Grow or go? Energetic constraints on shark pup dispersal from pupping areas

M N McMillan; J M Semmens; C Huveneers; D W Sims; K M Stehfest; B M Gillanders

doi:10.1093/conphys/coab017

Grow or go? Energetic constraints on shark pup dispersal from pupping areas

Conserv Physiol. 2021 Apr 28;9(1):coab017. doi: 10.1093/conphys/coab017. eCollection 2021.

Authors

M N McMillan^{1

2}, J M Semmens³, C Huveneers⁴, D W Sims^{5

6}, K M Stehfest³, B M Gillanders¹

Affiliations

¹ Southern Seas Ecology Laboratories, School of Biological Sciences, & Environment Institute, University of Adelaide, Adelaide 5005, Australia.
² Queensland Department of Agriculture and Fisheries, Animal Science, EcoSciences Precinct, Dutton Park 4102, Australia.
³ Fisheries and Aquaculture Centre, Institute for Marine and Antarctic Studies, University of Tasmania, Taroona 7053, Australia.
⁴ Southern Shark Ecology Group, College of Science and Engineering, Flinders University, Bedford Park 5042, Australia.
⁵ Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK.
⁶ Ocean and Earth Science, University of Southampton, National Oceanography Centre Southampton, Waterfront Campus, Southampton SO14 3ZH, UK.

Abstract

Many sharks and other marine taxa use natal areas to maximize survival of young, meaning such areas are often attributed conservation value. The use of natal areas is often linked to predator avoidance or food resources. However, energetic constraints that may influence dispersal of young and their use of natal areas are poorly understood. We combined swim-tunnel respirometry, calorimetry, lipid class analysis and a bioenergetics model to investigate how energy demands influence dispersal of young in a globally distributed shark. The school shark (a.k.a. soupfin, tope), Galeorhinus galeus, is Critically Endangered due to overfishing and is one of many sharks that use protected natal areas in Australia. Energy storage in neonate pups was limited by small livers, low overall lipid content and low levels of energy storage lipids (e.g. triacylglycerols) relative to adults, with energy stores sufficient to sustain routine demands for 1.3-4 days (mean ± SD: 2.4 ± 0.8 days). High levels of growth-associated structural lipids (e.g. phospholipids) and high energetic cost of growth suggested large investment in growth during residency in natal areas. Rapid growth (~40% in length) between birth in summer and dispersal in late autumn-winter likely increased survival by reducing predation and improving foraging ability. Delaying dispersal may allow prioritization of growth and may also provide energy savings through improved swimming efficiency and cooler ambient temperatures (daily ration was predicted to fall by around a third in winter). Neonate school sharks are therefore ill-equipped for large-scale dispersal and neonates recorded in the northwest of their Australian distribution are likely born locally, not at known south-eastern pupping areas. This suggests the existence of previously unrecorded school shark pupping areas. Integrated bioenergetic approaches as applied here may help to understand dispersal from natal areas in other taxa, such as teleost fishes, elasmobranchs and invertebrates.

Keywords: Connectivity; cost of transport; marine-protected areas; metabolic rate; nursery areas; ontogenetic habitat shift.