Of all environmental variables that affect contaminant toxicity to vertebrates, temperature has received more attention than any other. For example, a 1972 bibliography on the effects of tem- perature on fish compiled by Raney et al.5 contains more than 4000 references, and the present number is at least an order of magnitude greater. Guidelines for deriving temperature criteria for freshwater fish were prepared by Brungs and Jones6 and Houston.7 The latter reference also addresses the interactions of temperature and chemical toxicity, a subject reviewed in detail by Cairns et al.8 and Sprague.9 Information available for terrestrial vertebrates focuses more on effects of drugs than environmental contaminants.2 Our current understanding indicates that generalizations cannot be made across classes of contaminants. In part, this is because temperature can be both a lethal factor and a controlling factor, acting on a variety of biological processes such as metabolism.
23.2.1.1 Aquatic and Amphibious Forms
All fish, except large tuna and some sharks, are poikilothermic (ectothermic). Thus, body temperature tracks the environmental temperature rather precisely with little lag, even when tem- perature changes rapidly.10,11 The temperature tolerance zone varies greatly among species and to a lesser degree with the age, physiological condition, and temperature to which the fish has been acclimated.7,12 Exposure to sublethal concentrations of toxicants may reduce the upper and raise the lower lethal temperature thresholds of fish, thereby constricting the tolerance zone.13–17 Since fish show reduced growth and impaired swimming ability when subjected to the extremes of their temperature tolerance zone, sublethal concentrations of toxicants could have greater effects on these functions at these extremes.18
Because body temperature of a fish tracks that of the environment, many metabolic processes exhibit a direct relationship to environmental temperature. As a general rule, energy metabolism increases about twofold with every 10°C rise in temperature. This requires gill ventilation to rise proportionately to meet increased metabolic demands.19 A rise in water flow over the gills results in more rapid uptake of toxic chemicals through the gills, the major uptake route of waterborne
Figure 23.1 Physical and natural factor interactions with contaminants in an aquatic ecosystem. (Modified from Foran, J.A. and Ferenc, S.A., Eds., Multiple Stressors in Ecological Risk and Impact Assessment, SETAC Press, Pensacola, FL, 1997.)
Energy source
Habitat/
Geomorphology Contaminants
Temperature
DO Salinity
Water hardness Radiation
pH Photoperiod/Season
Hydrodynamics Biological
interactions Response of a values ecosystem component
chemicals in freshwater fish and to a lesser extent in marine species.20,21 It thus could be assumed that higher temperatures would result in greater toxicity at a constant chemical concentration in the water. However, this assumption is unwarranted. Although there are numerous examples of acute toxicity being directly proportional to temperature, there are also cases (especially with chronic exposure) where the opposite occurs, or where temperature has no effect on contaminant toxicity.22 This is because detoxication and excretion processes also increase with temperature, sometimes at rates equal to or exceeding contaminant uptake. It is important to note that rapid temperature changes coupled with toxicant exposure have more profound effects than responses observed when fish are first acclimated to the extreme temperature and then challenged with the toxicant.7,20 However, due to limited data on rapid temperature changes, in the discussion that follows, nearly all studies reviewed utilize thermally acclimated fish.
23.2.1.1.1 Acid
Although literature on acid toxicity to fish is extensive, information on the modulating effect of temperature is relatively scarce.23 In general, the higher the temperature, the shorter the survival time in a lethal pH for common carp (Cyprinus carpio) and brook trout (Salvelinus fontinalis).24,25 Elevated temperature had the same effect on survival when the median lethal pH was estimated for rainbow trout (Oncorhynchus mykiss) fingerlings.26 However, embryos of trout in this study exhibited the opposite response to temperature extremes (i.e., acidity was more harmful at low temperatures). This was attributed to prolonged incubation time at lower temperature, and thus there was more opportunity for the acid to exert effects on the developing embryo.
23.2.1.1.2 Ammonia
The toxicity of ammonia to fish is influenced greatly by pH and temperature because both factors affect ammonia ionization. Ionized ammonia (NH4+) has relatively little toxicity (however, see Section 23.2.2.1. on pH effects), whereas the unionized form (NH3) is highly toxic. A 10°C rise in temperature at any given pH results in a threefold increase in formation of unionized ammonia.27
In most ammonia toxicity studies, however, the unionized ammonia concentration is the only value reported. Under these circumstances, there is little effect on toxicity at temperatures above 10°C in freshwater fish, but at lower temperatures ammonia is actually more toxic.28 Hazel et al.29 found no temperature effect of ammonia on three-spined sticklebacks (Gasterosteous aculeatus) in freshwater, but when this euryhaline species was tested in brackish water or seawater, unionized ammonia was much more toxic at the higher temperature. However, in this same report, temperature had no effect on ammonia toxicity at any salinity to another euryhaline species, the striped bass (Morone saxatilis), so test species differences appear critical.29
23.2.1.1.3 Chlorine
Chlorine is used extensively as a biocide to prevent fouling of industrial and electric-power- generating cooling systems and as a disinfectant for municipal sewage discharges. In general, it is more toxic at higher temperatures during continuous exposure.30 However, many electric-power- generating facilities chlorinate intermittently (two or three times each day), thereby exposing the nontarget organisms to pulses of chlorine. Heath,31 using a laboratory simulation of this regime, found that temperature had little effect on chlorine toxicity for a wide variety of cold- and warmwater fish species. Instead, the fish species and form of chlorine (i.e., free chlorine vs. monochlora-mine) were much more critical in determining relative toxicity.
23.2.1.1.4 Cyanide
This highly toxic chemical appears to kill fish more rapidly at high temperatures, but only when acutely lethal concentrations are tested.8 Death occurs more rapidly at high temperatures because
uptake is rapid and metabolic demand is accelerated, while aerobic metabolism is blocked by cyanide. At acutely toxic cyanide concentrations, detoxication mechanisms are probably over- whelmed. At lower concentrations, temperature may have no effect on time to death. Fish are able to tolerate moderate concentrations of cyanide at high temperatures, probably because detoxication mechanisms (e.g., rhodanase enzyme activity) are also highly temperature-dependent. Rainbow trout are an important exception; cyanide toxicity (96-hour LC50 estimate) decreases at elevated temperatures.32
23.2.1.1.5 Metals
Despite the abundance of information on the toxicity of metals to fishes, relatively little work has been conducted on interactions with temperature. Arsenic can exist in waterways in several forms, but the most stable form is arsenate. Rainbow trout are more sensitive to acute doses of this metalloid at 5°C than at 15°C, but the reverse occurs with chronic arsenate exposure.33 Evidently, a critical body burden of arsenate must be achieved to cause death, which occurs more rapidly at warmer temperatures because of enhanced uptake rate. At lower exposure concentrations (when detoxication mechanisms are not overwhelmed), elevated temperature facilitates detoxication and excretion processes, thereby delaying or preventing accumulation of the lethal body burden.33
Zinc toxicity increases or is unaffected at high temperatures.8 The definitive study by Hodson and Sprague34 provides the probable explanation for the variety of responses reported in earlier papers. Using Atlantic salmon (Salmo salar) as a model, they concluded that fish were more sensitive to zinc at high temperatures, when exposures were at high concentrations and of short duration. As exposure duration was extended, temperature effects were progressively reduced until, at 2-week exposures, the LC50 was higher (less toxic) in warm water, a phenomenon similar to that seen with cyanide and arsenate. The mechanisms for the temperature effect may not be the same, however. Zinc causes death by destroying gill tissue. It was found that cold-acclimated fish expe- rienced more gill damage from low doses of zinc than did warm-acclimated fish, even though the latter had greater concentrations of zinc in the gills.34
Whereas fish are more sensitive to arsenate and zinc at cold temperatures, cold-acclimated (6°C) trout exhibited a threefold greater 10-day lethal threshold for cadmium compared with fish at 18°C.35 The elevated toxicity of cadmium at the higher temperature was correlated with enhanced plasma calcium suppression by cadmium. Hypocalcemia is a key mechanism of cadmium toxicity to fish.21 In addition, Eisler reported a threefold increase in toxicity of cadmium at 20°C compared to 5°C for mummichog (Fundulus heteroclitus).36
Because cadmium appears to be more toxic at higher temperatures, one might expect that fish would seek cooler water when exposed to cadmium. Contrary to expectations, brown bullhead (Ictalurus nebulosus) actually moved to a markedly higher temperature following cadmium expo- sure.37 The investigators hypothesized this response to be a mechanism compensating for cadmium- induced suppression of ventilation. Whereas most metals, including cadmium, cause an elevation in gill ventilation, such a response in the bullhead may be an exception.21
The effect of temperature on cadmium toxicity in tadpoles (Bufo spp.) would appear to be the reverse of that in fish. Ferrari et al.38 found that a mere 5°C rise in temperature (20–25°C) caused an approximate doubling of the cadmium LC50. This was attributed to enhanced detoxication mechanisms in the higher temperature, although no data were presented to test this hypothesis.
Despite the large amount of data available on copper toxicity, there is little information on interactions with temperature. Based on 96-hour LC50 estimates, copper-temperature interactions are insignificant for several species of teleosts.39 However, Dixon and Hilton40 observed that a high carbohydrate diet in trout increased the chronic toxicity of waterborne copper and that reduced temperature exacerbated this effect.40 In another study, Felts and Heath41 found that sublethal copper exposure of bluegills (Lepomis macrochirus) delayed metabolic acclimation to temperature change.41 Further study of copper-temperature interactions in fishes are warranted.
Mercury and lead exhibit elevated toxicity at higher temperatures, apparently due to a direct relation between metal accumulation and temperature.42,43 Mercury accumulates twice as fast with a 10°C rise in temperature.44 Metabolism (and therefore gill ventilation) show a similar rate of increase with temperature, which probably facilitates the uptake; however, excretory processes for mercury and lead may fail to rise at a comparable rate. Part of the detoxication process involves binding of the metal to metallothionein.21 Most measures of tissue accumulation do not differentiate between metal bound to metallothionein and that free in the cells, and thus there may not be a direct correlation between body burden and lethality. The greater accumulation of lead and mercury at high temperatures has relevance for predatory animals, including humans, that consume contaminated fish.
23.2.1.1.6 Organics
Polychlorinated biphenyl (PCB) accumulation rates are enhanced by increased temperature. Spi- garelli et al.45 explored this relation in adult brown trout (Salmo trutta) in both constant temperatures and a diel temperature cycle. About 90% of the PCB was taken in by ingestion of food and the remainder via gills. The accumulation rate followed the growth rate, and both responded to temperature as if the fish had been acclimated to the peak of the diel cycle. Such a finding would be interesting to test with other contaminants, including metals, because diel cycles are common in nature.
Among organic pesticides, organochlorine compounds are generally more toxic to fish than organophosphorus compounds.46 DDT has been reported to be more toxic at low temperatures in the laboratory. Decreased water temperature in streams two or three months after application can result in delayed mortality of trout.47,48 DDT also causes trout to choose warmer temperatures, although at high concentrations they may actually prefer cooler temperatures.49 Eisler50 found that the 96-hour mortality of Fundulus heteroclitus at a given DDT dose was least at 20°C and rose at temperatures above and below 20°C, suggesting the existence of a temperature optimum for minimal toxicity in that species.
Methoxychlor is also more toxic to fish in cold water.51 Such an interaction with temperature may be limited to salmonids. In tests with lindane, Johnson and Finley report a 2.3-fold decrease in toxicity to rainbow trout with increasing temperature from 2 to 18°C, but the opposite occurred in bluegills (a warmwater centrarchid) over a temperature range of 7 to 29°C.52 Macek et al.51 tested effects of four other organochlorine insecticides on bluegills and trout, and found that all the compounds to be more toxic (96-hour LC50 estimates) at high temperatures. In European eels (Anguilla anguilla), the highest LC50 estimate for lindane was at 22°C, while greater lindane toxicity was observed at 15 and 29°C.53 Thus, temperature effects on organochlorine pesticide toxicity are highly dependent on the species of fish and compound tested.
Although some organochlorine compounds are more toxic at cold temperatures, the opposite occurs for organophosphorus compounds.47,52,54,55 This is also true for carbaryl (a carbamate), although there are also marked species differences in temperature modulation of its toxicity.52 The time-course of temperature acclimation may be an important factor because the action of organo- phosphorus and carbamate insecticides is to inhibit acetylcholinesterase in nervous tissue, and the activity of this enzyme changes during the temperature-acclimation process in fish.56
Pyrethroid exposure studies in fish have demonstrated increased toxicity with reduced water temperature.57,58 One of the most pronounced thermal effects was seen with permethrin (a synthetic pyrethroid) exposure of rainbow trout wherein the 96-hour LC50 rose tenfold over a temperature range of 5 to 20°C.58 Thus, higher temperatures are clearly protective for this compound in trout.
Similar types of studies in amphibians have yielded somewhat inconsistent findings. Lethality of several pyrethroids in adult Rana pipens was noted to be dramatically enhanced by cold temperature (4 vs. 20°C).59 Using behavioral endpoints, recovery of newly hatched Rana clamitan and Rana pipiens tadpoles following sublethal exposures to permethrin and fenvalerate was slower at 15 vs.
20°C.60 In contrast, a moderately cool temperature (18 vs. 22°C) actually lowered lethality of esfenvalerate in tadpoles (Rana spp.).61
The cytochrome P4501A enzymes are an important detoxication mechanism for organic con- taminants in fish, and these enzymes are inducible by the presence of many toxic substances.62 Strong induction was detected in both winter- and summer-acclimated arctic char (Salvelinus alpinus);
however, the response was delayed and longer-lasting in the cold.63 It should be noted that species differences may be very important here, for Machala et al.64 found that acclimating carp (a warm- water species) to winter temperatures caused a “highly significant inhibition” of the induction process.
23.2.1.2 Terrestrial Forms
Ambient temperature influences the toxicity of contaminants in homeotherms by affecting metabolic rate, energetics, neural control of thermoregulatory function, and contaminant uptake, transformation, and detoxication. For many pollutants, toxicity is lowest within the thermoneutral zone and tends to increase outside this range, thereby exhibiting a “U-shaped” response curve.
23.2.1.2.1 Petroleum Crude Oil
Spillage of oil during transportation and discharge of petroleum hydrocarbons as industrial effluent frequently result in the exposure of birds externally, by the oiling of plumage, and internally, through the ingestion of oil while feeding or preening. Direct external exposure is probably the most important toxic effect because oiling of feathers causes insulating air to escape, resulting in loss of body heat and increased metabolic rate.65–68 Under such physiological conditions, birds exposed to low ambient temperatures (e.g., cold water or air) rapidly deplete their energy reserves and become hypothermic, which can lead to death. Ingestion of oil may alter metabolic rate in seabirds67 but does not seem to affect metabolic rate in domestic ducks (Anas spp.).69 Nonetheless, mild cold exposure seems to exacerbate the toxicity of chronically ingested crude oil in mallards (Anas platyrhynchos).70 Studies in England have revealed that avian mortality associated with oil pollution rises from a minimum in the summer to a peak in late winter.71
External oiling of wild mammals (e.g., sea otter, Enhydra lutris; polar bear, Urus maritimus) increases thermal conductance across the insulating fur layer, resulting in substantial heat loss; this is compensated by an elevated metabolic rate.72 Thermal effects have been predicted to be substan- tially greater upon exposure to cold air or water, although polar bears have exhibited a marked increase in core temperature following external oil exposure that might reflect a febrile response.
23.2.1.2.2 Organochlorine Contaminants
In Columbiformes and gulls (Larus fuscus), ingestion of DDT and PCB were associated with reduced metabolic rates, whereas elevated metabolic rates were reported when these compounds were fed to northern bobwhite (Colinus virginianus).73–76 Cold exposure following ingestion of 100 parts per million (ppm) DDT significantly decreased survival of quail.76 This response was attributed to the mobilization of stored DDT and its metabolites. Based upon egg loss in a ruffed grouse (Bonasa umbellus) population following a DDT spray, cool weather has been suggested to act synergistically on DDT toxicity.77 A retrospective study of the relationship between organochlorine contaminant concentration in herring gull eggs (Larus argentatus) and cold weather in the Great Lakes between 1962 and 1995 indicated that PCB levels were positively correlated with winter severity.78 This relation appears to reflect altered migratory and feeding behavior, as gulls move to more highly contaminated southerly Great Lakes locations during severe winters and apparently ingest larger quantities of fish.
23.2.1.2.3 Organophosphorus and Carbamate Pesticides
Studies with laboratory rodents show that the toxicity of cholinesterase-inhibiting pesticides are enhanced several fold at reduced and elevated ambient temperature.79,80 Considerable evidence indicates that this effect is due to disruption of central cholinergic and monoaminergic thermoreg- ulatory function, endocrine dysfunction, and altered pesticide absorption.81 Furthermore, ambient temperature has long been recognized to affect the environmental half-life of these pesticides when sprayed on crops.82
Juvenile northern bobwhite (C. virginianus) and mallard ducklings (A. platyrhynchos) acutely or subchronically exposed to anticholinesterase compounds (e.g., carbofuran, chlorpyrifos, teme- phos) exhibit decreased survival rates when maintained at low ambient temperatures compared with thermoneutral controls.83–85 A twofold increase in parathion lethality has been observed in northern bobwhite (C. virginianus) and Japanese quail (Coturnix japonica) maintained within environmental chambers at ambient temperatures below or above the thermoneutral zone.81,86 At sublethal parathion dosages, heat-exposed quail exhibited greater brain acetylcholinesterase inhibition than similarly dosed quail exposed to cold or maintained at thermoneutral temperatures. In contrast, recovery of brain acetylcholinesterase activity in brown-headed cowbirds (Molothrus ater) receiving dimethoate was actually slower in cold-exposed birds compared to thermoneutral controls.83 These alterations in toxicity are attributed to disruption of thermoregulatory function, as evidenced by hypothermia, and other metabolic and endocrine responses to heat and cold but not to effects on the activities of hepatic enzymes involved in anticholinesterase activation or detoxication (e.g., parathion oxidase, paraoxonase, and paraoxon deethylase).81,85,87,88 The circannual toxicity of parathion was investi- gated in European starlings (Sturnus vulgaris) housed in outdoor pens encountering a wide-range of temperatures during winter, spring, summer and fall.89 Based upon the acute LD50 of parathion, toxicity was greater during hot summer weather compared with cool winter weather (LD50 of 118 vs. 160 mg/kg).
In a field setting, low temperatures contributed to the poisoning of about 1500 geese (Anser anser and A. brachyrhynchos) that fed upon carbophenothion-treated winter wheat, and elevated ambient temperature was suggested to have been an exacerbating component in a sage grouse (Centrocercus urophasianus) die-off following dimethoate treatment of alfalfa in Idaho.90–92
Temperature-contaminant interaction studies in wild mammals are quite limited. Acute oral exposure to parathion has been demonstrated to evoke hypothermia in white-footed mice (Peromys- cus leucopus); however, parathion toxicity was not affected in mice maintained at 10°C, possibly because of their ability to undergo facultative torpor.93
23.2.1.2.4 Lead Shot
Lead poisoning from ingested shot is a major cause of waterfowl mortality throughout the world. In North America, most waterfowl that die from ingested lead shot succumb during the cold weather that accompanies the hunting season. Harsh winter weather is generally thought to exac- erbate lead toxicity in birds. This has been confirmed in part by studies of Kendall and Scanlon94 with ringed turtle doves (Streptopelia risoria); marked mortality and greater blood and liver lead concentrations were observed in doves exposed to 6°C compared with birds maintained at 21°C.
Comparison of lead-shot toxicity (mortality and body weight change) to mallards (A. platyrhynchos) and black ducks (Anas rubripes) housed outdoors in winter- and summer-dosing trials suggest that shot toxicity was greater in winter.95 Ambient temperature does not seem to affect the toxicity of alternative shot (e.g., bismuth, tungsten, tin) used for hunting of waterfowl in North America.
23.2.1.2.5 Other Contaminants
Temperature influences the toxicity of sodium monofluoroacetate (compound 1080), a com- monly used rodenticide. When compared to thermoneutral controls, acute toxicity was greater at