Written by Martin van Aswegen
We are pleased to share a new publication in The Journal of Physiology, entitled: Energetic cost of gestation and prenatal growth in humpback whales.
Authors: Martin van Aswegen, Andy Szabo, Jens Currie, Stephanie Stack, Kristi West, Nicholas Hofmann, Fredrik Christiansen, and Lars Bejder.
Figure 1. Graphical abstract summarizing key methods and findings from the study.
Abstract:
Improving our understanding of energy allocation in reproduction is key for accurately parameterizing bioenergetic models to assess population responses to environmental perturbations and anthropogenic disturbance. We quantified the energetic cost of gestation in humpback whales (Megaptera novaeangliae) using historical whaling records, non-invasive unoccupied aerial system (UAS) photogrammetry, and post-mortem tissue samples. First, we estimated relative birth size using body length measurements of 678 mother-fetus pairs from historical whaling records and 987 mother-calf pairs measured in-situ using UAS-photogrammetry. The total energetic cost of gestation includes fetal growth, heat increment of gestation, and placental tissue development. Fetal growth was modeled from conception to birth, with fetal volume and mass estimated using the volume-to-length relationship of perinatal calves and published humpback whale tissue composition estimates. Tissue-specific energy content was quantified using bone, muscle, viscera, and blubber samples from a post-mortem neonatal humpback whale. Placental tissue development was estimated using humpback whale placental tissue and published equations. Relative birth length was found to be 33.75% (95% CI: 32.10-34.61) of maternal length. Fetal growth rates and absolute birth size increased with maternal length, with exponential growth in fetal length, volume, and mass resulting in minimal energetic costs over the first two quadmesters (0.01-1.08%) before increasing significantly in the final quadmester (98.92%). Gestational heat constituted the greatest energetic cost (90.42-94.95%), followed by fetal (4.58-7.76%) and placental tissue growth (0.37-1.83%). Our findings highlight the energetic costs endured by capital breeding females preceding parturition, with the most substantial energetic costs of gestation coinciding with migration and fasting.
Figure 2. Aerial image of a newborn humpback whale calf off Maui, Hawaiʻi. Photo by Lars Bejder (Marine Mammal Research Program; NMFS permit 20311-01).
Study overview:
We quantified the energetic cost of gestation in humpback whales using body length measurements of mother-fetus pairs from historical whaling records (n = 678 pairs), length estimates of live mother-calf pairs (n = 987) measured in situ using aerial photogrammetry (Figure 1,2), and post mortem tissue samples. Tissue samples were collected from a post mortem newborn humpback whale calf with placental tissue collected off Maui, Hawaiʻi.
First, we found fetal growth rates and birth size increased with maternal length, with fetal length, volume, and mass increasing exponentially over gestation. This exponential growth had implications for maternal energy requirements later in gestation. For example, energetic costs over the first two thirds of gestation were negligible before increasing significantly in the final 100 days. Though larger females incur nearly twice the energetic cost of smaller females, they are likely buffered by greater absolute energy reserves, suggesting smaller females may be less resilient to disturbances and/or changes in prey availability.
We demonstrate the significant energetic costs incurred by pregnant humpback whales, with most of the energetic expenditure occurring over the final 100 days of gestation. Late-pregnant females are therefore particularly vulnerable to disruptions in energy balance, given periods of greatest energetic stress coincide with fasting and migration.
Figure 3. A pregnant humpback whale on the Southeast Alaskan feeding ground.
Given periods of greatest energetic stress coincide with fasting and migration to sub-tropical breeding grounds, we highlight a particularly vulnerable period for pregnant humpback whales. This is important because once these whales leave their high-latitude feeding grounds (Figure 3), they have a finite amount of energy available to invest in their offspring over a 3-5 month fasting period. We know offspring survival is linked to maternal characteristics like body size and condition, with offspring size and energy stores considered key determinants of their resilience and subsequent survival. It is therefore important to understand how reproductive females use energy for reproduction and how such energy use can impact offspring survival and subsequent population viability.
This work forms the basis for future studies investigating the energetic demands on humpback whales. The humpback whale health database, developed by the Marine Mammal Research Program and partners, is being used across several projects within the Marine Mammal Research Program and abroad. This database is comprised of 11,000 measurements of 8,500 individual whales collected across the North Pacific. These data become even more powerful when used in conjunction with fine-scale behavior and movement data (from biologging tags), reproductive and stress hormone data (from tissue and breath samples), and tissue data derived from post-mortem events. These studies will be used to better predict the resilience of large baleen whale species in the face of threats, including disturbance, entanglement, vessel collision, and climate change.
Funding:
Hawaiʻi fieldwork was funded through the University of Hawaiʻi at Manoa, DoD’s Defense University Research Instrumentation Program (#N00014-19-2612), 'Our Oceans', Netflix, Wildspace Productions and Freeborne Media, Office of Naval Research (#N000142012624), Omidyar Ohana Foundation, the National Marine Sanctuary Foundation (#21-10-B-334), and PacWhale Eco-Adventures as well as members and donors of Pacific Whale Foundation. Southeast Alaska research was funded through awards from the National Geographic Society (NGS), Lindblad Expeditions-National Geographic (LEX-NG) Funds, and North Pacific Research Board (#2114). Graduate Assistantships for M.v.A were funded by a Denise B. Evans Oceanography Fellowship, North Pacific Research Board grant (#2114), and the Dolphin Quest General Science and Conservation Fund. Stranding response, necropsy and tissue processing of the humpback whale calf was supported by the NOAA John H. Prescott Marine Mammal Rescue Assistance Grant Program.
Acknowledgements:
We acknowledge the cultural significance of humpback whales (koholā) in Hawaiian culture as 'aumakua and a manifestation of Kanaloa. Our work involves a rigorous permitting process and the use of minimally invasive techniques to interact with whales. We thank Linda Nichol (Cetacean Research Program, Pacific Biological Station, Fisheries and Oceans Canada) and Sue Burkett (International Whaling Commission Statistics Department) for providing valuable fetus morphometric data. We are grateful to Dana Bloch, Jessie Hoffman, Abigail Machernis, Grace Olson, Florence Sullivan, and Elizabeth Beato for their dedication and support with data collection and processing. We thank the numerous research assistants who helped with fieldwork and data processing across Hawaiʻi and Southeast Alaska. We are grateful to Zoltan Nemeth (cetek-art.com) for providing illustrations. We thank Paige Wernli, Ciara Branco, Abigael Jacka, Noah Harris, Sarah Perryman, Conner Humann, Tamako Delfino and the UH Health and Stranding Lab staff and volunteers for their assistance with stranding response, necropsy, and post-mortem tissue processing. We also thank PacWhale Eco-Adventures, Chrissy Lovitt and Emma Nelson (Maui Ocean Adventures), Lee James (Ultimate Whale Watch), Ed Lyman, Marc Lammers, and the Guth family for their logistical support. We thank the crew of Ocean Explorer (PacWhale Eco-Adventures), including Aaron Bement, Emily Johnson, Callen Miracle, and Alyssa Moser, for retrieving the placenta, and Dr. Ilse Silva-Krott, Abigail Machernis, Grace Olson, Elizabeth Beato, and Dan Kraver for their assistance in documenting and sampling the fresh placental tissue. Finally we are grateful to Paul Schofield, Javier Garcia, and Christopher Ferrante for volunteering their time to assist in the field.
Full citation:
van Aswegen, M, Szabo, A., Currie, J.J., Stack, S.H., West, K.L., Hofmann, N., Christiansen, F., & Bejder, L. (2024). Energetic cost of gestation and prenatal growth in humpback whales. The Journal of Physiology. doi:10.1113/JP287304.
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