Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size
Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopter...
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ftpubmed:oai:pubmedcentral.nih.gov:3443106 2023-05-15T15:36:11+02:00 Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size Potvin, Jean Goldbogen, Jeremy A. Shadwick, Robert E. 2012-09-14 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3443106 http://www.ncbi.nlm.nih.gov/pubmed/23024769 https://doi.org/10.1371/journal.pone.0044854 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3443106 http://www.ncbi.nlm.nih.gov/pubmed/23024769 http://dx.doi.org/10.1371/journal.pone.0044854 This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. CC-BY Research Article Text 2012 ftpubmed https://doi.org/10.1371/journal.pone.0044854 2013-09-04T12:57:02Z Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopteridae) exhibit an intermittent ram filter feeding mode, lunge feeding, which requires the abandonment of body-streamlining in favor of a high-drag, mouth-open configuration aimed at engulfing a very large amount of prey-laden water. Particularly while lunge feeding on krill (the most widespread prey preference among rorquals), the effort required during engulfment involve short bouts of high-intensity muscle activity that demand high metabolic output. We used computational modeling together with morphological and kinematic data on humpback (Megaptera noveaangliae), fin (Balaenoptera physalus), blue (Balaenoptera musculus) and minke (Balaenoptera acutorostrata) whales to estimate engulfment power output in comparison with standard metrics of metabolic rate. The simulations reveal that engulfment metabolism increases across the full body size of the larger rorqual species to nearly 50 times the basal metabolic rate of terrestrial mammals of the same body mass. Moreover, they suggest that the metabolism of the largest body sizes runs with significant oxygen deficits during mouth opening, namely, 20% over maximum at the size of the largest blue whales, thus requiring significant contributions from anaerobic catabolism during a lunge and significant recovery after a lunge. Our analyses show that engulfment metabolism is also significantly lower for smaller adults, typically one-tenth to one-half . These results not only point to a physiological limit on maximum body size in this lineage, but also have major implications for the ontogeny of extant rorquals as well as the evolutionary pathways used by ancestral toothed whales to transition from hunting individual prey items to filter feeding on prey aggregations. Text Balaenoptera acutorostrata Balaenoptera musculus Balaenoptera physalus baleen whales toothed whales PubMed Central (PMC) Rorqual ENVELOPE(-62.311,-62.311,-65.648,-65.648) PLoS ONE 7 9 e44854 |
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English |
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Research Article |
spellingShingle |
Research Article Potvin, Jean Goldbogen, Jeremy A. Shadwick, Robert E. Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size |
topic_facet |
Research Article |
description |
Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopteridae) exhibit an intermittent ram filter feeding mode, lunge feeding, which requires the abandonment of body-streamlining in favor of a high-drag, mouth-open configuration aimed at engulfing a very large amount of prey-laden water. Particularly while lunge feeding on krill (the most widespread prey preference among rorquals), the effort required during engulfment involve short bouts of high-intensity muscle activity that demand high metabolic output. We used computational modeling together with morphological and kinematic data on humpback (Megaptera noveaangliae), fin (Balaenoptera physalus), blue (Balaenoptera musculus) and minke (Balaenoptera acutorostrata) whales to estimate engulfment power output in comparison with standard metrics of metabolic rate. The simulations reveal that engulfment metabolism increases across the full body size of the larger rorqual species to nearly 50 times the basal metabolic rate of terrestrial mammals of the same body mass. Moreover, they suggest that the metabolism of the largest body sizes runs with significant oxygen deficits during mouth opening, namely, 20% over maximum at the size of the largest blue whales, thus requiring significant contributions from anaerobic catabolism during a lunge and significant recovery after a lunge. Our analyses show that engulfment metabolism is also significantly lower for smaller adults, typically one-tenth to one-half . These results not only point to a physiological limit on maximum body size in this lineage, but also have major implications for the ontogeny of extant rorquals as well as the evolutionary pathways used by ancestral toothed whales to transition from hunting individual prey items to filter feeding on prey aggregations. |
format |
Text |
author |
Potvin, Jean Goldbogen, Jeremy A. Shadwick, Robert E. |
author_facet |
Potvin, Jean Goldbogen, Jeremy A. Shadwick, Robert E. |
author_sort |
Potvin, Jean |
title |
Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size |
title_short |
Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size |
title_full |
Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size |
title_fullStr |
Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size |
title_full_unstemmed |
Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size |
title_sort |
metabolic expenditures of lunge feeding rorquals across scale: implications for the evolution of filter feeding and the limits to maximum body size |
publisher |
Public Library of Science |
publishDate |
2012 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3443106 http://www.ncbi.nlm.nih.gov/pubmed/23024769 https://doi.org/10.1371/journal.pone.0044854 |
long_lat |
ENVELOPE(-62.311,-62.311,-65.648,-65.648) |
geographic |
Rorqual |
geographic_facet |
Rorqual |
genre |
Balaenoptera acutorostrata Balaenoptera musculus Balaenoptera physalus baleen whales toothed whales |
genre_facet |
Balaenoptera acutorostrata Balaenoptera musculus Balaenoptera physalus baleen whales toothed whales |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3443106 http://www.ncbi.nlm.nih.gov/pubmed/23024769 http://dx.doi.org/10.1371/journal.pone.0044854 |
op_rights |
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1371/journal.pone.0044854 |
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PLoS ONE |
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7 |
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9 |
container_start_page |
e44854 |
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1766366521043451904 |