, when it occurs, is usually due to a longer developmental
time (from neonate to adult); in some cases there is also a decrease in
the number of eggs per clutch. A similar reduction in fitness is seen in
Daphnia exposed to carbaryl (Table 5). The synergistic effect of
both the kairomone and carbaryl (Table 4) reduced the population growth
to half or less of that predicted from the separate effects of the two factors.
Such a large reduction is particularly important to Daphnia, which
typically requires a high rate of population growth to persist through periods
of high mortality from predators (18,23,48-50). Thus, synergistic
effects among environmental factors, kairomones, and anthropogenic toxic
compounds are likely to result in depression or extirpation of Daphnia
populations in contaminated water bodies.
Swimming Behavior
Swimming behaviors also have ecological consequences. Abnormal behaviors
caused by toxic xenobiotics may result in higher mortality due to both vertebrate
and invertebrate predators. For example, an increase in swimming velocity
will increase encounter rate with predators and therefore increase the rate
of mortality (51).
Given the intense mortality often experienced by zooplankton such as
Daphnia (18), even a small increase in the mortality rate
may result in the disappearance of the population from a lake.
In addition to affecting swimming behavior, it is probable that xenobiotics
affect other behaviors such as feeding and mating. Reduction in feeding
activity at sublethal levels of xenobiotics has been well documented (23).
Synergisms
Natural stress factors such as low pH, low oxygen concentration, high
temperature (52), presence of kairomones, and low food density (53),
tend to reduce Daphnia growth rate. Some, or perhaps all, of these
stress factors interact synergistically with toxic xenobiotics. Thus, Daphnia,
and by implication zooplankton in general, may be especially susceptible
to low levels of toxic organic compounds when the population is also responding
to several natural stress factors.
Reproductive Effects
Male Daphnia are seldom ecologically (trophically) significant
in a direct way. However, the ecological and evolutionary role of male Daphnia
is to allow for sexual recombination in the population to produce offspring
that are different from the parents, therefore holding the possibility of
being adapted to changing environmental conditions. Without sexual reproduction,
it is possible that clones of asexually reproducing Daphnia would
be at a serious disadvantage in those years in which environmental conditions
do not match the requirements of the particular clones. Competition in suboptimal
years could result in the reduction or disappearance of Daphnia populations.
For some Daphnia genotypes, fertilization of haploid eggs is required
for the production of the resting eggs used to survive inhospitable environmental
conditions such as freezing, anoxia, or drying (54). For these genotypes,
suppression of males would result in immediate extirpation.
Daphnia are often important components of planktonic communities.
Daphnia biology is affected by a wide range of toxic xenobiotics
and appears to be particularly vulnerable to carbaryl and other toxic xenobiotics
(55). Daphnia are replaced by smaller and less efficient herbivores
in experimental ponds treated with doses as low as 10 ppm carbaryl (56).
Because of the important grazing role of Daphnia (57-59),
loss of Daphnia from a lake can reduce water quality and reduce the
efficiency of energy transfer from phytoplankton to fish (24). Reduction
or removal of Daphnia from a lake food web may result in a greener
lake that produces fewer fish and has a greater tendency toward winter kill.
Thus, subtle effects on Daphnia caused by sublethal concentrations
of toxic organics can have significant and readily apparent consequences
to lakes.
Summary
- Daphnia is a key member of the lake community. It occupies a
central position in the food chain and affects both water quality and fish
production.
- Smaller Daphnia, induced by low concentrations of carbaryl and
other xenobiotics, are less efficient herbivores. The lower efficiency
is potentially reflected as a reduction in water quality as algae become
more abundant.
- Lower reproductive rates, associated with nonlethal concentrations
of xenobiotics, result in a reduced ability of Daphnia to outproduce
their predators. If the Daphnia reproductive rate is insufficient
to match the losses to predators, the Daphnia population will decline
or disappear.
- Out-of-context induction of developmental, behavioral, or reproductive
changes by xenobiotics reduces Daphnia competitive ability relative
to other zooplankton species. The reduced competitive ability is the result
of energy allocated to changes that have no biological benefit.
- Abnormal swimming induced by xenobiotics reduces Daphnia survival
if it increases predation rate. This can lead to reduction or disappearance
of the Daphnia population.
- Loss of sexual reproduction, if caused by hormonelike activity of xenobiotics,
will decrease Daphnia adaptability to changing environments. If
sexual reproduction is necessary to produce resting stages that produce
the next generation, then suppression of males can lead to rapid extirpation
of the Daphnia population.
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