Chemical Stress and Metabolic Rate in Aquatic Invertebrates: Threshold, Dose–response Relationships, and Mode of Toxic Action

Abstract

Abstract-Four aromatic compounds were evaluated in laboratory studies to investigate their accumulation and toxicant-induced changes in the rate of heat dissipation in the freshwater invertebrates Chironomus riparius and Lumbriculus variegatus. The sublethal energetic response detected by direct calorimetry was related to tissue chemical concentration by the threshold model and an attempt was made to apply the critical body residue (CBR) concept. Below the compound-specific tissue threshold concentration or CBR, no correlations were found between the dose and the metabolic rate, and the slopes of the regression were close to zero. Above the threshold, depending on the chemical, metabolic rate either increased or decreased. An increase in heat output produced by 2,4-dinitrophenol (2,4-DNP), pentachlorophenol (PCP), and 2,4,5-trichlorophenol (2,4,5-TCP) was closely correlated with the dose. The order of toxicity for these phenols was 2,4-DNP ϭ PCP Ͼ 2,4,5-TCP, which reflects the interaction of compounds' lipophilicities and acidities and their combined influence on bioaccumulation and effects on the energy-transducing membrane by uncoupling oxidative phosphorylation. A decrease in the heat output caused by 1,2,4-trichlorobenzene (1,2,4-TCB) was more variable relative to dose. Also, 1,2,4-TCB required a much higher molar tissue threshold concentration (ϳ2.0 mol/g wet weight) than required by phenols to generate the response. Both the metabolic response and the chemical threshold value were those expected to result from narcosis. Results suggest that calorimetric measures can identify not only the integrated physiologic response but also have some resolution of the mechanism of toxic effects.

Metabolic Response of Lumbriculus Variegatus to Respiratory Uncoupler in Cold and Anoxic Water

“…In the first series, the aerobic dose-response relationship was established between the metabolic heat dissipation (metabolic rate) and an internal concentration of PCP. A detailed test procedure is given in Penttinen and Kukkonen [6]. Modifications included animals being exposed to a mixture of radiolabeled and nonlabeled PCP for 24 h in beakers that contained 100 ml of artificial freshwater (one animal per beaker; six or eight replicate beakers).…”

“…Previously, we studied physiological responses of L. variegatus involved in pollutants affecting the processes of energy metabolism. For example, pentachlorophenol (PCP) specifically affected the aerobic metabolism of L. variegatus by acting as an uncoupler of oxidative phosphorylation and thereby strongly accelerating the metabolic rate, as calorimetrically demonstrated at room temperature under fully aerobic conditions [6]. Therefore, the question arises whether the energetic response of a PCP-exposed worm is consistent under anaerobic conditions or whether the response implies an alteration in PCP's mode of toxic action.…”

Reduction of Energetic Demands through Modification of Body Size and Routine Metabolic Rates in Extremophile Fish

“…This contradicted previous hypotheses that predicted either lower metabolic rates (in response to energy shortage or the rampant hypoxia in sulfidic environments) or higher metabolic rate in sulfidic fish (in response to increased metabolic costs of sulfide detoxification; Riesch et al 2011b). It is important to note, however, that it remains unclear how routine metabolic rates measured in our experimental setup compare with routine metabolic rates in situ because all oxygen consumption measurements were conducted in the absence of H 2 S. In general, the presence of physiochemical stressors and toxicants can increase metabolic rates because coping strategies and detoxification pathways are energetically costly (Penttinen and Kukkonen 1998;Rose et al 2006;McKenzie et al 2007). In metazoans, H 2 S detoxification is primarily linked to the sulfide:quinone oxidoreductase pathway (Griesbeck et al 2000;Shahak and Hauska 2008), which oxidizes sulfide to less-toxic forms of sulfur while consuming energy (Ip et al 2004;Hildebrandt and Grieshaber 2008).…”

“…However, the evolution of increased metabolic rates in extreme environments is typically constrained by a reduced supply of resources required for metabolic expenditure (Waterman 1999(Waterman , 2001. While many studies have investigated immediate metabolic costs of exposure to physicochemical stressors and energy limitation (e.g., Haney and Nordlie 1997;Penttinen and Kukkonen 1998;Rose et al 2006;Wang et al 2006;McKenzie et al 2007;McCue 2010), it remains unclear how metabolic rates and metabolic rate plasticity evolve when populations adapt to diverse environmental stressors. Here, we explicitly tested for differences in body size and routine metabolic rate in the context of resource limitation in extremophile fish.…”

Comparative chronic toxicity of homo- and heterocyclic aromatic compounds to benthic and terrestrial invertebrates: Generalizations and exceptions

“…In the architomic fission process two fragments are formed and the missing segments are generated during a regeneration period that lasts more than a week (Leppanen and Kukkonen, 1998;Martinez et al, 2005). During this period the newly generated worms do not feed, and high sensitivity to toxicants in the sediment might be related to the high energy demands for segment regeneration, which could influence energy allocation to detoxification mechanisms (Penttinen and Kukkonen, 1998).…”