Unidirectional airflow in the lungs of birds, crocs…and now monitor lizards!?

December 11, 2013

1_MonitorLizard_AnatomyFlow

Image courtesy of Emma Schachner.

Gotta say, I did not see that coming.

Today sees the publication of a new paper by Emma Schachner and colleagues in Nature, documenting for the first time that unidirectional, flow-through breathing–previously only known in birds and crocodilians–happens in freakin’ monitor lizards. The image above, which is most of Figure 1, pretty much tells the tale.

Some quick background: until the early 1970s, no-one was quite sure how birds breathed. Everyone knew that birds breathe, and that the air sacs had something to do with it, and that the bird lungs are set up as a series of tubes instead of a big array of little sacs, like ours, but the airflow patterns had not been worked out. Then in a series of nifty experiments, Knut Schmidt-Nielsen and his students and colleagues showed that birds have unidirectional airflow through their lungs on both inspiration and expiration. Amazingly, there are no anatomical valves in the lungs or air sacs, and the complex flow patterns are all generated by aerodynamic valving. For loads more information on this, including some cool animations, please see this page (the diagram below is modified from versions on that page). For a short, eminently readable summary of how undirectional airflow in birds was first discovered (among many other fascinating things), I recommend Schmidt-Nielsen’s wonderful little book, How Animals Work.

Avian breathing

After 1972, biologists had almost four decades to get used to the idea that birds had this amazing miraculous lung thingy that was unique in the animal kingdom. Then in 2010, Colleen Farmer and Kent Sanders of the University of Utah blew our collective minds by demonstrating that alligators have unidirectional flow-through lungs, too. That means that far from being a birds-only thing, unidirectional flow-through lung ventilation was probably primitive for Archosauria, and was therefore the default state for non-avian dinosaurs, pterosaurs, the other ornithodirans and the hordes of croc-line archosaurs.

Crocodilian breathing - Schachner et al 2013a fig 10

Diagrammatic and highly simplified representation of airflow through the dorsobronchi and ventrobronchi during inspiration (A) and expiration (B) in the crocodilian lung, and inspiration (A) and expiration (D) in the avian lung. The avian model is a modification of the Hazelhoff loop (Hazelhoff, 1951). Arrows denote direction of airflow, white arrows show air flowing through the parabronchi, blue arrows show air entering the trachea, the red circled “X” demonstrates the location of the aerodynamic inspiratory valve (i.e., air does not flow through this location during inspiration). Colors represent hypothesized homologous regions of the lung in both groups. Abbreviations: d, dorsobronchi; P, parabronchi; Pb, primary bronchus; v, ventrobronchi. [Figure 10 and caption from Schachner et al. 2013a.]

The birdy-ness of crocodilian lungs was further cemented earlier this year when Schachner et al. described the lung morphology and airflow patterns in Nile crocs, which have lungs that are if anything even more birdlike than those of gators. I got to review that paper and blogged about it here.

Now…well, you read the headline. Monitor lizards have unidirectional airflow through their lungs, too. This falls at about the halfway point between “whatisthisIdonteven”–I mean, dude, unidirectional airflow in friggin’ lizards!–and “yeah, that makes a weird sort of sense”. Because to sum up a lot of science unscientifically, monitors just kick a little more ass than other squamates. They have crazy high aerobic capacities for animals that aren’t birds or mammals, they’re ecologically versatile and geographically widespread, they get waaay bigger than any other extant lizards (Komodo dragons) and until recently got even bigger than that (Megalania). Is it going too far to link the success of varanids with their totally pimpin’ flow-through lungs? Maybe, maybe not. But it seems like fertile ground for further study.

Schachner_fig3_labels

Phylogeny for Diapsida showing lungs of representative taxa.
Greyscale images are modified from Milani and transected. The coloured
three-dimensional images are the bronchial tree (right lateral view). Images are
not to scale. a, Diapsida. b, Sphenodon punctatus. c, Crocodile sp. (left) and
Alligator mississippiensis (right). d, Squamata. e, Iguana iguana (left) and
Polychrus marmoratus (right). f, Gekko gecko. g, Lacerta viridis. h, Python sp.
in dorsal view . i, Varanus bengalensis (left) and V. exanthematicus (right).
The blue regions of the phylogeny reflect the hypothesis that unidirectional
airflow evolved convergently; the green arrow shows the alternative hypothesis
of an ancestral origin. [Figure 3 and caption from Schachner et al. (2013b).]

Now, obviously the gigantic question looming over all of amniote biology like one of those monoliths from 2001 is: does this mean that unidirectional flow-through lung ventilation is primitive for all diapsids? That is a super-interesting possibility, and in the new paper Schachner et al. advance some evidence both for and against. On the “for” side, well, hey, there’s uniflow in monitors, crocs, and birds, and in all three cases, air flows down the primary bronchus into a sac at the caudal end, and then back cranially through series of interconnected sacs or tubes. On the “against” side, the patterns of airflow in varanids are similar to those in archosaurs but not identical: in archosaurs, the caudal-to-cranial flow goes through dorsal, tube-shaped secondary bronchi, whereas in varanids it goes through ventrolateral, sac-like bronchi. Also, varanids and archosaurs are phylogenetically distant, so if uniflow was primitive for diapsids, it would seem to have been lost in a lot of other lineages–potentially, all the non-varanid lepidosauromorphs.

On the gripping hand, uniflow would seem to have been lost in all those other lepidosauromorphs, but maybe it wasn’t. Maybe some of them are in the same state varanids were in until this year: they’ve had uniflow lungs forever and we don’t know because no-one has looked yet. And this is one of the concluding points in the new paper: we need to go look more at how living animals actually work.

A small sample of monitor lung diversity, from Becker et al. (1989).

A small sample of monitor lung diversity, from Becker et al. (1989).

In fact, we don’t just need to look at more critters in general, we specifically need to look at more monitors. I have been casually throwing around the terms “monitors” and “varanids” as if the findings of Schachner et al. (2013b) apply to all of them. They may not–the new paper is only about airflow in the savannah monitor, Varanus exanthematicus (same species as Mike’s “sauropod” Charlie), and monitor lungs are sufficiently diverse in form to have been used as taxonomic characters (Becker et al. 1989). So monitors may actually provide multiple windows into the evolution of unidirectional, flow-through lung ventilation. This is especially tantalizing because extant monitors cover a much wider range of body sizes and ecologies than extant crocs, so–just maybe–we can find out if and how diversity in lung structure and ventilation is related to body size and mode of life. Somebody get on that, stat.

Hypothetical bird lung intermediates - Perry 1992 fig 6

Figure 6 from Perry (1992).

My favorite part of all this? Something virtually identical to how monitor lungs work was proposed just over two decades ago by Steve Perry, as a hypothetical stage between saccular lungs and bird-like lungs. See the “Euparkerian grade” lung in the above figure, with perforations between adjacent chambers? Compare that to the diagram of the monitor lung in the image at the top of the post–they’re pretty darned similar. Now, two caveats. First, Steve was suggesting this as a plausible ancestral state for archosaurs, not monitors, and as mentioned above, monitors do things a little differently than archosaurs. Second, there are some things in this figure that are now known to be incorrect, primarily the lack of unidirectional airflow in the crocodilian lung. In fact, on the page opposite this figure, Steve explicitly discounted the possibility of unidirectional airflow in croc lungs. Still, he recognized that croc lungs and bird lungs share profound structural similarities, that they are really points on a spectrum of plausible intermediate conditions, and that crocs had the potential to shuttle air around their lungs because of the complex connections between chambers. So if Steve was not completely right, neither was he completely wrong; it might be most accurate to say that he was less wrong than anyone else at the time, and for about 20 more years after. Which is pretty darned good; I’ve had to rebut myself within the space of five years (Wedel 2007: prosauropod pneumaticity is equivocal. Yates et al. 2012: oh no it’s not!).

Here are the thoughts that have been tumbling through my head since I first learned about this. Obviously structures can be simplified or lost through evolution. Birds and turtles lost their teeth, numerous tetrapods have lost one or both pairs of limbs, and, heck, the platypus lost its stomach. But I rarely see hypotheses of derived simplification entertained for organs like hearts and lungs. There seems to be an unstated but widespread assumption that complex = better when it comes to core physiological processes like breathing.

Reptilian lung morphospace - Perry 1992 fig 2

Figure 2 from Perry (1992)

But it ain’t necessarily so. Following Steve Perry’s diapsid-lung-continuum diagrams, I have often wondered if croc lungs are derived from bird lungs instead of the reverse; maybe the ancestral archosaur had a fully bird-like lung/air-sac system and the non-diverticular, not-super-aerobic lungs of crocs represent a simplification of that system to suit their more sedate lifestyle as semiaquatic ambush predators. That’s pretty much what Seymour et al. (2004) suggested for crocodilian hearts, and it seems plausible given that so many early crocodylomorphs were long-legged, terrestrial, and possibly cursorial (e.g., sphenosuchians). In other words, maybe extant crocs are secondarily ectothermic, with secondarily and possibly paedomorphically reduced air sac systems.

Heck, maybe even bird lungs are simplified compared to their ancestral condition. Most birds have nine air sacs: paired cervical, anterior thoracic, posterior thoracic, and abdominal sacs, and an unpaired clavicular air sac. Some have reduced the number further through loss or fusion of adjacent air sacs. But they all start out with 12 embryonic air sacs (the extras fuse together, IIRC almost all of them becoming part of the clavicular sac), which suggests that the ancestors of birds might have had more than the standard nine.

If we assume that there was some diversity in respiratory anatomy in Mesozoic dinosaurs–which is not much of a stretch, given the diversity we see within (let alone among) monitors, crocs, and birds–it would be an awfully big coincidence if the only dinosaur clade to survive the end Cretaceous extinction just happened to have the fanciest lungs. As far as I know, no-one has proposed that birds survived because they out-breathed everyone else. If anything, the decent-to-high survival rates of mammals, crocs, and turtles across the K-Pg boundary, and the complete extinction of air-sac-equipped pterosaurs and non-avian saurischians, suggests that lung ventilation had nothing to do with survivorship. So what are the chances that crown birds have the most complex lungs among ornithodirans? (Don’t say “flight” because enantiornithines and pterosaurs had air sacs and died out, and bats don’t have air sacs and fly just fine.)

I’m not saying these “awesomeness came first” hypotheses are currently more parsimonious than the standard view. But they’re plausible, and at least potentially testable, and if nothing else an antidote to the idea that birds sit at the top of some physiological Great Chain of Being.

Back to the homology-vs-convergence question. If flow-through lungs are primitive for diapsids, maybe they’ll turn up in a few more critters. But maybe evolving undirectional airflow just isn’t that hard, and only requires poking some holes through the walls of adjacent lung chambers–as stated above, we need to go check more critters. But either way, the form and function of the lungs in V. exanthematicus are not only fascinating in their own right, they give us a window into what the early evolution of archosaurian–and maybe even early diapsid!–breathing might have been like. And that’s phenomenal.

I have some more thoughts on this, particularly the implications for sauropods and other dinosaurs, but those will have to wait for another post.

Images and figures from Schachner et al. (2013b) appear here courtesy of Emma Schachner (website), who kindly offered to let me look under the hood before the paper came out. She also created a cool video showing the 3D lung anatomy of V. exanthematicus. Thanks, Emma, and congratulations!

References

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30 Responses to “Unidirectional airflow in the lungs of birds, crocs…and now monitor lizards!?”

  1. Nick Says:

    I’m excited to know what will come next, especially being aware (but not having seen) that something is forthcoming on turtles and I look forward to seeing what happens as other lepidos are investigated.

  2. Duane Nash Says:

    I wonder if anyone has started to look for skeletal evidence of air sacs in mosasaurs? They were related, diverse, and probably very aerobically active.


  3. Saurischian respiration HAS been tied into survival through extinctions before, but in terms of the Triassic/Jurassic one (by Peter Ward), not the K/Pg.

    And yes: this came out of nowhere. Totally did not expect this!


  4. Nick, what do you know about that is going to be published on turtles?

  5. Anonymous Says:

    Pfft. Of course birds don’t sit atop the great chain of being. Sauropods do!

    On a more serious note, I’ve heard it suggested that the reason monitors are so weird compared to other lizards is because their method of gular pumping allows them to get around most of the issues of being an active animal and a sprawler. I’ve also seen mention of some monitor species being able to move using a semi-erect “high walk”. Any truth to this?

  6. Matt Wedel Says:

    Good point about saurischian respiration and the Tr/J extinction, Tom. You know I’m contractually obligated to ask how that paper is coming along! :-)

    Anon, I’ve heard the “gular pumping + costal ventilation = awesome” hypothesis too, and always thought it made sense. Now it turns out to actually be “gular pumping + costal ventilation + unidirectional airflow = even more awesome”. As for the high walk, I’ve seen monitors do something like that, but I’m not a locomotion guy so can’t comment usefully on the sprawling-to-upright continuum.


  7. […] Unidirectional airflow in the lungs of birds, crocs…and now monitor lizards!? (svpow.com) […]

  8. Jura Says:

    In regards to the posting from Anonymous, gular pumping has been shown to aid in lung filling during locomotion in Varanus, Uromastyx, Eublepharis, Tupinambis and Heloderma (Owerkowicz et al. 1999). This has been interpreted as a means of getting around a physical problem known as Carrier’s constraint (Carrier 1987). Though Carrier mentioned that sprawling may have an effect on breathing (through the use of respiratory muscles to help stiffen the thorax) the main crux of the argument was that lateral undulation was the main factor affecting breathing during locomotion. This tends to get missed in the later literature. Having an erect stance is going to do very little to effect locomotor stamina compared to just stiffening the thorax while moving. In regards to monitors doing this, Auffenberg (1981) observed that running Komodo dragons will hold their bodies and tails stiff, which should increase their ability to run aerobically (though at the cost of reduced stride length).

    Refs

    Auffenberg, W. 1981. The Behavioral Ecology of the Komodo Monitor. Florida University Press. p. 133

    Carrier, D.R. 1987. The Evolution of Locomotor Stamina in Tetrapods: Circumventing a Mechanical Constraint. Paleobiology. 13(3):326–341

    Owerkowicz, T., Farmer, C.G., Hicks, J.W., Brainerd, E.L. 1999. Contribution of Gular Pumping to Lung Ventilation in Monitor Lizards. Science. 284:1661–1663.

  9. LeeB Says:

    I agree with Duane; If varanids can develop unidirectional air flow in their lungs I would not be at all surprised if mosasaurs did too.
    If you can get more oxygen out of a lungful of air you can spend less time at the surface breathing where you are vulnerable to attack from below.
    And the rapid size increase and diversification of the mosasaurs suggests they were doing something(s) very right.

    Also on the topic of understudied modern animals, has anyone looked closely at how bats breathe especially when they are flying.
    There might be some interesting things going on that no-one has noticed.

    And comparing the breathing of pygmy monitors with komodo dragons and salvadori’s monitors would be a good way to look for the effects of size on their lungs; and looking at the lungs and breathing of perenties which have incredible stamina for a lizard would be a good idea too.

    LeeB.

  10. Matt Wedel Says:

    Or, is unidirectional airflow primitive for varanoids, inherited by varanids and mosasaurs alike, and lost–maybe–in snakes? In addition to checking more monitors, someone should have a look at Gila monsters and snakes. (I know there has been quite a bit of work on snake respiration already, but heck, there had been quite a bit of work on varanid and croc respiration and no-one caught the uniflow stuff until the past three years, so clearly someone needs to go look for uniflow in snakes.)

    As far as bats go, yeah, there has been a ton of work on their respiration. They breathe just like the rest of us mammals, and their alveolar lungs do not even allow the possibility of undirectional airflow since everything goes in and out by tidal flow through the entire bronchial tree. So unidirectional, air-sac-driven breathing may make flying easier, but it’s possible to be a successful powered flier without it.

  11. coherentsheaf Says:

    Are monitor lizards as a whole really that much more efficient?

    Reading Clementeset al. paper on varanid endurance, we see quite a bit of variance regarding their performance and a lot of overlap with other squamates. (See here: http://terrestrialecosystems.com/wp-content/uploads/2013/05/Clemente-endurance.pdf)

  12. David Marjanović Says:

    So much awesomeness!

  13. Mark Robinson Says:

    Just wow. Great summary Matt. I wondered about Mosasaurs too and have a couple of questions but will wait until the follow-up post about volant sauropods (or have I misinterpreted that?).

  14. Matt Wedel Says:

    coherentsheaf wrote:

    Are monitor lizards as a whole really that much more efficient?

    Reading Clemente et al. paper on varanid endurance, we see quite a bit of variance regarding their performance and a lot of overlap with other squamates.

    Thanks for the link to the paper. A few points:

    1. Endurance is only one variable, and there are many others an animal might optimize. A horse can outrun a cheetah, but only if given a long enough head start. :-)

    2. Varanids actually rock at endurance. See the max endurance graph in Figure 8, and note that it is on a log scale. The intercept for non-varanids looks to be 1.4, and the varanid intercept is about 1.7. Unpacked, those numbers are 28 and 50, which means that on average varanids have nearly twice the endurance of non-varanids!

    3. Yeah, there’s variation, but. As Clemente et al. note in the abstract, and show in Figure 5, the species with the poorest endurance are all sit-and-wait predators–and as Figure 8 shows, the endurance of even those lowest-performing monitors is still at or above the best-fit line for non-varanids.

    So the answer to your question is, “Yes”. As a whole they tend to have twice the endurance of other lizards, and even the crappiest monitors are still as good or better than non-varanids.

    Now what we need someone to do is take the endurance data from Clemente et al. and the lung morphology data from Becker et al. (1989) and mash them up. The first step would be to see if endurance can be predicted by the gross morphology of the lungs. The next step would be to Schachnerize those monitors and see if airflow patterns varied, and if that variation was linked to gross morphology, endurance, or both.

  15. Mike Taylor Says:

    I notice with amusement that the linked page on bird respiration opens with yet another demo of why scalebars are best avoided. I assume the caption has the 1 cm and 2 cm measurements switched.

  16. Mike Taylor Says:

    “I’ve had to rebut myself within the space of five years (Wedel 2007: prosauropod pneumaticity is equivocal. Yates et al. 2012: oh no it’s not!)”

    Not to rub it in, but: twice, actually (Wedel 2009: pneumatic hiatuses are diagnostic for abdominal air-sacs, Wedel and Taylor 2013b: oh no they’re not!)

  17. Mike Taylor Says:

    “So unidirectional, air-sac-driven breathing may make flying easier, but it’s possible to be a successful powered flier without it.”

    … at least somewhat successful. Bats have never got big, like pterosaurs and (to a lesser extent) birds. I wonder whether respiratory inefficiency is part of the reason. We mammals do seem to have got locked into some very inefficient local maxima; optimising the heck out of sac-shaped lungs looks like another one.


  18. crocs secondarily ecothermic – that’s an old old “news”! I was taught it in the late 90s, with lots of evidence behind it.


  19. These are fantastic news!

    Not only because I’m deep in love with all Toxicofera but also because I have a speculative dragon project where varanids are the closest relatives of the Draconiformes and I had a few problems with the design of the air sacs.

  20. Matt Wedel Says:

    Not to rub it in, but: twice, actually (Wedel 2009: pneumatic hiatuses are diagnostic for abdominal air-sacs, Wedel and Taylor 2013b: oh no they’re not!)

    Fat Hobbit is always so polite.

    … at least somewhat successful. Bats have never got big, like pterosaurs and (to a lesser extent) birds.

    Yeah, it’s an interesting problem. Mexican free-tailed bats have been tracked up to 11,000 feet when feeding on swarms of moths and on flights to hibernation caves, which can be cover hundreds of miles. But these feats fall far short of birds flying up to 30,000 feet and undertaking nonstop flights of thousands of miles. Plus, as you note, birds get a lot bigger and pterosaurs got bigger still. The question is, do bats underperform compared to birds because their respiratory system is less awesome, or because of ecological factors: hibernation caves are typically only a few hundred miles apart at most, bats larger than flying foxes might have a hard time finding things to hang from, etc. Or some combination of both?

    For max altitude anyway, the answer is almost certainly respiratory limitation, mammals just can’t hack it up that high. The reliance of most bats on hanging in repose could be seen as another local maximum, compared to the versatility of birds which only need an upward-facing surface to land on (and yeah, I know, small ones can land on vertical surfaces like tree trunks or even hang upside down themselves). Ken Dial gave a great talk at SVP this year on how birds actually get along with their wings and feet, and showed some photos of normally ground-living birds sitting on skinny branches with no problem, despite their lack of grasping toes. That does give me some pause, because it makes me wonder what bats are capable of that most of us just don’t know about.

  21. Mike Taylor Says:

    Fat Hobbit is always so polite.

    LOL!

  22. Matt Wedel Says:

    On the bird-bat front, there is a fabulously interesting paper by J.N. Maina from 2000 called, “What it takes to fly: the structural and functional respiratory refinements in birds and bats.” The section “Flight speed, endurance, and altitude” lists the records for both birds and bats, and that section is worth the price of admission all by itself. Or it would be, if admission had a price: the paper is freely available here.

  23. William Miller Says:

    If bats are inferior fliers to birds, why haven’t night-flying birds (owls, frogmouths, potoos, nightjars…) outcompeted them to extinction?

  24. Matt Wedel Says:

    If bats are inferior fliers to birds, why haven’t night-flying birds (owls, frogmouths, potoos, nightjars…) outcompeted them to extinction?

    Two possibilities come to mind. One, bats are inferior to birds at the edges of performance–max altitude, max distance, etc.–but may be able to compete very well in the comparatively low altitude, low-endurance regime where they spend most of their time.

    Two, I don’t know all the details, but I’ll bet that bat sonar smokes the vision and hearing of night-flying birds in terms of fidelity and detail, which would give bats a big advantage in any head-to-head contests. Circumstantial evidence for this comes from the predation of birds by bats on the wing.

  25. Matt Wedel Says:

    I’ll bet that bat sonar smokes the vision and hearing of night-flying birds in terms of fidelity and detail, which would give bats a big advantage in any head-to-head contests.

    Should have said, “as well as allowing them to outperform birds at catching insects on the wing.”

  26. William Miller Says:

    Ah – good point.


  27. […] Monitor lizards have unidirectional lungs like birds and crocs. […]

  28. Michael Reed Says:

    Nice research.


  29. […] ancestors. Crocodiles and monitor lizards have both been shown to have flow through systems. (See here.) Going back to the drawing above, crocodiles separated from line leading to birds way back when […]


  30. […] body of work by his students), Emma Schachner (not on pneumaticity per se, but too closely related [and too awesome] to ignore), Daniela Schwarz, and Jeff Wilson (and his students), plus important singleton papers […]


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