Gestation increases the energetic cost of breathing in the lizard, Tiliqua rugosa

Abstract

SUMMARYHigh gestational loads result in fetuses that occupy a large proportion of the body cavity and may compress maternal organs. Compression of the lungs results in alterations in breathing patterns during gestation, which may affect the energetic cost of breathing. In this study, the energetic cost of breathing during gestation was determined in the viviparous skink Tiliqua rugosa. Radiographic imaging showed progressive lung compression during gestation and a 30% reduction in the lung inflation index (rib number at which the caudal margin of the lung was imaged divided by total rib number). Pneumotachography and open flow respirometry were used to measure breathing patterns and metabolic rates. Gestation induced a twofold increase in minute ventilation via increases in breathing frequency, but no change in inspired tidal volume. The rates of O 2 consumption and CO 2 production did not change significantly during gestation. Together, these results suggest that a relative hyperventilation occurs during gestation in T. rugosa, which in turn suggests that diffusion and/or perfusion limitations may exist at the lung during gestation. The energetic cost of breathing was estimated as a percentage of resting metabolic rate using hypercapnia to stimulate ventilation at different stages of pregnancy. The energetic cost of breathing in non-pregnant lizards was 19.96±3.85% of resting metabolic rate and increased threefold to 62.80±10.11% during late gestation. This significant increase in the energetic cost of breathing may have significant consequences for energy budgets during gestation.

Pregnancy limits lung function during exercise and depresses metabolic rate in the skink Tiliqua nigrolutea

“…A relative hyperventilation can occur when changes in minute ventilation exceed those in metabolic rate. The hyperventilation measured during gestation in previous studies (Munns, 2013;Munns and Daniels, 2007) may be driven by a decrease in lung volume or a decrease in the rate of pulmonary oxygen diffusion. Elevated ventilatory rates may compensate for a decrease in lung volume or the rate of pulmonary gas diffusion by ensuring faster replenishment of fresh air in the lungs.…”

“…In contrast to T. rugosa, an armoured skink that gives birth to one to four large young (Munns, 2013), T. nigrolutea, has a more compliant, non-armoured body wall and gives birth to five to 17 small young (Edwards et al, 2002). Tiliqua nigrolutea's more compliant body wall and high number of small offspring are more representative of skinks in general compared with T. rugosa.…”

“…Such shifts in populations or species must be driven by the balance between the relative costs and benefits of the two modes of parity. A number of viviparous lizards have relatively high gestational loads, such as 19-38% in Tiliqua rugosa (Munns, 2013) and 43% in Tiliqua nigrolutea (Edwards et al, 2002). In species with high gestational loads, the maintenance costs of gestation are likely to be high and thus these species are ideal for investigating physiological mechanisms that result in the physiological and ecological costs of gestation.…”

“…Previous studies have shown that gestation in T. rugosa is associated with a relative hyperventilation, a threefold increase in the energetic cost of breathing (from 20% in non-pregnant lizards to 63% in late pregnancy), and a decreased ability to respond to increased respiratory drive (Munns, 2013;Munns and Daniels, 2007). A relative hyperventilation can occur when changes in minute ventilation exceed those in metabolic rate.…”

“…Elevated ventilatory rates may compensate for a decrease in lung volume or the rate of pulmonary gas diffusion by ensuring faster replenishment of fresh air in the lungs. Radiography and computerised tomography (CT) of pregnant T. rugosa (Munns, 2013;Munns and Daniels, 2007) suggest that lung volume decreases during pregnancy as a result of compression from the large developing fetuses, but no direct measurements of lung volume or lung diffusing capacity have been made in pregnant or gravid reptiles to date.…”