CONSEQUENCES OF INSECTICIDE USE ON NONTARGET ORGANISMSl

By L. D. NEWSOM

Department of Entomology, Louisiana State University, Baton Rouge, Louisiana

The existence of some excellent reviews dealing with the effects of pes­ticides on nontarget organisms (5, 31, 40, 49, 62, 68, 71, 85, 95, 125, 128. 131, 137, 150, 168, 169), permits concentration On areas of special signifi­

cance. Space limitations preclude consideration of many important subjects in this complex field. The chlorinated hydrocarbon insecticides only will be considered. They have been used more widely and longer, analytical tech­niques for identification of their residues are more efficient, and their ten­dency for persistence and concentration in biological systems is greater than is the case for other pesticides.

BACKGROUND

Adverse effects of insecticides on nontarget organisms have been gen­erally recognized by biologists. However, man has been forced to rely in­creasingly upon the use of chemicals for pest control by the demands for more high quality food and fiber and better protection from pests that affect his health and comfort. Use of insecticides has increased tremendously during the last two decades under the pressures of these demands. However. benefits

that have accrued to mankind from their use have been attended by some grave problems. That nontarget organisms have been seriously affected in many situations has become increasingly apparent.

Apprehension over the side effects of insecticide use increased during the late 1950's as "eradication" programs (146) were expanded. Applications of DDT and heptachlor to relatively large, contiguous areas for control of gypsy moth, Porthetria dispar, and the imported fire ant, Solenopsis saevis­sima richteri, respectively , resulted in obviously drastic effects on nontarget

organisms. Publication of Silent Spring (50), biased, emotional, and subjec­tive though it is, served the purpose of focusing attention of the general public on this serious problem.

Soil, air, water, and sunlight are the four basic ingredients of life on Earth. Of these, all except sunlight are polluted with one or more chlorinated hydrocarbon insecticides in measurable amounts. The consequences of expo­sure of many forms of life to this relatively new environmental factor are now beginning to be partially elucidated. Knowledge of the extent of occur­rence of such a factor is basic to an understanding of its effects. It appears to be ubiquitous.

1 The survey of the literature pertaining to this review was concluded in May 1966.

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WATER

Insecticides may contaminate water by direct application to water sur­faces, accidental application and drift, runoff from treated areas, and waste materials from insecticide and manufacturing plants.

The application of insecticides directly to water surfaces for control of rice pests and mosquitoes is a common practice (19, 48, 112). Rates of ap­plication are often high enough to give initial concentrations in excess of acutely toxic doses for many aquatic organisms (Table I).

TABLE [

RELATIVE TOXICITY TO AQUATIC ORGANISMS OF SOME CHLORINATED HYDROCARBON INSECTICIDES ApPLIED DIRECTLY TO WATER SURFACES FOR CONTROL OF

MOSQUITOES AND RICE PESTS

Oysters' Shrimp" Fish' Initial concentration Crassostrea Penaeus Mugil Phyto- inc ppm at rates

fJirginica spp. cu.rema p\anktonb recommended for Insecticide ---- % Decrease control of:

96-hour 48-hour 48-hour at 1 ppm

ECG. EC .. Le60 Mosquito Rice ppm ppm ppm larvae pests

DDT O.OO� 0.001 0.0006 77 0.03 0.60

Aldrin 0.005 0.0055 0.15

Chlordane 0.007 0.0044 0.0055 94 0.02 Heptachlor 0.027 0.00025 0.003 95 0.06

Dieldrin 0.034 0.0055 o.oon 85 0.03 0.15 Lindane (gamma BHC) 0.45 0.0004 0.03 29 0.06 1.20

a Data selected from (123). b Per cent decrease in productivity of natural phytoplankton communities including DunaUella

euchlara. Platymonas sp .. and others during a 4-hour exposure.

o Calculated from minimum amounts recommended. assuming water depth of 6 inches and deposi­

tion of total amount applied UPOII water surface.

About 5 per cent of the total land area of the United States is treated each year at the average rate of 2.5 pounds of insecticide per acre (81). Much of the 90,000,000 acres treated is in fertile alluvial areas adjacent to streams, lakes, and ponds where carelessness in application, drift, and runoff may be expected to result in substantial amounts of insecticides getting into water systems. Water erosion of soil particles to which insecticides have been ab­sorbed, with subsequent transport into streams by surface runoff, accounts for significant contamination of water systems (113, 139, 164).

Insecticides discharged in sewage and industrial wastes and in drainage from grossly contaminated areas may contaminate streams. Grzenda (79) reported the concentration of endrin in sewage sludge from an industrial plant draining into the Mississippi River to be one tenth that of a commer­cially formulated preparation used for control of sugarcane borer, Diatraea saccharalis. Much of the surface water in various areas of the world is now polluted with chlorinated hydrocarbon insecticides (95).

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PESTICIDES AND NONTARGET ORGANISMS

SOILS

259

Residues from applications to crops.-Substantial amounts of insecticides applied to crops reach the soil directly or indirectly. Residues from single applications to turf may persist for 4 to 12 years at levels amounting to 5 to 15 per cent of the initial amount applied (116). DDT has accumulated to as much as 7,11, and 54 pounds per acre in soils devoted to the production of potatos, corn, and apples, respectively (76).

Relatively low rates of application of some chlorinated hydrocarbon in­secticides to crops result in measurable amounts of residues in soils, more than 1 ppm of endrin in soils where sugar cane had received three to four applications per year at the rate of 0.25 to 0.33 pound per acre per applica­tion for five to six years, for example (113).

Residues from application to soils.-Insecticides used for the control of root-feeding pests are incorporated into the soils at depths of 1 to 6 inches, where many persist for a very long time (59, 115, 119, 173). At 38 months after application, DDT at 6, 15, and 60, and aldrin at 4 pounds per acre incorporated into the top 6 inches of silt loam soil were present at 75 to 77 per cent of the initial amount of DDT and 40 per cent of the aldrin (dieldrin) (63). About one fifth the amount of dieldrin applied at 2.5 ppm was still present nine years after application (173).

Rates of application usually recommended do not result in the accumula­tion of large amounts of residues in the soil. Decker et al. (59) reported that combined aldrin-dieldrin residues in 35 soils treated at rates ranging from 0.75 to 3.00 and averaging 1.66 pounds per acre for 3 out of 9 to 13 out of 13 years, ranged from 0.25 to 2.44 pounds per acre (0.12 to 1.22 ppm).They concluded that it would be improbable that accumulated residues would ever exceed the amount applied during one year. Their findings are similar to those of Wheatley (170), who reported residues of 2 ppm DDT and 0.5 ppm dieldrin for cultivated soils of the United Kingdom. Soils from some urban areas may contain residues as high as those in agricultural areas (67).

AIR

Relatively few data are available from studies on insecticide residues in air. All but 2 of 18 samples of ambient air collected from four California cities in the autumn of 1963 contained detectable amounts of DDT (168). The compound was reported at 0.0002 to 0.34 p,g per 1000 cc of filtered air collected over a 24-hour sampling period at 9 different stations (100). Air sampled at several localities in the United States and Canada in an attempt to learn the source of insecticides in remote, untreated areas contained DDT at levels from a trace, collected in 25 hours flying time over Canada, to 45 p,g in one-half hour over New Mexico (156).

.

Minute amounts of insecticides volatilized from surface applications, especially by codistiIIation with water vapor escaping from the soil, and small particles from spraying operations, may escape into the atmosphere

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(1, 5, 52). Wind erosion results in soil particles to which insecticides are absorbed being carried into the upper atmosphere in some areas as is prob­ably the case with pollen.

PLANTS

Translocation and concentration of insect·icide residues from soil.-During the last five years a body of data has been accumulated, with the aid of refinements in analytical techniques, to show that most of the chlorinated hydrocarbon insecticides penetrate plant tissues and are translocated at least to a limited extent (33, 42,117,126,146). Minute amounts of heptachlor or dieldrin residues on alfalfa hay fed to dairy cattle may result in detectable residues in milk produced by these animals. Dairy cows fed as little as 5 ppb of their daily roughage intake for a period of 28 days produced milk contain­ing 1.6 ppb (82). Residues of heptachlor epoxide equal to, or greater than this, were reported to have been translocated into the foliage of alfalfa (82, 118).

A highly significant recent development has been the establishment of the relationship of levels of insecticide contamination of crop seeds to their fat content (33, 42, 148). Oat, barley, corn, soybean, and peanut, representing a range of about 2 to 45 per cent oil content in the seed, grown on plots treated with heptachlor and aldrin at 2, 5, 10, and 20 pounds of the chemicals per acre, translocated residues into their seeds in detectable amounts (Table II), although that in corn, barley, and oat approached the minimum limits of detection. Soybean translocated about one tenth as much dieldrin or heptachlor epoxide into the seed as was present in the soil. At 1 ppm in the soil about 0.1 ppm can be expected in the seed. The consequences of an insecticide such as dieldrin being translocated into soybean seeds according to this relationship could be serious. Decker et al. (59) reported that 35 fields, considered to be representative of Illinois corn soils, con­tained an average of about 0.9 ppm dieldrin as a result of applications of aldrin to the soil for corn insect control (59). Soybean grown on such soils could be expected to accumulate about one tenth of the residue in the soil, and thus would contain almost 0.05 ppm without the addition of any insec­ticide to the crop. The ability of soybean to absorb insecticide residues from the soil and to translocate them to the seed is particularly significant because of the recent increase in acreage devoted to production of this crop.

The carrot is even more important than soybean in this respect, since it accumulates 12 to 100 per cent of the concentration of residues in soils in which it is grown (115, 126). Thus, carrots grown on many farms of England, Germany, and the United States could easily have residues of dieldrin or heptachlor epoxide in excess of permissible residues.

The chlorinated hydrocarbon insecticides are soluble in water at extremely small amounts ranging from DDT at about 0.0002 ppm to gamma BHe at about 10 ppm, for example. But, in natural oils such as linseed, peanut, or

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PESTICIDES AND NONTARGET ORGANISMS 261

cottonseed, DDT is soluble to the extent of 10 to 12 gm/100 cc. The direct relationship between residues of dieldrin and heptachlor epoxide in crop seeds and the percentage of oil in the seeds (42) suggests the possibility that minute amounts of insecticide dissolved in soil water and moving through the plant in the transpiration stream may be "captured" by oils occurring in the plant and deposited in the seeds. Mumma et al. (135) have hypo­thesized that chlorinated hydrocarbon insecticides are deposited in the sur­factant lipids of plants-phospholipids, sulfolipids and glycolipids-and may be physically or chemically associated with them.

ANIMALS INVERTEBRATES

Soil-inhabiting species.-Soil invertebrates have probably been studied less than any other group of animals. The comparative paucity of information in this area is attested to by the fact that only two general reviews have appeared in the literature (31, 58). The effects of insecticides on populations of these animals is illustrated by the report of Edwards & Jeffs (63). DDT at 6, 15, and 60, and aldrin at 4 pounds per acre incorporated into the top 6 inches of soil did not affect predatory mites but killed most other soil mites, greatly reduced most species of Collembola, and affected symphylids and pauropods only slightly. Earthworms, enchytraeid worms. and nema­todes were not affected. DDT was generally less toxic than aldrin (dieldrin) but killed high percentages of predatory mites, and at the higher dosage rates, killed the saprophagous mites. Collemboia increased at all treatment levels. suggesting the destruction of some of their predators. Symphylids and pauropods were affected more adversely by DDT than by aldrin; effects on earthworms, enchytraeid worms, and nematodes were similar for both chemicals.

Earthworms.-There has been more interest in possible adverse effects of insecticide applications on earthworms than other soil-inhabitating inverte­brates for two main reasons: The beneficial effects of earthworm activities in helping to maintain favorable physical properties of soils; and the possi­bility of earthworms carrying burdens of toxicants that could be transferred to other animals. especially birds. Davey (58) concluded that earthworms appear to be resistant to most insecticides except at very heavy dosages. Earthworm populations appeared to be unaffected by exposure to aldrin applications at two pounds per acre (36). However, rates such as those re­quired for control of Phyllophaga larvae, 10 pounds of chlordane or dieldrin per acre, for example, were toxic to Lumbricus terrestris and Allobophora calliginosa. Octolasium lacteum, L. terrestris. L. rubellus, and Helodrilus spp. contained residues as high as 53 to 204 ppm DDT and DDE (28). Birds whose diets were restricted to earthworms contaminated to this extent would be exposed to serious hazard.

Aquatic insects.-Acute toxicological effects of DDT on aquatic insects

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TABLE II N 0-

CONCENTRATION OF INSECTICIDES BY ANIMALS AND PLANTS EXPOSED TO KNOWN AMOUNTS OF RESIDUES N

Part Amount Ratio

Refe r-Species Insecticide Level of Exposure Stored Storagej

Analyzed Exposure

ence ppm

ANIMALS Earthworms Lumbricus terrestris DDT 9.9 ppm in soil Whole body 140.6 14 .2 (104) Allobophora caliginasa DDT 9.9 ppm in soil Whole body 140 .6 14 .2 (104) Sea squirt Styela plicata DDT 0.001 ppm in water for 10 days Whole body 10 10,000 (45) Aquatic invertebrates Toxaphene 0.63 ppb in water Whole body 1 .43 2,270 (166)

(not identified) Z Oyster Crassostrea virginica DDT 0.1 ppb in water for 40 days Whole body 7. 70,000 (45)

trl �

Dieldrin 1.0 ppb in water for 60 days Whole body 3.5 3,500 (45) (Jl

Shrimp Penaeus setiJerus DDT 0.0005 ppm in water for 72 hours Whole body 0.14 280 (45) 0 �

Scafed sardine Harengula pmsacolae DDT 0.0001 ppm in water for 7 days Whole bod)' 0.11 1,100 (45) White catfish Ictalurus calus DDD 0.02 ppm in water several years Edible flesh 200 10,000 (102) Rainbow trout Salmo gairdneri Toxaphene 0.41 ppb in water Whole body 7.72 18,829 ( 166) Cutthroat trout Salmo clarki DDT 0.1 ppm monthly in water baths Whole body 5. 70 51 (6) Pheasant Phasianus colchicus DDT 10 ppm in diet Adipose 29.1 2.91 (27) C attle Bas taurus Heptachlor 0.5 ppm in diet Adipose

tissue 7 . 1 14.2 (43) Milkb 0.87 1.74 (43)

Human Homo sapiens DDT 0.08 ppm in diet" Adipose tissue 12.0 150 (49 )

DDT 0.08 ppm in dieta Milk 0.37 4.63 (168)

a Estimated from data presented by Campbell et al. (49). b Converted from value given for butterfat .

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TABLE II-(Continued)

Part Species Insecticide Level of Exposure

Analyzed

PLANTS

Aquatic plants (not identified) Toxaphene 0.41 ppb ill water Foliage Cucumber Cucumeris sativus Aldrin 3.73 ppm in soil at harvest Fruit Alfalfa Medicago sativa Heptachlor 0.784 ppm in soil Plant parts

above ground

Carrot Dacus carota Heptachlor 0.19 ppm in soil Roots Potato Solanum tuberosum Heptachlor 0.19 ppm in soil Tubers Radish Raphanus saU'vus Heptachlor 0.19 ppm in soil Roots Peanut Arachis kypogaea Heptachlor 0.16 in soil at harvest Meats-hand

shelled Corn· Zea mays Heptachlor 1.0 ppm in soil Seed BarleY" Hordeum vulgare Heptacllior 1.0 ppm in soil Seed Oat" Heptachlor 1.0 ppm in soil Seed Soybean· Glycine max Heptachlor 1.0 ppm in soil Seed

• Amounts estimated from data presented in graphs.

Amount Stored

ppm

0.21 0.113

0.028 0.14 0.05 0. 03

0.67 0.005 0.007 0.02 0.11

Ratio Stora e/ Refer-

g ence Exposure

512 (166) 0.03 (118)

0.04 (118) 0.74 (118) 0.26 (118) 0.16 (118)

4.19 (33) 0.005 (42) 0.007 (42) 0 .02 (42) 0.11 (42)

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264 NEWSOM

were recognized from the time of its earliest applications for the control of mosquito larvae and resulted in thorough evaluations of the effects of aerial applications upon stream invertebrates (55, 96, 97, 106). Although many of these important fish-food organisms are highly sensitive to DDT and other chlorinated hydrocarbon insecticides, effects have been transitory in most cases because of the rapidity of re-establishment. Depending upon rates and growth of the species involved, insecticide, rate of application, immigration from other areas, formulation, and extent of area treated, effects on popula­tion of some species have been both drastic and long-lasting. The effect of aldrin applied at two pounds per acre on populations of aquatic insects in a small stream flowing through 23,000 acres of treated farmland illustrates the types of effects that may be expected (134). Both immature and adult populations of Ephemeroptera declined about 90 per cent and remained at this level for 18 months following treatment. On the other hand, populations of Trichoptera and Chironomidae more than doubled those of the controls during the first year and returned to normal during the second. The response of Trichoptera and Chironomidae populations is typical of "resurgences" observed in pest species and undoubtedly resulted from the adverse effect of aldrin on predator species.

Terrestrial insects and spider mites.-The chlorinated hydrocarbon insec­ticides were developed specifically for the control of insects and spider mites, and it is logical to expect that effects on nontarget members of these groups would be severely detrimental. Such effects occurred immediately wherever they were used extensively and were 50 drastic that they were the subject of an extensive review (150). Although a voluminous literature on the sub­ject has developed since this able treatment. of the effects of pesticides on the balance of arthropod populations, little that is new has emerged and no use­ful purpose is served in enumerating additional examples. The severe effects of these potent chemicals on natural enemies of arthropod pests demonstrate the high degree of natural control that is exerted upon them. Insecticide­induced outbreaks resulting from detrimental effects on predators and para­sites have probably done more to convince applied entomologists of the importance of natural control agents than anything else.

Two major types of pest outbreaks designated as "resurgences" and "traded pests" follow disruption of favorable equilibria of natural enemy­pest populations (29). "Resurgences" are characterized by rise to economic importance of a species which is relatively unaffected by the pesticide while its normally effective natural enemies are destroyed. Pests of this sort have become commonplace in all situations where the chlorinated hydrocarbons have been used. The Tetranychidae have probably attracted more attention in this respect throughout the world than any other group, and they illus­trate well the complexity of effects of insecticide applications on the arthro­pod fauna. Results of a survey by entomologists in Western Europe in 1953 listed Metatetranychus ulmi, Tetranychus urticae, and Bryobia praetiosa as

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PESTICIDES AND NONTARGET ORGANISMS 265

species th<j.t had become increasingly troublesome during the previous four to seven years (9). Use of pesticides resulting in the nonselective killing of natural enemies was the most generally accepted cause of the increasing importanc� of these pests, but a direct physiological effect of insecticides causing a higher reproductive rate of spider mites was also considered to be important. The adverse effects of the chlorinated hydrocarbon insecticides on natural enemies of spider mites is too well known to need further discus­sion here. Helle (91) neatly sums it up by stating, "In many situations the tetranychids were promoted from the role of a minor pest to that of a major pest as a result of the use of DDT. They have remained in this position because of resistance."

Direct effects of insecticide applications on predator and parasite popu­lations are recognized. Indirect effects, including starvation or forced emigra­tion from treated areas because of host shortage, have not been so well recognized (3). Nevertheless, these effects may be as important as direct toxicity in some cases.

The adverse effects of insecticides on nontarget arthropods have been stressed in the literature of economic entomology. Much less attention has been devoted to some other consequences of their use. Rise to the status of major pests by the Tetranychidae (143) and the red-banded leaf roller, Argyrotaenia velutinana, in apple orchards of North America as a result of the use of DDT for codling moth, Carpocapsa pomoneUa, control has received a great deal of attention. Much less attention has been paid to the fact that until about 1949, when DDT came into general use in northeastern Canada, Archips argyrospilus, which had been the most abundant leaf roller on apple,

often causing extensive damage, declined as rapidly as A. velutinana in­creased (94). Coincident with the disappearance of A. argyrospilus, popula­tions of Choristoneura rosaceana and Pandemus limitata declined precipi­tously.

Similarly, in the southern United States the cotton leafworm, Alabama argillacea, and cotton aphid, Aphis gossypii, declined to a position of negli­gible importance as a result of the use of chlorinated hydrocarbon and organophosphorus insecticides for control of the boll weevil, Anthonomus grandis, although Tetranychus spp. and Heliothis spp. have assumed in­

creased importance (138). Even the "eradication" program for Solenopsis saevissima richteri, widely

condemned for its effects on beneficial insects and various wildlife species and thus a large contributor to the increased awareness of problems connected with the use of chlorinated hydrocarbons, was not without some desirable consequences. Ticks-Amblyomma , Dermacentor, and Haemaphysalis-and the chigger, Eutrombicula aifreddugesi, were controlled for more than a year by heptachlor or dieldrin applied at the rate of two pounds per acre. The sugar cane borer, Diatraea saccharalis, and the rice stinkbug, Oebalus pugnax, developed infestations to levels previously unknown in areas treated in the

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"eradication" program, but the treatment provided excellent control of the rice water weevil, Lissorhoptrus oryzophilus, and some Tabanus and Chry­sops spp.

Examples are available to show that use of insecticides has allowed the replacement of pests by nonpests, and vice versa. Aitken & Trapido (4) report the replacement in Sardinia of the effective vector of malaria, Anopheles labrianche, by a non vector, A. hispaniola, as the resul t of insecticidal pressure of a malaria eradication program. But, in another part of the island, A. saccharovi, an effective vector of malaria recorded from Sardinia prior to 1940 but not found in a pre-eradication survey of the island in 1946, or in over 14 million inspections for larvae during 1947-1950, was present in six distinct localities of the island during 1952.

A complicated ecological change resulting from the "eradication" of A. darlingi and malaria from coastal areas of British Guiana has been reported (75). A rapid increase in human population, considerable social and economic improvement, expansion of agriculture, in.dustry, housing and industrial de­velopments, and rice cultivation took over most of the pasture land, thus displacing livestock previously abandoned around villages. Use of the horse, donkey, mule, and oxen as work animals was made obsolete by mechaniza­tion. Decrease in livestock population caused the abundant, formerly zoo­philous, A. aequesalis, to shift its attention to the human population on the Demerara River estuary, where malaria transmission had been interrupted

in 1947 and A. darlingi "eradication" maintained since, and was responsible for a sharp outbreak of Plasmodium viva�: malaria.

There is no reason to assume that the effects of insecticides should be any different on beneficial species than 011 pest species since the term "pest" is a human concept and has no biological validity. It seems entirely probable that the phenomena of "resurgences" and "traded pests" may apply as well to "beneficial" or "neutral" species. Indeed, this has been reported for Coccinellidae following treatment of potatoes with DDT (159) and in "over­recovery" of several species of predators following a boll weevil control program (100).

Effect of sublethal exposure to chlorinated hydrocarbon insecticides on repro­ductive potential.-The effects of chlorinated hydrocarbon insecticides on the physiology of insects resulting in greater or less fitness in populations are of great theoretical and practical interest (2, 22, 32, 101, 109, 111, 120, 155). Stimulation of egg production in the Tetranychid?e from exposure to DDT (101, 120, 155) could have a tremendous influence upon the reproductive potential of a species. However, these results could not be repeated (26, 145, 147). On the contrary, slight decreases in longevity and fecundity of spider mites exposed to DDT were usually observed. The lack of agreement be­tween European and North American workers on this subject remains un­explained. Exposure of the pink bollworm, Pectinophora gossypiella, to sub­

lethal doses of DDT shortened life span, reduced thc number of females that

mated, and caused significant reductions in the number of eggs produced (2).

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PESTICIDES AND NONTARGET ORGANISMS 267

Untreated females mated to treated males produced significantly more eggs than when they were mated to an untreated male. These results were similar to those obtained for Callosobruchus chinensis (109).

Although the preponderance of data available suggests that the effects of exposure to sublethal doses of insecticides are most often detrimental, little attention has been given to the possibility of exposure to insecticides affect­ing reproductive potential of beneficial species. Atallah & Newsom (24) reported such effects as decrease in longevity, prevention of oviposition, and reduction in survival of Fl progeny of adult ColeomegiUa maculata from expo­sure to sublethal doses. Beard's work (32) with the house fiy, Musca domes­tica, showing that suppression of egg laying involved the inhibition of ovarian development suggestive of a biochemical lesion, provides further evidence that exposure to sublethal doses of insecticides may have far more significant physiological and biochemical effects on insects than has been suspected.

Insect,i,cide resistance.-The development of resistance in pests of impor­tance to agriculture and public health (39, 40) suggests that resistance oc­curs also in insects other than pest species. Surely, it must be widespread among beneficial species as well. It would be incredible if only those species that man has labeled "pests" should prove to have the genetic plasticity for resisting such powerful selective agents as the broad spectrum chlorinated hydrocarbon insecticides. Yet, among beneficial species, few examples are known (2:3, 24, 25, 77). Undoubtedly, research would show insecticide resis­tance to be common in populations of predators, parasites, pollinators, scavengers, and species of importance in food chains.

Insecticide storage in insects.-The importance of insecticide residues in insects is another area which seems to have been neglected, especially in view of the importance of some species in food chains. The storage of one or more chlorinated hydrocarbon insecticides in amounts as high as 1.17 ppm in pupae of Heliothis zea, 12.88 in adults of Harpalus pennsylvanicus, 2.58 in adults of Thermonectes basilaris, 1.07 in adults of Hexagenia sp., 90. 1 1 in ColeomegiUa maculata adults, and 24.64 in eggs of this species (Table III), have been reported (23, 65). The presence of an insecticide so highly toxic to fishes and birds as endrin in an important component of their food chains is of special interest. Fishes, birds, and other animals whose diets contain a

high percentage of insects storing endrin in their tissues at levels as high as 0.46 ppm would be exposed to considerable hazard.

Estuarj:ne organisms.-Concern has increased during the last five years over the possibilities that shallow coastal waters, enormously rich in number and diversity of animal life, may be contaminated by insecticides to the extent of damaging populations of some of the more sensitive species. Many of the Crustacea are as susceptible to insecticides as are fish (Table I) (47, 136, 158) . The use of insecticides on tidal marshes for control of mosquitoes plus the contributions of insecticides from streams empyting into estuaries give cause for concern. The possibility of adverse effects of insecticides on the shrimp populations in coastal areas at the mouth of the Mississippi and

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TABLE III

RESIDUES OF INSECTICIDES IN INSECTS COLLECTED ALIVE FROM;

VARIOUS LOCALITIES IN LOUISIANA, U.S.A.

Species Pesticide ppm Reference

Coleomegilla maculata Adults DDE 90.1 (23) Eggs DDE 24.6 (23)

Heliothis zea Adults DDE 1.02 (65) Pupae DDE 1.17 (65)

H. virescens Adults DDE 0.38 (65) Trichoplusia ni Adults DDE 2.85 (65)

Adults Toxaphene Trace (65) Calosoma alternous Adults DDE 2.93 (65)

Adults DDT 4.34 (65) Harpalus pennsylvanicus Adults DDE 5.25 (65)

Adults DDT 0.10 (65) Agonoderus lecontei Adults DDT 9.16 (65) Tropisternus lateralis Adults DDE 0.12 (65)

Adults DDT 1.69 (65) Hydrapkilus triangularis Adults DDE 0.22 (65)

Adults DDT 1.32 (65) Thermonectes basuaris Adults DDE 2.58 (65) Hexagenia spp. Adults DDE 0.38 (65)

Adults Dieldrin 0.21 (65) Adults Endrin 0.46 (65) Adults Heptachlor epoxide 0.02 (65)

Atchafalaya Rivers has been suggested (78). The extreme sensitivity to chlorinated hydrocarbon insecticides of the shrimp species, Penaeus duora­rum, and P. setiferus, is sllch that populations of these animals should be among the first to show the effects of insecticides in estuarine environments. That these pesticides are present in estuarine waters is demonstrated by a report (46) that one sample of fresh shrimp and five samples of processed shrimp from the area analyzed during 1964 contained DDT at 0.02 to 0.07 ppm plus traces of BHC and heptachlor epoxide. However, populations of shrimp that develop in areas adjacent to the mouth of the Mississippi river have not been adversely affected by pesticides in their environment thus far. Record yields were obtained in 1963 and approached during 1965 (16).

VERTEBRATES

FISH

Effects of exposure to acutely toxic concentmtions.-The chlorinated hydro­carbon insecticides are almost unbelievably toxic to fish (Table I) . Acute effects were so obvious and so drastic that it was apparent from the beginning

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PESTICIDES AND NONTARGET ORGANISMS 269

of their use that these chemicals could not be used indiscriminately in agricul­ture or public health operations. Exposure to acutely toxic dosage rates has resulted in huge mortalities to various species of fish (20, 44, 66, 153).

Acute toxicity measurements are available for most of the commonly used insecticides for a few species, but the influence of environmental varia­tions on toxicity is so great that effects in nature are difficult to predict. Physical effects may range from passage downstream to a new area, dilution, absorption on surfaces, to co-distillation with water. Water chemistry, e.g., pH and salinity, may affect toxicity. Insecticides may be trapped on the surface of microorganisms or aquatic plants with or without degradation of the chemical. Microorganisms, higher animals, and aquatic plants may ac­cumulate pesticides with or without degradation of the chemicals, and with or without excretion of the original pesticide or of its metabolities. Circum­stantial evidence exists that most, if not all, of these factors are operative in nature, but little experimental verification is available from controlled studies.

Effects of exposure to subacutely toxic concentrations.-Interest in the re­sponse of fish to subacute exposure to insecticides has increased during the past five years under the stimulus of work showing that these animals have a tremendous capacity for concentrating insecticides when exposed to minute amounts Crable II) (6,44, 102, 166). Technological developments permitting the measurement of almost infinitesimally small residues have also stimu­lated interest .

The significance of pesticide residues in fish is not well understood. One of the most puzzling features is that exposure to levels as much as one half an acutely toxic dose can apparently be tolerated indefinitely (Table IV), and tremendous residues stored (6, 166).

Allison et al. (6) demonstrated that the cutthroat trout, Salmo clarki,

exposed to DDT in the diet or in water baths, concentrates and stores the chemical at approximately similar levels for both routes of exposure. Thus, it is not necessary to postulate magnification of the insecticide through food chains to explain concentrations in fish. Metabolic conversion of DDT to DDE occurred and was higher in fish exposed to low dosages. Lots exposed monthly to 1 ppm in water baths contained 48 to 76, 20 to 45, and 2 to 9 mean percentages of DDT, DDE, and DDD, respectively, compared with 12 to 44, 46 to 80, and 3 to 16 for lots exposed to 0.03 ppm. Dosage rates of DDT at 0.3 mg/kg per week in feed and 0.1 ppm monthly by contact appear to be near the threshold for acute effects in this species. At the latter rate, it accumulated about 6 ppm (Table II) . Surviving fish in high-dosage lots were significantly larger and exhibited about 50 per cent less disease incidence than survivors in the control and low-dosage treatments. The investigators explained these results on the basis of selective death of smaller and weaker fish with less growth potential in the high-dosage treatments, but call atten­tion to the possibility that the difference in incidence of disease between high- and low-dosage lots could have resulted in better growth of the former.

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TABLE IV

RESPONSE OF SOME AQUA1'lC ANIMAL�; TO ACUTE AND CHRONIC EXPOSURES TO INSECTICIDES

Species

Shrimp Penaeus sP.

Blue crab eallineeles sapidus

Oyster Crassas/rea

vi.rginica

Spot Leioslomus xanthurus xan/hurus

Rainbow trout, Sa/ma gairdneri

Atlantic salmon Salmo salar

Acute toxicity levels to specified insecticide

LCIO-24 hr 0.6 ppb-endrin

LClOo-8�days 1.0 ppb-DDT

EC..--96 hrs 0.009 ppm-DDT

LClOO-5 days 0.1 ppb­

endrin

LClOO-14 days 1 ppb­toxaphene

LClOo-14 days 1 ppb­toxaphene

Response to chronic exposure

Survived 2 mos at 0.025 ppb and stored 5.0 ppb

Survived 4 mos at 0.5 ppb and stored 5.36 ppm

No effect on growth at 0.1 ppb Concentrated DDT about 70,000 times the amount re­quired for EClO.

Survived 12 days at 1.0 ppb DDT and stored 14-20 ppm DDT In eggs and sperm.

Survived S mos at 0.05 ppb

with no effects Survived 280 days at 0.4 to

0.66 ppb. no effect on

growth. stored 13.7 ppm. Survived 255 days at 0.4 to

0.66 ppb. uo effect on growth, stored 5.50 ppm

Reference

(46)

(46)

(46)

(46)

(166)

(166)

DDT, at levels administered in their experiment, did not affect the rate of sexual development or gamete production of the adults. Fertilized eggs from treated adults developed as quickly as those from the controls, and survival was somewhat better. However, during a short period after hatch­ing, mortality was noticeably higher in offspring of the high-dosage than in low-dosage or control lots. Excessive mortality in all treated lots during this critical period may be explained by absorption of yolk material containing high residues of DDT and its metabolites. The amount of these materials passing into eggs averaged about one half the steady-state concentration in whole-body samples. Eggs having the highest residues had the highest mor­talities during periods of yolk-sac absorption. When the fry were old enough to accept food, the mortalities were about the same in alI treated lots. This effect was similar to that reported by Burdick et al. (44) for lake trout, Salvelinus namaycush.

Effects oj insecticides on populations.-·-Clear Lake, California, furnishes the best known example of concentration of insecticide in food chains. Fish in this lake have been exposed to DDD at about 0.02 ppm from applications made during 1949, 1954, and 1957 for the control of Chaoborus astictopus. White catfish, Ictalurus calus, sampled in 1958, contained residues ranging from 1700 to 2375 ppm in visceral fat, to 22 to 221 ppm in edible flesh (Table II). As yet, no data have been presented that suggest any adverse effects on fish populations have occurred.

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PESTICIDES AND NONTARGET ORGANISMS 271

Burdick et al. (44), on the other hand, reported that D DT applied to forests and campsites on watersheds of a number of lakes in New York had resulted in the virtual elimination of lake trout, S. namaycush, production.

The effects of insecticide use on populations of Atlantic salmon, Salmo salar, have been evaluated critically (66). DDT was used at 0.5 to 1 pound per acre for the control of a severe spruce budworm, Choristoneura fumiferana, epidemic in New Brunswick, Canada, during 1952-1957. Areas ranging from about 20,000 acres in 1952 to more than 25 per cent of the land area, covering nearly all of the salmon streams in the northern part of the province, were treated during 1957.

Data available on these populations prior to treatment allowed effects of the treatment to be determined with reasonable accuracy. Age classes were affected differentially with severity inversely related to age (107) . The num­bers of returning salmon declined during 1961-62 to about one sixth of the original numbers, but recovery of the population has been unexpectedly rapid. Elson & KerswiII (66) state,

... with no spraying in subsequent years, populations of young salmon recovered rapidly, being apparently dependent for the most part on the presence of sufficient parent stocks. Despite some more prolonged adverse changes in the stream insect fauna upon which young salmon feed, those that are hatched the year after spray­

ing find enough to eat that many can survive even though growth may be slowed a little.

They reported the catch of grilse during 1963 to be one of the highest ever recorded.

Mortality in a population of fish exposed to acutely toxic dosages of an insecticide may be virtually complete, but rates of reproduction are so high for most species that repopulation may occur rapidly. This is especially true in the case of species with comparatively short and simple life cycles.

Resistance to insecticides.-Ferguson and his associates (69, 70) reported that several species of fish have developed high levels of resistance to the chlorinated hydrocarbon insecticides. Populations involved were taken from the Missi:5sippi River and smaller streams that drain the cotton-producing areas subjected annually since 1946 to perhaps the heaviest applications of insecticides of any area of the world. Resistance 100-fold of the normal was established in populations of mosquito fish, Gambusia affinis; black bullhead, Ictalurus melas; yellow bullhead, Ictalurus natalis; golden shiners, Notemi­gonus crysoleucas; bluegill sunfish, Lepomis macrochirus; and green sunfish, L. cyanellus. These studies furnish evidence that residues of chlorinated hydrocarbon insecticides at levels high enough to exert selective pressure upon fish populations have existed in streams of the area for several years. The pattern of resistance resembles closely that in insects, including cross­tolerance and lack of resistance in populations from areas in which insecti­cides have either been used little or not at all.

The possibility of resistant forms being able to store much higher levels

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27 2 NEWSOM

of residues than susceptible forms calls attention to the rather grim prospect of even greater hazards in food chains. Little seems to be known about this possibility, and no reference to it having been studied was seen in the litera­ture reviewed. Ferguson (personal correspondence) recently reported that Gambusia from the Mississippi Delta can survive a two-week exposure to 500 ppb of endrin and to concentrate it to 214 ppm. Predators feeding on fish containing this amount of such a toxic chemical as endrin would be exposed to considerable hazard.

BIRDS

Effects oj exposure to acutely toxic concentrations.-The effects of insec­ticides on bird populations have received a great deal of attention, but rela­tively few sound data are available from which to draw conclusions. The status of the problem has been reviewed during the last decade (131 , 153) . I t has been claimed that poisoning of birds is increasing because of greater use of the broad spectrum insecticides, increasing use of seed-treatment prac­tices, and accumulation of toxic residues in foods of birds ( 152) . Exposure to acutely toxic levels, for example, rice seed treated with D DT at 20,000 ppm, or where large areas have been treated with heptachlor or dieldrin applied at the rate of two pounds per acre for control of the imported fire ant, Solenopsis saevissima richteri, or the J apanese beetie, PopiUia japonica, has often resulted in immediately obvious and extreme effects (60, 152, 157) . Mortality o f substantial proportions of exposed populations has occurred in many species exposed to such heavy rates of application. In resident spe­cies such as bobwhite quail, Colinus vil'ginianus, measurable effects may persist for several months; but it is generally difficult or impossible to show that use of insecticides has been responsible for changes in bird populations other than of a very transitory nature.

Effects oj exposure to subacutely toxic concentrations.-Appreciable levels of insecticide residues occur in the tissues of birds and their eggs (7, 34, 61 , 65, 90, 93, 103, 108, 121 , 131 , 133, 149, 161) (Table V) , b u t their significance is not understood. M uch effort has been devoted to establishing levels of residues in tissues, counting populations, and speculating about possible adverse effects of pesticide use on birds (7, 74, 121 , 132, 133, 149, 152, 1 65), but few studies with sound ecological bases have been made. Feeding studies usually have been made with diets approaching acute toxicity levels. Such studies with D DT have been made with pheasant, Phasianus colchicus (27, 73, 74), bobwhite quail, Colinus virginianus (61) , house sparrow, Passer domesticus (34) ; and brown-headed cowbird, Molothrus ater ( 163) . All of these species tolerated dosage levels up to 300 ppm in their diets and often gained weight, in some cases (74) outgaining the controls. Levels of DDT stored in tissues of birds fed such diets have been proportional to amounts in the diet. Although considerably more toxic than D DT, toxaphene and dieldrin pro­duce similar effects (74) .

Insecticides fed at high levels have had little or no effect on egg production

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PESTICIDES AND NONTARGET ORGANISMS 2 7 3

o r fertility, but often chick viability has been reduced significantly. Azevedo et aI. (27) , in their evaluation of the effects of DDT at 10, 100, and 500 ppm upon reproductive success in the pheasant, found that none of the concentra­tions affected egg production or fertility. Overall hatching success ranged from 73 to 81 per cent for treated animals and was 77 per cent for the con­trols. Chick mortality was significantly higher in the 500 ppm group than in the two lower groups and the control. The survival rate of chicks was most critical during the first few weeks after hatching. This is remarkably similar to effects reported for fish (6, 44) and suggests the interesting possibility that mechanisms of insecticide transfer from egg yolk may be similar in birds and fish. The difference in survival rate between the SOO-ppm rate and all other levels was highly significant, but it amounted to no more than S per cent. Based on the number of chicks per 100 eggs surviving at the end of six weeks, the number from the 500-ppm group would be reduced from 67 to 64. Such effects as these would be relatively minor when considered on a population basis, since the natural mortality of a stable pheasant population has been estimated to be about 73 per cent annually ( 127) .

Effects of insecticides on populations.-Residues in body tissues and eggs of wild birds (Table V) indicate that populations of many species have been exposed to hazardous concentrations of chlorinated hydrocarbon insecticides in their diets. Severe mortalities have been reported in local populations of the western grebe, Aechmophorus occidentalis ( 102) ; and the robin, Turdus migratorius (99) , from insecticide concentrations in food chains.

Fears have been expressed that populations of the woodcock, Philohela minor, would suffer catastrophic effects from exposure to DDT and hepta­chlor, both of which are concentrated by earthworms (58) , when these insec­ticides are applied over large areas of its summer breeding range and winter­ing grounds, respectively (152, 175). Like the robin, a substantial portion of the woodcock's diet is composed of earthworms. Woodcock that we�e fed on earthworms contaminated at an average of 2.86 ppm of heptachlor epox­ide suffered heavy mortality within 35 days, but at 0.65 ppm they survived the full 60 days of feeding experiments (162) . Breeding success of woodcock during 1958 in northern New Brunswick, where several applications of DDT had been made since 1954 for control of spruce budworm, was estimated to have been reduced by more than half when compared to untreated areas ( 175) . However, similar estimates based on a much l arger sample extending over a four-year period (129) showed no decline in reproductive success over the range as a whole from 1959 through 1962. Populations of this game spe­cies, in spite of being subjected to the hazard of highly contaminated food sources throughout its range, have fared so well that hunting seasons and bag limits have been increased since 1963 (20) .

No experimental evidence is available to support a conclusion that the continued existence of any species has been endangered by the use of insec­ticides. However, much circumstantial evidence is available to indicate that popUlations of some of the birds of prey-the golden eagle, Aquila chrysaetos;

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TABLE V

EXAMPLES OF CHLORINATED HYDROCARBON INSECTICIDE RESIDUES IN WILD MAMMALS AND BIRDS

Tissue Residues, ppm

Species Analyzed

Insecticide Found

Range Mean

Bear Ursus americana Adipose DDT+DDE + D D D 0 . 0 1- 0 . 34 0 . 06 Deer Odocoileus spp. Adipose DDT+DDE + D D D 0 . 01- 3 . 04 0 . 13 Elk Cervus canadensis Adipose DDT+ DDE + DDD 0 . 01- 0 . 58 0 . 09 Goat Oreamnos americanus Adipose DDT+DDE + D DD 0 . 01- 0 . 09 0 . 02 Antelope Antilocapra americana Adipose DDT+DDE + D D D 0 . 01- 0 . 2 1 0 . 10 Moose Alces alces Adipose DDT+DDE +D D D 0 .01- 0 . 1 7 0 . 10 Bald eagle Haliaeetus leucocephalus Muscle DDT+DDE + D D D 0 . 02- 68 . 1 9 . 4

Eggs DDT+DDE + D D D 1 . 1 - 36 . 9 15 . 9 Golden eagle Aquua chrysaetos Eggs Dieldrin+ DDE 0 .25- 10 .29 2 . 48 Osprey Pandion haliaetus Eggs DDT+DDE + D D D 3 5 . 0 - 100 .0 Canada goose Branta canadensis Muscle DDT +DDE + D D D 0 . 30- 3 . 90 1 . 85

Eggs DDT +DDE + D D D 0 . 4 - 1 . 0 Scaup Aythya marila Eggs DDT+DDE + D D D 1 .3 - 4 . 0 2 . 2 Pheasant Phasianus colchicus Adipose DDT+DDE + D D D 0 .0 -2 , 930 . 0 741 . 0

Dieldrin 0 .0 - 2 5 . 0 Eggs DDT+DDE +DDD 0 . 8 -1 , 020 . 0

Dieldrin 0 . 0 - 9 . 6

Reference

( 167) (167) ( 1 6 7 ) ( 167) ( 1 67 ) (167) ( 161 )

( 6 1 ) ( 1 2 1 )

( 7 ) (90)

( 156) ( 156) ( 103) ( 103) ( 1 03 ) ( 103)

N -l >I'-

Z tTl =;S Ul 0 �

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TA BLE V-(Conlinued)

Species

Woodcock Philohela minor

King rail RalJus elegans

Cormorant Phalacrocorax carbo

Herring gull Larus argentatus

Red breasted merganser Jiergus serrator Grebe Podiceps cristatus

Raven Corvus corax Magpie Pica pica Blackbird Turdus ericetorum Robin Turdus migratoriusb

Red-winged blackbird Agelaius phoeniceus

House sparrow Passer domesticus Ruby throated humming bird

Archilochus colubris

Tissue Analyzed

Whole carcass Whole carcass

Eggs Eggs Eggs Adipose Eggs Liver Eggs Eggs Eggs Eggs Brain

\\'hole carcass Whole carcass

Whole carcass

• DDT, ODE, dieldrin, heptachlor, and BHC isomers.

Insecticide Found

Heptachlor epoxide DDT Heptachlor epoxide DDT DDT+DDE+DDD DDE +Dieldrin DDT+DDE +D D D

D DT+DDE+DDD chlorinated hydrocarbon" chlorinated hydrocarbon" chlorinated hydrocarbon" DDE DDT+DDE+DDD

DDT D DT

DDT

Residues. ppm

Range Mean

Trace- 31 . 1 Trace- 1 7 . 9 Trace- 0 . 8 0 . 4

0 .4 - 0 . 9 1 . 6 0 . 7

1 . 8 - 2 . 6 2 , 441 . 0

227 .0 3 . 9 1 7 . 2 1 1 . 6 2 . 6 - 22 . 7 0 . 8 - 5 . 1 2 . 1 0 . 1 - 0 . 6 0 . 4

13 .5 - 122 . 2 1 7 . 0 - 1 88 . 0 64 . 0

5 . 15 35 .31

0 . 34

b Average of 35 tremoring specimens collected in areas treated for Dutch elm disease control.

Reference '1l tTl (fJ o-l

( 16 1 ) .....

('j (161) ......

C1 ( 16 1 ) tTl ( 16 1 )

(fJ

> ( 156) Z ( 132) C1

(93) Z (93) 0

Z ( 161)

� ( 133) � ( 149)

( 149) tTl o-l

( 165) 0 ( 1 63) �

� (65) Z

U; (65) a;: (fJ

(65)

N -:r <:.n

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the bald eagle, Haliaeetus leucocephalus; and the osprey, Pandion haliaetus-­may be endangered in some areas of their distribution from exposure to high concentrations of chlorinated hydrocarbon insecticides in their diets. Moore (131) concluded that populations of some of the raptorial species of the British Isles appeared to be in jeopardy from exposure to insecticides, but pointed out the importance of factors associated with increased urbanization in the decline of such species.

WILD MAMMALS, DOMESTIC ANIMALS, AND HUMANS

Wild mammals.-Little additional information has developed in this area since Rudd's ( 1 5 1) recent review. The most important development has been establishing that low levels of residues exist in tissues of many species (167).

Domestic animals.-Livestock do not contact insecticides in amounts enough to cause intoxication, except in an occasional accident. Like other animals, they are exposed to sublethal doses and accumulate detectable quantities of insecticides in their tissues. They provide some of the best evi­dence that exposure to these low levels of i nsecticide residues has no adverse effect on growth or reproduction. Any such effects would be readily apparent from records kept on milk, meat, and egg production.

The role played by livestock in the transfer of chemical residues to the human is one for concern, because it is in such products as meat, milk, and eggs that most of the insecticides in the human diet are found (49) . Concen­tration of chlorinated hydrocarbon insecticides in meat and milk of domestic animals can result from exposure to incredibly small amounts of insecticide. The accumulation of dieldrin and heptachlor epoxide to levels of about 1 1 ppm i n adipose tissue and 1 3 ppm i n butterfat (about 0.5 ppm i n milk) has been reported in cattle exposed to rangeland treated at two ounces per acre ( 1 1 ) . Hardee et al . (82) reported concentration of heptachlor epoxide in the milk of cows fed hay contaminated with as little as 5 ppb. Bruce et al. (43) call attention to the significant fact that the lower the concentration in the

diet the higher the percentage of intake stored.

HUMANS

Effects of insecticides on health.-Much research has been accomplished and more experience has been gained during the five years since Hayes' (85) review was published, but little has been learned that would make it neces­sary to change the substance of one of his concluding statements :

However, there is nothing to be gained in the long run by irresponsible statements that nothing now is known of the toxicology of the newer pesticides, or that no legal control of their use exists, or-in the absence of epidemiologic proof-that a wide variety of illnesses from which mankind has suffered for generations is now caused by intoxication by the newer economic poisons.

Similar views have been expressed in a number of reviews concerned with public health aspects of exposure to insecticides published during the last five years (49, 56, 62, 87, 88, 99) .

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The biological significance of long-term human exposure to insecticides in the environment is understood little, if any better than it was 10 years ago. Indeed, the conviction is growing that the delayed effects of long-term exposure may never be known (18, 141, 1 68) . The difficulties of species to species extrapolation are such that questions relating to toxicity and hazard must be found in human experience, epidemiologic studies, or by controlled studies in man (18, 141) . Even if controlled studies in man were possible, lack of suitable unexposed control groups would present a serious problem.

Human experience of exposure to residues of DDT for almost a genera­tion indicates no hazard at the concentrations involved. It is reassuring that the chlorinated hydrocarbon insecticides apparently conform to the general principle of pharmacology that a steady-state of storage is reached with tolerated intake of a chemical (88). At tolerated dosages, man approaches storage equilibrium of DDT in about one year (49, 88) . Apparently DDT storage in the population of the United States reached a "plateau" at about 12 ppm by 195 1 , or earlier (56, 62, 85, 87, 88, 89 99, 1 14), and has not changed SInce.

Insufficient data are available to establish storage "plateaus" for BHC, dieldrin, and heptachlor epoxide that have also been reported in human pop­ulations. Hunter et al. ( 105) have suggested that each of several pesticide residues in a mixture independently attains a concentration which is in equilibrium with its respective intake and excretio"n rate. This was found to be true for milk ( 174), for which it was reported that heptachlor was stored at the highest levels followed by dieldrin, endrin, and at appreciably lower amounts, DDT.

Effects on attitudes.-West's (168) statement that "Public health pesticide problems are noted for their technical complexity, scientific controversy, and public confusion" applies equally well to all other aspects of the effects of insecticides on nontarget organisms. Wigglesworth expressed concern over the possible effects of DDT on the "balance of nature" as early as 1945 (172) . From that time controversy on the subject has gained intensity.

Publication of Silent Spring (50) crystallized the necessity for critical ex­amination of some of the problems arising from the use of pesticides. A panel of the President's Science Advisory Committee was convened to examine the overall aspects of the problem, and its report ( 13) has had far-reaching and significant effects upon the vast and complicated field of environmental pollution. The report was remarkably similar in many ways to its British counterparts ( 10, 1 2) and was followed by others from the United Kingdom ( 14, 15) . The findings of these study groups may be summarized as follows : (a) There is no evidence of serious immediate hazard arising from the use of chlorinated hydrocarbon pesticides; (b) there is no evidence to support charges that they are serious liver poisons; (c) levels of the more toxic insec­ticides found in food are undesirable ; (d) there is circumstantial evidence for the view that the decline of certain predatory birds in both countries is re­lated to the residues found in such species arising from the use of aldrin, dieldrin, heptachlor, and DDT; and (e) widespread environmental contami-

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nation by the "long persistent" pesticides is cause for concern and justifies some restrictions on their use.

Under the stimulus provided by the /"ecommendations of the various committees appointed to study the consequences of use of pesticides, concern over environmental pollution in general crystallized to a degree never before known (17, 21) .

CONCLUSIONS

General contamination of ecosystems with measurable amounts of chlo­

rinated hydrocarbon insecticide residues has occurred during the last two decades. Since "pest" and "beneficial" are terms that have no biological validity, it is not surprising that both target and nontarget organisms have been affected and have responded in similar ways. Phenomena such as sus­ceptibility, refractoriness, resistance, "resurgence, " species displacement, specificity of response, and concentration of residues are known among both. It is unrealistic to assume that "desirable" species will be eliminated while "pest" species will become more difficult to control (53, 54, 152).

The potential effects of these biologically active chemicals on man and other organisms is poorly understood, or not at all, in many cases. Evidence available furnishes cause for both pessimism and optimism over their use. Aside from their benefits to mankind in effecting control of pest species to a

degree never before known, three consequences of their use are likely to result

in more good to mankind than all of their adverse effects combined. They

are : (a) Stimulating the development of concepts of pest control that trans­cend the parochial interests of entomologists, wildlife specialists, public health workers, and conservationists; (b) <:onvincing applied biologists of the necessity for developing pest control tec hniques based on ecological prin­ciples (51, 72, 83, 144, 160) ; and (c) arousing scientists and the public to an

awareness of the overall problems of environmental pollution.

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LI TERATURE CITED

1. Acree, F., Jr., Bcroza, M., and Bow­man, M. C. Codistillation of DDT with water. J. Agr. Food Chem., 1 1, 278 (1963)

2. Adkisson, P. L., and Wellso, S. G. Effect of DDT poisoning on the longevity and fecundity of the pink bollworm. J. Eeon. Enlomol., 55, 842-45 (1962)

3. Ahmed, M. K., Newsom, L. D., Emerson, R. B., and Roussel, J. S. The effect of systox on some com­mon predators of the cotton aphid. J. Ecan. Entornol., 47, 445-49 (1954)

4. Aitken, T. H. G., and Trapldo, H. Replacement phenomenon observed amongst Sardinian anopheline mos­quitoes. In Ecological effects of biological and chemical control of undesirable plants and animals. Intern. Union Conserv. Nature Nat. Resources, Tech. Meeting, 8th, War­saw, 1960, 106-14 (1960)

5. Akesson, N. B., and Yates, W. E. Problems relating to application of agricultural chemicals and result­ing drift residues. Ann. Rev. Ento­mol., 9, 285-318 (1964)

6. Allison, D., Kallman, B. J., Cope, O. B., and Valin, C. V. Some chronic effects of DDT on cut­throat trout. U. S. Fish Wildlife Serv., Res. Rept., 64, 30 pp. (1964)

7. Ames, P. L., and Mersereau, G. S. Some factors in the decline of the osprey in Connecticut. Auk. 81, 173-85 (1964)

8. Anderson, B. G. The toxicity of or­ganic insecticides to Daphnia. In Biological problems in water pollu­tion. Trans. Seminar Bioi. Probl. Water Pollution, 2nd, 1959, 94-95 (1960)

9. Anonymous. European Plant Protec­tion Organization. Red spiders in Western Europe. Plant Protect. Bull. FA O, 2, 71-74 (1954)

10. Anonymous. Toxic chemicals in agri­culture (risks to wildlife). SO Code No. 24-190-2 (H. M. Stationery Office, London, 1955)

11. Anonymous. Residues in fatty tissues, brain, and milk of cattle from insec­ticides applied for grasshopper con­trol on range land. J. Eeon. Ento­mol., 52, 1206-10 (1959)

12. Anonymous. Toxic chemicals in agri-

culture and food storage. Report of research study group appointed by Minister of Agriculture, Fisheries and Food, Minister of Health, Min­ister for Science and Secretary of State for Scotland. (H. M. Sta­tionery Office, London, 1961)

13. Anonymous. Use of Pesticides. Report of the President's Science Advisory Committee. (U. S. Govt. Printing Office, Washington, D. C., 25 pp., 1963)

14. Anonymous. Review of the persisteut organochlorine pesticides. (supple­mentary report) . SO Code No. 24-314-2 (H. M. Stationery Office, London, 1964)

15. Anonymous. Review of the persistent organochlorine pesticides (supple­mentary report) . SO Code No. 24-314-2 (H. M. Stationery Office, London, 1964)

16. Anonymous. U. S. Fish Wildlife S�rll. , La. Landings, Ann. Summaries, 1959-1965 (1965)

1 7. Anonymous. Restoring the quality of our environment. Report of the Environmental Pollution Panel President's Science Advisory Com­mittee. (The White House, Novem­ber, 1965)

18. Anonymous. Some considerations in the use of human subjects in safety evaluation of pesticides and food chemicals. Nail. A cad. Sci. Natl. Res. Council, Publ., No. 1270, 22 pp. (1965)

19. Anonymous. Suggested guide for the use of insecticides to control insects affecting crops, livestock and house­holds, 1965. U.S. Dept. A gr., A gr. Handbook, No. 290, Rev. (1965)

20. Anonymous. U.S. Fish Wildlife Serv., Migratory Bird Regulations (1962-63, 1963-64, 1964-65, 1965-66)

21. Anonymous. Waste management and control. A report by the Committee on Pollution. Nail. Aead. Sci. Nail. Res. Council Publ., No. 1400, 257 PP. (1966)

22. Asquith, D. Insecticides change the importance of segments of insect generations. J. Eeon. Entomol.. 53, 694-95 (1960)

23. Atallah, Y. H., and Nettles, W. C. DDT-metabolism and excretion in Coleomegilla maculata De Geer. J. Eean. Entomol. (In press, 1966)

Ann

u. R

ev. E

ntom

ol. 1

967.

12:2

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86. D

ownl

oade

d fr

om w

ww

.ann

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ws.

org

by U

nive

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ade

Fede

ral d

o A

maz

onas

on

04/2

4/14

. For

per

sona

l use

onl

y.

280 NEWSOM

24. Atallah, V. H., and Newsom, L. D. Ecological and nutritional studies on Coieomegilla maeulata De Geer. III. The effect of DDT, toxaphene and endrin on the reproductive and survival potentials. J. Eeon. Ento­mol. (In press, 1966)

25. Atkins, E. J., Jr., and Anderson, L. D. DDT resistance in honey bees. J. Eeon. Entomol., 55, 791-92 (1962)

26. Attiah, H. H., and Boudreaux, H. B. Influence of DDT on egg-laying in the spider mites. J. Eeon. Entomol., 57, 50-53 (1964)

27. Azevedo, J. A., Jr., Hunt, E. G., anti Woods, L. A., Jr. Physiological ef­fects of DDT on pheasants. Calif. Fish Game, 51, 276-93 (1965)

28. Baker, R. J. Notes on some ecological effects of DDT sprayed on elms. J. Wildlife Management, 22, 269-74 (1958)

29. Bartlett, B. R. Integration of chemical and biological control. In Biological Control of Pests and Weeds, 489-5 1 1 . (DeBach, P., Ed., Reinhold Pub!. Co., New York, 844 pp., 1964)

30. Bauer, K. Studien fiber Nebenwirk­ungen von Pflanzenschutzmitteln auf Fische und Fischnahrtiere. Mitt. Biol. Bundesanstalt Land­Forst,virtseh., Berlin-Dahlem, 105, 72 pp. (1961)

31. Bauer, K. Studien fiber Nebenwirk­ungen von Pflanzenschutzmitteln auf die Bodenfauna. Mitt. Biol. Bundesanstalt Land-Forstwirtseh., Berlin-Dahlem, 1 12, 42 pp. (1964)

32. Beard, R. Ovarian suppression by DDT and resistance in the house fly (Musca domestiea L.). Entomol. Exptl. Appl., 8, 193-204 (1965)

33. Beck, E. W., Dawsey, L. H., Wood­ham, D. W., Leuck, D. B., and Morgan, L. W. Insecticide residues on peanuts grown in soil treated with granular aldrin and hepta­chlor. J. Eeon. Entomol., 55, 953-56 (1962)

34. Bernard, R. F. Studies on the effects of DDT on birds. Mich. State Univ. Museum Publ. BiOi., 2, 155-92 (1963)

35. Bernard, R. F., and Gaertner, R. A. Some effects of DDT on reproduc­tion in mice. J. Mammal., 45, 272-76 (1964)

36. Bigger, J. H., and Decker, G. C. Con­trolling root-feeding insects of

corn. Illinois Univ. Agr. Expt. Sta., Bull., 716, 24 pp. (1966)

37. Boyd, C. E., and Ferguson, D. E. Spectrum of cross resistance to in­secticides in the mosquito fish Gambusia affinis. Mosquito News, 24, 19-2 1 (1964)

38. Boyd, C. E., Vinson, S. B., and Fer­guson, D. E. Possible DDT resis­tance in two species of frogs. Copeia, 2, 426-29 (1963)

39. Brown, A. W. A. The spread of insec­ticide resistance in pest species. A dvan. Pest Control Res., 2, 351-414 (1958)

40. Brown, A. W. A. Insecticides and hu­man health. World Rev. Pest Con­trol, 1, 6-17 (1962)

41 . Brown, W. A., Witt, J. M., Whiting, F. M., and Stull, J. W. Secretion of DDT in milk by fresh cows. Bull. Environ. Contamination Toxi­col., 1, 21-28 (1966)

42. Bruce, W. N., Decker, G. C., and Wilson, J. G. The relationship of the levels of insecticide contamina­tion of crop seeds to the fat content and soil concentration of aldrin, heptachlor and their epoxides. J. Eean. Entomor., 59, 179-81 (1966)

4;;. Bruce, W. N., Link, R. P., and Decker, G. C. Storage of heptachlor epoxide in the body fat and its excretion in milk of dairy cows fed heptachlor in their diets. J. A gr. Food Chem., 13, 63-67 (1965)

44. Burdick, G. E., Harris, E. J., Dean, H. J., Walker, T. M., Shed, J., and Colby, D. The accumulation of DDT in lake trout and the effect on reproduction. Trans. Am. Fisheries Soc., 93, 127-36 (1964)

4.5. Butler, P. A. Commercial fishery in­vestigations. In Pesticide-wildlife studies, 1963. U. S. Fish Wildlife Serv., Cire., 199, 5-28 (1964)

46. Butler, P. A. Commercial fishing in­vestigations. In The effects of pesti­cides on fish and wildlife. U.S. Fish Wildlife Serv., Cire., 226, 65-77 (1965)

47. Butler, P. A., and Springer, P. F. Pesticides--a new factor in coastal environments. Trans. North A m. WildJije Conf., 28th, 1963, 378-90 (1963)

48. Burton, V. E., Deal, A. S., Grigarick, A.A., and Swift, J. E. Pest and dis­ease control programs for rice.

Ann

u. R

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ol. 1

967.

12:2

57-2

86. D

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sona

l use

onl

y.

PESTICIDES AND NONTARGET ORGANISMS 2 8 1

Calif. Unill. Agr. Expt. Sta., Leaf­let, 177, 6 pp. (1965)

49. Campbell, J. L., Richardson, L. A., and SChafer, M. L. Insecticide residues in the human diet. A rch. Environ. Health, 10, 831-46 (1965)

50. Carson, R. Silent Spring. (Houghton Miffiin Co., Boston, Mass., 368 pp., 1962)

51. Chant, D. A. Strategy and tactics of insect control. Can. Entomologist, 96, 182-201 (1964)

52. Chisholm, R. D . • and Koblitsky, L. Pesticides and controls : Accumula­tion and dissipation of pesticide residues in soils. Trans. North Am. Wildlife Conf., 24, 118 (1959)

53. Cole, L. C. Man's ecosystem. Bio­Science, 16, 243-48 (1966)

54. Cottam, C. The ecologist 's role in problems of pesticide pollution. BioScience, IS, 457-63 (1965)

55. Crouter, R. A., and Vernon, E . H. Effects of black-headed budworm control on salmon and trout in British Columbia. Can. Fish Cul­turist, 24, 23-40 (1959)

56. Dale, W. E., Copeland, M. F., and Hayes, W. J., Jr. Chlorinated in­secticides in the body fat of people in India. Bull. World Health Organ., 33, 471-77 (1965)

51. Dale, W. E., Gaines, T. B., and Hayes, W. J., Jr. Storage and excretion of DDT in starved rats. Toxieol. Appl. Pharmaeol., 4, 89-106 (1962)

58. Davey, S. P. Effects of chemicals on earthworms: A review of the litera­ture. U.S. Fish Wildlife Serv., SPec. Sci. Rept. Wildlife, 74, 20 pp. (1963)

59. Decker, G. C., Bruce, W. N., and Bigger, J. R. The accumulation and dissipation of residues resulting from the use of aldrin in soils. J. Econ. Enlomol., 58, 266--7 1 (1965)

60. DeWitt, J. B., and George, J. L. Pesticide-Wildlife Review, 1959. U.S. Fish Wildlife Serv., Cire., 84, 36 pp. (1960)

6 1 . DeWitt, J. B., Stickel, W. R., and Springer, P. F. Wildlife studies, Patuxent wildlife research center 1961-62. In Pesticide wildlife studies. U.S. Fish Wildlife Serv., Cire., 167, 74-96 (1963)

62. Durham, W. F. Pesticide residues in foods in relation to human health. Residue Rev., 4, 31-95 (1963)

63. Edwards, C. A., and Jeffs, K. A. The persistence of some insecticides in

soil and their effect on soil animals. Proc. Intern. Congr. Entomol. 12th, 559-60 (1965)

64. Edwards, R. W., Egan, H., Learner, M. A., and Maris, P. J. The control of chironomids in ponds using TDE (DDD). J. Appl. Eeol., I, 97-1 1 7 (1964)

65. ElSayed, I. Chlorinated hydrocarbon insecticide residues in selected in­sects and birds found in association with cotton fields. (Master's thesis, on file Louisiana State Univ., Baton Rouge, La., 1965)

66. Elson, P. E., and Kerswill, C. J. Forest spraying and salmon an­gling. A tlantic Salmon J., 3, 20-29 (1964)

67. Fahey, J. E., Butcher, J. W., and Murphy, R. T. Chlorinated hydro­carbon insecticides residues in soils of urban areas, Battle Creek, Mich. J. Econ. Entomo!., 58, 1026-27 (1965)

68. Falk, R. L., Thompson, S. J., and Katin, P. Carcinogenic potential of pesticides. Arch. Environ. Health, 10, 847-58 (1965)

69. Ferguson, D. E., Cotton, W. D., Gardner, D. T., and Culley, D. D. Tolerances to five chlorinated hy­

. drocarbon insecticides in two spe­cies of fish from a transect of the lower Mississippi River. M issis­sippi J. Sci., 1 1, 239-45 (1965)

70. Ferguson, D. E., Culley, D. D., Cotton, W. D., and Dodds, R. P. Resistance to chlorinated hydro­carbon insecticides in three species of freshwater fish. BioScience, 14, 43-44 (1964)

7 1 . Finlayson, D. G., and McCarthy, H. R. The movement and persis­tence of insecticides in plant tissues. Residue Rev., 9, 1 14-52 (1965)

72. Geier, P. W., and Clark, L. R. An ecological approach to pest con­trol. ProG. Intern. Union Conser". Nature Nat. Resources, Tech. Meet­ing 8th, Warsaw, 1960, 10-18 (1960)

73. Genelly, R. E., and Rudd, R. L. Chronic toxicity of DDT, toxa­phene and dieldrin to ring-necked pheasants. Calif. Fish Game, 42, 5-14 (1956)

74. Genelly, R. E., and Rudd, R. L. Ef­fects of DDT, toxaphene and diel­drin on pheasant reproduction. Auk, 73, 529-39 (1956)

75. Giglioli, G. Ecological change as a

Ann

u. R

ev. E

ntom

ol. 1

967.

12:2

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86. D

ownl

oade

d fr

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ww

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sona

l use

onl

y.

2 8 2 NEWSOM

factor in renewed malaria trans­mission in an eradicated area. Bull. World Health Organ., 29, 131-45 (1963)

76. Ginsburg, J. M., and Read, J. P. A survey of DDT accumulation in soils in relation to different crops. J. Eeon. Entomor., 47, 467-74 (1954)

77. Graves, J. B., and Mackensen, O. Topical application and insecticide resistance studies on the honey bee. J. Eeon. Enlomol., 58, 990-93 (1965)

78. Gresham, G. Pesticides vs. wildlife. Louisiana Conservationist, 14, 6-8 (1962)

79. Grzenda, A. R. Investigations of in­secticide pollution in and in the vicinity of Memphis, Tennessee. In Report on pollution of the lower Mississippi River. 60-81 (U.S. Public Health Serv., Unpublished Rept., May 5, 1964)

80. Grzenda, A. R., Lauer, G. J., and Nicholson, H. P. Water pollution by insecticides in an agricultural basin. II. The Zooplankton, bot­tom fauna, and fish. Limnol. Oceanog., 9, 318-23 (1954)

81. Hall, D. G. Use of insecticides in the United States. Bull. Entomol. Soc. Am., 8, 90-92 (1962)

82. Hardee, D. D., Gutenmann, W. H., Keenan, G. I., Gyrisco, G. G., Lisk, D. J., Fox, E. H., Trimbeyer, G. W., and Holland, R. F. Residues of heptachlor epoxide and telodrin in milk from cows fed at part per billion insecticide levels. J. Eeon. Entomol., 56, 404-7 (1964)

83. Harley, K. L. S., and Wilkinson, P. R. A comparison of cattle tick control by "conventional" acara­cidal treatment, planned dipping, and pasture spelling. Australian J. AgT. Res., IS, 841-53 (1964)

84. Hayes, W. J., Jr. The toxicity of dieldrin to man. Bull. World Health Organ., 20, 891-912 (1959)

85. Hayes, W. J ., Jr. Pesticides in relation to public health. Ann. Rev. Entomol. 5, 379-404 (1960)

86. Hayes, W. J., Jr. Statement before the Hearings, Subcommittee on Reorganization and International Organization of the Committee on Government Operations. (U.S. Sen­ate, Pt. 2, 410, 1963)

87. Hayes, W. J., Jr., Dale. W. E .• and

Birse, V. W. Chlorinated hydro­carbon pesticides in the fat of people in New Orleans. Life Sci., 4, 1611-15 (1965)

88. Hayes, W. J., Jr., Dale, W. E., and LeBreton, R. Storage of insec­ticides in French people. N atuTe, 199, 1 1 89-91 (1963)

89. Hayes, W. J., Jr., Durham, W. F., and Cueto, C., Jr. The effects of known, repeated oral doses of chlorophenothane (DDT) in man. J. Am. Med. Assoc., 162, 890-97 (1956)

90. Heath, R. G., and Stickel, L. F. Monitoring pesticide residues in waterfowl. In The effects of pes­ticides on fish and wildlife. U.S. Fish Wildlife Serv., Cire., 226, 8 (1965)

91 . Helle, W. Resistance in the Acarina: mites. Advan. A carol., 2, 71-93 (1965)

92. Hickey, J. J., and Hunt, L. B. Initial songbird mortality follow­ing a Dutch elm disease control pro­gram . J. Wildlife Management, 24. 259-65 (1960)

!/J. Hickey, J. J., and Keith, ]. A. Pesti­cides in the· Lake Michigan ecosys­tem. In The effects of pesticides on fish and wildlife. U.S. Fish Wildlife Serv., Cire., 226, 1 1 (1965)

94. Hikichi, A. The status of apple leaf rollers in Norfolk County Ontario. Proe. Entomol. Soc. Ontario, 94, 38-40 (1964)

95. Hindin, E., May, D. S., and Dunstan, G. H. Collection and analysis of synthetic organic pesticides from surface and ground water. Residue Rev., 7, 130-56 (1964)

96. Hoffmann, C. H., and Drooz, A. T. Effects of a C-47 airplane applica­tion of DDT on fish food organisms in two Pennsylvania watersheds. Am. Midland Naturalist, 50, 172-88 (1953)

97. Hoffmann, C. H., Townes, H. K., Sailer, R. I., and Swift, H. H. Field studies on the effects of DDT on aquatic insects. U.S. Bur. Entomol. Plant QuaT., E-702, 20 pp. (1946)

98. Hoffmann, D. A., and Oliver, J. R. The effects of rotenone and toxa­phene upon plankton of two Col­orado reservoirs. Limnol. Oeeanog., 6, 219-22 (1961)

99. Hoffmann, W. S., Fishbein, W. I., and Andelman, M. B. Pesticide storage

Ann

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12:2

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in human fat tissue. J. Am. Med. Assoc., 188, 819 (1964)

100. Huddleston, E. W., Ashdown, D., and Herzog, D. C. A comparison of the effects of the 1964 and 1965 High Plains boll weevil control program on population trends of non-target arthropods. (Texas Tech. ColI. Entomo!' Dept., 66-1, 13 pp., 1966)

101. Hueck, H. ]., Kuenen, D. J., DenBoer, P. J., and Jaeger-Draafsel, E. The increase of egg production of the fruit tree red spider mite (M eta­tetranychus ulmi Koch) under in­fluence of DDT. Physiol. Camp. Oeeol., 2, 371-75 (1952)

102. Hunt, E. G., and Bischoff, A. 1. Inimical effects on wildlife of periodic DDD applications to Clear Lake. Calif. Fish Game, 46, 9 1-106 (1960)

103. Hunt, E. G., and Keith, J. O. Pesti­cide-wildlife investigations in Cali­fornia-1962. Proe. Con!. Use Agr. Chem. Calif., 2nd, 29 pp. (1963)

104. Hunt, L. B. Kinetics of pesticide poisoning in Dutch elm disease control. In The effects of pesticides on fish and wildlife. U.S. Fish Wild­life Serv., Cire., 226, 12-13 (1965)

105. Hunter, C. G., Robinson, ]., and Richardson, A. Chlorinated hydro­carbon insecticide content of human body fat in Southern England. Brit. Med. Jr., I, 221-24 (1963)

106. Ide, F. p. Effects of forest spraying with DDT on aquatic insects of salmon streams. Trans. Am. Fisheries Soc., 86, 208-19 (1957)

107. Keenleyside, M. H. A. Effects of spruce budworm control on salmon and other fishes in New Brunswick. Can. Fish Cuiturist, 24, 1 7-22 (1959)

108. Keith, J. A. Reproductive success in a DDT-contaminated population of herring gUlls. In The effects of pesticides on fish and wildlife. U.S. Fish Wildlife Serv., Cire., 226, 1 1-12 (1965)

109. Kiyoku, M., and Tamaki, H. Modi­fication in biotic potentials of in­sects surviving exposure to an in­secticide. Sci. Rep!. Fac. A gr. Okayama Univ., 14, 1-5 (1959)

1 10. Kraybill, H . F. Federal activities in the field of pesticides. Paper pre­sented at Short Course on Occupa­tional Health Aspects of Pesticides,

(Univ. Oklahoma, Oklahoma City, Nov. 20-22, 1963)

1 11 . Kuenen, D. J. Influence of sublethal doses of DDT upon the mUltiplica­tion rate of Sitophilus granarius. Entomol. Expel. Appl., I, 147-52 (1958)

1 12. Kuwada, A. Developments in insec­ticidal control of the rice stem borer in Japan. Symposium on the major insect pests of rice. (Intern. Rice Res. lnst., Los Banos, Laguna, Philippines, Sep. 13-18, 1964)

1 13. Lauer, G. J., Nicholson, H. P., Cox, W. S., and Teasley, J. I. Pesticide contamination of surface waters by sugarcane farming in Louisiana. Trans. Am. Fisheries Soc., (1966)

1 14. Laug, E. P., Prickett, C. S., and Kunze, F. M. Survey analyses of human milk and fat for DDT con­tent. Federation Proe., 0, 294-95 (1950)

1 15. Lichtenstein, E. P., Myrdal, G. R., and Schulz, K. R. Effect of formu­lation and mode of application on the loss of aldrin and its epoxide from soils and their translocation into carrots. J. Eean. Entomol., 57, 133-36 (1964)

1 l 6. Lichtenstein, E. P., and Polivka, ]. B. Persistence of some chlorinated hydrocarbon insecticides in turf soils. J. Eeon. Entamol., 52, 289-93 (1959)

1 1 7. Lichtenstein, E. P., and Schulz, K. R. Translocation of some chlorinated hydrocarbon insecticides into the aerial parts of pea plants. J. Agr. Food Chem., 8, 452-56 (1960)

1 18. Lichtenstein, E. P., Schulz, K. R., Skrenting, R. F., and Stitt, P. A. Insecticidal residues in cucumbers and alfalfa grown on aldrin or heptachlor treated soils. J. Eean. Enlomol., 58, 742-46 (1965)

1 19. Lilly, J. H. Soil insects and their con­trol. A nn. Rev. Entomol., 1, 203-33 (1956)

120. Locher, F. J. Der Einfluss von Di­chiorodiphenyitrichlomethylmethan (DDT) auf einige Tetranyehiden. Z. Angcw. Zool., 45, 201-48 (1958)

121. Lockie, J. D., and Ratcliffe, D. A. In­secticides and Scottish golden eagle eggs. Brit. Birds, 57, 89-102 (1964)

122. Long, W. H., Newsom, L. D., and Mullins, A. M. Endrin residues in the fat of lambs grazed on endrin-

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284 NEWSOM

treated pasture. J. Ecan. Entomol., 54, 605-6 (1961)

123. Lowe, J. The effects of pesticides on estuarine animals. Proc. Gulf Conf. Mosquito Suppression Wildlife Management, 1st . Lafayette, La., 1 964

124. Ludwig, G., Weis, J., and Korte, F. Excretion and distribution of al­drin-BC and its metabolites after oral administration for a long period of time. Life Sci., 3, 123-30 (1964)

125. Mahoney, C. H. Flavor and qUality changes in fruits and vegetables in the United States caused by ap­plication of pesticide chemicals. Residue Rev., I, 1 1-23 (1962)

126. Maier-Bode, H. Neuere Untersuch­ungsergebnisse libel' Pflanzen­schutzmittel-Riickstande. Mitt. Biol. Bundesanstalt Land-Forst­wirtsch., Berlin-Dahlem, 1 15, 91-101 (1965)

127. Mallette, R. D., and Harper, H. T. Population studies of ring-necked pheasants in California. Calif. Fish Game, 50. 292-304 (1964)

1 28. Marth, E. H. Residues and some ef­fects of chlorinated hydrocarbon insecticides in biological material. Residue Rev., 9, 1-89 (1965)

1 29. Martin, F. W., Geis, A. D., and Stickel, W. H. Results of woodcock wing collections, 1959 to 1962. J. Wildlife Management 29, 121-31 (1965)

130. Mehner, J. F., and Wallace, G. J. Robin populations and insecticides. A tlantic Naturalist, 14, 4--9 (1959)

131. Moore, N. W. Pesticides and birds-­A review of the situation in Gl"eat Britain in 1965. Bird Study, 12, 222-52 (1965)

132. Moore, N. W. Organochlorine insec­ticide residues in the eggs of sea birds. Nature, 207, 42-43 (1965)

133. Moore, N. W., and Walker, C. H . Organic chlorine insecticide resi­dues in wild birds. Nature, 201, 1072-73 (1964)

134. Moye, W. c., and Luckmann, W. H. Fluctuations in populations of cer­tain aquatic insects following ap­plication of aldrin granules to Sugar Creek, Iroquois County, Illinois. J. Eean. Entomol., 57, 318-22 (1964)

135. Mumma, R. 0., Wheeler, W. B., Frear, E. H., and Hamilton, R. H . Dieldrin: extractions o f accumula-

tions by root uptake. Science, 152, 530-31 (1966)

136. Muncy, R. J., and Oliver, A. D., Jr. Toxicity of ten insecticides to the red crawfish, Procambarus da/·ki (Girard) . Trans. Am.. Fisheries Soc., 92, 428-31 (1963)

137 . M urphy, E. F., Briant, A. M ., Dodds, M. L., Fagerson, 1. S., Kirkpatrick, M. E., and Wiley, R. C. Pesticides and food flavor effect of insecticides and fungicides on the flavor quality of fruits and vegetables. J. Agr. Food. Chem., 9, 214 (1961)

138. Newsom, L. D. The boll weevil prob­lem in relation to other cotton in­sects. Proc. Boll WeetJil Res. Symp., State Call., Miss., March 1 962, 83-91 (1962)

139. Nicholson, H. P. Insecticide pollution of water resources. J. Am. Water Works Assoc., 51, 981-86 (1959)

140. Nicholson, H. P., Grzenda, A. R., Lauer, G. J., Cox, W. S., and Teasley, J. I. Water pollution by insecticides in an agricultural basin. 1. Occurrence of insecticides in river and treated municipal water. Limnol. Oeeanog., 9, 310-17 (1964)

141. . Oser, B. L. The experimental induc­tion of cancer by pesticide residues and food additives: its rationale and interpretation. Pesticide RetJ., I, 1-10 (1962)

14:Z. Ozburn, G. W., and Morrison, F. O. The selection of a DDT-tolerant strain of mice and some charac­teristics of that strain. Can. J. Zool., 42, 519-26 (1964)

1403. Paradis, R. O. Factors in the recent impol"tance of the red-banded leaf roller, Argyrotaenia velutinana (Walker) in Quebec apple orchards. Quebec Soc. Protection Plants, Rept. No. 38, 45-48 (1956)

H4. Pickett, A. D., and Leroux, E. J. Progress in harmonizing biological and chemical control of orchard pests in Eastern Canada. Proe. Intern. Congr. Entomot., 10th, Mon­treal, 1956, 3, 1 69-74 (1958)

US. Pielou, D. P. The effect of DDT on oviposition, and on behavior, in the European red mite, . Pananychus ulmi (Koch) . Can. J. Zool., 38, 1 147�51 (1960)

Vl6. Popham, W. L., and Hall, D. G. Insect eradication programs. Ann. Rev. Entomol., 3, 335-54 (1958)

1.47. Putrnan, W. L. Lack of effect of DDT

Ann

u. R

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ntom

ol. 1

967.

12:2

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04/2

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PESTICIDES AND NONTARGET ORGANISMS 285

o n fecundity and dispersion of the European red mite, Panonychus ulmi (Koch) in peach orchards. Can. J. Zool., 41, 603-10 (1963)

148. Randolph, N. M., Chisholm, R. D., Koblitzky, L., and Gaines, J. C. Insecticide residues in certain Texas soils. Texas Agr. Expt. Sta., Misc. Publ., MP 447 (1960)

149. Ratcliffe, D. A. Organa-chlorine resi­dues in some raptor and corvid eggs from northern Britain. Brit. Birds, 58, 65-81 (1965)

150. Ripper, W. E. Effect of pesticides on balance of arthropod populations. Ann. Rev. Entomol., 1, 403-38 (1956)

151. Rudd, R. L. The ecological conse­quences of chemicals in pest con­trol, particularly as regards their effects on mammals. In The eco­logical effects of biological and chemical control of undesirable plants and animals. Intern. Union Conserv. Nature Nat. Resources, Tech. Meeting, 8th, Warsaw, 1960, 38-47 (1960)

152. Rudd, R. L. Pesticides and the Living Landscape. (Univ. Wisconsin Press, Madison, Wis., 320 pp., 1964)

153. Rudd, R. L., and Genel1y, R. E. Ef­fects of DDT, toxaphene and dieldrin on pheasant reproduction. A uk, 73, 529-39 (1956)

154. Schoettger, R. A., and Olive, J. D. Accumulation of toxaphene by fish­food organisms. Limnol. Oceanog., 6, 2 1 6-19 (1961)

155. Seifert, G. Der Einfluss von DDT auf die Eiproduktion von Metatetrany­thus ulmi Koch. Z. A ngew. Zool., 48, 441-52 (1961)

156. Sheldon, M . G., Mohn, M. H., Ise, G. A., and Wilson, R. A. Pesticide residues in waterfowl found in the field. In Pesticide Wildlife studies, 1963. U.S. Fish Wildlife Serv., Circ., 199, 55 (1964)

1 5 7. Smith, R. D., and Glasgow, L. L. Effects of heptachlor on wildlife in Louisiana. Ann. Conf. Southeastern Assoc. Game Fish Comm., 17th, 140-54 (1963)

158. Springer, P. F., and Webster, J. R. Biological effects of DDT applica­tions on tidal salt marshes. Mos­quito News, 11, 67-74 (1951 )

1 59. Steiner, P., Wenzel, F., and Baumert, D. Zur Beeinflussung des Arthro­podenfaunanordwestdeutscher Kar-

toffelfelder durch die Anwendung synthetischer Kontaktinsektizide. Mitt. Bioi. Bundesanstalt Land­Forstwirtsch. Berlin-Dahlem, 109, 38 pp. (1963)

160. Stern, V. M., Smith, R. F., van den Bosch, R., and Hagen, K. S. The integration of chemical and bio­logical control of the spotted alfalfa aphid. The integrated control con­cept. Hilcardia, 29, 81-101 (1959)

161. Stickel, L. F., Wildlife studies, Patux­ent wildlife research center. In Pes­ticide-wildlife studies, 1963. U.S. Fish Wildlife, Serv., Cire., 139, 77-96 (1964)

1 62. Stickel, W. H., Hayne, D. W., and Stickel, L. F. Effects of heptachlor contaminated earthworms on wood­cock. J. Wildlife Management, 29, 1 32-46 (1965)

163. Stickel, L. F., Stickel, W. H., and Christensen, R. Residues of DDT in brains and bodies of birds that died on dosages and in survivors. Sci­ence, 151, 1549-51 (1966)

1 64. Tarzwell, C. M., and Henderson, C. Toxicity of dieldrin to fish. Trans. Am. Fisheries Soc., 86, 245-5 7 (1957)

1 65. Taylor, A., and Brady, J. Chlorinated pesticide residues in wild bird eggs. Bird Study, 1 1, 192-97 (1964)

166. Terriere, L. C., Kiigemagi, V., Ger­lach, A. R., and Boronicka, R. L. The persistence of toxaphene in lake water and its Uptake by aquatic plants and animals. J. A gr. Food Chem., 14, 66-69 (1965)

1 67. Walker, K. C., George, D. A., and Maitlen, J. C. Residues of DDT in fatty tissues of big game animals in the states of Idaho and Wash­ington in 1962. U.S. Dept. A gr., A RS-33-105, 21 pp. (1965)

1 68. West, 1. Pesticides as contaminants. Arch. Environ. Health 9, 626-36 (1964)

1 69. West, 1., and M ilby, T. H. Public health problems arising from the use of pesticides. Residue Rev., 11, 141-59 (1965)

1 70. Wheatley, G. A. The persistence, ac­cumulation and behavior of organo­chlorine residues in soil. Proc. In­tern. Congr. Enlomol., 12th, 556-57 (1965)

1 7 1 . Whitcomb, W. H., and Bell, K. Predaceous insects, spiders, and

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286 NEWSOM

mites of Arkansas cotton fields. Arkansas Unill., Fayetteville, Agr. Expt. Sta., Bull., 690, 84 pp. (1964)

172. Wigglesworth, V. B. DDT and thc balance of nature. A tlantic Monthly, 176, 107-13 (1945)

173. Wilkinson, A. T., Finlayson, D. G., and Morley, H. V. Toxic residues in soil 9 years after treatment with aldrin and heptachlor. Science, 143, 681-82 (1964)

1 74. Williams, S., Mills, P. A., and Mc­Dowell, .R. E. Residues in milk of cows fed rations containing low concentrations of five chlorinated hydrocarbon insecticides. J. Assoc. OjJic. Agr. Chemists, 47, 1124-28 (1964)

175. Wright, B. S. Woodcock reproduction in DDT-sprayed areas of New Brunswick. J. Wildlife Manage­ment, 24, 419-20 (1960)

Ann

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ol. 1

967.

12:2

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