Sclerosaurus and the evolution of turtle respiration

Lyson et al. 2014 brought us their view
on the origin of ventilation (= respiration) in turtles using fossils and extant taxa. Similarly, and in the same year, Hirasawa et al. 2014 did the same from a different perspective: turtle embryos.

Unfortunately
neither put their finger on the correct phylogenetic origins of turtles (Fig. 1) due to taxon exclusion. You can’t get a valid phylogenetic solution without a valid phylogeny.

Figure 1. Carbonodraco enters the LRT alongside another recent addition, Kudnu, at the base of the pareiasaurs + turtles.

Figure 2. Subset of the LRT focusing on the dual turtle clades (pink) and their ancestors.

Both sets of authors
overlooked/omitted the ancestor taxa of turtles recovered by the large reptile tree (LRT, 1694+ taxa; subset Fig. 1), which tested all current candidates for turtle ancestry. That means both sets of authors stepped into the morass that is convergence.

Figure 8. Sclerosaurus insitu. This turtle ancestor still bas a flexible spine, but the pectoral girdle has migrated anterior to the dorsal ribs. A hypoischiuum is present.

Figure 2. Sclerosaurus insitu. This turtle ancestor still bas a flexible spine, but the pectoral girdle has migrated anterior to the dorsal ribs. A hypoischiuum is present.

Here,
the LRT (subset Fig. 1) minimizes taxon exclusion due to its wide gamut of included taxa. Here turtles had dual origins from small horned pareiasaurs. Basal to hard-shell turtles, Elginia documents the genesis of cranial traits. Post-crania is poorly known. Basal to soft-shell turtles, Sclerosaurus (Figs. 2–4) documents the genesis of soft-shell turtle traits. These remain (at present) the best clues we have to the genesis of stem hard-shell turtle post-cranial traits. Those are lacking until we go back to the large pareisaur Bunostegos.

Figure 1. Softshell turtle ancestor, Sclerosaurus animated walking in dorsal view. Dorsal armor initially does nothing to prevents lateral undulation here, as shown by the in situ fossil.

Figure 1. Softshell turtle ancestor, Sclerosaurus animated walking in dorsal view. Dorsal armor initially does nothing to prevents lateral undulation here, as shown by the in situ fossil.

Key to the present discussion,
Sclerosaurus had a wide set of dorsal ribs that were not immobilized by the sprinkling of armor over the dorsal vertebrae. The specimen (Fig. 2) is preserved bending far to the left. So it undulated when it walked (Fig. 3). Sclerosaurus lacked a plastron and/or gastralia.

Figure 4. Sclerosaurus walking with an imagined ventral cross-brace, a plastron. Now this more closely resembles turtle locomotion.

Figure 4. Sclerosaurus walking with an imagined ventral cross-brace, like a turtle plastron. Now Scleromochlus locomotion more closely resembles turtle locomotion. Compare to figure 1.

Immobilzation of the thorax in soft shell turtles
occurs with the genesis of the plastron in Odontochelys (Fig. 5). If we give Sclerosaurus a hypothetical ventral cross brace to stiffen its thorax in the above animated graphic (Fig. 4), it suddenly walks like a turtle (Fig. 4). At first that permits breathing while walking by overcoming Carrier’s constraint. Extant turtles have such a low metabolism that breathing is the last thing they think to do. Sea turtles hold their breath for long periods underwater.

Immobilization of the thorax in Odontochelys
prevented costal ventilation (expanding the ribcage). This is reflected in turtle embryos, which lose intercostal muscles as they develop a rigid shell, according to Hirasawa et al. 2014. Three sets of internal thoracic (hypaxial) muscles take over respiration, expanding to press on the lungs between them or relaxing to initiate inspiration, according to Lyson et al. 2014.

Figure 3. Sister taxa according to Bever et al. Eunotosaurus purportedly nests between Ascerosodontosaurus and the turtles. The large reptile tree, on the other hand, finds that only the turtles are related to each other.

Figure 5. Sister taxa according to Bever et al. Eunotosaurus purportedly nests between Ascerosodontosaurus and the turtles. The large reptile tree, on the other hand, finds that only the turtles are related to each other.

Lyson et al. 2014 
suggested, “the ventilation mechanism of turtles evolved through a division of labour between the ribs and muscles of the trunk in which the abdominal muscles took on the primary ventilatory function, whereas the broadened ribs became the primary means of stabilizing the trunk.” Unfortuantely their ‘early member of the turtle stem lineage’ was the unrelated turtle mimic, Eunotosaurus (Figs. 5, 6). We discussed taxon exclusion errors several times earlier here, here and here.

Figure 3. Subset of the LRT with Martensius added to the base of the Caseasauria + another clade of similar lepidosaurs, all derived from Milleretta.

Figure 6. Subset of the LRT with Martensius added to the base of the Caseasauria + another clade of similar lepidosaurs, all derived from Milleretta. Note the placement of Eunotosaurus with sisters, none of which is close to turtles in the LRT.

Lyson et al. hypothesized,
“an easing of structural constraints through division of function (divergent specialization) between the dorsal ribs and the musculature of the body wall facilitated the evolution of both the novel turtle lung ventilation mechanism and the turtle shell.”
This is likely correct, but they used the wrong outgroup taxon, a turtle mimic, rather than a valid stem turtle. Lyson et al. thought the initial thoracic stiffening occurred in the carpace, as it does in Eunotosaurus, which lacks a plastron or more than 5 pairs of slender gastralia not in the radiating pattern of a plastron. Some Eunotosaurus specimens have overlapping ribs. Turtles don’t do this. Mutual side-by-side suturing is the turtle rib pattern and that’s just the beginning of a long list of non-turtle traits found n Eunotosaurus, which nests with Acleistorhinus and other near caseids in the LRT (Fig. 6), all with lateral temporal fenestrae, making them all synapsid mimics.

As you’ll note above,
Sclerosaurus does not have expanded ribs. They begin to expand with Odontochelys (Fig. 5). By contrast, the turtle-mimic, Eunotosaurus, has much more expanded dorsal ribs than those in Odontochelys. That’s the reverse of the order one would expect. The LRT indicates that Lyson et al. should have expanded their taxon list. Sins of omission are also considered sins in paleontology.

Lyson et al. fell prey to a classic error in paleontology
when they ‘Pulled a Larry Martin,‘ listing traits the turtle mimic, Eunotosaurus, shares with turtles. That’s why a good taxonomist saves listing traits until AFTER a comprehensive phylogenetic analysis determines what is related to what and what converges with what.

Hirasawa et al. 2014
attempted to provide ‘answers to the question of the evolutionary origin of the carapace… Along the line of this folding develops a ridge called the carapacial ridge (CR), a turtle‐specific embryonic structure.’ More important to the present discussion is the genesis of the plastron.

A little backstory on Sclerosaurus
Sclerosaurus armatus (Meyer 1859) Middle Triassic ~50 cm in length, was originally considered a procolophonid, then a pareiasaurid, then back and forth again and again, with a complete account in Sues and Reisz (2008) who considered it a procolophonid.

Here, based on data from Sues and Reisz (2008), Sclerosaurus nests between pareiasaurs and basal softshell turtles like ArganacerasOdontochelys and Trionyx. Their analysis also suffered from taxon exclusion. Sclerosaurus is also a sister to another small horned pareiasaur, Elginia and thus is only slightly more distantly related to Meiolania, the hard-shelled horned basalmost turtle in the LRT.

Overall smaller than other pareiasaurs, Sclerosaurus had a wide, flat body, like the horned lizard, Phrynosoma. The backbone remained quite flexible, as shown by the in situ fossil. Only a sparse sprinking of dermal bones lined the dorsal vertebrae. Note the hypoischium posterior to the ischium and the position of the pectoral girdle anterior to the dorsal ribs, as in Odontochelys.


References
Hirasawa T, Pascual‐Anaya J, Kamezaki N, Taniguchi M, Mine K and Kuratani S. 2015. The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage. J. Exp. Zool. (Mol. Dev. Evol.) 324B:194–207.
Lyson TR et al. (7 co-authors) 2014. Origin of the unique ventilatory apparatus of turtles. Nature Communications 5:5211.
Meyer H von 1859. Sclerosaurus armatus aus dem bunten Sandestein von Rheinfelsen. Palaeontographica 7:35-40.
Sues H-D and Reisz RR 2008. Anatomy and Phylogenetic Relationships of Sclerosaurus armatus (Amniota: Parareptilia) from the Buntsandstein (Triassic) of Europe. Journal of Vertebrate Paleontology 28(4):1031-1042. doi: 10.1671/0272-4634-28.4.1031 online

wiki/Sclerosaurus

Genesis of air breathing in basal tetrapods

The genesis of limbs and toes 
from lobes and fins gets most of the publicity in transitional fish-tetrapods.

Today we look at the less popular transition
from water breathing with gills to air breathing with a nose and lungs.

Like most fish,
Onychodus (Fig. 1) drew in oxygenated water by opening its mouth. At this moment, the gill covers are closed to prevent backdraft. Closing the mouth and raising the basihyal (medial bone between the mandibles) until it presses against the solid palate reduces the mouth volume, pushing that mouthful of  water posteriorly past the gills where oxygen and carbon dioxide are transferred. At this time the gill covers are open to permit that water to exit, completing the cycle. The dual nares have nothing to do with respiration at this point, only olfaction, with water passively entering the anterior opening and passively exiting the posterior opening (Fig. 1). The air bladder arising from the gut tube anterior to the stomach is not involved in respiration at this stage.

Among lobefin fish,
coelacanths, like Latimeria, have this primitive system.

Figure 1. Onychodus is typical of most fish having dual external nares strictly for olfactory sensing. Gill covers are part of the respiratory apparatus.

Figure 1. Onychodus is typical of most fish having dual external nares strictly for olfactory sensing. Gill covers are part of the respiratory apparatus.

Among lobefin lungfish (Late Silurian to present),
like Kenichthys (Fig. 2), Youngolepis, Polypterus (the extant bichir) and Howidipterus, oxygen-poor water, supplemented by gulps of dry air, once again enters the mouth and is passed back over the gills and out the gill covers. Both the incurrent and excurrent nares migrate ventrally. (Not sure why.) Worthy of a Nature article, the excurrent opening is parked on the jaw margin between the premaxilla and maxilla in Kenichthys, so half the excurrent exited outside the mouth, while the other half exited inside the mouth (see ventral view in Fig. 2), all passively. (Not sure why this migration took place either, except that with the lips sealed inhalation and exhalation can still take place… slowly… in and out of both openings, perhaps to retain mouth moisture during aestivation (hibernation in dry mud.) Note the pinprick size of each opening.

Figure 1. Kenichthys Images from Zhu and Ahlberg 2004, colors added. The authors made a convincing argument that Kenichthys represented a transitional taxon between Youngolepis and Eusthenopteron. Note the lack of vomer fangs and a distinctly different set of skull sutures in Kenichthys, which does not nest with Eusthenopteron in the LRT.

Figure 2. Kenichthys Images from Zhu and Ahlberg 2004, colors added. The authors made a convincing argument that Kenichthys represented a transitional taxon between Youngolepis and Eusthenopteron. Note the lack of vomer fangs and a distinctly different set of skull sutures in Kenichthys, which does not nest with Eusthenopteron in the LRT.

Among basal lobefin crossopterygians (Early to Late Devonian),
like Gogonasus, Eusthenopteron, and elongate, flattened Cabonnichthys, Elpistostege, Tiktaalik and Panderichthys the tiny excurrent nasal opening just barely enters the rim of the mouth cavity and is thereafter considered a choana. The tiny external incurrent opening is thereafter considered a naris. Based on their tiny sizes, both remain useless for respiration. Large gill covers and a solid palate are retained for traditional water respiration supplemented by dry air gulping as needed.

Figure 4. Panderichthys palates. Note the lateral line below the naris is not continuous, contra Lombard and Bolt.

Figure 3. Panderichthys palates. Note the lateral line below the naris is not continuous, contra Lombard and Bolt.

When the gill covers disappear in fossil taxa
that signals the genesis of air-breathing from mouth to paired air bladders (now called ‘lungs’) rather than past the disappearing gills. According to the LRT, this occurred twice (if we don’t count the ontogenetic transformation of juvenile tadpoles (with gills) to adult frogs (with lungs) and other similar basal tetrapods).

In clade one: primitive Koilops retained and operculum (gill cover). Derived, but lobe-finned Tiktaalik and Spathicephalus did not have an operculum.

In clade two: weak limbed, four-fingered Trypanognathus (Fig. 4), Deltaherpeton, Collosteus, PholidogasterGreererpeton and Ossinodus, all lacked an operculum.

Figure 2. Animation of air-breathing in basal tetrapods with weak lungs inflated by contraction and expansion of the throat sac, rather than gill irrigation powered by the reduced here buccal bones.

Figure 4. Animation of air-breathing (tidal ventilation) in basal tetrapods with weak lungs inflated by contraction and expansion of the throat sac, rather than gill irrigation powered by the reduced ceratobranchials, still present at right. Air-tight nose flaps had to be present in order for this system to work. 

Clade two exceptions: Robust-limbed, eight-fingered Acanthostega (Fig. 5) and Ichthyostega retained tiny gill covers (operculum) as adults. And they had primitive tiny nares and choana, still not suitable for air-breathing. These convergent exceptions are here considered reversals due to a suite of derived traits nesting these two famous taxa apart from more primitive tetrapods and apart from each other in the LRT.

Figure 2. the MGUH VP 8160 specimen attributed to Acanthostega. Note the many similarities to Ymeria.

Figure 5. the MGUH VP 8160 specimen attributed to Acanthostega. Note the many similarities to Ymeria. Note the spiracle openings surrounded by the supratemporals. This provides an accessory respiration opening, convergent with bottom-dwelling skates and rays from the shark clade.

The signal that air-breathing respiration through the nostrils had begun
(Fig. 4) is when the nares and choana of fossil taxa enlarge to handle the larger volume of tidal ventilation coming through them. The nares also migrate higher on the skull so that they are at least partly visible in dorsal view. The internal nares are fully inside the mouth, which must be able to seal shut to divert air through the nares, rather than leaking past the lips. Gill covers are absent. Air-tight nose flaps had to be present in order for this system to work. The pterygoids reduce and retreat posteriorly (Fig. 4), creating large, pliable openings in the formerly solid palate (Fig. 3), expanding the potential volume of the mouth.

According to the LRT,
(subset Fig. 5) the enlargement and migration of the nares and choana occurred several times because several clades of derived basal tetrapods retained tiny lateral nares and choana despite having fully developed limbs.

Figure 3. Subset of the LRT focusing on basal tetrapods and their narial openings.

Figure 5. Subset of the LRT focusing on basal tetrapods and their narial openings.

Dorsal ribs
Basal tetrapods depend on an expanding and contracting the gular sac for tidal ventilation of the lungs, mimicking their lobe-finned ancestors. These same basal tetrapods (Fig. 6) were all low and wide with relatively straight, laterally-oriented ribs incapable of expanding and contracting the torso and lungs. Not until dorsal ribs elongated and started curling around the inside of an increasingly round (in cross-section) torso where they able to expand and contract the volume of the torso and the lungs inside. In that way mobile ribs gradually replaced a mobile throat sac for tidal ventilation.

Figure 6. Dorsal and ventral views of Panderichthys and several basal tetrapods demonstrating the low, flat skulls and bodies with small limbs and relatively straight ribs.

Figure 6. Dorsal and ventral views of Panderichthys and several basal tetrapods demonstrating the low, flat skulls and bodies with small limbs and relatively straight ribs, all to scale. Note the brevity of the tail in thee taxa.

The irony is
we know of Ichthyostega-grade tetrapods walking on land in the Middle Devonian. By that I mean, we know of tetrapods with relatively large limbs and supernumerary digits capable of elevating the belly off the substrate. Phylogenetic analysis indicates the trackmaker was a mouth-breather with tiny lateral nares. This was a short-lived experiment (as far as we know at present) leaving only Late Devonian descendants, like Icthyostega, that disappeared by the Early Carboniferous.

The longer lasting clade,
the one that produced all the other tetrapods including reptilomorphs, living amphibians and microsaurs, all had a long, low, flat body and skull with smaller 4-fingered limbs not capable of elevating the belly off the substrate, like Greererpeton and Trimerorhachis (Fig. 6). Only later, and by convergence did descendants rise off their belly with stronger limbs, mimicking those pioneer Middle Devonian tetrapod trackmakers.


References
Schoch RR and Voigt S 2019. A dvinosaurian temnospondyl from the Carboniferous-Permian boundary of Germany sheds light on dvinosaurian phylogeny and distribution. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2019.1577874.xxx

This blogpost comes not in response to a new academic paper, but to revisiting some of the taxa in the the large reptile tree (LRT, Figs. 5, 6) at this transition. Thanks to reader Dave M for the impulse to reexamine these taxa.

 

 

 

Gill chambers in basal chordates and vertebrates, pt. 2

Yesterday we looked at several basal chordates
that use their large atria / gill chambers to capture planktonic prey. Today, we’ll peek at a few morphologies that modify the gill chamber in diverse ways and take planktonic feeding to new levels in prehistoric and extant taxa.

We’ll start with a taxon we looked at yesterday,
the Middle Cambrian first fish: Metaspriggina (Fig. 1). It had relatively few body parts. The torso was dominated by swimming muscles, followed by the much smaller gill chamber, liver, gut, heart and eyes, in that order.

Figure 1. An early jawless, finless, lancelet-like fish from the Cambrian, Metaspriggina. Compare the placement of the eyes here with Birkenia in figures 2 and 3.

Figure 1. An early jawless, finless, lancelet-like fish from the Cambrian, Metaspriggina. Compare the placement of the eyes here with Birkenia in figures 2 and 3.

Ordovician Arandaspis
took body armor to turtle-like heights with a dorsal carapace and ventral plastron along with armored gill openings (Fig. 2) surrounding this basal fish / advanced lancelet. Compared to Metaspriggina (Fig. 1, the gill chamber of the Panserfische, Arandaspis, was several times larger, still servicing a small oral cavity. The eyes were still tiny and faced only forwards. Evidently Arandaspis wasn’t concerned with prey sneaking up from behind. If swallowed, it might have been too tough to bite and digest. No predatory arthropods could dismantle it. Like ancestral lancelets, perhaps Arandaspis burrowed into sandy sea floors.

FIgure 3. Arandaspis lived inside its gill chamber shell and armored tail.

FIgure 2. Arandaspis lived inside its gill chamber shell and armored tail.

Late Silurian Poraspis
 (Fig. 4) had fewer and larger tail plates. All gill plates were fused into one with a single lateral atrial water exit on the sides. The skull plates remained large and solid, protecting the head, still dominated by the enormous atrium / gill chamber. With the first appearance of a rostrum since the lancelet, Branchiostoma, the eyes moved laterally, protected by knight-like armor. Lateral line sensory canals first appear in such taxa.

Figure 4. Poraspis fuses the lateral gill plates together for greater armor, leaving only a slender single common opening for the exiting water. This was probably a sedentary taxon due to its inability to respire at a great rate.

Figure 3. Poraspis fuses the lateral gill plates together for greater armor, leaving only a slender single common opening for the exiting water. This was probably a sedentary taxon due to its inability to respire at a great rate.

Early Devonian Drepanasipis
evolved a flattened armor to protect its huge gill chamber with posterior atrial openings. 

Figure 4. The large gill chamber (cyan) of Early Devonian Drepanaspis.

Figure 4. The large gill chamber (cyan) of Early Devonian Drepanaspis.

Distinctly different was Middle Silurian Birkenia
(Fig. 5). This late survivor from an early undocumented Ordovician radiation did not have stiff, plate-like armor like AndraspisPoraspis and Drepanaspis (above). Instead Birkenia was surrounded, supported and protected by hundreds of splinter-like, interwoven cartilage / bone, permitting much greater flexibility for this more mobile taxon. The tail fin was new, improving the efficiency of the swimming muscles. Small, barely mobile pectoral fins first appeared here. The eyes were larger, still protruding dorsally like those of Metaspriggina (Fig. 1) or a mudskipper like Periophthalmus. The rostrum of Birkenia extended anteriorly beyond the eyes. The oral cavity remained lancelet-like and lancelet-sized, with cilia surrounding the ventral opening. Likewise, the atrium / gill chamber remained relatively small. Nine gill openings were retained, a few more than in Metaspriggina (Fig. 1).

Figure 2. Birkenia is basically an armored Metaspriggina with a tail fin.

Figure 5. Birkenia is basically an armored Metaspriggina with a tail and pectoral fin.

These newest members of
the large reptile tree (LRT, 1611+ taxa; Fig. 6) nest at the base, helping us understand relationships among major groups, which have shifted slightly since their addition.

Figure 4. Subset of the LRT with the addition of several jawless taxa.

Figure 6 Subset of the LRT with the addition of several jawless taxa.

Metaspriggina walcotti (Simonetta and Insom 1993; Morris and Caron 2014; Cambrian, 500 mya; up to 10cm) is an early chordate, naked, jawless and finless, but with two anterodorsal eyes. The orbits comprise the proto-skull. The swimming muscles are larger, so this was probably a mobile feeder, using its eyes to seek prey and avoid predators. Not sure if an atriopore is present here, or if gill slits opened directly.

Arandaspis prionotolepis (Ritchie and Gilbert-Tomlinson 1977; Ordovician, 465mya; 15 cmlong) is a member of the Arandaspididae that looked like a large, armored tadpole. This jawless, finless filter feeder was basically an armored lancelet, like Metaspriggina, with a much larger gill chamber and a tail to improved propulsion. Both eyes and nostrils faced forward above the jawless mouth. Several armored gill slits appeared between the dorsal carapace and ventral plastron.

Poraspis brevis (Kiaer 1930; Late Silurian to Early Devonian, 410mya) is traditionally considered a member of the Heterostraci.

Drepanapis gemuendenensis (Schlüter 1887; Gross 1963; Early Devonian 405mya) was a flattened arandaspid with a superficially ray-like armored body. The common gill opening exited posteriorly. This bottom feeder with widely-spaced eyes is traditionally considered a member of the Heterostraci. This skull differs from diagrams produced by Gross 1963.

Birkenia elegans (Traquair 1899; Middle Silurian; up to 10cm) is a jawless, finless chordate with scales, twin nostrils and a hypocercal tail. Bony hooks top the dorsal region. Cilia line the permanently open jaws. Gill bars and gill openings are present. Birkenia is ancestral to Hemicyclaspis and the sturgeon Pseudoscaphirhynchus, along with all other extant fish and tetrapods.

Tomorrow,
we’ll look at several more taxa dominated by their gill chambers.


References
Kiaer J and Heintz A 1935. The Downtonian and Devonian vertebrates of Spitsbergen. V. Suborder Cyathaspida. Part I. Tribe Poraspidei, Family Poraspidae Kiaer. Skrifter om Svalbard og Ishavet 40:1-138.
Ritchie A and Gilbert-Tomlinson J 1977. First Ordovician vertebrates from the Southern Hemisphere. Alcheringa 1:351-368.
Simonetta AM and Insom E 1993. New animals from the Burgess Shale (Middle Cambrian)and the possible significance for the understanding of the Bilateria. Bolletino Di Zoologia 60:97–107.
Traquair RH 1899. Report on fossils fishes. Summary of Progress of the Geological Survey of the United Kingdom for 1897: 72-76.

wiki/Branchiostoma
wiki/Metaspriggina
wiki/Arandaspis
wiki/Poraspis
wiki/Birkenia
wiki/Drepanaspis

Sauropod nostrils: Where were they?

Short answer:
For whatever reason, derived sauropods shifted the external naris away from the mouth. It would appear illogical to extend soft nostrils back close to the mouth, as Witmer 2001 proposes, over the exterior of the maxillary basin (Fig. 1), which varies greatly (Fig. 2).

Figure 1. From Witmer 2001 showing brachiosaur sauropod skull, colors added. Witmer suggests the nostril might have been located at point 'B' in the maxillary basin (blue) rather than in the external naris (red).

Figure 1. From Witmer 2001 showing brachiosaur sauropod skull, colors added. Witmer suggests the nostril might have been located at point ‘A’ of ‘B’ in the maxillary basin (blue) rather than in the external naris (red).

Witmer 2001 proposed an anterior nostril position
within the nasal basin anterior to the bony external naris in sauropods (positions A and B in Fig. 1, green dot in Fig. 2) and a similar anterior position in other dinosaurs based on an anterior position in most lepidosaurs, crocs and birds. In every photo example presented by Witmer the nostril forms only a small opening relative to the bony external naris.

Witmer 2001 also provided several exceptions to that pattern:

  1. “Cormorant (Phalacrocorax) simply lacked a ßeshy nostril altogether (a diving adaptation)
  2. The bony nostril of geckos is so small that the fleshy nostril occupied almost its entire extent.
  3. The most significant exception was among monitor lizards (Varanus). Some species (e.g., V. griseus, V. dumerili, V. exanthematicus) have a fleshy nostril located in the middle to caudal half of the much enlarged bony nostril.”
  4. Witmer concludes: “Given the diversity of amniotes, one would expect to find additional exceptions.”

As everyone knows,
all tetrapods are capable of inhaling and exhaling through the mouth, which becomes important in panting for internal cooling and when exercise requires more oxygen. The external naris is principally for olfaction and the anterior position of the nostril within the naris maximizes the amount of soft tissue that can be exposed to incoming odors and pheromones.

Figure 1. Four sauropods with external nares identified in pink, internal nares in blue.

Figure 2. Four sauropods with external nares identified in pink, internal nares in blue, Witmer’s proposed nostril in green. Note the external naris already forms a restriction to the airway. For whatever reasons, more derived sauropods phylogenetically shift the nares away from the mouth. Thus there seems to be little reason to imagine the nostrils maintaining an anterior position, nor any reason to further restrict the dimensions of the nostril. When dipping the head down to drink, the internal naris were able to fill with water that drained into the throat whenever the skull was elevated.

A tracing of the external and internal nares in sauropods
(Fig. 2) and a simplified guess connecting the two in lateral view, shows

  1. the elevation of the external naris (pink) relative to the internal naris (blue)
  2. the spacious airway (blue) in sauropod skulls.
  3. the reduced airway proposed by Witmer (green) if skin extended the external naris to the anterior nasal basin
  4. the easy drainage of rainwater if allowed to directly enter the nostrils (pink) in sauropods (probably unimportant, but thought I’d mention it since most nostrils/nares, except whales and crocs, are anterior to lateral, not dorsal)
  5. When dipping the head down to drink, the internal naris were able to fill with water that drained into the throat whenever the lips were sealed and the skull was elevated. That is marginally different from the ostrich drinking behavior (below).
  6. Based on the ostrich example, the sauropod nostril may have extended from 1/3 to 2/3 the area of the external naris in brachiosaurs, to the entire naris in the relatively small external naris of Diplodocus (Fig. 2).

Witmer 2012 (YouTube video below)
provided an ostrich skull in which tissue labeled ‘airway’ completely filled the external naris.

Unfortunately,
the Witmer video does not show the nostril seen in an ostrich photo (Fig. 3). Confusing. That should have been somehow clarified, because the nostril is present in vivo, not in the µCT scan. Added January 22, 2019: The external naris above is the yellow patch at the far anterior tip of the naris. Thank you JB.

Figure 3. Ostrich skull compared to ostrich head with nostril appearing within the external naris.

Figure 3. Ostrich skull compared to ostrich head with nostril appearing within the external naris. The skull may belong to a younger ostrich with a higher cranium than the adult shown here. Note the nostril is about 1/3 the size of the external naris. This may be instructive considering the small head on the end of a long neck on this ostrich, comparable to the small head and long neck in sauropods.

Added January 22, 2019: The following image of a young ostrich
still does not fit the Witmer 2001 ostrich skull. Even when distorted to fit the skull (Fig. 4) the naris does not match the red patch provided for clarification. Something is wrong here. Who can help?

Figure 4. Baby ostrich naris still does not match patch from Witmer 2012 video.

Figure 4. Baby ostrich naris still does not match patch from Witmer 2012 video.

The small head on the end of a long neck
of an ostrich is analogous to the small head and long neck of sauropods when it comes to breathing and drinking. In the ostrich the nostril is one third the size of the naris and located within the naris, more or less anteriorly. Drinking would have been similarly done, with similar problems to get over, like transferring a throat-full or snout-full of water to the stomach by elevating the head and neck.

In a future post
we’ll look, from a scientist’s perspective, why scientists shy away from attempting to replicate discoveries. On the other hand, I revel in testing published hypotheses because so often they leave their work unfinished or misguided one way or another. All the loose ends need to be tidied up.

References
Witmer LM 2001. Nostril position in dinosaurs and other vertebrates and its significance for nasal function. Science 293, 850-853. PDF

Caseid diaphragms? Bogus, bogus, bogus…

Lambertz et al. 2016 imagine
a diving aquatic niche for caseids like Cotylorhyhnchus (Fig. 1), and in order to breathe upon surfacing, a mammal-like diaphragm must have been present.

One of the authors, Dr. Steven Perry, has been working on the origin of the diaphragm for many years. Perry et al. 2010 wrote: despite over 400 years of research into respiratory biology, the origin of this exclusively mammalian structure remains elusive.” (But see below)

According to Wikipedia: “Mammals have diaphragms, and other vertebrates such as amphibians and reptiles have diaphragm-like structures, but important details of the anatomy vary, such as the position of the lungs in the abdominal cavity.” 

And Tegu lizards are known to possess a proto-diaphragm, which separates the pulmonary cavity from the visceral cavity. While not actually capable of movement, it does allow for greater lung inflation, by taking the weight of the viscera off the lungs.”

And “Crocodilians have a muscular diaphragm that is analogous to the mammalian diaphragm. The difference is that the muscles for the crocodilian diaphragm pull the pubis (part of the pelvis, which is movable in crocodilians) back, which brings the liver down, thus freeing space for the lungs to expand.” 

And this important and pertinent note to pet lizard owners:
“If you turn them over and stroke their bellies, they zonk out… Cute?.. NO, Stop! Lizards do not have diaphragms to help them breath. Their ribs moving in and out actually cause their lungs to inflate and deflate. When a dragon is held upside down or on its back, its stomach pushes on its lungs making it difficult for it to breath and will eventually result in suffocation.” Other similar cautionary notes are compiled here.

Unfortunately, Lambertz et al. also revert to an old invalid tradition,
that caseids are basal synapsids. For over five years it has been known that caseids are not basal to synapsids. The large reptile tree nests caseids as sisters to Feeserpeton and Australothyris and all are derived from a sister to Milleretta within the Lepidosauromorpha, not the Archosauromorpha, in which the Synapsida nests. Thus if you want to know if caseids had a diaphragm, you need to look at living lizards, all of which lack a working diaphragm.

Cotylorhynchus romeri

Figure 1. Cotylorhynchus romeri. Extant lizards lack a diaphragm, so caseids also lacked a daphragm.

Given that backstory Lambertz et al. report:
“The origin of the diaphragm remains a poorly understood yet crucial step in the evolution of terrestrial vertebrates, as this unique structure serves as the main respiratory motor for mammals. Here, we analyze the paleobiology and the respiratory apparatus of one of the oldest lineages of mammal-like reptiles: the Caseidae. [1] Combining quantitative bone histology and functional morphological and physiological modeling approaches, we deduce a scenario in which an auxiliary ventilatory structure was present in these early synapsids. Crucial to this hypothesis are indications that at least the phylogenetically advanced caseids might not have been primarily terrestrial but rather were bound to a predominantly aquatic life. Such a lifestyle would have resulted in severe constraints on their ventilatory system, which consequently would have had to cope with diving-related problems. [2] Our modeling of breathing parameters revealed that these caseids were capable of only limited costal breathing and, if aquatic, must have employed some auxiliary ventilatory mechanism to quickly meet their oxygen demand upon surfacing. [3] Given caseids’ phylogenetic position at the base of Synapsida [4] and under this aquatic scenario, it would be most parsimonious to assume that a homologue of the mammalian diaphragm had already evolved about 50 Ma earlier than previously assumed.” [5]

  1. Not valid for the last five years. Caseids are derived from millerettids and are related to non-synapsids with a convergent lateral temporal fenestra. Hence the confusion.
  2. No one imagines caseids as divers. Maybe shoulder deep in shallow streams.
  3. Diving turtles have no such problems upon surfacing.
  4. Wrong again. See above.
  5. This is a ‘just-so’ story built on taxon exclusion and a couple of big IFs. See below for a hypothesis built on phylogenetic bracketing and skeletal morphology.

So while we’re on the topic of diaphragms,
let’s take a look at another possibility in stem mammals. Since basalmost mammals, like the platypus, Ornithorhynchus, have a diaphragm we’re looking for the origin of this lung muscle in earlier taxa.

A likely place to look 
is at the transition from lateral undulation to limb rotation during locomotion. Only at that stage, where both lungs can inflate simultaneously during locomotion (see Carrier’s constraint), can the diaphragm develop.

Figure 2. Chiniquodon had erect hind limbs and sprawling forelimbs, the first stage in parasagittal locomotion, a requirement for the invention of the diaphragm.

Figure 2. Procynochus, Thrinaxoon, Chiniquodon transition to erect hind limbs while keeping sprawling forelimbs. This was the first stage in parasagittal locomotion, a requirement for the invention of the diaphragm and the most likely stage for its origin.

That transition began with the hind limbs on
derived cynodonts (Fig. 2) which slowly evolved parasagittally rotating hind limbs while retaining sprawling fore limbs. Monotreme mammals continue to retain sprawling forelimbs. Parasagittal forelimbs first appear with Juramaia and the later Therians.

Coincidentally (#1)
The lumbar ribs began to shrink in derived cynodons (Fig. 2) disappearing completely in basalmost mammals.

Coincidentally (#2)
The dorsal rib cage becomes pear-shaped in dorsal view (Fig. 3), with narrower ribs anteriorly and wider ribs posteriorly, near the developing diaphragm.

Coincidentaly (#3)
The dorsal vertebrae become differentiated into dorsal and lumbar vertebrae with neural spines angled posteriorly and anteriorly respectively and shorter and longer vertebral lengths respectively.

Coincidentally (#4)
Sternal ribs, sternebrae, a manubrium and xiphoid process all appear in basalmost mammals, likely signaling the completion of the evolution of the diaphragm.

Coincidentally (#5)
the vertebral column in vivo develop an arch in lateral view (Fig. 3) with a rise to the base of the rib cage followed by a lumbar decent to the sacrals.

Coincidentally (#6)
The external nares become anteriorly oriented, confluent and the premaxillary ascending process disappears, facilitating greater volumes and velocities with every breath.

Figure 1. Megazostrodon, an early mammal, along with Hadrocodium, a Jurassic tiny mammal.

Figure 3 Megazostrodon, an a Jurassic mammal, along with Hadrocodium, a Jurassic tiny mammal.

In summary
in the transition from Cynodontia to Mammalia many changes occurred in the rib cage. Such changes are the most likely skeletal markers for the origin of the soft tissue diaphragm. Such changes are not seen in caseids, which, in any case, are related to lizards not mammals.

I have not read the Lambertz paper,
only the abstract, but with caseids unrelated to mammals, they are sadly barking up the wrong tree. Based on a false premise, that paper was a complete waste of time to produce. Build your papers on a solid phylogenetic foundation and everything will into place naturally.

References
Lambertz M, Shelton CD, Spindler F & Perry SF 2016. A caseian point for the evolution of a diaphragm homologue among the earliest synapsids. Annals of the New York Academy of Sciences (advance online publication) DOI: 10.1111/nyas.13264. http://onlinelibrary.wiley.com/doi/10.1111/nyas.13264/full
Merrell AJ and Kardon G 2013. Development of the diaphragm – a skeletal muscle essential for mammalian respiration. FEBS Journal 280(17): 4026-4035.
Perry SF, Similowski T, Klein W and Codd JR 2010. The evolutionary origin of the mammalian diaphragm. Repiratory Physiology & Nuerobiology 171(1):1-16.
Zimmer C. 2015. Behind Each Breath, an Underappreciated Muscle. The New York Times 04/07/2015.

Where are the internal nares in plesiosaurs?

Simosaurus and Anningasaura. Somewhere between these two the internal and external nares of these protoplesiosaurs became much smaller, almost useless vestiges. Apparently breathing continued through the mouth alone.

Figure 1. Simosaurus and Anningasaura. Somewhere between these two the internal and external nares of these protoplesiosaurs became much smaller, almost useless vestiges. With such a tiny nostril in Anningsaura, apparently breathing continued through the mouth alone. The placement of the internal nares did not shift much. Is that a secondary choana (internal naris) between the pterygoids? Probably not because it’s not much larger than the real choana, so no advantage. There is no medial extension of the maxilla here as in other reptiles with a secondary palate (see below).

The recent paper on pliosaur palates by Schumacher et al. (2013) considered the placement of the internal nares in plesiosaurs (Figs. 1, 3). They noted Buchy et al. (2006) questioned the various placements and offered evidence for a functional secondary palate in plesiosaurs, shifting the internal nares to the back of the palate, posterior to the pterygoids, similar to the situation in crocodilians (Fig. 2). However in crocs, as you can see, the maxillae and palatines contact medially producing a standard sort of secondary palate.

The palate of Alligator. Note the posterior placement of the internal nares with paired maxillae, palatines and pterygoids forming the secondary palate.

Figure 2. The palate of Alligator. Note the posterior placement of the internal nares with paired maxillae, palatines and pterygoids forming the secondary palate.

The traditional view
holds that a pair of very small openings in the anterior half of the plesiosaur palate (Figs. 1,3), anterior to the palatines, represent the internal nares through which respiration took place.

Another traditional view
Williston (1903) accepted such a position for Dolichorhynchops, but not for Brachauchenius. Instead, despite the retention of internal nares in the traditional place, Williston placed the internal nares between the pterygoids separated by the parasphenoid (see Plesiosaurus in figure 3) as in crocodilians.

More recently, Schumacher et al. (2013) reported, “We have independently concluded that the posterior interpterygoid vacuity…should be called the internal nares.”

The Schumacher Hypothesis
Such a posterior position of the internal naris would be due to the development of a secondary palate in plesiosaurs, according to Schumacher et al. (2013). Benefits: Shifting the internal nares posteriorly, as in crocodiles, separates nasal respiration from oral functions (like biting, chewing, reorienting and swallowing). Problems: Small nares restrict air passage and ventilation. Since the posterior openings are typically slightly larger than the anterior ones Schumacher et al. (2013) suggest that the shift was made by soft tissue within the skull and the tiny anterior openings would have been covered with mechanosensory or chemosensory tissue, thereby completely blocking respiration there. According to Schumacher et al. (2013) respiration would then have taken place at the back of the palate where the slightly larger interpterygoid opening is.

Enaliosaur palates

Figure 3. Click to enlarge. Enaliosaur palates beginning with Claudiosaurus (upper left). The internal nares shrink in Anningasaurus, Pisotosaurus and Plesiosaurus compared to Simosaurus and Pachypleurosaurus. The palate is open posteriorly only in Plesiosaurus, but that does not appear to be a channel for respiration.

Sea turtle with secondary palate. Here the palatines join medially to shelve the respiratory tract and shifting the internal nares to mid palate.

Figure 4. Sea turtle with secondary palate. Here the palatines join medially to shelve the respiratory tract and shifting the internal nares to mid palate. From Brown and Madara 2000. See Proganochelys for a turtle without a secondary palate.

Of course
All that presupposes that plesiosaurs actually breathed through those tiny nostrils and internal nares. Maybe they didn’t. Maybe, once the nares became sufficiently tiny (vestigial), plesiosaurs began to breathe through their mouth, like the sea turtle in figure 5. This makes all the more sense in hyper-long-necked elasmosaurs, as the mouth offers no respiratory restrictions while elevating the skull above the water surface (even slightly above as in fig. 5). This also makes sense in giant-jawed pliosaurs where breathing might have taken place with the jaws just barely open and air respiring between the slightly gaped giant teeth, perhaps while “spy-hopping,” or during less obvious maneuvers.

Figure 6. Sea turtle breathing at the surface. Both the nares and the mouth are open. (Photo by Joe Raedle/Getty Images)

Figure 5. Sea turtle breathing at the surface. Both the nares and the mouth are open. (Photo by Joe Raedle/Getty Images)

Phylogeny Clues
If we look at a series of plesiosaurs and their ancestors (Fig. 6) we see that Claudiosaurus, with its tiny skull, had the relatively largest internal nares. The nothosaurs (Pachypleurosaurus, Lariosaurus, Simosaurus (Fig. 1) had a smaller, but still substantial internal naris. In contrast, Anningasaura and Pistosaurus had vestigial internal nares, obviously unusable for respiration. Other marine taxa (Fig. 3) also had tiny internal nares.

Something changed.
Between Simosaurus and Anningasaura both the internal and external nares shrank to vestiges (Fig. 1). I think it’s likely that Anningasaura and its plesiosaur and pliosaur descendants were breathing through their mouth.

Secondary palate development in a series of synapsid cynodonts leading to mammals.

Figure 6. Secondary palate development in a series of synapsid cynodonts leading to mammals. In  the eutheriodont and Procynosuchus the secondary palate is incomplete. In Thrinaxodon and all subsequent cynodonts, including all mammals, the secondary palate is complete when the maxillary palatal processes meet each other along with the palatine palatal processes. Note the gradual posterior shift of the internal naris from Thrinaxodon to Morganucodon. Image from Hopson 1991.

In a real secondary palate,
as in synapsids (Fig. 6), the development of a secondary palate (maxillae and palatines meet medially) can be traced through a series of fossils. The same holds true for crocodilians (Fig. 2, see Scleromochlus and Terrestrisuchus for taxa without a palate), sea turtles (see Proganochelys for a taxon without a palate) and pterosaurs (Fig. 7, see Cosesaurus for the primitive condition). Champsosaurus doesn’t have a secondary palate, just a longer snout and the internal nares stayed put.

Evolution of the pterosaur palate from Eudimorphodon to Pterodaustro.

Figure 7. Click to enlarge. Evolution of the pterosaur palate from Eudimorphodon to Pterodaustro. The secondary palate formed by maxillary palatal processes meeting at the midline shift the internal nares posteriorly. A similar expansion of the maxillae and migration of the internal nares is not documented in sauropterygians.

Sauropterygians do not document a similar gradual shift of the internal nares. Rather the nares simply shrinks reflecting a lack of usage while shifting to respiration through the mouth. There is no medial extension of the maxilla or palatine. Various valves would have been present to open and shut the esophagus (to the stomach) and epiglottis (to the lungs). Otherwise, no bony changes document the development of a secondary palate as in other reptiles (contra Schumacher et al. 2013). And there’s no real benefit to that marginally larger interpterygoid opening. The presupposition that the nares were used for breathing is at the heart of the problem. The problem goes away when that supposition goes away.

References
Buchy M-C, Frey E and Salisbury  2006. Internal cranial anatomy of Plesiosauria (Reptilia, Sauropterygia): evidence for a functional secondary palate. Lethaia 39:290-303.
Hopson JA 1991. Systematics of the nonmammalian Synapsida and implications for patterns of evolution in synapsids, in H-P Schultze & L Trueb [eds], Origins of the Higher Groups of Tetrapods: Controversy and Consensus. Comstock, pp. 635-693.  Schumacher BA, Carpenter K and Everhart MJ 2013. A new Cretaceous Pliosaurid (Reptilia, Plesiosauria) from the Carlile Shale (middle Turonian) of Russell County, Kansas. Journal of Vertebrate Paleontology 33(3):613-628.