BOSTON PUBLIC LIBRARY 3 9999 06317 793 3 / EFFECTS OF ENVIRONMENTAL CONTAMINANTS ON REPTILES: A REVIEW UNITED STATES DEPARTMENT OF THE INTERIOR FISH AND WILDLIFE SERVICE Special Scientific Report— Wildlife No. 228 Library of Congress Cataloging in Publication Data Hall, Russell James, 1943- Effects of environmental contaminants on reptiles. (Special scientific report— wildlife ; no. 228) Supt.of Docs, no.: I 49.15/3:228 1. Pesticides and wildlife. 2. Reptiles— Diseases. 3. Reptiles— Phys- iology. I. Title. II. Series. SK361.A256no. 228 [QL669.2] 639.9'0973s [597.9'0424) 80-607012 NOTE: Use of trade names does not imply U.S. Government endorsement of commercial products. EFFECTS OF ENVIRONMENTAL CONTAMINANTS ON REPTILES: A REVIEW By Russell J. Hall UNITED STATES DEPARTMENT OF THE INTERIOR FISH AND WILDLIFE SERVICE Special Scientific Report— Wildlife No. 228 ^wupo^ Washington, D.C. • 1980 Effects of Environmental Contaminants on Reptiles: A Review By Russell J. Hall U.S. Fish and Wildlife Service Patuxent Wildlife Research Center Laurel, Maryland 20811 Abstract The literature relating to the effects of environmental contaminants on reptiles is reviewed and certain generalizations based on studies of other kinds of vertebrates are presented. Reports of reptilian mortality from pesticide applications are numerous enough to establish the sensitivity of reptiles to these materials. Reports of residue analyses demonstrate the ability of reptiles to accumulate various contaminants, but the significance of the residues to reptilian populations is unknown. A few authors have reported the distribution of residues in reptilian tissues; others have investigated uptake or loss rates. Physiological studies have shown that organochlorines may inhibit enzymes involved in active transport and have correlated the activity of potential detoxifying enzymes with residue levels. There is some suggestion that pesticide residues may interfere with reproduction in oviparous snakes. Needs for future research are discussed. Our knowledge of the effects of pesticides and other environmental contaminants on reptiles is severely limited. The literature consists of reports of reptilian mortality in field applications, reports of residue analyses, and a mere handful of studies designed spe- cifically to investigate reptilian responses to contami- nants. Not only is the available information frag- mentary, but it relies on a confusing array of test conditions, analytical procedures, and methods of reporting results. Opportunities for misinterpretation are many; despite nearly 40 years of study we have only scant knowledge of which chemicals may be par- ticularly hazardous to reptiles. Further, we can only speculate on the significance of residues of environ- mental contaminants found in tissues of reptiles. It is the purpose of the present review to summarize the available literature in a way that will permit future studies to be more responsive to the many questions that remain. For guidance one may turn to the literature on birds, which are close relatives of the reptiles, but even that extensive literature permits few generalizations. The most recent reviews of the effects of environmental contaminants on amniote vertebrates (Stickel 1973; Stickel 1975) do not deal at length with reptiles, but they indicate that the following six generalizations may apply to reptiles, based on findings with other groups: (1) Even closely related species may differ con- siderably in their sensitivity to a given toxicant. Taxo- nomic affinity may have some predictive value, but only to a limited extent. Falconiform birds, for example, are generally sensitive to certain organo- chlorines, but different species may differ considerably in relative sensitivity. (2) Species at higher trophic levels tend to suffer most from persistent contami- nants which cannot readily be detoxified or excreted. (3) The effects of contaminants vary considerably, de- pending on the physiological state of the animal. This is particularly true of fat soluble toxicants whose absorption and mobilization are strongly related to fat body cycling. (4) Metabolites of pesticides and other contaminants may be more or less toxic than the parent compound and more or less subject to storage. Toxicity thus depends on the form of the contaminant to which the animal is exposed. (5) Most contaminants appear to affect specific enzyme systems at the cellu- lar level and thus would be expected to produce a variety of sublethal effects in different organisms. (6) Species with long life cycles are more likely to be af- fected by persistent contaminants than the short-lived species characteristic of unstable habitats. Different classes of contaminants tend to have dif- ferent sites of action in adversely affecting verte- brates. The organochlorine insecticides seem to inhibit active transport of cations and acutely toxic amounts probably act by inhibiting nervous transmission. Also, organochlorines may act subacutely to impair eggshell deposition in birds of certain groups. PCB's are known to inhibit reproduction in certain mammals. The exact mechanisms of these reproductive effects are poorly 1 known because of yet another effect produced by organochlorines. The enzymes induced to detoxify certain organochlorines are relatively nonspecific and may also deplete steroid hormones; such depletion may have a variety of effects on the organism's homeo- static balance. Rarely organochlorines have been shown to mimic the effects of estrogens. Organophos- phate and carbamate insecticides act at the synapse, blocking nerve transmission by the inhibition of the enzyme acetylcholinesterase. Lethal action is thought to result from nerve blockage in the brain, but specific levels of inhibition are often difficult to relate to ef- fects on the whole organism. Also, delayed neurotox- icity, a secondary phenomenon resulting from demyel- ination, has been attributed to certain organophos- phates. Heavy metals may have various effects. More information on these phenomena can be found in the reviews cited above, in Matsumura (1975), and in Baron (1976). Effects of Pesticide Applications on Reptiles Reptiles have been killed by pesticides, usually as nontarget organisms receiving direct exposure to pesticides or by secondary poisoning resulting from the consumption of dead or moribund prey. Pesticides have been advocated as a means of snake control (Anon. 1957), but most large-scale mortality seems to have resulted from efforts directed at insects. In a recent article on control of vertebrate pests, Marsh and Howard (1978) reported that various organochlor- ines are toxic to reptiles and that DDT was formerly used successfully against snakes. The authors noted that no chemicals are presently registered for snake control, but that such control is often a "side benefit" of pesticides applied to houses and lawns for other pur- poses. Reptiles have been reported to be more sensi- tive to the effects of pesticides than are homeotherms, and reptilian mortality has been observed with dose levels that are generally safe for birds and mammals (Rudd and Genelly 1956). Such apparent sensitivity may result from the low metabolic rate of reptiles and their resultant inability to quickly detoxify contami- nants. Reptiles are apparently less sensitive than fish, but are not directly comparable to them because fish are continuously exposed to dissolved toxicants in their exchange of respiratory gases and thus may pas- sively accumulate some chemicals. Much of the literature on observed effects on reptiles from pesticide usage (Table 1) dates from the early years of organochlorine use. More recent accounts of die-offs of reptiles are relatively rare, probably because the lethality of pesticides to reptiles is well known and such reports are no longer considered to be of scientific interest. Also, recent uses of pesticides have tended toward less hazardous types and generally more judi- cious applications. Despite much evidence that organochlorine pesti- cides are toxic to reptiles, there have been few efforts to determine their acutely or chronically toxic levels. Logier (unpublished data) fed capsules with 0.01 g DDT to captive snakes and observed mortality in some individuals. Herald (1949) similarly reported both primary and secondary poisoning from DDT to reptiles. Indications that Agkistrodon piscivorus may be less sensitive to DDT than are various colubrid snakes were believed by Herald to be artifacts. Lizards (Anolis) were affected but not killed by eating dosed insects. Pond turtles {Chrysemys) seemed less sensi- tive than softshells {Trionyx) or mud turtles (Kino- sternon). Surprisingly, there have been no more recent investigations of the toxicity of pesticides to reptiles other than those of Brock (1965), and Braverman (1979) who investigated the hazards to snakes of sec- ondary poisoning by rodenticides. Reports on the symptoms of DDT intoxication in reptiles (Herald 1949; Logier, unpublished data) cite the tremors, loss of motor control, and paralysis that are characteristic of neurotoxicity. Similar behavioral effects were seen (Finley 1960) in a case of toxaphene poisoning. DeWitt and George (1960) summarized numerous observations on reptiles in areas treated with hepta- chlor (2.2 kg per hectare; 2 lb per acre) for fire ant control. One set of observations recorded the dis- appearance of a marked population of Agkistrodon piscivorus together with the elimination of Storeria and Natrix (=Nerodia). Snakes of the genus Tham- nophis persisted, but exhibited signs of poisoning. Observations on another area indicated that Nerodia were most affected and no ill effects were seen in Thamnophis, Heterodon, or Agkistrodon species. Nerodia are probably more thoroughly aquatic than the other species observed. Virtual elimination of aquatic turtles and reduction of populations of box turtles (Terrapene Carolina) were reported. In a detailed account of the aforementioned studies, Matschke (1961) presented convincing evidence that widespread mortality affected the populations ob- served. Apparent widespread mortality of lizards (Eumeces, Anolis) was observed following one application. Rosa to and Ferguson (1968) fed endrin resistant mosquitofish to a variety of vertebrate species. The fish developed resistance to endrin in areas of heavy usage of the pesticide and they pose a considerable hazard to their predators. Four species of reptiles were killed by eating resistant fish which were found to contain upwards of 1,000 ppm of endrin in the tissues. On an approximate dosage basis, 2 mg/kg were Table 1. Effect of pesticide applications on reptiles. Pesticide Application Species Effects Authority DDT Not stated Thamnophis sirtalis Storeria occipitomaculata Some killed Logier, unpubl. data DDT 0.6 kg/ha (0.5 lb/acre) Turtles None Couch (1946) DDT 4.9 kg/ha (4.4 lb/acre) Opheodrys aestivus Sceloporus olivaceous Some killed George and Stickel (1949) DDT 2.2 kg/ha (2 lb/acre) Nerodia sp. "Blacksnake" Killed Goodrumetal. (1949) DDT 0.3-0.7 kg/ha (0.3-0.6 lb/acre) 9 spp. snakes 1 sp. turtle 1 sp. lizard 2 spp. turtles Killed Killed "Sublethal effects" Herald (1949) DDT 1.1 kg/ha (1 lb/acre) Water snakes Killed Hoffman and Surber (1949) DDT 2.2 kg/ha (2 lb/acre) Terrapene Carolina No effects on population Stickel (1951) DDT 0.2 kg/ha (0.2 lb/acre) Nerodia fascia ta compressicauda Killed Mills (1952) DDT In cage Agkistrodon piscivorous Killed Munro(1949) DDT and BHC Up to 2.2 kg/ha (2 lb/acre) Malaclemys terrapin Terrapene Carolina None Springer (1961) Dieldrin Locally at tsetse breeding sites 2 spp. lizards Killed Koemanetal. (1971) Dieldrin Locally at tsetse breeding sites 10 spp. lizards 8 spp. snakes Killed Wilson (1972) Dieldrin and Heptachlor 2.2 kg/ha (2 lb/acre) Nerodia erythrogaster Storeria dekayi Killed Baker (1958) Dieldrin and Heptachlor 2.2 kg/ha (2 lb/acre) 3 spp. snakes Killed DeWittetal. (1960) Endrin Secondary intake Chrysemys scripta Nerodia erythrogaster N. rhombifera Agkistrodon piscivorus Killed Rosato and Ferguson (1968) Heptachlor 2.2 kg/ha (2 lb/acre) Nerodia sp. Agkistrodon piscivorus Killed Glasgow (1958) Heptachlor 2.2 kg/ha (2 lb/acre) 10 spp. snakes 2 spp. turtles Some killed DeWittand George (1960); Matschke(1961) Heptachlor 2.2 kg/ha (2 lb/acre) 2 spp. turtles 1 sp. lizard 5 spp. snakes Killed DeWittetal. (1962) Heptachlor 2.2 kg/ha (2 lb/acre) Chrysemys sp. Killed Roseneetal. (1961) Heptachlor 2.2 kg/ha (2 lb/acre) 2 spp. turtles 1 sp. lizard 4 spp. snakes Killed Ferguson (1963) Heptachlor 2.2 kg/ha (2 lb/acre) Turtles 2 spp. lizards 6 spp. snakes Killed Smith and Glasgow (1965) Vapona Topical Snakes None Lentz and Hoessle (1971) Table 1 (cont.) Pesticide Application Species Effects Authority Phosphamidon 1.1 kg/ha Agkistrodon spp. None Oliver (1964) and Bidrin (1 lb/acre), 0.3 kg/ha ('■a lb/acre) Nerodia spp. Six rodent Secondary Pituophis catenifer None Brock (1965) poisons intake Strychnine Alkaloid Secondary intake Pituophis catenifer Killed Brock (1965) Fluoroacetamide Secondary intake 3 spp. snakes None Braverman(1979) (1081) Toxaphene 2.2 kg/ha Chrysemys picta Killed Finley(1960) (2 lb/acre) Thamnophis sirtalis Killed required to kill the reptiles, whereas bird and fish species required an average of 9 and 13 mg/kg. Al- though dying on generally lower doses, the reptilian species always survived longer than the fish, amphib- ian, or avian species tested. In most instances in which reptiles were reported to have survived or been killed by pesticide applications, there was no determination of the amount of toxicant that had actually reached the animals. Such reports are of limited value in producing replicable data, but they are of great practical value in assessing the hazards posed to reptiles by pesticide applications. Kinetics of Contaminant Residues in Reptiles Reports of residues found in dead and surviving reptiles (Table 2) have shown that these animals can accumulate contaminants in different tissues in greatly differing amounts. However, because a variety of species, different methods of analysis, and exami- nation of different tissues have been used, few conclu- sions can be drawn concerning their significance. Im- proved technology has permitted increased accuracy in the detection and quantification of contaminant residues. These advances have often cast doubts on the accuracy of residue reports published before wide- spread application of the new methods. It was discov- ered, for example, that PCB's often interfere with quantification of DDT, DDD, or DDE (see Dustman et al. 1971). PCB's are nearly ubiquitous in wild animals and the failure of a report to mention PCB's may be cause for suspicion that PCB's are misreported as pesticide residues. PCB's and toxaphene are complex mixtures with components that are metabolized selec- tively by certain animals. Their quantification is dif- ficult and has not been standardized; comparisons of PCB residues are risky and probably valid only when reports are from the same laboratory and when PCB's are extracted from similar tissues. Another problem may arise when laboratories experienced in measuring residues in water, soil, or plants err by underesti- mating the problems of extraction and cleanup of resi- dues from animal tissues. All these factors may lead to erroneous residue reports. Residues are expressed on different bases (whole body or organ weights; wet weight, dry weight, lipid weight) and reports ex- pressed in these different ways cannot be compared directly. Organochlorines tend to accumulate in fat and large amounts of these materials may be safely stored by reptiles in the relatively isolated fat bodies. However, increased metabolism of fat may mobilize the residues, making them more available to other tissues. Fat may protect animals by partitioning insecticide residues, but the presence of fat in large amounts may actually enhance the storage of contaminants which might otherwise be detoxified or eliminated. Thus, although fat often has easily detected and quantified residues (Fleet et al. 1972; Lawler 1977; Stafford et al. 1976), their concentrations could be expected to vary greatly depending on the nutritional and reproductive state of the animal. Whole-body residues of contaminants may be more indicative, but these also depend on the amount of fat present, and percentage lipid probably should also be recorded to make such data more mean- ingful. Residues of other contaminants such as heavy metals also may be sequestered in inactive sites (for example, lead in bones) making residue levels difficult to interpret. The action of most organochlorine pesti- cides is probably in the brain; brain levels are diag- nostic of death in some homeotherms, but the lit- erature records no attempts to determine lethal levels in reptiles. Several investigators have attempted to show the rates of uptake and loss of environmental contami- nants in reptiles, or the distribution of these materials Table 2. Residues of environmental contaminants reported in dead and surviving reptiles. Authority Species Application (if reported) Sample type; basis on which residues are expressed3 Contaminants (max. cone, in ppm) DeWitt and George (1960) Reptiles 2.2 kg/ha (2 lb/acre) Whole body; dry weight Heptachlor epoxide (6.6) DeWittetal. (1960) 3 spp. snakes 2.2 kg/ha (2 lb/acre) Whole body; dry weight Dieldrin (77.5) Heptachlor epoxide (11.3) Finley(1960) Chrysemys picta 2.2 kg/ha (2 lb/acre) Whole body; dry weight Toxaphene (154) DeWittetal. (1962) Matschke(1961) Box turtle 8 spp. snakes 5 spp. snakes Terrapene Carolina 2.2 kg/ha (2 lb/acre) 2.2 kg/ha (2 lb/acre) Liver, heart, kidney, whole body; dry weight Whole body, liver, kidney; dry weight Heart, liver, kidney; dry weight Heptachlor epoxide (173.9) Heptachlor epoxide (66) Heptachlor epoxide (308) Roseneetal. (1961) Hognose snake Red-eared turtle 2.2 kg/ha (2 lb/acre) Whole body; dry weight Heptachlor epoxide (172- turtle) Keith and Hunt (unpubl. data) Trionyx spinifer Fat; lipid weight "Flesh," wet weight Viscera; wet weight DDE (700) DDT (32) DDE (8) DDT (0.43) DDE (12.5) DDT (3.7) Dieldrin (3.5) Heptachlor epoxide (1.1) Toxaphene (1.0) Cully and Applegate (1967a) 3 spp. Cnemidophorus Various tissues including fat; wet weight BHCU1.5) Methyl parathion (4.2)b Parathion (4.1) DDE (45.9) DDD(34.8) DDT (44.3) Cully and Applegate (19676) 3 spp. Cnemidophorus Muscle; wet weight BHCI2.0) Methyl parathion (5.1) Parathion (4.6) DDE (7.0) DDDI6.0) DDT (4.7) Meeks(1968) 3 spp. turtles 2 spp. snakes 0.2 kg/ha (0.2 lb/acre) Various tissues including fat; dry weight DDT (36.4) Applegate (1970) 5 spp. lizards Whole body; wet weight Methyl parathion (0.7)b Parathion (0.1) DDE (1.69) DDDd.50) DDT (1.50) Korschgen(1970) Thamnophis sirtalis Pituophis sayi 25.1 kg/ha (22.4 lb/acre) total over 17 years Whole body; wet weight Aldrin (0) Dieldrin (14.40) DDT (0.48) Koemanetal. (1971) Agama agama Panaspis dahomeyense Local applica- tions Whole body; wet weight Dieldrin (0.83) DDEK0.05) Table 2. (cont.) Authority Laubscheretal. (1971) Devine and Wilcox (1972) Dustman et al. (1972) Fleet etal. (1972) Ogdenetal. (1973) Snyder etal. (1973) Brisbin etal. (1974) Hillestad etal. (1974) Thompson etal. (1974) Vermeer etal. (1974) Bauerleet al. (1975) Species Application (if reported) Sample type; basis on which residues are expressed" Contaminants (max. cone, inppm) Pituophis melanoleucus Nerodia sipedon Thamnophis sirtalis 12 spp. snakes American alligator [Alligator mississippiensis) American crocodile [Crocodvlus acutus) 1.1 kg/ha (1 lb/acre) Sceloporus clarki S. jarrovi 19 spp. snakes Caretta caretta Chelonia mydas Caiman sclerops Pituophis catenifer 13 pesticides in variable amounts Liver, fat; wet weight Whole body; wet weight Carcass; liver; wet weight Fat; lipid weight Eggs; wet weight Whole body; wet weight Whole body; wet weight Tissue samples; wet weight eggs; wet weight Eggs; wet weight Brain, liver; wet weight Fat (for organo- chlorines); lipid weight Liver (for lead) DDE (8.5) DDD (0.047) DDT (1.6) Dieldrin (0.057) Trichlorfon(<0.05) DDVPK0.05) Mercury (0.60) DDE (1009.4) DDD (7.3) DDT (38.5) Dieldrin (13.8) DDE (3.23) DDD (0.16) DDT (0.59) Dieldrin (0.053) PCB (0.40) Arsenic (0.2) Mercury (0.71) Cadmium (0.05) Zinc (11) Lead (0.5) Copper (15) DDE (0.01) Radiocesium (1032.6 pCi/g) DDTRI0.30) Dieldrin (0.06) Mercury (0.09) Zinc (32) Cadmium (0.56) Copper (6) Lead (12) DDE (0.009) PCB (0.22) DDT (< 0.01) Dieldrin (< 0.01) EndrinKO.Ol) Pentachlorophenol (0.24) Mercury (0.41) DDE (1.06) DDT (0.05) Dieldrin (0.04) Oxychlordane (<0.01) Heptachlor epoxide (<0.02) cv-BHC(O.Ol) (i-BHC (0.013) PCB (0) Lead (0.659) Table 2. (cont.) Authority Species Application (if reported) Sample type; basis on which residues are expressed8 Contaminants (max. cone, in ppml Dimondetal. (1975) Janssenetal. (1976) Reeves etal. (1977) Woodhametal. (1977) Lawler(1977) Thamnophis sirtalis Aquatic snakes 4 spp. turtles Lizards, snakes Drymarchon corais Rolfe etal. (1977) Stafford etal. (1976) Fleet and Plapp( 1978) Hall etal. (1979) Thamnophis sirtalis T. radix Nerodia spp. Agkistrodon spp. 10 spp. snakes Crocodylus acutus Holcomb and Parker (1979) Punzoetal. (1979) Chrysemys scripta Terrapene Carolina 4 spp. snakes 1.1 kg/ha (1 lb/acre) Multiple appli- cations 8 pesticides, multiple appli- cations 8.4 kg/ha (7.5 lb/acre) total of 4 applications 8.4 kg/ha (7.5 lb/acre) total of 4 applications Whole body; wet weight Fat; lipid weight Whole body; (minus shell) wet weight Whole body; wet weight Fat; lipid weight Whole body; dry weight Fat; lipid weight Fat; lipid weight Eggs; wet weight Liver; dry weight Eggs; dry weight Liver; dry weight Eggs: dry weight Fat; lipid weight DDT (3.20) DDE (31.6) DDD (3.9) DDT (4.7) Dieldrin (0.9) DDE (3.81) DDD (0.08) DDT (0.07) Dieldrin (0.01) Endrin(O.Ol) Ethyl parathion (0.01) IS-BHC (0.02) Heptachlor epoxide (0.0 1 ) Dieldrin (0.04) DDTR (57.85) Dieldrin (13.3) Heptachlor epoxide (4.02) frarcs-nonachlor (2.42) Octachlor epoxide (=oxychlordane)(2.39) Mirex (17.20) PCBU2.3) Lead (9.6) Lead (69.7) DDE (1,161.2) PCB (123.3) DDE (596.6) DDT (14.6) DDE (2.9) DDD (0.07) DDT (0.23) Dieldrin (0.03) Heptachlor epoxide (0.04) Oxychlordane (0.07) c/s-chlordane (0.01) frans-nonachlor (0.04) ds-nonachlor (0.03) Mirex (0.02) PCB (1.4) Mirex (2.1) Mirex (2.2) Mirex (4.1) Mirex (2.5) DDE (0.22) Dieldrin (0.13) Heptachlor epoxide (0.05) Table 2. (cont.) Authority Species Application (if reported) Sample type; basis on which residues are expressed3 Contaminants (max. cone, in ppm) Punzo et al. (1979) 2 spp. turtles 9 spp. lizards Snake eggs (3 spp.) Turtle eggs (1 sp.) Fat; lipid weight Carcass or viscera Wet weight Wet weight DDE (0.02) Dieldrin (0.07) DDE (0.25) Dieldrin (0.01) DDE (0.06) Dieldrin (0.05) Heptachlor epoxide (0.04) DDE, Dieldrin, Hepta- chlor epoxide not detected aWhole body wet weights yield the lowest apparent levels, relative to organochlorine residue loads. When expressed on a dry weight basis, the same loads will yield apparent levels about 4 times as great. When expressed on the basis of lipid weight, the levels reported are usually many times those based on the actual body weight. bMost other investigators have been unable to confirm residues of parathion and methyl parathion. among various tissues. Meeks (1968) reported DDT residues in several species of reptiles inhabiting a marsh that had been treated with 0.2 kg per hectare (0.2 lb per acre). In Chelydra serpentina, Emydoidea blandingi, and Chrysemys picta, the highest levels (up to 16.5 ppm) were found in fat. The liver contained the next highest residues (up to 2.7 ppm). The highest brain residue level found was 1.2 ppm which evidently was below the lethal level for E. blandingi. Fat resi- dues up to 36.4 ppm were found in Nerodia sipedon and one of these water snakes had a brain residue level of 11 ppm. Kidney residue levels in this species and Elaphe vulpina were high (up to 7.3 ppm) and tended to exceed liver levels. The residue levels reported in reptiles exceeded those in the birds, mammals, and fish tested. Owen and Wells (1976) fed captive turtles DDT, sacrified them at various times and assayed brain, liver, and fat for residues. In both Chrysemys scripta and C. picta, there was little significant accumulation in the first 24 h. In turtles dosed weekly for 3 weeks, there was significant accumulation in fat, but also a large concentration of DDD in the brain (17.19 ppm) was reported in C. scripta. Total residues in fat (97.9 ppm in C. scripta) were largely in the form of DDT and DDD. Cully and Applegate (1976a, 19766) analyzed for var- ious pesticide residues in three species of Cnemido- phorus and noted a decline from June to August. They attributed this loss to egg laying; pesticide residues were removed from the females when eggs were laid. This was supported by the finding that eggs contained five times the residue levels of adult females. Fleet and Plapp (1978) showed a decline in residues of DDE and DDT after a 3-year period following ces- sation of DDT application. The loss rate was slow (a 50% decline in 3 years) and there was a general in- crease in the amount of DDE relative to DDT. Holcomb and Parker (1979) showed that mirex resi- dues in two turtle species declined almost contin- uously over an 8-year period. Hall et al. (1979) com- pared residues of organochlorines in crocodile eggs col- lected in 1977-78 with residues recorded 5 years earlier. They noted significant declines in DDD and DDT, but no significant decrease in the amounts of DDE or dieldrin. Pearson et al. (1973) injected Chrysemys scripta adults with 20 mg/kg of dieldrin in a single dosing and analyzed tissues from animals sacrificed at various intervals after dosing. They found the highest concen- trations (up to 1,329 ppm) in fat 70 days after dosing. Liver and most other tissues also increased in residue levels continuously over the 70-day test period. Brain levels reached nearly 27 ppm without reported ill effects. Part of the concentration reported in tissues apparently resulted from starvation during the test. Robinson and Wells (1975) orally dosed Trionyx spinifer with 2 mg of cadmium acetate per animal. They found apparent concentration in the liver and kidney. However, their data indicate that part of the dose remained in the gut and absorption was not com- plete in the 96-h duration of the test. The studies by Owen and Wells (1976) and Pearson et al. (1973) cited above may be somewhat diminished in value by indications that the animals used had sig- nificant prior exposure to organochlorine pesticides. Similarly, the turtles used by Robinson and Wells (1975) had a history of exposure to high levels of heavy metals. Table 3. Residues in animals thought to have been killed by pesticides. Species Chemical Mean residue level (ppm) Reporting basis Authority Storeria dekayi Dieldrin 77.5 Panaspis dayhomeyense Dieldrin 0.83 Nerodia sp. Heptachlor epoxide 11.3 Heterodon sp. Heptachlor epoxide 4.2 Agkistrodon piscivorus Heptachlor epoxide 13.2 Nerodia erythrogaster Heptachlor epoxide 24.6 Nerodia rhombifera Heptachlor epoxide 18.5 Lampropeltis getulus Heptachlor epoxide 54.0 Thamnophis sauritus Heptachlor epoxide 18.1 Thamnophis sauritus Heptachlor epoxide 4.6 Masticophis flagellum Heptachlor epoxide 4.6 Nerodia sp. Heptachlor epoxide 11.7 Chrysemys sp. Heptachlor epoxide 2.2 Lizard sp. Heptachlor epoxide 5.0 Chrysemys sp. Heptachlor epoxide 172.0 Chrysemys picta Toxaphene 154.0 Whole body, dry weight Whole body, wet weight Whole body, dry weight Whole body, dry weight Whole body, dry weight Whole body, dry weight Liver, dry weight Liver, dry weight Whole body, dry weight Whole body, dry weight Whole body, dry weight Whole body, dry weight Whole body, dry weight Whole body, dry weight Whole body, dry weight Whole body, dry weight DeWittetal. (1960) Koemanetal. (1971) DeWittetal. (1960) DeWittetal. (1960) Matschke(1961) Matschke(1961) Matschke(1961) Matschke(1961) Matschke(1961) DeWittetal. (1962) DeWittetal. (1962) DeWittetal. (1962) DeWittetal. (1962) DeWittetal. (1962) Roseneetal. (1961) Finley(1960) Correlation of Residues With Lethality The few instances in which mortality of reptiles can be related to specific residue levels have resulted from test sprayings, mostly conducted in the early 1960's (Table 3). Variation and sources of error in the re- ported residues include the possibility that the animal may not have died as a direct result of pesticide poisoning. Also, it is probable that an individual could assimilate far more than a lethal dose of a pesticide before its toxic effects are felt. Matschke (1961), working in an area treated with heptachlor, collected for chemical analysis specimens killed by the pesticide. He was also able to collect sur- viving individuals of Thamnophis sauritus. Two sur- vivors contained whole-body residues of heptachlor epoxide of 5.9 and 7.9 ppm (dry weight) and two killed individuals had 17.6 and 18.5 ppm. Various tissues of box turtles contained from 24 to 308 ppm (dry weight) heptachlor epoxide. Only turtles surviving the spray were reported because none of the numerous indi- viduals killed by the spray was recovered in suitable condition for analysis. The report by Lawler (1977) exemplifies the prob- lems of diagnosing deaths of individuals as contami- nant-related. Fat samples from eastern indigo snakes (Drymarchon corais) which had died in captivity in the Atlanta Zoo had residues of a number of pesticides in varying amounts. Because of the variables affecting storage of residues in fat and the lack of comparative evidence on mortality, little can be said about the rela- tions of these residues to the condition of the snakes. One male had 13.3 ppm dieldrin, but this is close to the amount reported by Fleet et al. (1972) in apparently healthy water snakes. Also, it is possible that the resi- dues in the indigo snake had been concentrated as a result of emaciation. Sublethal Effects of Contaminants on Reptiles Fleet et al. (1972) sampled snakes from two areas in Texas, one with a long history of pesticide use and the other relatively free of pesticide applications. They found high residues in snakes from the heavy appli- cation area and a statistically different species com- position between the two areas. Oviparous species were nearly absent from the high-residue area, pos- sibly resulting from interferences with reproduction similar to those seen in certain birds. This phenom- enon has not been investigated in more detail. How- ever, when Fleet and Plapp (1978) resampled the area 3 years later, they found a decrease in DDT residues and an apparent increase in the proportion of egg-laying species. Phillips and Wells (1974) and Wells et al. (1974) reported on the effects of organochlorine insecticides on adenosine triphosphatase activity in various species of turtles. Using in vitro methods, they dosed excised tissues with three levels of pesticide and assayed for total Na*-, K*-, and Mg2*-dependent ATPases. Phillips and Wells (1974) found these systems to be affected by DDT; however, at the lowest dose level the effect was stimulatory. Results were generally similar for the five species (Graptemys geo- graphica, Chelydra serpentina. Trionyx spinifer, Chrysemys scripta. and C. picta) tested. Wells et al. (1974) used various tissues of Graptemys geographica to investigate the effects of aldrin and dieldrin on the 10 same enzyme systems. They found inhibition at all three dose levels chosen and observed greater effects from dieldrin than from aldrin. Neither study used brain tissue in assays although it is the presumed pri- mary site of action by the pesticide. Stafford et al. (1976) noted the differences in species composition and residue levels reported by Fleet et al. (1972) and attempted to explain these differences by interspecific differences in detoxifying mechanisms. The enzyme systems thought to function in pesticide metabolism were NADPH microsomal oxidase which acts on organochlorines, and glutathione-dependent alkyltransferase, which acts on organophosphate insecticides. For assays, the breakdown of radioac- tively labelled testosterone and fenitrothion was meas- ured. They found that Agkistrodon spp. had greater NADPH microsomal oxidase activity in the liver than did species of Nerodia, apparently explaining the lower residue levels in Agkistrodon from the same habitats as Nerodia. Alkyltransferase activities were also higher in A. piscivorus, but were relatively lower in A. contortrix. Low activities of both enzymes in N. rhombifera were suggested to account for its absence from high-residue areas. The authors concluded that microsomal oxidase activity is more closely correlated with residues and distribution patterns than is alkyl- transferase. Stickel (1951) studied the effects of an annual aerial application of DDT (2.2 kg per hectare; 2 lb per acre) on survival and growth in a natural population of box turtles. No significant effects on growth or survival were found, suggesting that a variety of physiological mechanisms were functioning normally. Needs for Future Research Research on the effects of environmental contami- nants on reptiles should proceed on several fronts. A series of experiments should examine whether certain contaminants have sublethal effects of possibly great consequence in nature, as have been seen in other kinds of vertebrates. Behavioral and reproductive studies could be carried out on relatively small captive populations, following the protocols that have already been well tested. Both lethal and sublethal effects are strongly related to the kinetics of the contaminants in reptiles and a second line of research should investi- gate this aspect of the problem. Reptiles are active and predatory for the most part, yet they are metabol- ically less able than homeotherms, suggesting that reptiles' uptake and loss patterns of contaminants would differ greatly from those of homeotherms. Ki- netic studies would not only be of intrinsic interest, but they might also help in the interpretation of the residue data that have accumulated. Work on levels of cholinesterase inhibition that are diagnostic of lethal exposure to organophosphate and carbamate pesticides is proceeding in other kinds of vertebrates and should be pursued in reptiles. Com- parative studies of fish, birds, and mammals (e.g., Murphy et al. 1968) have shown remarkable dif- ferences in sensitivity to different organophosphorus insecticides. Other studies (Andersen et al. 1977) have shown amphibians to be many times less sensitive to most organophosphates than other groups tested. Sur- prisingly, no information on reptilian sensitivity to these chemicals is available. Some studies on the effects of certain cholinesterase inhibitors on reptiles are under way at Patuxent Wildlife Research Center, but additional work is necessary. Reptiles offer certain advantages for physiological study (Pearson et al. 1973), and it is likely that studies with reptilian subjects to investigate the mode of action of pesticides will continue. Although usually undertaken with other goals, such studies might lead to information of significance to reptilian biologists concerned with contaminants in the field. Petroleum hydrocarbons, either leaking slowly from permanent sources or catastrophically from accidental spills, may threaten aquatic or marine reptiles. Mor- tality of sea turtles (Chelonia and Lepidochelys) has been associated with the IXTOC I oil spill (Patuxent Wildlife Research Center, unpublished data). Also, there is some fear that sea turtle nests may be con- taminated with oil and that the eggs may be as vul- nerable to tiny amounts of oil as are bird eggs. Synthetic pyrethroids are a new class of insecticide that may be widely used in the future. They are said to be highly toxic and more persistent than organophos- phates. Their effects on reptiles are unknown. Closer attention to contaminant-produced episodes involving reptiles would help to identify sensitive species and particularly hazardous chemicals. Further, this attention would suggest research that might lead to conclusions of specific or general applicability. As for threatened or endangered species, special attention should be devoted to determine whether pollutants might be contributing to the status of their popu- lations. When working with threatened or endangered species which are not available for experimental veri- fication of suspected contaminant problems, certain experimental subjects might have high potential for predictive value. For example, experiments on the American alligator (Alligator mississippiensis) might be of great value in dealing with contaminants in the many endangered species of crocodilians. In summary, the efforts devoted to contaminant effects on birds, mammals, and aquatic organisms should be duplicated on reptilian subjects. Such ef- forts might not only protect reptilian populations, but also might benefit populations of other kinds of verte- 11 brates because reptiles might strongly show effects which are expressed only subtly in birds and mam- mals. Acknowledgments L. F. Stickel and W. H. Stickel read the manuscript at different stages in its preparation and provided val- uable technical suggestions. References Andersen, R. A., I. Aaraas, G. Gaare, and F. Fonnum. 1977. 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GPO 855- 592 As the Nation's principal conservation agency, the Department of the Interior has responsibility for most of our nationally owned public lands and natural resources. This includes fostering the wisest use of our land and water resources, protecting our fish and wildlife, preserv- ing the environmental and cultural values of our national parks and historical places, and providing for the enjoyment of life through out- door recreation. The Department assesses our energy and mineral resources and works to assure that their development is in the best interests of all our people. The Department also has a major responsi- bility for American Indian reservation communities and for people who live in island territories under U.S. administration. UNITED STATES DEPARTMENT OF THE INTERIOR FISH AND WiLOLIFE SERVICE EDITORIAL OFFICE AYLESWORTH HALL. CSU FORT COlLIMS. COLORADO 80S23 POSTAGE AND FEES PAID U.S. DEPARTMENT OF THE INTERIOR INT 423 NOTE: Mailing lists are computerized. 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