THE CONDOR A JOURNAL OF AVIAN BIOLOGY I_\! Volume 92 Number 1 February 1990

MAROh WI0 The Condor 92: 1-28 Q The Cooper Ornithological Society 1990 WVERSITY OF ~[4br-fJ- DRINKING MECHANISMS IN THE ZEBRA FINCH AND THE BENGALESE FINCH’

J. HEIDWEILLER AND G. A. ZWEERS~ Department of NeurobehavioralMorphology, Zoological Laboratory, Universityof Leiden, The Netherlands

Abstract. Two kinds of drinking behavior were studied by film and radiogram analysis of tip down drinking Zebra Finches (Poephilaguttata) and tip up drinking BengaleseFinches (Lonchurastriata) which use similar scoopingtongue motions to carry water into the mouth. Water transport through the pharynx differs: the Zebra Finch usesa scoopingmotion of the larynx that reoccurs in every motion cycle, while the beak is kept down. The Bengalese Finch elevates the head allowing water to flow downward due to gravity and pharyngeal properistalsis.Extensive analysesshow the anatomy of the speciesto be highly similar. The Zebra Finch is able to drink by a double scoop mechanism, because-unlike the Bengalese Finch-reflexes for glottis closure and esophagealperistalsis are used. Integration of these reflexesand a shift in timing of the larynx-scoophas modified tip up into tip down drinking. Thus, tip down is more complex than tip up drinking, since here actions from different cyclesand patterns are integrated in one motion cycle. Increased kinematic complexity is, apart from any historical scenario,an argumentthat tip down is derived from tip up drinking in Estrildidae. An evolutionary scenario is presented in which developments of scooping anatomical elements are seen as preadaptations.These developed by selectionon elements serving the highly specialized kind of feeding on seedsof Gramineae under high predator pressurein open fields, and allowed a wide secondaryextension of the feeding area. Key words: Drinking; oropharyngealanatomy: Estrildidae;Zebra Finch; BengaleseFinch.

INTRODUCTION fication, however, is not sufficient to understand Estrildid finches exhibit two kinds of drinking: which drinking mechanism really operates in a tip up drinking and suction drinking (Poulsen given speciesbecause several kinds of mecha- 1953; Wickler 1961; Immelmann 1962, 1965). nisms are found within each of the two main To understand how divergence in the evolution categoriesof drinking. The same is true for both of these two different kinds of behavior for one of the two successivesteps in drinking behavior: role may have developed, we need to know the intake of water into the mouth, and transport of physical mechanisms used in such drinking. the water from the mouth through the pharynx These two kinds of drinking can easily be clas- and into the esophagus. sified into the two main categories of avian For example, water is taken into the mouth in drinking since estrildid drinking patterns are the Cacatuinae by scooping the water with the characterizedby the same names (Wickler 196 1): lower beak (Homberger 1980); in Gallus, the beak tip up drinking, and suction drinking in mouth opens and closes several times, taking which the beak tips are kept down. This classi- some water each time (McLelland 1979); in Anus, a complex interplay of capillary action and pres- sure changesin the different areas of the mouth ’ ’ Received 23 May 1989. Final acceptance2 October serves to transport the water into and through 1989. the mouth (Kooloos and Zweers 1989). A similar 2Address reprint requeststo Dr. G. A. Zweers. feature is found in the category labeled “suction 111 2 J. HEIDWEILLER AND G. A. ZWEERS drinking.” For example, Psittacinae ladle water ing. Therefore the Zebra Finch and the Bengalese with the tip of the tongue, and Lorriculinae drink Finch (Lonchura striata) have been selectedfor with a suctioning action (Homberger 1980) analysis. The Zebra Finch is one of the eight whereas for Columba a double suction mecha- species of Australian Estrildidae that show tip nism has been proposed,in which lower air pres- down swallowing. The Bengalese Finch which sure develops first in the mouth and immediately originally lived in SoutheastAsia is a tip up, poly thereafter in the pharynx (Zweers 1982a). draught swallower of water. Several conclusions may be drawn from the The morphology of the interior of the mouth reviews of Schonholzer (1959) Homberger and pharynx at first looks similar in the different (1980) and Kooloos and Zweers(1989). The main species of Estrildidae. Therefore differences in difference found between the two categories of drinking behavior may either be correlated with avian drinking is in the transport of the water minor differencesin the epidermal structure, or from the mouth through the pharynx into the may be identified as “different applications of esophagus.In tip up drinking behavior, this part similar epidermal elements.” In the latter case, of the water transport occurswhile the beaks are the muscle-bone apparatus, the modal action kept in a “tipped up” position, whereas in suc- patterns for drinking, or both may be different. tion drinking behavior, the same transport oc- A secondaim of this researchwas to test whether curs while the head is “tipped down.” Further, the assumption holds that different kinematic tip up swallowing occurs in a series of drinking patterns may serve in highly similar morpholo- bouts which resemble poly draught behavior, gies to elicit different drinking mechanisms. whereas tip down swallowing comprises one Therefore the anatomy of the epidermal struc- drinking bout which has a mono draught ap- tures and the lingual muscle-bone elements must pearance.Therefore, we proposeto apply the fol- be compared. Since we have found no anatom- lowing descriptive terms to the main categories ical descriptions in the literature that are suffi- ofdrinking: tip up swallowing and tip down swal- ciently accurate, these must be included here. lowing. Both categoriesare certainly present in Description of the lingual muscle-bone appara- the Estrildidae. tus does, however, not serve for functional ex- Immelmann (1962) takes estrildid tip up planation of that apparatus, but rather for gath- drinking as a self evident feature, while for suc- ering anatomical evidence that lingual and tion drinking he proposesthat peristalsis of the pharyngeal integumental elements are equipped cranial part of the esophaguspumps in water. In suchthat they may carry out similar motion pat- the literature, the drinking mechanisms of the terns. eight suctiondrinking estrildid speciesare thought The development in highly similar morphol- to be identical with the drinking mechanism in ogiesof different behavioral patterns for the same pigeons(Poulsen 1953). Wickler (196 1) also con- role may have a specificcause. Immelmann and cluded that the drinking behaviors of Geopelia Immelmann (1967) consider tip down swallow- cuniata (Columbidae) and Poephila acuticauda ing of water to be a mechanism with a selective (Estrildidae) were identical. Immelmann (1965) advantage for those Estrildidae that must rely statedthat Zebra Finches (Poephilaguttata) drink upon desert water holes for their water needs. in a pigeon-like manner. Immelmann and Im- Their argument is that suction drinking allows melmann (1967) assumed,as did Lorentz (1939) much faster intake of water than tip up drinking, for pigeons, that sucking is caused by peristaltic so that predator pressuredecreases when the fast- movements of the anterior part of the esophagus. er mechanism develops. Their view includes the Fisher et al. (1972) suggestedthat Zebra Finches assumption that suction drinking is derived from drink like honey eaters. These authors provide tip up drinking. no further evidence for the proposed models. As a second cause of the development of suc- However, Zweers (1982a) has shown that Co- tion drinking, Immelmann and Immelmann lumba livia does not drink by peristalsis in the (1967) assume that in semiarid climates small esophagus,so that either the mechanisms must dewdrops are the only water source available, be different or suction drinking Estrildidae must and that these drops can only be ingested via the drink by the same double suction mechanism suction mechanism they propose. These two as- that has been proposedfor C. livia. The first aim sumptions need further testing. A third aim here of this paper is to analyze mechanisms for drink- is thus to measure the different kinds of perfor- DRINKING MECHANISMS IN ESTRILDIDAE 3 mance of both mechanisms and to apply the re- sults to a discussion of selection pressure. It is not only selectionpressure, however, which CAUDAL determines changein a system that is as complex \ as the oropharyngeal system. For example, to elicit appropriate drinking behavior, over 30 muscles in the mouth and pharynx must act in an orderly fashion. Internal constraints and physical boundary conditions also determine the direction of development. These may or may not have created a discontinuity between the two mechanisms. A comparison is needed to see which factors are important here. We start from a hypothetical ancestral tip up, poly draught drinking mechanism for Estrildidae that is rel- atively simple and closeto the drinking behavior seen in Gallus: water is scoopedwith the lower beak, then the head is tipped up; water runs down through the pharynx due mainly to gravity plus some pharyngeal properistaltic actions (Mc- Lelland 1979). Whether the two drinking mech- anisms may be deduced from this mechanism in one series or in two diverging directions is then ROSTRAL discussedto see if the mechanisms themselves FIGURE 1. The points at which measurementswere suggestboundaries or constraints which, in ad- made in analysisof drinking are illustrated for the Ze- bra Finch. The reference line of the neurocranium is dition to an evolutionary scenario, may have de- indicated by two markers (1 and 2). The upper beak termined how development has occurred. line runs from the beak tip to a marker at the cranio- facial joint (3). The lower beak line connectsthe beak METHODS AND MATERIALS tip with a marker at the quadrato-mandibularjoint (4). ANATOMY Three markers representthe rostral, intermediate, and caudal mouth floor (5, 6, 7). Additional points were Fresh and preserved specimens of the Zebra Finch the very tips of the beak and tongue. (Poephila guttata castanotis(Gould 1873)) and the BengaleseFinch (Lonchura striata (L.) var. domestica)were used for dissection of the mus- lard Bolex 16-mm camera, using Kodak Plus X cle-bone apparatus of beak and tongue. The pre- reversal film at 67 fps, as well as with a Teledyne served specimenswere perfused via the left ven- highspeed camera using Eastman Ektachrome tricle with 4% formalin. For each species,a total Video Newsfilm at 250 fps. The head was marked head was embedded in Epon C and cut in trans- with a seriesof triangular white markers as shown verse sectionsof 10 p to allow microscopic com- in Figure 1. The reflexes of tongue and larynx, parisons. Sections were stained according to a which occur when water drops fall upon the low- combined Mallory-hematoxylin staining proce- er beak tip and the lingual base, were filmed at dure (Zweers et al. 1977). Beaks of embedded 67 fps, while the birds were slightly anesthetized specimens were closed, and tongue and larynx with equithesin and were fixed in a stereotactic were brought into similar positions. SEM pho- apparatus (Zweers 1971) with their beaks wide tographs were made to locate orifices of glands open. and to enable the description of epidermal struc- About 100 radiograms were taken laterally of tures. The anatomical terminologies of Baumel both species drinking a suspension of barium (1979) and McLelland (1979) adapted according sulfate in water. The X-ray generator (Siemens- to Zweers (1982b), were used. Reiniger; Gigantos) was adjusted at 120 KV, 450 mA, and 0.003-see exposure time. Radiofilms KINEMATIC ANALYSIS were made with a camera (Arriflex) connected Cinematographyand radiography. The drinking to the X-ray apparatus, which was adjusted at behavior of both specieswas filmed with a Pail- 110 KV, 25 mA, and 0.0 1-set exposure time. 4 J. HEIDWEILLER AND G. A. ZWEERS

The radiogramswere put in an order representing sured with an accuracy of 0.01 ml. Further, a a general drinking bout by comparison with films cathode was placed in the water box, and the taken simultaneously. stick in front of the water box was made of con- Analysis offilms. Films were digitized frame ductive material to form an anode. When a bird by frame with a graphic tablet (Tectronic 4049) put its bill in the water box, contact was made. connected to a Vax computer (Digital Inc.). The The current was recordedby an oscillomink, thus following parameters were measured (Fig. 1): (1) determining water intake speed(ml/set). The time The distance between the beak tips (gape). (2) the bill is in the water is only a minor part of the The angle between the neurocranium reference drinking behavior in L. striata. To determine line and the upper beak line. (3) The angle be- drinking speed,the total time spent drinking was tween the neurocranium reference line and the measured from the films. Lonchura striata often lower beak line. (4) Height of the water level interrupts swallowing actions to inspect the en- between the beaks relative to the beak tip. (5) vironment. This inspection time was subtracted The distancebetween the rostra1mouth floor and from total swallowing time. the reference line on the neurocranium. (6) The The ability to drink small drops of water was distance between the intermediate mouth floor tested as follows: for five successivedays, the and the reference line on the neurocranium. (7) only water available to the birds was in small The distancebetween the caudal mouth floor and drops on a perspex sheet, offered for 3 min, five a reference line on the neurocranium. (8) The to 10 times a day. The drops were made smaller distance between the tip of the tongue and a line each day, but each time the total quantity of connecting the quadrato-mandibularjoint mark- water was 4 ml. On the first day, the birds were er with the lower beak tip (dorsoventral motion). offered four drops of 0.1 ml per session. The (9) The distance between the tip of the tongue drops were reduced to 0.067,0.05, and 0.03 ml; and a line connecting the beak tips (rostrocaudal on the last day, 40 drops of 0.01 ml were sup- motion). plied. These experiments were recorded on film The terminology used in the movement anal- and videotape to determine drinking speed and ysis is as follows: a bout of drinking is called a possiblechanges in drinking patterns. Birds were scene. A scene is composed of phases,each in- assumedto be performing drinking actions when cluding one or more cycles of typical motion movements of the throat and floor of the mouth patterns. Each motion cycle may be subdivided were visible. The birds had accessto food ad into stages.A sceneruns from the fixation of the libitum during all experiments. head a few centimeters above the water to the point at which the head is again in rest position RESULTS and the water has entered the esophagus.Tip up ANATOMY behavior comprisesthe phasesof head approach, beak immersion, head upstroke, beak tip up, and Integument return to rest position (cf. Kooloos and Zweers Epidermal structures.In this paper the oral cav- 1989). Tip down behavior comprisesa head fix- ity is defined as the area running from the beak ation, a head approach, and a beak immersion, tips to the transverse plane connecting the Plica after which the head returns to a rest position lingualis (i.e., the caudal edgeof the lingual wings) (cf. Zweers 1982a). and the caudal edge of the transversely oriented Corpus cavemosum maxillare. The pharynx ex- DRINKING PERFORMANCES tends from this plane caudally to the plane con- The birds were kept in pairs in cagesto which necting the tips of the dorsal and ventral pha- small bay windows were attachedfor filming pur- ryngeal scrapers (cf. Zweers 1982b). The main poses.The birds were trained to drink in an ex- epidermal elements are shown in Figures 3-7. perimental setup designed to determine water The roof of the mouth in P. guttata consists intake speed(Fig. 2). A pipette (filled with water of a layer of keratin with a system of pronounced and closed on top) was placed in a small (16 x hard ridges (Figs. 3a, 6B). These longitudinal 6 x 8 mm) water box. The pipette was sawn rugaeplay an important role in seedhusking (Zis- obliquely open at the lower end so that the level wiler 1965, 1967, 1979). During closure of the of the meniscus of the water box did not change beak, the tomial edge of the mandible is placed while a bird was drinking. Water intake was mea- between the sharp Ruga palatina lateralis and DRINKING MECHANISMS IN ESTRILDIDAE 5

FIGURE 2. Experimentalarrangement used to mea- suredrinking speed. Markers for film analysisare shown asused for theBengalese Finch. The water-filledpipette keepsthe level in the waterbox constant.The length of contactbetween the beaktips and waterbox is mea- suredvia an electriccircuit (A, K). I SCu TMn CCL OPG AL BL ’ dl La 6G VPF I:I‘ intermedialis. Caudal to the rugae lies the Corpus FIGURE 3. Main anatomicalelements in mouthand cavernosum maxillare. That cushion consistsof pharynxof theZebra Finch. a. Ventral view of the roof a relatively thick epidermis, loosely packed con- of the mouth and pharynx.The positionof the three nective tissue, and many venous sinuses (Figs. major salivaryglands is indicatedby brokenlines and 4d; 6B, C, D). The shape varies from an H to a solid dots(orifices). The fat dot rostra1to the Corpus horseshoe,tending more toward the former. This cavemosummaxillare indicates the orificeof the an- terior palatinegland. b. Dorsalview of the floorof the epidermal element has smooth, curved walls that mouth and pharynx.(See the list of abbreviationsfor are perpendicularto the surfaceof the upper beak. explanation.) The roof of the mouth in L. striata has the same elements seen in P. guttata. The cavernous body the dorsal edgesof which tend to curve caudally is equally variable, but tends more toward a to medial. Most of this gutter is filled with the horseshoeshape. lingual masswhile a slit-like area, the oropharyn- In P. guttata, the roof of the pharynx carries geal groove, lies between the mandibular walls over 20 small, caudally directed, and rather flex- and the lingual mass(Figs. 3b; 6C, D). The tongue ible spines. The secondarychoana lies in the me- carries a seed cup at its rostra1 end. The hairs dian caudal to the cavernous body (Figs. 4d, 7A) that form the seed cup develop from the ventral and diverges somewhat caudad (Fig. 7B). The side of the tongue (Fig. 4b). Caudal to the seed edgescarry about 10 somewhat enlarged spines cup lies a bulging area that forms the mid-part oriented mediocaudad (Fig. 4d). Caudal to the of the tongue. This area contains a large structure secondarychoana lies an infundibulum. The me- consistingof venous sinusesseparated by loosely dian ridge in the secondarychoana gradually ap- packed reticular and collagen fibers and sur- proaches and merges caudally into the roof of rounded by a network of connective tissue, form- the pharynx. The gape of the internal choana is ing the Corpus cavemosum linguale (Fig. 6C). actively changeable. The dorsal pharyngeal The thick dermis of this area has many papillae scrapers(syn. Papillae pharyngealesdorsales) lie piercing into the epidermis, which contain nu- caudal to this area. These are bilateral flaps, each merous corpusclesof Herbst and Merkel (Krulis carrying a seriesof some 10 flexible papillae with 1978). Caudal to this bulging lingual area lie the a spine projecting ventrocaudad (Figs. 3a, 4a). erectable bilateral Alae linguales (Figs. 3b, 4c, The roof of the pharynx in L. striata has a similar 7A). At their caudal edge,these carry about three appearanceexcept that the edgesofthe secondary large and several smaller flexible spines,pointing choana carry somewhat larger spines (Fig. 4e). caudally. The cartilaginous laterocaudal pro- The floor of the mouth of P. guttata is a deep cessesof the paraglossalpoint into the most lat- gutter between the high walls of the mandibles, eral spines (Fig. 7A). The floor of the mouth in 6 J. HEIDWEILLER AND G. A. ZWEERS

FIGURE 4. SEM photographs of the main anatomical elements in mouth and pharynx. a. Bilateral dorsal pharyngeal flaps with orifices of the gll. sphenopterygoideiin the BengaleseFinch (top is rostral). b. Seeckup at the lingual tip in the BengaleseFinch. c. Floor of the pharynx in the BengaleseFinch. From left to ril mt (i.e. from rostra1to caudal): lingual alae, lingual base and transversal folds of the integument, larynx and glottis, bilateral ventral pharyngealflaps, rostra1end of esophagus.d. Roof of the mouth and pharynx in the Bengalese Finch. From left to right (i.e. from rostra1to caudal): Corpus cavemosum maxillare, secondarychoana. palate DRINKING MECHANISMS IN ESTRILDIDAE I

L. striata has the same elements as that of P. guttataexcept that the gutter of the lower beak is somewhat deeper. The slightly wider lingual wings carry a few more, but smaller, spines. At its most rostra1point, the floor of the phar- ynx in P. guttatahas a widely extendable, smooth lingual base (Figs. 3b; 4c; 7A, B). From this area, deep but narrow lateral pharyngeal grooves run caudolaterad along the laryngeal area. In the me- dian lies the large larynx, covered with many small spines (Fig. 7C). These spines are larger along the glottal edges. Dorsocaudal upon the LI-LSA LSP MP MA CA larynx lie the ventral pharyngeal scrapers(syn. FIGURE 5. Schemeillustrating the positionand size Papillae pharyngeales ventrales). These carry of the salivaryglands and their orifices(solid dots) in some 10 large flexible spines pointing caudally the floorof mouthand pharynx.The upperhalf refers (Figs. 3b, 4~). The cartilaginous Processusdor- to the BengaleseFinch and the lowerhalf to the Zebra Finch. (Seethe list of abbreviationsfor explanation.) socaudalis arytenoideus extends into the most medial spine. The larynx as a whole can be el- evated and the scraper area can also be actively At approximately 1 mm and 2.5 mm caudal erected by the elevation of the procricoid area to the mandibular symphysis, the floor of the (Zweers and Berkhoudt 1987). The floor of the mouth showsthe two pairs of orifices of the large pharynx in L. striatahas the same elements as Gl. mandibularis anterior (there are three pairs in P. guttataalthough there are larger and more present in L. striata).The gland runs along the numerous spines on the dorsocaudal procricoid whole floor of the pharynx medial to the jaw area of the larynx. adductor muscles and dorsal to the geniohyoid Glands.Granivorous birds like the Estrildidae muscle. Rostrally, the efferent ducts merge more have well-developed glands due to their diet of and more, until two pairs of ducts remain (Figs. dry food (McLelland 1979). The glands are ar- 5; 6C, D; 7A, B). These extend rostrad in the ranged in the pattern typical for granivorous song floor of the mouth. The tongue contains a few birds, and are relatively large (Figs. 3a, 5). The Gil. linguales inferiores and Gil. linguales super- terminologies of Anthony (1920) and Baumel iores anteriores, which, in P. guttata,lie ventral (1979) adapted according to Zweers (1982b), to the Corpus cavernosum linguale (Fig. 6D) and were used. in L. striata,dorsal to that structure. A few ef- The two main groups of the Gil. palatinae and ferent ducts run dorsocaudad and open at the the Gil. sphenopterygoideae(Figs. 3a; 7A, B) are base of the lingual alae. found in the roof of the pharynx. The internal The floor of the pharynx contains the Gil. and external portions of the Gil. palatinae an- mandibulare posteriores, Gil. linguales super- teriores form one rather large volume of glands, iores posteriores (Fig. 4f) and the Gil. cricoary- with a length of 6.5 mm and a width of 2 mm, tenoideae (Fig. 7). The posterior mandibular that run along the secondary choana. The left gland is laterally flattened and lies medial to the and right efferent tubes extend rostrad and merge Gl. mandibularis anterior from the cricoid to the into each other. Their joint orifice lies rostra1to rictus level. The four efferent ducts open in the the Corpus cavernosum maxillare in the median. deep groove lateral to the lingual base. The Gil. In and lateral to the infundibulum lie the Gil. linguales superiores posteriores extend over the palatinae posterioreswhich have 1O-20 orifices. whole lingual base and a field of orifices are pres- In the dorsal pharyngeal flaps lies a field of nu- ent (Figs. 5, 7). These are surrounded by taste merous orifices of the Gil. sphenopterygoideae buds (Fig. 4f). Caudally, this field of glands (Fig. 4e). changesinto that of the Gil. cricoarytaenoideae, e and infundibulum. e. Secondarychoana with spinesalong the edgesin the BengaleseFinch (top is rostral).f. An orificeof thegll. lingualessuperiores posteriores with orificesof two tastebuds at thelingual base in the Zebra Finch. The barsindicate 1 mm, exceptthe bar in f whichis 0.1 mm long. 8 J. HEIDWEILLER AND G. A. ZWEERS

A 6B6C 6D 7A7B7C

Mx

RPM RPI RPL

scu

Mn

Mx

PIE CCM

Mn

CCL

PAL PIE

CCM GH

w . --/- MP FIGURE 6. Microscopic crosssections of the mouth of the Zebra Finch. The position of the sectionsis indicated in A. (See the list of abbreviations and text for explanation.) DRINKING MECHANISMS IN ESTRILDIDAE 9

PAL

SC PIE

MA ’ ’ \ ’ \ StH GP HT MP CG 4 HVM BH /-‘ IM HVL

LSP CrH HT CB MP

GHC

FIGURE 7. Microscopic cross sections of the pharynx of the Zebra Finch. The position of the sections is indicated in Figure 6A. (See the list of abbreviations and the text for explanation.) 10 J. HEIDWEILLER ANLIG. A. ZWEERS

which run along the dorsal side of the larynx and hyoglossusobliquus and M. ceratoglossus.En- in the ventral pharyngeal flaps. Only slight dif- gels (1938) did not describe these adaptations ferences are found between P. guttata and L. and hence a number of differences in lingual striata. All glands in L. striata are somewhat myology in the Zebra Finch and BengaleseFinch larger and run somewhat more to caudal than in relative to other families was observed. There- P. guttata (Fig. 5). fore, Engels’ description is not sufficiently de- tailed for our goal. This goal is, as said earlier, Osteologyand myology to gather sufficient anatomical evidence to test Jaw apparatus. The functional morphology of the assumption that the integumental elements feeding upon seeds in Estrildidae has been ex- of tongue and pharynx floor are equipped with plained by Ziswiler (1965). He distinguished two a lingual muscle-bone apparatus that may carry main kinds of seed husking: husk cutting out similar motion patterns in both species. (“schneiden”) and husk crushing (“quetschen”). Therefore a summary of the anatomy is in order. Most Estrildidae feed upon seedsof Gramineae (Upon request an extensive anatomical descrip- and apply the husk-crushing mechanism (Zis- tion of the tongue apparatus is available in a wiler 1979). The cutting mechanism requires a Dutch laboratory report.) highly complex pattern of jaw motion, in which Lingual osteology.The lingual bony elements protraction, retraction, laterad motion, and el- have the general avian composition (Figs. 6, 7, evation and depression of the lower jaw occurs. 8a). The paraglossalis a bilateral S-shaped ele- The crushing mechanism shows only elevation ment. Left and right paraglossalsfuse at their and depressionof the mandibles. For this reason rostra1tips. At their midpoints they have a me- we do not expect qualitative differences in the dial horizontal extension, the Ala medialis par- jaw apparatusesof P. guttata and L. striata. We aglossalis,which articulates with the basihyal by refer to Sims (1955) for the descriptions of the a heterocoelous,saddle-shaped joint. This allows jaw apparatus that are accurate enough for the elevation and depression as well as rotation of present goal. the paraglossalsalong their longitudinal axis. In Tongueapparatus. The tongueapparatus shows the median between the rostra1part of the par- much variation in birds (McLelland 1979). These aglossalslies the oval-shaped hypoglossal (Fig. variations are often closely related to feeding spe- 8a; OS hypentoglossum,in Ziswiler 1979) a neo- cializations (e.g., Homberger 1980). George and morph that sustainsthe Corpus cavemosum lin- Berger (1966) reviewed descriptions of tongue guale. The basihyal and urohyal are fused. They musculature in various bird species. Their de- form a heavy rod that is flattened laterad at the scription for Passeriformeswas basedon the work rostra1 part and flattened dorsoventrad at the of Engels (1938). Engels described the tongue caudal end. The caudal end bears a horizontally musculature of 19 species in seven passerine flattened cartilaginous disc, the Cartilago urohy- families. alis, that lies ventral to the cricoid. This element Ziswiler (1979) explains that in estrildids the sustains the larynx and guides the protraction tasks of orienting and locating a seed for proper and retraction of the larynx relative to the lingual crushing, expulsion of the shell parts, and seed apparatus. The basihyal has, at its midpoint, a transport, are functions of the lingual apparatus. lateral processthat articulates with the cerato- In thosepasseriform families in which the tongue branchial. The ceratobranchialsare relatively long plays the rolesjust mentioned during seedeating, (7.7 mm) and heavy elements. The epibranchials each family examined has a different kind of stiff- and pharyngobranchials lie more caudally and ening of the external tongue portion. Ziswiler they are much shorter (4.5 and 0.7 mm, respec- arguesthat in these families several elements of tively); the latter element is cartilaginous and its the lingual apparatushave adapted to theseroles, caudal tip points to dorsal. independently. In the estrildids these adapta- Lingual myology.(Figs. 6,7,8) There are three tions are found in the shape of the paraglossals, lingual muscle groups:intrinsic, extrinsic and ex- the development of the Corpus cavernosum lin- ternal lingual muscles. The terminology applied guale, and a neomorph bony element, the “OS here is according to Vanden Berge (1979) as hypentoglossum.” Further he assumes that the adapted by Zweers (1982b). There are two in- high mobility of the paraglosso-basihyalarticu- trinsic lingual muscles, which connect lingual lation is accomplished by modifications in M. bones: M. hyoglossusobliquus and M. cerato- DRINKING MECHANISMS IN ESTRILDIDAE 11 glossus;there is no M. hyoglossusanterior. M. hyoglossusobliquus originates along the ventro- lateral side of the basihyal, from its cranial tip up to and including the capsule of the basihyal- ceratobranchial joint. This muscle inserts on the ventral and medial sides of the paraglossal,cau- da1 to the joint between paraglossalsand basi- hyal. M. hyoglossusobliquus is trapezium-shaped in lateral view and V-shaped in crosssection. It runs perpendicularto the axial length of the hyoid apparatus.The muscle is relatively large and pro- vides the apparatus with a rather long working Mn TMn HG PG BH CB UH EB PB arm; its contraction causeselevation of the tip of the tongue. The antagonist, M. ceratoglossus, originates along the full length of the cerato- branchial and inserts via a strong aponeurosison the caudoventral side of the paraglossal,rostra1 to the basihyal-paraglossaljoint. Five extrinsic lingual musclesare present, con- necting the lingual bones to the jaws, the larynx and trachea or other elements (Fig. 8~). M. gen- iohyoideus is a large protractor muscle compris- I I I I III I I I HT CrH Cr TLD CIV VPF ing two separateportions. The rostra1part orig- HVL CG UH TLV CIC TR inatesalong the ventromedial side at the midpoint of the mandible. The caudal part originates from GPGHRGHC GH UH Mn SH the ventrolateral side of the mandible at the level of the foramen mandibularis. Both slips insert along the epibranchials and pharyngobranchials. M. stylohoideusis a large, flat, triangular-shaped retractor muscle that originates ventrocaudola- teral at the angular part of the mandible and inserts dorsal to the rostra1part of the basihyal- ceratobranchialjoint. M. ceratohyoideusretracts the strand of connective tissue that proceedscra- nially in the median raphe of the intermandibu- MR PG IM iiH StH CH CB ES & lar muscle. The muscle connectsthe medial side of the caudal end of the ceratobranchial with the FIGURE 8. Osteologyand myology of lower jaw and tongueapparatus in the Zebra Finch. a. Osteology.The median strand mentioned, and may elevate the lowerjaw has an extensive,strong symphysis and sharp floor of the pharynx. tomial edges;at the rictus level the dorsal edges slant M. hyovalvularis (cf. Zweers 1982b), pars me- mediad. The hypoglossalis a relatively small element dialis, connectsthe caudal part of the area dorsal that lies dorsomediad to the rostra1tips of the para- glossals.b. Myology. Intrinsic lingual musclesand the to the basihyal-ceratobranchial joint to the der- musclesconnecting lingual and laryngealelements are mis of the Papillae pharyngealesventrales. Pars shown. c. Myology. Ventral view ofmuscles connecting lateralis connectsthe dorsomedial side of the ros- the lingual and jaw apparatusare drawn. The jaws are tral end of the ceratobranchial to the dermis of rotated slightly laterad so that the lingual apparatusis the ventral pharyngeal flaps. The two parts are visible. All musclesare presentbilaterally, but they are drawn on only one side. (See the list of abbreviations only separated near their origin by M. hyotra- for explanation.) chealis. M. hyovalvularis runs dorsolateral to M. hyotrachealis (contrary to the position as drawn somedial to the latter muscle; it originates caudal in Fig. 8b) and medial to the ventral pharyngeal to the origin of M. hyovalvularis and runs to the groove. M. hyovalvularis may elevate the flaps rostra1edge of the cricoid. M. hyotrachealis con- and/or procricoid area of the larynx (Zweers and nects the area dorsorostral to the basihyo-cera- Berkhoudt 1987). M. cricohyoideus runs dor- tobranchial joint to the lateral side of the first 12 J. HEIDWEILLER ANDG. A. ZWEERS tracheal ring. The last three musclesmay protract glands: (1) The Gl. mandibularis anterior has the laryngeal area relative to the tongue. three rather than two pairs of efferent ducts. (2) External lingual muscles indirectly determine The Gil. linguales inferiores lie dorsal, not ven- the position of the lingual apparatus (Fig. 8b, c). tral, to the Corpus cavemosum lingualis. (3) The There are four muscles that may retract or de- Gl. mandibularis anterior and posterior lie more pressthe pharyngeal floor area. M. claviculocri- lateral. (4) The caudal part of the lingual base coideus and M. claviculovalvularis originate contains fewer glands. Finally, the muscle-bone jointly from the rostrodorsaledge of the clavicle. apparatus in L. striata shows two more small They run dorsorostradalong and interwoven with differences:(1) M. geniopharyngealishas an extra the dermis of the ventral neck, then split and slip that connectsthe mandibular symphysisand crossthe subcutaneal area ventral to the larynx, the paraglossal,just caudal to the paraglossal- attaching separatelyto the cricoid and to the der- basihyal joint. (2) M. ceratohyoideus is less ex- mis of the ventral pharyngeal flaps, respectively. tended to rostral. The very long M. trachealis lateralis runs along and closely connected to the trachea, separate DRINKING IN THE ZEBRA FINCH from the previous muscles. The dorsal and ven- Kinematics of a drinking bout. Drinking bouts of tral portions originate at the tracheal ring dorsal Zebra Finches are very similar. They all include to the syrinx and run craniad along the trachea, almost identical phases,each composed of one inserting into the dorsal side of the first complete or more cyclic motion patterns. Only slight dif- tracheal ring and into the cricoid, respectively. ferences between drinking bouts occur. These Three muscles may elevate the depressedoro- represent the flexibility of the behavior, since pharyngeal floor. A relatively very heavy M. in- they are related to motivation and to circum- termandibularis attaches to the medial side of stances such as how the water is offered and the dorsal edge of the mandible, from the sym- whether the birds feel comfortable or not. The physis to the level of the corner of the mouth. differences are found in the amplitudes and in Left and right musclesrun ventrad and turn me- the number of repetitions of a cyclic motion pat- diad at the level of the ventral edge of the man- tern. Therefore we have developed a generalized dible, meeting each other at a median raphe; in picture of a drinking scenethat will be illustrated cross section, they form a U shape. They may by describinga representativedrinking scene(Fig. elevate the gutter they form for the tongue. A flat 9). and strong M. serpihyoideus originates ventral The head is kept fixed about 2 cm above to the auditory meati from the exoccipital; the the water for O-20 msec, with the eyes focused muscle runs ventrorostrad, turns mediorostrad binocularly upon the offered water. A fast head at the ventral edge of the mandible and attaches approachtowards the water follows, lasting 120- to the same median raphe as, and ventral to, M. 160 msec, during which time the beak tips open ceratohyoideus.A broad, very thin, M. cutaneus to a gape of about 1 mm. The beaks are im- colli, closely connectedto the dermis, of the neck mersed, but not further than one-third of their may increasethe elevation of the pharyngealfloor. length. Water intake now occurs during the im- mersion phase. As many as 50 cyclic repetitions Anatomicaldifferences between the of protraction and retraction of the tongue occur Zebra Finch and the BengaleseFinch with a frequency of 18-20 Hz, so that one tongue The morphologies of the two species are very cycle takes about 50 msec. The gape increasesto similar. There are a few minor differencesin the a maximum of 3 mm. The average duration of integument. In L. striata: (1) the Corpus caver- the immersion phasesfilmed is 1,120 msec, but nosum maxillare tends to be shaped more like a the phase may last a few seconds. During the horseshoethan like an H; (2) the papillae and upstroke phase, the head is once again elevated. spines at the palate and along the edges of the The beak is kept wide open during the 100 msec secondary choana are larger and extend further that this phase may last. As soon as the head caudad; (3) the mandibular gutter is slightly reachesa horizontal position the beak is closed. deeper; (4) the lingual wings are wider and carry During the next phase,the tip up phase, the head more but smaller papillae; and (5) there are more is kept in a tipped up position for about 420 msec and larger spines on the procricoid area. Lon- while several cyclic throat motions occur; the chura striata also exhibits a few differencesin the head then returns to rest. DRINKING MECHANISMS IN ESTRILDIDAE 13

(many motion cycled I I I 1300 1400 1800 Ob eQqMSEC.

FIGURE 9. Schematicrepresentation of a drinking scenein the Zebra Finch (upper part) and in the Bengalese Finch (lower part). The sequenceof the successivephases has been indicated along the abscissa.The immersion phase of the Zebra Finch is made up of many motion cycles.For the BengaleseFinch, two drinking scenesfrom a bout including several more are shown.

Kinematicsof an immersioncycle. The pre- These are partly visible on the films: depression vious description of a drinking bout still did not of the rostra1and midpoints on the floor of the allow the formulation of models for water intake mouth (throat) and elevation of the caudal point and transport mechanisms. Therefore, we made indicate that protraction of the lingual apparatus a quantitative frame-by-frame analysis of 20 occurs. cycles representative of the behavior in the mid- The immersion cycle may be subdivided into dle of the immersion phase (Fig. lo), and we five stages,as follows (Figs. 10, 11): the tongue developed a generalized immersion cycle (Fig. begins to protract at the start of stage 1 while the 11). An immersion cycle is defined as beginning beaks are already depressingand the gape is in- when the tongue starts protracting. creasing slightly. Stage 2 starts when the beak The upper and lower beaks rotate simultan- motions reverse: elevation begins and the gape ously in the same direction over very small an- startsto decrease.At the same time, lingual pro- gles. The elevation of the upper beak is in most traction continues, and a rapid elevation of the immersion phasessomewhat larger than that of lingual tip occurs.The lingual protraction is con- the lower beak sothat the gapeofthe beak changes firmed by the motions of the mouth floor mark- slightly. During elevation of the beak the gape ers. The rostra1point continues to depress,and increases,but less than 0.4 mm. Often the gape the midpoint depressesslightly more or does not does not change at all, but in the course of the move becausethe lingual apparatus has already whole immersion phase the elevation of the up- passedthat point. The caudal marker continues per beak increases, resulting in a slight overall to elevate for the same reason. Stage3 startswith increase in the gape. Every gape cycle occurs si- a reversal of lingual motions: the tongue retracts multaneously with a cycle of lingual motions. very fast, the lingual tip depressesvery fast, and 14 J. HEIDWEILLER AND G. A. ZWEERS

STAGE NO. 12345 123 4 123 4 5

UPPER BILL LOWER BILL E

GAPE

MANDIBLE

I RETRACTION

I m I I II DEPRESSION

9.0. CAUDAL MOUTH 8.5. \‘ 80. / FLOOR ,LE”ATmN‘ 0 40 80 120 160 200 240 280 320 MSEC. FIGURE 10. Representative kinetogram of six mo- tion cyclesfrom the middle section of a drinking bout of the Zebra Finch. All measurements are in milli- meters, except for the angles of the beaks with the neurocranium, which are in degrees.For the frames in which the tongue tip is not visible, the positions mea- IMMFRlnN sured are connected by dashed lines. .I....._, ._._.. 1 .,....._, ._._. . _. TAENIOPYGIA LONCHURA the beaks and gape continue to elevate and de- FIGURE 11. Generalized kinetograms of drinking. The left column representsthe immersion cycle of the crease,respectively. The lingual motions are again Zebra Finch; the middle and right columns show the confirmed by the motions of the mouth floor immersion cycleand tip up cycleof the BengaleseFinch, markers: the rostra1point elevates, the midpoint respectively. Protraction and retraction of the man- is stable, and the caudal point depresses. dible could be included for the BengaleseFinch in the right column. Dashed lines indicate kinetogramsfound A sudden secondreversal of the lingual motion occasionally.(See text for explanation.) pattern marks the start of stage 4: a very fast second elevation of the lingual tip occurs, while lingual retraction comesto a halt or even reverses In the radiograms, the water is black due to the into protraction for a moment. The small shoul- barium sulfate, and the larynx appears as a light der in the curve which describes the elevating grey area at the end of the trachea. For clarity, rostra1mouth floor marker confirms these sud- a few preliminary remarks about the water trans- den lingual motions. The gape starts to increase port mechanism are given in the following para- while the beaks continue to elevate. Stage 5 be- graph. These indicate the relationship of the ra- gins with the reversal of the lingual elevation, diograms to the model, and will be explained in which once again rapidly depresses;lingual re- the next section. traction is continued. In this stagethe beaks can Radiogram (a) representsthe start of a drink- show either elevation followed by a fast depres- ing bout: the beak is open, the larynx and lingual sion, or a rather slow depression. apparatus are retracted and depressed.This ra- To allow the formulation of a model for the diogram demonstrates the rise of the water level mechanism of water intake, this description of a along the beaks (by adhesion). Radiogram (b) is cycle in the immersion phaserequires additional from the start of stage 1: the larynx is retracted information from X-ray analysis about motions and in dorsal position. The tongue is retracted ofwater and larynx. Six radiograms were selected and elevated, the lingual alae are positioned that represent the most typical water and larynx against the Corpus cavernosum maxillare. The positions during the immersion cycle (Fig. 12). narrow space between tongue and upper bill is DRINKING MECHANISMS IN ESTRILDIDAE 15

a b

FIGURE 12. A selectionof radiogramsof the Zebra Finch drinking a barium sulfate suspension.(See text for explanation.) 16 J. HEIDWEILLER AND G. A. ZWEERS

FIGURE 13. A schematic representation of the double scoop drinking mechanism of the Zebra Finch. The first scoop is a lingual scoop occurring at the end of stage 2 (c), whereas the second scoop is a larynx scoop, performed in stages3 and 4. (See text for explanation.) filled with water (by capillary action). Some water enters the choana (Figs. 12c, d, t), that densely from the previous scoop is present, still on the packed separate water doses are visible in the lingual base. Radiogram (c) is from the start of esophagus(Figs. 12c, d, e) (indicating that peri- stage 2: the tongue is protracted and still de- stalsis occurs), and that variation in beak posi- pressed; the larynx is also protracted and ele- tions may occur relative to the more stable mo- vated against the Corpus cavernosum maxillare. tion pattern of the tongue. (From the latter position, the tongue scoopsthe Tip down drinking by a double scoopmecha- water caudad while the larynx is rapidly de- nism. The mechanism for water intake and water pressed.This is shown in radiogram (d).) A large transport can now be formulated as a double dose of water is present on top of the tongue. scoop mechanism. This mechanism is effected The preceding water dose lies in the esophagus, first by the lingual tip and second by the rostra1 caudal to the pharyngeal haps. Radiogram (e) tip of the larynx. One dose of water is taken into representsthe start of stage4. The larynx is pro- the mouth and transported through the pharynx tracted as far as possible and its rostra1 part is during each immersion cycle (Figs. 11, 13). elevated against the Corpus cavemosum max- In stage 1 the tongue runs rostrad along the illare (therefore it now scoopsa dose of water). mouth floor; some water remains in the opening The water doseis on the caudal part of the larynx mouth by adhesion to the beaks. In stage 2, the and caudal to it. From this position, the elevated tongue protracts still further and the lingual tip larynx is retracted (radiogram (f), mid-stage 5) is elevated very rapidly (first scoop) while the (pushing the water doseinto the esophagus).Fur- mouth once again closes.Some increase of pres- ther, the radiogramsdemonstrate that somewater sure in the rostra1 mouth, together with the DRINKING MECHANISMS IN ESTRILDIDAE 17 scoopingaction of the lingual seedcup,forces the was dripped on the lingual base. Further, in this water dose to run over the tongue between the situation, the tongue as well as the larynx showed lingual wings to the lingual base. The depression clearly the same scooping motions as derived of this area causesa pressuredecrease. In stage from film and radiogram analyses. 3 the rostra1tip of the larynx is protracted and elevated very fast relative to the tongue (second DRINKING IN THE ZEBRA FINCH scoop).This action ofthe larynx pushesthe tissue Kinematicsof a drinking bout. A generalized of the lingual base against the lingual wings so drinking bout was formulated under the same that the lingual tip is again depressedvery fast.The conditions as for P. guttata;a representativescene somewhatfolded tissuemass of the rostra1tongue will be described (Fig. 9). The scene is made up base and the lingual wings are pressed against of the same phases as described for P. guttata; the palate at the end of stage 3. That mass of thus only differenceswill be mentioned. The ap- tissue keeps the water dose, which during this proach phase lasts about 250 msec and the im- stageis held above the lingual base, from running mersion phasedoes not take more than 350 msec. back into the oral cavity. The protracting and During this time only three to maximally eight elevating larynx brakes the retraction of the cycles of beak and lingual motions occur. The tongue so that the lingual retraction comes to a gape does not exceed 1.5 mm; by the end of the halt for a moment in stage4. Then the elevated immersion phase, the beak is almost closed. The larynx retracts along the palate. As a result, the upstrokephase lasts about 100 msecduring which water dose is pushed caudad and the folded lin- the head is elevated and positioned horizontally. gual baseonce again unfolds. In stage5, the water The tip up phase shows a series of clear cyclic dose is pushed into the esophagusby the retract- throat and beak motions. From this description, ing larynx, the lingual retraction slowsdown, and it may be expected that water intake and the the tip of the larynx and all lingual elements are collection of several water dosesin the oropha- depressed so that the mouth and pharynx are ryngeal cavity will occur during the immersion prepared for the next intake of a water dose. In phase, and that transport of water to the esoph- the esophagus,water is transported by peristalsis. agus occurs during the tip up phase. Two remarks must be added: an extra dose of Kinematicsof the immersioncycles. Four or water may be moved to the pharynx in stage 3. five similarly composed immersion cycles are The very rapidly depressing tongue may press usually found, during which the amplitudes of the water, that is present due to capillary action, the motions involved gradually change(Figs. 11, in the lateral oropharyngeal groovesbetween the 14). The start of an immersion cycle is defined tongue and mandible, caudad. Further, a mouth- as the point at which the beak begins to open. ful ofwater is moved caudad in the mouth during The cycle is subdivided into four stages.In stage the upstroke by a slight increasein the gape. This 1, the beak opens and the upper beak elevates feature may be compared to a drop of water run- while the lower beak depresses.The mouth floor ning away from the tips of a pair of forceps as at the rictus level depresseswhile the cranial, they are slowly opened. The water is swallowed mid-, and caudal markers upon the throat also in a way similar to that used during immersion. depress.At the end of the cycle, the caudal mark- Additional evidence for the presenceof a dou- er stops depressing.The latter motions indicate ble scoopmechanism comes from reflex studies. that the tongue is protracting along the floor of It might be expected that, if the water is trans- the mouth. In stage2 all motions continue except ported directly over the larynx and along the that of the mid-throat marker, which reverses choana, these wide openings would show a clos- into elevation but does not elevate to its original ing reflex when touched by water arriving ros- level. In stage 3 all motions continue, with the trally on the lingual base. This assumption was exception of the rostra1throat marker which now tested. Water was dropped at several points in elevates. In stage 4 the mouth closesagain, the the oropharynx and the reflex reactions of the upper beak depresses,and the lower beak ele- choana and larynx were filmed while the head vates. Closure occurs faster than does opening. was fixed in a stereotacticapparatus. The closing The mouth floor motions continue except at the reflex of the glottis occurred and the choana nar- rictus level where elevation again occurs. The rowed, but it did not completely closewhen water mouth floor markers indicate lingual protraction 18 J. HEIDWEILLER AND G. A. ZWEERS

STAGE NO. 123 4 (Due to this tongue movement, water flows cau- dad on top of the tongue. When the tongue is in a fully protracted position, the lingual tip is el- evated [lingual scoop] and the tongue retracts.) The onset of this motion is shown in radiogram (c) (stage 3) which shows a more retracted lar- ynx, still elevated up to the palate, and a larger amount of water on top of the lingual base. In radiogram (d) (stage 4) the larynx is in its most caudal position, keeping the entrance of the esophagusclosed. There is still some water in the rostra1 part of the esophagus.The small black line is either some barium sulfate left lateral to the larynx or a little water running back since it is possible that not all the water from the pre- MID 15.5- / Ft%Z 15.0- vious dose will have run into the crop. The lin- 14.5. gual base is fully depressedand the pharyngeal area above the lingual base is full of water. The CAUDAL 14.0. r----I,+/ tongue is retracted, the lingual alae are elevated k%~ 13.0. and the tip depressed.Radiogram (d) also indi- 1ELEVATION cates that the esophagusof L. striata does not 0 40 80 120160200 MSEC. show peristaltic contractions. FIGURE 14. Representativekinetograms of the im- Kinematicsof the tip up cycles.Usually about mersion phase of the BengaleseFinch. All measure- five to seven cycles occur. These cycles are re- ments are in millimeters, except for the angles of the beaks relative to the neurocranium, which are in de- markable for two reasons (Figs. 11, 16): strong grees. and increasingprotractions and retractions of the mandible occur, as do increasing and strong la- and retraction. The lingual tip is only visible in ryngeal motions. The start of a tip up cycle is a protracted position when the tip is seen to be defined as the start of the opening of the beak; elevated. that moment coincideswith the start of the man- In the course of the phase some changes do dibular protraction. Five stages may be de- occur. The gape increaseswhile the position of scribed. In stage 1 the beak opens, the mandible the beak tips rotates ventrad. Depressions are protracts,and the throat markers depress.In stage larger than elevations for all of the markers along 2 the same motions occur, except that the caudal the throat. This means there must be a gradual throat marker elevates very fast. In stage 3 all increase in the spaceavailable at the level of the motions are continued except that the caudal rostra1part of the pharyngeal cavity. throat marker is again depressedvery rapidly and Figure 15 showsfour radiograms (a-d) that are the rostra1 marker is now elevated. At the end representative for the immersion cycle of drink- of stage4 the beak begins to closeand the motion ing BengaleseFinches. Stagesl-4 refer to the water of the caudal throat marker is reversed into el- intake mechanism and are explained in a later evation while the rostra1 marker continues to section. Radiogram (a) shows the start of the elevate. In stage 5, beak motions continue while immersion phase.The tongue and larynx are both the throat markers again reverse from elevation in a depressedposition and are already partly to depression. protracted (stage 1). The area above the tongue The remarkable motion of the caudal throat is still empty. In radiogram (a) the rise of the marker is explained as follows. In the first cycle water level along the beaks (due to adhesion) is drawn in Figure 16, the extra dip in the curve, clearly visible. Radiograms (b), (c), and (d) dem- illustrating the elevation and depression of the onstrate the processof water intake in L. striata. marker which separatesstages 2 and 3, is absent. Radiogram (b) shows the larynx in an elevated However, this dip develops in the second cycle and protracted position. The tongue is in a de- and increases in subsequent cycles. The larynx pressedand retracted position (start of stage 2). lies dorsal to this marker so that this extra dip From this position the tongue moves rostrad. in the curve must be causedby an extra up-down DRINKING MECHANISMS IN ESTRILDIDAE 19

FIGURE 15. A selection of radiograms of the BengaleseFinch drinking a barium sulfate suspension.a-d. These radiograms represent stagesduring the immersion phase. *h. These radiograms illustrate stagesduring the tip up phase. (See text for explanation.) 20 J. HEIDWEILLER ANDG. A. ZWEERS

are elevated, which decreasesthe volume avail- able for the water mass on top and along the lingual base and larynx. (This motion squeezes water along the larynx into the esophagus.)In radiogram (h), tongue and larynx are both de- pressed(stage 5) in order to squeezethe last water from the lateral pharyngealgrooves into the space above the lingual base. This radiogram demon- stratesagain that peristalsisdoes not occur in the BengaleseFinch. Separate mechanisms for water intake and water transport. Two separate mechanisms op- erate to transport water into the esophagus.The first mechanism occurs during the immersion phase, transporting water to the rostra1 part of

80 240 320 MSEC. the pharynx. The second occurs during the tip FIGURE 16. Representativekinetograms of the tip up phase,transporting water into the esophagus. up phaseof theBengalese Finch. All measurementsare The intake of water is a delicate interplay of in millimeters,except for the anglesof the beaksrel- several mechanisms: adhesion, capillarity, and ative to the neurocranium,which are in degrees. changing pressure (Fig. 17). The mechanism of water intake during immersion is as follows: in motion of the larynx, superimposed upon the stage 1, water runs between the beak tips as a cyclic protraction and retraction of the linguo- result of adhesion and capillary action. During laryngeal apparatuses.This motion may be in- stages 2 and 3, the slow opening of the beak terpreted as a scooping motion. causeswater to run further into the mouth as a Figure 15 (e-h) showsfour radiograms that are result of capillary action, again comparable to a representative for a cycle of the tip up phase. In water drop running back along a pair of spreading the following description,a few remarks are added forceps. In stages2 and 3 the lingual base de- about the swallowing mechanism. They are ex- presses,although the larynx keeps its elevated plained in the next section. Radiogram (e) shows position. That enlarges the rostra1 part of the the buccal cavity completely filled with water. pharyngeal cavity, which causesa decreasein air Some water has also entered the secondary pressure.As a result this area is prepared to re- choana. Water that has adhered to the outside ceive water. Further, the protractingtongue builds of the lower bill may run down along the throat up extra pressurein the rostra1part of the mouth. as a big drop. The bill tips are slightly separated. During the protraction of the tongue in stages2 In radiogram (e) (stage 1) the tongue is in a re- and 3, the lingual tip is depressedand the lingual tracted and elevated position while the larynx is alae elevated.That tongueposition preventswater in a protracted and depressedposition, so that already collected on the lingual base from retro- the rostra1part of the larynx is below a fold of grade flow. In stage 4, water is scooped by the the lingual base. Radiogram (0 is from stage 3. elevating lingual tip and transported into the Tongue and larynx have the same position rel- pharynx by the retracting tongue. The closing ative to each other as in radiogram (e) except mouth and elevating tongue cause increasing that the rostra1part of the lingual base and the pressurein the mouth so that the scoopedwater larynx are depressedeven more. Now water runs as well as the water present by capillary action from the oral cavity through the bilateral oro- in the narrow oropharyngeal grooves is pressed pharyngeal groovesto the rostra1part of the pha- caudad into the rostra1 part of the pharyngeal ryngeal cavity. This water is added to the water cavity. As soon as the tips are dipped in water, mass collected at the lingual base during the im- these actions transport doses of water from the mersion phase. Radiogram (g) is from the end of water mass running between the beak tips due stage3. The tongue is still retracted and elevated. to adhesion and capillary action. Eventually, rep- In this stagethe caudal part of the larynx is de- etition of these actions moves dosesof water to pressedwhile the rostra1part and the lingual base the caudal oral and rostra1pharyngeal area. The DRINKING MECHANISMS IN ESTRILDIDAE 2 1

TIP UP

FIGURE 17. A schematicreoresentation of the drinking mechanismin the BengaleseFinch. See text for explanation. increasing depression of the pharynx floor con- and the lingual base and larynx are depressed. firms the mechanisms proposed for water stor- These actions transport water from the oral into age. the pharyngeal cavity. Water transport during the tip up phase has While the tongue is kept in its elevated and two aspects:(1) transport from the mouth to the retracted position, the lingual base and larynx rostra1pharynx; and (2) transport from the phar- elevate again while moving from rostra1to cau- ynx into the esophagus.Both aspects occur in dal. In this way the water in the pharyngeal one motion cycle, the latter due to the interplay grooves and the water in the pharyngeal cavity of laryngeal scoopingand a kind of properistaltic is scoopedand squeezedcaudad into the esoph- action of the pharynx. With the mouth full of agus during stages4 and 5 (properistalsis). The water and a water mass above the lingual base, water staysin the esophagusdue to gravity. Since the beak is tipped up. Becauseof the position of no peristaltic action is seen in the radiograms, the head, gravity, in addition to adhesion and apparently transport through the esophagusoc- capillarity, keeps the water in the mouth and curs due to gravity. pharynx. Then in stage 1, the larynx, which has This proposedmechanism is supported by the been in a retracted and elevated position, de- back and forth movements of the clearly visible pressesand protracts rapidly. At the same time rostra1end of the water mass in the beak (Fig. the tongue retracts so that the rostra1part of the 16). During stages 1, 2, and 3 the water mass larynx must run below a fold of the integument moves caudad due to the depressinglingual base of the lingual base, an action which closesoff the and larynx. In stage 4, during the larynx scoop, glottis. During these movements the gape is en- the water in the beak runs rostrad for an instant. larged to make space for the water pushed ros- In stage 5, the closing of the beak decreasesthe trad. In stage 2, tongue and larynx protract si- space in the oral cavity which causesthe water multaneously into a depressedposition while the still present to again move in a rostra1direction. gape increases.In stage3, the tongue is elevated Additional evidence for a scooping action of 22 J. HEIDWEILLER AND G. A. ZWEERS

TABLE 1. Drinking performances. n = number of observations, SD = standard deviation.

Poephila guffata Lonchura striata SD n SD n

Mean daily water intake 1.58 ml 0.61 28 1.59 ml 0.87 14 Mean water intake speed 0.50 ml/set 0.16 24 0.27 ml/set 0.06 27 Mean drinking speed 0.44 ml/set 0.20 12 0.04 ml/set 0.01 10

the larynx comes from films of reflex studies of DISCUSSION birds fixed in a stereotacticapparatus while drops EARLIER MODELS FOR ESTRILDID of water were applied to several points in the DRINKING ” mouth and pharynx. These films show that the The double scoop model proposed in this study choana partly closedand the glottis did not close for P. guttata does not support the drinking at all when water was applied at the lingual base. mechanism proposed by Immelmann and Im- But two other reactions were clear: first, the lar- melmann (1967). These authors assumed water ynx was pulled rostrad underneath a fold of in- intake was caused by esophagealsuction result- tegument of the lingual base; second,strong pro- ing from peristaltic movements. Although peri- tractionsand retractionsmoved the dropscaudad. stalsis indeed occurs, such a mechanism is im- The glottis also did not close if the protracted probable for two reasons. First, there are no tongue was kept fixed, and so much water was musclesto enlarge the esophagus.Second, P. gut- dropped upon the lingual base that it began to tata drinks with a wide open beak which is not run into the trachea. This water was blown out completely immersed. Thus even if an area of by powerful exhaling. lower air pressuredevelops due to peristalsis of DRINKING PERFORMANCES the esophagus,air will be swallowed instead of water. The averagewater dosetaken per immersion cycle A secondgenerally acceptedopinion about es- was calculated by dividing the measured volume trildid drinking is also not confirmed by the pres- of water ingested per bout by the number of im- ent study: e.g., Wickler (196 1) and Immelmann mersion cycles that was seen on the films. The (1965) suggestthat Zebra Finches drink by suck- average was determined from 22 filmed bouts. ing in a pigeon-like manner. This requires further The water dose taken per cycle was somewhat discussion. It has been proposed that the drink- larger in the Zebra Finch (0.024 ml, SD = 0.005, ing mechanism of the pigeon (Columba livia) n = 12) than in the BengaleseFinch (0.021 ml, SD = 0.005, IZ = lo), but the difference is not significant (P > 0.05 ANOVA model II Sokal ml/s .1O-2 and Rohlf 198 1). The averagedaily water intake, 8- the average water intake speed, and the average n drinking speed are listed in Table 1. The two (u 6. 4 0 speciesdrink about the same amount per day in _ our study. The average water intake speedof the P 2‘ 4 P Zebra Finch is about two times higher than that .E of the BengaleseFinch. Becausethe Zebra Finch G - is able to swallow the water during intake, its c7 22 P average drinking speed is 10 times higher. Average drinking speedsfor drops of varying sl 4 P 7 I I I I I I I I, 1 volumes are illustrated in Figure 18. This figure .02 .04 .06 .08 0.1 clearly showsthat the drinking speedof the Zebra volume of water drops ml Finch increaseswhen drops increasein size, while the drinking speedof the BengaleseFinch is rath- FIGURE 18. Differencesin drinking performance of the Zebra Finch and the BengaleseFinch. The graph er constant at a low level. Finally, these data illustratesthe relation between drinking speed(ml/set) show that both species are quite able to drink and drop volume for the Zebra Finch (circles)and the small drops. BengaleseFinch (triangles). DRINKING MECHANISMS IN ESTRILDIDAE 23 operates like a double suction pump. Zweers for water intake. Thus far, no clear parallels can (1982a) summarizes this mechanism as follows be seen that make it possible to define tip up (p. 3 13): “As a result of the retraction of the drinking as based upon one general behavioral tongue in the mouth (acting as a piston in a cyl- mechanism, other than that this is a two-step inder) low air pressure develops in the buccal mechanism-one for water intake during im- cavity and water is sucked into the mouth. Sec- mersion and one for swallowing water during tip ondly, lower air pressuredevelops in the pharynx up-each accomplished by different mecha- as a result of a depressionof its floor, so that the nisms. water in the mouth is given a momentum cau- dad, by which it is forced over the larynx into DIFFERENCES BETWEEN THE TWO SPECIES the esophagus.Neither peristaltic action, nor an The major differences in drinking behavior be- alternative lower air pressurearea is recorded in tween the tip down, mono draught drinking P. the esophagus.The collection of the swallowed guttataand the tip up, poly draught drinking L. water at the lowest place occursby gravity.” This striatahave been describedin the literature (e.g., study indicates that the pigeon’s drinking mech- Immelmann and Immelmann 1967). These are anism is effective only if the gape is very small. confirmed at the level of scene analysis. How- In contrast, the beak of the Zebra Finch must be ever, one level of organization lower, the differ- wide open to allow the tongue to make the scoop- ences are much smaller. The basic behavioral ing movements neededfor fast drinking. Further, elements of tongue and larynx movements that anatomical differencesbetween P. guttataand C. make up drinking behavior are quite similar in livia make it rather improbable that these birds both species.For example, the lingual scooping drink by similar mechanisms. motion that causesthe transport of water to the Whether Zebra Finches drink like honeyeaters, lingual base is basically the same in both species. as suggestedby Fisher et al. (1972) is still un- The difference is that P. guttata protracts its known since the drinking mechanism of these tongue without elevating the lingual alae. Clear- birds has not been analyzed on a functional-an- ly, there is no need for such an elevation: there atomical level. The drinking mechanism of Lon- is no water on the lingual base that might run churaseen in the present study, involving two back into the water box, becauseeach water dose separate sequences of two different kinds of is immediately transported further into the scoops,has not previously been describedin birds. esophagus.For the same reason,P. guttatais able A few studies described below specify tip up to drink with a much wider gape than L. striata. drinking, but these descriptions point to mech- A further striking similarity occurswhen the two anisms other than those proposed here for L. speciesdrink very small drops. When P. guttata striata. drinks small drops, it opens its beak, quite like According to White (1970) the chicken (Gal- L. striata,but over only a small distance, and lus gallus) collects water on the lingual base by the water transport to the lingual basetakes place quick rostro-caudadmovements. In the swallow- via the same sort of lingual scooping as in L. ing phasethe water runs laterally along the larynx striata.This similarity explains two features.First, into the esophagusby gravity. Further, in con- intake speedsin the two speciesare equal when trast to the observations for L. striata, Schon- they drink small drops. Second, L. striatais, de- holzer (1959) statesthat the Black Swan (Cygnus spite being a tip up drinker, quite able to “suck atratus)stretches its neck and points its bill into in” small water volumes by applying the same the air, which probably causeswater to run into lingual scooping actions found in P. guttata. the esophagusby gravity without tongue or lar- The small differences in the anatomy of the ynx movements. A model for drinking in the two speciesmay relate to small advantages in- Mallard (Anasplatyrhynchos)has been proposed herent in each of the two kinds of drinking. The by Kooloos and Zweers (1989). These authors anatomical differences and their assumed ad- conclude from a quantitative study that water vantages are: L. striatahas a somewhat smaller transport through the mouth is accomplished by mass of glands in the lingual base so that L. capillarity and pressuredifferentials in two small striatamay easily pull the larynx underneath the tubes and two chambers, respectively. Delicate integument to close the glottis. This motion is lingual motions change the Mallard’s mouth, not neededin P. guttatasince the arytenoids close which is built to expel water, into a mechanism the glottis as soon as a water dose arrives. In L. 24 J. HEIDWEILLER ANDG. A. ZWEERS striata, this reflex pattern is missing, but a large no reason to consider galliform drinking to be a mass of water can neverthelesscollect at the lin- specialized or highly compromised mechanism. gual base. Thus the alternative way of glottis clo- Therefore the main lines of McLelland’s (1979) sure, via an integumental fold, also servesin L. description-based on White’s (1970) analysis- striata to enlarge the space for collecting water. may preliminarily serve as a starting point for Further, the many large palatal papillae of L. an ancestral mechanism for passeriform, e.g., es- striata may be an advantage because they in- trildid, drinking. creasesurface area and keep water on the lingual Although further functional-anatomical anal- base by adhesion. In contrast to L. striata, P. ysis is needed, White’s description envisions lin- guttata has only a few small palatal papillae. This gual retraction as the main causefor the transport enablesthe larynx to scoopwater along the palate of water into the pharynx, while laryngeal re- easily. traction-comparable to what has been called “properistalsis” in this study-serves for trans- HISTORICAL POLARITY IN AVIAN port into the esophagus.There is no indication DRINKING MECHANISMS of any lingual or laryngeal scooping. However, To allow integration of the proposed mecha- it is clear that once a scoop-like element has been nisms into an evolutionary context, ancestral developed at the lingual tip, this element is a drinking mechanisms need to be known. Unfor- clear preadaptation for the lingual scoopthat op- tunately, we know of no relevant studies. There- eratesin both estrildid drinking mechanisms ex- fore the following approach appears reasonable. amined here. Cracraft (1988) arguesin a review that it is gen- erally acceptedthat the galliforms are one lineage HISTORICAL POLARITY IN ESTRILDID of the earliest dichotomy in the monophyletic DRINKING MECHANISMS Neognathae (e.g., Sibley and Ahlquist 1986). The differencebetween the two kinds of drinking Cracraft also showsa summarizing dendrogram reported here may be explained as a difference in which all avian orders-including the Passer- in behavioral complexity. The two mechanisms iformes-radiate from the next point of bifur- are basically similar in their two main behavioral cation, except possibly the Anseriformes (but see elements: lingual scooping and laryngeal scoop- Olson 1985). If cladograms reflect genealogy, as ing. The main differenceis that in tip up behavior cladists suggest,Galliformes and Anseriformes these elements occur in two separatesequences, are ancestral to Passeriformesand hence to Es- involving different kinds of motion cycles, trildidae. Bock (pers. comm.) concludes that es- whereas in tip down behavior both behavioral trildid drinking mechanisms may have devel- elements are incorporated in one single type of oped from galliform-like drinking becauseof the motion cycle, which is repeated many times. In relative rarity of the estrildid mechanisms. If the L. striata a seriesof lingual scoopingcycles trans- rarity and genealogy assumptions hold the con- ports water to the rostra1pharynx during the im- clusions point in the same direction. In order to mersion phase, and next a series of laryngeal make progressin the explanation of the devel- scoopingplus properistaltic motion cycleswhile opment of a drinking mechanism, the only op- the beak is tip up squeezesthe water into the tion is to assume that the evolution of drinking esophagus.Neither glottis closurenor esophageal behavior in all ordines, e.g., Passeriformes, be- peristalsis is involved. In P. guttutu a lingual gan from a mechanism close to either galliform scoopmoves a water dose into the rostra1esoph- or anseriform drinking. agusin each motion cycle; it is immediately car- Anseriformes have a highly specializedfeeding ried into the rostra1 esophagusby a laryngeal apparatus for straining. Although a tip up drink- scoop, while the glottis closes, the secondary ing mechanism is used, it is very complex. A choana narrows and esophagealperistalsis trans- delicate lingual motion pattern modifies the ports the water dose directly into the crop. mouth-built to expel water-into a mouth that It is apparent that the main behavioral ele- keepswater in (Kooloos and Zweers 1989). How- ments, which occur separately in L. striata, are ever, an ancestralestrildid drinking behavior may closely connected in P. guttata. Further, behav- not have been derived from the anseriform ioral elements from quite different patterns, such drinking mechanism, becauseof its highly com- as glottis closureand esophagealperistalsis-part promised and specialized design. So far, there is of respiration/vocalization and ingestion, re- DRINKING MECHANISMS IN ESTRILDIDAE 25 spectively-are found in separate phases in L. be manipulated into a position for being either striata, but, in P. guttata are seento be integrated crushed or cut open (Ziswiler 1965). Only the into one motion cycle. Generally speaking, such lingual tip can perform this action. Development an increase in complexity may occur as a result of a seedcupcomposed of numerous keratin hairs of decoupling and recoupling of behavioral ele- at the lingual tip without doubt creates a very ments. First different kinds of behavioral ele- useful element for seed manipulation. Previous ments occur successively in a chain of subse- sections have shown that the development of quent motion cycles (e.g., L. striata), and then such a lingual seedcupmay serve as an anatom- these behavioral elements are found recoupled ical preadaptation for drinking. (Homberger and functionally present in one highly integrated [ 19801 arrived at a similar conclusion for the pattern ofjust one motion cycle (e.g., P. guttata). development of drinking mechanisms in par- Thus the tip down mechanism is of a much higher rots.) There is apparently no real need for drink- level of complexity (i.e., of integration of func- ing by lingual scooping.But since both the scoop tionally meaningful behavioral elements per unit element and the required musculature for scoop- of time) than the tip up mechanism. Such an ing are available, the behavioral ability to scoop increase in complexity is in itself an argument water lingually may have developed neutrally. that indicates historical polarity if the anatomical Once present, small advantages in terms of im- elements do not differ. An example of decoupling proved water intake may have fixed the lingual and recoupling of behavioral elements is offered scoop mechanism, and moreover, extended the here (see Roth and Wake 1989). Therefore, it is niche: the lingual scoopmay have improved the concluded that the tip down mechanism de- ability to drink the small drops ofwater on blades scribed here is derived from/advanced in com- of grassafter rain, or alternatively, to ingest dew- parison to the proposed tip up mechanism. drops. This capability may have generated an energy gain by decreasingtravel costs to water, thus increasing time available for feeding. This EVOLUTIONARY SCENARIO FOR narrative may serve as an example of the theme ESTRILDID DRINKING of evolutionary changecalled “possessingthe be- havioral capacity to utilize a new ecological op- Based on the analyses presented, the following portunity” (Lauder et al. 1989). scenariois proposed(Fig. 19) and open to further The next step in the scenario is the develop- testing (cf. methods in Bock 1985). The ancestral ment of tip down drinking. Unfortunately nei- estrildids are assumed to have lived in humid ther functional anatomical nor performance woodlands, some invading nearby open grass- analysesare available regardingtransport of seeds lands bordered by semiarid and arid areas (Im- through the pharynx. But clearly the develop- melmann 1965). This assumption is supported ment of any anatomical element or motion pat- by the fact that all recent Estrildidae feed on grass tern that speedsup the transport of husked seeds seeds(Ziswiler 1979). The ancestralestrildids are through the pharynx is subject to strongpredator assumed to have fed upon rather small seedsby pressureselection because of the long day of feed- pecking, and to have drunk by tip up behavior ing in rather open fields. For example, devel- comparable to the galliform-like mechanisms in- opment of a mechanism that scoops a husked dicated above as the ancestral ones. Selection seedfrom the palatal cavernousbody and scrapes favoring anatomical elementsthat enable fast seed it off onto the caudal palatal papillae is a first eating must certainly have occurred,due to pred- option. One obvious element that could serve ator pressure on ancestral estrildids feeding in this goal is the rostra1cricoid edge. Once such a relatively open fields (Immelmann 1965, Im- mechanism has developed, it too is of course a melmann and Immelmann 1967): proper diges- clear preadaptation. This preadaptation later tion of the small seeds of Gramineae requires makes the laryngeal scoop available for use in that they be huskedbefore being swallowed. This double scoopdrinking, which allows water to be assumption is supportedby findings showingthat swallowed 10 times fasterthan in tip up drinking. almost all recent Estrildidae husk grassseeds (cf. The behavioral pattern for double scoop drink- Ziswiler 1967, 1979), and that husking theseseeds ing could have developed neutrally. But, once is a very time consuming act (Morris 1955). A available, tip down drinking would have strongly first requirement for seedhusking is that the seeds supported the extension of the feeding area for 26 J. HEIDWEILLER AND G. A. ZWEERS

Extension and Selective change Preadaptations from Primarily neutral change of habitat in Feeding selection on change in mechanisms Feeding mechanisms Drinking mechanisms 4 Double scoop (Tip down) Semi-desert Rostra1 cricoid edge 1 Super transport to esophagus Single scoop I 4 (TiD UD) Grasslands Lingual seed cup 4 /L- Husking seeds in mouth

/ f Woodlands Galliform-like pecking Galliform-like tip up f / - _ drinking

Ancestral estrildidae

FIGURE 19. Diagram of a tentative evolutionary scenario for estrildid drinking mechanisms in relation to the development of feeding mechanisms under selection from economizing and predator pressure.Increased behavioral complexity occurred primarily neutral by de- and recoupling of behavioral elements. Functionally meaningful patterns may secondarilyhave been fixed by selection on advantagesin extended and subsequently changed habitats such as drinking small drops, drinking upside down, economizing water intake, decreaseof traveling costs to water sources,decrease of predator pressureat waterholes.

three reasons: first, drinking places where a bird similar basic behavioral elements. However, the must drink upside down now became accessible tip down mechanism is much more complex. (as observed in Poephila species drinking from Here, all behavioral elements plus some extra cattle troughs; Immelmann 1965). Second, due elements from different patterns are integrated to the higher rate of drinking for larger dewdrops, in one motion cycle, whereasin the tip up mech- that source may meet their water needs; less trav- anism these elements occur in separate phases el from feeding area to water would, again, reduce and patterns. Increase in behavioral complexity energy losses. A third advantage of the double is in itself an argument for historical polarity, if scoop mechanism is the fact that predator pres- the morphologies are similar. Our anatomical sure at water holes in semiarid areas would be analyses strongly support this argument. Thus, diminished strongly. However, it should be re- tip down is taken to be derived from tip up drink- marked that Zebra Finches need additional water ing in Estrildidae. The literature provides argu- becausethey spendmuch time bathing. This does ments that estrildid tip up drinking is derived not falsify the scenario proposed, becausebath- from chicken-like ancestral tip up drinking. An ing may decreaseif water becomes scarce.Fur- evolutionary scenario is developed here, based ther ecomorphological and function morpholog- upon strong selection on anatomical elements ical analyses are clearly needed to test these as- which serve to speed up specialized feeding on sumptions. These analyses should include the seedsof Gramineae, due to predator pressurein Estrildidae living in the dry parts of Africa, to open fields. It has been shown that some of these test whether their lack of tip down drinking is elements are clear preadaptations for specialized due to their more insectivorous feeding habits, drinking mechanisms. The behavioral patterns as suggestedby Immelmann and Immelmann involved may have developed neutrally by de- (1967). Again this narrative scenario is felt to be coupling and a different but functionally ade- an example of behavioral capacity to use new quate recoupling of behavioral elements. But the ecological opportunities (Lauder et al. 1989). mechanisms, once available, allowed a strong To sum up, the evidence suggeststhe follow- secondary extension of the feeding area. Selec- ing: tip up drinking and tip down drinking are tion may then have fixed the increased behav- different behavioral patterns comprising highly ioral complexity. DRINKING MECHANISMS IN ESTRILDIDAE 27

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KFCANENBURG-VOOGD. 1977. Mechanics of feed- HO M. hyoglossisobliquus ing of the Mallard (Anus platyrhynchos L.; Aves; H-I- M. hyotrachealis Anseriformes). Contrib. Vertebr. Evol. 3:1-l 10. HVL M. hyovalvularis pars lateralis HVM M. hyovalvularis pars medialis IM M. intermandibularis INF Infundibulum La Larynx APPENDIX LPG Lateral pharyngeal groove LIST OF ABBREVIATIONS LI Gl. lingualis inferior LSA Gl. lingualis superior anterior LSp Names are in Latin exceptbony, cartilageousand Gl. lingualis superior posterior some integumental elements. MA Gl. mandibularis anterior AL Ala lingualis Mn Mandibula A0 Gl. anguli oris MP Gl. mandibularis posterior BH Basihyal MR Median raphe BL Basis lingualis Mx Maxille CA Gl. cricoarytenoidea OPG Oropharyngeal groove CB Ceratobranchial PA Procricoid area cc M. cutaneus colli PAL Palatinum CCL Corpus cavernosum linguale PB Pharyngobrancheal CCM Corpus cavemosum maxillare PG Paraglossal CG M. ceratoglossus PGr Pharyngeal groove CH M. ceratohyoideus PIE Gl. palatina anterioris intema et ex- ClV M. claviculocricoideus tema Cr Cricoid PM Pterygoid muscles (jaw adductors) CI M. cricointerarytenoideus (larynx PP Gl. palatina posterioris closers) RPL Ruga palatina lateralis CrA M. cricoarytenoideus (larynx open- RPI Ruga palatina intermedialis ers) RPM Ruga palatina medialis CrH M. cricohyoideus SC Secondary choana cu Cartilago urohyalis scu Seedcup DPF Papillae pharyngeales dorsales (dor- SH M. serpihyoideus sal pharyngeal flaps) SP Gl. sphenopterygoidei EB Epibranchial StH M. stylohyoideus GH M. geniohyoideus TLD M. trachealis lateralis dorsalis GHC M. geniohyoideus pars caudalis TLV M. trachealis lateralis ventralis GHR M. geniohyoideus pars rostralis TMn Tomium mandibulare Gl Glottis Tr Trachea GM Gl. maxillaris UH Urohyal GP M. geniopharyngealis VPF Papillae pharyngealesventrales (ven- HG Hypoglossal tral pharyngeal flaps)