Insect population responses to environmental stress and pollutants

Insect population responses to environmental stress and pollutants

DAVID PIMENTEL Department of Entomology and Section of Ecology and Systematics, Cornell University, 6 /26 Comstock Hull, Ithuca, NY

14853-0999, U.S.A.

Received August 5, 1993 Accepted October 22, 1993

PIMENTEL, D. 1994. Insect population responses to environmental stress and pollutants. Environ. Rev. 2: 1-15. Insects and other related arthropods make up about 90% of all plant and animal species in the world. They are vital to the

functioning of the ecosystem and biosphere, and neither of these systems can operate effectively without insect interactions. Because of their major ecological and economic roles in nature and society, the beneficial and pest activities of insects need to be clearly understood. Insect populations are being stressed directly by the action of temperature, moisture, and a wide array of chemical pollutants (pesticides, fertilizers, air pollutants, and numerous other chemicals) that are dispersed through air, water, and soil. Insects are affected by this same group of stresses indirectly, through their food plants, parasites, and predators. Depending on the species and the particular stress affecting it, insect populations respond by increasing or decreasing in numbers. The responses of insect populations to various direct and indirect environmental stresses and chemical pollutants are assessed. Some insect populations increase, while others decline. The responses were determined by the particular environmental stress, the insect species, and the stage at which they were exposed to the stress.

Key words: insects, environment, pollutants, stress, water, herbicides.

PIMENTEL, D. 1994. Insect population responses to environmental stress and pollutants. Environ. Rev. 2 : 1-15. Les insectes et d'autres arthropodes apparent& constituent environ 90% de toutes des espkces animales et vegetales du

monde. Ces organismes sont essentiels au fonctionnement de I'6cosystkme et de la biosphkre et aucun de ces systkmes ne peut fonctionner efficacement sans interactions avec les insectes. Compte-tenu de leurs r8les ecologiques et economiques primordiaux dans la nature et pour la societe, il est essentiel de bien comprendre les activites benefiques et nuisibles des insectes. Les populations d'insectes subissent les stress directs de la temperature et de l'humidite ainsi que d'un ensemble de polluants chimiques (pesticides, fertilisants, polluants atmospheriques, et de nombreuses autres substances chimiques) qui sont dispersees par l'air, l'eau et le sol. Les insectes sont aussi affect& indirectement par le meme groupe de stress qui les agressent, par les plantes dont ils se nourissent, par leurs parasites et par leurs prkdateurs. Selon I'espkce d'insecte et le stress spkcifique qui l'affecte, les populations de l'insecte rkagissent en augmentant ou en diminuant leurs nombres. L'auteur kvalue les reactions des populations d'insectes aux divers stress environnementaux directs ou indirects et aux polluants chimiques. Certaines populations d'insectes augmentent et d'autres diminuent. Les reactions sont dkterminkes par le stress environnemental particulier, I'espkce d'insecte et le stade a lequel ils sont exposes au stress.

Mots clks : insectes, environnement, polluants, stress, eau, herbicides. [Traduit par la redaction)

Introduction

Insects and other arthropods are the dominant group of species in nature, making up approximately 90% of all species of plants and animals in the world. Nearly 1 million species of insects and other arthropods have been described, and at least an additional 8 million species are yet to be documented (Wilson 1988).

Insects facilitate the functioning of the ecosystem and biosphere, and neither can function successfully without insect activity. For instance, insects play a vital role in pollinating crops and natural vegetation; they control numerous pest arthropods and weeds; they help degrade and recycle wastes produced by society and natural organisms; and they provide food for birds, fish, and various other organisms (Pimentel et al. 1980). Although most insects and related arthropods are beneficial and play an essential role in nature, unfortunately about 1% of the species are pests of agriculture and humans (Pimentel 1991). The estimated 9000 species of arthropod pests worldwide destroy about 13% of food and fiber crops, despite the application of about 1 billion tons of insecticides each year (Pimentel 199 1).

Because of their important ecological and economic roles in nature and society, the beneficial and pest activities of insects in both natural and managed ecosystems need to be better understood. The objective of this paper is to analyze

the responses of insect populations to environmental stress and pollution now occurring in various ecosystems.

Responses to climate change

Combustion of fossil fuel, especially coal, is a major con- tributor to increasing carbon dioxide concentration in the atmosphere, thereby contributing to global warming (Abrahamson 1989; Rosenzweig et al. 1993). This is con- sidered to be one of the most serious environmental threats throughout the world because of its potential impact on food production and other vital aspects of a productive environment (Department of Energy 1989; Abrahamson 1989; Rosen and Glasser 1992; Pimentel et al. 1992; Rosenzweig et al. 1993). Various models suggest that the accumulation of greenhouse gases will increase the earth's temperature between 1.5 and 4.5"C or more, increase rainfall in some areas, and cause other areas to become arid (Pimentel et al. 1992; Rosenzweig et al. 1993). The greatest increases in temperature are projected to occur at high latitude.

These potential climate changes could cause substantial ecological effects on insects. For example, an increase in temperature of as little as OS°C can increase the number of generations of insect species per unit time, as well as alter the growing season of crops and natural vegetation (Pimentel et al. 1992). In addition, some insect species, because of the

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2 ENVIRON. REV. VOL. 2, 1994

projected higher temperatures, could expand their ranges and spread northward (Chippendale 1979).

Overall crop losses due to insects are generally higher in warmer regions than in cooler regions. For instance, potato losses to insects in northern Maine average only 6%, whereas in Virginia, under warmer conditions, they average about 15%, despite the application of insecticides (Zehnder and Evanylo 1989).

Both increasing and decreasing rainfall are known to cause substantial changes in the abundance and distribution of insects (Andrewartha and Birch 1954). Heavy rainfall kills certain types of insects such as aphids and leafhoppers. High moisture levels make some insects more susceptible to fungal and other types of pathogens that help control their numbers (DeBach and Rosen 1991). Reducing moisture levels can have the opposite effect. However, arid conditions frequently have a negative ecological effect on various insect species. In general, because of their small size, insects are susceptible to the stress imposed by high evapotranspiration rates (Allee et al. 1949).

Furthermore, changes in temperature and moisture level influence the host plants and in turn affect the insects feeding on the plants. As with insects, changes in temperature and moisture alter the abundance and distribution of host plants, which in turn influence the abundance and distribution of their associated insects. Changes d a y also be indirect. For example, Wellington (1952) reported that outbreaks of the eastern spruce budworm (Choristoneura fumiferana) occurred in fir forests in northern Ontario after two consecutive springs that were earlier than normal. In laboratory studies, Campbell (1989) found that in warm-day plant species the western spruce budworm (Choristoneura occidentalis) larvae fed and grew better; pupae were 20% larger than those from larvae that fed on shoots produced during cool, wet springs. Appar- ently the weather changes altered the nutritive value of the fir tree host, which in turn influenced the growth of the budworm larvae.

Responses to temperature stress

Temperature is a dominant environmental factor that influ- ences both insect populations and plant ecology. Furthermore, other important abiotic factors, such as relative humidity and water availability, are affected by temperature levels. Often it is difficult to vary the temperature level experimentally in a crop plant - insect system without influencing several environmental factors. In fact, temperature stress in plants is frequently impossible to separate from drought stress and other forms of plant stress (Benedict and Hatfield 1988). Therefore, plant - insect herbivore relationships are affected by temperature levels in positive and negative ways. Changes occur in plant physiology and plant resistance as well as in insect behavior and development (Tingey and Singh 1980). In addition, insect pest problems frequently increase with a rise in temperature, whereas the efficacy of insecticides may be im- proved or reduced by changes in temperature (Hinks 1985; Fabellar and Mochida 1988).

The physiology, behavior, intrinsic rate of increase, and survival of insects are responsive to temperature. Because of the predictable response of insects to temperature, models have been developed that analyze the population dynamics of exposed insect species. For example, Got and Rodolphe (1989) created a model to predict the development of the European

corn borer larva. The model accurately simulated the development of all instars with the exception of the first. The only information needed for the model was the temperature given in degree-days and the variability of the population development time for the different instars.

Thus, using temperature data, the feeding rate and the number of pest generations can be predicted for some pests. For instance, the development of the Colorado potato beetle from egg to adult takes 56.4 days at 15"C, whereas at 28°C development is completed in 20.7 days (Ferro et al. 1985). Similarly, the feeding rate of the beetle increased with temperature: at 15°C adult Colorado potato beetles consumed a leaf area of 8.4 cm2 in 10 days, whereas at 24°C they consumed a 96.5-cm2 leaf area in the same number of days. Therefore, the feeding rate increased more than 10-fold when the temperature increased by 9°C. Because of the influence of temperature, the population and the number of generations of the beetle differ from location to location, depending on the average regional temperature. Trouvelot (1935) and Hurst (1975) observed a relationship between the number of potato beetle generations and the mean summer (July, August, and September) isotherms. Three generations occurred south of the 26°C isotherm, e.g., in Texas and the Carolinas. In this region, one cycle had a duration of only 25-30 days, and the first generation developed by the end of April or early May. Two generations occurred between the 17 and 26°C isotherms, e.g., in the Midwest, where one cycle lasted 30-40 days and the first generation developed in May or early June. Only one generation was found between the 14 and 17°C isotherms, e.g., in the southern parts of Canada. In this latter region the generation occurred in the period from June to August, and the cycle had a duration of 50-60 days.

Similarly, the codling moth on apple, which has on average one generation in Nova Scotia, usually has two full generations and often a partial third in the southern United States (Putnam 1963). For this reason, the codling moth is a more serious pest of apples grown in the south than in Nova Scotia.

High temperatures can also stress various insects. For instance, as temperatures increased from 20 to 30°C, fertility in Drosophila robusta and Drosophila tripunctata decreased significantly (Seager 199 1).

The feeding rate, development, population growth, and the number of generations of insects are mainly determined by the temperature during the period of plant growth. Further- more, the temperature during the fall, winter, and spring determines whether most insect species can survive in a given area. When winter temperatures fall below the tolerance level of the overwintering stage of an insect, it cannot survive. Note that in the United States, the fall armyworm (Spodoptera frugiperda), which is a species of tropical origin, is able to overwinter only in the southern parts of Texas and Florida (Luginbill 1928; Barfield et al. 1978). In spring, this pest advances northward by flight, each generation spreading farther north. In normal years, the gulf-coast invasion peaks in April and reaches the region from northern Texas to North Carolina by June. The dissemination continues during the growing season, and subsequently, by September and October, the armyworm can be found from Nebraska to Pennsylvania. In favorable years, more northerly areas, such as New York State, can be invaded. The number of generations varies according to the latitude of the habitat. In the southern regions, where the species lives throughout the year, six or

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PIMENTEL 3

more generations occur, while in the northern regions, usually only one generation occurs (Luginbill 1928).

Insects that feed on plants are frequently attacked by predators and parasites, and these interrelationships can be affected by temperature. For instance, Tamaki et al. (1981) observed that without predators the green peach aphid grew exponentially on sugar beets. However, the rate of aphid increase decreased as temperatures rose. When predatory species (Geocoris bullatus and Nabis alternatus) were added to the aphid-plant system, the growth rates of the aphids were significantly reduced at all temperatures. Overall, predation was most efficient at high temperatures.

As Benedict and Hatfield (1988) point out, there is no direct evidence that insect populations increase on temperature- stressed plants as a result of altered plant metabolism. How- ever, because plants produce different defensive chemicals, and the synthesis and concentration of these secondary compounds may be affected by temperature change, they suggest that host-plant resistance declines with increasing temperatures. Sosa (1979) found that the wheat cultivar Abe, which is resistant to the Hessian fly (Mayetiola destructor), main- tained this resistance at a soil temperature of 18°C. However, when 'Abe' was exposed to 27°C for 1 day, the resistance was reduced by 50%, and after 7 days at 27°C resistance was lost completely.

In rice, temperature stress Gas found to influence varietal resistance to the whitebacked planthopper. Both high- and low-temperature stress in rice plants increased their susceptibility to the whitebacked planthopper (Salim and Saxena 1991). The researchers suggested that before resistant rice plants are released, they should be tested against planthoppers over a wide range of temperatures.

Temperature change also affects fungal pathogens of insects. For example, the mortality of the green peach aphid due to the fungal pathogen Zoophtera phalloides is greatest (44-55%) between 12 and 18°C (Glare et al. 1986). At 18"C, about 8 days were required to kill all infected insects; at 12°C it took longer, or about 14 days. At lower temperatures the mortality decreased and the time to kill all infected aphids increased to about 20 days. At 22°C the mortality in the aphid population was only 2%.

Studies by Chen et al. (1990) demonstrated that some insects evolve in response to selective pressures in their particular environment. This was confirmed with tropical and temperate flies. Two flesh fly species (Peckia abnormis and Sacodexia sternodontis) from a tropical lowland region were more susceptible to both cold- and heat-shock damage than similar temperate fly species (Sacophaga crassipalpis and Sacrophaga bullata) and a fly (Blasesoxipha plinthopyga) from tropical high-altitude cool conditions. Although the two groups of flies have a similar mechanism for increasing their high temperature tolerance, only the temperate fly species appeared capable of responding rapidly to cold stress.

Predaceous insects are also adversely affected by temperature extremes and other stresses. For example, temperature, starvation, and other stresses, when applied individually and in various combinations, significantly increased the susceptibility of the predatory insect Chysopa carnea to the fungal pathogen Beauveria brassiana (Doregan and Lighthart 1989).

The effect of insecticides on insect-pest mortality is frequently temperature dependent. Hinks (1985) and Fabellar and Mochida (1988) tested the susceptibility of some insects

to insecticides under different temperatures (range 15.6- 37.8"C), and found that pyrethroids and some carbamate insecticides were most effective at lower temperatures. In contrast, they found that organophosphate insecticides were more effective as temperatures increased. Insect species also differ in their response to pesticide-temperature changes. Fabellar and Mochida (1988) evaluated the LDso of seven insecticides applied at six different temperatures (18-33°C) to two insect pests of rice, the brown planthopper and the green leafhopper. The LDso of deltamethrin (a pyrethroid) at 18°C was 1.5 times higher than at 33°C for the brown planthopper, but 5.9 times higher for the green leafhopper. How- ever, the LDso of malathion (an organophosphate) was 4. l times higher with the brown planthopper and only 1.7 times higher with the green leafhopper at 33°C than at 18°C.

Understanding how temperature changes affect insect populations, and alter plant hosts, beneficial insect species, and the effects of pesticides, helps entomologists understand insect population dynamics and the control of insect pests.

Responses to water stress Water directly affects the development, reproduction, and

behavior of insects as well as the status of their plant host (Rhoades 1983; Ferro 1987). All of these factors, separately and in combinations, plus the nutrient makeup of the host plant, affect the ecology of insect populations.

Direct efSects of water stress Excess soil water may drown insects, especially eggs and

young larvae. Also, flooding can force insects to move to the soil surface, where they can be attacked by predators and (or) parasites (Beirne 1970). For some pests, such as the olive- green cutworm (Dargida procincta), flooded soils are favorable (Beirne 1970). In Ghana, outbreaks of grasshoppers (Hierogliphus dagonensis) have followed flooding (Agyen- Sampong 1975). The Australian plague locust is another example of an insect that seems to be favored by exceptionally wet conditions (Beekey 1940; Varley et al. 1973).

Even small amounts of water benefit some insects. For example, Egwuatu and Taylor (1976) reported that the grain moths Ephestia cautella, E. ellutella, and E. kuhniella had higher fecundities when free water was available to them. Similarly, females of another grain insect (Acanthonia tomen- tosicollis) had a 4-fold higher fecundity and greater longevity than females reared without available water.

Relative humidity interacting with temperature affects the development of some insects. Pen (1947) reported that eggs of the confused flour beetle survived best under dry conditions. When the humidity was raised to 90% or more, no hatching occurred, primarily because of fungal infections in the eggs. The opposite occurred with the bean weevil (Bru- chus obtectus), which had shorter development times and grew larger under high-humidity and high-temperature conditions (Pen 1947).

Indirect efSects of water stress Water may influence the population density of predaceous

and parasitic insects, which in turn may affect the number of insects attacking plant hosts. Beirne (1970) reported that wet weather favored parasitic fungal diseases that attack grasshoppers. Wet weather also causes fungal outbreaks in aphids, redbacked cutworms, diamondbacked moths, and wireworms (Beirne 1970; Varley et al. 1973). However, in some

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situations, excessive rainfall reduces insect parasites of aphids Irrigation practices and insect populations and the pale western cutworm (Beirne 1970). Beirne (1970) noted that the increase in population density of various cutworms and wireworms that follows flooding is probably caused by the destruction of their natural enemies. This also explained the increase in parasitism rates on the wheat stem sawfly with increased rainfall.

Variability in response to water is illustrated by predation on the spider mite Tetranychus ludeny, which increased at low humidity levels and declined at high moisture levels (Puttaswamy and Channa Basawanna 1980), whereas predation on the green leafhopper Nephotettix virescens increased at high humidity levels (Upadhyay 1983).

Water stress, plants, and insects Too much or too little water available to plants affects their

biochemistry and biophysics, including changes in the os- motic pressure in phloem and xylem, as well as in concentrations of soluble chemical compounds in cell sap. These changes may in turn affect the insect populations associated with the plant, especially sucking insects (Holtzer et al. 1988). Some water-stressed plants produce larger quantities of soluble amino acids like proline and valine (Biswas et al. 1982; Cockfield 1988; Holtzer et al. 1988; Mattson and Haack 1987a, 1987b). The levels of these same amino acids increase in leaves that begin to become senescent. The accumulation of free amino acids in plant leaves could explain the increase in abundance of some herbivorous insects feeding on water- stressed plants (White 1969, 1984; Mattson and Haack 1987a, 1987b). Drought stress has been found to reduce plant defenses; sometimes it increases levels of phagostimulants, leading to increased feeding of some insect species (Holtzer et al. 1988).

Holtzer et al. (1988) attributed the decrease of aphid numbers (Aphis.fabae) on drought-stressed plants to low turgidity in plants cells. However, Miles et al. (1982) reported that the cabbage aphid reached maturity more rapidly when feeding on drought-stressed plants then did cabbage aphids feeding on normal plants. In other studies, the longevity, fecundity, and reproduction of the aphid Schizaphis graminum, declined with increased drought stress in wheat (Summer et al. 1983). Also, damage to drought-stressed wheat plants was found to be greater than to normal plants (Walker 1954; Dorschner et al. 1986). In the field, low humidity and high temperatures increased the numbers of S. graminum. In contrast to that of aphids, the development of the cabbage white butterfly caterpillar was not affected when it fed on water-stressed plants. Similarly, the caterpillar Paraopsis atomaria was unaffected when i t fed on water-stressed plants (Miles et al. 1982).

Also, the net reproductive rate of the potato leafhopper declined on water-stressed alfalfa (Hoffman and Hogg 1991; Hoffman et al. 1991). In addition, the leafhoppers preferred well-watered alfalfa over water-stressed alfalfa (Hoffman and Hogg 1992). However, a negative association was found between cotton-leaf moisture and oviposition by Heliothis virescens.

In Australia, water stress on curly Mitchell grass had a detri- mental impact on populations of the common armyworm and the Australian plague locust (Phelps and Gregg 199 1 ). A mini- mum of 20 mm of rainfall was vital for survival of these insects, and even at 60 mm, development was restricted in certain cases.

Increasing the availability of water by irrigation extends the season for plant growth and thereby increases crop yields. However, extending the growing season also enables insect- pest populations to continue to grow, and perhaps eventually to reduce crop yields (Office of Technology Assessment (OTA) 1979). This situation occurred with cotton in Texas.

Rao and Rao (1983) reported that heavy irrigation of rice and close spacing of the plants created favorable conditions for outbreaks of the rice-gall midge and the yellow rice-stem borer. They postulated that the close spacing of the plants increased the relative humidity in the canopy, which favored both insect-pest populations.

Watson et al. (1978) found that limiting the period of irrigation in cotton reduced the numbers of cotton pink bollworm larvae overwintering in cotton fields. Therefore, for some crops, irrigation can be a practical method for controlling some insect populations. Altering the time of irrigation made cotton less attractive to the cotton bollworm and tobacco budworm (El-Zik and Frisbie 1985). Similarly, in Egypt the caterpillar Spodoptera littoralis was controlled on cotton by restricting the irrigation of clover after the beginning of May. This procedure reduced the abundance of caterpillars on clover and prevented their movement onto the adjacent cotton crop (Khalifa et al. 1979).

Because irrigation favors oviposition by the cotton bollworm moth and improves larval survival, restriction of irrigation might be used to reduce cotton bollworm numbers (Slosser 1980). In contrast, the cotton whitefly population was reduced by weekly irrigation (El Khidir 1965). In this situation, frequent irrigation increased the relative humidity in the crop, thereby reducing whitefly numbers. Similarly, frequent irrigation reduced damage from the cabbage rootfly (Coaker 1 965).

Some insect problems, become more severe under heavy irrigation, however (Rivnay 1972; Faragalla 1988; Harpaz 1986). For example, in Israel the sorghum shootfly (Atheri- gonia varia soccata) is a rare insect pest of sorghum under dry-land farming conditions, but under irrigation it becomes a serious pest. This response to irrigation is also typical of the onionfly (Hylemya antiqua), spiny bollworm, and Spodoptera littoralis on cotton; the scale Saissetia oleae on olives and citrus, the aphid Aphis pomi on apple (Rivnay 1972), and alfalfa aphids and the leopard moth (Zeuzera pyrina) on olive trees (Harpaz 1986).

Responses to chemical pollution Insect populations are affected by fertilizer nutrients, pesti-

cides, air pollutants, and other chemical stresses. These chemicals may increase insect abundance and distribution as well as decrease their numbers, depending on the sensitivity and response of the insect species to the various chemicals.

Fertilizer nutrients and plant .feeding by insect herbivores Populations of herbivorous insects on plant hosts may be

influenced by the application of nitrogen (N), phosphorus (P), and potassium (K) present in chemical fertilizers, manures, and composts (Painter 1951; Jones 1976; Scriber 1984; Brodbeck and Strong 1987). Although fertilizer and insect relationships have been studied by many investigators, the interactions among insects, fertilizers, and plants are not always consistent. The variation appears to be due to differ- ences in insect species, plant varieties, and the environmental

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PIMENTEL 5

and soil conditions in which the insects and plants interact. apple trees grown on clean cultivated soil than on trees grown The stress effects of N, P, and K levels on insects and plants are assessed below.

Nitrogen N is essential for the structural and physiological develop-

ment of both insects and plants, and appears to have a major influence on insect -plant interactions (Maxwell 1972; McNeill and Southwood 1978; Scriber 1984). Plants contain an average of about 2% N, whereas insects average 7% N in their tissue (Dale 1988). This suggests that insects must con- centrate N from plant tissues into their bodies. To provide themselves with N, many insects feed on young, actively growing plant tissues and seedlings that contain relatively high levels of N (McNeill and Southwood 1978; Mattson 1980; Denno 1985).

Different species of plants and (or) cultivars contain varying kinds and proportions of amino acids, and these dif- ferences are thought to affect insect development (Auclair 1963; Markkula and Roukka 197 1 ). Auclair ( 1963) reported that aphids were more abundant on plants with high levels of water-soluble N in their tissues. However, various amino acid combinations in plant tissues can diminish the susceptibility of plants to phytophagous insect feeding. For example, most dicots convert mineral N to the amine form shortly after absorption from the soil, dhereas many grasses maintain a high level of nitrates and ammonium ions in their tissues after absorption. Neither of these two forms of N in plant tissue can be used by insects in their nutrition (Brodbeck and Strong 1987).

Drought-stressed, senescent, and heat-stressed plants may frequently contain greater amounts of soluble amino acids such as proline and serine than normal plants (Cockfield 1988). These amino acids favor the development and increase of insects that feed on old and (or) more stressed plant tissues (White 1984). Cockfield's observations stimulated White (1984) and other investigators to speculate that stressed plants are more palatable to insects. To investigate this hypothesis Thomas and Hodkinson ( 199 1) exposed trees of two species (Betula pendula and Salix cinerea) to varying levels of water and N amounts, both individually and in combination, and the feeding and survival of three lepidopteran species (Smerinthus ocellantus, Phalera bucephala and Mimax tiliae) were care- fully measured under controlled conditions. Generally the plants reacted to water stress by increasing the concentration of water-soluble N in their systems. Similar effects were noted with high levels of N. In general, the insects grew larger and more abundant when N levels in the plants were high. This suggests that the plants do not have to be stressed to be attractive to feeding insects, and that high N levels will also make them attractive to insect herbivores.

Sometimes pesticide applications stress plants, increase their N level, and thus make them more attractive to feeding insects (Chaboussou 1976; Adzhemyan 1980; White 1 984). For example, herbicides increased the soluble protein-N levels in corn and other plants (Oka and Pimentel 1974, 1976; White 1984). In addition, the exposure of plants to airborne pollutants increased the level of free amino acids in damaged plant tissues (White 1984).

Both White (1984) and Perrenoud (1977) reported that soil- nutrient stress caused an increase in soluble N in plants. In experiments by Schimdle et al. (1975), leaf analysis showed that N concentration was significantly higher in the leaves of

with cover crops. They reported that populations of the codling moth, rose apple aphid, and other insect pests were significantly greater on apple trees with high N levels (Schimdle et al. 1975).

Heavy N fertilizer applications often increase the level of N in crops and trees and alter the amino acid patterns in the vegetation, making them more susceptible to insect attack (Jones 1976). Also, Scriber (1984) reported that several studies have shown increased insect abundance on plants grown with high levels of N. Similarly, high levels of N in the soil doubled pest numbers per unit area on collards compared with plants receiving low-N fertilizer (Culliney and Pimentel 1986; Eigenbrode and Pimentel 1988). Also, high levels of N as calcium nitrate and ammonium sulfate applied to Norway spruce doubled the homopteran (Cinara pilicornis) population feeding on the trees (Holopainen et al. 1991).

N fertilization of some plant varieties is reported to increase the level of certain amino acids, alkaloids, and (or) allelo- chemicals, which in turn may suppress arthropod pests (Scriber 1984; Brodbeck and Strong 1987). Further, the kind of N fertilizer applied affects the population levels of insects. For example, Moore and Clements (1984) demonstrated that plots of rye receiving N as ammonium sulfate had 20% more damage from stem-borer larvae (Oscinella sp., Geomyza tripuncata) than did rye in plots treated with calcium nitrate fertilizer.

Phosphorus P is also an essential element for plant growth and develop-

ment. The impact of P on insect populations, however, appears to be less dramatic than that of N. For instance, P applied to mustard, corn, sugarcane, sunflower, groundnut, cowpea, and rice was found to have little or no effect on several insect species (Waghray and Singh 1965; Ramakrishnan et al. 1983). However, heavy applications of P to citrus seedlings increased the populations of scale insects (Salama et al. 1985), and P applied to pigeon pea increased the number of Heliothus armigera caterpillars (Ramakrishnan et al. 1983).

Also, heavy fertilization of alfalfa with P and K produced populations of the alfalfa weevil 34% larger than those on the light fertilization stands (Shaw et al. 1986). In contrast, populations of the potato leafhopper on alfalfa were 43% more abundant after light fertilization then after heavy fertilization. This illustrates that insect species vary in their nutritional requirements and in their response to various plant nutrients.

In an investigation with another legume, soybean, treated with P, K, and magnesium (Mg), Funderburk et al. (1991) reported that larval populations of the velvetbean caterpillar were more abundant on the high-P treatments. The response to K was mixed, and there was no confirmed increase in the numbers of larvae on plants treated with Mg.

Potassium High levels of K applied to plants often suppress insect

populations on crops (Perrenoud 1977). The accumulation of soluble chemical compounds in plants suffering from K deficiency is often accompanied by increased pest numbers (Perrenoud 1977; Dale 1988). This is probably due to the effect of K in reducing free amino acids and soluble carbohydrates in plant tissue. Further, high levels of K in combination with P can change plant structures and physiology,

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and thereby improve their resistance to insect attack (Perrenoud 1977).

Stamp and Harmon (1991) illustrated the influence of K and sodium (Na) on the fecundity and survival of the Japanese beetle by topically treating leaves of the host plant, Japanese knotweed. They found that the beetles survived best on the untreated leaves and that in a few of the K treatments the beetles produced more eggs. In a few treatments, Na reduced egg production.

Manure Organic fertilizer in the form of manure did not affect the

abundance of the leafhopper Ernpoasca devastant or cotton aphid on cotton (Jayaraj and Venugopal 1964). However, heavy applications of cow manure to planted collards significantly reduced the number of flea beetles, cabbage white butterflies, diamondbacked moths, aphids, and other insects compared with collards treated with commercial fertilizer and untreated controls (Culliney and Pimentel 1986; Eigenbrode and Pimentel 1988). It appears that manure per se does not directly reduce insect numbers (Geisler 1988), but probably improves soil conditions for plant growth. The resulting im- provement in the biochemical and physical characteristics of the plants may enhance their resistance to insects.

Pesticide stress on insects *

Pesticides, because they are toxic chemicals, stress insects, plants, and most other living organisms exposed at suitable dosage levels and for a sufficient period of time. The effects may be direct or indirect and are sometimes difficult to trace.

For example, pesticides can affect the reproductive rate of insects, most often reducing the rate of production. However, low dosages of insecticides sometimes increase the rate of reproduction in insects. Sublethal doses of DDT, dieldrin, and parathion, for instance, increased egg production by the Colorado potato beetle after 2 weeks' exposure by 50,33, and 65%, respectively (Abdallah 1968). Sometimes when insecticides are applied there is mortality in one species of insect but none in another. For instance, Kerns and Gaylor (1993) reported that when sulprofos was applied to cotton for control of the cotton bollworm and cotton budworm, it caused no mortality in the cotton aphid population. They suggested that this treatment for the two caterpillar species induced outbreaks in the cotton aphid population.

In natural and agroecosystems, many species of insect predators and parasites control herbivorous insect populations. Indeed, natural enemies play a major role in keeping populations of many insect and mite pests under control (DeBach 1964; Huffaker 1977; Pimentel 1988), and make it possible for ecosystems to remain "green." With the parasites and predators keeping insect-herbivore populations at relatively low levels, only a relatively small amount of plant biomass is removed each growing season (Hairston et al. 1960; Pimentel 1988).

All too frequently, beneficial natural enemies are adversely affected by pesticides (van den Bosch and Messenger 1973; Adkisson 1977; Ferro 1987; Croft 1990). For example, the following pests have reached outbreak levels in cotton and apple crops following the destruction of their natural enemies by pesticides: in cotton: cotton bollworm, tobacco budworm, cotton aphid, spider mites, and cotton loopers (Adkisson 1977; OTA 1979); in apple: European red mite, redbanded leafroller, San Jose scale, oystershell scale, rosy apple aphid,

woolly apple aphid, white apple aphid, twospotted spider mite, and apple rust mite (Tabashnik and Croft 1985; Messing et al. 1989; Croft 1990; Kovach and Agnello 199 1). Signifi- cant pest outbreaks have also occurred in other crops (Huffaker and Kennett 1956; Huffaker 1977; OTA 1979; Croft 1990; Pimentel 199 1 ). Peach aphid populations on potato greatly increased, for various reasons, when carbaryl was applied to potatoes (Ferguson and Chapman 1993). Because parasitic and predaceous insects often have complex searching and attack behaviors, sublethal insecticide dosages are thought to alter this typical behavior and thereby disrupt the effectiveness of their biological control (L.E. Ehler, Uni- versity of California, personal communication, 199 1).

The use of fungicides can contribute to pest outbreaks when they reduce fungal pathogens that are naturally parasitic on many insects. Note that the use of benomyl reduced populations of entomopathogenic fungi, which resulted in the increased survival of velvetbean caterpillars and cabbage loopers in soybeans, and ultimately reduced soybean yields (Ignoffo et al. 1975; Johnson et al. 1976).

D. Rosen (Hebrew University of Jerusalem, personal communication, 1991) estimates that natural enemies account for up to 90% of the control of pest species achieved in agroecosystems and natural systems; I estimate that at least 50% of the control of insect species is due to natural enemies. Pesticides give an additional control of 10% (Pimentel et al. 1978), while the remaining 40% is due to host-plant resistance and other limiting factors present in the agroecosystem (Pimentel 1988).

Some herbicides not only affect weeds and crops, they can also directly affect insects. Baker et al. (1985) treated cotton with the herbicide monosodium methanearsonate, and found that the number of thrips (Frankliniella spp.), insidious flower bugs, damsel bugs, Nabis spp., leafhoppers, and adult tarn- ished plant bugs was significantly reduced. In no instance were insect numbers directly increased by herbicide use. The indirect effects of herbicides on insect populations are dis- cussed in the next section.

Pesticide stress on plants afSects insect populations Plants are stressed by pesticides, including insecticides,

fungicides, and herbicides (Pimentel 1971; McEwen and Stephenson 1979; Campbell 1988; Riley 1988). Plants under stress from pesticides experience alterations in their physiology and growth patterns, and it is these changes that affect crop productivity.

Phorate insecticides applied to cotton increased the carbohydrate and P content of the treated plants and at the same time decreased their N content (Hacskaylo 1957). Cole et al. (1968) demonstrated how low insecticide dosages may stress and alter the nutritional makeup of plants. They reported that heptachlor and DDT applied to soil at only 1 ppm increased some, and decreased other, macro- and micro-element constituents (N, P, K, Ca, Mg, Mn, Fe, Cu, B, Al, Sr, and Zn) in corn and beans.

Other investigators found that insecticides applied to rice reduced the total amount of reducing sugars while increasing the amount of amino-N, when measured 15 days after exposure (Rao and Rao 1983). Also, when rice was treated with carbofuran insecticide, the levels of N, K, Zn, and Fe increased, but the amounts of Cu and Mn decreased (Venugopal and Litsinger 1983 cited in Riley 1988).

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TABLE 1. Susceptibility to insect attack in plants exposed to various herbicides

Herbicide Insect species Plant species Attack Reference

Acifllurofen Banvel D Banvel D B arb an Barban B arban Bentazon Caragard Combi 2,4-D 2,4-D 2,4-D 2,4-D (sublethal) 2,4-D (sublethal) 2,4-D 2,4-D 2,4-D 2,4-D Fluazfopbutyl Fluazfopbutyl Fluazfopbutyl Gramoxone MCPA MCPA Melfluidide Melfluidide MSMA MSMA Reglone Semparol Sethoxydim Sethoxydim

Geocoris punctipes English grain aphid Oat bird-cherry aphid English grain aphid Oat bird-cherry aphid Greenbug Geocoris punctipes Spider mites Sugarcane borer Wireworms Grass hopper Aphids Aphids Rice stem borer Corn leaf aphid Corn borer Yellow Stem Borer Ceratoma trifurcata Corn earworm Mexican bean beetle Spider mites English grain aphid Oat bird-cherry aphid Ceratoma trifurcata Corn earworm' Whitefly Lygus bug Spider mites Spider mites Ceratoma trifurcata Corn earworm

Soybeans Barley Barley Barley Barley Barley Soybeans Grapes Sugarcane Wheat Weeds Fava bean Broad bean Rice Corn Corn Rice Soybeans Soybeans Soybeans, beans Grapes Barley Barley Soybeans Soybeans Cotton Cotton Grapes Grapes Soybeans, beans Soybeans

Increased eggs + hatch Increase Increase Increase Increase Increase Increased eggs + hatch Outbreaks Increase Increase Nymphs abundant Increase Increase Increase Three-fold increase 28% increase Increase Larvae abundant Larvae abundant Treatments preferred Outbreaks Increase Increase Larvae abundant Larvae abundant Increase Increase Outbreaks Outbreaks Treated leaves preferred Larvae abundant

Farlow and Pitre 1983 Hintz and Schulz 1969 Hintz and Schulz 1969 Hintz and Schulz 1969 Hintz and Schulz 1969 Hintz and Schulz 1969 Hintz and Schulz 1969 Boller et al. 1984 Ingram et al. 1947 Fox 1948 Putnam 1949 Maxwell and Harwood 1958 Maxwell and Harwood 1960 Ishii and Hirano 1963 Oka and Pimentel 1976 Oka and Pimentel 1976 Moody 1990 Agnello et al. 1986b Agnello et al. 1986b Agnello et al., 1986a Boller et al. 1984 Hintz and Schulz 1969 Hintz and Schulz 1969 Agnello et al. 1986b Agnello et al. 1986b Stam et al. 1978 Stam et al. 1978 Boller et al., 1984 Boller et al. 1984 Agnello et al. 1986b Agnello et al. 1986b

In addition, chlordimeform-treated cotton that was already under some drought stress tended to have higher concentrations of Ca, P, Mg, and K after 2 weeks than untreated cotton (Weaver and Bhardwaj 1985). Belanger et al. (1985) reported that N fixation in birdsfoot trefoil increased when it was treated with carbofuran, although the number of nodules on the legumes did not increase.

At some dosages, insecticides may actually stimulate the growth of some plants. For example, when vegetables, cotton, tobacco, corn, sorghum, and rice plants were exposed to DDT, toxaphene, aldrin, dieldrin, carbamate, azinphosmethyl, meth- omyl, and carbofuran, they grew larger than unexposed plants (Chapman and Allen 1948; Hacskaylo and Scales 1959; Schultz 1961; Brown et al. 1962; Reed 1964; Hagley 1965; Apple 1971; Pless et al. 1971; Wheeler and Bass 1971; Daynard et al. 1975; Yein et al. 1979; Thompson and Harvey 1980; Duveiller et al. 1981; Venugopal and Litsinger 1983 cited in Riley 1988). However, when many of these same crop plants were exposed to some of the same insecticides at different dosages, plant growth was suppressed. Therefore, not only is the particular insecticide a factor that determines plant response, but also, its dosage.

Altering the nutritional makeup and (or) growth pattern of a plant will change the susceptibility of the plant to insect attack (Painter 195 1 ; Pimentel 1977, 1988; White 1984; Riley 1988). Whether the susceptibility will increase or decrease depends on the type of changes occurring in the plant and the insect species involved.

Changes in the nutrient content and growth pattern of plants caused by herbicides may increase or decrease the abundance of insects (Pimentel 197 1 ; Campbell 1988). As expected, changes in the physiology of plants exposed to herbicides are generally more extensive than those caused by insecticides and fungicides, because herbicides are designed to alter the physiology of plants (Pimentel 197 1; Oka and Pimentel 1976). For example, higher levels of amino acids, protein, and N were reported in a wide array of crop plants treated with normal dosages of 2,4-D (Maxwell and Harwood 1960; Pimentel 197 1; Oka and Pimentel 1976).

The various changes in the physiology of the plants caused by herbicide stress are generally followed by increased insect attack on the plants (Table 1). Sometimes there can be as much as a 3-fold increase in the abundance of insects on a herbicide- stressed plant. Note that in most instances the herbicides that stressed the crop plants were applied at recommended dosages.

In contrast, some reports indicate that insect pest numbers were reduced on herbicide-stressed plants (Pimentel 197 1 ; Campbell 1988). The reduced insect abundance in these instances was attributed to an increase in natural plant toxicants, such as cyanide and potassium nitrate, that was stimulated by the herbicide (Pimentel 197 1).

Based on the many studies dealing with the effects of pesticide treatments on plant physiology and the resulting insect attacks, no general statements as to precise changes can be made. Particular plants, pesticides, and their dosages all influence the nature and extent of changes. However, data

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substantiating the existence of the effects of pesticides are sufficient that each major plant to be treated should be studied to ensure that the crop will not be stressed and made vulner- able to insect attack.

Responses to airborne pollution Evidence suggests that insect populations and their host

plants are stressed by air pollutants and that significant changes in the ecology of both insects and plants may result (Laurence 198 1; Hughes and Laurence 1984; Madden and Campbell 1987; Hughes 1988; MacKenzie and El-Ashry 1988; Heliovaara and Vaisanen 1993). This assessment will focus on the following air pollutants: acid rain, ozone, sulfur dioxide, cadmium (Cd), and lead (Pb).

Acid precipitation The direct effect of acid precipitation on insects is mixed:

some insect populations increase, while under some circum- stances high levels of acidity reduce insect numbers (Heliovaara and Vaisanen 1993). For example, in laboratory tests, when European pine sawfly eggs on Scots pine were sprayed with simulated acid precipitation that ranged from a pH of 2 to 6, and with a distilled water control, the larval hatch increased from about 62 to 78% as the acidity increased (Heliovaara et al. 1992). Although the increased acidity of the pine needles may have helped the survival of the pine sawfly eggs, the investigator reported that the direct application of acid induced some changes in the eggs themselves.

A study by Wolters (1989) showed that the abundance of Collembola, Protura, and Diplura in soil significantly increased at the base of beech trees when acidity increased to a pH below 4. He reported that Collembola and Protura reached their greatest populations in the most acidic soil.

Air pollution, and especially acid rain in nature, changes the pH of soil and the numbers of organisms that exist in it. Huhta et al. (1983) reported that increasing soil acidity from pH 6.9 to 4.5 increased the numbers of oribatid mites and several species of Collembola, although a few species of the Collembola declined in numbers. In contrast, sulfuric acid in rainfall near a Canadian paper mill appeared to reduce ground beetle populations (Freitag and Hastings 1973). Because many ground beetles are predaceous, a substantial reduction in their numbers may cause significant changes in prey insect species populations.

In addition to influencing some insect species directly, acid precipitation may also affect insect populations by altering their sensitivity to common parasitic diseases. For instance, acid precipitation increased the resistance of the European pine sawfly to its nuclear polyhedrosis virus (Neuvonen et al. 1990). Fewer virus infections would enable the sawfly population to increase in number on its host tree.

Acid precipitation has the potential to influence the ecology of host plants, thereby altering the abundance and distribution of the insect herbivore populations associated with the plants. For example, in several studies changes in the susceptibility of a host plant to insect attack resulted from the effects of acid rain because the nutritional quality of the host plant was altered (Sierpinski 1970; Wiackowski and Dochinger 1973; Evans et al. 198 la , 198 1b; Hughes and Laurence 1984; White 1984). Other investigators report that altered chemical toxins and attractants that develop in exposed plants increase plant host susceptibility to insects (Laurence et al. 1983; Hughes and Laurence 1984; Averill et al. 1987).

Hagvar et al. (1976) reported that pines, when stressed by acid rain, appeared to be more susceptible to attack by the pine bud moth. Also, the present decline in sugar maple in eastern Canada is believed to be caused by a complex inter- action of insect damage (tent caterpillar), weather, and stress caused by acid precipitation (McLaughlin et al. 1978; Martin and Brydges 1986). Experiments with fruit trees demonstrated that at a pH less than 3.8, the apple maggot fly was more likely to oviposit on fruit, and thus increase damage (Averill et al. 1987). Aphids on silver birch trees produced 40-100% more progeny when feeding on trees exposed to simulated acid rain with a pH of 3.5 (Neuvonen and Lindgren 1987). Similarly, two pine-feeding aphids, Schizolachnus pineti and Eulachnus agilis, exposed to an acid mist on pines, increased their populations by 33% and more than loo%, respectively (Kidd 1990).

Holopainen et al. (1993) found that sulfur concentrations significantly increased in the needles of Scots pine and Norway spruce growing in the vicinity of a pulp mill. They reported that reproduction in the spruce shoot aphid in June was higher 0.2 and 0.5 km from the pollution site than at more distant sites. However, in mid-July the numbers of aphids started to decline near the pollution source.

Ozone stress Ozone is produced by a series of photochemical reactions

involving nitrogen dioxide, a common air pollutant produced by automobiles. Nitrogen dioxide is converted into nitric oxide by the action of sunlight, freeing an oxygen atom which reacts with oxygen, 0 2 , to form ozone, 03. Most often ozone affects plants but at high concentrations it can also affect certain insects.

Exposure of house flies to high concentrations of ozone for prolonged periods was found to stimulate oviposition, but did not alter other aspects of their growth and survival (Beard 1965). When fruit flies and stable flies were exposed for long periods to high concentrations of ozone, oviposition was stimulated and the number of eggs laid by female flies increased. However, egg hatching decreased by 15%, therefore the numbers of both larvae and pupae were unaffected (Levy et al. 1972).

In general, the effects of ozone on insect populations occur through the impact of ozone on the plant hosts of the insects. For instance, both the western pine beetle and mountain pine beetle were more prone to attack ponderosa pines with ad- vanced symptoms of air pollution injury caused by ozone and other pollutants than unstressed trees (Miller 1983). Trees exposed to high ozone levels appeared to have reduced levels of oleoresin exudate pressure and this tended to make the trees more susceptible to attack by the bark beetles (Cobb et al. 1968a, 1968b; Miller et al. 1968; Stark et al. 1968).

When ornamental milkweed plants were exposed to controlled dosages of ozone, significant changes in soluble carbohydrates, amino acids, cardolides, and phenolics were found in their leaves (Bolsinger et al. 1991). Some of the changes might influence the nutritional quality of the plant and affect insect herbivores. In fact, in a later study, Bolsinger et al. (1991) demonstrated that third-instar larvae of the monarch butterfly significantly preferred the ozone-treated leaves of the milkweed over the untreated leaves.

In laboratory tests, Whittaker et al. (1989) found that chrysomelid beetles (Gastrophysa viridula) fed heavily on the ozone-fumigated plant Rumex obtusifolius. The beetles

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produced more eggs over a shorter period of time than beetles feeding on unexposed plants, and survival through the three larval stages to pupation was significantly greater on exposed plants.

When another chrysomelid beetle, the willow leaf beetle, had a choice, it preferred to feed on the ozone-exposed foliage of eastern cottonwood rather than on the controls (Jones and Coleman 1988). However, female beetles preferred to oviposit on unexposed cottonwood foliage.

Sap-feeding aphids appeared to exhibit mixed reactions to ozone-exposed foliage. Population growth of the blackbean aphid was limited on beans exposed to ozone at 40 nL/L (Braun and Fluckiger 1989). Yet, population growth of another aphid (Phyllaphis fabae) increased on beech exposed to the same dosage of ozone. Blackbean aphid population growth was suppressed on faba beans exposed to ozone at 85 nL/L (Dohmen 1988).

Ozone exposure can also change the acceptability of some trees to insect herbivores. For instance, black cherry is a sub- optimal food source and yellow-poplar an unacceptable food source, for gypsy moth larvae. However, third-instar larvae readily consumed leaves from trees of these two species that had been exposed to ozone pollution (Endress et al. 1991).

Hiltbrunner and Fluckiger (1992) observed that the beech weevil (Rhynchaenus fagi) greatly preferred feeding on beech foliage that had been exposed td ambient air polluted with ozone.These results suggest that trees exposed to polluted-air stress would be subject to greater feeding pressure from wee- vils than trees growing in unpolluted air.

Cadmium stress Cd is readily absorbed by the roots of plants and is trans-

ported from there throughout the plant. The rate of absorption and transport varies among plant species. Cd is toxic to locusts and the toxicity varies with the age and sex of the locusts (Martoja et al. 1983).

Zn in the diet of insects will sometimes reduce the toxic effects of Cd in the food of insects. The growth of confused flour beetle larvae was reduced when the larvae were fed 50 pg Cdlg of food containing minimal levels of Zn, but was normal when the food was supplemented with zinc (Medici and Taylor 1967).

Populations of a collembolan (Orhesella cinta) and an oribatid mite (Platynothrus peltifer) were affected differently when exposed to Cd in their food, green algae (Van Straalen et al. 1989). Although Cd decreased growth in female collem- bolans, it did not adversely affect reproduction by females. In contrast, mite reproduction was reduced by Cd. Cd residues were significantly higher in the mite than the collembolan, and this may be the reason for the reduced reproduction in the mite.

Cd is known to accumulate in some insects, tending to make them more susceptible to subsequent dosages of Cd. Accumu- lation of Cd in the grasshopper Chorthippus brunneus Cd was 10 times that in soil, whereas the level was 7 times higher in the host plant (Hunter et al. 1987). Thus, the grasshopper bioconcentrated Cd via its feeding on the host plant. However, not all insects accumulate Cd. For example, larvae of fruit flies contained Cd concentrations about 20% lower than the level present in their food (Maroni and Watson 1985).

Also, in Sweden, Cd levels were investigated in 14 herb- plant species and in the adults of six species of insects that were feeding on the herbs. Lindqvist (1988) found that the

Cd concentrations in the herbivorous insects were about twice that found in the host plants. As might be expected, predaceous insects feeding on Cd-contaminated prey also accumulate Cd in their bodies. For instance, the predatory beetle Thanasimus formicarius was found to have twice as much Cd as its bark-beetle prey (Vogel 1988).

Lead stress Lead (Pb) is a ubiquitous element in the environment. In

the past, large quantities were released from leaded gasoline, but the change to unleaded gasoline is helping to control this pollution. Apparently some arthropods are sensitive to lead pollution. For example, total arthropod density and biomass were found to be extremely low near a lead mining and smelting complex where the organic litter had high concentrations of Pb (Watson et al. 1976).

Laboratory studies have confirmed that Pb is highly toxic to soil arthropods. For instance, the collembolan Orchesella cincta, when fed Pb-contaminated algae, exhibited reduced growth, respiration, and egg production (Joosse and Verhoef 1983). A number of similar studies with this collembolan confirmed that high levels of Pb in contaminated fungi increased their mortality and reduced growth, reproduction, and overall population growth (Bengtsson et al. 1983, 1985a, 19856).

Conclusion No accurate generalizations can be made concerning the

responses of insect populations to direct environmental stresses from temperature, moisture, and various chemicals found in soil, air, and water. Some populations increase while others decline. The responses are determined by the particular environmental stress and the particular insect species and stage exposed to the stress.

The picture becomes exceedingly complex when the environmental stress is indirect and affects insect populations through their host plants and (or) parasites and predators. Some herbicides, as well as various air pollutants, change the chemical composition of the insects' food and its suitability for their survival. The response of insects to such changes varies with the species of insect and the particular environmental stress and (or) chemical pollutant. Sometimes insects prefer to feed on the affected vegetation; in some cases the exposed foliage appears more nutritious for insects and as a consequence, their populations may increase to outbreak levels.

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Insect population responses to environmental stress and pollutants