Environmental Health Perspectives Volume
103, Supplement 4, May 1995
[Citation
in PubMed] [Related
Articles]
Possible Interrelations among Environmental Toxicants, Amphibian Development,
and Decline of Amphibian Populations
Cynthia Carey and Corrie J. Bryant
Department of Environmental, Population and Organismic Biology, University
of Colorado, Boulder, Colorado
Abstract
Many amphibian populations are declining in a number of geographical
locations throughout the world. In most cases, the cause or causes are unknown,
but are assumed to result from man-made alterations in the environment.
We review existing evidence concerning how environmental xenobiotics could
contribute to declines of amphibian populations by impacting growth and
development of the young. This paper examines the potential roles of toxicants
in: a) affecting the susceptibility of young to disease; b)
retarding growth and development of amphibian young; c) affecting
the ability of larvae to avoid predation; d) affecting the development
of physiological, morphological, or behavioral processes in a manner that
subsequently impairs the ability of the young for future reproduction; and
e) directly causing mortality of young. These issues are not well
studied, and more studies are needed before the roles of environmental xenobiotics
in amphibian declines are fully understood. -- Environ Health Perspect
103(Suppl 4):00-00 (1995)
Key words: amphibians, amphibian development, immune system, immunosuppression,
xenobiotics, heavy metals
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.
This study was supported by grants from the National Science
Foundation (IBN-921396 and DEB-9400333), American Philosophical Society,
IUCN/SSC, Declining Amphibian Population Task Force, the University of
Colorado Global Change Program, and the University of Colorado Council
on Research and Creative Work.
Address all correspondence to Dr. Cynthia Carey, Dept.
of EPO Biology, University of Colorado, Boulder, CO 80309. Telephone (303)
492-6014. Fax (303) 492-8699.
Introduction
It has become apparent over the last few years that many amphibian populations
are declining and that extinction has occurred in a few populations (1,2).
These phenomena have been documented in a variety of habitats on six continents
(3). In a few cases, a man-made change in the environment has been
extreme enough to be implicated as the direct cause of the death of individuals
and, in some cases, extinction of amphibian populations. For instance, spraying
of DDT in the forests of Oregon caused mortality in a population of western
spotted frogs (Rana pretiosa) (4); increased UV radiation
resulting from atmospheric ozone depletion has been correlated with mortality
of amphibian eggs (5); and habitat destruction, disturbance and fragmentation
are accepted causes of local extinctions (3). However, other attempts
to demonstrate that man-made causes have been severe enough to cause amphibian
mortality have failed (6). In most cases, the cause or causes are
unknown (3). Man-made factors are suspected because of the breadth
of geographical areas affected and the rapidity with which these declines
are occurring. Environmental toxicants (trace metals, pesticides, industrial
chemicals and their by-products, etc.), UV radiation, introduction of nonnative
predators (usually fish) or competitors, and acid rain have all been suggested
as potential causes, acting singly or synergistically (7). It is
likely that no single factor or group of factors has been the causative
agent throughout the world; each locality may have its own particular cause
or causes.
Environmental change could cause population declines in a number of different
ways. A lethal change in the environment can kill a population--some or
all age classes including eggs and larvae--directly or indirectly by suppressing
the immune system and allowing subsequent infection with opportunistic pathogens.
Or, population size could be reduced by reproductive impairment. Reproductive
success could be impaired by environmental interference with adult reproductive
function (inhibition of breeding behavior, manufacture of gametes, or of
fertilization) or by disruption of development and growth of the young.
While each of these possibilities merits serious attention, this paper will
focus on the evidence supporting the hypothesis that environmental toxicants
could contribute to amphibian declines by affecting growth and development
of the young.
Reproduction is a vulnerable period in the life cycle of amphibians,
even in the absence of environmental toxicants. Adults are more at risk
from predation when they congregate around breeding ponds than after they
have dispersed, and few of the hundreds to thousands of eggs laid by each
species normally survive to become breeding adults. For instance, only 4%,
4.4% and 3.3% of wood frog (Rana sylvatica), spotted frog (Rana
pretiosa), and tiger salamander (Ambystoma tigrinum) eggs, respectively,
survive to metamorphosis (8). Over a 5-year period, survivorship
of spotted salamanders (Ambystoma maculatum) between the egg stage
and dispersal of newly metamorphosed young in a pond in Massachusetts varied
from 1 to 12.6% (9). Although this mortality has been assumed to
be naturally caused by predators, by desiccation of eggs as breeding ponds
evaporate, by flooding of the breeding pond, or by low temperatures (8,9),
the role of environmental toxicants in mortality of young amphibians in
the field is less understood. Environmental toxicants may interfere with
amphibian growth and development in a number of ways: a) sublethal
concentrations of toxicants may indirectly cause death by promoting susceptibility
of eggs and larvae to pathogenic organisms and disease; b) sublethal
levels of toxicants may indirectly affect survival by retarding growth and
metamorphosis with the result that larvae are unable to metamorphose and
depart breeding ponds at the appropriate time; c) sublethal levels
may inhibit the ability of larvae to avoid predators; d) toxicants
that have estrogenic, antiestrogenic, thyroid-disrupting, androgenic, or
anti-androgenic properties may either impair or totally inhibit future reproduction
by disrupting developmental processes; or e) lethal concentrations
of toxicants might directly cause mortality of the eggs, larvae, or metamorphosing
individuals. We will review existing evidence on these five possibilities
and point out areas in which more data are needed before firm conclusions
can be reached.
Potential Role of Toxicants in Increasing Susceptibility
of Young to Disease
A recent hypothesis suggests that amphibian mortality in the field does
not necessarily have to be caused by severe environmental changes that are
directly lethal (2). Sublethal environmental changes, acting singly
or synergistically, could stress larval or postmetamorphic amphibians sufficiently
that their immune systems become compromised; infection by opportunistic
pathogens is followed by death (2). This proposal is based on observations
that local die-offs and even extinctions of amphibian populations have been
associated with infections of opportunistic bacteria such as Aeromonas
hydrophila (1,2,10). These bacteria are ubiquitous in fresh water,
present on the skin and in the digestive tracts of healthy organisms, and
apparently, successfully attack immunosuppressed individuals (11).
Laboratory studies indicate that immunosuppression can be induced by injection
of corticosterone (one of the hormones associated with responses to stress)
or exposure to heavy metals, certain pesticides or industrial chemicals,
and cold (12-14). Therefore, it is possible that sublethal changes
in one or more of these factors can cause immunosuppression, leading to
infection and subsequent death in amphibian populations in the field. This
hypothesis is currently being tested.
Since resistance to pathogens results from a complex, multifaceted immune
system that gradually develops during ontogeny, amphibian eggs, larvae,
and metamorphosing, individuals might be more vulnerable to environmentally
influenced disruption of immune function than adults. Although many existing
reports of die-offs due to bacterial infection document only mortality of
adults and subadults (2) or mortality of both adults and larvae (10),
a few observations raise the possibility that larvae or particular size
classes of newly metamorphosed individuals might be more susceptible to
disease than adults. For instance, infection of Aeromonas hydrophila
was more prevalent in larval than adult leopard frogs (Rana pipiens)
in a population in Minnesota (15). Infection by Aeromonas hydrophila
caused mass mortality of larval wood frogs (Rana sylvatica) in ponds
in Rhode Island, but adults in the same pond appeared unaffected (16).
Most smaller frogs in one population of yellow-legged frogs (Rana muscosa)
in the Sierra Nevada succumbed to an infection of Aeromonas hydrophila
or Enterobacter sp., while larger frogs survived (1). Most
newly metamorphosed Rana yavapiensis were killed during an epidemic
of Aeromonas hydrophila, whereas most adults in the same pond near
Phoenix, Arizona, survived (M Sredl, unpublished observation). Finally,
two mass die-offs of tiger salamander (Ambystoma tigrinum) larvae
and newly metamorphosed young in montane ponds of Colorado were associated
with the presence of Aeromonas hydrophila and Acinetobacter sp.,
but adult carcasses were not found (CJ Bryant and C Carey, unpublished observation).
It is unclear whether the salamander adults had left the pond before the
onset of the bacterial epidemic, or whether they were unaffected by disease.
Could developmental differences in amphibian immune function result in differential
abilities of larvae, individuals undergoing metamorphosis, and adults to
resist disease when subjected to environmental stress?
Considerable diversity exists among amphibians in body form, breeding
characteristics, and habitats (ranging from completely aquatic to completely
terrestrial). The class Amphibia is comprised of at least 4000 living species
grouped into three orders: salamanders (Caudata), caecilians (Gymnophonia),
and frogs and toads (Anura) (17). Important differences in structure
and function of the immune system may well exist in each taxonomic group,
but research has focused on relatively few species. The immune system of
the African clawed frog (Xenopus laevis) has been studied intensively,
and immune function in a few species of Rana, Ambystoma, and
Bufo has received considerable attention, but the most frequently
studied species in these genera account for less than 1% of the total species
in the Amphibia (17). No information is available concerning the
immune system of the vast majority of species. Therefore, the generalizations
given below concerning the amphibian immune system derive from the specific
findings from studies on Xenopus laevis, and possibly also from those
on Rana, Ambystoma and Bufo.
Amphibian eggs are enclosed in a jelly capsule at laying. The jelly capsule
of Xenopus has three layers, each of which is composed of different
amounts of polysaccharides and proteins (18). The fact that the composition
of each layer differs from that of the others suggests that each layer may
have a different function. Little information exists on whether the jelly
capsule or the egg is provisioned with anti-pathogenic defenses or whether
the jelly capsule simply functions as a mechanical barrier. However, the
observations that Bufo eggs develop fungal infections following handling
(C Carey, unpublished observation) suggest that eggs and embryos are protected
until hatching by one or more defense mechanisms in intact and undisturbed
jelly. Recent observations show that fungal infections (Saprolegnia ferax)
of eggs resulted in almost complete reproductive failure of one population
of boreal toads (Bufo boreas boreas) in the Cascades of Oregon (19).
It is unclear whether such infections result from recent introduction of
fish carrying the fungus into breeding areas of these toads, or whether
environmental factors are reducing protective qualities of the jelly capsule
against such pathogens.
The tissues that play important roles in amphibian immunological responses
are thymus, spleen, bone marrow, kidney, liver, and various aggregations
of lymphoid cells that resemble mammalian lymph nodes (20). The relative
role and importance of each tissue differ between larvae and adults. Ventral
and dorsal cavity bodies play an important lymphogenic role in Xenopus
larvae but disappear after metamorphosis. Lymphoid nodules are present in
the intestine of adults but are absent in larval Xenopus. The bone
marrow of Xenopus develops as limbs develop and becomes calcified
after metamorphosis. The liver of Xenopus retains lymphopoietic function
throughout life, but this function disappears after metamorphosis in other
anurans, which have been examined. The thymus begins development around
day 3 after fertilization (about stage 40 of development), grows to contain
roughly 1x106 lymphocytes within 45 days (stage 58), shrinks
during metamorphosis, and then grows during the first 2 to 3 months after
metamorphosis to contain about 1 to 3x107 cells; it undergoes
a final regression at the onset of sexual maturity (21). Primordial
spleen cells appear about 12 to 14 days after fertilization in Xenopus;
once functional, the spleen continues as a lymphopoietic organ throughout
life (21).
Immune systems of Xenopus larvae acquire the ability to recognize
and destroy transplants of foreign tissue within about 12 days (stage 49)
after hatching, but full response to allografts does not occur until well
after metamorphosis (21). B-cells, which produce antibodies, begin maturation
in the liver within 5 days of hatching (stage 45), and the first antibodies
(IgM and IgY) appear in the serum by days 10 to 13 (stages 49-51). Xenopus
larvae begin recognition of foreign antigens by days 19 to 20 (stage 51-52).
During metamorphosis, the larval antibody repertoire is completely replaced
by adult antibodies. These observations provide support for the idea that
immune systems of young may be more vulnerable to environmental disruptions
of immune function than those of adults because the full suite of defenses
is not completely developed until well after metamorphosis (21).
Potential Role of Toxicants in Retarding Growth and
Development of Young Amphibians
Some larval amphibians complete development and metamorphosis within
their first summer, while others overwinter as larvae and go through metamorphosis
during their second summer (22). In some species such as bullfrogs
(Rana catesbeiana), larvae overwinter at least 1 year in the northern
parts of their range in the United States, but long growing seasons in the
southern parts of their distribution foster metamorphosis of larvae in their
first summer (23). The ability to overwinter in a larval form undoubtedly
requires special adaptations that maximize survival in aquatic surroundings,
such as the ability to tolerate anoxia (24). Larvae that typically
complete metamorphosis by the end of their first summer undoubtedly survive
their first winter with a different suite of specializations than those
overwintering as larvae. These specializations, such as the ability to tolerate
freezing, would foster survival in a variety of environments (soil, subterranean
cavities, or under water). If growth and development of larvae that commonly
complete metamorphosis their first summer and overwinter as metamorphosed
individuals are delayed by toxicants so that they are forced to overwinter
as larvae, they may not survive the winter because their population or species
may not have evolved the specializations that promote winter survival in
the larval form.
Retardation of growth may have other negative effects. Rapid growth has
a selective benefit for many amphibian species because they are subjected
to size-specific predation. Rapidly growing larvae suffer a lower cumulative
risk of death because they spend less time in smaller, more vulnerable stages
than do slower growing ones (25).
A recent experiment documents that exposure to various combinations of
low pH and aluminum (as AlCl3.6H2O) retards growth
and development of green treefrog (Hyla cinerea) tadpoles (26).
Low pH was tested in conjunction with aluminum because heavy metals tend
to be leached out of soils in contact with acidic water (27). Body
length of larvae maintained for 96 hr at lower pH (5.5 and 4.5) and higher
concentrations of aluminum (up to 400 µg/l ) was significantly reduced
compared to controls (pH 7.0, no aluminum), whereas length of tadpoles maintained
at lower pH alone was not significantly affected.
Another example of the relation between exposure to toxicants and amphibian
growth is provided by a study on the effect of freshwater petroleum contamination
on hatching success and growth rates of young Hyla cinerea. The findings
indicated that while hatching success was not significantly impacted by
exposure to 10, 55, and 100 mg/L of crankcase oil, growth rates of larvae
exposed to higher concentrations of oil were significantly retarded (28).
It is unknown exactly how pH, aluminum, or various other pollutants retard
growth in these tadpoles; interference with food acquisition, food digestion,
uptake of digestive nutrients, or synthesis of new tissues are only a few
of many possibilities. Acute exposure to low pH (2.5-4.0) causes a reduction
in sodium influx and acceleration in sodium efflux in leopard frog (Rana
pipiens), bullfrog (Rana catesbeiana), and green frog (Rana
clamitans) tadpoles (29). The energetic costs of active transport
necessary to counteract changes in sodium flux at low, but not lethal, pH
could potentially detract from energy available for growth. While more studies
testing single and synergistic effects of pH and environmental toxicants
are needed, these results support the contention that environmental change
could lead to decreases in size of amphibian populations by retarding normal
growth and development.
Amphibians undergo metamorphosis at a small fraction of adult body size
and grow substantially after metamorphosis. For instance, an average ranid
frog completes metamorphosis at a larval mass corresponding to about 6%
of adult body mass. Post-metamorphic growth typically accounts for 80 to
99% of the adult body mass in anurans (22). The effect of environmental
toxicants on postmetamorphic growth of any amphibian species is unknown.
Potential Roles of Toxicants in Affecting Larval Ability
to Avoid Predation
Predation can be a major cause of larval mortality in amphibian populations
(30). Insect larvae, fish, snakes, birds, and other amphibians are
probably the major predators on amphibian larvae. Larvae that are slow swimmers
are more frequently predated upon than more rapid swimmers (31).
Exposure of amphibian larvae early in development to high, but sublethal,
levels of toxicants causes deformities in the body or tail that clearly
impact swimming ability (32). Even when toxicant levels do not result
in deformities, either because toxicant concentrations are low or because
exposure occurred after larvae had passed certain critical stages in development,
swimming ability may still be compromised. A recent study on the effects
of low pH and aluminum concentrations on swimming performance and susceptibility
to predation indicated that Hyla cinerea larvae exposed to pH of
4.5 and 100, 200, or 400 µg/L Al exhibited reduced swimming performance
compared to controls (pH 4.5, 0 µg/L Al), even when differences in
body length were taken into account (26). Tadpoles exposed to pH
4.5 and 150 µg/L Al were more susceptible to predation by dragonfly
larvae (family Libellulidae) than controls (pH 7.0, 0 µg/L Al). The
dragonfly larvae may have eaten more experimental than control tadpoles
because they were easier to capture at a slower swimming speed, because
their relatively smaller size made it easier for the dragonfly larvae to
eat, or because dragonflies had to eat more of them in order to fill their
nutritional needs (26). The mechanism by which low pH and aluminum
impair swimming performance is unknown.
Reduction in swimming performance is not necessarily the only way in
which toxicants increase the susceptibility of amphibian larvae to predation.
Exposure to certain environmental toxicants causes a period of hyperactivity
in amphibian larvae. Rana temporaria tadpoles treated with DDT swam
rapidly, twisted their bodies, and lashed their tails prior to becoming
moribund and dying (33). Warty newts (Triturus cristatus)
prey on significantly more of the hyperactive tadpoles than slow swimming
tadpoles (33).
Potential Role of Toxicants in Disruption of Developmental
Processes Leading to Alteration of Reproductive Potential
It is now firmly established that many man-made chemicals (pesticides,
industrial chemicals and by-products, heavy metals, etc.) disrupt endocrine
systems of wildlife (34). The fact that many of these compounds either
mimic the effects of estrogen or androgens or have anti estrogen or anti-androgen
effects has received a great deal of attention because of the serious consequences
for reproduction; sexual behavior, fertility, development of the gonads
and sexual organs, etc. can all be negatively affected by exposure of young
to these compounds. Unfortunately, very few studies yet exist on whether
reproduction of amphibian populations in the wild has been affected by environmental
toxicants. It is interesting to speculate that members of the last remaining
population of the endangered Wyoming toad (Bufo hemiophrys baxteri)
may have been negatively impacted by endocrine-disrupting chemicals. Males
exhibited little clasping behavior at the appropriate breeding time in spring
and hatchability of the few clutches resulting from amplexus was very low
(A Anderson, unpublished observation). In another study, Ambystoma tigrinum,
inhabiting a lagoon polluted with secondary domestic sewage and perylene
(a component of jet fuel), were reproductive as neotenes, rather than as
metamorphosed adults. Metamorphosis may have been inhibited by environmental
pollutants. Furthermore, the majority of the neotenes in the polluted lagoon
also suffered skin lesions; 84% were neoplasms. The effects of pollutants
were not permanent because, when animals were transferred out of the polluted
lagoon into an adjacent, relatively unpolluted pond, they metamorphosed
within 6 to 9 months, and many of these lesions regressed (35).
It has been assumed that tissue concentrations of toxicants below levels
at which they can be detected by chemical analysis are safe (36).
However, because endocrine- disrupting toxicants can have effects at tissue
levels well below detectable levels, toxicants designated as safe should
not be considered to be free of endocrine-disrupting effects until proven
otherwise.
Potential Roles of Toxicants as Lethal Agents for Young
Amphibians
A wealth of data exists on tolerance levels of amphibian larvae to various
environmental toxicants. The acute toxicity effects of over 211 different
pollutants have been studied on at least 45 different species of amphibians,
and effects of at least 54 different substances have been studied in field
applications (37). For instance, reproductive success in a population
of Rana temporaria was reduced after spraying of atrazine nearby
(38), and northern cricket frogs (Acris crepitans) died in
a stream adjacent to a cotton field in which DDT had been applied (39).
While a variety of results have been obtained because of the number of species,
life stages, and techniques used, the literature suggests that adult and
larval amphibians are not necessarily more sensitive to chemicals than are
other land or aquatic vertebrates (37). However, it is interesting
to note that anurans are remarkably more resistant to cholinesterase inhibitors
than are other vertebrates, including urodeles (37).
Despite the importance of the large amount of information gathered in
laboratory and field studies, the latter of which have mostly been conducted
in agricultural areas or heavily polluted areas, we are lacking much information
concerning toxicant exposure of amphibians in pristine areas of the western
United States where populations are declining rapidly. Since deposition
of airborne pollutants is greatest in montane areas where highest levels
of snowfall occur, animals living in montane habitats are likely to be exposed
to higher levels of toxicants, especially during snowmelt, than are those
living at lower altitudes (D Haddow, personal communication). Exposure information
is badly needed; we need baseline data on tissue levels of toxicants in
amphibians and on toxicant concentrations in sediments, water, and prey
in a wide variety of habitats. The time frame remains to be determined within
which application of various toxicants would prove lethal in the field.
The relative vulnerability of eggs, larvae, and adults of various amphibian
species to different toxicants in the field has yet to be established. Therefore,
estimation of the extent to which environmental xenobiotics have contributed
directly to amphibian population declines is extremely difficult to determine
at this time.
Summary
In most cases, causes of amphibian population declines are unknown. This
paper has reviewed several ways in which these declines could have been
caused by environmental toxicants, but critical data are lacking in most
instances. Coordinated studies in both the field and laboratory are needed
to establish whether causal relations exist between levels of environmental
toxicants and the demise of amphibians.
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