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[dinosaur] Review of Bois & Mullin (2017)

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!

John Bois & Stephen J. Mullin (2017): Dinosaur nest ecology and predation 
during the Late Cretaceous: was there a relationship between upper [sic] 
Cretaceous extinction and nesting behavior? Historical Biology online early: 11 
pp. DOI: 10.1080/08912963.2016.1277423

The paper does not, as I feared, proclaim "mammals ate all their eggs" as the 
only cause of extinction; it offers this as one of several factors that 
happened to coincide in time and therefore caused the mass extinction together. 
It does not, however, try to quantify the contribution of this factor (or that 
of any other factor).

More generally, it hardly tries to quantify anything.

That's quite a pity. A population of tetrapods can sustain its numbers if just 
over two of the eggs a female lies in its lifetime result in hatchlings that 
survive to reproductive age. Table 3 cites a reference saying that 95 % of 
ostriches die in their first year (it isn't mentioned if this is counted from 
hatching or from egg-laying). Given such and similar numbers, it should be 
possible to estimate, with reasonable error margins, how many eggs a 
*Triceratops* female may have had to lay in a lifetime, given the terminal 
Cretaceous array of potential predators on eggs and hatchlings, so that two 
would on average result in reproductive adults. If that number is ridiculously 
high (say, 30,000 eggs in 15 years), well, then we're looking at a likely cause 
of extinction! But such a test, or any hint of one, is absent from the paper.

== The appearance of mammalian nest predators ==

I wondered about the gobiconodontids. John, are you still here? Over the years, 
you've discussed your hypothesis several times, and I remember bringing up the 
gobiconodontids several times; I don't remember getting an explanation for why 
they didn't singlehandedly wipe out most dinosaurs from Laurasia in the Aptian 
or so. The paper doesn't contain one either. It doesn't even try. The following 
paragraph from p. 4:

"There is evidence that non-avian dinosaurs had always experienced egg and 
hatchling predation by mammals (Hu et al. 2005), varanids, and crocodilians, as 
well as other dinosaurs (Ruxton et al. 2014; and references therein). One could 
argue that, because they had survived under that predatory regime, non-avian 
dinosaurs could respond similarly to an increased diversity of birds, mammals, 
and snakes. However, the large body size of non-avian dinosaurs conferred the 
disadvantage of relatively long generation times. Therefore, their ability to 
adapt quickly to sudden changes in their environment was decreased (Hone & 
Benton 2005). We suggest that additional environmental pressure from a growing 
guild of offspring predators would cause unsustainable attrition of offspring."

contains the only mention of gobiconodontids: Hu et al. (2005) is the paper on 
*Psittacosaurus* hatchlings as stomach content of *Repenomamus*. That's it. On 
the other 10 pages there isn't a whiff of a hint of them; they are brought up 
and promptly forgotten.

The argument in that paragraph is that large egg-layers can't adapt to sudden 
increases in the amount of egg/hatchling predators, because they're large and 
therefore have too long generation times. So far, so good! However, the 
application of this argument to the K-Pg mass extinction rests on two unspoken 
assumptions: that the supposed rise of large eutherians, metatherians, 
multituberculates and gondwanatheres in the Maastrichtian was sudden by this 
measure, and that the appearance and diversification of the gobiconodontids in 
the early Aptian was not sudden. Not only aren't these assumptions mentioned, 
they aren't defended either (explicitly or implicitly, let alone with any 

The Berriasian through Barremian terrestrial fossil record isn't terribly good, 
so, while the appearance and diversification of the gobiconodontids looks 
sudden enough to me, I can't say that it actually was. At least some of the 
large mammals of the Maastrichtian, however, have some history behind them. 
Table 1 features *Didelphodon* and cites Wilson et al. (2016) for it; yet, that 
same paper provides a handy overview in its fig. 3 which shows that 
*Didelphodon* and its fellow stagodontid *Eodelphis* go back deep into the 
Campanian. There's nothing sudden about the rise of large stagodontid 
metatherians! We're talking about more than 10 million years before the end of 
the K here. Further, table 1 features *Nanocuris*; that's a deltatheroidan, and 
the large deltatheroidan *Deltatheridium* goes back at least as far.

The same table misspells *Yubaatar*; and the reference for *Altacreodus*, Fox 
(2015), is missing from the references list. It is:
Richard C. Fox (2015): A revision of the Late Cretaceous–Paleocene eutherian 
mammal Cimolestes Marsh, 1889. Canadian Journal of Earth Sciences 52: 
1137–1149. DOI: 10.1139/cjes-2015-0113

At the other end of the Cretaceous, we find *Triconodon mordax*, probably as 
bitey as its name says, which was the size of a cat (lower-jaw length = 8 cm). 
Ground-nesting dinosaurs lived with large carnivorous mammals the whole 
Cretaceous, which lasted longer than the entire time that has passed since its 
end. And yet these same mammals are supposed to have made a noticeable 
contribution to doing them in?

And never mind the Cretaceous. Table 1 gives the masses of *Altacreodus* and 
*Nanocuris* as 565 and 523 g. *Castorocauda* from the Middle Jurassic has been 
estimated to 500–800 g, and *Sinoconodon* from the Early Jurassic to up to 500 

== The appearance of avian nest predators ==

The diversification of "ornithurine" (euornithean) birds in the Late Cretaceous 
is mentioned in a confused three-paragraph section that also mentions the 
extinction of nonavian dinosaurs and the extinction of non-"ornithurine" 
dinosaurs, but not the extinction of non-neornithean euornitheans. No attempt 
is made to show that any Cretaceous euornitheans were potential nest predators, 
or that any enantiornitheans were not potential nest predators; no attempt is 
made to show that any Cretaceous euornitheans nested in trees or that any 
enantiornitheans did not. Nothing is quantified.

== The appearance of ophidian nest predators ==

There's *Sanajeh* in sauropod nests at the very top of the Cretaceous. The 
authors point out the presence of other madtsoiids in "Madagascar, Patagonia, 
Spain and France" before acknowledging that the Romanian *Nidophis insularis* 
was probably a bit to small to do any damage to the hadrosaur nests it was 
found in. Well. The fossil record of madtsoiids is not good enough that we 
could tell when and where madtsoiids started preying on sauropod nests, or how 
quickly they spread. (An SVP presentation last year associated Madtsoiidae and 
*Dinilysia*...) What we can say for sure is that many dinosaur eggs were too 
small for *Sanajeh* and that whole continents (North America in particular) 
appear to have remained madtsoiid-free.

== Large ground-nesting birds in the Cenozoic ==

According to the paper's main hypothesis, there shouldn't be any large 
ground-nesting birds in the presence of Cenozoic levels of nest predation. 
Therefore the paper hypothesizes that all large Cenozoic ground-nesting birds 
have lived in environments that provided protection against nest predation – 
although no attempt is made to quantify how much protection that is.

Ostriches, emus and phorusrhacids are explained away as being tied to 
grasslands. Fair enough, if we grant that eggs are exceptionally hard to find 
in grasslands (see below). Rheas and dromornithids are also explained away as 
being tied to grasslands. Problem is, the Paleocene rhea *Diogenornis* lived at 
a time when grasslands simply didn't exist yet, and the same holds in Australia 
for all Eocene and Oligocene dromornithids. Brontornithids are not mentioned.

The existence of cassowaries, moas and kiwis is interestingly blamed on 
supposed lack of predation on the adults, not on the eggs and hatchlings. The 
aepyornithids are mentioned in the same paragraph, while a later one blames 
their existence on wetlands. Wetlands are also made responsible for the 
Paleocene/Eocene wide distribution and subsequent extinction of the 
gastornithids, because wetlands hinder "access by mammalian predators" (with 
references that all seem to be about small birds; "waterfowl" and "the purple 
swamphen" are mentioned in 2 of the 4 titles). I do have to wonder: you can't 
just lay an elephant-bird egg into a swamp...? And what kind of "wetland" is it 
that is too muddy to allow herpestids or oxyaenids to simply walk into it, but 
not muddy enough that a quarter-ton bird would get stuck? Mordor is supposed to 
be rather dry...? I'm aware that at least one species of aepyornithid was 
apparently called vorompatra, meaning "swamp bird" (vorona + patra), but that 
doesn't mean it was able to nest like a duck or a sedge warbler. Further, 
gastornithids are known from all three northern continents; were there really 
enough "wetlands" for them to nest in and nonetheless spread around the Earth?

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*.

Finally, from the "Wetlands" section on p. 8, let me quote this gem: 
"_*Aepyornis*_. The elephant bird (~500 kg) likely owed its success to the 
existence of wetland habitat for nesting; wetland contraction is implicated in 
the extinction of *Aepyornis* (Heuvelmans 2014)." That's the whole paragraph. 
Yes, you may trust your eyes: the only cited source is a posthumous reprint 
(not marked as such in the references list!) of the famous cryptozoological 
work from 1955 (English translation 1958). (Heuvelmans died in 2001.) 
Catastrophic wetland contraction throughout this huge island within the last 
thousand years, right at the same time when humans settled the place? Some of 
the paleontology in Heuvelman's book was probably already outdated in 1955, and 
yet it's uncritically cited in Historical Biology in 2017. (Note also that 
*Mullerornis* is not even implicitly mentioned; not all Holocene aepyornithids 
are *Aepyornis*.)

Back to grasslands. P. 7: "Ratites might be analogous to non-avian dinosaurs in 
that, unlike their adult forms, their eggs and juveniles are susceptible to 
predation by a wide range of species and size classes (Tables 2 and 3). Magige 
et al. (2009) found that all observed nests failed in the Serengeti ecosystem. 
Predation accounted for 80% of these failures. Studying ostrich reproductive 
success in Nairobi National Park, Davies (2002) found a 73% failure rate of 
nests (mainly attributable to predation) and of those chicks that hatched, 88% 
were taken by predators. Without the concealment property of grasses, this rate 
might be higher. Indeed, the chicks of both rhea and emu are known to utilize 
grasses for concealment when danger threatens (Bruning 1974; Davies 2002). This 
factor is particularly relevant for large oviparous species because the 
disparity of adult versus hatchling size necessitates that small oviparous 
offspring spend a proportionally greater period of their early life-history at 
risk of predation."

Again: "Without the concealment property of grasses, this rate might be 
higher." Indeed it might. By how much? Would it ever reach 100 %, or 95, or 
even just 90? No attempt is made to answer this question at all.

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?

== 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 

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 ==


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 

* 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).