New Publication: Daily Energetic Expenditure and Energy Consumption of Short-Finned Pilot Whales

We are excited to share our new publication in the Journal of Experimental Biology, titled: Daily Energetic Expenditure and Energy Consumption of Short-Finned Pilot Whales (https://journals.biologists.com/jeb/article-lookup/doi/10.1242/jeb.249821). The paper is accompanied by a JEB Spotlight article.

Authors: William Gough, Brijonnay Madrigal, Augusta Hollers, Jens Currie, Robin Baird, Kristi West, Andreas Fahlman, Frank Fish, Lewis Evans, Martin van Aswegen, Brian Stirling, Aude Pacini, Grace Olson, Stephanie Stack, Ashley Blawas, William Walker, Lars Bejder

Figure 1. Methodological schematic for data types and energetic modeling in the short-finned pilot whale. (A) The four primary data types in our analyses: UAS-photogrammetry, CATS tag deployments, stomach content analysis, and satellite tag deployments. (B) Schematic synthesis showing how our data are used in the various equation to generate estimates of energetic expenditure and intake.

Abstract

Diving is one of the most important behaviors undertaken by marine mammals. Pilot whales (Globicephala spp.) are oceanic dolphins that regularly forage at extreme depths (∼600–1000 m) and maintain body sizes similar to beaked whales. They are also listed as data deficient, with little known about their population dynamics. To help fill this knowledge gap, we estimated their energetic demands through a combination of multiple data streams (e.g. unoccupied aerial systems photogrammetry, high-resolution accelerometry tag data, stomach content analysis and long-duration dive data from satellite tags) from short-finned pilot whales (Globicephala macrorhynchus) in Hawaiian waters. We estimated and compared pilot whale field metabolic rates from breathing frequency against a more granular cost of transport method developed from morphometrics and swimming kinematics, finding that these methods gave similar estimates of energetic expenditure during foraging dives. We then combined expenditure and intake estimates into an exploratory model of daily net energetic balance. Using an estimate of prey size derived from squid beaks collected from a stranded animal, we found that an average of 142 ± 59.8 squid day^-1; 52,000 ± 21,800 squid year^-1) is enough for an average adult short-finned pilot whale to reach a neutral net energetic balance. This species has an estimated population abundance of ∼8000 individuals in Hawaiian waters, suggesting that the population as a whole would require 416 ± 175 million squid (at an average of 559 ± 126 kJ squid^-1) or approximately 88,000 ± 37,000 tonnes of squid annually, assuming similar energetic requirements for each animal.

Why pilot whales?

Energy is the primary currently of life, with its acquisition and use affecting the physiology, behavior, and long-term fitness of species in profound ways. As we enter deeper into the Anthropocene and hope to conserve and protect species against changing environments, we must have a baseline understanding of their biology – starting with their energetic budgets. In Hawaii, there are multiple charismatic cetacean species that have garnered significant attention, either for their close proximity to shore and spectacular surface behavior (humpback whales), their epic battles with colossal squid (sperm whale), or their ability to dive down to 3 km for over an hour (goose-beaked whale). In comparison, the short-finned pilot whale (Globicephala macryrhunchus) is a lesser known oceanic dolphin that dives to ~1km and feeds primarily on small squid, but members of this species do not have some of the singular physiological bells and whistles seen in other deep divers. As a result, they have attracted less intensive study and are considered to be “data deficient” by the IUCN in Hawaiian waters. Like their more physiologically unique relatives, we believe that short-finned pilot whales deserve to have comprehensive energetic baselines set in place to assist species managers and conservationists of the future.

New Methods – New Results

Cetacean biologists have been very lucky over the last ~20 years, as both UAS (unmanned aerial systems) and biologging tag technologies have advanced considerably. At the MMRP lab, we are uniquely positioned with expertise on both methods, allowing us to combine insights from animal-attached biologgers and UAS-photogrammetry in new ways. For this study, we combined fine-scale kinematics (on a tailbeat-by-tailbeat basis) with morphometrics of the body and tail to estimate the thrust power produced by eight short-finned pilot whales as they swam, dove, and foraged (presumably) off the western coast of Lanai. This thrust power could then be used as a proxy for energetic expenditure, allowing us to determine periods of high and low energy usage.

This “thrust method” not wholly new, having been built on the herculean efforts of previous researchers to quantify the hydrodynamics and energetics of cetacean swimming in captive environments. But, to our knowledge, this is the first attempt to use such a fine-scale method to quantify the energetics of free-swimming cetaceans.  And to validate our resulting energetic values, we compared against a well-known method that uses breathing frequency as a proxy for energetic expenditure over a period of time. Our two methods aligned well during foraging dives (only 6.7 ± 11% different), while our energetic estimates for non-diving periods showed a larger divergence between methods (41.5 ± 5.5% different).

How Much Does a Pilot Whale Eat?

To determine the overall daily energetic budget of a short-finned pilot whale in Hawaii, we combined our estimates of energetic expenditure (using our “thrust method”) with related estimates of energetic intake – modeled through the combination of daily diving rates (from satellite tags deployed by Dr. Robin Baird and his team from Cascadia Research Collective), prey size estimates from the stomach contents of a stranded short-finned pilot whale (collected by UH Manoa’s Dr. Kristi West), and estimates of the caloric densities of various squid species found in Hawaii (from literature sources).

Fig. 5. Zoom segment of data around three foraging buzzes derived from acoustic data. Subplots show the jiggle-derived swimming speed (A), jerk (B) and spectrogram (C), as well as a further zoom period of the spectrogram (D) around one of the foraging buzzes (Buzz 2). Orange dotted lines denote the end positions of each buzz. (E) Images taken from the CATS video record and show conspecifics near the surface as well as the ocean floor and what appears to be a squid ink cloud appearing <2 s from the end time of Buzz 2.

If an individual captures enough prey to maintain a neutral net energetic balance, that translates into an average of 52,000 ± 21,800 squid whale^-1 year^-1 or 11 ± 5 tonnes of squid year⁻¹. The most recent abundance estimate of short-finned pilot whales in 2017 puts their population around ∼8000 individuals in Hawaiian waters. At this population, we estimated the overall biomass of squid removed from the ecosystem at 416 ± 175 million squid year^-1, or 88,000 ± 37,000 tonnes year^-1. Luckily for short-finned pilot whales, squid typically display rapid life cycles (~1 year or less) and high growth rates, positioning them as an abundent and reliable prey resource.

Acknowledgements

We thank the staff and support crew at Pacific Whale Foundation for their logistical and field support during tag data collection efforts, and for providing analytical support and feedback on the manuscript. Thanks to the Cascadia Research Collective for providing their dataset of satellite tag deployments. We thank the members of the Marine Mammal Research Program at UH Manoa’s Hawai‘i Institute of Marine Biology for their substantial feedback on the structure and content of this work. We thank Dr Peter Madsen for his helpful feedback on the manuscript and figures. Finally, we thank Cameron Nemeth and Dr Kalikoaloha Martin for their help in drafting the Hawaiian language abstract for this manuscript. This paper represents HIMB and SOEST contribution numbers 2009 and 11991, respectively.

Permitting

All data were collected under appropriate NOAA NMFS/MMPA permits (no. 15330, 18786, 20605, 21321, 21476, 26596, and 27099) and university or Cascadia Research Collective IACUC protocols. UAS flights were operated by Part-107 authorized pilots in compliance with standards set by the Federal AviationAdministration.

Funding

This research was funded in part by grants from the Office of Naval Research (no. N00014-22-1-2721), the United States Pacific Fleet Environmental Readiness Division (no. W9126G2220033), NOAA Fisheries via the Cooperative Ecosystem Studies Unit (CESU) award NA19NMF4720181, and the DoD’s Defense University Research Instrumentation Program (N00014-19-1-2612 and N00014-21-1-2249). Stomach content collection and analysis was funded by the Office of Naval Research (no. N00014-17-1-2789) and with support of the NOAA National Marine Fisheries Service Johan H. Prescott Marine Mammal Rescue Assistance Grant Program. Satellite tagging field efforts performed by Cascadia Research Collective were supported by multiple sources, including: the Office of Naval Research, United States Navy Living Marine Resources, United States Navy Pacific Fleet, the NOAA Pacific Islands Fisheries Science Center, and a NOAA Species Recovery Grant. Additional funding was provided by the members and supporters of Pacific Whale Foundation and by the Omidyar Ohana Foundation.