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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
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
"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,
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).