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