Re: [dinosaur] Review of Bois & Mullin (2017)

[Tim Williams <tijawi@gmail.com>]

David Marjanovic <david.marjanovic@gmx.at> wrote:

> Having finished 2 of the 3 peer reviews I've been asked to write lately, I 
> figured I might as well do some post-publication review.
> Discussion is welcome!

First of all, I'd like to add my thanks to you taking the time to
review this paper.

Secondly...

> The Paleogene European "ratites" (*Palaeotis*, *Remiornis*, *Eleutherornis*) 
> are not mentioned, and neither is *Eremopezus*
> from Fayûm. Messel was full of mammals and crocodiles (in fact, I have no 
> idea how the adults of the _small_ flightless bird
> *Messelornis* managed to survive), and Fayûm was a scary environment with 
> potential nest predators up to and including
> *Gigantophis*.
[snip]
> The "concealment property of grasses" is supported only by two anecdotes, by 
> the way. I quote the preceding paragraph in full:
>  "James and Olson (1983) argued that flightlessness evolved on islands in the 
> absence of predation. We suggest that grasslands,
> especially in their more arid ranges, are ‘islands’ of low predator density 
> where large oviparous species can effectively conceal
> their nests. Bertram (1992) noted that he could not detect an ostrich nest to 
> within 10 m, but that it is sited within a territory of >2
> km². Rheas of South America, also nest in grassy open habitat (Bruning 1974) 
> and are similarly inconspicuous (Darwin 1839)."
> Comparisons to other vegetated landscapes, quantified or anecdotal, are not 
> provided. How easy is it to find a cassowary nest?
> We aren't told. And, again, why is it that rheas, emus, dromornithids, 
> apparently ostriches (assuming they're related to some or
> all of the Paleogene European "ratites") and possibly phorusrhacids were 
> already flightless and pretty large before the forests
> they lived in turned into grasslands?


I entirely agree with your reservations.  Further, I'm not certain
that flightlessness in birds is always a consequence of a
(terrestrial) predator-free environment.  This tends to imply that
birds are so feeble that it's only by virtue of the absence of
predators that they have the luxury of losing the power of flight.  I
have no doubt that island-dwelling birds are more likely to become
flightless (because of reduced predation pressure); that's beyond
dispute.  But I'm not convinced that all flightless birds evolved on
islands and/or in the "absence of predation".

The hypothesis that Cretaceous terrestrial birds were flightless
because of a predator-free environment is not supported by the few
known examples. _Gargantuavis_ shared its insular habitat with
dromaeosaurids and abelisaurids.  The much smaller _Patagopteryx_, a
continental bird that was not just flightless but also rather slow
(based on its hindlimb proportions), lived alongside snakes,
crocodyliforms (including notosuchians), and _Velocisaurus_ (regarded
by Bonaparte [1991] as an extremely cursorial theropod, though
possibly not a predator, but maybe omnivorous).

For Cenozoic flightless birds, there are quite a number of lineages
that produced flightless representatives in continental ecosystems.
There seems to have been a propensity of large and flightless
terrestrial birds at or near the base of the Neornithes, including
various palaeognath lineages and basal neognaths like dromornithids,
gastornithids, and brontornithids. Within Neoaves there's
phorusrhacids, bathornithids, idiornithids, eogruids,
ameghinornithids, and so on.

Mayr (2016) notes that the Messel ecosystem (Eocene) is remarkable for
the large and diverse number of flightless birds (_Palaeotis_,
_Gastornis_, _Strigogyps_, _Dynamopterus_).  He attributes this to the
absence of  large mammalian carnivores - not to the absence of
predators per se.  There were small mammalian carnivores at Messel,
including the miacids _Paroodectes_ and _Messelogale_, and the
hyaenodontid _Lesmesodon_. These placental predators might not have
been able to tackle adults of these flightless birds, but the eggs and
chicks would have been targets.  Yet, these birds survived.  The
extinction of the flightless Messel bird lineages has been tied to the
appearance of larger and more derived placental predators.  But there
is also the possibility that competition with new large mammalian
herbivores (conspicuously absent from Messel) also played a part.
Also, many lineages of volant Messel lineages (especially arboreal
ones) also went extinct.  So the reason(s) for the demise of
flightless terrestrial birds in Messel and other ecosystems might be
quite complex.

I don't think the ability of flightless birds to co-exist with
terrestrial predators is always a consequence of the environment.
(Island-dwelling birds are different - if they lose flight in response
to low predation pressure, as tends to happen on islands.)  Maybe
large birds are actually quite adept at defending themselves (and
their progeny) from terrestrial predators.  Under this hypothesis,
terrestrial birds in continental ecosystems evolved ways to become
better able to evade or fend off terrestrial predators - and over time
spent more time on the ground, and eventually lost the ability to fly.
Flight is a highly energetically expensive process.  So a terrestrial
bird that didn't need to fly would abandon this ability - particularly
if the bird was a herbivore, since being flightless releases the
constraint on size, allowing a herbivorous bird to feed on larger
quantities of nutrient-poor plant material.










>
> == You can't run, you can't hide, you can't fight and you can't swamp? ==
>
> Many terrestrial egg-layers today take various measures to reduce predation 
> on their nests: they run, hide, fight, and/or swamp the predators. For 
> dinosaurs above a certain unspecified size, hiding the nest is argued to be 
> impossible because the eggs are just too big and/or the brooding adults (if 
> any) are detectable from afar. (No quantification of course.) "Running" off 
> to an inaccessible location, like a treetop, a cliff or a remote island, 
> requires the ability to fly or at least climb and is thus out of the question 
> for most if not all nonavian dinosaurs. Swamping is apparently considered 
> impossible, because (p. 5):
>
> "Perhaps intrinsic to the idea of multiple unattended clutches, is the idea 
> of predator swamping. We contend that it is unlikely that a colony of 
> dinosaurs could abandon their nests and survive excessive offspring predation 
> by overwhelming or satiating predators. For this strategy to be effective, 
> non-avian dinosaurs would have to limit the intensity of destruction of their 
> offspring by avoiding predation and/or limiting temporal access to their eggs 
> and hatchlings. Reproductive effort by many turtle species benefits from both 
> of these factors and provides a relevant contrast to nonavian dinosaur 
> nesting ecology because, even when discovered, the contents of turtle nests 
> swamp predators (Santos et al. 2016)."
>
> As far as I can tell, "we contend that it is unlikely" is the entirety of the 
> argument. The concept of predator swamping is mentioned nowhere else in the 
> paper.
>
> On remote nesting I have to say that there are degrees of remoteness. Surely 
> such islands as Egg Mountain and Egg Island afforded _some_ protection? 
> *Maiasaura* did survive the presence of *Gobiconodon* after all.
>
> If we accept that no attainable degree of remoteness is enough and that even 
> a titanosaur nesting colony couldn't swamp nest predators, that leaves nest 
> defense. The authors correctly point out that nest defense can never be 
> perfect (p. 6):
>
> "If dinosaurs actively defended their nests, we question the effectiveness of 
> this strategy in the face of an emerging guild of small predators for at 
> least two reasons: (i) dinosaurs needed to maintain structural integrity of 
> their nests and lacked the capacity to defend them against burrowing animals. 
> As a modern analogy, the hairy armadillo (*Chaetophractus* sp.) burrows 
> beneath the nest of the much larger rhea (*Rhea americana*) parent (Fernandez 
> & Reboreda 1998). While this source of predation causes many nests to fail, 
> rheas have no defensive response to it."
>
> And yet, they still haven't died out. How can that be? It can't be the fact 
> that they nest in grassland – if anything, grassland soil should be easier to 
> dig through than the sand under a rainforest with all those roots in it. I 
> guess that counts as swamping.
>
> "(ii) small [sic] nocturnal predators have an advantage over large diurnal 
> oviparous species. Ostriches that effectively defend the nest from 
> black-backed jackals (*Canis mesomelas*) in the daylight, apparently abandon 
> the nest under similar attack at night (Bertram 1992). Some non-avian 
> dinosaurs might have been nocturnally active (Schmitz & Motani 2011); 
> however, this interpretation has not been widely accepted (e.g. Hall et al. 
> 2011)."
>
> This is followed by evidence for a nocturnal/fossorial origin of mammals and 
> snakes (all with the implication that Mesozoic dinosaurs were nightblind like 
> ostriches). And yet, ostriches aren't extinct either. Is it the grassland 
> this time? But if so, what happens when a fox or dingo or singing-dog or 
> historically a "Tasmanian" "tiger" attacks a cassowary nest at night?
>
> Crocodiles can't really hide their nests or nest in remote places either, so 
> they defend them. This is implied to be insufficient on its own in the 
> following paragraph from p. 7:
>
> "Nest defense is practiced by most species of crocodilians (Somaweera et al. 
> 2013). This represents an exception to our claim that dependence on nest 
> defense cannot be a viable strategy amid extant predators. We argue that 
> crocodilians have experienced a relatively reduced frequency of offspring 
> predation because their hatchlings find refuge in water. Factors such as 
> turbidity and submerged aquatic vegetation probably enhance crocodilian 
> reproductive success in wetlands (Somaweera et al. 2013); and the 
> semi-aquatic habitat is a particularly effective refuge from mammalian 
> predation (Pasitschniak-Arts & Messier 1995)."
>
> Crocodylian hatchlings are, of course, eaten by all sorts of large 
> actinopterygians, large frogs, birds, varanids (often good swimmers) and 
> adult crocodylians. Unsurprisingly, parents guard and defend their hatchlings 
> in the water well after hatching, too. I conclude that hiding is insufficient 
> on its own in this very case and needs to be supplemented by defense. Whether 
> defense would be sufficient on its own isn't testable, because hiding is 
> cheaper.
>
> == What about those that could in fact hide? ==
>
> P. 6: "In comparison to almost all extant terrestrial oviparous vertebrates 
> of <30 kg in body mass, the large size of non-avian dinosaurs precluded 
> stealth when laying and incubating their eggs. We recognize that several 
> small carnivorous non-avian dinosaurs remained into the latest Cretaceous 
> (Turner et al. 2007; Benson et al. 2014; Larson et al. 2016), and that 
> concealment was a likely strategy for them. However, we argue that no single 
> extinction hypothesis can consider every extinct species. Indeed, other 
> scenarios invoke the extinction of carnivorous species following the 
> disappearance of their herbivorous prey (e.g. Alvarez et al. 1980), and we 
> predict a similar fate for the smaller members of the clade Deinonychosauria."
>
> Come on, authors. Don't you agree that the small deinonychosaurs (< 30 kg) 
> were ideally suited to eat the diversifying mammals? Would they really care 
> if the hadrosaurs died out?
>
> I argue that a single hypothesis for the cause of a _mass extinction event_ 
> should – parsimony! –, and indeed can, consider every species that took part 
> in that event. As far as I can tell, the Chicxulub impact has little trouble 
> explaining the extinction of all deinonychosaurs and a whole lot of mammals 
> at the same time as loads and loads of haptophytes and planktonic 
> foraminifera. But I digress.
>
> == Conclusion ==
>
> Fail.
>
> No, not "epic fail". WAIR was a case of epic fail: a coherent hypothesis that 
> has ended up teaching us a lot about extant and extinct animals with 
> borderline flight capabilities and was slain by one ugly fact, the fact that 
> it requires the ability to lift the wings far dorsal of the shoulder joints. 
> It was a research program; it was useful. Probably we'd already be singing 
> songs about it if that were our culture.*
>
> I was surprised to find that the paper had four reviewers. All of them are 
> anonymous, and any responsible editor is not mentioned (some journals do 
> this, some don't).
>
> BTW, the authors and the reviewers seem to have expected that the manuscript 
> would be copyedited. Of course it wasn't; very few journals do that anymore. 
> Various typos abound, and (as mentioned above) there's at least one missing 
> reference.
>
> * I've long thought that we scientists have become our own tribe with our own 
> culture. Other people have long begun to notice; to avoid a long digression, 
> I'll just mention the secret language called Damin or Demiin – check out the 
> story of why there's any research on it!
>
> == So, why aren't there more large flightless birds in the Cenozoic? ==
>
> Why weren't there more large flightless birds in the Mesozoic, seeing as 
> *Gargantuavis* proves the concept? I suspect the reason is the same: the 
> ecological niches in question were already occupied. In the Cenozoic, mammals 
> mostly happened to get there first; "everything is the way it is because it 
> got that way" (D'A. W. Thompson, 1917: On Growth and Form).