Lunging is expensive, jaws can be noisy, and what's with the asymmetry? Rorquals part III

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Not only am I now unable to edit my blogroll (a very minor thing, but one that bugs me nonetheless), I am also incapable of understanding how ResearchBlogging is supposed to work. I registered, but cannot get my posts to appear there, so am going to give up. Oh well, it's not like it matters I suppose (hmm, or does it?). Am currently busy with the books, and am also (with co-authors) putting the finishing touches to some very neat papers... on which all will be revealed in due time. Anyway, to business, and to the last of those rorqual articles. Please see part I and part II first. The article was originally produced in 2006 and a few relevant studies have been produced since, hence inserts below...

In the previous post I discussed the basic anatomy and behaviour involved in lunge-feeding, a style of predation practiced by rorquals, the biggest, fastest and most dynamic of baleen-bearing cetaceans [feeding Fin whale, from the Right Whale Aerial Surveys site, shown here]. By engulfing literally tons of water within a unique, flexible buccal pouch, rorquals change from 'a cigar shape to the shape of an elongated, bloated tadpole' (Orton & Brodie 1987, p. 2898). Their feeding style is anything but passive: Paul Brodie, an expert on rorqual feeding, has described it as 'the largest biomechanical action in the animal kingdom'. After discussing rorquals with whale expert Nicholas Pyenson, my good friend Matt Wedel, in one of several blog posts on rorquals and other mysticetes (that's three separate links there), provided the most excellent quote...

The big baleen whales pick their targets and engulf them with their giant jaws and extensible mouth/throat region. They are often feeding on swarms of krill that measure kilometers in extent. Rather than think of big whales as filter feeders, we should think of them as predators that take bites off of superorganisms that are hundreds of times larger. The fact that the krill are strained out of the water by the baleen is a matter of processing - it comes after the whale has taken a bite.

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That's great: I'll be stealing it for use in lectures. The photo here features the gargantuan jaws of an Antarctic blue whale, kept at Washington D.C.'s Garber Facility (part of the National Museum of Natural History), and is borrowed from Nicholas Pyenson's fin whale page. The far smaller jaws of a sperm whale can be seen sitting inside the blue whale jaws. The two humans are both Jeremy Goldbogen [image below shows Jeremy Goldbogen with blue whale skeleton (from Goldbogen's site). Some of you might know that skeleton well].

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Recent studies show that lunge-feeding is not just dynamic, it is also extremely expensive in metabolic terms. Even though rorquals glide as they lunge (thereby conserving some energy), it still seems that lunge-feeding is so energetically costly that constraints are imposed on rorqual behaviour. Theoretically, large-bodied species store more oxygen thanks to their size, and therefore have a higher theoretical aerobic dive limit (TADL). Indeed in marine mammals as a whole there is a trend of increasing dive depth and duration with increasing body size. If we look at the largest rorquals - the blue and fin - we find TADLs of 31.2 and 28.6 minutes. Yet the actual aerobic dive limits of the two species are respectively 7.8 and 6.3 minutes (Croll et al. 2001). For comparison, right whales - which weigh about half as much as blue whales - spend about twice as long foraging under water as blue whales. To quote Acevedo-Gutiérrez et al. (2002) 'the largest predators on earth have the shortest dive durations relative to their TADL' (p. 1747). Note also that rorquals don't dive deep for their size: fin whales have been reported to dive down to 470 m, but that's not deep for such a big animal (total length 18-25 m), nor were the dives in question long in duration at less than 13 minutes.

Goldbogen et al. (2006) studied the kinematics of diving and lunge-feeding fin whales and showed that the rapid acceleration attained during lunge-feeding is immediately met by a relatively larger deceleration, presumably caused by the opening of the buccal pouch. The whales also rolled their bodies during lunging and may in fact spin about their long axis during feeding events, and at the bottom of a feeding dive a whale undertook a series of vertical excursions. It seems that the rapid acceleration and deceleration, and the dynamic movement, involved in lunge-feeding is highly costly, forcing rorquals to limit their dive time, and to increase the time that they need to spend at the surface recovering (Acevedo-Gutiérrez et al. 2002).

Some very interesting implications result from this expensive feeding style. Because lunge-feeding is so costly, it is likely only profitable where prey concentrations are high. Lunge-feeding rorquals cannot make a living wherever there is suitable prey, therefore, but are ecologically tied to productive regions such as submarine canyons and the Southern Boundary of the Antarctic Circumpolar Current. A blue whale has been estimated to require one metric ton of krill per day.

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When this is combined with the fact that some of the prey that rorquals depend upon, such as krill, are declining, it becomes clear why certain rorqual populations are struggling to recover from the days of commercial whaling. Indeed work on African hunting dogs Lycaon pictus has shown that high metabolic costs incurred during predation cause some species to be competitively inferior to others, forcing their populations to remain at low levels (Gorman et al. 1998). So lunge-feeding is a high-maintenance activity, and we should not be surprised that lunge-feeding rorquals that lunge-feed only on specific prey species are endangered, and liable to decline [UPDATE: since I wrote the above text, Goldbogen et al. (2007) have looked at the drag incurred during feeding lunges in fin whales. They showed that fin whales engulfed 60-82 cubic metres of water - a volume that exceeds that of the whale's entire body - and that drag, work against drag, and drag coefficients increased substantially during a lunge. Goldbogen et al. (2008) showed that lunging costs were similarly very high in humpacks. This work involves tagging humpacks (see adjacent journal cover) and seeing how heavily they breathe after lunge-feeding].

Here it's worth noting that different rorqual species specialize on different prey, though some (the minkes and the fin whale) seem to be opportunists. Sei whales specialize on crustaceans, in particular on copepods, and blue whales are specialist krill predators (Sigurjónsson 1995). Furthermore, not all rorqual species feed by lunging - the sei in particular uses a technique called skimming, whereby the whale keeps its mouth slightly open and moves forward through a body of prey at a continuous speed. It would be interesting to know how the morphology, kinematics and energetics of the sei compare to those of lunge-feeding rorquals, but so far as I know these issues remain largely unstudied. We do know that its baleen is particularly fine, allowing it to filter the comparatively small copepods [photo below, also from the Right Whale Aerial Surveys site, shows a feeding sei. It's feeding on its side. Hmm].

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Thanks to the work of August Pivorunas, Paul Brodie and colleagues, the engulfing mechanism of rorquals has been reasonably well understood since the 1970s. However, questions always remained. How is it that, during lunge feeding, agile, highly reactive prey remain within the mouth cavity prior to the mouth's closure? Man-made devices of similar size are incapable of retaining prey without them escaping prior to the devices' closure (Brodie 1978). When a rorqual carcass is processed at a whaling station, the soft tissue of the throat is removed by flensing. Using cables and straps, the jaws are then winched open, and the tendons and muscles holding the mandibles in place are then cut, freeing the jaw from the skull. Because the jaw is winched open without the very heavy throat tissue attached, its movement during the procedure approximates the natural movement of the jaw when the animal is alive and underwater. As the jaw is winched open 'a familiar sequence of sounds was observed to originate from the jaw apparatus ... a growl or rumble, a low hydraulic suction noise, following by a powerful knock, the latter seeming to emanate from the tip of the jaw' (Brodie 1993, p. 546). The noise reverberated throughout the jaw, making the entire structure vibrate. Unusual loud noises have been reported from live, feeding fin whales, so what Brodie reported apparently occurs in live whales, and not just dead ones.

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What might cause these noises? Could it be that the articular condyles of the jaw bones were grinding against the bones of the skull? Well, no, as large masses of collagen and lipid are sandwiched between the lower jaw and skull, and in the specimens Brodie examined there was no suggestion that this tissue had been compromised. Could it be that the jaw tips were grinding together? Again, no, as soft tissue separates the jaw tips and, anyway, the jaw tips were being forced apart when the noises were being made, not together. Brodie (1993) concluded that the noise was a consequence of the stretching apart of a synovial capsule located between the jaw tips. And, funnily enough, here we have something that is of direct relevance to all of us (well, most of us. Well, those of us who have heard our joints make crack noises).

As synovial capsules are forced apart, a partial vacuum forms in the joint cavity. Adjacent water vapour and blood gases from surrounding tissues rush to fill the vacuum, and as it collapses a noise results. Such noises range from low rumbles to loud knocks. This process is termed pseudocavitation (to distinguish it from cavitation: the process whereby the medium actually ruptures), and I've just realized that this solves one of the greatest mysteries in all of biomechanics: why our knuckles crack. I can't tell you how many times I've sat around with colleagues, pondering this very question.

If the lower jaws of fin whales really do make a loud bang or crack when they are opened to full gape, we can speculate that the whales might use this to help them retain prey within the mouth during engulfment. Captured prey would be startled away from the jaw edges by the noises, and this isn't unlikely given that we've long known that rorquals exploit the behavioural traits of their prey to concentrate them during predation (it is well known that humpbacks use bubbles to encircle prey, and in fact fin and Bryde's whales have been reported doing this too). To my knowledge, the 'noisy jaw' hypothesis has only been proposed for fin whales. Is it unique to this species, or practiced more widely?

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And speaking of fin whales.... generally speaking, tetrapods have symmetrical bodies and symmetrical arrangements of pigmentation. Why then are fin whales asymmetrical? Mostly dark on the left side of the head (this goes for the baleen and the left side of the tongue), they are mostly light on the right side (and, again, this goes for the baleen and tongue). While individuals belonging to various species sometimes exhibit asymmetrical pigmentation (and rorquals, such as minkes and sei whales, are among them), fin whales are consistently like this: all of them.

Does this serve a function? Mostly it has been thought that it is something to do with counter-shading: if the whale swims anti-clockwise around its prey it might be camouflaged against the water and hence be invisible, or is it that it swims clockwise around its prey, frightening them with its vivid whiteness and causing them to bunch up? Both ideas have been proposed (Ellis 1982). Most recently, cetologists seem to have favoured the idea that fin whales actually swim on their right side while lunge-feeding, thereby using a sort of rotated counter-shading. I've seen photos that apparently support this idea of right-sidedness, but I don't know if there any good studies on the subject. There is widespread evidence for handedness across Tetrapoda (including in whales), so does this mean that all fin whales are right-handed, or left-handed?

That's it on rorquals for now, though I plan at some stage to talk about the recently resurrected and recently discovered taxa, such as the Pygmy blue whale, Antarctic minke and Omura's whale. And what is it with the name Balaenoptera musculus? [minke whale below from wikipedia].

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One last thing. I can't go without relating the amazing tale of how I personally encountered Brodie's 1993 paper 'Noise generated by the jaw actions of feeding fin whales'. While collecting papers at Southampton University's Boldrewood Biomedical Science Library one day, I decided to find and photocopy this paper. All I knew was that it had been published in Canadian Journal of Zoology. I had no idea which volume it had been published in, nor in what year it had been published. The problem is that the Boldrewood library has a near-complete run of Canadian Journal of Zoology, with many metres of shelving being taken up by volume after volume after volume. In a futile effort to begin my search, I pulled out a single volume, at random, and opened it, at random. I had found the paper. Ha - and people tell me I'm not psychic! :)

Next: The Tet Zoo body farm! With pictures.

Refs - -

Acevedo-Gutiérrez, A., Croll, D. A. & Tershy, B. R. 2002. High feeding costs limit dive time in the largest whales. The Journal of Experimental Biology 205, 1747-1753.

Brodie, P. F. 1978. Alternative sampling device for aquatic organisms. Journal of the Fisheries Research Board of Canada 35, 901-902.

- . 1993. Noise generated by the jaw actions of feeding fin whales. Canadian Journal of Zoology 71, 2546-2550.

Croll, D. A., Acevedo-Gutiérrez, A., & Tershy, B. R. & Urbán-Ramírez, J. 2001. The diving behavior of blue and fin whales: is dive duration shorter than expected based on oxygen stores? Comparative Biochemistry and Physiology 129A, 797-809.

Ellis, R. 1982. The Book of Whales. Alfred Knopf, New York.

Goldbogen, J. A., Calambokidis, J., Croll, D., Harvey, J., Newton, K., Oleson, E., Schorr, G. & Shadwick, R. E. 2008. Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge. Journal of Experimental Biology 211, 3712-3719.

- ., Calambokidis, J., Shadwick, R. E., Oleson, E. M., McDonald, M. A. & Hildebrand, J. A. 2006. Kinematics of foraging dives and lunge-feeding in fin whales. The Journal of Experimental Biology 209, 1231-1244.

- ., Pyenson, N. D. & Shadwick, R. E. 2007. Big gulps require high drag for fin whale lunge-feeding. Marine Ecology Progress Series 349, 281-301.

Gorman, M. L., Mills, M. G., Raath, J. P. & Speakman, J. R. 1998. High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 391, 479-481.

Orton, L. S. & Brodie, P. F. 1987. Engulfing mechanisms of fin whales. Canadian Journal of Zoology 65, 2898-2907.

Sigurjónsson, J. 1995. On the life history and autecology of North Atlantic rorquals. In Blix, A. S., Walløe, L. & Ulltang, Ø. (eds) Whales, Seals, Fish and Man. Elsevier Science, pp. 425-441.

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fin whales have been reported to dive down to 470 m

Why do they dive that deep at all? Is there anything to eat down there?

By David MarjanoviÄ (not verified) on 04 Mar 2009 #permalink

Great article. But why krill didn't evolve not to spook about loud rumbles during these aeons they were eaten by whales?

Just a nasty biologist question...

Actually, I wonder if whale can simply stun or kill krill inside mouth with shock wave of powerful sound?

Having read somewhere that Sperm whales may use " a shock
wave of powerful sound" to stun squid, I wondered the
same thing...especially given the distance that whale
'song' can travel. Do baleen whales use any form of
echo location in hunting?

By Craig York (not verified) on 04 Mar 2009 #permalink

Do baleen whales use any form of echo location in hunting?

No, they completely lack the equipment for it. Echolocation is, among whales, a unique feature of toothed whales.

By David MarjanoviÄ (not verified) on 04 Mar 2009 #permalink

The clicking jaw is news to me, interesting stuff. Like others have said its reminisant of the sperm wahles using sound to stun squid.
Talking of whales feeding, theres footage of Btyde's whales feeding in tonights 'natures great events', for those in the UK.
ANd on the subject of the books, you happen to need any photos of common frogs do you? Because I somehow managed to take 900+ photos of my local breeding 'colony' :O :D

The issue about the origin of the sounds which occur at the opening of the fin whale´s mouth remind me on a similar issure about the strange noise some people produce when they move their mandibles. I think the current idea is that pathological processes can cause a dis-orientation of the Discus articularis in front of the Caput mandibulae instead of being on the top. During the movement of the mandible the Discus articularis gets compressed against the Processus articularis and finally slips in a new position over the Caput mandibulae what is thought to cause this noise. It is hard to explain how this actually works without having any illustrations.

Like Craig mentioned, there is evidence that various odontocetes stun their prey with sounds they produce, although I'll admit I haven't read much up on the subject.

If you ascribe to Jurassic Fight Club, sperm whales can use their echolocation superpowers to liquify the internal organs of the giant shark C. megalodon!

On a serious note, if I remember correctly, the stunning noises are likely high frequency; odontocetes are adapted for producing higher frequency noises, and mysticetes are adapted for hearing (and apparently producing) low frequency sounds.

Great post!

Sordes: I can demonstrate this jaw noise any time you like. It began after landing on my chin one time too many.

By Nathan Myers (not verified) on 04 Mar 2009 #permalink

The "skimming" you describe sei whales as doing is something like the normal feeding strategy of balaenids (right whales). The balaenid mouth has assorted special features to make this possible/efficient. (I've seen an article on right whale mouth hydrodynamics within the last few years: maybe in JEB? And don't remember anything. But the rear margin of the lower lip in right whales is low: I think this is to provide an outflow channel at the "corners" of the mouth, so they don't have to close the mouth and contrack the throat to expel water the way balaenopterids do.)
So: is there any story out about morphological differences between mouth regions of Sei and other rorquals that would correlate with the difference in preferred feeding strategy?

By Allen Hazen (not verified) on 04 Mar 2009 #permalink

contrack

Contract. :-)

By David MarjanoviÄ (not verified) on 05 Mar 2009 #permalink

The countershading theory makes a lot of sense. I seem to remember something about fish hunting killer whales seeming to flash their white bellies to schools of fish to help in corraling them while other members of the pod feed.

Does anyone know what the field of vision is for a whale of that size though? I would assume that binocular vision is out of the question with a head that size.

DN: "Not only am I now unable to edit my blogroll (a very minor thing, but one that bugs me nonetheless..."

FOR goodness sakes Darren, do the scientific thing and apply for a grant and establish an R&D center to fix it. Yes, I AM serious, mostly.

I know that baleen whales lack the equipment for echolocation, but here are a few questions for ya:

1) Odontocetes and Mysticetes are sister groups, was echolocation present in their common ancestor, and simply lost in myticetes?

2) Is the sperm whale more closely related to dolphins than baleen whales, or did dolphins split off the main whale lineage prior to the appearance of sperm whales/mysticetes? Or are dolphins odontocetes?

3) Are porpoises taxonomically distinct from dolphins, or is "porpoise" a common term with no scientific basis?

Zach:

2) Dolphins are odontocetes. The odontocetes include the dolphins, porpoises, river dolphins, sperm whales and dwarf sperm whales, beaked whales, narwhal and beluga.

3) Porpoises are a distinct group, the Phocoenidae. I've heard of dolphins being referred to as porpoises, but porpoises are a completely different family of small cetaceans.

Thanks, Hai. The odontocetes form a huuuuuge group! Does the sperm whale have any close living or fossil relatives? It seems to be the odd one out.

Zach, good questions -

1) The currently held idea is that echolocation arose only once, and within monophyletic odontoceti.

2) There was a hypothesis during the early 1990's that (based on a molecular study with very, very limited taxon sampling) placed mysticetes and sperm whales as sister taxa, and the rest of toothed whales in a paraphyletic odontoceti. This was by Michel Milinkovitch. More recent molecular and morphological studies with more extensive taxonomic sampling have disproved this phylogeny.

All modern cetaceans with adult teeth are odontocetes.

3) As Hai-Ren states, porpoise are phocoenids, a small group of toothed whales. They have a number of synapomorphies (which I won't list), and a gradually expanding Mio-Pliocene Pacific fossil record. Their fossil record suggests they were far more diverse than they are today, and stranger, for that matter (i.e. the 'skimmer porpoise' from the San Diego Formation).

Milinkovitch, M. C., G. OrtÃ, and A. Meyer. 1993. Revised phylogeny of whales suggested by mitochondrial ribosomal DNA sequences. Nature 361:346-348.

>If you ascribe to Jurassic Fight Club, sperm whales can >use their echolocation superpowers to liquify the internal >organs of the giant shark C. megalodon!

They actually put that in the show? Wow...
...if they could do that, wouldn't they have to worry about accidentally liquifying each other's internal organs? C. megalodon wasn't *that* much smaller, and sharks are pretty sturdily built... who okayed that one?

By William Miller (not verified) on 05 Mar 2009 #permalink

I recently came across your blog and have been reading along. I thought I would leave my first comment. I don't know what to say except that I have enjoyed reading. Nice blog. I will keep visiting this blog very often.

Alessandra

[thanks for your comment; I have taken the liberty of removing the urls as they looked like spam]

By Alessandra (not verified) on 05 Mar 2009 #permalink

Echolocation clearly appears to be an odontocete-only thing; the predatory mysticetes like Janjucetus had big eyes instead.

By David MarjanoviÄ (not verified) on 05 Mar 2009 #permalink

> Does the sperm whale have any close living or fossil
> relatives? It seems to be the odd one out.

Zach,

the pygmy sperm whale (*Kogia breviceps*)and the dwarf sperm whale (*Kogia simia*) are the closest living relatives of the sperm whale, dolphin-sized animals with fierce teeth and skin folds behind the head that form a 'false gill' and gives them a somewhat shark-like appearance.

The fossil relatives of the sperm whale are much more spectacular and include the Miocene 'killer sperm whales' *Brygmophyseter* and *Zygophyseter*, animals that were somewhat similar to extant orcas in size and ecology.

As several other commentors have already mentioned, *Brygmophyseter* was featured in an episode of Jurassic Fight Club, beating the crap out of *Megalodon*.

And, in case you've forgotten (which I'm sure you haven't), sperm whales small and large have previously been featured on Tet Zoo here (kogiids), here (Scaphokogia), here (stem-group macropredatory sperm whales) and here (Acrophyseter)! Tsk tsk Zach, you are not doing your homework :)

I still have to cover Physeter at some stage though.

Fascinating!

While I understand the logic of the asymmetrical shading for "camouflage/prey herding:anti-clockwise/clockwise" hypothesis, I'm confused as to what the implications of swimming on their right side are... Could someone reword or expound on this?

Cheers!

So, about new species of whales. I have a question after the reading of B. Zenkovich's "Around the world for whales". He mentions among described and well-known right whales the undescribed variety from Sea of Okhotsk and says possible it may be a separate species. There is also a photo:
http://www.sivatherium.h12.ru/library/Zenkovic/gl_14.htm
(chapter is about sei whale, photos at the end of the chapter show from the top: blue whale on the deck of "Aleut" whaling ship, North Atlantic right whale and the undescribed whale from Sea of Okhotsk, but the last photo is too uninformative).
There is a name "poggy" (sorry, I don't know the original script of this name). What can you say about this whale? Is it a new species or only local variety?

By Pavel Volkov (not verified) on 06 Mar 2009 #permalink

I found this in Lyall Watson's 1981 Sea Guide to Whales of the World, on Balaena mysticetus (the bowhead):

Alaskan Eskimos... recognise 2 forms, kairalik and the smaller ingotok ('poggy' to nineteenth-century American whalers) but ingotok is probably an immature animal.

It's not young bowhead - Zenkovich mentions it is about 18 m long (bowhead - about 20 m long), but its baleen plates are only 2 m long as at Eubalaena glacialis (at bowhead up to 5 m long).

By Pavel Volkov (not verified) on 07 Mar 2009 #permalink

Darren, great info filling a gaping void ( :-D ) in my knowledge of whales... and I look forward to the future Physeter feast foretold (have you read Moby Dick? strange book...)

I readily believe your statistically-implausible finding of that paper, having experienced a similar thing myself. Ok, slightly similar.

I was out on my bike a few years ago and to meet a practical need mid-journey was consciously seeking precisely 6 carrier bags... and I found 6 pristine carrier bags (ok tied up neatly in a further bag, which I count as a bonus)... all poised just inside the top of a pristine-binliner-lined (but otherwise totally-empty) wheelie bin... the first (and so of course only!) bin I looked in... a bin I had no prior knowledge of. It just seemed the place to go, open and look in.
(How often do you encounter a bin, clean, lined, with nothing in it except the very thing you want?)

It seemed to me afterward that I had experienced an unusually calm and open frame of mind, expectant/accepting/thankful, as I sought those bags, not questioning that I would find what I sought... just wondering how/where it would occur.

And there they were, 'as requested' so to speak. Like your paper.

That experience made me feel very well looked-after!

By Graham King (not verified) on 07 Mar 2009 #permalink

And some more about "poggy". Zenkovich mentions this whale is (was?) especially numerous near Shantara Islands (south of Sea of Okhotsk, near the north of Sakhalin Island). Does bowhead migrate so far to the south?
The description in Zenkovich's book is not detailed, the description of the appearance of "poggy" is absent.

By Pavel Volkov (not verified) on 08 Mar 2009 #permalink

Wasn't the specific epithet of musculus, or mouse-like, intended to be a bit of a joke on Linnaeus's part?

It's been inferred to have possibly been a joke on Linnaeus' part - Linnaeus never personally explained his reasons for his name choices (after all, his readers already knew Latin).

Carl Zimmer wrote about the most recent paper from Goldbogen:

Goldbogen J. A., Potvin, J and Shadwick, R. E. 2009 Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales. Proceedings of the Royal Society B ( doi: 10.1098/rspb.2009.1680 )

(Which is open-access, as it turns out.)

(In a bit of science blog cross-fertilization, I left a comment on Zimmer's blog linking back to here.)

By Owlmirror (not verified) on 11 Dec 2009 #permalink