Trade-off between aerobic capacity and locomotor capability in an Antarctic pteropod

Abstract

At ؊1.8°C, the waters of Antarctica pose a formidable physiological barrier for most ectotherms. The few taxa that inhabit this zone have presumably made specific adjustments to their neuromuscular function and have enhanced their metabolic capacity. However, support for this assertion is equivocal and the details of specific compensations are largely unknown. This can generally be attributed to the fact that most Antarctic organisms are either too distantly related to their temperate relatives to permit direct comparisons (e.g., notothenioid fishes) or because they are not amenable to neuromuscular recording. Here, as a comparative model, we take advantage of 2 pelagic molluscs in the genus Clione to conduct a broadly integrative investigation on neuromuscular adaptation to the extreme cold. We find that for the Antarctic congener aerobic capacity is enhanced, but at a cost. To support a striking proliferation of mitochondria, the Antarctic species has shed a 2-gear swim system and the associated specialized neuromuscular components, resulting in greatly reduced scope for locomotor activity. These results suggest that polar animals have undergone substantial tissue-level reorganizations to accommodate their environment, which may reduce their capacity to acclimate to a changing climate.Antarctica ͉ Clione antarctica ͉ Clione limacina ͉ temperature adaptation ͉ mitochondria C lione antarctica, which passes its complete life cycle below 0°C, and Clione limacina (Fig. 1A), normally found between Ϸ5 and 12°C in the north Atlantic and Pacific, occupy nearly identical ecological niches (1) despite their presumed separation by the circumpolar current Ͼ30 million years ago (2). They both feed exclusively on the thecosomatous pteropod Limacina helicina (3) and, although planktonic, rely on 2 wing-like parapodia for locomotion. The predatory arsenal of C. limacina, which has been studied in great detail, includes a multigeared neuromuscular swimming system that drives the parapodia to sweep through an arc of Ϸ180°(4, 5). During routine swimming, animals shift between slow (Ϸ1-2 Hz) and fast (2-5 Hz) modes, based on their wing-beat frequency (5, 6). The present study was prompted by the simple observation that C. antarctica has never been seen swimming in the fast mode (4, 6) (Movies S1-S3).For C. limacina, the cellular underpinnings of the locomotory system, and its ability to shift speeds, have been uncovered by using a reduced preparation that contains only the parapodia, the wing nerves, and the 2 pedal ganglia (Fig. 1B), structures sufficient to generate the entire swim cycle (6, 7). Neural control of swimming is generated within the pedal ganglia. A pair of interneurons establish the basic wing-beat frequency (7, 8), one controlling dorsal phase flexions of the parapodia and the other ventral phase flexions. They inhibit each other by the process of postinhibitory rebound (9). Each interneuron is connected to multiple small motoneurons that drive small fields of slowtwitch, mitochondria-rich muscle fibers in the par...

Temperature compensation of aerobic capacity and performance in the Antarctic pteropod,Clione antarctica, compared to its northern congener,C. limacina

“…These two types of muscle fibers occupy distinct regions in the muscle bundles, with anaerobic fibers occupying ~50% of the bundle (Rosenthal et al, 2009). In stark contrast, muscle bundles in the swim musculature of C. antarctica consist entirely of oxidative, mitochondria-rich fibers.…”

“…As such, they are suitable for investigating cold-temperature compensation and adaptation (Seibel et al, 2007;Rosenthal et al, 2009). Clione antarctica in the cold waters of the Southern Ocean is ecologically similar to, and has been described historically as a subspecies of, Clione limacina, which lives in temperate and polar waters in the northern hemisphere.…”

“…In stark contrast, muscle bundles in the swim musculature of C. antarctica consist entirely of oxidative, mitochondria-rich fibers. The anaerobic fibers, as well as the giant swim motoneurons that control contraction of anaerobic fibers in C. limacina, are absent in C. antarctica (Rosenthal et al, 2009). The proliferation of oxidative, mitochondria-rich fibers displaces mitochondria-poor fibers in muscle bundles of C. antarctica and presumably offsets the temperature-induced decrease in aerobic capacity (Rosenthal et al, 2009).…”

“…are also a unique model in that when the wings and ganglia are dissected free from the rest of the body they maintain rhythmic contractions that approximate those exhibited by adult animals. Thus, the physiological performance of the swim system can be studied independently from the whole animal Rosenthal et al, 2009).…”

“…Locomotor musculature in C. limacina, as investigated previously, includes four layers of muscle bundles consisting of both mitochondria-rich (oxidative) and mitochondria-poor (anaerobic) muscle fibers (Satterlie et al, 1990;Rosenthal et al, 2009). These two types of muscle fibers occupy distinct regions in the muscle bundles, with anaerobic fibers occupying ~50% of the bundle (Rosenthal et al, 2009).…”