Tipping Points and Indicators Fact Sheet - Copper
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47906
COPPER IN A NUTSHELL:
• Copper negatively effects fish and macroinvertebrates in various body systems across multiple life stages
• Copper exposure depresses liver and immune system function in various fish species
• Some behavioral changes in fish from copper exposure include increased prey handling time (which ultimately decreases growth rate), altered locomotor activity, as well as altered migration patterns
• In metal combination tests (i.e. where fish are put into tanks that have mixtures of various heavy metals), copper exerts the most toxic effects
• Fish have the ability to adapt to chronic copper exposure, however, it is metabolically expensive and take away energy that would otherwise be allocated towards increased growth or reproduction
Copper is an important trace metal and is required for normal physiological function in animals in miniscule concentrations. However, in larger amounts, its general effect is detrimental to physiological development and function in organisms. Waterborne concentrations of copper are often the result of human activity, such as mining (Heath 1995). Arrays of biomonitoring and toxicological studies have revealed that waterborne copper has several negative effects on freshwater aquatic organisms, such as fish and benthic macroinvertebrates.
Toxicological studies on benthic macroinvertebrates have shown that copper negatively affects various life history stages, often affecting some if not all of them, depending on how tolerant the organism is. For example, multiple species in subclass Oligochaeta have reduced survival, increased mortality, decreased growth or development, and decreased reproduction or emergence (of larva). In the more tolerant taxa Family of Chironomidae, fewer of these life history traits are affected (Anderson et al. 1980, Bonacina et al. 1987, Widerholm et al. 1987)
In fish, copper has been linked to observed damages in various body systems and functions such as the reproductive system, the immune system, liver functions, and sight across multiple life stages. The larval stage of fish has often been identified as the most sensitive stage in development (META SOURCES). In larval striped bass, copper has been reported to cause damage to the cornea (Bodammer 1985).
In spawning fathead minnows, egg production was severely reduced at copper concentrations that had little or no effect on eggs, fry, or adults (Mount 1968). Kumar and Pant (1984) found that 2-4- month exposures of an Indian teleost to copper cause histopathological changes in both testes and ovaries. Copper can cause the disappearance of oocytes in ovaries.
In hatchlings, von Westernhagen (1988) discovered that copper causes considerable effects on viable hatch, which refers to the number of emergent fish larvae, at concentrations as low as 30-90ug/L in both fresh and saltwater. Compounding this is that copper transfers readily from the mother fish into her eggs (Coyle et al. 1993), which may further limit viable hatch.
Depressed immune system function in relation to copper exposure has been detected in various fish species. Immunosuppression of antibody-producing cells in rainbow trout was discovered when tested in vitro (Anderson et al. 1989) and air-breathing catfish exposed to copper at several very low concentrations for 28 days exhibited a dose-dependent depression of antibody production, phagocytic activity of spleen and kidney macrophages, and prolonged eye allograft rejection time (Khangarot and Tripathi 1991), the last indicating suppression of T-cell activity. Zebrafish exposed to copper or zinc at several different concentrations for 7 days, displayed a dose-dependent suppression of kidney lymphocyte number and natural cytotoxic cells. Copper was more potent at the aforementioned suppression. Additionally, copper caused marked decrease in macrophage activity both in vitro and in vivo.
Liver functions were also damaged at relatively low copper concentrations; 0.05 or 0.1mg of Cu/L for 4-7 days caused a variety of alterations in liver cellular structure revealed by transmission electron microscopy (TEM) in livers of the snake-headed fish (Khangarot 1992). These changes included extensive proliferation of smooth endoplasmic reticulum (ER), dilation of rough ER (RER), loss of mitochondrial structure, proliferation of lysosomes, and accumulation of electron dense bodies. The most dominant changes were those of the RER and mitochondria. Khangarot attributed the RER changes with detoxification activities while mitochondrial changes were interpreted as clearly pathological (these two changes most dominant). Additionally, sublethal levels of waterborne copper cause a small but consistent rise in the water content of muscles and/or livers of freshwater fish (Heath 1984). In bluegills, exposure to sublethal concentrations of copper was followed by hypoxic stress similar to what might be experienced in a pond becoming hypoxic at night. In general, copper caused a more severe response to the hypoxia-like conditions caused by copper and delayed recovery after copper levels subsided. (Heath 1991).
Several behavioral changes were also observed in various species of exposed freshwater fish. Bluegill exposed for 4 days to 4 concentrations of copper ranging from 5-1700ug/L showed altered predation behavior in terms of prey handling time. Prey handling time is the interval between when prey items are eaten and the fish begins to hunt another item. In this experiment, 2 species of Daphnia, an amphipod, and two sizes of zygoptera were used as prey. Both copper-treated and untreated prey was tested. Prey handling time was the most consistent parameter altered and increased significantly with increasing copper concentrations, and caused overall consumption rate of prey to go down in a dose-dependent fashion, ultimately depressing growth rate (Sanheinrich and Atchison 1989).
The effect of locomotor activity appears to vary with species. At low sublethal concentrations, copper stimulated locomotor activity in brook trout (Drummond et al. 1973). Henry and Atchison (1979a, 1979b, 1986) used a variety of body movements of bluegill as indicators of sublethal concentrations of Zn, Cu, Cd. Coughs, yawns, jerk swimming, fin flickering, agonistic behaviors, and chafing against objects were counted visually and found to increase in a dose-dependent manner. Species differences also occurred in the data on angular orientation, which, according to authors, is probably controlled by different neurophysiological mechanisms.
Avoidance behavior of copper is complicated (Steele et al. 1990), affecting the attraction of fish to other compounds. For example, Alanine is a ubiquitous constituent of prey odor, which attracts predator fish. Fish would avoid Cu at levels of 10 ug/L, however fish would not avoid 10ug/L Cu combined with alanine. In contrast, a copper concentration of 1ug/L suppressed attraction to alanine. Giattina et al. (1982) also found conflicting avoidance behaviors in rainbow trout; namely, high copper concentrations attracted rainbow trout, while low ones caused avoidance behaviors. For example, fish exhibited avoidance at concentrations well below the 96-h LC50 (acute values). This corresponds to the notion that copper is avoided at very low concentrations by fish whereas high concentrations or steep gradients may actually cause attraction. Atchison et al. (1987) found that avoidance behaviors may occur even at the LOEC (lowest observed effective concentration), as determined by today’s standard chronic tests. It seems that fish possess an ability to sense the presence of some metals at really low concentrations and in some instances at a concentration below that which causes reductions in reproduction (Heath 1995).
Copper avoidance behaviors also affect migration patterns. Sprague (1967) reported that adult Atlantic salmon on their upstream migration actively avoided areas contaminated with copper and zinc at concentrations that were clearly sublethal. Based on both field and lab data, they concluded that concentrations above 38ug/L Cu (and 480ug/L Zn) would effectively block migrations. Similarly, Sutterlin and Gray (1973) found that copper concentrations as low as 44ug/L have been shown to change the attractiveness of homestream water to migrating salmonids. In experimental studies, copper has been shown to alter olfactory response of fish, and 44ug/L is well above the threshold for causing inhibition of olfaction sensitivity, which may explain the avoidance behavior of salmonids. Estuarine fish exposed to high doses of copper (0.5-5mg/L Cu) exhibited histological lesions of the olfactory mucosa (Gardner and LaRoche 1973). At lower doses, it is thought that copper inhibits the ability of receptor cells to convert the presence of smells into nerve impulses (Winberg et al. 1992).
In addition to receptors for smell, the function of taste receptors is also blocked by copper (Sutterlin and Sutterlin 1970), and therefore is thought to have a broad inhibitory effect on chemoreceptors. While increasing the calcium level (i.e. hardness) in water reduces the inhibitory effect of copper on the receptor function of the olfactory bulb (Bjerselius et al. 1993), natural water bodies host an amalgam of contaminants, that when interacting together with copper, increase the toxicity of copper.
Studies involving combinations at realistic concentrations of various trace metals (Al, Cd, Cu, Fe, Pb, Ni, Zn) indicate that some combinations are far more toxic than others. Combinations involving either aluminum or copper were most harmful, with copper being worse than aluminum (Sayer et al. 1991). Combinations of chemicals also cause fry to have reduced whole-body calcium, sodium, and potassium content. The good news is that fish show adaptive physiological responses after copper exposure; fish sampled from areas along the coast of Spain contaminated with iron, copper, and other heavy metals exhibited elevations in antioxidant enzymes when compared with a reference site (Rodriquez-Ariza et al. 1993). These observations exemplify the important concept that toxic chemicals may induce various types of biochemical changes in fish, who in turn, can adapt to chemical stressors. These include detoxification of enzymes such as those associated with cytochrome P450, metallothionein (MT), and the antioxidant enzymes described here (Heath 1995). Fish exposed to copper also have relatively fast detoxification rates after being placed in clean water. However, these physiological adaptations are metabolically expensive, and take away energy that would otherwise be allocated to further growth and/or reproduction. Also, given the synergistic interactions of copper with other metals, it is not clear whether these adaptations will be adequate enough to cope with enhanced toxicity.