Extreme capital breeding for giants: Effects of body size on humpback whale energy expenditure and fasting endurance

Baleen whales are extreme capital breeders, capable of fasting for more than half a year while migrating thousands of kilometres and nursing rapidly growing offspring that quadruple in body size over the same period. To understand this energetic conundrum, bioenergetic models that quantify the energy expenditure of baleen whales relative to their body energy reserves (body condition) are required. However, due to the difficulty in measuring the physiology and bioenergetics of large whales, few empirically informed models are available. Here we develop a bioenergetic model for humpback whales (Megaptera novaeangliae) off Western Australia to quantify their daily and seasonal energy expenditure over the breeding season. Specifically, we hypothesised that body size (length) would have a negative effect on the mass-specific energy expenditure of whales, and reduce female reproductive costs. A larger body size would also increase the absolute energy reserves, and hence fasting ability of humpback whales. To test this, we used a unique combination of field methodologies, including behavioural focal follows, aerial photogrammetry, and satellite tagging. To quantify the daily energetic cost of body maintenance, activity, somatic growth, and reproduction (gestation and lactation), we combined fine-scale behavioural and body morphometric data. Seasonal energy loss was estimated from changes in body condition, using aerial photogrammetry data. Migration timing and swim speed were calculated from satellite tag movement data. The resulting bioenergetic model showed that body size had a strong negative effect on the mass-specific energy expenditure of whales, and a positive effect on the fasting ability and residency time of juveniles and adults. Maternal body size had a positive effect on calf birth size and growth, so that calves of larger females reached their departure size quicker and begin their migration back to the Antarctic feeding grounds. The body condition loss during the breeding season declined with body size for juveniles (26.9-14.4%) and lactating females (28.3-7.8%), while adults maintained a constant loss (14.4-15.0%) by increasing their residency time. The ability of humpback whales to support such high seasonal energetic costs with only stored energy reserves highlights the energetic benefits that gigantism provides in these extreme capital breeders.