Wednesday, January 12, 2011

Birds, Hearing and Ears

Note: This is my 400th post. It’s just a number, but kind of a big number, and certainly far more posts than I ever intended this project to include. This post is around 3,800 words. If I guesstimate that the average post is ~3,000 words long, that’s ~1.2 million words*, which is roughly 10-15X the length of an average novel.

*Probably around half of which are tangents.

The other night I woke up with a start in the middle of the night* and had a heck of a time falling back to sleep. It was still early enough (2:30AM) that it wasn’t worth getting up, and so I tossed and turned for a while. As I did so I noticed that I’m always hearing things. Winter nights in our neighborhood are super-quiet- no birds, no crickets, windows shut tight, but it seems like I’m always hearing stuff: Awesome Wife’s breath, the click of the thermostat, the air moving through the heating vents, even my own pulse as my head lies sideways on the pillow. You can close your eyes, but you really can’t ever “close” your ears.

*Yes, like many middle-agers, I often awake at odd times. But this was different: it was “dream shock”. You know, when you’re so startled or alarmed or scared in a dream that you wake yourself up.

Oh, you want to know what the dream was? OK, I’ll tell, even though it’s kind of personal and embarrassing and borderline TMI, because that’s just the kind of blog this is. It was a Pee Dream. You know, one of those dreams where you have to pee real bad and you’re looking for a place to go, but can’t manage to find a bathroom? I dreamt I was waiting my turn to start in a race. The race was- I am not making this up- a Night Snowblade Race. Excell_snow_blades_skiboards Remember snowblades? They were like these super-short mini-skis that were briefly popular in the late 90’s, and you could ski downhill on them or skate along on the flats. (I tried a friend’s once- total blast.) Anyway, racers were heading out on these things, with headlamps, one after another at regular intervals, like some kind of night-time-trial. I looked up on this open, snow-covered hillside (the race was somewhere up around Kimball Junction), and saw little dots of headlamps moving downward on the descent. My turn was coming up, and I realized I had to pee, so I thought I’d just step a ways off in the bushes (it was dark, you know) and pee real quick. But I stepped away, and was still in view, so stepped a little further away, and then a little further, and all of a sudden I was standing along someone’s driveway. But the house was dark, and I thought, “I’ll just pee in their bushes real quick…” and I was just getting ready to go and then all of a sudden the garage door started opening and a car pulled into the driveway and someone was yelling at me and I was like all panicked and that’s when I woke up.

Visually-oriented as we are, we’re always hearing, but mostly half-consciously. We tend to think about our own hearing when we hear something significant- music, birdsong, waves crashing- but largely ignore it otherwise. But if you stop and listen, say right now- in your home, office, wherever- hearing is really remarkable. You’re constantly receiving all sorts of information- machines running, people passing, cars outside, planes overhead. We get all sorts of cool details about these things- presence, direction, speed, distance- all the time, without even looking, without focusing, without even having to turn our heads. We’ve all seen shows or read stories about psychics, telepaths, or people with special powers who can somehow sense or detect things that can’t be seen. But with hearing, all of us have a sense that’s far more real, more precise and more powerful than any Yuri Geller trick.

Over the course of this project I’ve kept bumping into hearing, but never really gave ears much thought. But the research I did for the All About Heights post got me curious about them, and then the Owl post got me wondering (again) about birds’ ears, and so I started reading and one thing lead to another, and, well it turns out that ears are not just way cool, but have an absolutely amazing story.

In a side note to the heights post I wondered about balance in birds, and whether the ear played a similar role in birds- specifically a vestibular sense- as it does in mammals. The short answer is yes, but the story behind it is a bit more complicated. But first, to tell the story, we have to know just a bit about the human ear.

All About Ears

You’ve probably heard that the ear has 3 major chunks: the Inner, Middle and Outer Ears. The outer ear is the only part you see, and consists of the pinna and the ear canal. The pinna is the part on the outside that your junior high school girlfriend/ boyfriend stuck their tongue inside when they gave you a Wet Willie*. The pinna is strictly a mammal thing; birds, reptiles and amphibians don’t have them.

Mammal Ear1 The role of the pinna is twofold: to amplify the sound delivered to the middle ear, and to provide information about the direction of sound. Many mammals of course have really big pinnae (in relation to their head/body size) which play an important role in detecting prey, predators or (in the case of bats) the physical world around them. Human pinnae are proportionally much, much smaller and for a long time it was assumed that they were vestigial, playing no real role in our modern-day hearing.

*Over the years, I’ve come to believe that there are 3 categories of human sexual foreplay. The first is things you used to do when you were in high school, and still do with your spouse/partner 20+ years later. The second is things you used to do when you were in high school, and now no longer do, but kinda-sorta-sometimes wish you still did. The third is things you used to do when you were in high school, no longer do now, and can’t for the life of you remember why you ever would have wanted to do such a thing. For me, Wet Willies are firmly in the third category.**

**Along with hickies.

But it turns out that our pinnae do help our hearing. Between 1.5KHz and 7KHz, the pinna and ear canal amplify sound by between 5 and 20dB. Above 6KHz, the pinna plays a significant role is helping to determine the direction of sound.

HearingRanges4 Extra Detail: As we saw in the bat post, human hearing ranges from about 20 Hz to 20 KHz. Human speech generally runs between 80 and 400 Hz. Middle C is 261 Hz. The highest note on a piano is a little over 4KHz, which is BTW roughly the same frequency as a chainsaw or fingernails on a chalkboard*.

*Unfortunately, I was unable to find out the frequency of a chainsaw slicing through a chalkboard. But man that’s gotta hurt.

Side Note: But there is a part of the human pinna that is vestigial, Dtubercule1and which appears in about 10% of humans, including- yes, that’s right- me!* It’s called Darwin’s tubercule, and is a slight thickening/protuberance of the rim of the pinna, about 2/3 of the way up (2 o’clock on the left ear, 10 o’clock on the right.) it corresponds to the point of pointy-eared mammals, and is believe to be a vestigial remnant of our presumably pointy-eared ancestry. Sometimes it’s more of a bump or protuberance pointed away from the ear canal, creating an almost Spock-like effect.

*I have it on the right ear only.

Birds also have an outer ear (pic left, not mine), ear_ghowhich also has an ear canal, but does not have a pinna. Instead birds have evolved special feathers, called auricular feathers, which protect the canal opening, as well as direct and amplify sound into it. Reptiles don’t really have an outer ear. In those with external ears (many reptile ears are internal-only) the tympanic membrane, which marks the beginning of the middle ear, is often visible on the side of the head.

Bird Ear1 At the opposite end of the ear-assemblage is the inner ear, set inside the skull, and constructed out of the hardest bone in the human body (diagram left, not mine). It has separate sections for hearing and balance. The hearing section is the vestibularsystem4cochlea, which consist of 3 fluid-filed chambers lined with specialized hair cells. The motion of this fluid is directed by vibrations received by the outer ear and transmitted to the cochlea via the middle ear- which we will get to momentarily- and detected by the hair cells, which then transmit this information, via the cochlear nerve, to the brain, where it is interpreted as noises.*

*Or perhaps images, if you are a bat.

The balance section is a fluid-filled chamber called the vestibule, which branches off into 3 semi-circular canals. The canals, which are also fluid-filled and lined with current-detecting hairs, are orthogonal to one another, so as to detect motion and position in 3 dimensions, which is transmitted to the brain via the vestibular nerve.

All amniotes* have this same basic inner ear structure, which we apparently inherited from a common amphibian ancestor. All amniotes use the inner ear not only for hearing but for balance. It’s suspected- but not agreed**- that the amphibian ear may have evolved out of a sense organ called the lateral line in fish, which consists of a line of pressure receptors- called neuromasts- than run along each side of the fish. The lateral line enables fish to detect small disturbances in the water, and is why large schools of fish are able to maneuver elegantly en masse in close quarters without bumping into each other.

*Amniotes = “Reptiles on up”, or reptiles, birds and mammals, but not amphibians. Technically they’re tetrapod vertebrates with land-adapted eggs. The egg can be external, or internal- like the amniotic sac of a mammalian fetus.

**An alternative hypothesis is that the neuromast and the inner ear evolved out of the same ancestral structure, which might-could-maybe have been some sort of statocyst-like thing. A statocyst is a balance organ found in some aquatic invertebrates, including various little plankton-y things and, our old friends, the echinoderms. It’s a little fluid-filled sac lined with sensing-hairs and with a little mineralized sand-grain inside called a statolith. Kind of like a teensy 1-flake snowglobe. Statocysts BTW are the reason that Brittlestars and Seastars (which I blogged about in this post)- which do not have brains- can tell when they’re upside-down (which they want to avoid, so as to deny predators an open shot at their soft juicy undersides…)

Extra Detail: Just because we all share the same basic inner ear structure doesn’t mean it’s stopped evolving. Our cochlea for example is coiled up like a little snail shell, very much unlike that of birds or reptiles. The coiling- which may be an adaptation to support longer sensing hairs- occurred sometime after our ancestors split from monotremes, but before we split from marsupials. Kangaroos have it, platypuses don’t. Another evolved feature is the presence of both tall hairs and short hairs inside the inner ear, something both mammals and birds- but not reptiles- came up with. In our ears the short hairs have “lost” their wiring, and don’t transmit information neurally. Instead they function by moving in response to current in the fluid, setting up motions that are in turn detected by the tall hairs. In birds short hairs perform a similar mechanical function, but also still transmit information neurally themselves as well.

OK, stick with me- we’re almost to the good part. The middle ear begins with a thin membrane- the ear drum- blocking the end of the ear canal. Vibrations received on this membrane are transmitted by a series of 3 connecting, successively smaller bones- the malleus, incus and stapes- through the air-filled chamber of the middle ear to the inner ear.

Mammal Ear2 These bones- together called ossicles- get successively smaller going from outermost (malleus) to innermost (stapes) such that the “footplate” of the stapes has a surface area only a small fraction that of the eardrum. The ossicles are arranged in a lever-like formation, the action of which serves to significantly concentrate and amplify the sound delivered to the inner ear.

The middle ear of a bird or a reptile is set up more or less the same way, with one glaring exception: their ears have but one ossicle- the stapes-equivalent- which is called the columella. Because of this difference, mammalian ears are capable of detecting much higher frequencies than bird or reptile ears. (Finally, something we do better than birds!)

Bird Ear2 So why don’t bird and reptile ears have 3 ossicles? Did they lose them or something? Actually they still have them, but they serve their original, reptilian function, that of lower jawbones.

Fish don’t have middle ears. The stapes/columella- in all amniotes- is a modified bone from a fish’s upper jaw. Fish have several bones in their lower jaws which in amniotes have fused together in different ways. In birds and reptiles, most of these bones have fused together into what is called the mandible. In mammals, some of the these same bones have been fused together into our modern lower jawbone, but 2 of them have moved back and shrunk until they were tiny little things set way back in our heads- the 2 additional ossicles (malleus and incus).

Extra Detail: In some reptiles the mandible is not completely fused, and the extra bones make possible a double-jointing of the lower jaw, as is the case with many snakes. (Snakes don’t actually “unhinge” their jaws; they just have a joint that we don’t.)

Side Note: There’s kind of a cool corollary here. When a bird opens its mouth, the hinge of its jaw is in a fundamentally different place in its skeleton- located where we would think of as the middle of our middle ear. What does it feel like when a bird opens its mouth? Does it feel like it feels to us when we open our mouths? Or does it feel more akin to popping our ears?

Now at this point, seeing as mammals evolved from some kind of ancient reptile, you may be wondering how the middle ear could have evolved from 1 to 3 ossicles. How could an intermediate, or transitional form possibly have functioned? The answer is that the middle ear evolved independently in mammals and reptiles. And birds. In fact the middle ear appears to have evolved independently at least 4 times among amniotes, following 4 different basic designs. It evolved once in mammals (or maybe proto-mammals or mammal-like reptiles/synapsids). It evolved separately in archosaurs (superset of dinosaurs) along a design that is present today in birds and crocodilians. It evolved another way in turtles and tuataras*, and a fourth way in lizards and snakes**.

*I didn’t know what they were either. Tuataras, Sphenodon sp., are a genus (2 species) of couple-foot-long lizards native to New Zealand that are, uh, not actually lizards. Meaning that if you or I saw one, we’d say “Hey, that’s a lizard”, but zoologists don’t consider them as such. Their teeth, heart, lungs, brain and mode of walking are all different. They’re sometimes called “living fossils”, as they are the sole survivors of a once-diverse order, and are thought to be anatomically more similar in some respects than other modern reptiles to early amniotes. They have ears, just not external ones.

**It’s actually a little more complicated than this. Turtles and tuataras share a design which probably evolved first, then after the ancestors of lizards and snakes branched off from tuataras, they evolved a significantly different middle ear. The turtle/tuatara middle ear architecture is sort of the stem-reptile default, a structure which they share, even though tuataras are believed to be more closely-related to lizards and snakes than they are to turtles. Got it?

So the middle ear evolved multiple times among amniotes. That’s cool, but it’s really not amazing. At this point in the project we’ve seen countless examples of parallel evolution, from eyes to CAM to C4 to wings to pale skin in humans. But there are 2 cool things about the parallel evolution of the middle ear: a little cool thing, and a Way Freaky Cool thing.

The Little Cool Thing

The little cool thing is the contrast between eyes and ears among amniotes. Think about it. We’ve talked a lot about eyes and vision, and the various differences between bird and mammal vision. But even with all of the remarkable differences between our eyes and bird eyes, the structure of our camera-style eyes is the same basic thing, working on the same principles, and it’s the same basic design we’ve all had since long before our lungfish-y ancestors first flopped up out of the water. But our middle (and outer) ears have evolved completely independently, with significant fundamental structural differences. Imagine if our amphibian ancestors had come up onto land with no eyes, and then the ancestors of birds and mammals evolved them completely independently along fundamentally different structures. Like if birds evolved camera-style eyes and we evolved compound bug-eyes or something. That’s more or less what did happen with the middle ear.

The Way Freaky Cool Thing

But the Way Freaky Cool thing is the timing of the evolution of the middle ear. Middle ears- all four versions- evolved during the Triassic, between 220 – 250 million years ago. That sounds like a huge range of time until you put it into context. Amniotes appeared at least 340 million years ago. Synapsids (mammal-like reptiles) branched off not much later (~324 million years ago) followed later by the archosaurs. And earlier, amphibians were present for maybe 10 or 20 million years before amniotes came about.

Middle Ear evo So in other words, 4-legged critters were running around on land for something like a hundred million years during which time everyone heard like crap. Then, “suddenly”, over just 30 million years, middle ears evolved independently multiple times amongst different groups of now-way-distantly-related critters. It’s like, for some reason, hearing well- and in particular hearing higher frequencies well- became really important. Why?

Tangent: My wild guess is that once one group of amniotes got decent hearing, it became a huge competitive advantage for both predators and prey. But what’s interesting- if that’s the case- is that that one group to evolve a decent middle ear first didn’t just replace all the other groups relatively promptly, but that the other groups managed to come up with the same gizmo in relatively short order. In any case, it’s weird to think that for like a 100 million years, there were all sorts of animals running around, and none of them ever heard leaves* rustling in the breeze**.

*Well, more like fronds I guess back then.

**Not counting bugs of various sorts, who have a whole different array of “ears” and natural history of hearing.

Just because they don’t hear as high as the highest-hearing mammals doesn’t mean birds don’t have great hearing. The asymmetric supersensitive ears of the Great-Horned Owl are just one example.

Side Note: Now’s a good time to return to a topic that’s bugged me for a while, and which I’ve touched upon a couple of times in previous posts: Why don’t birds rule the skies at night? Or in other words, why don’t they do the bat thing? Maybe it’s the high-frequency hearing limitations of their single-ossicle ear-architecture. There are echolocating birds, but their echolocating frequencies are significantly lower than those of bats. Oilbirds for instance echolocate at frequencies between 1 and 15KHz, swiftlets between 4.5 and 7.5KHz. Using such relatively low frequencies means longer wavelengths, and so neither can effectively echo-detect anything smaller than about 6 cm, which means that they can “see” walls and such, but not flying insects. No bird is known to be able to detect any frequency higher than 29 KHz. Bat-sonar ranges from 11 – 212KHz.

Of course hearing isn’t just in the ears. Just as our brains turn input from our optic nerves into images, they convert input from our cochlear nerve into sounds. And it appears that bird brains may process their input differently than ours do. Birds recognize sounds more quickly than we can. We need to hear a note for at least 1/20th of a second to recognize it. Birds can do so in just 1/200th of a second, which means they can hear multiple notes where we might hear just one.


Another cool thing about birds and hearing is that they seem to have something like perfect pitch. Perfect pitch is the ability to recognize a specific note at a specific frequency- for example you hear a note on a piano and say (with no other tonal context) Oh yeah, that’s middle C (261 Hz). Or to just sing middle C. Very few people can do this- maybe 1 in 10,000.

Extra Detail: It’s unclear whether there’s a genetic basis for perfect pitch. Early musical instruction and training appear to help. Native speakers of tonal languages, such as Chinese and Vietnamese, seem to be a bit likelier to have the ability.

But birds just seem to nail it, hitting the right note every time. They generate the right notes, and seem to recognize the right notes as well. How do we know that they recognize the right notes? Because they seem, conversely, to lack relative pitch.

Relative pitch is the ability to recognize the relative intervals between different tones, regardless of pitch. Syrinx Expand-O[9]Or in other words, a melody. For example, suppose I play Twinkle, Twinkle Little Star* on the piano, starting at middle C. Then let’s say I play it again, starting one octave lower. Or higher. Or maybe I just drop down 2 notes and start the tune at middle A. In all cases, you’ll recognize the tune as the same melody. But a bird won’t; it hears them as different tunes.

*Then again, my own relative pitch leaves something to be desired. I was over 40 before I realized that Twinkle Twinkle Little Star and the Alphabet (ABC…) Song were the same melody. I mentioned this last week to Awesome Wife, who pointed out that it was also the same melody as Bah-Bah Black Sheep…. which I never realized until right then.

Birds do some cool things with hearing. In many species, chicks communicate with their parents before they hatch. Some chicks, such as pelicans, actually complain if too hot or cold while still inside the egg, while others, like quail, chirp to synchronize their hatching. Birds’ ability to discern notes quickly helps them to recognize the calls of parents and chick, which is critical in species that nest in huge, noisy colonies, such as gannets.

So while bird ears and hearing are in many ways similar to ours, they’re also very different. I started this project with only a passing interest in birds, and only gradually became interested in various little things they seemed to do differently- and sometimes better- than we do. But over time I’ve learned that they do all kinds of things differently than we do, having evolved different solutions to so many of the same problems our own ancestors faced. Birds are like the “What if?” version of us, how we might have turned out in a parallel or alternate universe. Except that they did turn out that way, and they’re right here and now, all around us, outside every day. Birds are way cool.

Note about sources: Evolutionary info on the middle ears of amniotes came from Cochlear mechanisms from a phylogenetic viewpoint*, Geoffrey A. Manley, Your Inner Fish, Neil Shubin, the absolutely awesome blog Evolution of Hearing and the TalkOrigins Archive’s 29+ Evidences for Macroevolution. Info on bird, reptile and other ears came from Winged Wisdom/Pet Bird Magazine, the Earthlife Web website, Melissa Kaplan’s Herp Care Collection and Wikipedia.

*The “Middle Ear Evolution in Amniotes” Awesome Graphic in this post is a re-formatted (WTWWU-ized) version of Figure 1 of this paper.


KanyonKris said...

Congrats on post 400 - it's a good one.

I can't recall ever having a pee dream. Maybe I've just forgotten. What an anxiety-laden dream you had!

I never tried those ski blades and now I want to. Think I can find those at a thrift store or somewhere?

I'm kinda hung up on why the first branch of amniotes to develop hearing did cause one or more of the other branches to become extinct? Certainly hearing would be a huge survival advantage. Then again, perhaps the non-hearing branches did shrink in population but enough survived (in small numbers, in remote locations, etc.) until they evolved hearing. If nothing else, it's fun to think about.

KanyonKris said...

Oops, typo. Should read: "..why the first branch of amniotes to develop hearing DIDN'T cause one or more of the otehr branches to become extinct."

Anonymous said...

congrats on 400
you should write a book

sorry to hijack but must make mention of my favourite, smallest and coolest muscle in the body
"stapedius" - attaches to the stapes
it and tensor tympani (another muscle attaching to the ear drum) dampen vibration and protect the inner ear from loud noises - how cool is that

Anonymous said...

I hear ya on the ear

hey i still have a pair of short skate skiis. i took the binding off for some reason, but am going to put them back together and try to use them.

Watcher said...

Anon- how cool is that..."

Way cool.Reminds me of the specialized "muting" organ some bats have to keep from blowing out their own eardrums.

(And it's not "hijacking", it's adding. Thanks!)

Oilcan, KKris- The blades are still sold new online for ~$200, so I'm sure you can pick up a used pair for maybe <$100. I only used them once (at Solitude) but had a great time. Your turning radius is tiny, so things like moguls become a cinch (so long as you don't plow into them head-on; the tips catch easily). I found them easier w/out poles, and when you get stuck on the flats, skating is super-quick and easy.

KanyonKris said...

Oh, and for the record, I got up after reading this post and checked my ears. I have a bump on the left side only.

Anonymous said...

Why did everyone evolve middle ears in the Triassic?

One possibility is the arms race, absolutely.

Another is that something was going on with the air. Atmospheric composition, density and pressure has varied quite a bit over the Phanerozoic (basically the last 500 million years and change since the Cambrian Explosion). The details are still pretty hotly disputed, but atmospheric density has varied over a range of maybe 30%, while oxygen levels have varied by over 100%.

A third possibility -- which I don't consider too likely, but I throw in for completeness' sake -- is that good hearing needed X, and all these lineages developed X around the same time. My candidate for X would be "brain processing power". Of course, this just punts the question -- why did a whole bunch of amniote lineages need to develop better brains in the Triassic?

-- Apropos of sounds and arms races: there used to be a lot of cephalopods with internal shells. This was true until relatively recently. But today there are hardly any, and most are pretty vestigial (like the internal "pen" shell that some squids have).

Why? Well, in the middle of the Cenozoic -- IMS sometime in the Miocene -- at an otherwise undistinguished time horizon not associated with mass extinctions or climate change or anything -- whoosh, cephalopods across multiple lineages dramatically shrunk their internal shells or gave them up entirely.

And why did /that/ happen? Well, we may never know for sure -- but the disappearance of cephalopod shells comes right around the same time that we think, based on molecular evidence and a few fossils, cetaceans first started using sonar. An open-water cephalopod with a large, sturdy internal shell would give off an absolutely gorgeous sonar signal. So, the tentative theory is that early sonar-using cetaceans put tremendous selective pressure on the 'pods to reduce or get rid of their shells.

(I say tentative because, while it fits the known facts, the error bands on the development of cetacean sonar are still pretty wide. So we have to wait for more bones to be dug up.)

Anyway: by way of analogy, maybe the Triassic saw the rise of a clade of dangerous predators who were just /loud/.

Doug M.

Ski Bike Junkie said...

Good stuff, once again. I'm left wondering, though, how a cochlear implant works. Maybe I'll look it up and post as a follow-up comment.

Oh, and would it work in a bird or reptile? Hmm...

Watcher said...

Doug M.- The possible sonar/cephalopod is fascinating.Can you suggest a source for more info?

Interesting hypothesis re: atmo-density. And the oxygen thing reminds me of the whole why-didn't-the-world-burn-up-during-the-Carboniferous topic...

SBJ- A cochlear implant is an external mike/transmitter connected to a surgically-implanted receiver which converts the sound to electrical impulses, which are delivered to a bunch of electrodes inside the cochlea. Since birds and reptiles have cochleas, in theory it would work, so far as a cochlear implant can be said to really "work". (Tons of controversy around them...)

Unknown said...

Awesome! Sorry for an earlier comment, I did hear it first here!

Geoff Manley said...

I liked your summary of bird hearing very much. Well done! Over the past years, one aspect you mention (that because of the three ossicles, mammals can hear much higher frequencies than non-mammals) has had to be modified. The main reason for this lies in experiments on lizards and mammals that show that the function of the middle ear is dependent on the inner ear, which "reflects" its properties back to the middle ear. Thus the ossicles don't "restrict" the hearing range in the way we thought. It is likely that other mammalian developments had more influence on the hearing range. See my new review regarding this (Manley, G.A. (2012) Evolutionary paths to mammalian cochleae. JARO 13, 733-743. DOI 10.1007/s10162-012-0349-9). Oh, and btw, it isn't short and tall "hairs" that differ between mammals and non-mammals. There are two hair-cell (!) types in both birds and mammals and the differences here have nothing to do with the range of hearing.

Anonymous said...

I recently discovered that an owl's feathery ears do not enhance their hearing at all. Instead they've compensated by having necks so flexible as to allow the face to swivel right around, plus a left-right asymmetry in the ear, something unknown in any mammal.