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Lunge feeding in early marine reptiles and fast evolution of marine tetrapod feeding guilds.

ABSTRACT: Traditional wisdom holds that biotic recovery from the end-Permian extinction was slow and gradual, and was not complete until the Middle Triassic. Here, we report that the evolution of marine predator feeding guilds, and their trophic structure, proceeded faster. Marine reptile lineages with unique feeding adaptations emerged during the Early Triassic (about 248 million years ago), including the enigmatic Hupehsuchus that possessed an unusually slender mandible. A new specimen of this genus reveals a well-preserved palate and mandible, which suggest that it was a rare lunge feeder as also occurs in rorqual whales and pelicans. The diversity of feeding strategies among Triassic marine tetrapods reached their peak in the Early Triassic, soon after their first appearance in the fossil record. The diet of these early marine tetrapods most likely included soft-bodied animals that are not preserved as fossils. Early marine tetrapods most likely introduced a new trophic mechanism to redistribute nutrients to the top 10 m of the sea, where the primary productivity is highest. Therefore, a simple recovery to a Permian-like trophic structure does not explain the biotic changes seen after the Early Triassic.

SUBMITTER: Motani R

PROVIDER: S-EPMC4354009 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project 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 VO2 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 VO2|max. 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.

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Lunge feeding in early marine reptiles and fast evolution of marine tetrapod feeding guilds.

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