One of the quintessential depictions of prehistoric times is that of an ancient, often volcano ridden, landscape full of animals bearing large showy sails of skin stretched over their backs. Sailbacked animals are rather rare in our modern day and age, but back in the Mesozoic and Paleozoic there were sails a plenty.
By far the most popular sailbacked taxa of all time would be the pelycosaurs in the genus Dimetrodon. These were some of the largest predators of the Permian (up to 4.6 meters [15 feet] long in the largest species). Dimetrodon lived alongside other sailbacked pelycosaurs including the genus Edaphosaurus. These were large herbivores (~3.5 m [11.5 ft] in length) that evolved their sails independently from Dimetrodon. The Permian saw many species of sphenacodontids and edaphosaurids, many of which sported these showy sails (Fig. 1. [1–8]).
However sails were hardly a pelycosaur novelty. The contemporaneous temnospondyl Platyhystrix rugosus (Fig. 1 [9]) also adorned a showy sail.
Fast forward 47 million years into the Triassic and we find the rauisuchians Arizonasaurus babbitti,Lotosaurus adentus, Xilousuchus sapingensis, and Ctenosauriscuskoeneni , all bearing showing sails on their backs (Fig. 1 [10–13]). Much like in the Permian, many of these taxa were contemporaneous and, while related, many likely evolved their sails separately from one another.
There are currently no fossils of sailbacked tetrapods in the Jurassic (as far as I know. Feel free to chime in in the comments if you know of some examples). However the Early Cretaceous gave us a preponderance of sailbacked dinosaurs (Fig. 1 [14–19]) including the cinematically famous theropod Spinosaurus aegyptiacus, the contemporaneous hadrosaur Ouranosaurus nigeriensis, the gharial-mimic Suchomimus tenerensis, the potentially dual sailed sauropod Amargasaurus cazaui, as well as the allosauroids Acrocanthosaurusatokensis, and Concavenator corcovatus. Lastly, the discovery announced last year (and just now coming to light in the news) of better remains for the giant ornithomimid Deinocheirusmirificus have revealed that it too may have sported a small sail along its back.
Once again we find a group of related, largely contemporaneous, animals, most of which probably evolved their sails separately.
Such a huge collection of sailbacked animals all living around the same time (and sometimes the same place) has begged for some type of functional explanation. The usual go-to for large, showy surfaces like these or the plates of Stegosaurus has been thermoregulation. The thinking being that blood pumped through a large surface area like this, when exposed to the sun, has the ability to warm up faster than other areas of the body. Conversely when the sail is placed crosswise to a wind stream, or parallel to the orientation of the sun, heat will radiate out into the environment faster than other areas of the body. That most sailbacked dinosaurs were “localized” to equatorial areas, coupled with the large sizes of all the taxa (1-10 tonnes depending in species) has favoured a cooling mechanism function for dinosaur sails. Whereas a heating function has been presumed to be the primary function for sails in Dimetrodon and Edaphosaurus. No real function has been ascribed to the sails in rauisuchians or Platyhystrix, though this is probably due to a lack of knowledge/interest in these groups.
Alternate functions proposed for these sails have included a self-righting mechanism for swimming, sexual signaling and other presumed display functions. In certain cases, namely Spinosaurus aegyptiacus and Ouranosaurus nigeriensis, it has even been argued that the enlarged spines did not support a sail, but rather were supports for a large, fatty hump akin to that of camels or bison (Bailey 1996, 1997).
Given the wealth of hypotheses for potential sail functions it would be beneficial to first understand what extant sailbacked taxa use their sails for. Unfortunately—though unsurprisingly—there are few if any scientific studies on sail use in extant sailbacked animals. This has lead to the apparent assumption that there are no extant vertebrates with sailbacks.
There are, in fact, quite a few sailbacked animals alive today. These include various fish, amphibians and even reptile species. Learning what these taxa use their sails for may offer us a glimpse at what extinct animals were doing with their sails. Continue reading → Post ID 1048
Yutyrannus artwork by Brian Choo. Sciurumimus artwork by Arkady Rose
This year has seen the discovery of two big deal dinosaur specimens. At least they are a big deal in regards to dinosaur integument and, possibly, metabolism.
First off from a few months ago we had the announcement the theropod Yutyrannus hauli, the “beautiful feathered tyrant.”
Xu, X., Kebai, W., Ke, Z., Qingyu, M., Lida, X., Sullivan, C., Dongyu, H., Shuqing, C., Shuo, W. 2012. A Gigantic Feathered Dinosaur from the Lower Cretaceous of China. Nature. Vol.484:92-95
This was not just a single fossil, but a collection of three fossils (one might be tempted to call it a family group, but that would only be speculation). As with all other dinosaur fossils that have been found to have filamentous integument, these guys come from Liaoning, China. They are suspected to have come from the Jehol Group in the Yixian formation. I say suspected because the complete three specimen set was a purchase from a fossil dealer, an all too common occurrence for Chinese fossils. As such the provenance information is unknown. A lot of Chinese fossil dealers don’t like to give away the location of their find due to the potential loss of other profitable specimens. This current trend in China is a good example of what happens when capitalism comes into play with fossil collecting (something that the U.S. has been mostly, but not entirely, able to avoid). So it is currently uncertain whether these fossils are from the Yixian. However given that all the others guys are too it is probably a good bet. Given the sketchy nature in which many Yixian fossils are collected, coupled with the possibly large consequences of the find, one should naturally be skeptical of the fossil. Had it been one individual on multiple slabs I would question its validity as a real thing. However since Y.huali is known from three individuals, and the filaments seem to follow a consistent pattern around the body (compare that to the helter-skelter nature of Tianyulong‘s preservation), forgery seems unlikely. These guys are probably the real deal. This has some potentially far reaching consequences to interpretations of Late Cretaceous coelurosaurs and the Jehol Biota itself (more on this in a bit).
The second announcement came just a few weeks ago. This was the discovery of a potentially new, miniscule theropod from Bavaria Germany.
Rauhut, O.W.M., Foth, C., Tischlinger, H., Norell, M.A. 2012. Exceptionally Preserved Juvenile Megalosauroid Theropod Dinosaur with Filamentous Integument from the Late Jurassic of Germany. PNAS Early Edition:1203238109v1-201203238.
The specimen is exceptionally well preserved. So well preserved in fact that it actually looks like a plastic toy. While this degree of preservation warrants importance all its own, the main interest behind this new guy—dubbed: Sciurumimusalbersdoerferi (Albersdörfer’s squirrel mimic)—is the apparent presence of filamentous integument on the body coupled with its apparent placement among much more basal theropods. This discovery has far reaching consequences for theropod integument interpretations. Note: As with Y.hauli, Sciurumimusalbersdoerferiwas also purchased from a private collector. I don’t suspect forgery here either as this was in Germany, where fossil dealing is neither a big problem nor a lucrative business. The exceptional detail on the specimen would also require a substantial amount of theropod knowledge to pull off. Anyone having that amount of knowledge is more likely to be a real paleontologist than a get rich quick forger.
Aegisuchus witmeri goes to town on a Mesozoic lungfish. Illustration by the talented Henry Tsai
Oh hey look, the blog has come to life again, if just for a bit. As has been typical these few years, things IRL have taken up much of my time and the website has suffered because of it. I still have a few posts that I have been sitting on as I try to find the time to finish them. Until then small updates like this will have to do.
Congratulations to the internet’s own Nick Gardnerfor helping get this guy published.
Stomatosuchus was the quintessential "duck faced" croc. Illustration by Dmitry Bogdanov
The croc in question — Aegisuchus witmeri— was a member of the Aegyptosuchids. They were a strange group of eusuchians that are known mostly for their weird, flat “duck faces.” As there are no living crocodylians that even come close to these guys in skull shape, it is difficult to imagine what these guys were doing with these flattened rostra. One hypothesis was that, given their numerous small teeth, these guys were filter feeders.
Holliday and Gardner describe a preserved braincase and compare it to other published data on Aegyptosuchids. Results suggest that this guy was huge by modern croc standards (~9 meters) and no slouch for a Mesozoic croc. Muscle scars indicate the presence of strong jaw opening abilities in this taxa, which would go well for a possible filter, or suction feeder.
Probably the most interesting feature of this guy, and the one likely to spark the most controversy, was the presence of an enlarged boss on the top of the skull. Inferred vasculature to this region suggest that Aegisuchus witmeri was using this part of its skull for something. That thing might have been a display structure such as an “eyespot” or just a particularly bright patch of skin. Though speculative, there are reasons to consider this possibility, including the fact that extant crocodylians use their heads in all manner of displays.
All in all this was a pretty cool critter. The species epithet was named in honour of professor Lawrence Witmer, PhD, prolific paleontologist, comparative anatomist and even blogger. He is my mentor and was Dr. Holliday’s back in his PhD days. It might not be Archaeopteryx, but getting named after a bad-ass ancient crocodile isn’t half bad.
_Polycotylus latippinus_ mother giving birth to young in a very cetacean-like fashion. Illustration by: S. Abramowicz
Just announced today in Science, researchers at the Marshall University and the Los Angeles County Museum described the presence of fossil young inside the body of the plesiosaur: Polycotylus latippinus. The results of their find seem to confirm what has been suspected for quite some time now, that plesiosaurs were viviparous animals.
O’Keefe, F.R., Chiappe, L.M. 2011. Viviparity and K-Selected Life History in a Mesozoic Marine Plesiosaur (Reptilia, Sauropterygia). Science. Vol.333(6044):870-873
The evidence had been mounting for some time now. While plesiosaurs came in numerous shapes and sizes, most of those sizes were in the large to giant range measuring in at multiple tonnes (e.g. Liopleurodon and Kronosaurus). That is a lot of weight to attempt to drag up on a beach for egg laying. Further, though the rib cage is well braced ventrally, the limb girdles are not braced against the vertebral column. This would make it very hard for a large landlubbing plesiosaur to make any kind of headway as the limbs would have no leverage against the body for dragging itself on land.
Lastly, and perhaps most importantly, we have known of at least one plesiosaur fossil that had embryos in it. This has been known for at least five years now (I learned of it four years ago, and it has been hinted at before [Smith 2008]). Sadly this specimen still remains unpublished. This new paper by O’Keefe and Chiappe goes on to mention the relatively large size of the young, estimated at 1.5 meters when born. This was much larger than the young of other large extinct and extant marine reptiles. The authors (cautiously) suggest that this might hint at a different life history for plesiosaurs vs. other marine reptiles. They posit that plesiosaurs might have nurtured a small amount of relatively large young, which in turn might have meant that they were more social than previously thought.
Naturally this has resulted in the inevitable comparison to whales. While a “pod of plesiosaurs” does sound interesting, we have far too little evidence to say if such a thing ever happened (and the authors state this too). What we do know is that young plesiosaurs have been found in shallow marine settings. These have been posited to have been “nurseries” where young could stay out of sight from predators while reaching adult size (Martin et al. 2007). Whether, or not adults stayed around, or if they joined a “pod” later (if at all) is all unknown. Still, it is nice to see some validation to what seemed almost necessary for so long.
Admittedly not everyone is convinced (a good thing to see in science). Dr. Ken Carpenter of the Utah State Museum offered Science magazine a dissenting view, suggesting that the position of the young could still indicate that these were juveniles that had been eaten. The O’Keefe and Chiappe considered this in the paper and pointed out that the skeletons lacked any signs of acid etching, as well as showed numerous skeletal bones that did not appear fully ossified. Further analysis could shed more light on this. Publishing on that other plesiosaur could really help things out too.
Viviparity - could these guys be next? Image from the Nature Museum in Stuttgart.
Assuming that we are looking at viviparous plesiosaurs, that just leaves two other large marine reptile groups of the Mesozoic. Turtles and Crocodylomorphs. In both cases we have extant animals that are obligate oviparous animals, but there might still be reason to think that live birth might have evolved in these groups too. Again, much like with the plesiosaurs, the groups in question (protostegid sea turtles and the podocnemid Stupdendemys, as well as metriorhynchid crocodylomorphs) have members that grew extremely large. While Protostega gigas may have been able to haul itself out on land as extant leatherbacks (Dermochelys coriacea) do, it seems harder to justify that in the much larger Archelon ischyros; an animal that has been estimated to tip the scales at 2 tonnes. Given the amount of effort it takes a large female leatherback (~1 tonne) to haul herself up and down a beach (not to mention the damage it causes to the animals in the short term), it would be all the more amazing if A.ischyros was able to pull off such a feat. The same would go for the metriorhynchids, who had adapted completely to a marine lifestyle (i.e. they had flippers and a tailfin). If a 5 meter Gavialis gangeticus can barely move around on land, I’d hate to see what a 5 meter Dakosaurus would look like. To date we have no evidence one way, or the other for these last two groups. There is a bit more resistance to the idea of viviparity in these groups as no extant members exhibit viviparity. This has lead some to wonder if the calcified eggs of archosaurs (and many chelonians) might prove a phylogenetic constraint on live bearing (the young absorb calcium from the shell, which could mess up calcium absorption in a taxon evolving along the lines of viviparity). The chelonian shell — in turn — may also have been constraining on the size of young that can be held in the body cavity. Still, to date, there are no nests, eggs, or embryos for any of these taxa, thus leaving the matter open for debate. It is interesting that neither protostegids, nor metriorhynchids got to the huge sizes of mosasaurs, ichthyosaurs and plesiosaurs, but that could have been for any number of reasons including the simple lack of finding the larger taxa yet. Until then the physics vs. phylogeny argument remains unresolved.
Anyway, compelling evidence for live bearing in at least some plesiosaurs. Woohoo!
~Jura
References
Martin, J., Sawyer, F., Reguero, M. Case, J.A. 2007. Occurrence of a Young Elasmosaurid Plesiosaur Skeleton from the Late Cretaceous (Maastrichtian) of Antarctica. 10th Int.Symp.Antarctic Earth Sciences.
O’Keefe, F.R., Chiappe, L.M. 2011. Viviparity and K-Selected Life History in a Mesozoic Marine Plesiosaur (Reptilia, Sauropterygia). Science. Vol.333(6044):870-873
A classic regression line showing metabolism scaling with mass. From: universereview.ca
Last timeI gave a brief (?) run through the various types of metabolic rates that we find in the animal kingdom, along with the various ways in which they were measured. There was one last metabolic rate type I wanted to cover, but instead only teased; that of mass specific metabolic rate (MSMR). This type of metabolic rate measurement is fundamentally different from all the others that we talked about previously, and coupled with the sordid history behind this concept, it seemed appropriate to give MSMR its own post.
So without further ado, let’s get this party started.
MSMR = Mass Specific Metabolic Rate
Dinosaur fanatics will no doubt recognize this infamous phrase. It tends to pop up a lot in literature dealing with dinosaur energetics. Mass specific metabolic rate differs from other MR measurements because it is not an actual measurement. Rather, MSMR is a mathematical abstraction taken from actual metabolic rate measurements of multiple taxa spanning a wide range of sizes. Ultimately what MSMR does is show us how metabolism scales with size. That in itself deserves a brief digression.
Scaling and biology
Size can radically change an organism’s structure, and function. The reasons for this relate back to some fundamental physical properties of all things. For instance, consider the metrics of height, width and length. Each of these measurements, taken by themselves, represent one dimension only. If one wants to get the idea of the size of a two dimensional object, one need only combine (multiply) any two of these measurements. If we combine all three we can get a good 3-D representation of how much space an object takes up.
If any structure is to grow isometrically (i.e. everything grows at the same rate) then for any increase in a linear measurement (length, width, or height) the area of that object will double, while the volume of the object will triple.
For instance, if an object that was 1 meter long, suddenly doubled in size isometrically, its area would increase by:
2m x 2m = 2m2, or 4 meters in area (4 square meters).
While the object doubled its length, it quadrupled its area.
Physical laws on scaling mean that ants of this size and shape will always remain in the realm of fiction…on Earth. Pic from Undead Backbrain
Meanwhile the volume of that object will increase by a multiple of all three linear measurements:
2m x 2m x 2m, = 2m3, or 8 meters in volume/mass (8 cubic meters).
So now the object that has increased its linear measurements by 2, increased its surface area by 4 and increased its mass by 8.
This has immediate implications for any organism. If we look at just vertebrates we find that the strength of things such as bone and muscle are determined by their cross sectional area.
To put this in more practical terms: for any given change in length, width or height of an isometrically growing organism, strength is going to double while weight is going to triple. The obvious problem here being that eventually (and rather quickly) weight is going to outpace strength. This puts a limit on how big an organism can get. It also explains why the short guy in gym class can always do more chin ups than the taller guys.
The way that life has found around this isometry problem is to just dump the concept of isometry altogether. Instead, organisms will grow different body parts at accelerated, or decelerated rates (e.g. increasing bone density and muscle size faster than other organs for large animals). This is referred to as allometry. In general, allometric equations are generally some type of variable regressed against body mass. By doing so, one is able to determine how that variable is changing in relation to a change in size. It tends to look something like this:
y = aMbb
Where a is an experimentally determined allometric coefficient, Mb is body mass, and b is the allometric exponent.
For the purposes of this discussion the general rule is that bigger vertebrates will have relatively bigger bones and muscles than a smaller vertebrates scaled up to their size.
Rubner, Kleiber and metabolic scaling: battle of the Maxes.
If bigger creatures generally show an allometric increase in size for various body parts, then one would expect to find some kind of similar allometric effect for metabolism. After all, a bigger animal is going to be composed of more cells, which will require more energy to power. So then should we expect metabolic rate to scale to mass (i.e. to increase by the third power?). Perhaps, but one should also keep in mind that as each of these cells expends energy, they are also producing a little bit of heat. Thus more cells results in a hotter critter. In animals, heat is lost primarily via conduction; a process that is intimately associated with surface area. Perhaps, then, it would be better if metabolic rate followed surface area instead, and increased by the second power.
However which way metabolism scales it looks like it should relate somehow to these two variables.
In order to figure this out, one must measure the lowest metabolic rate of one’s animals — the BMR/SMR. The reason for using BMR/SMR is that one is theoretically looking at the “metabolic floor.,” or the MR level that must be maintained to avoid death (and, thus the MR that is not likely to be affected by food acquisition, exercise, stress, etc.). The importance of using BMR will come up again further down.
One measures the BMR/SMR of one’s animals and plots those metabolic rates against the size of the animals measured. From this one should be able to acquire a ratio of metabolic rate to mass. Often the data must be regressed first in order to achieve any kind of statistical analysis.
The first attempts at this were done using mammals, and one of the most influential people to try this out was Max Rubner. Rubner measured the metabolic rate of dogs and regressed these data against mass. What he found was that as body size increased, metabolic rate increased by approximately 2.325 times. Rubner took this one step further and found that his exponent for metabolic rate could be made mass independent by simply subtracting it from the exponent for mass (3.0). The end result: mass specific metabolic rate for dogs appeared to increase by the 0.675 power, or the 2/3rds power (Rubner 1883).
So what does all of this mean? Essentially it means that metabolism increases slower than body mass. So if we were to graph out metabolism in relation to the amount of mass that that metabolism is powering, we would discover that the data form a negative slope, with bigger animals falling further towards the low end of the slope than smaller animals. To put it more succinctly, it takes less relative metabolic energy to power a larger mass than it does to power a smaller mass. This is mass specific metabolism.
A common misconception about MSMR is that metabolic rate goes down as one gets larger, but this is not the case at all. The metabolism of a large animal is still larger than that of a small animal, it is just that for a given mass, the increase in metabolism is less than one would expect. For example if you took the BMR of a large beagle (14kg) and the BMR of a boxer (30kg), one would expect the boxer to show a basal metabolic rate that is at least twice as fast as that of the beagle (since it is roughly twice the mass of the beagle). If we input the data into the allometric equation mentioned earlier, we get:
*The 89kcal/day/kg is the allometric constant given by Rubner 1883. It is the average BMR for his dogs after correcting for mass.
A visual example for the scaling of metabolic rate.
What we find is that the boxer does have a higher metabolic rate than the beagle, but it is only 1.67 times greater, instead of 2. This lower than expected metabolic rate will translate to lower than expected food costs as well. To put it another way: it would be cheaper to feed one boxer than to feed two beagles of roughly the same size, or to shift things away from dogs: it is cheaper to feed one elephant than it is to feed an elephant’s weight in shrews.
Rubner’s discovery was amazing and his equation elegant. It became to be referred to as: Rubner’s surface law of metabolism; a law that would stay in practice for 50 years afterward. It wasn’t until 1932 that this law was officially challenged, and by another Max at that. Swiss agricultural chemist Max Kleiber studied MSMR in mammals ranging from rats to cows. He plotted their body masses and BMRs on a logarithmic scale, and came to the conclusion that Rubner’s 2/3rd surface area law was incorrect. Rather mass-specific metabolism followed a “higher power.” That of 3/4, or 0.75. It’s interesting to note that the result Kleiber found was in fact not quite 0.75 (it was 0.73). This number was rounded to 0.75 in order to make it more “slide rule friendly” (Schmidt-Nielsen 1984)
Quarter power laws for everyone.
A simple illustration based off of Brody’s (1945) infamous mouse to elephant curve. Note the negative slope showing how much energy is used per hour by each gram of tissue
So Rubner’s law was broken, and Kleiber’s law came in to replace it. For over 70 years Kleiber’s law was held up as that rare case of a biological constant Subsequent BMR studies of mammals (Brody 1945) and other organisms including bacteria (Hemmingsen 1960) found results that “hovered” around 0.75, thus suggesting that this biological law was not just a mammal thing, but rather a hallmark of all organisms.
This leads us to the obvious question of why?
Typically, the response to this question is a thermal one. Small animals lose heat easier than large animals, due to their larger relative surface area. If a large animal has an easier time retaining body heat, then it would make sense that its body would need to produce relatively less of it. The problem with this answer is that it only works for automatic endotherms (i.e. mammals and birds). However the MSMR phenomenon is present in bradymetabolic thermoconformers too. Therefore this answer cannot be the only one.
The answer to this question had remained elusive up until 14 years ago, when West et al proposed that the quarter power scaling laws that we see in nature appear to be the result of the fractal nature of delivery networks (West et al 1997), which in the case of vertebrates, are blood vessels. West et al. proposed that the fractal nature of blood vessels, combined with area preserving branching patterns could be used to explain why metabolism scales to the 3/4 power. The work by West et al was the first real attempt to explain why metabolism should scale to the 3/4 power, and has since been referred to as the metabolic theory of ecology.
Data on MSMR calculations from Brody and Hemmingsen all seemed to show that everything followed the 3/4 exponent rule. These two papers, along with Kleiber’s influential work, are some of the most cited papers in the physiological literature. One the one hand this illustrates just how influential their findings were for biology in general, but on the other hand it also suggests that their work should be the most thoroughly scrutinized. Scientists occasionally take the work of others for granted. This can lead to unpleasant side effects and near dogmatic views of things (e.g. the old saw about swamp bound dinosaurs). In general, it is a good idea to occasionally go back to these seminal works and verify that the authors got things right the first time.
Dodds et al. (2001) did just that. The authors looked back at the work of Brody, Hemmingsen, Keliber and others in the field of MSMR, in order to see if the 3/4 power law was a real thing, or mathematical error. Their results found that data from as far back as 1982 suggested that there was a problem with the 3/4 power law. Much of the data that had come out since Kleiber, Brody and Hemmingsen’s time suggested that the exponent for metabolic power should lie much closer to 2/3rds than 3/4. Dodds et al. went even further and challenged the metabolic theory of ecology by citing apparent mathematical errors in the work by West et al. in 1997. This challenge to the model by West et al. remains controversial, with arguments that continue to sling back and forth (e.g. Kozlowski and Konarzewski 2004, Brown et al 2005). Dodds et al (2010) recently took on the nutrient supply approach spearheaded by West et al, but looked at it from a purely geometric point of view (rather than fractal.). Their results found strong support for nutrient networks being the limiting factor for metabolic rate. Their results also found that these structures scaled to the 2/3rd power.
Kleiber’s faux pas; or: why MR type matters.
In 2003, White and Seymour gave a critical re-evaluation of Kleiber’s initial work. Kleiber was an agriculturist, and at least part of his impetus for looking at MSMR was to produce a greater yield in biomass, for farm animals. It is no surprise, then, that most of Kleiber’s study animals were of the barnyard variety. The problem with using livestock to determine MSMR is that domestic animals — especially ones that are raised for food — have been under extensive selection to produce larger animals for less cost. Thus, they are unlikely to be accurate representatives of a “wildtype” metabolic rate. Another, much larger, problem was the over-representation of artiodactyls in Kleiber’s study. In fact, both Kleiber, and Brody (and by extension Hemmingsen, as he re-used most of Brody’s data) had artiodactyls encompassing over 20% of their data.
Okay, so what exactly is the problem here?
The problem is that artiodactyls only make up approximately 5% of all extant mammals. To increase this representation by 4 times is going to skew the results. Also, as White and Seymour pointed out (2003), many of these animals were on the upper edge of the regression line, resulting in a disproportionate influence over the scaling exponent.
Topping it all off was the biggest issue of all, and one that crops up time and time again with many metabolic studies. As mentioned in part 1 of this series, BMR and RMR are not the same thing. If one is going to measure the mass specific metabolism of an animal, one must get it from the basal metabolic rate. There are strict methods for acquiring these data (McNab 1997), not the least of which is the necessity of measuring the metabolism of an animal that is in a post-absorptive state. This is a time in between eating and fasting, where the body is not doing any digestion at all. This is important because digestion can actually ramp up basal/standard metabolism substantially over resting/fasting levels. Perhaps the most dramatic example of this would be data from Burmese pythons (Python molurus) in which feeding metabolism increases SMR by over 44 times the resting rate (Secor and Diamond 1996)!
Ensuring that an animal is in a postabsorptive state is no easy task. Some taxa, such as very small mammals (e.g. shrews, hamsters, etc) run so close to the thermal edge that it might be impossible to get them in a postabsorptive state without killing them. As Speakman et al (1993) wittingly put it: “Before small shrews become post-absorptive they enter a state of profound rest in which they have zero metabolism and from which they never recover!” One might wonder, then, if BMR = RMR in such a situation (but see McNab 1997 for a counterpoint).
Guys like these can take up to 7 days to fully absorb a meal! cows from: icanhasinternets.com
The problem with artiodactlys is that they are ruminants. That is to say they rely on bacterial degradation of cellulose in order to extract nutrients from their food. Because of this, the digestive phase for ruminants can last for a substantially long time. Typically, artiodactyls are fasted for 72 hours before having their BMR measured, yet data on digestion in ruminants suggests that they can last as long as 7 days before entering a postabsorptive state (White and Seymour 2005), if at all (McNab 1997). When this is not taken into account, one winds up measuring RMR instead of BMR, which raises the overall exponent to the mass specific metabolic rate equation.
Now, to be fair, Kleiber did note that his extensive use of artiodactyls (three cows and a sheep) could have an unwanted effect on his data if they were not being measured in a postabsorptive state. Thus, he performed an analysis with and without his ruminants. Interestingly, the results still hovered around 3/4ths (0.72-0.73). White and Seymour (2005) argued that the reason behind this still high exponent might be due to the relatively high BMRs of domestic carnivores (Kleiber used dogs) and humans. The authors later went on to show that the removal of these data points ultimately drops the exponent down to the 2/3rds that seem to be so commonplace among other metabolic studies.
Another aspect of BMR studies that tends to get overlooked when researchers attempt MSMR calculations is the need to measure animals in a thermoneutral environment. This is an environment in which the animal is not actively thermoregulating, otherwise known as the thermoneutral zone. Automatic endotherms are often lauded for their ability to maintain body temperatures regardless of the external environment. This seems to have lead to the assumption that the environmental temperature should not matter, which results in experiments that grab metabolic rate data from animals that are in fact, rather stressed (e.g. Hanski 1984, who measured “BMR” in shrews that were 7°C below their thermal neutral zone). White and Seymour noted that mass and body temperature showed an intimate relationship in mammals (White and Seymour 2003), and that in order to get a useful comparative estimate of BMR for mammals that encompasses the full range of masses seen in this group, BMR should be standardized to a common body temperature. This is very intriguing for White and Seymour have essentially taken BMR and converted it to SMR. As mentioned previously, automatic endotherms do not escape the Q10 effect, but instead keep it at bay by keeping their cells encased in a bubble of stable temperatures. This means that one can use Q10 values to adjust BMR to fit an appropriate “universal” temperature with which to compare taxa. That temperature turned out to be 36.2°C with a Q10 of 3.0.
White and Seymour discovered that when BMR was standardized to a universally comparable temperature, the mass specific exponent for metabolic rate was approximately 0.67, or 2/3rds. Even more fascinating: when data for birds are given the same rigorous treatment, they also scale to the 2/3rds power (McKechnie and Wolf 2004). So it appears that Rubner had it right all along. For seventy years we have been using a formula that suffered from some hefty methodological errors.
Well at least that’s all fixed now, right?
One power law to rule them all? Probably not.
Dodds, Rothman, Weitz (2001), White and Seymour’s (2003) works to turn over the established 3/4 power law belief in physiology did not go unquestioned Savage et al (2004) gave a particularly in depth critique of their analyses, pointing out some questionable assumptions that White and Seymour had made, as well as the disproportionate amount of data available for mammals (i.e. some genera were over-represented with multiple BMR measurements, while others might not have any data at all). This violates a fundamental assumption of practically every statistical analysis. Namely that data points are independent. Savage et al pointed out that most BMR data exists for mammals that are less than 1kg in size. This is going to bias the regression statistic (indeed, Dodds et al. [2001] noted that the 2/3rd power only seemed effective for mammals up to about 10kg. The authors cited a lack of data for larger taxa as a likely cause of this strangeness).
Savage et al decided to repeat the statistical analyses of White and Seymour, as well as a few other authors. In the process they found various errors in each analysis that resulted in some major discrepancies (e.g. basal metabolic rates that varied over an order of magnitude for the same species in the same study, the exclusion of large chunks of Mammalia that spanned the larger size ranges, thus reducing their dataset). The authors separated their taxa into “bins” that covered various size ranges. The idea being that by separating mass into sections like this, they could turn mass into a treatment effect, which should allow the statistical analysis to better analyze the effect of BMR as described by body mass.
The result of Savage et al’s study showed that the scaling exponent for BMR to body mass was around 0.712 +/- 0.012. This new regression suggested that the “true” exponent for BMR in relation to mass, was neither 2/3rds, nor 3/4ths, but something in between. The authors noted this unexpected result, but quickly pointed out that this was for data that was heavily biased for small size (mostly rodents). This was where the “binning” idea would come into effect. By essentially forcing a uniform distribution across the mass ranges available the authors results revealed an exponent of 0.737 +/- 0.025, or an exponent that lives around 3/4ths.
The authors took this a step further by looking for exponents to describe field metabolic rate and maximal metabolic rate. Their reasoning being that these are more easily obtained measurements that have more biologically meaningful results to them. I am less confident of these results, as FMR encompasses many aspects of an organism’s lifestyle, while MMR can be difficult to fully obtain. Further, I would argue that the benefits of BMR is that they indicate what the bare minimum energy requirements of an organism should be. That has the potential to be extremely useful for paleontology. Especially if one is looking to figure out how much food (at minimum) an organism would need to eat to survive in some environment (and thus, infer something about thermophysiology).
White et al . (2006) responded back, by doing a more thorough analysis of available data. They disregarded Savage et al’s notion of mass “binning” (which was fine, as Savage et al. disregarded the need to adjust for temperature, citing negligibility of the results as the reason), and used data from 938 species ranging from 158mg (0.35 lbs) to 138kg (304 lbs), and covering every major vertebrate class. Data were only used if they fit the strict criteria for BMR mentioned previously, and each group was compared to a standard temperature (38°C and 20°C), after accounting for Q10 effects. Once again, White and Seymour found strong support for a 2/3rds exponent…for mammals and birds.
And this is where we come to the punchline in all of this. While the arguments had previously focused on automatic endotherms, data started to appear in both those groups, and (especially) the groups outside
Figure 1 from White et al 2006 illustrates the mess likely represents a more accurate look of how metabolism scales with mass. Note how the automatic endotherms actually scale up slower than everyone else.
Mammalia and Aves, that a universal metabolic exponent appeared not to exist. This was tackled more formally by White et al. (2007) who reviewed the current literature citing numerous examples where the single exponent view was not being met empirically. This was followed up by a final analysis by the authors on 127 published allometric exponents for taxa that spanned the range of animal classes. Following Felsenstein (1985) they incorporated independent contrasts to remove the effects of phylogeny (which has a tendency to screw the pooch for independence of data points) . The authors then assigned the exponents found to one of three categorical variables:
Taxonomy (Amphibia, Arthropoda, Aves, Actinopterygia/Chondrychthys [“fish”], Mammalia, Reptilia, Prokaryotes)
Thermoregulation (automatic endotherm, or bradymetabolic “ectotherm”)
Metabolic state (FMR, RMR, MMR, BMR/SMR)
Then, after assigning some fancy statistical mojo (weighted generalized mix model, for those that are into that kind of stuff), the authors found that among their three categories, only thermoregulation seemed to show any real affect on where the exponent wanted to go (i.e. it “pushed” the exponent towards some kind of “true mean”). This suggests that a true discrepancy between these modes of thermophysiology ultimately affect metabolic rate. Surprisingly, White et al’s study seemed to show that automatic endotherms converge at an exponent closer to 2/3rds, while everyone else hovers closer to 3/4ths. However there is still considerable sway around these exponents. So much so that White et al. urge researchers to do away with the 2/3rds 3/4ths argument altogether, as it has become quite apparent that choosing one, or the other is going to both bias results and obscure pertinent data. The authors do offer some alternatives that might be used such as statistics that incorporate multiple exponent models, accounting for body mass by using it as a variable in an analysis of covariance (ANCOVA) model, or just choosing the right exponent for the job (e.g. the 3/4ths exponent seems to work well for FMR of mammals, but overestimates the FMR of birds).
Where are we now?
So here we are, finally at the end of this long winded blog entry, and what do we have to show for it? Well…mostly that biological laws are so few and far between that any relationship, or phenomenon that has the audacity to be referred to as a “law” or “rule” should probably be taken with a grain of salt.
Another thing to take away from this is just how complicated metabolic physiology studies really are. They have to account for so many unexpected variables that is amazing we can say anything at all about extant animals. One thing I did not touch upon was the fact that all MSMR equations use regression as their model of choice. A severe limit to this approach (and one that is violated all the time) is that regression models can really only predict — with any certainty — the estimated MSMR of an animal that falls within the size range measured. Once one starts to extrapolate beyond the maximum, or minimum size of the available data, one is practically just speculating.
Regression graph showing trend line for a range of predicted values (bold line) and possible real distributions that exist beyond the measured data (grey dotted lines). Hence why regression predictions should always be limited to the range of data used.
Lastly, given what little we are able to say about extant animal metabolism and its limits, just think about how much less we can confidently say about extinct taxa. This is especially true for paleontological studies that attempt to use metabolic scaling exponents to infer the possible thermophysiology of extinct organisms. Thus any study that attempts to do this kind of paleophysiology, would be best served by computing hypothetical BMR/SMRs that used a wide range of metabolic exponents.
And that, in a nutshell, is what all the fuss is about for MSMR.
~ Jura
References
Brody, S. 1945. Bioenergetics and Growth. New York: Reinhold Publishing Corporation.
Brown, J.H., West, G.B., Enquist, B.J. 2005. Yes, West, Brown and Enquist’s Model of Allometric Scaling is both Mathematically Correct and Biologically Relevant. Funct.Eco. Vol.19:735-738
Castellini, M.A., Kooyman, G.L., Ponganis, P.J. 1992. Metabolic Rates of Freely Diving Weddell Seals: Correlations with Oxygen Stores, Swim Velocity and Diving Duration. J. Exp. Biol. Vol.165; 181-194
Dodds, P.S. 2010. Optimal Form of Branching Supply and Collection Networks.Phys.Rev.Let. Vol.104 (4); 048702
Dodds, P.S., Rothman, D.H., Weitz, J.S. 2001. Re-Examination of the “3/4-Law” of Metabolism. J.Theor.Biol. Vol.209:9-27
Felsenstein, J. 1985. Phylogenies and the Comparative Method. Am.Nat. Vol.125:1-15
Frappell, P. 2006. Respirometry, The Gold Standard. The Physiologist. Vol.49; 12.
Hanski I. 1984. Food Consumption, Assimilation and Metabolic Rate in Six Species of Shrews (Sorex and Neomys). Ann. Zool.Fenn. 21:157-165
Hemmingsen, A. M. 1960. Energy Metabolism as Related to Body Size and Respiratory Surfaces, and its Evolution. Rep. Steno Memorial Hosp. Nordisk Insulinlab. Vol.9;1-110
Heusner, A.A. 1991. Size and Power in Mammals. J.Exp.Biol. Vol.160(1);25-54
Kleiber, M. 1932. Body Size and Metabolism. Hilgardia. Vol.6;315-353
Kozlowski, J., Konarzewski, M. 2004. Is West, Brown and Enquist’s Model of Allometric Scaling Mathematically Correct and Biologically Relevant? Funct.Ecol. Vol.18:283-289
McKechnie, A. E., Wolf, B. O. 2004. The Allometry of Avian Basal Metabolic Rate: Good Predictions Need Good Data. Physiol.Biochem.Zool. Vol.77:502-521
McNab, B. K. 1997. On the Utility of Uniformity in the Defnition of Basal Rate of Metabolism. Physiol. Zool. Vol.70; 718-720
Nagy, K.A., Girard, I.A., Brown, T.K. 1999. Energetics of Free-Ranging Mammals, Reptiles and Birds. Annu.Rev.Nutr. Vol.19;247-277
Nespolo, R.F., Franco, M. 2007. Whole-Animal Metabolic Rate is a Repeatable Trait: A Meta-Analysis. J.Exp.Biol. Vol.210;2000-2005
Packard, G.C., Birchard, G.F. 2008. Traditional Allometric Analysis Fails to Provide a Valid Predictive Model for Mammalian Metabolic Rates. J.Exp.Biol. Vol.211;3581-3587
Savage, V.M., Deeds, E.J., Fontana, W. 2008. Sizing up Allometric Scaling Theory. PLoS Comput.Biol.Vol.4(9):e1000171.
Savage, V. M., Gillooly, J. F., Woodruff, W. H., West, G., B., Allen, A. P., Enquist, B. J., Brown, A. C. 2004. The Predominance of Quarter-Power Scaling in Biology. Funct.Ecol. Vol.18:257-282
Schmidt-Neilsen, K. 1984. Scaling: Why is Animal Size so Important? U.K.: Cambridge University Press.
Secor, S.M., Diamond, J. 1996. Determinants of the Postfeeding Metabolic Response of Burmese Pythons, Python molurus. Phys.Zool. Vol.70(2):202-212
University of Vermont. 2010. Spherical Cows Help to Dump Metabolism Law. ScienceDaily. Retrieved February 27, 2011, from http://www.sciencedaily.com/releases/2010/02/100203101124.htm
West,G.B., Brown,J.H., Enquist,B.J. 1997. A General Model for the Origin of Allometric Scaling Laws in Biology. Science. Vol.276:122-126
White, C.R., Cassey, P., Blackburn, T.M. 2007. Allometric Exponents do not Support a Universal Metabolic Allometry. Ecology. Vol.88(2):315-323
White, C. R., N. F. Phillips, and R. S. Seymour. 2006. The Scaling and Temperature Dependence of Vertebrate Metabolism. Biol.Letters Vol.2:125-127
White, C.R., Seymour, R.S. 2003. Mammalian Basal Metabolic Rate is Proportional to Body Mass 2/3. Proc.Natl.Acad.Sci. Vol.100(7);4046-4049
From archaea to blue whales. Metabolism is a hallmark of all living things
Metabolism, and metabolic rate tend to feature pretty highly in literature related to dinosaurs and other reptiles. For instance it is often stated that reptiles have metabolic rates around 1/10th those of similar sized mammals and birds, but what exactly does that mean? Talks of thermoregulation focus heavily on the role of metabolism, while allometric studies focus on how metabolism is affected by size. Given the prevalence of metabolic terminology in dinosaur and reptile papers/books, I thought it might be best to quickly give a review of metabolism, metabolic studies, and what all of that means for real animals.
Metabolism is everything
Metabolism is defined as the sum total energy expenditure of an organism. That is to say metabolism is the total energy an organism uses during its life. It is often broken up into the chemical reactions that build up resources (anabolism) and the reactions that break those resources down (catabolism). The amount of metabolism, or energy expenditure during a specific interval of time (seconds to days) is referred to as metabolic rate. From bacteria to blue whales, metabolism is the measure of all the energy that lets these critters go, and metabolic rates determine how much energy that is going to take. It can be measured in a variety of ways from respirometry to doubly labeled water and heart rate telemetry. The diversity of metabolic rate measurements is reflected in the units used to measure metabolism; which can range from watts/hour to milliliters of oxygen per minute, and even to joules per second.
Specificity is important
A key thing about metabolic rates is that they are plastic. They change depending on the situation presented. For instance one could measure the metabolic rate of a sleeping cat, and then compare it to measurements from that same cat while playing, or after eating a big meal. Metabolic rates ramp up when energy demand increases, and then ramp down when that energy demand decreases, or when the environment demands drastic energy cuts (e.g. starvation). Thus when measuring the metabolic rate of an animal it is important to decide exactly what kind of metabolic rate you are trying to measure.
And boy, oh boy are there a lot of different flavours to choose from.
One can measure: BMR, SMR, RMR, MMR, AMR, and FMR just for starters.
Those are a lot of initialisms, and they are just the most common ones. The choice of metabolic rate that one decides to measure is also going to dictate the technique that will be employed. So what do all these things stand for, and what technique is best for what? Let’s find out. Continue reading → Post ID 1048
A Galapagos tortoise struts about, secure in the knowledge that no one will ever know where the hell it came from. Photo from petcaregt.com
This is a long overdue follow up to my original Turtle Power article back in…yeah never mind the date.
As established previously, turtles are a strange, and highly diverse group of animals, but how did they come to be this way?
The turtle bauplan has been a phylogenetic double edged sword. On the one hand, the unique shell design, and the necessary body contortions associated with it, make chelonians a very easy group to classify. However, it is these same peculiarities that keep us from finding the ancestor to turtles. To date, there are no “half-turtles.” No good transitionals between one reptile group to that of turtles. As such, the list of turtle ancestors runs all over Reptilia. Some paleontologists believe the origin lies at the base with reptiles like procolophonoids, and pareiasaurs. Others believe turtles are a bit more closely related to extant reptiles, and belong in, or alongside the sauropterygians (plesiosaurs, nothosaurs, and placodonts). There is even some evidence to suggest turtles are actually in the same reptile group as dinosaurs and crocodylians (Archosauria).
Curse that shell! - Photo by tompain
How can the list be this extensive? Read on to find out.
So if you have yet to get your copy of The Complete Dinosaur, or have been itching to snag the most comprehensive book ever written on Deinosuchus, ankylosaurs, or mosasaurs, but didn’t have the necessary funds; now is your chance to get them for cheap.
The old "cold blooded or warm blooded" argument once again rears its ugly head.
[Editor’s note: A response from the authors can be found here. It answers many of the questions I had about the paper, though I feel the biggest question remains open for debate. I appreciate the authors taking their time to answer my questions, and PLoS ONE for allowing this type of open communication.]
This post has taken an inordinate amount of time to write up. Mostly because it required finding enough free time to sit down and just type it out. So I apologize ahead of time for bringing up what is obviously old news, but I felt this paper was an important one to talk about, as it relied on a old, erroneous, but very pervasive, popular and rarely questioned hypothesis for how automatic endothermy (mammal and bird-style “warm-bloodedness”) evolved.
Back in November, a paper was published in the online journal: PLoS ONE. That paper was:
Using muscle force data for the hindlimbs of theropods, and applying it to a model based on Pontzer (2005, 2007), the authors were able to ascertain the approximate aerobic requirements needed for large bipedal theropods to move around. Their conclusion was that all but the smallest taxa had to have been automatic endotherms (i.e. warm-blooded).
Time to stop the ride and take a closer look at what is going on here.
In 2004, John Hutchinson – of the Royal Veterinary College, London UK – performed a mathematical study of bipedal running in extant taxa. He used inverse dynamics methods to estimate the amount of muscle that would be required for an animal to run bipedally. He then tested his models on extant animals (Basiliscus, Iguana, Alligator, Homo, Macropus, Eudromia, Gallus, Dromaius, Meleagris, and Struthio). The predictive capacity of his model proved to be remarkably substantial and stable (Hutchinson 2004a). A follow up paper in the same issue (Hutchinson 2004b) used this model to predict bipedal running ability in extinct taxa (Compsognathus, Coelophysis, Velociraptor, Dilophosaurus, Allosaurus, Tyrannosaurus and Dinornis). Results from this study echoed previous studies on the running ability of Tyrannosaurus rex (Hutchinson & Garcia 2002), as well as provided data on the speed and agility of other theropod taxa.
The difference between effective limb length and total limb length in the leg of Tyrannosaurus rex
Meanwhile in 2005, Herman Pontzer – of Washington University in St. Louis, Missouri – did a series of experiments to determine what was ultimately responsible for the cost of transport in animals. To put it another way: Pontzer was searching for the most expensive thing animals have to pay for in order to move around. One might intuitively assume that mass is the ultimate cost of transport. The bigger one gets, the more energy it requires to move a given unit of mass, a certain distance. However experiments on animals found the opposite to be the case. It actually turns out that being bigger makes one “cheaper” to move. So then what is going on here?
Pontzer tested a variety of options for what could be happening; from extra mass, to longer strides. In the end Pontzer found that the effective limb length of animals, was ultimately the limiting factor in their locomotion. Effective limb length differs from the entirety of the limb. Humans are unique in that our graviportal stance has us using almost our entire hindlimbs. Most animals, however, use a more crouched posture that shrinks the overall excursion distance of the hindlimb (or the forelimb). By taking this into account Pontzer was able to find the one trait that seemed to track the best with cost of transport in animals over a wide taxonomic range (essentially: arthropods – birds).
This latest study combines these two technique in order to ascertain the minimum (or approx minimum) oxygen requirements bipedal dinosaurs would need in order to walk, or run.
As with the previous papers, the biomechanical modeling and mathematics are elegant and robust. However, this paper is not without its flaws. For instance in the paper the authors mention:
We focused on bipedal species, because issues of weight distribution between fore and hindlimbs make biomechanical analysis of extinct quadrupeds more difficult and speculative.
Yet this did not stop the authors from applying their work on bipeds, to predicting the maximum oxygen consumption of quadrupedal iguanas and alligators. No justification is ever really given for why the authors chose to do this. Making things even more confusing, just a few sentences later, it is mentioned (ref #s removed to avoid confusion):
Additionally, predicting total muscle volumes solely from hindlimb data for the extant quadrupeds simply assumes that the fore and hindlimbs are acting with similar mechanical advantage, activating similar volumes of muscle to produce one Newton of GRF. This assumption is supported by force-plate studies in other quadrupeds (dogs and quadrupedal chimpanzees)
The force plate work cited is for quadrupedal mammals. However, mammals are not reptiles. As Nicholas Hotton III once mentioned (1994), what works for mammals, does not necessarily work for reptiles. This is especially so for locomotion.
In many reptiles (including the taxa used in this study) the fore and hindlimbs are subequal in length; with the hindlimbs being noticeably longer and larger. Most of the propulsive power in these reptiles comes from the hindlimbs (which have the advantage of having a large tail with which to lay their powerful leg retractor on). The result is that – unlike mammals – many reptiles are “rear wheel drive.”
The last problem is by far the largest, and ultimately proves fatal to the overall conclusions of the paper. The authors operated under the assumptions of the aerobic capacity model for the evolution of automatic endothermy.
It is here that we come to the crux of the problem, and the main subject of this post.
This blatant case of slander has raised the question of what one should do in this situation. It has also brought up the broader question of how scientists should handle the media. Should we just sit back, hoping that the interviewers will present the facts as best they can, and then deal with any possible blowback if/when that fails? Should scientists demand tighter editorial control over what is shown in videos like these? We are their scientific consultants after all. Theoretically they need us for legitimacy; which gives us a bargaining chip.
I don’t know what the right answer is. The least I can do is help Matt pass this info along so future researchers who are asked for an interview, can ask the production crew for assurances that they won’t be slandered in the final product.
