The Function of the Oesophagus in the Bittern's

196 TheOesophagus ofthe Bittern. [Auk[April

THE FUNCTION OF THE. OESOPHAGUS IN THE BITTERN'S BOOMING.

rY •,•ES r. C•Am•.

Plate VI

ON May 4 1921 the American Museum receivedfrom West .arousedNyack, N.Y., our interest,an adult because male Americanof the unusualBittern which thickeningimmediatelb, of the skin of its neck. This exhibited a flabby, oedematouscondition like that commonlymet with in the "brood-spot"on the breast of an incubatingbird. The loosenessand great width of this skin, thanks to the sparsenessof the feathers on the back of the neck,are well shownin P1. I, Fig. 2, from a photographof the dead bird. I was • at once reminded of the condition I had observed in the male of an African Rail, Sarothruraelegans, which seemed beyond a doubt to inflate its oesophaguswith air to use it as a resonatingorgan for its remarkable voice. Thus we sought to inflate the neck of the Bittern, blowing through a glasstube. By insertingthis in the glottis it was a simplematter to expandthe air-sacsof the body, especiallythe .abdominalones, but also a pair just behind and below the wings, and the "cervical" sacs between the clavicles. Yet there was clearly no connectionhere with any air-sac in the neck proper, and indeed the Hornbills are almost the only birds kno•aa to possesssuch a connectionin the pneumatic system. A number of other birds, however,the best type of which is the Marabou Stork (Leptoptilos),do have so-called"cervico-cephalic" sacs that extend down the neck from the head, and receive air from the nares, whenceit passesthrough the spacebeneath the eye-ball. Our Bittern was tested for such sacs in the neck by blowing stronglyinto the internalnares. A slightbulging of the sub-ocular regionresulted, but this did not extend to any air-cavity in the neck;nor couldwe obtain any better result by blowingdirectly into the air-spaceunder the eyethrough a largehypodermic needle. Cervico-cephalicair-sacs were entirely wanting. This left only oneorgan in the neckthat might be filledwith air: the oesophagusitself. Blowing straight into the gullet it was ,easy to distend the neck throughoutits whole length, until it TIlE AUK, VoL. XXX[X. PL>,?•: VI.

Fig. 1. Adult maleAmerican Bittern in breedingseason when oesophagus is blowm up with air; gl. indicatesthe positionof .the glottis at this time: p/. marksthe point wherethe white plumesare insertedin the skin. Inasmuchas the air-sacsof the body are alsoexpanded, it will be evident that none of them is concernedwith elevating the white feathers, here scarcelyvisible. Fig. 2. Bittern in the breedingseason, to showthe width of the neck herecomvletely deflated. (Photossupplied by the AmericanMuseum of Natural History). Vol.1922XXXIX] J CHArXN,The Oesophagus ofthe Bittern. 197

measured 10 centimeters in diameter; and when the bill was held closed,this air escapedonly very slowly, even though no effort was made to closethe nostrils. To make the photographshown in P1.VI, Fig. 1, it wasnecessary to placea smallrubber band round the bill, and a small piece of damp cotton in the mouth. The glottis seemedunusually free from the hyoid arch or base of the tongue,and lay relativelyfar back in the throat. XYhenthe neck was moderatelydistended with air, the glottis was situatedsix centimetersbehind the posteriorangle of the gape, while the tip of the long slendertongue still reachedjust to the angle of the gonys, quite well out in the beak. One unusual feature of this Bittern?s mouth still remains to be mentioned.' When the tonguecame up it passedbetween or below two curiouselongated pads placed on the inside of the mandibularranhi, and nearly touchingin the center. These we had' never noticed before in any member of the Heron family, and it may well be that they have somethingto do with keeping the air in the gullet, especiallysince their inte•mal structure re- semblesthat of the thickened skin of the neck, and they are apparently only enlargedtemporarily. When the bill is closed these padslie well in h•nt of the internal na•s as may be seenin l½igure2, so they cannot serve to block the nostrils,but rather to closethe mouth itself more tightly. Supposingthen that the Bittern doesswell its oesophaguswith air, how does this proceed? It might conceivablyswallow one gulp of air through the action of the tongue and hyoids,but I do not think it could engulf a secondmouthful while still retaining the first. As for suckingair into the lower oesophagus,there is no adequatemechanism available. Far more likely I should considerit, that the air is forcedinto the oesophagusthrough the trachea,by closingthe beak and driving the breath from the air- sacsof the body. The distanceto which the glottis can be re- tracted into the throat renders this more probable. Thus far my statementsmay seemhighly hypothetical,and I confessthat I have neverseen a Bittern dilate its neck. I simply believedthat it mightdo sofrom analogywith otherbirds like the PectoralSandpiper, in which the practiceis well known.x But fortunately there is an excellentand detailed account,in Brad-

• Cf. Nclson, Auk, 1884, pp. 218-221. 198 C•.•r•N,The Oesphagus ofthe Bittern. AprilAuk

tv. east.

tiss.

,//J Fig. 2

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Fig. 1 ;Fig. 3 Vol.1922XXXIX] J CHArIN,The Oesophagus of the Bittern. 199

{ord Torrey's'Everyday Birds' (1901) pp. 69-81, o{ the actions o• severalBitterns as seenduring their spring "pumping" in a Massachusettsmarsh. .On taking up this charminglittle book, a•ter many years'neglect, I was surprisedto find how closelymy hypothesistallied with Torrey's conclusionsafter watching the live bird. I cannot do better than to quote him directly: "The Bittern has been standingmotionless " "Suddenlyhe lowershis head,and instantlyraises it againand throwsit {orwardwith a quick,convulsive jerk. This movementis attendedby an openingand shuttingof the bill, which in turn is accompaniedby a sound which has been well comparedto a violent hiccough. The hiccough--withwhich, I think, the click o• the big mandiblesmay sometimesbe heard--is repeateda few times, each time a little louder than before; and then succeedthe real pumpingor stake-drivingnoises. "These are in sets of three syllableseach, of which the first syllableis the longest,and somewhatseparated {rom the others

"But the looker-onis likely to quite as muchimpressed by what he seesas by what he hears. During the whole performance, but especiallyduring the latter part o• it, the bird is engagedin the mostviolent contortions, suggestive of nothingbut a patient sufferingfrom uncontrollablenausea. Moreover,as soonas the preliminaryhiccoughs begin, the lowerthroat or breastis seent ø be swelling;the dilatationgrows larger and largertill the pumping is well underway; and sofar as my companionand I coulddetect, doesnot subsidein the leastuntil the noiseshave ceased altogether.

Explanation of figures on p. ]98. Fig. 1. Neck of the Bittern, partly dissected, skin removed from lower side, le•ving superficial muscles intact. Oesophagus not iafated; conn. riss., mass of swollen connective tissue at sides of throat; gem by., genin-hyoid muscle; by., hyoid axch; oes.,oesophagus; sk., thickened skin, seenin section; stern. by., sterno- hyoid muscle, enshe•thing the aeck below. thyr. cart., thyroid cartilage, lying beneath glottis; trig., base of tongue, as seen through floor of mouth. One- third natural size. Fig. 2. Open mouth of male Bittern in Spring; int. nrs., the opening of the internal nares; p., one of the pads on the inside of the mandible, between which the tongue, t, protrudes. (From photo supplied by the American Museum of l•atural History.) Fig. 3. Skinned head of Bittern, from above, showing the occipital portion of the cucullaris muscle, cuc., attached to back of skull. One-third natural size. 200 CItA?IN,The Oesophagus of the Bittern. [April[Auk

"How are the unique, outlandishnotes produced? I cannot professto know. Our opinion was that the bird swallowedair into his gullet, gulpingit downwith each snapof the beak. To all appearanceit was necessaryfor him to inflate the crop in this way before he could pump, or boom. "I madesome experiments afterwards, by way of imitating the noises,and these experiments,together with the fact that the grandbooming seemed to be really nothingmore than a develop- ment of the preliminaryhiccoughs, and the further fact that the swellingof the breastdid not go downgradually during the course of the performance,but suddenlyat the close:--allthese incline me to believethat the notesare mainly if not entirely causedby the inhalation or swallowingof the air "

The only point on which I cannot agree with Torrey is the "swallowing" of the air, which is mechanicallyso difficult to explain. I believerather that it comesfrom the tracheathrough the glottis. To examinefurther the structureof the accessoryvocal organs, sinceit wouldseem still as thoughthe soundmust originatein the syrinx,I madea thoroughexamination of the neckand its coveAng, Rolling up the skin of the neck from below, I found the walls of the oseophagusas thin as usual, and extensibleas they always are in a Heron's or Bittern's neck. There was no trace of true air-sacs,all dilation must involvethe oesophagusalone. But the skin of the neck, downto a point closeto the shoulders,was very much thickenedall the way round save for the mid-dorsalline, whereit remainedas thin as normally. The •hickening was due mainly to the bloated conditionof the connectivetissue forming the deeperlayer of this skin,now five millimetersthick overa large part of the neck. Besidesan infiltration of lymph, a very rich supply of small blood-vesselswas also noticeablein this tissue, which extendedfrom near the baseof the neckup to a point close to the back of the skull. Just behind the head, more deeply placed,and closeto the hornsof the hyoid, there was a loosemass of similarlymphold tissue on eachside of the throat; and as already stated,the elongatepads inside the lowerjaws were filled with the sametissue, all of which would undoubtedlysubside if not corn- Vol.1922XXXIX'[ • CriAPIN',The Oesophagus ofthe Bittern. 201 pletely disappearafter the breedingseason. On the inside of this heavy skin of the neck, moreover,there was a thin layer of muscle,its fibersrunning in an antero-posterior direction,and lacking only on the median dorsalline. Posteriorly no attachment to the body was noticed,at most it was slight, and the musclewas closelyunited with the skin; but anteriorly there weretwo pairedattachments. The upperones were on the occipital regionof the skull, and showedthat the greaterpart of this muscular layer representsthe longitudinallayer of the cucullaris muscle,present in very manybirds. On the lowerside of the neck, two muscularbands presumablyrepresenting the sterno-hyoid, insertedanteriorly on the thyroid cartilage,whence other muscular strands continuedto the hyoid. (See Figures i and 3.) The contraction of this sheet of derreal muscle would shorten the skinof the neck,and rather than to draw air into the oesophagus it wouldtend to expellit; so the explanationof the processis not to be found here. What we can say with certainty is that the AmericanBittern, in producingits well-known"pumping" notes, doesdistend the oesophaguswith air, and that in connectionwith this habit there is developedin the breedingseason a remarkable thickeningof the skin of the neck,with perhapsa modificationof parts of the liningof the mouththat serveto help in retainingthe air. Another adult male Bittern, skinned by our taxidermist about a fortnight earlier, is stated by him to have had the neck in the same condition. Probably only the male birds exhibit these modifications,for they alone are known to pump or boom. The use of the .oesophagusin such a manneris by no means confinedto the Bitterns. It is perhapsbest known in the case of the PectoralSandpiper, though accordingto Pycraft• many of the Pigeonsproduce their incessant"cooing" in this way; and even the male Ostrich is said to fill his gullet with air, and then produceby its expulsionthe loud soundknown as "bromming."a A somewhat similar action has been observed in the case of an African Bustard, Neotis caCradenhami, which utters a loud bark like that of a Bushbuck,3 yet has no pharyngealsacs like thoseof

'A History of Birds,' 1910, pp. 148, 149. See Duerden, American •Naturalist, LIV, 1920, p. 306. Forbes, Proc. Zool. Soc. London, 1880, p. 478. 202 TheOesophagus of th• Bittern. AprilAuk Otistarda; and an Australianmember of the samefamily, Eupodotis australis,--Pycrafttells us-- likewiseemploys its gulletas a vocal sac. Further, the male of an African Rail, Sarothruraelega•s, whichis responsiblefor a clear,long-drawn note recalling a tuning- fork, and heard usuallyat night, undoubtedlyshares the habit of inflatingthe oesophagus,and has a thickeningof the skin of the neck nearly comparable to that of the American Bittern. This I have examinedpersonally in the Congo. Finally, there are severalpasserinc birds with patchesof bare skin at the sidesof the neck, for examplethe A•rican Camaroptera superciliarisand Bathmedoniaruea, as well as the South American Donacobi•satricapill•s • in which somethingof the sort appears to take place. A word may here be appendedconcerning the displayof fluffy white plumesby many male AmericanBitterns in the mating season,to which attention was called by Mr. William Brewster someyears ago. • Thesecan be erectedconspicuously at the sides of the upperback. The specimenwe havebeen describing possessed such tufts of cream-coloredfeathers, arising from the anterior part of the pectoraltracts, a little in front of, and lateral to, the fore endof the largepowder-downs. Mr. Brewsterwas not satisfied as to just how theseplumes could be raised,though it had been suggestedto him that the skin of this regionmight be inflated; but from what has alreadybeen said, it will be dear that no air- spaceexists beneath them. Instead the mechanismfor elevating them was seen to consistof the superficialmuscle commonly foundat the baseof the neck,the cervicalportion of the eueullaris, which runs obliquely downward and backward from the mid- dorsalline at this point. Its lower edge,in this case,was found to be insertedin the skin about the basesof these white feathers, which are usually concealedby the dark streakedones lying just in front. So the contraction of this muscle would snfl]ee to elevate the plumesin exactlythe way Mr. Brewsterdescribed it. Perhaps alsothe shorteningof the longitudinalmuscle strands beneath the skin of the neck would pull that of the baseforward, and aid in the process. AmericanMuseum oe Natural ttistory, New York, N.Y.

See lVuertes, Bird-Lore, XV, 1913, p. 342. 'Auk,' 1911, pp. 90-100.