This file was created by scanning the printed publication.
Errors identified by the software have been corrected;
however, some errors may remain.
Environmental Contaminants
and the Management of Bat
Populations in the United
States1
Donald R. Clark, Jr.2
Several species of bats in the U.S.
Form large aggregations in caves, old
mines, or other shelters, and many of
these colonies are of management
concern to biologists working for the
states or federal government (e.g.
Prichard 1987). Four taxa, the gray
bat (Myotis grisescens), Indiana bat
(M. sodalis), Ozark big-eared bat (Plecotus townsendii ingens), and Virginia
big-eared bat ( P . t. virginianus), are of
particular concern because they are
endangered (USDI, FWS 1987).
Habitat destruction such as deforestation, water pollution, stream
channelization, and stream sedimentation (Tuttle 1979, Prichard 1987)or
direct human disturbance and destruction of bats (Tuttle 1979, for a
recent example see Anon. 1987) are
primary known threats to bat colonies. However, environmental contaminants, such as organochlorine
pesticide residues and heavy metals,
probably have been involved in some
declines of bat populations. In this
paper I discuss the management implica tions of these contarninants.
(Note: for purposes of this discussion, "management" refers broadly
to human activities undertaken in the
interest of a bat colony with the goal
'Paper presented a t symposium Management of Amphibians, Reptiles, and
Small Mammals in North America. [Flagstaff, AZ,July 19-21, 1988.)
2DonaldR. Clark, Jr., is Research Wildlife
Biologist, US. F E and
~ Wildlife Service,
Patuxent Wildlife Research Center, Laurel,
MD 20708.
Abstract.-Food-chain Residues of organochlorine pesticides probablv have been involved in
declinesof some U.S. Bat popu~ations;examples include free-tailed bats at Carlsbad Cavern, New
Mexico, and the endangered gray bat at sites in
Missouri and Alabama. If a long-lived contaminant
has not been dispersed in large amounts over large
areas, its impact may be controlled by administrative action that stops its use or other environmental
discharge, or that results in physical isplation of localized contamination so that it no longer enters food
chains.
that colony size will remain at a
steady, sustainable level or will increase to such a level.)
Examples of Possible Food-Chain
Contaminant Impacts on Bat
Populations
from heavy DDT use in New Mexico
before its ban in 1972; however, other
more-recent inputs have been postulated to explain high DDE levels in
wildlife in parts of Texas, New Mexico, and Arizona (Clark and Krynitsky 1983, Hunt et al. 1986, White and
Krynitsky 1986).
Free-Tailed Bats at Carlsbad
Cavern, New Mexico
Gray Bats in Missouri
The Carlsbad population of Mexican
free-tailed bats (Tadarida brasiliensis
mexicana) was estimated at 8.7 million bats in 1936 (Allison 1937) but
only 200,000 bats remained in 1973
(Altenbach et al. 1979). Several dieoffs occurred during this interval
(Altenbach et al. 19791, and none was
linked directly to pesticide poisoning; however, routine testing of tissues was not available. The question
of pesticide involvement was addressed by simulating migratory
flight in young bats taken from the
colony in 1974 (Geluso et al. 1976).
Some of these bats died of DDE (1,l'(dichloroethylidene)bis[4-chlorobenzene]) poisoning (DDE is the principal metabolite of DDT; 1,l'-2,2,2(tricholoroethylidene)bis[4-chlorobenzene]) due to mobilization of
DDE received in their mother's milk
and stored in their fat (Geluso et al.
1976). This result suggests that DDT
has contributed to the decline of this
population.
High DDE concentrations in the
Carlsbad colony probably resulted
Dieldrin (3,4,5,6,9,9-hexachlorola,2,2a,3,6,6a,7,7a-o~tahydro-2,7:3,6dimethanonaphth[2,3-bloxirene)
killed gray bats in 1976,1977, and
1978 in two maternity colonies in
Franklin County, Missouri (Clark et
al. 1978b, 1953a).Residues of heptachlor-related chemicals
(1,4,5,6,7,8,8-heptachloro-3af4,7,
7atetrahydro-4,7-me thanoindene) in
bats from both colonies increased to
potentially dangerous concentrations
in 1977 and remained elevated in
1978 (Clark et al. 1983a).Population
size at one colony was estimated at
1,800 bats in 1976 and 1978, but no
bats were present from 1979-82
(Clark et al. 1983a,b). Dieldrin, perhaps in conjunction with heptachlor,
may have caused the decline and disappearance of this colony. Dieldrin
also killed gray bats at three Boone
County, Missouri, caves in 1980,
1981, and 1982 (Clark et al. 1983b,
Clawson and Clark in manuscript).
Death of gray bats were attributed
to dieldrin because this chemical was
measured in the bats' brains at con-
centrations known to be lethal in
other species (Clark et al. 1978b).Dieldrin and heptachlor-related residues came from the use of aldrin
(Dieldrin's parent compound) and,
subsequently, heptachlor, to control
cutworms (moth larvae, Family Noctuidae) in corn.
Gray Bats at Cave Springs Cave,
Alabama
DDT was manufactured at Redstone
Arsenal near Huntsville, Alabama,
from 1947 to 1970, and massive
amounts of DDT and its metabolites
(DDD; 1,11-(2,2-dichloroethy1idene)bisl4-chlorobenzene and DDE) were
discharged into the Tennessee River
via Huntsville Spring Branch-Indian
Creek (Fleming and Atkeson 1980).
Local biota remains heavily contaminated (O'Shea et al. 1980, Fleming
and Cromartie 1981, Fleming et al.
1984, Reich et al. 1986.).
Samples of dead or dying bats and
bat guano collected between 1976
and 1986 from four gray bat colonies
as far as 140 km downriver contained
residues from this former discharge
(Clark et al. 1988).Residues were
identifiable by their high DDD to
DDE ratio, which resulted from their
breakdown under anaerobic conditions. Cave Springs Cave at Wheeler
National Wildlife Refuge houses the
colony nearest the contaminant
source-about 20 km. Biologists
judged that bat mortality at Cave
Springs Cave was far above normal
in 1978,1985, and 1986. Residues of
DDT, DDD, and DDE in brains of
dead or dying bats from this cave,
a1though elevated in comparison
with residues from colonies upstream from Redstone Arsenal, were
well below concentrations believed
to be lethal (Clark et al. 1988). The
single exception was a bat collected
in 1978 with sufficient DDD in its
brain (29 ppm wet weight) to have
been poisoned (Clark et al. 1988).The
measured residues, therefore, did not
explain the observed mortalities.
Although there is no explanation
for this mortality yet, another contaminant may by involved. A guano
sample collected from Cave Springs
Cave in 1987 was analyzed for heavy
metals and cadmium measured 8.5
Ppm (dry weight). This amount may
be compared with 2.2 Ppm cadmium
in guano (mixed gray and southeastern bats, M. austroriparius) from a
Florida cave where the bats were exposed to contaminations from a battery salvage plant. Kidneys of southeastern bats from this Florida cave
averaged 0.89 Ppm (wet weight) cadmium with a maximum of 2.9 Ppm.
Concentrations of cadmium as low as
3.4 Ppm in kidneys of voles (Microtus
pennsylvanicus) were associated with
reduced survivorship in enclosed
populations. Also, six gray bats
found dead in Cave Springs Cave in
June 1986 were examined by the U.S.
Fish and Wildlife Service's National
Wildlife Health Research Center,
Madison, Wisconsin. There was no
evidence of injury or infectious disease, but all bats showed mild renal
tubular degeneration. Because cadmium caused kidney damage (Nomiyama 19811, this metal, perhaps in
combination with DDD and DDE,
may have caused the recent die-off of
gray bats at Cave Springs Cave. The
cadmium source is unknown. Additional samples for chemical analysis
will be collected in 1988.
Management of Contaminant
Impacts on Bat Populations
Screening for Possible
Contaminant Problems in
Apparently Healthy Colonies
Contaminants that biomagnify or
bioaccumulate in ecosystems include
organochlorine pesticides such as
DDT (and its metabolites DDE and
DDD), dieldrin, heptachlor-related
chemicals, and the industrial polychlorinated biphenyls (PCBs). Also
included are heavy metals such as
lead, cadmium, chromium, zinc, and
mercury. For chemicals that biomagnify or bioaccumulate, analyses of
guano samples collected from the
surface of a guano deposit can indicate body burdens in bats during
their most recent activity season.
Samples from greater depths may
indicate contaminant concentrations
in previous years.
Relationships between concentrations in guano and carcasses of bats
from the same colony have been described for dieldrin, heptachlor epoxide, and DDE (Clark et al. 1982).
Limited data are available on concentrations of lead, cadmium, chromium, zinc, and mercury in guano
from contaminated colonies (Petit
and Altenbach 1973, Clark 1979,
Clark et al. 1986, this paper). About
20 grams of guano, dry weight, are
necessary for analyses.
Sublethal exposure of bats to the
newer organophosphorus and carbamate insecticides is demonstrated
by depressed brain cholinesterase
(ChE) activity in exposed individuals. Depression is determined by
comparison to normal ChE activity
for a sample of control bats of the
same species. Measurement of ChE
activity (for methods, see Ellman et
al. 1961, Hill and Fleming 1982)involves removal of the brain, hence
death of the bat.
Recognizing Organochlorine
Pesticide-Induced Mortality in Bat
Colonies
Managed colonies are usually censused annually so that any significant
decline will be recognized. By also
estimating numbers of dead and
dying bats at these censuses, managers can differentiate between "normal" mortality and increased mortality, which may be the first sign of a
contaminant problem.
May of the colonies considered
most important are maternity colonies, and in maternity colonies, organochlorine chemicals kill mostly
young bats. There are two reasons
for this. First, organochlorines become concentrated in the fat of
mother's milk and these chemicals
continually and rapidly accumulate
in the young as they nurse.
For example, insects collected in
foraging areas of Missouri gray bats
contained a maximum of 3.1 Ppm
(wet weight) dieldrin, but milk taken
from the stomach of a young dead
gray bat contained 89 ppm (wet
weight) dieldrin (Clark and Prouty
1984).Second, young bats are 1.9
Times more sensitive than adults to
dieldrin and 1.5 Times more sensitive
to DDT (Clark et al. 1978a, 1983a).
Young bats dying of organochlorine
poisoning may still have milk in their
stomachs unlike young dying of starvation. Therefore, increased infant
mortality in a maternity colony with
some young having milk in their
stomachs may indicate poisoning by
an organochlorine chemical.
Diagnosing Chemical Poisoning in
Bats
Diagnosis for organochlorine chemicals requires analyses of brains and
interpretation of the resulting measurements. However, because concentra tions in brains are closely correlated with concentrations in carcass
fat (Clark 1981a), analyses of carcasses may serve if brains are unavailable. For example, analysis of
carcasses may be the only option
when bats are partly decomposed.
Correlations between brain and carcass fat concentrations only have
been quantified for DDE, DDT, and
dieldrin (Clark 1981a).
Lethal brain concentrations for
DDE, DDT, dieldrin, and PCB (Aroclor 1260) have been determined for
at least one species of bat (Clark
1981b).Because lethal brain levels are
fairly similar among mammals and
birds, comparisons can provide clues
about the effect on a populations,
even though the lethal level for the
species under investigation has not
been determined yet.
Diagnosis of death in bats from
heavy-metal poisoning is less certain,
but interpretations often can be made
based on other species of mammals
(Clark 1979, this paper). Diagnosis
for heavy metals involves analyzing
liver and kidneys along with histological examination for damage.
Death in bats caused by the anticholinesterase insecticides could be
diagnosed by measurement of depressed brain ChE in combination
with detection of an anticholinesterase chemical in the contents of the
gastrointestinal tracts or other tissues
of the affected bats. Lethal depression of brain ChE has been measured
in little brown bats (M. lucifugus) in
the laboratory for methyl parathion
(phosphorothioic acid 0,O-dimethyl
0-(4-nitrophenyl )ester) and
Orthen@ (acephate; acetylphosphoramidothioic acid 0,s-di-methyl ester)
(Clark 1986, Clark and Rattner 1987).
Even though a firm diagnosis of
contaminant-induced mortality requires tissue analyses, analysis of a
guano sample, as a first step, may
indicate whether organochlorines or
metals are involved.
Chemical analyses of tissues or
guano are not something that managers usually can perform themselves.
However, an Environmental Contaminant Field Specialist from the
U.S. Fish and Wildlife Service can be
contacted (there are 1-3 in each
state); if he or she determines that the
situation warrants, analyses can be
done. The Specialist also may send
specimens to the National Wildlife
Health Research Center if disease is
suspected.
Bat specimens for diagnostic study
generally should be frozen immediately. However, examinations for
diseases and histopathology require
that specimens be kept refrigerated
but not frozen until organs can be
removed and preserved in fluid.
Control specimens of the same species are necessary for diagnosis of
depressed brain ChE activity. Guano
does not iequire freezing or refrigeration. The Contaminant Field Spe-
cialist can provide detailed instructions for specimen collection and
handling.
Possible Impacts of New
Generation Pesticides on But
Colonies
Most organochlorine pesticides have
been banned or their use otherwise
reduced in the U.S., And some wildlife-related problems have improved.
Organochlorines largely have been
replaced by organophosphorus (e.g.,
Acephate, diazinon [phosphorothioic
acid 0,ediethylO-[6-methyl-2-(1-
methylethy1)Q-pyrimidinyllester],
and methyl parathion) and carbamate (e.g., Aldicarb [2-methyl-2(methy1thio)propanal0-[(methylamino)carbonyl]oxime],carbaryl [lnaphthalenol methylcarbamate], and
carbofuran [2,3-dihydro-2,2-dimethyl-7-benzofuranol methylcarbamate]) insecticides. These chemicals are relatively short-lived and
generally d o not accumulate in food
chains. Exposure in bats probably
occurs when they feed over fields or
orchards that are being, or have just
been, sprayed. In these cases, bats
might be sprayed directly and receive the chemical through their skin
and lungs. Pesticides are frequently
sprayed in the evening, at night, or
early in the morning to avoid killing
honey bees, to kill adult mosquitoes,
or to take advantage of quiet wind
conditions and thereby avoid drift.
Bats also may be exposed by eating
insects that have just been sprayed
but are still alive.
New-generation pesticides have
not yet been linked to bat die-offs,
but, in 1968, ranchers and farmers in
a cotton-growing area of Arizona reported "...unusual Numbers of dead
or dying (free-tailed) bats in their
fields.. .Many Were found convulsing, incapable of flight" (Reidinger
and Cockrum 1978).This mortality
was attributed to DDT; however,
chemical analyses indicated that neither lethal residues of DDT nor its
metabolites had been present in these
bats (Clark 1981b). Because methyl
parathion also was commonly used
on cotton in this region, mortality
may have been caused by this organophosphorus pesticide. The mortality pattern described by ranchers
and farmers where bats were scattered on the ground in an incapacitated condition suggests quick intoxication after direct contact with a
chemical of high acute toxicity such
as the organophosphate methyl parathion (see Clark 1986).
Reducing Contaminant Impacts in
Bat Colonies
What can be done once it is determined that bats have died from a
food-chain contaminant? The answer
will depend on the contaminant, its
source, and on the ability or authority of the manager to change local
practices or obtain cleanup procedures.
When large quantities of a longlived chemical have been incorporated into soils over vast areas, such
as DDE in New Mexico or dieldrin in
Missouri, the chemical will continue
to enter food chains for many years.
The manager of an affected bat colony can only protect the colony form
other sources of damage and hope
that it survives until the contamination dissipates. If the colony is extirpated, the manager can protect the
site so that it might be recolonized
from outside the contaminated area
in the future.
After a colony is known to be
heavily contaminated with an organochlorine or metal, annual analyses of guano can determine whether
contamination is decreasing, increasing, or remaining stable, and also can
alert the manager to potential problems. For example, in Missouri, heptachlor epoxide increased from minor amounts in bats in 1976 to near
lethal levels in 1977 (Clark et al.
1983a).Such information promptly
passed to the state authorities might
persuade them to recommend a different pesticide to farmers before the
problem chemical becomes heavily
dispersed over wide areas.
The Alabama example given previously shows that large cleanup efforts are possible if the contamination is, in total or in part, localized.
State and federal agencies represent
routes open to managers. In this instance, the U.S. Environmental Protection Agency exercised its authority. Whether alarge cleanup effort
would be undertaken if only bats
were affected is not known; however,
if organochlorine contamination is
heavyenough to cause mortality in
bat colonies, it probably affects other
wildlife as well. Bat colonies are
good places to look for food-chain
contaminant problems because bats
feed over wide areas but congregate
in only a few roosts. Thus, problems
from many potential areas are
brought to a single site where symptoms may be seen as dead or dying
bats. The disadvantage is that it may
be difficult to locate the source area,
or areas, unless the feeding locations
of the bats are known.
Heavy metals in the environment
often have industrial point sources
that are subject to existing emission
regulations. Therefore, such contamination may be easier to stop.
Acknowledgments
I thank R.L. Clawson, E.L. Flickinger,
K.N. Geluso, C.E. Grue, and T.H.
Kunz for critical reviews of the
manuscript.
Literature Cited
Allison, Vernon C. 1937. Evening bat
flight from Carlsbad Caverns.
Journal of Mammalogy 18:80-82.
Altenbach, JScott, Kenneth N.
Geluso, and Don E. Wilson. 1979.
Populations size of Tadarida brasiliensis at Carlsbad Caverns in 1973.
p. 341-348. In H.H. Genoways and
R.J. Baker, eds. Biological investigations in the Guadalupe Mountains National Park, Texas. Proceedings and Transactions Series
Number 4, National Park Service.
Anonymous. 1987. Thornhill cave bat
killer convicted. Bats, December
5:2,8.
Clark, Donald R., Jr. 1979. Lead concentrations: bats vs. Terrestrial
small mammals collected near a
major highway. Environmental
Science and Technology 13:338341.
Clark, Donald R., Jr. 1981a. Death in
bats from DDE, DDT or dieldrin:
diagnosis via residues in carcass
fat. Bulletin of Environmental
Contamination and Toxicology
26:367-374.
Clark, Donald R., Jr. 1981b. Bats and
environmental contaminants: a
review. United States Fish and
Wildlife Service Special Scientific
Report-Wildlife, Number 235.
Clark, Donald R., Jr. 1986. Toxicity of
methyl parathion to bats: mortality and coordination loss. Environmental Toxicology and Chemistry
5:191-195.
Clark, Donald R., Jr., Fred M. Bagley,
and W. Wynon Johnson. 1988.
Northern Alabama colonies of the
endangered gray bat Myotis grisesens: organochlorine contarnination and mortality. Biological Conservation 43:213-225.
Clark, Donald R., Jr., Christine M.
Bunck, and Eugene Cromartie.
1983a. Year and age effects on residues of dieldrin and heptachlor in
dead gray bats, Franklin County,
Missouri-1976,1977, and 1978.
Environmental Toxicology and
Chemistry 2:387-393.
Clark, Donald R., Jr., Richard L.
Clawson, and Charles J. Stafford.
1983b. Gray bats killed by dieldrin
at two additional Missouri caves:
aquatic macroinver tebrates found
dead. Bulletin of Environmental
Contamination and Toxicology
30:214-218.
Clark, Donald R., Jr., and Alexander
J. Krynitsky. 1983. DDT: recent
contamination in New Mexico and
Arizona? Environment 25:27-3l.
Clark, Donald R., Jr., Thomas H.
Kunz, and T. Earl Kaiser. 1978a.
Insecticides applied to a nursery
colony of little brown bats (Myotis
lucifugus): lethal concentrations in
brain tissues. Journal Mammalogy
59:84-91.
Clark, Donald R., Jr., Richard K.
LaVal, and Douglas M. Swineford.
1978b. Dieldrin-induced mortality
in an endangered species, the gray
bat (Myotis grkescens). Science
199:1357-1359.
Clark, Donald R., Jr., Richard K.
LaVal, and Merlin D. Tuttle. 1982.
Estimating pesticide burdens of
bats from guano analyses. Bulletin
of Environmental Contamination
and Toxicology 29:214-220.
Clark, Donald R., Jr., and Richard M.
Prouty. 1984. Disposition of dietary dieldrin in the little brown bat
and correlation of skin levels with
body burden. Bulletin of Environmental Contamination and Toxicology 33:177-183.
Clark, Donald R., Jr., and Barnett A.
Rattner. 1987. Orthene" toxicity to
little brown bats (Myotis lucifugus):
acetylcholinesteraseinhibition, coordination loss, and mortality.
Environmental Toxicology and
Chemistry 6:705-708.
Clark, Donald R., Jr., Anne Shapiro
Wenner, and John F. Moore. 1986.
Metal residues in bat colonies,
Jackson County, Florida, 19811983. Florida Field Nat. 14:38-45.
Ellman, George L., K. Diane Courtney, Valentino Andres, Jr., and
Robert M. Featherstone. 1961. A
new rapid colorimetric determination of acetylcholinesterase activity. Biochemistry and Pharmacology 7:88-95.
Fleming, W. James, and Thomas Z.
Atkeson. 1980. Situation report:
heavy DDT contamination at
Wheeler National Wildlife Refuge.
Proceedings of the Annual Conference of the Southeast Association
of Fish and Wildlife Agencies
34:453-461.
Fleming, W. James, and Eugene Cromartie. 1981. DDE residues in
young wood ducks (Aix sponsa)
near a former DDT manufacturing
plant. Pesticides Monitoring Journal 14:115-118.
Fleming, W. James, Burline P. Pullin,
and D.M. Swineford. 1984. Population trends and environmental
contaminants in herons in the Tennessee Valley, 1980-81. Colonial
Waterbirds 763-73.
Geluso, Kenneth N., J. Scott Altenbach, and Don E. Wilson. 1976. Bat
mortality: pesticide poisoning and
migratory stress. Science 194:184186.
Hill, Elwood F., and W. James Fleming. 1982. Anticholinesterase poisoning of birds: field monitoring
and diagnosis of acute poisoning.
Environmental Toxicology and
Chemistry 1:27-38.
Hunt, W. Grainger, Brenda S.
Johnson, Carl G. Thelander, Brian
J. Walton, Robert W. Risebrough,
Walter M. Jarman, Alan M. Springer, J. Geoffrey Monk, and Wayman Walker 11.1986. Environmental levels of p,p'-DDE indicate
multiple sources. Environmental
Toxicology and Chemistry !XI -27.
Maly, Mark S. 1984. Survivorship of
meadow voles, Microtus pennsylvanicus, from sewage sludgetreated fields. Bulletin of Environmental Contamination and Toxicology 32:724-731.
Nomiyama, Kazuo. 1981. Renal effects of cadmium. p. 643-689. In
J.O. Nriagu, ed. Cadmium in the
environment; part 2 health effects.
Environmental Science and Technology: A Wiley Series of Texts
and Monographs. John Wiley and
Sons, Inc., New ~ o r k .
O'Shea, Thomas, J., W. James Fleming 111, and Eugene Cromartie.
1980. DDT contamination at
Wheeler National Wildlife Refuge.
Science 209:509-510.
Petit, Michael G., and J. Scott Altenbach. 1973. A chronological record
of environmental chemicals from
analysis of stratified vertebrate
excretion deposited in a shelteted
environment. Environmental Research 6:339-343.
Prichard, Dennis E. 1987. Managing a
national wildlife refuge for bats.
Bats, December 5:6,8.
Reich, Andrew R., Jimmy L. Perkins;
and Gary Cutter. 1986. DDT con-'
tamination of a north Alabama
aquatic ecosystem. Environmental
Toxicology and Chemistry 5:725736.
Reidinger, Russell F., Jr., and E. Lendell Cockrum. 1978. Organochlorine residues in free-tailed
bats (Tadarida bmsiliensis) at Eagle
Creek Cave, Greenlee County,
Arizona. p. 85-96. In R.J. Olembo,
J.B. Castelino, and F.A. Mutere,
eds. Proceedings of the Fourth
International Bat Research Conference, Kenya Literature Bureau,
Nairobi.
Tuttle, Merlin D. 1979. Status, causes
of decline, and management of
endangered gray bats. Journal of
Wildlife Management 43:l-17.
United States Department of the Interior, Fish and Wildlife Service.
1987. Endangered and threatened
wildlife and plants, April 10,1987,
50 CFR 17.11 and 17.12. United
States Government Printing Office.
White, Donald H., and Alexander J.
Krynitsky. 1986. Wildlife in some
areas of New Mexico and Texas
accumulate elevated DDE residues, 1983. Archives of Environ-.
mental Contamination and Toxicology 15:149-157.
.