One more look at Rhamphorhynchus growth

Powered flight is one of the most energy-consuming locomotion types in tetrapods, therefore high growth rates and a superprecocial onset of the flying lifestyle in a highly developed hatchling are mutually exclusive developmental parameters. The validity of this simple trade-off model is supported by the fact that the only extant superprecocial fliers, the megapod birds have very low if not the lowest growth rates among extant birds.” Prondvai et al. ignore the fact that megapodes have their rapid growth phase inside the egg shell. Hatchling megapodes are relatively “very large with a wingspan up to half that of the adult).”  By contrast, pterosaurs hatch at 1/8 the height of the adult and 1/8 the wingspan.

In support of supreprecocial flight…
…pterosaur hatchlings had adult proportions. Tiny adults, the size of sparrows and hummingbirds, had larger pterosaur proportions. The smallest pterosaur that Prondvai et al. tested had wing tips that extended way over their heads when folded and quadrupedal (Figs. 1, 2). We’ve seen the short wings of flightless pterosaurs. Hatchlings of volant taxa don’t have short wings. Tiny adult pterosaurs may have ‘rapidly growing” bone microstructure because they matured quickly, reproduced as often as possible then died early, like tiny mammals do. More on this below:

Sexual maturity vs. size:
Prondvai et al. report, “According to the hypothesis presented here, the onset of powered-flight in Pterodaustro occurred after attaining 53% of adult size. Here we prefer the hypothesis that bone growth is slowed down by the initiation of a new, and much more energy consuming locomotory activity, namely powered flight.” Not by coincidence, this is the size that Chinsamy et al. (2008) determined that sexual maturity was attained. After observing the morphology of the embryo Pterodaustro, which matches the morphology of the adult, there is no supporting evidence for the Prondvai et al. hypothesis.

Archosaur vs. lepidosaur
Prondvai et al. do not consider the growth strategies and histology of lepidosaurs, only archosaurs. So they are making comparisons to the wrong clade. Pterosaurs nest within the Lepidosauria. Growth patterns in lepidosaurs are distinct and do not follow archosaur growth patterns (Masisano 2002). But this may not be the key factor in observed differences.

Chinsamy and Hurum 2006
looked at the basal lepidosaur, Gephyrosaurus. “The [bone] compacta consists of essentially parallel−fibred bone tissue interrupted by several lines of arrested growth (LAGs). The first LAG visible from the medullary cavity appears to be a hatchling line with its more haphazardly oriented, globular-shaped, osteocyte lacunae.”  This was not a phylogenetically miniaturized taxon even though it was a basal lepidosaur.

More to the point
Chinsamy and Hurum 2006 also looked at the basal and phylogenetically miniaturized mammal, Morganucodon. They report on, “distinct woven bone tissue with large, irregularly oriented osteocyte lacunae and several primary osteons. No secondary osteons were visible, though several enlarged erosion cavities are evident in the compacta. In the same section, it appears that substantial endosteal resorption had occurred, and parallel−fibred bone tissue is evident only in a localized area peripherally. This area includes several rest lines, which indicate pauses in the rate of bone formation, and hence, pauses in growth.” Perhaps these pauses indicate a lifespan of “several” years. Note the “woven bone” texture description.

Figure 2. Several tiny Rhmphorhynchus adult sister taxa, among them is the n7 specimen tested by Prondvai et al. and considered a juvenile by them shown here about 7/10 of in vivo size. As you can see, these pterosaurs do not appear to have any impediments to flapping and flying. However their tiny hatchlings would probably not have flown based on their high surface/volume ratio. The adults had juvenile traits due to phylogenetic miniaturization.

The smallest sampled Rhamph bone microstructure
Prondvai et al. report about the tiny Rhamph, BSPG 1960 I 470a, (n7 in the Wellnhofer 1970 catalog, Fig. 2): “A thin layer of lamellar bone of endosteal origin rims the medullar [central] cavity. There seem to be only a few longitudinally oriented vascular canals, but these have rather large diameter in relation to the overall thickness of the cortex. The bone matrix is typically woven with some poorly defined, immature primary osteons, hence the majority of the cortex does not show the mature fibrolamellar pattern yet. The osteocyte lacunae are large and plump throughout the cortex, and possess an extremely well-developed system of dense, radially oriented canaliculi implying extensive communication and nutrient-exchange between the osteocytes. No LAGs or any other growth marks can be observed.”  Maybe LAGs were never present if this taxon if it lived for just a short time. Remember, we’re talking about phylogenetic miniaturization here.  If the small precocial Rhamphorhynchus specimens were maturing quickly and laying eggs early, they likely followed the life patterns of other tiny tetrapods, like Morganucodon (above) and died early, perhaps living only one or two years, not five or more as in mid-sized pterosaurs.

Note: Like Morganucodon (above) the phylogenetically miniaturized mammal, 
the bone structure in the smallest tested Rhamphorhynchus is described as “woven”.

Age vs size:
Prondvai et al. report, “The ontogenetic validity of the smallest size category of Bennett is clearly supported by the overall microstructure found in the bones of the three small specimens.” Unfortunately, without a phylogenetic analysis, Prondvai et al. did not realize that the smallest specimens were small due to phylogenetic miniaturization. Their ancestors were larger. Thus small Rhamphs retained juvenile and embryonic traits into adulthood, including the typical short rostrum and smaller wings. These traits also included juvenile “woven” bone tissue. Essentially these tiny pterosaurs were precocious sexually active adults in the former juvenile phase of development.

Precocial hatchling?
Prondvai et al. report, “Superprecocial embryos require substantial amount of nutrients stored in their eggs to reach an advanced level of somatic maturity state by the time the embryo hatches. If the egg volume of Darwinopterus was relatively as low as that of squamates, then how could it have contained so much yolk as to cover the energy requirements of an extremely well-developed, volant hatchling?” Prondvai are assuming that pterosaur eggs developed outside the uterus. As lepidosaurs, pterosaur embryos developed inside the uterus and the super thin eggshell was deposited last. Thus they could “cover the energy requirements.”

Apparently Prondvai et al. are not looking
at verified pterosaur hatchlings (in eggs), which are identical in morphology to adults. In some cases large embryos can be larger than small adult sister taxa! The Prondvai team know that the tiny Rhamps don’t have the same morphology as the medium or big rhamphs. Unfortunately, and this is a continuing problem… they don’t realize those changes are phylogenetic, not ontogneric.

With similar proportions of bone and muscle,
but at 1/8 as tall and therefore (8 cube rooted or) 1/512 as massive, juvenile pterosaur bone tissue would have been strong enough for sustained flight in such lightweight specimens. But that overlooks reality, where the specimens Prondvai are looking at are in fact tiny adults with juvenile bone structure, as in Morganucodon. We don’t know where small, medium and large Rhamphorhynchus laid its eggs, which were likely ready to hatch shortly after deposition. We don’t have any hatchling Rhamphorhynchus fossils. Hatchlings of the small and tiny adults would have been in danger of desiccation (high surface area/volume ratio), so we can presume they grew up in moist environs. Unfortunately Prondvai et al. did not test the one verified juvenile among in the Rhamphorhynchus clade, NHMW 1998z0077/0001 (Fig. 3), the Vienna specimen. No one thinks this juvenile could not fly based on its age/relative size.

Figure 3. Two specimens attributed to Rhamphorhynchus longiceps along with a third specimen, NHMW 1998z0077/0001, that nested with the larger of the two with identical scores, thus identifying it as a juvenile R. longiceps. No one thinks this Rhamph could not fly, despite its young age.

To their credit, Pronvai et al. suggest (following a hypothesis first presented here): “Alternatively, Rhamphorhynchus hatchlings could have been precocial to the effect that they could have left their nests immediately after hatching, but they must have been exclusively terrestrial or rather arboreal. They could have clambered around quadrupedally on the branches of trees feeding themselves with smaller invertebrates or vertebrates without any parental contribution.”

No universal growth strategy in pterosaurs
Prondvai et al. report, “In the light of the histological results it becomes evident that there is no universal pattern in the growth strategy of pterosaurs.” I am concerned that this conclusion was made without the the benefit of a phylogenetic analysis and without knowledge of phylogenetic miniaturization in the clade.

To their credit
Prondvai et al. report, “In contrast to Bennett’s  suggestion, the second size category of Rhamphorhynchus does not only include subadult but also adult specimens, hence it cannot be used as an indicator of real ontogenetic stage.”

References
Chinsamy A, Codorniu ́ L, Chiappe L 2008. Developmental growth patterns of the filter-feeder pterosaur, Pterodaustro guinazui. Biol Lett 4: 282–285.
Chinsamy A and Hurum JH 2006. Bone microstructure and growth patterns of early mammals. Acta Palaeontologica Polonica 51 (2): 325–338.
Maisano JA 2002. Terminal fusions of skeletal elements as indicators of maturity in squamates. Journal of Vertebrae Paleontology 22: 268–275.
Prondvai E, Stein K, O0 si A, Sander MP 2012. Life History of Rhamphorhynchus Inferred from Bone Histology and the Diversity of Pterosaurian Growth Strategies. PLoS ONE 7(2): e31392. doi:10.1371/journal.pone.0031392
Sekercioglu C 1999. Megapodes: A fascinating incubation strategy. Online article.