Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates Inna M. Sokolova a, * , Markus Frederich b , Rita Bagwe a , Gisela Lannig c , Alexey A. Sukhotin d a Department of Biology, University of North Carolina at Charlotte, Charlotte, NC, USA b Department of Marine Sciences, University of New England, Biddeford, ME, USA c Alfred-Wegener Institute for Polarand Marine Research, Integrative Ecophysiology, 27570 Bremerhaven, Germany d White Sea Biological Station, Zoological Institute of Russian Academy of Sciences, 199034 St. Petersburg, Russia article info Article history: Received 23 December 2011 Received in revised form 6 April 2012 Accepted 10 April 2012 Keywords: Energy metabolism Stress tolerance Multiple stressors Metabolic markers Aerobic scope Bioenergetics Marine invertebrates abstract Energy balance is a fundamental requirement of stress adaptation and tolerance. We explore the links between metabolism, energy balance and stress tolerance using aquatic invertebrates as an example and demonstrate that using key parameters of energy balance (aerobic scope for growth, reproduction and activity; tissue energy status; metabolic rate depression; and compensatory onset of anaerobiosis) can assist in integrating the effects of multiple stressors and their interactions and in predicting the whole- organism and population-level consequences of environmental stress. We argue that limitations of both the amount of available energy and the rates of its acquisition and metabolic conversions result in trade- offs between basal maintenance of a stressed organism and energy costs of fitness-related functions such as reproduction, development and growth and can set limit to the tolerance of a broad range of envi- ronmental stressors. The degree of stress-induced disturbance of energy balance delineates transition from moderate stress compatible with population persistence (pejus range) to extreme stress where only time-limited existence is possible (pessimum range). It also determines the predominant adaptive strategy of metabolic responses (energy compensation vs. conservation) that allows an organism to survive the disturbance. We propose that energy-related biomarkers can be used to determine the conditions when these metabolic transitions occur and thus predict ecological consequences of stress exposures. Bioenergetic considerations can also provide common denominator for integrating stress responses and predicting tolerance limits under the environmentally realistic scenarios when multiple and often variable stressors act simultaneously on an organism. Determination of bioenergetic sustainability at the organism’s level (or lack thereof) has practical implications. It can help identify the habitats and/or conditions where a population can survive (even if at the cost of reduced reproduction and growth) and those that are incapable of supporting viable populations. Such an approach will assist in explaining and predicting the species’ distribution limits in the face of the environmental change and informing the conservation efforts and resource management practices. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction Energy metabolism plays a central role in organism’s survival and function, as well as in stress adaptation and tolerance. The amount of available energy, the rate at which it can be gained and metabolically transformed as well as the capacity to store it are inevitably limited in any organism. Therefore, regulation of energy expenditure and its allocation to different functions are funda- mental to the organism’s fitness. Environmental stress can strongly affect the energy balance of an organism due to the additional energy needed to recover and maintain homeostasis that can put strains on the systems involved in energy acquisition, conversion and conservation. The potential energy cost of stress response and homeostatic regulation against the environmental disturbances have been discussed in several excellent reviews (Calow, 1983, 1989; 1991; Calow and Forbes, 1998; Van Straalen and Hoffmann, 2000). However, up until recently, few experimental studies have explicitly tested the energy cost of stress response and its role in stress tolerance to validate the theoretical framework proposed in these reviews. The past few decades saw a steady growth in the number of studies focusing on metabolic responses to stress. An important common theme emerging from these studies points * Corresponding author. E-mail address: ISokolov@uncc.edu (I.M. Sokolova). Contents lists available at SciVerse ScienceDirect Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev 0141-1136/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.marenvres.2012.04.003 Marine Environmental Research 79 (2012) 1e15