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

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. By engulfing literally tons of water within a unique, flexible buccal pouch, rorquals change shape 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.

That’s great: I’ll be stealing it for use in lectures. The photo at top features the immense 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 here on Matt's blog site.

Recent studies show that lunge-feeding is not just dynamic, it is also extremely expensive in metabolic terms, and 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 [adjacent photo, from the Right Whale Aerial Surveys site, shows a feeding Fin whale].

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 anywhere 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.

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.

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 [adjacent photo, also from the Right Whale Aerial Surveys site, shows a feeding sei. It’s feeding on its side. Hmm].

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.

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?

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 the right side of the tongue). While individuals belonging to various species will 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 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?

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 what 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! :)

For the latest news on Tetrapod Zoology do go here.

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-Gutierrez, 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., 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.

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.

From cigar to elongated, bloated tadpole: rorquals part II

More on rorquals (for part I go here), this time looking at the basics of their morphology and feeding behaviour. The rostrum in rorquals is long and tapers to a point (though it is comparatively broad in blue whales) and, in contrast to other mysticetes, a stout finger-like extension of the maxillary bone extends posteriorly, overlapping the nasals and abutting the supraoccipital (the shield-like plate that forms the rear margin of the skull). The dorsal surfaces of the frontals (on the top of the skull) possess large depressions while the ventral surfaces of the zygomatic processes (the structures that project laterally from the cheek regions) are strongly concave, again unlike the condition in other mysticetes.

Rorqual lower jaws are immense, beam-like bones that bow outwards along their length. The symphyseal area (the region where the jaw tips meet) is unfused, as is the case in all mysticetes (even the most basal ones) but not other cetaceans, meaning that the two halves of the jaw can stretch apart at their tips somewhat. Exceeding 7 m in blue whales, rorqual lower jaws are the largest single bones in history (ha! Take that Sauropoda).

A section of blue whale jaw was once ‘discovered’ at Loch Ness and misidentified as the femur of an immense, hitherto undiscovered tetrapod. Occasionally rorqual skulls have been discovered in which the long lower jaws have been stuck wedged inside various of the skull openings and with their tips protruding like tusks. People unfamiliar with cetacean skulls have then naively assumed that the skull belonged to some sort of tusked prehistoric sea monster. Ben Roesch discussed cases of this (go here), and also noted the case of the Ataka carcass of 1956: a giant beached animal possessing divergent ‘tusks’ that are in fact the separated halves of a rorqual’s lower jaw (see adjacent image).

I’ve come across another case of this sort of thing. The accompanying newspaper piece, from The Telegraph of June 29th 1908, features a skull trawled up by the Aberdeen vessel Balmedie (sailing out of Grimsby), and thought by the article’s writer to be that of ‘some prehistoric monster’, apparently with tongue preserved. It’s clearly a rorqual skull, and the pointed, narrow rostrum and posterior widening of the mesorostral gutter indicates that it’s a minke whale skull.

Moving back to the morphology of the rorqual lower jaw, a tall, well-developed coronoid process – way larger than that of any other mysticete – projects from each jaw bone and forms the attachment site for a tendinous part of the temporalis muscle, termed the frontomandibular stay.

All of these unusual features are linked to the remarkable feeding style used by rorquals. How do they feed? Predominantly by lunge-feeding (also known as engulfment feeding): by opening their mouths to full gape (c. 45º), and then lunging into a mass of prey. Those depressed areas on the frontals and zygomatic processes have apparently evolved to allow particularly large temporalis and masseter muscles, the muscles involved in closing the jaw. The frontomandibular stay provides a strong mechanical linkage between the lower jaw and skull and seems primarily to amplify the mechanical advantage of the temporalis muscles.

As a rorqual lunge-feeds, an immense quantity of water (hopefully containing prey) is engulfed within the buccal pouch, transforming the whale from ‘a cigar shape to the shape of an elongated, bloated tadpole’ (Orton & Brodie 1987, p. 2898). While a rorqual uses its muscles to open its jaws, the energy that powers the expansion of the buccal pouch is essentially provided by the whale’s forward motion, and not by the jaw muscles. In other words, the engulfing process is powered solely by the speed of swimming. Orton & Brodie (1987) noted that the engulfed water ‘is not displaced forward or moved backward by internal suction, but is simply enveloped with highly compliant material’ (p. 2905). Rorquals do not, therefore, set up a bow wave as they engulf.

A rorqual may engulf nearly 70% of its total body weight in water and prey during this action, which in an adult blue whale amounts to about 70 tons (Pivorunas 1979). In order to cope with this, the tissues of the buccal pouch must be highly extensible and able to cope with massive distortion. The ventral surface of the pouch is covered by grooved blubber, on which the 50-90 grooves extend from the jaw tips to as far posteriorly as the umbilicus. The ventral grooves can be extended to 4 times their resting width, and to 1.5 times their resting length. Internal to the grooved blubber is the muscle tissue of the buccal pouch, and this is unique, containing large amounts of elastin, and consisting of an inner layer of longitudinally arranged muscle bands and an outer layer where the bands are obliquely oriented (Pivorunas 1977).

When a rorqual lunges, delicate timing is needed, otherwise the buccal pouch will rapidly fill with seawater and not with prey. How then do rorquals get their timing just right? It seems that rorquals possess batteries of sensory organs within and around the buccal pouch: there are laminated corpuscles closely associated with the ventral grooves that might serve a sensory function, and located around the edges of the jaws, and at their tips, are a number of short (12.5 mm) vibrissae. Long assumed to be vestiges from the time when whale ancestors had body hair, it now seems that these structures have a role in sensing vibrations.

Once a mass of prey is engulfed, a rorqual then has to squeeze the water out through its baleen plates while at the same time retaining the prey. Rorqual baleen plates number between 219 to 475 in each side of the jaw (the number of plates is highly variable within species, with sei whales alone having between 219 to 402), and each plate ranges in length from 20 cm (in the minkes) to 1 m (in the blue). As the whale stops lunging forward, the pressure drops off, allowing deflation of the buccal pouch. Passive contraction of the blubber grooves and active contraction of the muscle layer within the buccal pouch also occurs at this time.

For an outstanding sequence of photos illustrating engulfment in action, see Randy Morse’s photos of a feeding blue whale here.

So that’s the basics. But there’s so much more to the subject than this. How is it that, during lunge feeding, agile, highly reactive prey remain within the mouth cavity prior to the mouth’s closure? Why do some rorquals make loud noises during lunge-feeding? Why, given their immense size and theoretical high aerobic dive limit, do big rorquals not spend more time lunge-feeding beneath the surface? Why do some rorquals exhibit strongly asymmetrical patterns of pigmentation? And don’t forget that not all rorquals lunge-feed. More on these issues in the following post.

The painting at top is from Valter Fogato's site.

For the latest news on Tetrapod Zoology do go here.

Refs - -

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

Pivorunas, A. 1977. The fibrocartilage skeleton and related structures of the ventral pouch of balaenopterid whales. Journal of Morphology 151, 299-314.

- . 1979. The feeding mechanisms of baleen whales. American Scientist 67, 432-440.

A 6 ton model, and a baby that puts on 90 kg a day: rorquals part I

I’ve said it before but it’s worth saying again: everyone interested in animals is, I assume, fascinated by whales. All secondarily aquatic tetrapods are neat, but here we have a group that has evolved giant size, suspension feeding, macropredation, deep-diving and echolocation, among other things. Right now, I have rorquals on my mind, and I’m not quite sure why: I haven’t been doing any research on them lately, nor have they been in the news or anything*. However, later this week my family and I are visiting the Natural History Museum (London) and I’m particularly looking forward to showing Will (who’s 5) the life-sized Blue whale Balaenoptera musculus model that hangs in the Mammal Hall (the room formerly known as the Whale Hall). I’m so interested in this model that I feel it worthy of a short digression.

* Bar the news that Iceland is resuming low-level whaling. Yay Iceland.

Late in the 1920s plans to replace the old whale hall of the British Museum (Natural History) were fulfilled. The new, steel-girdled hall finally allowed the 1934 display of the Blue whale skeleton [image above, from here] that had been kept in storage for 42 years due to lack of space. Measuring 25 m in length, the animal had stranded at Wexford Bay, SE Ireland, in 1891. It – as in, the skeleton alone – weighs over 10 tons. But some people at the museum wanted more, and in 1937 taxidermist Percy Stammwitz (1881-1954) made the bold suggestion that a life-sized model of a Blue whale could be constructed within the Whale Hall itself. Later that year Stammwitz and his son, Stuart, began work on the project, their technical advisor being cetologist Francis C. Fraser (1903-1978).

Scaling up from a clay model, a wooden frame was constructed, and this was then covered in wire mesh and plaster. A trapdoor on the stomach was constructed for (I presume) internal maintenance, though apparently the workmen would sneak inside the model for secret smoking. On several occasions I’ve heard rumours that a time capsule was left inside this trapdoor before it was sealed: Stearn (1981) made no mention of this specifically, but did write that a telephone directory and some coins were left inside (p. 132). The completed model weighed between 6 and 7 tons and, when the time came for the whale to be painted, Stammwitz and Fraser disagreed, eventually choosing bluish steel-grey. Completed in December 1938, it was the largest whale model ever constructed though larger models, constructed from the same design templates, have since been produced by several American museums [adjacent image from here].

What are rorquals? They are the eight or so Balaenoptera species of the mysticete family Balaenopteridae*, all of which open their jaws wide to engulf masses of prey and possess a highly distensible throat pouch and extensible longitudinal grooves on the throat and belly. They occur in seas worldwide and range from 6 to 30 m in length. The only other living balaenopterid** is the Humpback Megaptera novaeangliae, and it is generally regarded as the sister-taxon to the rorquals. I’ve seen two explanations for the term rorqual. The commonest is that it derives from the Norwegian rørhval and means ‘grooved whale’ – a reference to those longitudinal grooves. The less common explanation is that it originated from the French for ‘red throat’, this supposedly being a reference to the reddish colour visible between the throat grooves when the whale’s buccal pouch is extended (Berta & Sumich 1990).

* Most books on whales state that there are five rorqual species. As with so many tetrapod groups, the number of recognised species has increased in recent years, both as ‘old’ species have been resurrected from synonymy (Antarctic minke B. bonaerensis and Pygmy bryde’s B. edeni), and as new species have been described (Omura’s whale B. omurai).

** Some workers have included the Grey whale Eschrichtius robustus within Balaenopteridae. It is mostly agreed, however, that Eschrichtius belongs to a small clade (Eschrichtiidae) best regarded as the sister-taxon to Balaenopteridae.

Rorquals grow fast, reaching sexual maturity at between 5 and 12 years of age in the larger species. They can produce up to 1.5 calves per 2-year period, though three years between calves is probably more normal. Pregnant females increase their weight by 26% and, thanks to lipids stored in their visceral fat and blubber, increase their total energy budget by a staggering 80% (Víkingsson 1995). After a pregnancy of 10-13 months, babies are suckled for 4-10 months and (in blue whales) are provided with 200 litres of milk a day. Unsurprisingly, babies increase their weight substantially during this time, with a 2-3 ton newborn blue whale putting on 90 kg a day, and reaching 20 tons by the time it is weaned. They are the fastest growing baby mammals. Rorquals are long-lived, with minkes B. acutorostrata reaching their forth or fifth decades, Sei B. borealis surviving to 65 or so, and Fins B. physalus to 85 or 90, or possibly 100. Incidentally, right whales (balaenids) are thought to survive into their second century, but they’re not rorquals.

We all know that rorquals are big, that they possess baleen, and that they feed by engulfing crustaceans, small fish and other prey. They spend summer in the polar regions, where they feed and put on weight, and then they migrate in the winter to the tropics, where they breed and give birth to their enormous calves… but they don’t _all_ do this, with some populations of some species being non-migratory. Of course, there’s more, a lot more, and in the next few posts I’d like to introduce a few details that you might not have encountered before… unless, that is, you’re a cetologist, or a close friend of one.

Thanks – mostly – to aerial photography, most of us are now familiar with the true body shape of live rorquals. They are shockingly gracile and incredibly long-bodied, with a shape that (when seen in dorsal view) has been likened to that of a champagne flute. While people had known this for a while (Roy Chapman Andrews wrote in 1916 of the Fin whale’s ‘slender body … built like a racing yacht’, for example), what may or may not be surprising is that only recently have people in general come to realize that rorquals are shaped like this. Basing their reconstructions on beached carcasses, or on rorquals killed by whaling vessels, artists and scientists had previously thought that rorquals were stouter, with fat bellies and flabby throats. Rorquals were still being depicted this way as recently as the 1960s, as in (for example) the excellent paintings and drawings of Sir Peter Scott [see above, borrowed from the Wildlife in Danger Brooke Bonds card set].

By photographing live sei and minke whales, underwater, from close range, Gordon Williamson (1972) argued that the traditional ‘baggy-throat’ reconstructions failed to show the true body shape of the animals. His drawings, reconstructed from his photos (which invariably failed to capture the entire animal in the frame), were dead accurate and among the first to depict rorquals in this way. Williamson’s whales were all captured, by harpoon, from a commercial whaling vessel. No explosive was placed in the harpoon head (normally, the harpoon head explodes within the body of the whale), so a harpooned whale was not killed immediately and was simply tethered to the ship. As it swam around, gradually tiring, Williamson approached it in the water and took his photos [the accompanying image, showing a young rorqual that beached in Florida in 2002, is borrowed from VisitGulf.com].

More on rorquals in the next post, this time focusing on the biomechanics of feeding: From cigar to elongated, bloated tadpole: rorquals part II. For the latest news on Tetrapod Zoology do go here.

Refs - -

Berta, A. & Sumich, J. L. 1999. Marine Mammals: Evolutionary Biology. Academic Press, San Diego.

Stearn, W. T. 1981. The Natural History Museum at South Kensington. Heinemann, London.

Víkingsson, G. A. 1995. Body condition of fin whales during summer off Iceland. In Blix, A. S., Walløe, L. & Ulltang, Ø. (eds) Whales, Seals, Fish and Man. Elsevier Science, pp. 361-369.

Williamson, G. R. 1972. The true body shape of rorqual whales. Journal of Zoology 167, 277-286.