The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities

Abstract

The rates of metabolism in animals vary tremendously throughout the biosphere. The origins of this variation are a matter of active debate with some scientists highlighting the importance of anatomical or environmental constraints, while others emphasize the diversity of ecological roles that organisms play and the associated energy demands. Here, we analyse metabolic rates in diverse marine taxa, with special emphasis on patterns of metabolic rate across a depth gradient, in an effort to understand the extent and underlying causes of variation. The conclusion from this analysis is that low rates of metabolism, in the deep sea and elsewhere, do not result from resource (e.g. food or oxygen) limitation or from temperature or pressure constraint. While metabolic rates do decline strongly with depth in several important animal groups, for others metabolism in abyssal species proceeds as fast as in ecologically similar shallow-water species at equivalent temperatures. Rather, high metabolic demand follows strong selection for locomotory capacity among visual predators inhabiting well-lit oceanic waters. Relaxation of this selection where visual predation is limited provides an opportunity for reduced energy expenditure. Large-scale metabolic variation in the ocean results from interspecific differences in ecological energy demand.Keywords: metabolism; deep sea; scaling; oxygen consumption; locomotion; marine INTRODUCTIONThe rates of metabolic processes in animals vary tremendously throughout the biosphere (e.g. Bennett 1991; Seibel 2007). The origins and scope of this variation are a matter of active debate. Some emphasize geometric and environmental constraints or resource limitation as its source (e.g. Gillooly et al. 2001;Brown et al. 2004), while others emphasize the diversity of ecological roles that organisms play and the associated energy demands (Childress 1995;Suarez 1996;Reinhold 1999;Clarke 2004;Seibel 2007) as a primary driver of metabolic variation. With this in mind, the present paper addresses three seemingly simple questions: (i) what is the extent of variation in the rate of metabolism across diverse taxa and environments, (ii) what environmental and ecological demands act on organisms to drive selection for high metabolic capacity, and (iii) under what environmental circumstances might such selection be relaxed or capacity be constrained?These questions have been pursued vigorously for decades but the clarity of the debate has been diminished by the subtlety of differences in capacity between the taxa most thoroughly studied, that often

Vampire squid: detritivores in the oxygen minimum zone

“…Vampyroteuthis has the lowest metabolic rate recorded for any cephalopod, comparable to that of a scyphomedusa of the same size [26,44], but this characteristic alone is insufficient for survival in the OMZ [20]. Permanent residents of the OMZ have a variety of respiratory and morphological adaptations [25].…”

“…This results in high bacterial growth at depth as a result of the decomposition of organic carbon in sinking particulate matter, yielding very low oxygen concentrations [19]. While species from many taxa (including copepods, euphausiids, cnidarians, ctenophores, fish and squid) live entirely or part of the time (during diel or ontogenetic vertical migrations) within the most pronounced OMZs [20,21], many organisms are stressed or die under hypoxic conditions [22], and overall abundance and species diversity are reduced. OMZs have dramatic effects on the spatial distribution patterns of animals in the water column, and zones of enhanced biological and biogeochemical activity exist at the OMZ's upper and lower boundaries [23,24].…”

Environmental constraints upon locomotion and predator–prey interactions in aquatic organisms: an introduction

“…Not surprisingly, it has been assumed that metabolism in the deep sea is universally low and environmentally constrained. Seibel & Drazen (2007) argue, however, that although our knowledge of metabolic rates in aquatic organisms is limited, there is growing evidence that metabolic rates are not typically low and constrained. Although the metabolism of several important animal groups declines strongly with depth, the metabolism of others is similar between abyssal species and ecologically equivalent, shallow-water species.…”

“…Most notable is the high metabolic demand that results from strong selection for locomotor capacity among visual predators inhabiting the well-lit epipelagic zone and the reduction in metabolic rates that follows relaxation of this selection in darkened bathypelagic waters. As pointed out by Seibel & Drazen (2007) technological limitations play an increasing role in defining our understanding of the relationship between organisms and their environment in deeper waters. Large organisms pose specific challenges to scientific enquiry.…”

“…(c) Technological developments To answer the questions posed above, and many others within the field of ecophysiology, there is a pressing need for development in technologies to monitor activity of organisms in the field, especially in areas such as deep and pelagic waters where the behaviour of aquatic organisms is poorly described (Bailleul et al 2007;Davis & Weihs 2007;Seibel & Drazen 2007). This should be approached at three levels to: (i) monitor the physical environment, (ii) monitor the basic physiological processes of free living organisms, and (iii) monitor their behaviour.…”