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- Materials and methods
In most chemical regulatory schemes, effects on populations of aquatic invertebrates are generally inferred from chronic or long-term studies (e.g. a Daphnia sp. 21-day reproduction study, OECD 1998; and a Chironomus sp. 28-day emergence study, OECD 2001) that examine the effects of a toxicant on the survival, growth and/or reproduction of an individual. However, the results of these studies are not usually expressed in terms of population growth rate (PGR), the usual ‘currency’ of population ecologists. Some researchers use life table response experiments (LTRE; Allen & Daniels 1982; Bechmann 1994; Levin et al. 1996) to examine toxicant effects on PGR, but in the majority of these studies organisms are exposed individually or at low density and are provided with adequate food. In contrast, most natural populations are regulated by density dependence and fluctuate around the environmental carrying capacity as a result of individual competition for resources. Because ecotoxicology aims to make reliable population projections of toxicant impacts in the field, an understanding of how resource-limited or high-density populations respond to environmental chemicals is essential and should be considered in ecological risk assessments (Sibly 1999a).
In general, increasing density and increasing chemical concentration reduce PGR when applied separately (Sibly & Hone 2002) but few studies have investigated how populations respond to both stressors when applied simultaneously. Concerns arise because populations regulated by density dependence have fewer resources and therefore less energy available for defence against environmental stress, and so may be more susceptible to toxicant stress (Sibly 1999b). LTRE carried out at low densities may therefore underestimate the population response to chemical stress. However, simulation studies indicate that when survival or production rates are density dependent, mortalities caused by the toxicant may alleviate the intensity of the density dependence because more resources per capita would be available to the survivors (Calow, Sibly & Forbes 1997; Grant 1998; Hansen, Forbes & Forbes 1999). Consequently, resource-limited or high-density populations may compensate for the negative effects of a chemical stressor. LTRE may therefore overestimate toxicant effects on field populations.
In a recent review, Forbes, Sibly & Calow (2001) considered the possible ways in which density dependence (operating mainly via food limitation) and toxicants may affect PGR. They described three general types of interaction: additive, less than additive and more than additive. In the additive model, the combined effects of density dependence and toxicant concentration are independent (i.e. no interaction). In the less than additive model, toxicant effects are buffered or compensated. Conversely, in the more than additive model toxicant effects are exacerbated at high density.
The aim of this study was to measure the joint effects of population density and chemical stress on the life history and PGR of an important ecotoxicological indicator species, Chironomus riparius Meigen, under controlled laboratory conditions. The synthetic pyrethroid cypermethrin was selected as the chemical stressor. Pyrethroids have been widely used for more than 20 years to control insect pests in a variety of crops. The toxicity, behaviour and fate of these lipophilic insecticides have been well studied in both the laboratory (Stephenson 1982; Sakata et al. 1986; Maund et al. 2002) and in the field (Crossland, Shires & Bennett 1982; Hill, Shaw & Maund 1994; Farmer, Hill & Maund 1995). Pyrethroids have a short half-life in the water column (generally less than 2 days) and rapidly adsorb to suspended particulate material and sediments, which greatly reduces their bioavailability to water column organisms. However, the potential exists for benthic organisms like C. riparius to be exposed by direct contact or ingestion of contaminated sediment particles or via the interstitial (pore) water. We hypothesized that high-density C. riparius populations exposed to cypermethrin in a sediment–water test system would compensate for the initial mortalities caused by the toxicant (as in the less than additive model) because more resources (food and space) would be available to the survivors.
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- Materials and methods
We aimed to determine the joint effects of population density and 14C-cypermethrin on the life history and PGR of C. riparius under controlled laboratory conditions. Increasing density had a negative effect on PGR, whereas exposure to increasing chemical stress had a positive effect on PGR when populations were initiated at high density. These results support the hypothesis that high-density or resource-limited populations compensate for toxicant effects, as in the less than additive model outlined by Forbes, Sibly & Calow (2001).
In agreement with a previous study (Hooper et al. 2003), increasing density had a negative effect on all the measured life-history traits of C. riparius. Exposure to 14C-cypermethrin had a direct negative effect on juvenile survival, presumably within the first 24 h of exposure, because the chemical rapidly dissipated from the water column. A reduction in the initial larval densities resulted in an increase in the available resources (food and space) for the survivors, which emerged sooner and started producing offspring earlier than the control populations. The chemical stressor therefore had an indirect positive effect on juvenile development time when populations were initiated at high densities. Regardless of density, exposure to 14C-cypermethrin had no significant effect on estimated fecundity, the number of offspring per population and adult body weight.
At low density, juvenile development time was unaffected by the pesticide and the survivors emerged at a similar time (day 15–17). However, toxicant-related mortalities were compensated for by breeding earlier, which resulted in similar estimates of PGR at low density. It has been reported that in most chironomid species females emerge with eggs that are one-third to one-half developed (Oliver 1971). As the exposed females reached the critical body size (Hooper et al. 2003) within the hypothesized minimum juvenile development period, the increase in resources and therefore energy (as a result of toxicant-related mortalities) may have been diverted towards egg maturation, thus allowing reproduction to occur sooner.
The data reported here are in broad agreement with observations of chironomid populations in mesocosm studies. In a study where cypermethrin was sprayed over the surface of mesocosms, equivalent to spray drift following application at the typical field rate, concentrations in water samples taken 1 h after application were around 0·03 µg l−1 and after 24 h had declined to about 0·009 µg l−1 (Farmer, Hill & Maund 1995). These measured concentrations and the reported effects on chironomid populations are comparable with the present laboratory study in that exposure to cypermethrin initially reduced the number of larvae but recovery was rapid and 8 weeks after application estimated densities were up to three times higher in the treated mesocosms than the controls (Farmer et al. 1995).
Previous work has shown that when food alone is limiting, laboratory populations of C. riparius buffer the effects of a chronic stressor, cadmium (Postma et al. 1994). Exposed food-limited populations attained a higher PGR than the food-limited controls because mortalities occurred during the early larval stages, leaving more food for the survivors as reported here. In contrast to our results, food-limited populations compensated for the negative effects of cadmium by an increase in the fecundity of the surviving females (Postma et al. 1994), not by a reduction in juvenile development time. Interestingly, PGR declined with increasing cadmium concentrations when populations were well fed, as mortalities occurred during the late juvenile stages and juvenile development time increased with cadmium concentration (Postma et al. 1994).
Results from the present study and Postma et al. (1994) suggest that high-density or food-limited C. riparius populations buffer or compensate for the effects of both acute (cypermethrin) and chronic (cadmium) chemical stressors, although different life-history traits are affected. Perhaps this is not surprising as Forbes & Calow (1999) found no consistent pattern in the data obtained from 41 experimental studies (mostly on cladocerans) regarding which life-history traits were most or least sensitive to toxicant exposure. Because our prime interest was in determining the population response using an efficient experimental design, our method did not allow detailed schedules of individual life-history traits to assess directly their relative sensitivities across treatments and their contribution to PGR.
Cadmium has been the model chemical stressor in a number of laboratory studies examining the response of food-limited cladoceran populations. Less than additive effects on PGR were reported for Daphnia galeata mendotae (Marshall 1978) and Moinodaphnia macleayi (Barata, Baird & Soares 2002). In both studies, food-limited populations compensated for the cadmium-related mortalities in the same way as C. riparius (Postma et al. 1994), by an increase in the reproductive rate of the survivors. However, cadmium effects on other food-limited cladocerans, Daphnia magna (Kluttgen & Ratte 1994) and Echinisca triserialis (Chandini 1988), were additive and more than additive, respectively. We have some confidence in ignoring the Kluttgen & Ratte (1994) study, as the daphnids were exposed individually so mortality effects at the population-level were not incorporated in the experimental design. In Chandini's (1988) study, cadmium concentration had little effect on PGR when food was available but PGR declined with increasing concentration when food was limited, mainly due to a decrease in the reproductive rate. Although toxicant-related mortalities resulted in more food per surviving individual, Chandini (1988) concluded that cadmium stress suppressed the feeding rate of the survivors. The joint effects of density dependence and chemical stress may therefore differ among closely related species and may also differ with toxicant concentration, as observed in the marine polychaete Capitella sp., exposed to fluoranthene (Linke-Gamenick, Forbes & Sibly 1999). The joint effects were less than additive at low concentrations and more than additive at high fluoranthene concentrations, as reproduction was completely inhibited (Linke-Gamenick, Forbes & Sibly 1999).
From an increasing number of recent studies of the joint effects of density and chemical stress it is beginning to appear that population density may modify toxicant effects and often, although not always, toxicant effects are compensated for when resources are initially limiting, as in the less than additive model. In general, low levels of chemical stressors may paradoxically increase carrying capacity (density when PGR = 0) by reducing juvenile competition for resources, so more and perhaps better quality or fitter adults are produced. This is similar to the effects of predators and culling, which may directly improve the quality of prey populations (Cox 1993). However, toxicant exposure may result in survivors that are less tolerant to changing environmental conditions. More specifically, if less than additive effects are typical in the field, standard regulatory laboratory studies that are carried out at low densities may overestimate the effects of environmental chemicals. However, further studies over a wide range of chemical stressors and life-history types are needed before any general recommendations can be made.