Today a guest post by Edina Prondvai. Edina and her work group have a new paper out looking at the growth rates of specimens of the ubiquitous Solnhofen pterosaur Rhamphorhynchus which has important implications for the ecology of young animals. Here she takes us through the work (which is in PloS ONE and so available to all right here):
Since its first appearance, the idea about superprecocial, slowly growing Rhamphorhynchus babies that were capable of powered flight immediately after hatching has gained wide acceptance among pterosaurologists as well as paleontologists working on other vertebrate groups. This conception was merely based on the frequent occurrence of very young individuals in the Solnhofen limestones with wing bones exhibiting similar morphometric ratios to those found in the adults. Paleohistology, on the other hand, implied relatively fast growth for pterosaur hatchlings in general, and on the basis of a single study, for Rhamphorhynchus too. The contradiction of these inferences of morphological vs. bone histological studies have largely been ignored and thus remained unresolved so far. Did Rhamphorhynchus hatchlings grow fast but were altricial, defenseless babies being in the need of constant parental care? Or were they real superprecocial, independent flaplings which flew off shortly after getting rid of the last bits of the eggshell but paid a high price for this “superdeveloped” state, namely the abdication of fast growth? For reasons based on the simple trade-off in energy allocation of biological systems, fast growth and sustained powered flight cannot occur simultaneously: either you allocate a lot of your energy supply to grow fast or you invest more to move fast.
Various sizes of Rhamphorhynchus specimens sampled. From Prondvai et al., 2012.
So which strategy did Rhamphorhynchus babies use?
A new study of an ontogenetic series of Rhamphorhynchus has deciphered a significant part of this issue showing that neither and both of the previous notions were true. Based on the bone histological features of five Rhamphorhynchus specimens ranging from 30 cm up to 1.5 m in wingspan, it has been demonstrated that their ontogeny can be characterized by an initial short growth burst that was followed by a prolonged slow-growth phase. Namely, babies grew fast only up to the attainment of 30-50% of adult wingspan and 7-20% of adult body mass, whereupon growth rate decreased significantly in late juveniles but continued for a long period. Interestingly enough, of the seven, histologically considered specimens none exhibited evidence of complete cessation of growth in its bone microstructure. This probably indicates that the animals would have been capable of further growth at the time of their death, which also means that even the largest specimen with 1.5 m wingspan was not fully grown when it died. On the other hand, the latter as well as another specimen with approximately 90 cm wingspan are skeletally as well as histologically mature, which refers to the occurrence of considerable size differences among adult individuals.
Histological sample of a small Rhamphorhynchus (wingspan under 35 cm). From Prondvai et al., 2012.
Fast growing babies and slowly growing juveniles? What could have induced this baffling growth strategy? Similar kind of alteration in growth rate has also been detected in the bones of the Early Cretaceous filter feeder pterodactyloid Pterodaustro at 56% of adult body size, and was interpreted as the sign of sexual maturation which reallocated energy from growth to reproduction. In Rhamphorhynchus however, this change in the overall pattern of bone histology happens much earlier during ontogeny, which makes reproduction as cause of this transition very unlikely. The onset of powered flight, which is the major type of locomotion in most pterosaurs, on the other hand is an adequate explanation for this histological alteration. In fact, the initiation of the energy consuming flight must have left its signature in the bone tissue of Pterodaustro too. Thus, it is more probable that powered flight and not reproduction accounts for this consistent histological transition in both, distantly related pterosaur groups. This notion is further supported by the fact that there is no extant volant vertebrate known in which the onset of reproduction precedes the onset of powered flight.
Histological sample of a large Rhamphorhynchus (wingspan just under 150 cm). From Prondvai et al., 2012.
Going back to the starting-point:
Q1: Were Rhamphorhynchus hatchlings superprecocial flaplings?
A1: Definitely not. Both smallest investigated specimens, which were certainly non-embryonic, showed evidence of fast growth in their bone tissue which precludes powered flight as the major mode of locomotion.
Q2: Were Rhamphorhynchus hatchlings altricial, defenseless babies?
A2: This is quite unlikely, too. Both of the smallest individuals exhibited well developed morphology, which implies a precocial but nonetheless non-volant nature of the early juveniles. But what does this mean in terms of lifestyle? Hard to say for sure, but the most probable sequence is that hatchlings left their nest as soon as they got dry, but not on wings; they must have climbed up on a tree trunk, clambering among the branches hunting for arthropods by themselves. They might even have been able to glide from tree to tree to invade new hunting areas, but sustained flapping flight could not have been performed.
Q3: Was Rhamphorhynchus an early flier?
A3: Compared to most of the extant volant vertebrates, they certainly were. With only 30-50% of adult wingspan and 7-20% of adult body mass they started flying, while the majority of birds and all bats begin to fly after reaching full adult size. There is only one extant bird family, Megapodiidae in which some species are capable of doing so; however, they are even more extreme in that. Their hatchlings are the real superprecocial flaplings, flying off for the bushes immediately after hatching. However, those are highly terrestrial birds using short burst flight mostly to escape dangerous situations; a lifestyle that is not comparable to that of Rhamphorhynchus. Based on histological investigations of early birds such as enantiornithines, it has been hypothesized that this strategy is in fact the plesiomorphic one for birds. Not so for pterosaurs, in which the earliest forms have shown fast growth throughout their development until reaching adult body size, which implies a late onset of flight during ontogeny. In this sense, the developmental strategy of Rhamphorhynchus can be considered as an innovation, which has been evolved probably independently in Pterodaustro, too. The multiple independent appearance of this strategy speaks for some sort of adaptive advantage in the environments concerned.
The diversity and convergences of different growth strategies in phylogenetically as distant groups as pterosaurs, birds and bats have shown how much influence the timing of the onset of flight has on the life history of all volant vertebrates.
Dave Hone's Archosaur Musings 
“it has been hypothesized that this strategy is in fact the plesiomorphic one for birds” – It’s not entirely clear from the text what “this strategy” refers to. Being “highly terrestrial” is mentioned in the sentence before, but I take it it refers to being “superprecocial” instead?
Is there a specific study you are thinking of when you said that this may be the plesiomorphic life-history strategy for birds? I would like to chase this down, if possible.
“Is there a specific study you are thinking of when you said that this may be the plesiomorphic life-history strategy for birds?”
Probably Elzanowski 1981. However, based on what I’ve read (E.g. See the Norell et al. quote), there isn’t any evidence for said hypothesis.
Quoting Norell et al. ( http://www.gwu.edu/~clade/faculty/clark/embryo.pdf ): “Several authors (Elzanowski, 1981; Geist and Jones, 1996) have attempted to correlate the degree of ossification or the histology of dinosaur fossil embryos with specific developmental postnatal strategies of extant Aves. Elzanowski (1981), for exam- ple, regarded the high degree of ossification of certain Late Cretaceous embryos, usually attributed to the enantiornithine Gobipteryx minuta, as indicative of superprecociality, and proposed that this was the ancestral de- velopmental mode of Aves.
In a histological study of extant Aves and nonavialan dinosaurs, Geist and Jones (1996) argued that nonavialan dinosaurs were pre- cocial rather than altricial. Embryogenetic studies of Aves, however, have shown that the relative degree of ossification is a weak indicator of developmental modes (Starck, 1993; Starck and Ricklefs, 1998), thereby raising objections to these specific correla- tions. Although the degree of ossification of precocial hatchlings is significantly greater than that of altricial hatchlings, the degree of ossification of superprecocial, precocial, and semiprecocial hatchlings differs little (Starck, 1993). Furthermore, the degree of ossifica- tion of altricial embryos is comparable to that of other embryos for the first three-quar- ters of their embryogenesis (Starck, 1993), and the specific developmental stages of fos- sil embryos are hard to evaluate.”
“There is only one extant bird family, Megapodiidae in which some species are capable of doing so; however, they are even more extreme in that. Their hatchlings are the real superprecocial flaplings, flying off for the bushes immediately after hatching.”
Also at least one species of Odontophoridae is capable of short flight hops after hatching out.
Great article!
A cool study and nice article. Thanks!
“…the most probable sequence is that hatchlings left their nest as soon as they got dry, but not on wings; they must have climbed up on a tree trunk, clambering among the branches hunting for arthropods by themselves.”
I find it somewhat unlikely that pterosaur hatchlings would have had a completely different ecology and diet for a very short time before onset of powered flight, without any obvious morphological adaptations for such mode of life, while *still* getting enough energy to grow faster than when flying. I mean, if non-flying arthropod-hunting baby pterosaurs were energetically that much more efficient, why fly at all?
Of course, the mortality caused by predators might have been the selective pressure to prevent the evolution of flightless neotenic pterosaurs. But I’d suspect that baby pterosaurs were not that good at getting food for theirselves, instead being fed by their parents until they could fly, which would explain the fast growth rates. They fit nicely into a phylogenetic bracket of animals with parental care, after all.
Of course, I’m no professional. It was just an idea. What do you think?