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Transition of Eocene whales from land to sea: evidence from bone microstructure.

Houssaye A, Tafforeau P, de Muizon C, Gingerich PD - PLoS ONE (2015)

Bottom Line: Conversely, hind-limbs in basilosaurids became strongly reduced with no involvement in locomotion but display strong osteosclerosis in the femora.Our study confirms that Remingtonocetidae and Protocetidae were almost exclusively aquatic in locomotion for the taxa sampled, which probably were shallow water suspended swimmers.Basilosaurids display osseous specializations similar to those of modern cetaceans and are considered more active open-sea swimmers.

View Article: PubMed Central - PubMed

Affiliation: UMR 7179 CNRS/Muséum National d'Histoire Naturelle, Département Ecologie et Gestion de la Biodiversité, Paris, France; Steinmann Institut für Geologie, Paläontologie und Mineralogie, Universität Bonn, Bonn, Germany.

ABSTRACT
Cetacea are secondarily aquatic amniotes that underwent their land-to-sea transition during the Eocene. Primitive forms, called archaeocetes, include five families with distinct degrees of adaptation to an aquatic life, swimming mode and abilities that remain difficult to estimate. The lifestyle of early cetaceans is investigated by analysis of microanatomical features in postcranial elements of archaeocetes. We document the internal structure of long bones, ribs and vertebrae in fifteen specimens belonging to the three more derived archaeocete families--Remingtonocetidae, Protocetidae, and Basilosauridae--using microtomography and virtual thin-sectioning. This enables us to discuss the osseous specializations observed in these taxa and to comment on their possible swimming behavior. All these taxa display bone mass increase (BMI) in their ribs, which lack an open medullary cavity, and in their femora, whereas their vertebrae are essentially spongious. Humeri and femora show opposite trends in microanatomical specialization in the progressive independence of cetaceans from a terrestrial environment. Humeri change from very compact to spongious, which is in accordance with the progressive loss of propulsive role for the forelimbs, which were used instead for steering and stabilizing. Conversely, hind-limbs in basilosaurids became strongly reduced with no involvement in locomotion but display strong osteosclerosis in the femora. Our study confirms that Remingtonocetidae and Protocetidae were almost exclusively aquatic in locomotion for the taxa sampled, which probably were shallow water suspended swimmers. Basilosaurids display osseous specializations similar to those of modern cetaceans and are considered more active open-sea swimmers. This study highlights the strong need for homologous sections in comparative microanatomical studies, and the importance of combining information from several bones of the same taxon for improved functional interpretation.

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Left humerus of Qaisracetus arif.GSP-UM 3318 in virtual longitudinal (A) and transverse (B) sections. The longitudinal section is in posterior view. Scale bars equal 5 mm. Arrows point to LAGs. GC: growth center.
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pone.0118409.g007: Left humerus of Qaisracetus arif.GSP-UM 3318 in virtual longitudinal (A) and transverse (B) sections. The longitudinal section is in posterior view. Scale bars equal 5 mm. Arrows point to LAGs. GC: growth center.

Mentions: Only the distal half of a humerus is available. The mid-diaphysis is nevertheless well preserved. In longitudinal section, important variations in micro-organization occur along the shaft (Fig. 7A), as in the femur of Rodhocetus (see above). Around the center of growth, there is a small and off-center open medullary cavity in a spongious rather small medullary area that is surrounded by a thick layer of compact bone (Fig. 7B). Differences in grey levels (see Fig. 7) seem to indicate the transition between primary periosteal bone (light grey) and secondary bone of both periosteal and endochondral origin (dark grey), as suggested by the observation of LAGs in the light grey area. Periosteal bone appears thus only slightly remodelled. Compactness is very high around the growth center (CI = 91.7 and 92.5) and remains high at some distance from this point. However, it then strongly decreases proximally and distally towards the metaphyses because of thinning of the compact cortical layer and also transformation of the medullary area from more compacted to looser spongiosa (see Fig. 7A).


Transition of Eocene whales from land to sea: evidence from bone microstructure.

Houssaye A, Tafforeau P, de Muizon C, Gingerich PD - PLoS ONE (2015)

Left humerus of Qaisracetus arif.GSP-UM 3318 in virtual longitudinal (A) and transverse (B) sections. The longitudinal section is in posterior view. Scale bars equal 5 mm. Arrows point to LAGs. GC: growth center.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4340927&req=5

pone.0118409.g007: Left humerus of Qaisracetus arif.GSP-UM 3318 in virtual longitudinal (A) and transverse (B) sections. The longitudinal section is in posterior view. Scale bars equal 5 mm. Arrows point to LAGs. GC: growth center.
Mentions: Only the distal half of a humerus is available. The mid-diaphysis is nevertheless well preserved. In longitudinal section, important variations in micro-organization occur along the shaft (Fig. 7A), as in the femur of Rodhocetus (see above). Around the center of growth, there is a small and off-center open medullary cavity in a spongious rather small medullary area that is surrounded by a thick layer of compact bone (Fig. 7B). Differences in grey levels (see Fig. 7) seem to indicate the transition between primary periosteal bone (light grey) and secondary bone of both periosteal and endochondral origin (dark grey), as suggested by the observation of LAGs in the light grey area. Periosteal bone appears thus only slightly remodelled. Compactness is very high around the growth center (CI = 91.7 and 92.5) and remains high at some distance from this point. However, it then strongly decreases proximally and distally towards the metaphyses because of thinning of the compact cortical layer and also transformation of the medullary area from more compacted to looser spongiosa (see Fig. 7A).

Bottom Line: Conversely, hind-limbs in basilosaurids became strongly reduced with no involvement in locomotion but display strong osteosclerosis in the femora.Our study confirms that Remingtonocetidae and Protocetidae were almost exclusively aquatic in locomotion for the taxa sampled, which probably were shallow water suspended swimmers.Basilosaurids display osseous specializations similar to those of modern cetaceans and are considered more active open-sea swimmers.

View Article: PubMed Central - PubMed

Affiliation: UMR 7179 CNRS/Muséum National d'Histoire Naturelle, Département Ecologie et Gestion de la Biodiversité, Paris, France; Steinmann Institut für Geologie, Paläontologie und Mineralogie, Universität Bonn, Bonn, Germany.

ABSTRACT
Cetacea are secondarily aquatic amniotes that underwent their land-to-sea transition during the Eocene. Primitive forms, called archaeocetes, include five families with distinct degrees of adaptation to an aquatic life, swimming mode and abilities that remain difficult to estimate. The lifestyle of early cetaceans is investigated by analysis of microanatomical features in postcranial elements of archaeocetes. We document the internal structure of long bones, ribs and vertebrae in fifteen specimens belonging to the three more derived archaeocete families--Remingtonocetidae, Protocetidae, and Basilosauridae--using microtomography and virtual thin-sectioning. This enables us to discuss the osseous specializations observed in these taxa and to comment on their possible swimming behavior. All these taxa display bone mass increase (BMI) in their ribs, which lack an open medullary cavity, and in their femora, whereas their vertebrae are essentially spongious. Humeri and femora show opposite trends in microanatomical specialization in the progressive independence of cetaceans from a terrestrial environment. Humeri change from very compact to spongious, which is in accordance with the progressive loss of propulsive role for the forelimbs, which were used instead for steering and stabilizing. Conversely, hind-limbs in basilosaurids became strongly reduced with no involvement in locomotion but display strong osteosclerosis in the femora. Our study confirms that Remingtonocetidae and Protocetidae were almost exclusively aquatic in locomotion for the taxa sampled, which probably were shallow water suspended swimmers. Basilosaurids display osseous specializations similar to those of modern cetaceans and are considered more active open-sea swimmers. This study highlights the strong need for homologous sections in comparative microanatomical studies, and the importance of combining information from several bones of the same taxon for improved functional interpretation.

Show MeSH
Related in: MedlinePlus