Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes

Abstract

Many similarities exist between the key characteristics of muscular metabolism in marine invertebrates and those found in vertebrate striated muscle, even though there are important phosphagens and glycolytic end products that differ between groups. Lifestyles and modes of locomotion also vary extremely among invertebrates thereby shaping the pattern of exercise metabolism. In accordance with the limited availability of integrated ecological and physiological information the present paper reports recent progress in the exercise physiology of cephalopods, which are characterized by high rates of aerobic and anaerobic energy turnover during high velocity hunts or escapes in their pelagic environment, and a sipunculid worm, which mostly uses anaerobic resources during extended marathon-like digging excursions in the hypoxic marine sediment. Particular attention is paid to how lifestyle and oxygen availability in various marine environments shapes the use and rates of aerobic and anaerobic metabolism and acidosis as they depend on activity levels and energy saving strategies. Whereas aerobic scope and, accordingly, use of ambient oxygen by blood oxygen transport and skin respiration is maximized in some squids, aerobic scope is very small in the worm and anaerobic metabolism readily used upon muscular activity. Until recently, it was widely accepted that the glycolytic end product octopine, produced in the musculature of these invertebrates, acted as a weak acid and so did not compromise acid-base balance. However, it has now been demonstrated that octopine does cause acidosis. Concomitant study of tissue energy and acid-base status allows to evaluate the contribution of glycolysis, pH and free ADP accumulation to the use of the phosphagen and to the delayed drop in the Gibb's free energy change of ATP hydrolysis. The analysis reveals species specific capacities of these mechanisms to support exercise beyond the anaerobic threshold. During high intensity anaerobic exercise observed in squid, the levels of ATP free energy change finally fall to critical minimum levels contributing to fatigue. Maintenance of sufficiently high energy levels is found at low but extended rates of anaerobic metabolism as observed in the long term digging sipunculid worm. The greatest aerobic and anaerobic performance levels are seen in squid inhabiting the open ocean and appear to be made possible by the uniform and stable physicochemical parameters (esp. high O and low CO levels) that characterize such an environment. It is suggested 2 2 that at least some squid operate at their functional and environmental limits. In extremely different environments, both the worm and the squids display a tradeoff between oxygen availability, temperature, performance level and also, body size. ᮊ

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

“…One consequence of this has been a striking convergence of adaptations among disparate epipelagic taxa that permits high-speed locomotion and high aerobic and anaerobic metabolic capacity. Such convergence has been thoroughly described between various groups of fish ( Farrell 1991;Dickson 1995Dickson , 1996Bernal et al 2001;Block & Stevens 2001;Donley et al 2004) as well as between fish and cephalopods (O'Dor & Webber 1986;Packard 1972;Pö rtner 2002;Webber et al 2000). Although less data exist, a case could also be made for convergence towards high metabolic and locomotory capacity in marine mammals ( Williams 1999), pelagic decapod crustaceans (Quetin et al 1994;Childress 1995) and marine reptiles (Humphries & Ruxton 2002).…”

“…In fact, active squids consume all available oxygen from the blood on each pass through the body leaving no venous reserve and must acquire as much as 60% of their total oxygen demand across the skin (Pö rtner 2002). The additional oxygen taken up across the skin, in combination with maximized circulatory performance (Shadwick et al 1990;Pö rtner 2002), allows squids to achieve athletic performance comparable to heterothermic fish.…”

Integrating climate-related stressor effects on marine organisms: unifying principles linking molecule to ecosystem-level changes

“…In special cases, such as in adult crustaceans, ventilation of the egg masses is also limited by capacity (Cohen & Strathmann 1996, Fernandez et al 2000, Woods & Moran 2008. The balance between oxygen supply and demand shapes the dependence of maximum body size in marine invertebrate phyla on temperature-dependent oxygen availability (Chapelle & Peck 1999, Pörtner 2002b. These principles thus appear unifying in shaping the environmental border conditions of aquatic and possibly terrestrial animal life (Pörtner & Farrell 2008).…”

Muscle bioenergetics of speeding fish: In vivo 31P‐NMR studies in a 4.7 T MR scanner with an integrated swim tunnel

“…Muscle physiology and energy metabolism under basal and exercise conditions have received significant attention, both for an understanding of the factors enabling and limiting exercise and, more recently, for an understanding of the role of temperature adaptation and acclimation shaping exercise performance in marine animals from various climate regimes (1)(2)(3). The function and organization of muscle tissue from ectothermic animals living at low or polar tempera-tures is especially interesting, and studies revealed unique features of adaptation for living and swimming in cold waters at all organismic levels.…”

“…An understanding of these special adaptations is becoming even more important in the framework of climate change, questioning how animals specialized on limited climate and temperature regimes can cope with rising temperatures? A model explaining the oxygen limitation of thermal tolerance has recently been developed and tested in an ecological context with the goal to explain these phenomena (1)(2)(3)10). These analyses revealed a key role for the thermal sensitivity of aerobic scope and the mechanisms shaping the thermal window of aerobic scope.…”