THE CONDOR

A JOURNAL OF AVIAN BIOLOGY

Volume 97 Number 2 May 1995 UNlVflRSlTyOF IDAHO The Condor 9’71297-324 0 The Cooper OmitholqticalSociety I995

MAY3 0 8% FILTER FEEDING IN (PHOENICOPTERUS RUBER)’ LIBRARY

G. ZWEERS, F. DE JONG AND H. BERKHOUDT Institute of Evolutionary and EcologicalSciences, Van der Klaauw Laboratory, Leiden University, P.O. Box 9516. 2300 RA Leiden. Netherlands

J. C. VANDEN BERGE NorthwestCenter for Medical Education, Indiana University,School of Medicine, Gary, IN 46408

Abstract. We propose a model of filter feeding in (Phoenicopterusr. ruber) and Greater Flamingos (P. r. roseus)that is based on a description of the oropharyngeal integument, using SEM and radiography,and analysisof kinematics and performances.Our model extendsthat of Jenkin (1957). We proposea lingual back-and-forth pump, that causes a lateral in- and outflow of water. Outflow of water is manipulated by directing water more distally to passsomewhat larger lamellar meshes,or more proximally to passslightly smaller meshes.Performance analysisof filtering monotypic suspensionsof seedsranging from 0.1 to 10.0 mm cross-sectionshows peak performancesat 2-4 mm. Sixessmaller than 0.5 mm and larger than 6.0 mm are not filtered. Performance analysisof filtering suspensionsof two seed types shows that discrimination capacity, though not perfect, is accurate if food of preferred size is offered. In addition to touch, taste also controls discrimination. We present a provisional morphospace of avian filter feeding mechanisms derived by nomological deduction from an initial pecking mechanism and develop in this domain preliminar his- torical-narrative hypothesesof the of avian filter mechanisms.The morphospace connects chicken-like pecking, considered as the initial type of feeding, through initial probing, to five categoriesof filtering. These categoriesare: accidental filtering (as in Phal- aropus),ram filtering (as in Pachyptila), grasp-pump filtering (as in Anser), (inverted) back- and-forth pump filtering, causinga lateral in- and outflow (as in Phoenicopterus),and through- pump filtering, causingdistal inflow and proximal outflow (as in Anus). The evolutionary hypotheses consider probing as developed from ancestral pecking, and filter feeding as branching early from that route.

Key words: Filterfeedingmechanism;jlamingo; Phoenicopterus tuber; morphology;mor- phospace;evolution.

INTRODUCTION ported through the mouth by a “catch and throw” The in flamingos (Phoenicopterus) is re- mechanism. Smaller-sized particles like insect markably well adapted to gather large quantities larvae and seedsare filtered from the water. Very of small food organisms by filtering in shallow small items such as micro-organisms are gath- lagoonsand lakes. However, relatively large par- ered through scrapingtop soil and ingestingmud, ticles are grasped with the beaktips and trans- or by very specialized filtering. Present knowledge about the mechanism of filtering is based on three sources:(1) anatomical dissectionof the integument of mouth and tongue, ’ Received 18 October 1994. Accepted 3 1 January (2) analysis of food present in the environment 1995. and that found in stomach-contents, and (3)

12971 298 G. ZWEERS ET AL. studiesthat detail ecobehavioralobservations and Allen (1956) and Jenkin (1957) differ as fol- analysesin the field and in zoos. However, direct lows. Allen assumed that a seriesof processesat measurements of filter kinematics by film-anal- the back of the tongue are the major filtering ysis and performance analysis of filter capacity elements, while the outer marginal lamellae on are unavailable. the upper mandible have a secondaryfunctional Models for filter mechanisms in flamingos are role. Jenkin, however, assumed that the lingual proposed by Allen (1956) and Jenkin (1957) and processesserve for food transport, while the large subsequentauthors refer to these studies (see re- outer marginals in combination with the smaller view in Kear and Duplaix-Hall 1975). Allen submarginals of the upper mandible are the only (1956:89) described filtering as follows “(flamin- filtering elements. Both authors describe the jet goes) . . . dragged their mandibles through the streams at the base of the beak and the back- mud and water, rocking their heads from side to and-forth stream of the water along the lamellae. side. . . pumping movements of the gular region, Sanderson and Wassersug (1990, 1994) con- and the twin jets of muddy water that were shot cluded that, apart from a preliminary paper of outward from the comer of the mouth [were ob- de Jong and Zweers (198 l), a functional anatom- served] . . . Certainly a suction was being set up ical model for filtering based on direct measure- in the mouth opening . . . evidently a combina- ments from kinematics and filter capacity is still tion of a pumping and a sucking through the lacking. The current study is designed to under- opening of the gullet. Then, as the upper man- stand the filter mechanism from cinematic anal- dible clamped shut, streams of mud and water ysis, to measure performances of filtering of food were found forced outward, certain portions be- particles under different circumstances, and to ing retained within . . . processesalong the upper determine the specific integumental adaptations edge of the tongue . . . with an additional strain- for filter feeding. Such an analysis requires de- ing effect from the lamellae on the mandibles.” tailed description of the oral cavity and oro- Allen also writes that these eat mud and pharyngeal . Therefore we will extend that small molluscs are sieved from the mud in Jenkin’s (1957) careful description of the integ- the same way. ument of the mouth. In a separatestudy we will Jenkin (1957) proposeda different mechanism address how the pump and filter are driven by for filtering. She developed a reconstruction of muscular actions, what specific adaptations the the filter mechanism by identifying the anatom- muscle-bone apparatuses of jaws and tongue ical elements that are possibly responsible for have, and how they relate to the evolution of exclusion (to keep from entering the mouth) and avian filter feeding systems. for filtering (to keep within the mouth). There- Filter feeding has also been analyzed in several fore she compared sizes of the grit particles taxa of and Procellariidae. The filter sieved. She estimated the functional mesh-size mechanism in Mallards (Anusplutyrhynchos) has of the filter and concluded that neither the inner been described (Zweers 1974, Berkhoudt 1977, lamellae of the upper mandible nor those of the Zweers et al. 1977, Kooloos et al. 1989). Van der lower mandible contribute to the filter process. Leeuw and Zweers (1994) analyzed filter feeding Moreover, Jenkin stated that the idea that only in geese.Morgan and Ritz (1982), Harper (1987) the outer marginals serve as filter must be re- and Klages and Cooper (1992) analyzed filtering considered: “The filter differs from the previ- in prions (Procellariidae). Feduccia (1976, 1978, ously assumedby having spacesbetween the up- 1980) and Olson and Feduccia (1980a, 1980b) per hooks and leaflets subdivided by submargin- proposeda filter mechanism for the extinct Pres- als and the lower outer lamellae” (1957:466). byornzk Rubega and Obst (1993) suggestedthat The meshes produced in this way allow the fil- surface tension feeding in phalaropes is a poten- tering of particles larger than 0.5 mm. Jenkin tial step in the evolution of avian filter feeding. postulated that the exclusion of particles larger We intend to integrate presentknowledge of these than 4 mm occurs by manipulating the gape. systems by developing a preliminary morpho- Rooth (1965) confirmed Jenkin’s ideas, and he space of avian filter feeding mechanisms based added a second type of filtering by which parti- on maximizing the avian pecking mechanism for cles do.5 mm can be filtered. In this mechanism filter feeding requirements, following the meth- the beak is presumedto be closedwhile the tongue odology of Zweers (199 1a, 199 1b) and Zweers et pumps water through the filter, the water being al. (unpubl. ms.). Provisional evolutionary hy- expelled at the base of the beak. pothesesfor the development of avian filter feed- FILTER FEEDING IN FLAMINGOS 299 ing mechanisms are then developed using a mod- The birds were filmed while feeding from a ification of the methodologies of Baum and Lar- homogenous suspension of seeds.Filter feeding son (199 1) and Losos and Miles (1994). was analyzed by a frame-by-frame analysis. For the kinematic analysis the terminology of Zweers (1982) was used. We were not allowed to phys- MATERIALS AND METHODS ically mark the birds, but the following points of NOMENCLATURE, DISSECTION, AND SEM identification were used (letters refer to Fig. 1): We adapt the systematic nomenclature of Kear a) tip of the lower mandible; b) tip of the upper and Duplaix-Hall (1975) and the anatomical no- mandible; c) a spot halfway along the lower man- menclature of Baumel et al. (1993), Baumel and dible; d) distal tip of the nostril; e) center of the Witmer (1993) and Vanden Berge and Zweers eye; f) intersection of an arc from e) and the (1993). We dissectedtwo skulls and four heads silhouette of the head; g) fronto-nasal border of (two fresh) of adult specimens of the Caribbean the cover; h) center of the seed kernels; (Phoenicopterusruber ruber L, 1758), i) the most ventral projection of the retracted and one skull and two heads of the Greater Fla- tongue in the throat; j) intersection of an arc from mingo (Phoenicopterusruber roseusPallas, 18 11). c) and the bony silhouette of the lower mandible; The study of lamellae and other integumentary k) intersection of perpendicular from i) at the structures, e.g., taste bud outlets, by scanning line c/j. electron microscopy and pontamine skyblue, fol- These points of identification allowed mea- lows techniques described by Berkhoudt (1976, surement of the following parameters: 1) gape, 1977). as the distance between the tips ofthe mandibles; 2) dorso-ventral motion of the tongue; 3) rostro- caudal motion of the tongue; 4-l 1) represent the EXPERIMENTAL ARRANGEMENT X- and Y-coordinates of the identification points Conditioning. Specimens borrowed from the at the eye (4, 5) the fronto-nasal edge (6, 7) the Avifauna Zoo (Alphen aan den Rijn, Nether- tip of the upper and lower mandibles (8-l 1); 12) lands) of the Caribbean and the angle (cy)of upper mandible and skull; 13) were available for close-up, high-speed filming the angle (p) of lower mandible and skull; XY- in the lab. We transported the birds following coordinates of kernels (h). techniques described by Sprunt (1975) and The dorsoventral motion of the tongue was Sprunt and Crego-Boume (1975). Birds were kept measured by placing a cardboard model of the in a concrete basin of 370 x 120 x 16 cm. One bony lower mandible over the silhouette of the half of the basin was covered with 10 cm sand lower mandible at each frame measured. Then and the other half was filled with water at 10-l 5 the ventral silhouette-line of the bony mandible cm depth (Kear 1974). The backwall was tiled, was drawn at an XY-table, while a line was drawn whereas left and right walls were hardboard, 1.5 connecting spot c) and the intersection of an arc m high. The front was a wire-netting, 40 cm high. from c) with the bony, mandibular silhouette line Four birds were restrained in a harness in the (i). The length of the perpendicular from the top experimental cages for a few days after their of the bulging skin of the throat on the con- arrival. They were conditioned stepwise to the structed line representsthe dorsoventral motion experimental set-up in the next six weeks and of the tongue. The distance between spot c) and experimentation was done over the next five the intersection ofthe perpendicular and the con- months. The birds eventually were filter feeding structed line representsthe rostrocaudal motion at 90 cm in front of the camera. Tests could only of the tongue. To measure 12) and 13) a line was be performed if birds had other birds nearby. drawn representing the head, connecting the cen- Cinematography. A Teledyne Camera, 1OO- ter of the eye and the intersection of an arc from 125 fps., l/650 set exposure, was used. Birds the eye center and the head silhouette (line S in were protected from the heat of the spotlightsby Fig. 1). The line representing the lower mandible a perspex sheetof 30 x 20 cm which formed one connects the beak tip and the spot on the lower side of the feeding box. The box had an adaptable mandible. The line representing the upper man- width of 7-15 cm. We were able to train only dible connects the upper mandible tip and the one for experimental purposesand therefore rostra1tip of the nostril. all specific data collected is based on observa- Capacity to jilter and to discriminate specific tions of this single specimen. seedsizes. A diet was composedfollowing Ridley 300 G. ZWEERS ET AL.

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FIGURE 1. Identification points and measured parameters for the analysis of filter kinematics. Line a/b = length of gape; Line a/c = axis of the lower mandible; Line b/d = axis of the upper mandible, Line e/f = axis of the head, Angle 01 = intersection of Line b/d and Line e/f, and defines the excursion of the upper mandible on the skull; Angle B is the intersection of Line a/c and the Line e/f, and defines the angular excursion of the lower mandible on the skull; Line i/k = dorsoventral motion of the tongue; Line c/k = rostrocaudalmotion of the tongue. See the text for the key to the letters and numbers.

(1954), Ridley et al. (1955) and Wackemagel well as exclusion of seeds. Mass, volume and (1975). Data from feeding of the Greater Fla- form parameters are shown in Figure 2 and Table mingo were analyzed. Foods and seeds offered 1. These data refer to 40 kernels of each type. in testswere mostly ovoid: cut grass,broken mil- The specificgravity of theseseeds is slightly high- let, poppy seed, millet, grass seed, barley corn, er than 1. This feature and the strong turbulence milo, mung beans, corn, peas, marrow fats, in the suspension caused by the filter feeding pieces of bread. The largest crosssectional seed- assurean almost homogenous offer of seed diameter is taken as a reference for comparison suspensions in the performance tests. Suspen- since that is the major constraint for filtering as sions for kinematic analysis comprise >2,000

TABLE 1. Form and size of seedsoffered in test sessions.Width and depth representthe smallestand largest cross sectional diameters. Averages are taken from 40 particles; standard deviations are in parentheses;SG is specific gravity; particles eaten by filter feeding are shown in the right column.

FOOd Width &Pth Length SG Filter 1. Cut grass co.25 2. Cut grass 0.25-0.50 3. Broken millet 0.52 (0.10) 0.80 (0.2 1) 1.42 (0.20) _ 4. Poppy seed 0.59 (0.09) 0.96 (0.09) 1.23 (0.08) _ 5. Millet 1.45 (0.25) 1.74(0.11) 1.95 (0.30) 1.36 + 6. Grass seed 1.52 (0.11) 2.03 (0.11) 2.87 (0.18) 1.26 + 7. Barley corn 2.77 (0.23) 3.58 (0.26) 8.03 (0.5 1) 1.10 + 8. Milo 2.62 (0.25) 3.94 (0.35) 4.37 (0.28) 1.02 + 9. Mung bean 3.6 1 (0.32) 3.62 (0.30) 4.81 (0.59) 1.20 + 10. Broken corn 3.75 (0.48) 4.99 (0.76) 8.30 (1.14) 1.26 + 11. Pea 8.19 (0.51) 8.84 (0.63) 10.8 (0.62) - 12. Marrow fat 8.19 (0.54) 10.3 (0.99) 11.8 (0.84) _ 13. Bread >lO 210 >102 _ FILTER FEEDING IN FLAMINGOS 301

10 120- 120

@l loo- 10 100 b E - E .G 80- 80 .& 42 - g f 60- 60 $ 9 6 - 9 b 7 ; 40- 7 40 E .m I - -8 8 B 20-

2 3 4 5 6 diameter of seeds in mm FIGURE! 2. Volume and mass of the seedsused to analyze kinematics and capacitiesof filter feeding. Key to the numbers: 5, millet; 6, grassseed, 7, barley corn; 8, milo; 9, mung bean; 10, broken corn. particles of cut grass, 1,000 parts broken millet, sharply ventrad just rostra1to the nostrils. The 1,000 parts of poppy seed, 500 parts of barley, oblong apertura nasalis may be closed by the grassseed, millet, milo and mung bean, respec- large valvula nasalis. The midsagittally keeled tively, 100 parts of large peas, and 50 marrow upper mandible fits closely along the broad man- fats. dibular rims of the deep trough-like lower man- Suspensionsfor performance testswere offered dible. The external shape of the slender distal after 24 hr of food deprivation. The results of part of the upper mandible is straight and flat- the first 60 set of uninterrupted straining were tened dorso-ventrally, with a longitudinal ridge used for analysis. Homotypic suspensionsof 800 particles of millet, grassseed, barley, milo, mung bean and broken corn were used to test filter TABLE 2. The total seednumber in mixtures offered capacities.In addition, single discrimination tests for discrimination testsand the number filtered per 60 sec. Test 3 has been done twice; these data are added were performed by offering mixtures of two seeds in parentheses. (Table 2). The seedsoffered represent form and size of the natural food of Greater and Caribbean Otlkd Filtered flamingos. Mixture numbers numbers Depth 1. Broken millet > 1,000 120 0.8 RESULTS Grass seed > 1,000 1,200 2.0 ANATOMY OF THE ORAL CAVITY AND 2. Poppy seed > 1,000 - 1.0 OROPHARYNX Grass seed > 1,000 - 2.0 Jenkin (1957) reviews the literature on the in- 3. Grass seed 800 (550) 254 (219) 2.0 Barley corn 800 (550) 278 (20) 3.6 tegument of the oropharynx including Owen 4. Grass seed 800 660 2.0 (1832),Gray(1869),MihreEdwards(1869-1871), Milo 800 14 4.0 Weldon (1883), and Shufeldt (1901) and adds 5. Grass seed 800 1,074 2.0 her own accuratedescription. Neither the review Mung bean 800 2 3.6 of Kear and Duplaix-Hall ( 197 5) nor more recent 6. Milo 800 260 4.0 papers add to the work of Jenkin (1957). We Barley corn 800 235 3.6 describe these anatomical areas adding new de- 7. Milo 800 6 4.0 tails from X-ray and SEM analyses. Mung bean 800 - 3.6 Beak (Fig. 3). The deep beak of the Caribbean 8. Poppy seed 4,800 570 1.0 Milo 800 420 4.0 and Greater Flamingo curves as much as 50” 302 G. ZWEERS ET AL.

FIGURE 3. Head of the CaribbeanFlamingo (Phoenicopterus ruber ruber). a. A wide openbeak. The smooth tonguesurface clearly follows the curvatureof the beaks.On the proximalhalf of the tonguelies a seriesof large caudallypointing spines,and the main body of the tongue clearly lies in the trough-like lower mandible. The flexible skin of the throat ventrocaudallyof the lower beak showsa slightbulging. This is the area that will bulge outward when the tongue is retracted. b. Head with closedbeak. Presenceof a seriesof lamellar meshesalong the beaks is clearly visible. Distal meshesdiffer in shapefrom the proximal onesat the curvatureof the beaks.

laterally just dorsal to the tomial edge. Within tongue is very much larger and that it is sup- the lower mandible lies a large and fleshy tongue ported by bilateral, large, semi-circular para- that closely fits along the inner rami. Ventrally, glossalsgiving the ventral tongue-body a non- the external integument of the distal lower man- flexible circular shape. Retraction of the tongue dible is very hard with a few longitudinal shallow requires therefore much spacein the mouth floor, grooves.The lateral walls of the mandible extend but this spaceis not present. However, the flex- caudad with a hard keratin cover, but midven- ible throat skin allows a strong bulging outward trally the skin becomes soft and flexible at the of the throat when the large body of the tongue level of the distal end of the beak curvature. is retracted. Tongueand mouthfloor (Figs. 3,4,5; numbers Dorsolaterally on the tongue lies a bilateral in parenthesesrefer to fig. 4). The lateral, external series of about 20 flexible spines, the papillae appearanceof the tongue follows the curved shape linguae rostralis (5), almost entirely in the non- of the beaks. The large fleshy tongue completely curved proximal part of the beak. The spines fills the mouth when the beak is closed and the point dorsally, slightly caudo-laterally and de- tongue protracted. The flexible distal part of the crease in size from 5 to 3 mm rostra1to caudal. tongue (3) is dorso-ventrally flattened and point- When the beak is in closedposition and the tongue ed, followed caudally by lateral extensions form- protracted, these spines lie along the maxillar ing the lingual bulges (4). Radiograms (Fig. 5) keel (16). During tongue retraction they are in a show that the fleshy proximal portion of the position to sweep along the inner lamellar series FILTER FEEDING IN FLAMINGOS 303

1 2 3 4 5 6 7 8 9 10 11 12 13

kp mouth+- pharynx+

14 15 16 17 18 19 20 21 22 23 24 25 13

bp mouth v pharynx--)

FIGURE 4. Integument of oral cavity and oropharynx. a, b. Dorsal view of the floor of mouth and pharynx. The rami of the lower mandible are spread laterad, c, d. Ventral view of the roof of mouth and pharynx. Key to the numbers: 1) Mandibular nail, 2) Symphysis,3) Lingual tip, 4) Lingual bulges,5) Papillae linguaerostralis, 6) Median lingual groove, 7) Torus linguae, 8) Papillae linguae caudalis, 9) Basis linguae, 10) Rostra1tip of cricoid bone, 11) Larynx, 12) Papillae pharyngis caudo-ventralis, 13) Esophagus,14) Maxillary nail, 15) and 17) Outer and inner maxillary lamellae, 16) Median maxillary ridge, 18) Maxillary tomial edge, 19) Orificis glandulaemaxillaris, 20) Rictus, 21) Papillae pharyngisrostralis, 22) and 23) Narrow and wide parts of internal choana, 24) Infundibulum, 25) Papillae pharyngiscaudo-dorsalis. 304 G. ZWEERSET AL.

FIGURE 5. Scheme of the open mouth. The position and view of the SEM pictures in Figure 6 are indicated by the two rectanglesalong the upper mandibles. Dashed lines indicate the outlines of the fleshy portion of the tongue (1); stippled areasare the curved semi-circular paraglossal(2),the stout basihyal(3) and ceratobranchial (4) (taken from radiograms). The torus lingualis overlies the paraglossale-basihyalejoint. The larynx (5) lies dorsal to the ceratobranchiale,the dorsal black spot is the ossifiedportion of the arytenoid and the ventral spot, the ossified portion of the cricoid. The flexible throat skin (6) will bulge out if the tongue is retracted. The oblique shaded area representsthe pharynx.

of upper (17) and lower (2) mandibles. A shallow over a relatively large distance. The elevated lar- median lingual groove (6) runs between these ynx (11) forms the caudal part of the pharyngeal series of spines. At the end of the series lies a floor. The glottal mound is characterized by a slight elevation of the lingual mass forming a rostrally elevated tip of the cricoid (10) -forming lingual cushion, the torus linguae (7), that runs the caudal border of the lingual base-and bi- along the mouth roof if the beak is closed. lateral longitudinally orientated arytenoids. The Pharynxfloor (Fig. 4). At the caudal end of the caudal border of the larynx is a transverseseries lingual cushion lie two parallel, transverse series of 20 spines, the papillae pharyngis caudoven- of some 20 flexible spines pointing caudad, the tralis (12), marking the transition from the phar- papillae linguae caudales (8). These series mark ynx into the esophagus(13). the entrance into the oropharynx and the tran- Mouth and pharynx roof (numbers in paren- sition from the external tongue into the lingual thesesrefer to Fig. 4). The shallow maxillar keel base (9). Radiograms (Fig. 5) show that this ex- is smooth. Lateral to the keel is a bilateral shal- ternal transition is marked internally by the ar- low groove converging rostrally and ending in ticulation of the median, pronounced basihyal the very hard keratin nail at the beak tip (14). and the curved bilateral paraglossals.The lingual Two conspicuousbilateral seriesof lamellae mn base carries rostrally a lateral series of 10 soft, along the whole beak rim, the outer (15) and caudad pointing spines, the papillae pharyngis. inner (17) maxillary lamellae. The smooth roof The lingual base also showsnumerous transver- changescaudally at the comer of the mouth (ric- sal folds, indicating that the area can be extended tus) (20) into slightly bulging structurescarrying FILTER FEEDING IN FLAMINGOS 305 some 40 caudally pointing spines (21), marking Mandibular lamellae. There is a seriesof blade- the entrance into the oropharynx. This palatal like, serratedmandibular marginals that opposes area ends with a transverse series of 10 spines; the seriesof outer maxillary marginals. As a rule, then follow the narrow (22) and wide (23) parts opposite each 10 maxillary marginals stand 25- of the secondarychoana and the midsagittal, small 28 mandibular marginals. This number decreas- infundibulum (24). Just caudal to the latter runs es to 20 caudally. They are 1. l-l .4 mm high and a second transverse row of 10 caudally pointing each lamella runs from latero-rostra1 to medio- spines, which marks the entrance into the esoph- caudal. Their height decreasesto 0.64.8 mm at agus (13). the curvature of the beak. The inner mandibular Maxillary lamellae (Figs. 3,5,6). Jenkin (1957) lamellae are much less pronounced, run trans- describeslamellar sizes and structuresof several versely, and are less than one-third of the height flamingo species. Our SEM analysis shows the of the lateral marginals. following details. The maxillar rami carry inner Functional meshes.The functional mesh-sizes and outer series of keratin lamellae. The outer in Phoenicopterusruber are formed by the large maxillar lamellae are of two types: large, mar- marginal and the smaller submarginal maxillary ginal lamellae and smaller submarginal lamellae. lamellae in juxtaposition with the marginal man- The following data are from three specimens,the dibular lamellae (Fig. 12). If the beak is closed larger specimen representing the higher values. and the upper mandible tip is pushed against the The large marginal lamellae are again of two lower, a slit of about 2 mm high is left between types. There are 40-50 tooth-like, inward point- the beak rims, equivalent to the height of max- ing marginals along 60-70 mm of the distal illary marginals. The mesh-sizes along the beak straight portion of the maxilla (Fig. 6). Interla- change in size and shape from rostra1to caudal. mellar distances vary from 1.1-1.9 mm. Their The functional mesh-size with the beak in closed height varies from 3.2-4.0 mm, and on the av- position along the distal portion with the tooth- erage it increasesfrom distal to proximal. They like marginals varies considerably: 1.6(height) x are flexible in rostro-caudal direction, but much l.‘l(width)mm (kO.4). The mesh size at the less flexible in lateral direction. curved portion of the beak with the blade-like In the curvature of the maxilla the shape of marginals also varies: 2.0(height) x 0.7(width) theselamellae rapidly becomesblade-like, point- mm (kO.2). ed, thin, and convex (Fig. 6a). There are 60-80 Tuning the gape adjusts mesh-size. The gape of these transversely positioned marginals. They along the straight, distal portion of the beak is gradually decreasein size and disappear.The first almost constant over the full length of that por- 10 blade-like lamellae along the curvature are tion when the beak tips gape to about 3 mm. 3.43.7 mm high, with an interspace of 0.5-1.0 About the first 1.5 mm of such gaping produces mm. an increase of the functional mesh since that is Just medial to the outer tooth-like marginals the height of the mandibular marginals, repre- lies a seriesof 100-l 30 smaller, inner, tooth-like senting the overlap with the maxillary marginals. submarginals. They often show up as a pair of The fact that the marginals rub along each other small teeth behind and between a pair of the by the caudo-rostral shift of the mandible in this larger teeth (Fig. 6b), but this is not a rule (e.g., stageof gaping does not influence the mesh size one or three submarginals may be present per since the lamellae are flexible in rostro-caudal interspace). If two or three submarginals are direction. The other 1.5 mm of such gaping pro- found, often the rostral one is larger than the duces an extra, constant slit of 1.5 mm between caudal one. The height of the largest submargin- the tips of the upper and lower marginals along als per interspace varies from 0.8-l. 1 mm in the the distal portion of the beak. Wider gaping is region of the tooth-like marginals. In the region assumed to be non-functional for filter feeding of the caudal blade-like marginals they are half since much wider distances develop proximally this size and merge more caudally with the inner than distally. This does not allow size discrim- maxillary lamellae. The inner maxillary lamellae ination. are much less pronounced and appear as trans- Taste and touch organs. Jenkin (1957) found versal rows of very small blades. These blades no evidence of taste organsin the beak or tongue. are aligned in rows that run from rostro-lateral However, Bath (1906) described a group of taste to caudo-medial (Fig. 6). buds in the mucosa of the ventral esophagus, 306 G. ZWEERS trr AL.

FIGURE 6. SEM-prints of the maxillary lamellae. a. Two distal, tooth-like, large marginals are shown. Just medial to the marginals lie two pairs of smaller submarginals.Behind these lamellae, more medially are parallel series of the inner lamellae. They lie in both diagonal and transversal series. b. Seven plate-like lamellae are shown at the curvature of the beaks. The submarginal lamellae are present as the most lateral lamella of the inner lamellae. They are positioned in transverseas well as in diagonal rows. FILTER FEEDING IN FLAMINGOS 301 caudal to the tongue, in two bilateral folds sup- protractions and elevated retractions of the lar- ported by the hyoid horns, adjacent to the larynx. ynx. Finally, the papillae pharyngis caudoven- These regions of taste buds have not been ob- tralis sweep the bolus into the esophagus.Often served in (Berkhoudt 1977, 1985), which the bolus can be seen travelling downward as a suggeststhe possibility that their location in fla- swelling even though the bolus may follow an mingos is an adaptation to the inverted posi- oblique course. tioning of the filter mechanism when flamingos The search,filter, transport, and swallowphases filter feed. Further, just proximal to the maxillar each have characteristic, cyclic motion patterns. curvature the orifices of the monostomatic glan- The filter and transport phasesare highly repet- dulae maxillares (gl. palatina anterior; 19 in Fig. itive and merge gradually into each other. Sim- 4) open bilaterally. SEM and rapid surfacestain- ilar patterns are found for seedsranging from 2 ing with pontamine skyblue show that each is to 4 mm in cross-sectionaldiameter. In the next surrounded by about 10 orifices of taste buds section we show that the filter capacity peaks (Fig. 7a). These glandular outlets and taste buds sharply for these seed sizes and the motion pat- are near the bill tips in ducks, as in most birds tern is most clearly visible when millet, grass (Berkhoudt 1977, 1985), which suggestagain an seed, barley corn or milo is filtered. Represen- adaptation of their location to specificfilter feed- tative portions of phaseshave been selectedfor ing in flamingos. Much higher numbers of taste frame-by-frame analysis. bud pores were found in the circumference of the Filter cycle in suspensionsof monotypic seeds openings of the numerous gll. spheno-pterygoi- (Figs. 8, 9). The motion characteristics of the deae, 3 to 6 around each duct-outlet (Fig. 7b). filter cycle derived from filtering barley corn and Dissections of the maxillar, ophthalmic and grassseed are as follows. The frequency is about mandibular trigeminal rami all along the beak 12.8 Hz and the cycle duration about 78 msec. show that directly under the maxillar and man- If the head is kept in the inverted position, which dibular marginals, there lies a dense field of cor- is normal for filtering, the horizontal motions of pusclesof Herbst (also cf., Schildmacher 193 1). the identification points at the lower and upper They are innervated by numerous nerve branch- mandibles are rather small, and thoseat the fron- es from these very large trigeminal rami. tal and the eye are almost zero. However, the vertical motions of these points at upper and KINEMATICS OF FILTER-FEEDING lower mandibles are considerable, while those at Behavioral phasesoffilter feeding. A behavioral the frontal bone and the eye are again almost scene of filter feeding contains four phases.The zero. Thus, the head is rocking each cycle around pattern starts with food searching by a head de- a center near the eye and frontal bone in such a pression and the immersion of the straight, distal way that the beak tips move up and down each beak portion in a nearly horizontal position. The cycle. The amplitude of the upper mandible is head may then be swept sidewayswhile the birds somewhat larger than that of the lower mandible, walk slowly. A filter phasefollows in which cyclic which may be due to a larger independent motion motion patterns of beak, tongue and head pro- of the upper beak relative to the head motion. duce a stream in and out the mouth while par- The generalized picture for filtering the opti- ticles are collectedby sieving. The head is rocking mal food size of 24 mm is derived from rep- each cycle and either one or the other side of the resentative figures as shown in Figure 8. The beak may be pushed in the top soil serving as generalized filter cycle for grassseeds is as follows the leading side for lateral head motion. (Fig. 9). The gape increasesduring the first stages; Gradually the filter phasechanges into a trans- is steady during the second half of stage 2 and port phasein which the food collectedat the level decreasesduring stage3; the beak is kept closed of the beak curvature is transported from the during stage 4. Lingual retraction is very fast mouth into the pharynx, the food having been during stage 1, comes to a halt in stage 2, then left on the lingual base. This occurs by a some- slow protraction occurs in stage 3, followed by what different cyclic motion pattern of mandi- fast protraction in stage4. Lingual elevation/de- bles and tongue while the head is elevating. A pressionoccurs in stages1 and 2, and depression/ swallowing phaseof a few cyclesfollows in which elevation in stages3 and 4. Hence, the lingual the food bolus, collected at the lingual base, is body retracts elevated and protracts depressed. transported from the pharynx into the esopha- The rocking head pushesthe straight portion of gus. This is accomplished by cycles of depressed the beaks (horizontally) down and forward in 308 G. ZWEERS nr AL.

FIGURE 7. SEM-printsof bud orifice. a. Orifice of tastebud around the outlet of the monostomaticgl. maxilla& b. Orificesof tastebuds around the numerousoutlets of the gll. sphenopterygoideae.

stages 1 and 2, and pulls it up and backward in We have observed water expelled as a beam from stages3 and 4. In lateral motion the head is often the beak tip and also by two jet streamscaudally tilted so that the leading beak rim is pushed fur- at the curvature of the beak. Generally water is ther down than the contralateral rim. expelled along the straight, distal portion of the Motion of seedsshows that the water suspen- beak when the beak is or has been closed. sion flows in only along the distal, straight por- Filter cycle in mixtures of d$erent seed sizes. tion of the beak when the gape increases.Water If smaller millet is filtered, the difference from flows out when the tongue protractsand the beak the generalized pattern is that gape amplitude is has been closed in the last part of the cycle. The smaller, 1 mm, while the major water-outflow is outflow of the water is all along the beak rim. directed at the beak curvature. If larger-sized FILTER FEEDING IN FLAMINGOS 309

COLLECTING 1 TRANSPORTING

jI

GAPE ’ 3 frame no FIGURE 8. KinematicsI of filtering. Motion patterns of head, eye, mandibles and tongue while filtering barley corn (upper figure) and mung beans (lower figure). Two types are recognized:collecting and transporting food. See text for explanation. 310 G. ZWEERS ETAL.

Filtering Transporting Filtering single-sized mixed sizes seeds of seeds open Gape

closed L protr. Tongue retr. elev. Tongue depr. in Flow distal Out in Flow prox.

Out Filter

Excluder “P Head rocking down Stages 1 2 3 4 FIGURE 9. Generalizedpicture of waterllow,lingual and gapechanges during filtering and transporting.Left column:Filtering seedsof 1.74.0 mm in crosssectional diameter in monotypicsuspensions. Middle column: Filtering seedmixtures where the largerseed is filteredand the smallerone is washedthrough the lamellar meshes.Right column:Filtering seedmixtures where the largerseed is excludedand the smallerone is filtered. Seetext for explanation. mung beans are filtered the gape is wider, about pro- and retraction mn parallel to lingual ele- 3 mm, while the water flows out along the vertical vation and depression. beak portion and the beak curvature. If a mixture of grass seed and mung bean, or barley corn or milo is filtered, gape changesper cycle are from FILTER PERFORMANCES 1 mm (maximally “closed’ position) to 3 mm Acquisitioncapacity and tolerance.Cut grassand (maximally “open” position). broken millet are pumped in and out through the Transportationcycle. The characteristicsofthe filter while the beak is kept closedduring the full transportation cycle are illustrated for barley corn motion cycle. The birds lose interest very fast in in Figure 8. In Figure 9 the cyclic pattern is shown filtering cut grass.Poppy seed is also readily re- to be almost similar to the filter cycle. Of course, fused as food to filter. All other types of seeds other anatomical elements are set to function are acceptedafter a short period of conditioning. now. The differences are as follows. The cycle The birds show a normal filter motion pattern, if lasts a bit longer, about 86 msec, hence the fre- they filter peas or marrow fats, however their quency is about 11.6 Hz. The rocking motion is motivation decreasesfast. After a few trials they slightly less; the head is elevating, and the gape apparently accept that they cannot filter these motion appears less regular. The water is ex- large seeds;however, they do not changeto peck- pelled mostly along the proximal part of the beaks ing. Pieces of bread are taken by pecking only. at the beak curvature and caudal to it. Lingual Performance measurements are taken in the tol- FILTER FEEDING IN PLAMINGOS 311

640

560

E 480 co : 400 - ’

P 320 &

$ 240 z % .&

160 g 2

I3

2 4 6 8 10 diameter of seeds in mm

FIGURE 10. Graph illustrating the number, mass and volume of seeds filtered per second from a homogeneous monotypic suspension. Key: 1, very small cut grass; 2, cut grass; 3, broken millet; 4, poppy seed, 5, millet; 6, grass seed; 7, barley corn; 8, milo; 9, mung bean; 10, broken corn; 11, pea; 12, marrow fat. erance range that runs from millet to broken corn. lamellae may play a role by fixating the seeds After a few trials the birds refused to filter milo. during water expulsion. The filter capacities for different seed sizes in monotypic suspensionsare summarized (Fig. 10). DISCRIMINATION CAPACITY In terms of numbers of food items filtered, the In the field, flamingos meet much more complex system peaks sharply for millet and grass seed situations then single-sized food items. Carib- which have cross-sectional size-levels of 1.7 to bean flamingos in and Yucatan feed 2.1 mm, respectively. Also, in terms of ingested exclusively on small molluscs (Cerithium) (Klin- volume or mass the system peaks sharply, but gel 1942). Allen (1956) concludesfrom reviewing now the peak has shifted to barley corn and milo the literature on food presence in the natural at size-levels of 3.6 and 4.0, respectively. No environment that the diet comprises (1) small intake is found for very small items as cut grass, molluscs (Cerithiidae), (2) organic ooze consist- broken millet and poppy seeds,or for very large ing of 80% bacteria, algae, diatoms, nematods, items such as peas and marrow fats. molluscs and arthropods, as well as seeds of Almost all seedsmust be suckedin with a beak euryhalin plants like widgeon grass,Ruppia and slightly gaping since the functional mesh width Salicornia, (3) (Artemia), and (4) with closed beak is about 1.6 x 1.7 mm. Only larvae and chrysalids of salt fly (Ephydra sp.). the crosssectional diameters of the smallest seed, Jenkin (1957) mentions from analysis of stom- millet (about 1.4-1.8 mm), allow filtering while ach-contents that Cerithium (5 x 25 mm) and the beak is kept closed. In the case of the larger Artemia (3 x 20 mm) are gathered by filtering, seeds,the water is washed away while the beak while green and blue algae (Spirulina; 0.03 x 0.1 is still slightly gaping. Apparently, not only the mm) and diatoms (0.02 x 0.07 mm) are gathered large marginals retain food, but also the internal by scraping and ingesting organic ooze. Rooth 312 G. ZWEERS ET AL.

18- I , f+O) 9, 2 (800) 16- I

14_ “Filter action” I “Excluder action”

I I

I 6; i&iO) I 8; 14 (800) 4; (ZOO, 8; 423 (800) I I

6;‘(800) 554 (800) s; 6; (500) 7; 20 (550) 7; 235 (800)

::4ff~o(;,ooo), , , 8;jaao)(ocsqo) ,

0.5 1 2 3 4 5 diameter of seeds in mm FIGURE 11. Resultsof the experiments where homogenouslymixed suspensionof two seedtypes were offered for filtering. The graph shows the number of seedsof the type that was most frequently ingested.Numbers in parenthesesindicate the amount of seeds of both types offered. The amount of seedsthat is Eltered from the lesser filtered seed type is also shown. To the left of the vertical line are mixtures shown in which seeds are filtered while smaller seedsare washed through. To the right of this line are mixtures where the larger seed is excluded while the smaller one is filtered. See Figure 10 for the key to the lettering and see text for explanation.

(1965) adds that larvae and chrysalids of the salt ination capacities. These tests were completed fly (Ephydragracilis; slender and 12 mm long) with only a single bird, and could not be repeated form the staple food, while the following taxa are because of demands based on duration of the also filtered: Cerithium minimum, Cerithidea initial loan of the birds and the required physical costata,Artemia salina (5-10 mm), organic ooze conditions for the testing. However, these tests, and small cyprinoids. The Caribbean and Great- although limited, do lead to the following results er Flamingos are able to greatly alter their diet. (Fig. 11, Table 2). Rooth (1975) observed a change in staple food Grass seed is in the peak of filter capacity. from the salt fly (Ephydra)to small molluscs Therefore, the discrimination capacity for grass (Cerithiumsp. and Cerithideasp.) as a result of seed was tested against four other seed sizes: a drasticchange in habitat. Extensive diet changes (1) A mixture of grassseed and broken millet are also recorded in zoo populations. Poulson was offered. There were 1,200 grass seeds (2.0 (D75) mentions that mixed food pellets, dried mm) ingested per minute, but only 120 broken shrimp, and lucem and peppers(Capsicum) suf- millets (0.8 mm). This means that broken millet fice well. Jenkin (1957) mentions that many seeds is suckedin with the grassseed and is then washed of 24 mm are filtered from Cyperus,Medicago, away through the meshespresent when the beak Juncus,Lesia and many Papilionaceae. is closed, while the grass seed is filtered. The We tested whether the birds had size-discrim- outflow of broken millet can only occur along FILTER FEEDING IN FLAMINGOS 313

a

.I mandibu lamell F--T 17 / ““yua ’ / A Distal Mesh B Proximal w/ lingual bulges (4) ..~ I Mesn -=%c--b - - FIGURE 12. a. Main motions of lingual and laryngealelements. Numbers refer to Figure 4. a, b. Generalized picture of the minimal lamellar mesh size along distal (b) and proximal beak rims (c). Maxillary marginal and submarginallamellae as well as mandibular marginal lamellae are shown. the distal portion of the beak, since the proximal and milo (4.0 mm) the bird ingested 235 barley meshes are too small. The system is not perfect corns and 260 milos. Hence, both seeds were since both seed sizes and mesh sizes vary. accepted.This does not mean that the birds can- (2) A mixture of grass seed and poppy seed not discriminate these sizes by tuning the gape. was offered. There were no grassseeds (2.0 mm) They like both types as food and moreover the ingested when it was mixed with poppy seeds barley corn is almost twice as elongated (8.0 mm) (1.0 mm). Poppy seeds are not fully spherical, as milos (4.4 mm). Therefore, the following test but are somewhat crescent-like, therefore they was conducted. may jam the filter since they can stick between (7) The birds apparently preferred not to ac- the maxillary marginals and submarginals if the cept the mung beans. Since mung beans have beak is fully closed.The lamellar filter apparently almost the same size range as milos (3.6 mm vs. cannot discriminate this mixture by filtering. 4.0 mm), both were offered in a mixture. There (3) There were two tests made with grassseed were six milos and no mung beans filtered. Hence, (2.0 mm) mixed with barley corn (3.6 mm). In although with low overall efficiency, the lamellar the first test 254 grassseeds and 278 barley corns filter was used as a filter for milos and as an were filtered. In the second,however, there were excluder for mung beans. This was seen in the 219 grass seedsand only 20 barley corns. Thus film when a specific mung bean was followed the filter mechanism acts in the first test as aJilter entering the mouth accidentally. When the mung for sizes ranging from 2.0 to 3.6 mm, but in the bean touched the lower mandibular lamellae it second the same apparatus operates as an ex- was apparently ‘recognized’ as non-acceptable cluder for the larger barley corns. and worked away by an outflow. This ‘recogni- (4) A mixture of grass seed and milo was tion’ may be done in two ways. First the mung offered. There were 660 grass seeds (2.0 mm) bean is slightly larger (3.6 x 3.6 x 4.8 mm) than filtered, but only 12 milos (4.0 mm). Thus, the the milo (2.6 x 4.0 x 4.4 mm), and second it lamellar sieve works almost exclusively as an has a hard smooth cover. Thus, apparently the excluder for large milo and as a filter for grass generality in this filtering is that barley corn is seed. filtered and mung beans are excluded. (5) From a mixture with mung beans (3.62 To determine whether the jamming ofthe filter mm) there were 1,074 grass seedsingested and by poppy seeds is due to the mesh size of the only two mung beans. Thus, the lamellar sieve filter in the outflow ifgrass seedsand poppy seeds again operated as an excluder for the larger mung are mixed, poppy seeds were also offered in a beans and as a filter for grassseed. To seewhether mixture with milos. Milos (4.0 mm) are much the bird discriminates differences among larger larger than grassseeds (2.0 mm) in crosssection sized seedsby setting the lamellar sieve, the fol- and therefore they may allow a larger mesh size lowing tests were done. in the outflow to let poppy seeds(1 .O mm) pass. (6) From a mixture of barley corn (3.6 mm) (8) The test shows that 570 poppy seedsand 314 G. ZWEERS ET AL.

4 !;... ,7:. .,z:.:.. WATERFLOW & .J .: ’ . GRAINFILTER

I :. ;;;“““’

4 &I

JTRANSPORTING(

GRAINCARRIER 8, BRISTLES

FIGURE 13. Filtering and transporting of seeds. Beak rims and throat are drawn in full lines. The lingual tip, lingual bulges, papillae linguae rostralis, torus lingualis, papillae linguae caudalis, basis linguae and larynx are drawn by dashed lines. Dotted areas represent cavities of mouth, pharynx and esophagus, respectively. The gape is represented by the bar to the left of the beak tip. The arrow above the head represents the rocking of the head. The perpendicular arrows to the left of the throat indicate lingual motion. The vertical bar represents pro- FILTER FEEDING IN FLAMINGOS 315

420 milos are filtered. We conclude that the filter to diameters of about 4.0 mm. The discrimina- is not jammed, and poppy seedsare also filtered. tion studies lead to the conclusion that the la- This may be the effect of the fact that the con- mellar system can act as a filter in the outflow centration of poppy seedswas very high (4,800 and as an excluder in the inflow. Iamellar mesh- items) compared to 800 milos. Thus, about 12% es vary along the beak, therefore size discrimi- of all poppy seedsand over 52% of all milos were nation cannot be perfect. Nevertheless the ac- ingested. Given that the system is not perfect curacy of the filtering system is about OS-l.0 because mesh size and seed size vary, the dis- mm, both for excluding and filtering in the range crimination efficiency is high. of 1.0 to 4.0 mm for the largest cross sectional diameter of elongated, oval-like seeds. Back-and-forth pump causinga lateral in- and outflow. The following model for the filter mech- DISCUSSION anism is proposed(Figs. 9, 12-l 4). A generalized LINGUAL BACK-AND-FORTH PUMP pump-filter cycle is described from Figure 13 CAUSING A LATERAL IN- AND OUTFLOW (upper part). In stage 1 the beak has been closed Filter patterns. Kinematic analysesof films show and the elevated tongue has been protracted. In that filter feeding has four phases (1) head ap- stage2 the beak opens, the tongue depressesand proach including grasping;(2) collecting food; (3) retracts while the torus lingualis is kept against transport of food into the pharynx, and (4) swal- the palate, and as a result the volume of the lowing-each having a specificcyclic motion pat- mouth cavity increases and water is sucked in tern. The filter cycle is characterizedby mutually laterally along the distal beak portion. The rock- tuned mandibular, maxillary and lingual motion ing head rotates and the beak rims are pushed patterns. There are two adjustable features rec- in the suspension. In stage 3 all these motions ognized in the generalized mandibular-lingual proceed and inflow increases.In stage4 the gape motion cycle. First, size and duration of the gape is closing, lingual retraction reverses into pro- are manipulated to adjust the mesh size of the traction, while lingual depressioncontinues. This inflow and outflow to filter preferred food size increases the space at the beak curvature and a in the range of crosssectional diameters of 1.O- flow caudad is generated by the momentum of 4.0 mm, and to exclude other food sizes.Second, the water suctioned in. Outflow occurs since the the amplitudes of lingual motions are manipu- torus linguae is kept elevated. Mandibular mar- lated to adjust pumping capacity. In addition, ginal lamellae and maxillary marginal and sub- the timing of lingual protraction-retraction rel- marginal lamellae sieve the grains. In stage5 the ative to lingual elevation-depression is manip- beak closesvery fast, the lingual bulges protract ulated to direct a portion of the water outflow and begin elevating, causing a strong outflow of along proximal rather than distal lamellae to water along the curvature and distal portion of match mesh size to filtering of smaller food size. the beak. Also distal lamellae sieve the grains. Video recordings of a six-week-old flamingo In stage6 the beak has been closedand the lingual show that kinematics of filter feeding are present, bulges protract and elevate producing a strong including the water pumping (unpubl. data). outflow along the distal portion of the beak so However, at this age flamingos have no lamellae, that grains are filtered. In stage7 lingual motions and filter capacity must be extremely low. We forcefully squeeze out all water. These motions therefore conclude that filter behavior is already end in stage8 and thereafterthe cycle startsagain. present before it is functional. It is clear that in the course of pumping the wa- Tolerance and acquisition testsshow that filter terflow is reversed and that part of it is pumped capacity peaks at crosssectional seedsizes of 1.7 through as a result of its own momentum. The to 2.0 mm in terms of numbers of seedsfiltered; birds apparently are able to manipulate this bal- it is also high in terms of ingested total mass up ance. While surface filtering, the through-flow

e and retraction, and the horizontal bar elevation and depression.a. A generalizedcollecting/filtering cycle shown in 7 stages.The black dot representsa seed. The seed is drawn in and filtered. Small arrows along the beak indicate relative size and direction of the water flow. b. A generalizedtransporting cycle shown in 8 stages.The black dot representsa seed.The seedis transportedinto the pharynx, by action primarily of the papillae linguae rostralis. 316 G. ZWEERS ET AL.

b FIGURE 14. Filtering, washing out, and excluding of seeds.a. The outflow of the food suspensionin a closed beak while filtering. The beak is drawn in upside down position which is normal for filter feeding. The relatively largegrass seed is filtered by direct impact. The smaller, crescent-likepoppy seedjams the mesh sinceit is caught between a large maxillary marginal and a small maxillary submarginal.The small millet is washed out with the water. The size of the mesh is determined by the lamellae. b. The inflow of the food suspensionin a slightly gapingbeak. The relatively smaller grassseed is suckedin with the water stream, while larger milo is excluded. The size of the mesh is now clearly determined by tuning of the gape.

portion may prevail; while feeding submergedin mm, producing a maximal size of about 4 mm densemixed suspensions,the back-and-forth flow for ingested food in the inflow. We assume that prevails (Fig. 14). tuning and restricting the gape is now controlled A remarkable feature of filter feeding is that by the sliding mandibulo-jugal articulation that beyond seed sizes of the range of 1.54.0 mm, lies far rostra1to the quadrato-mandibular joint. filter and discrimination capacities strongly de- This feature may be a specific adaptation of the crease. This may be connected to a specific an- jaw apparatus to filtering staple-food sizes most atomical feature of the jaw apparatus, unknown economically. in any other avian taxa. Exerting mechanical The anatomical studies show that the func- pressureon the frontal bone above the orbit and tional mesh size varies as follows. With closed simultaneously at the same level on the mandible beak distal meshes along the straight portion of opens the beaks to a maximal gape of about 3 the beak are about 1.6 mm wide and 1.7 mm FILTER FEEDING IN FLAMINGOS 317 high. They effectively allow passageof oval-like, and that rejection is performed as early and as crosssections that have diameters not larger than easy as possible in the food processingroute. 2 x 1.5 mm. Along the curvature of the beak Transportthrough the mouth.The transport- meshesbecome smaller, 2.0 mm high x 0.7 mm ing cycle is characterized by the same motion wide. The crescent shape of the marginals re- pattern as found in the filter cycle. The difference ducesthe mesh to be passedeffectively from 0.6- is that different anatomical structures are set to 1.O mm. They allow the washing through of oval- function. In Figure 13 (lower part) the odd num- like cross sections that have diameters of about bered stagesrepresent the transport by papillae 0.6-1.5 mm. However, more caudally they dis- linguae rostralis. The even numbered stagesil- appear at the comer of the mouth. These mesh- lustrate the transport along the lingual torus. In sizes clearly fit to accurately filtering the staple stage 1 one seed of a bolus gathered by filtering food-sizes. In addition they allow the accurate is drawn, the tongue is protracted and elevated. discrimination of preferred sizes in the range of In stage 3 the depressedtongue retracts so that 0.1 to 4.0 mm, assuming that the maximal gape rostra1lingual teeth take the seedcaudad. In stage for filtering is 3 mm. 5 lingual retraction reversedinto protraction and The significanceof the straight distal beak por- lingual depressioninto elevation, so that the cau- tion is important for accurate discrimination of dad pointing papillae slide underneath the seed particular sizes.Sanderson and Wassersug(1990) leaving the seed caudal along the palate. In stage and Bildstein (1993: 13 1) noted that “as a result 7 this procedure is continued. In a next cycle the of nearly parallel curvature, the distance between seedis assumed to arrive at the level of the torus the upper and lower mandibles of a partially linguae as shown in stage2. In stage4 the tongue opened decurved beak varies lessover the length is maximally retracted and slightly depressedso of the bill than it would in straightened bills of that the torus becomes depressedalso. The ele- the same length. A long straightened bill would vated larynx protracts along the palate closing open relatively more near the tip of the bill and the choanae which prevents llow of food and lessnear the basethan doesthe decurved version. water into the nasal cavity. Evidence for this For example, flamingos, which filter-feed . . . are assumption comes from the fact that air bubbles able to do so effectively because strongly de- leave the nostrils at this stage.In stage6 the torus curved bills enable them to spacetheir upper and protracts. The seed is held back by the papillae lower mandibles equally along most of the gape.” pharyngis rostralis while the torus protracts. In This feature producesrather uniform mesh sizes stage 8 the lingual protraction and elevation along the distal portion of the beak. comes to an end, leaving the seedjust caudal to Aspectsof sensorycontrol of jiltering. A so- papillae linguae caudalis at the basis lingualis in phisticated direct-touch system is required to the pharynx (see stage 1). control fine tuning of the gape. The sensorsneed- Filter and transportation cycles occur simul- ed for such a system are present as a network of taneously, but the lingual elements that function corpuscles of Herbst directly underneath each shift caudad during a full behavioral scene of marginal of upper and lower mandibles. A highly filter feeding. First, the lingual bulges are in- developed bill tip touch as found in wa- volved in pumping, hence collecting seeds,and terfowl and probing may be present, but then the rostra1lingual papillae start functioning not yet described. An equivalent control system to sweep the seeds beyond the beak curvature has developed laterally along the tomial edgesin caudad. Thereafter, the torus lingualis and cau- flamingos. da1 lingual papillae transport the seedsinto the Many birds (e.g., waterfowl, and pigeons; pharynx. Our tests therefore confirm Jenkin’s Berkhoudt, 1985; Bath, 1906) have taste buds phoenicopterid filter feeding model (1957), but around the two orifices of the rostral maxillary we extend that model considerably. glands. These glandular orifices lie just caudal to the maxillary nail where the hard keratin changes COMPARISON OF FILTER FEEDING into the soft palatal mucosa. In flamingos, how- MECHANISMS IN BIRDS ever, the position of the maxillary taste buds has Filter feeding has been analyzed for several avian shifted to caudal. This conforms to the point taxa. Morgan and Ritz (1982) proposefor Short- where best food discrimination by taste is ex- tailed Shearwaters(Pufinus tenuirostris) that the pected. The location of that point must meet the bill architecture producesa lower pressurein the demand that all gathered food pass that point mouth while it is pushed through the water, 318 G. ZWEERS ET AL. thereby gathering water and krill. This is called bulges serve as a piston with an open valve al- ‘ram filter feeding’ (Sanderson and Wassersug lowing the water to flow caudad over the lingual 1994). Caudally pointing lingual papillae overlap bulges by its momentum. Kooloos et al. (1989) with rows of caudally pointing, recurved, palatal have studied filter feeding in Mallards, Tufted papillae. As the water is squirted out over a per- Ducks, and Shovelers (Anas platyrhynchos,Ay- manent rictal ridge, krill are trapped by the pa- thya jiiligula, and Anas clypeata, respectively). pillae which are erected by the water outflow. They concluded that filtering occurs by inertial For Fairy Prions (Pachyptila turtur), they suggest impact at the lamellae in Shovelers. However, a gular pouch sucking in and squirting out water, in Tufted Ducks and Mallards, in addition to while krill are being filtered, although the papil- direct impact, they hypothesize that food items lae are much smaller. Harper (1987) and Klages smaller than the interlamellar mesh are centri- and Cooper (1992) confirm that observation and fuged out the main stream by vortices that de- suggestthat suction is createdby the voluminous velop along the lamellae. The filtered particles tongue; water and copepods are collected in a are transported into the pharynx left and right large mandibular pouch that squeezeswater out along (not over) the lingual cushion by a bilateral while copepodsare filtered. series of strong scrapers. Rubega (1990) and Rubega and Obst (1993) Van der Leeuw and Zweers (1994) analyzed describe a prey transport, known as surface-ten- filter feeding in geese (e.g., Anser anser). Filter sion feeding in Phalaropus lobatus. Here, prey is feeding has a collection and a transport phase. transported in &water drop that runs very rapidly During the collection phase, water and food are up along the beak due to surface tension, while graspedand suckedin at the beak tips during bill the beak is opening. Then the mouth closes opening, mainly by a retracting tongue with a abruptly, the throat skin is elevated, water ap- depressedtip and lingual bulges,while the lingual pears at the rictus running distally along the beak cushion is kept elevated, serving as a piston. Wa- to collect in a drop at the tip, and vigorous head ter is largely expelled laterally by bill closure and shakingthrows the drop off. Rubega (pers.comm.) a protracting tongue with an elevating tip. The suggeststhat this type of transport may be wide- food is retained since the tongue pressesit against spread among shorebirds. Gerritsen (1988) pho- the mouth roof, where caudally pointing spines tographed a similar kind of drop transport in add to retainment while the tongue protracts. sandpipers (e.g., Calidris alpina) but did not ob- The transport phaseis characterizedby large ver- serve prey in a drop. Both Zweers (1990) and tical movements of the lingual cushion, causing Rubega and Obst (1993) propose that this type an over-tongue transport of the food and a food of water transport is a potential step in the evo- retainment by the spines in the mouth roof dur- lution from pecking to filter feeding. Feduccia ing protraction. Grass is transported in a similar (1980) and Olson and Feduccia (1980a, 1980b) way. consider Presbyornisas a filter feeding ancestor Comparison of the anatid model with that for of modern ducks starting from an ancestral flamingos shows that flamingo pumping is ba- shorebird stock, based on features such as beak sically a “back-and-forth pump” causinga lateral shape, the large sized proc. retro-articularis and in- and outflow, while the anatids have ‘a grasp additional post-cranial elements as evidence. pump or a through-pump’ causing frontal inflow They consider the line to flamingos diverged be- and lateral outflow. Comparison of the fore Presbyornisappeared. model and the geesemodel showsthat they differ Zweers (1974) and Zweers et al. (1977) propose in pumping and in transporting food. Ducks use for Mallards (Anatidae) a suction pressurepump the lingual bulges primarily as a piston and a in which the tongue draws water in at the beak valve, while geeseuse them primarily to retain tips and expels it latero-caudally along the beak food and to aid in suction. Ducks have a smooth rims. This pump is a “through pump” in which mouth roof, while they scrape the filtered food the water enters at one end and leaves at the laterally along the lingual cushion, which is kept other end. During their elevated retraction, the elevated during filtering; geese,however, trans- lingual bulges and cushion serve as pistons with port the food over the lingual cushion, while cau- a closed valve in the cylinder-like beak so that dally directed flexible spines retain it during lin- the water is expelledcaudally along the beak rims. gual protraction. During development in geese, During their depressedprotraction, the lingual first pecking and then grazing develops by com- FILTER FEEDING IN FLAMINGOS 319 bining a grasp and a headshake, followed by a phospace.(In Figure 15, numbers in parentheses lingual inertial (slide and glue) transport through refer to numbers in the text, and the names the mouth; thereafter filter feeding develops. at the top line refer to the appearance of known filter mechanisms.) We recognize that a func- MORPHOSPACE AND PHYLETIC tional and performance analysis of the filter feed- EVOLUTION OF FILTER FEEDING ing is only known in flamingos and ducks and MECHANISMS not for other filter feeding mechanisms. More- Methodological remarks. Here, we first develop over we restrict the development of the mor- the concept of a morphospace, and then intro- phospaceand of evolutionary hypothesesof avi- duce the correlation that existsbetween the mor- an filter feeding to the following guidelines de- phospace and historical narrative explanations rived from proposalsby Baum and Larson (199 l), (see Bock 1988,199l; andzweers 1991a, 1991b and Losos and Miles (1994): 1) Identification of for further explanation of terminology and meth- integumental charactersin routes that were cru- odology). We initially analyze one (yet unex- cial in the change from pecking to filter feeding; plained) morphologyby deducingit from a known 2) Identification of functional capabilities lead- morphology, transforming the latter through an ing to performance advantages for filter feeding; explanatory theory. The explanatory theory, in 3) Identification of new selective regimes driving turn, is a maximization of a known initial sys- new developments. We first summarize maxi- tem, for the functional requirements of a differ- mization and evolutionary route of the pecking ent system in which the morphology is to be mechanism for probing requirements and then explained. For example, we consider the avian show how filter feeding development may branch pecking mechanism to be the initial system and off from this line. Finally, we show how different then maximize its morphology for the functional types of filter feeding can be deduced and how requirements of a probing mechanism by anal- they may have evolved by increasing intake ca- ysis of the latter for tolerance and performance. pacities and filter specialization. We include here This deductive methodology producesa branch- only the integument, and omit the muscle-bone ing transformation pattern which describes the apparatus and its mechanics. domain of structures of probing mechanisms as We assume that the ancestral avian feeding deduced from a pecking mechanism. By using mechanism was a grasping mechanism (l), like “maximization for certain functional require- that assumedfor Archeopteryx.This mechanism ments,” a polarity is introduced which is purely is characterized by a long beak, teeth along the of a nomological deductive nature. To establish mandibles, and (probably) a prokinetic skull, a correlation between such a morphospace and though less advanced than in modem birds an historical narrative evolutionary explanation, (Btihler 1985). We also assume that the grasping we must consider historical initial and boundary mechanism was a precursorto the pecking mech- conditions. We consider a pecking mechanism anism, the latter is considered as the ancestral to be the “historical initial condition” for the feeding mechanism of modem birds (2). That avian feeding mechanism (Zweers 199 1a, 199 1b, mechanism comprises conical, tooth-less, kera- Zweers et al. 1994). We define certain anatomical tin-covered beaks, and a prokinetic skull. Food and behavioral changes to be “boundary con- is transported by “catch and throw,” comprising ditions”; that is, some changesare permitted and head jerks, as well as by a lingual inertial trans- others are not. For example, we would specify port in which only the tongue moves. That initial that the particular configuration of bones in a mechanism is defined as the de-specialized peck- jaw apparatus is not allowed to change, but the ing mechanism in the chicken (Gallus), i.e., the size, shape, and orientation of the bones would top soil breaking specializations are omitted (7). be allowed to change. Such initial and boundary See Zweers (1990) and Zweers et al. (1994) for a conditions are often vaguely described as “phy- discussion of its ancestry and appearance. logenetic constraints.” A remarkably modifiable feeding design had Morphospace and evolution. Based on the been developed with this mechanism. Zweers methodology as outlined above we summarize a (1990) and Zweers et al. (unpubl. ms.) predicted provisional morphospacefor avian filter feeding, by deduction, and tested, transformation from deduced from a pecking mechanism and hy- initial pecking to initial probing (3), to air/water pothesize evolutionary routes in that same mor- hole probing (4), and subsequently to mud pen- 320 G. ZWEERS ET AL.

Phasianidae Phalaropodidae Procellaridae Phoenicopteridae Presbyornitidae Gal/us Phalaropus Pa chyp tila Anser Phoenicopterus Anas Recurvirostra Puffinus Phoeniconaias Aythya I I I (*I+1 (1 Suction filter feeding I I I

-controlled -distal inflow, lateral outflow water intake by gape tuning -throat squeezing -papillae retain food

-increased water intake \I , ./ Air- & waterhole probing 6 -Water grasping

FIGURE 15. Preliminar morphospacefor filter feeding mechanisms.Five stepsof deduction are shown. 1) A pecking mechanism (2) is the initial feeding mechanism that is deduced from a graspingmechanism (1) and defined as the despecializedpecking mechanism in chicken (e.g., top-soil breaking specializationsare omitted) (7). 2) The morphospaceof filter feeding mechanismsis considered to branch from the morphospacededuced by maximizing the pecking mechanism for probing requirements (3-5). That branch occursat the level of an initial, probing that foragesalong shores.Branching is assumedto be allowed by the integration of two epiphenomena (6). These are: water is grasped while the bird pecks at submerged food, and surface-tension drop-transport occurs along the mouth while the beak is opened slightly to transport the pecked food. Once these two featuresare integrated, this configurationcan accidentally filter feed (8). 3) Maximization of the water intake volume forcesthe deduction to a transition from the surface-tensiontransport mechanism to two parallel lines, one of gulping in which mouth floor motions occur (9), and one of suction mechanismsin which lingual motions are involved (10-13). 4) Depending upon the type of lingual actions in combination with mandible motions three types of suction-pump mechanismsare deduced (10, 11, 13). 5) In addition to the deduction of suction mechanismsthe filter capacity is maximized by deducing lamellae along the tongue and/or the tomial edgesof the mandibles (1 O-l 3). FILTER FEEDING IN FLAMINGOS 321

etration (5). They showed that a slightly length- (a) First, gulping requires a gular pouch, and ened and slenderized beak must first progres- enlarged beaks that are draggedthrough the wa- sively elongate, and then become secundarily ter to collect food (i.e., “ram filter feeding,” San- wedge-shaped.The beak may curve or recurve, derson and Wassersug 1990). The gular pouch is and finally develop rhynchokinesis and a remote squeezedempty by an elevating mouth floor. An touch sensory system in the beak tip. enlarged elevating tongue holds particles against Filter feeding, however, cannot directly be de- the mouth roof. Additionally, in the outflow, el- duced from pecking by maximizing it for filter ements that retain food particles may develop. feeding requirements. First, an intermediate stage This configuration, the gular pouch squeezing(9), must be defined. The reasoning for that stageis is deduced to branch off from the surface-ten- as follows. If the initial probing mechanism of sion/water-grasping line, since throat squeezing slightly slenderizedand lengthenedmandibles (3) was already present in that line. Alternatively, is deduced for birds that feed by run-and-peck gular pouch squeezingcould have been deduced hunting along shores and in shallow waters (as as the first line branching away from the “in- seen in Charadrius sp.), then two epiphenomena creasedwater intake” line, since it is the simplest (concomitant features) (6) necessarily accompa- configuration for increasing water intake. It is ny the transformation. These are: (a) If thesebirds present in Pu$inu.sand Pachyptila (Morgan and peck their prey in water they must necessarily Ritz 1982). graspwater, and (b) If thesebirds thereafter open For an evolutionary interpretation we assume their beak slightly, the water necessarilyruns up that, once the benefit of water as a transport along their beak as a result of surface tension. mechanism for food is selected upon, selection Such a configuration, the surface tension trans- tends to drive increase of the intake-volume of port (8), is found in Phalaropus (Rubega and the food-suspension,as well as development and Obst 1993), possibly in Recurvirostra (M. Rub- improvement of structures that retain food par- ega, pers. comm.) and in Calidris (Gerritsen ticles from that suspension. 1988). A similar situation occurswhen thesebirds (b) Second, enlarged beaks and lingual volume grub, graspor graze vegetation in shallow waters. for a simple lingual pumping mechanism are de- For an evolutionary interpretation of this de- duced for increased water intake, and structures duced line we assume that birds have the be- in the mouth that retain food particles for an havioral capacity to anticipate such epiphenom- increased filter capacity are deduced. Grasping ena and experiencethem; that is, they can “learn” water, sustained by a small effect from surface that graspedfood can be transported in the drop tension, and a larger effect from lingual suction, that is moved along the beak. Given that learning can develop from the two mentioned epiphe- potential, an intake mechanism can be devel- nomena (6) by adding simple lingual retraction. oped that is faster and more economical than the The closing beak and the protracting tongue ancestral type of transport in the pecking mech- squeeze the mouth empty and simultaneously anism. Selection can then work on this mecha- secure the particles between tongue and mouth nism. This configuration may accidentally show roof. There is still and over-tongue transport(food simple filter feeding if papillae are effective to is transported over the lingual cushion) into the retain food particles while the water is squeezed pharynx as has been defined for the initial peck- out by throat elevation (as observed in Phala- ing mechanism. This configuration, the grasp ropes by Rubega and Obst 1993). pump (lo), may occur as the first branch along Branching to a line of advanced filter feeding, the pump-line. It is found in Amer. For an evo- which could have occurred several times, is de- lutionary interpretation, Van der Leeuw and duced as follows. The surface tension transport Zweers (1994) proposethat this maximization is mechanism soon reachesthe limits of its capac- an adaptation to pump specialization which may ity. To enlarge the intake volume, mechanisms occur simultaneous with adaptation to grazing of gulping or suction must take over from those that leads to a compromise that is dominated by of surface tension. The take-over may be pro- grazing demands for a stout broad based beak. vided by several gulping and pumping mecha- That grazing develops first during ontogeny and nisms (see below: a-d). They are deduced sub- filter feeding somewhat later adds to the parsi- sequently according to the parsimony principle, mony argument to position this type of filter which leads to deduction of increasing special- feeding as the first branch along the pump-line. ization. (c) Third, deduction of even more enlarged 322 G. ZWEERS ET AL.

beaks and a lingual pumping that is now discon- craft (198 1, 1988) proposed phylogenetic rela- netted from the sieving are deduced as further tionships from cladistic analysis at the organis- increase of water flow capacity. For the func- mic level. However, it would be premature to tional requirement of filtering the superficial soil compare phylogenetic hypothesesto our provi- layer in shallow water by skimming, primary spe- sional morphospace and historical-narrative hy- cializations are an inverted head posture con- pothesesfor development of filter feeding mech- netted to a curved beak with a straight distal anisms. portion. Specialized filtering is served by lamel- lae along the beak rims and the lingual pumping ACKNOWLEDGMENTS is basically a protraction and retraction of the tongue that forcesthe water flow laterally in and The authorsacknowledge the directorsof the bird park out the mouth. This configuration, the back-and- “Avifauna,” Alphen aan den Rijn, NL, for their co- operation by the loan of 2 Greater, 1 Caribbean and 1 forth pump (1 l), branches offas the second branch . We are indebted to Dr. C. King, along the pump-line. It is observed in Phoeni- from Rotterdam Zoo (NL), for her kind cooperation copterusand Phoeniconaias.For an evolutionary in takingvideo-shots of a youngCaribbean Flamingo. interpretation, we assume that strong selection We thank Drs. K. Bildstein,A. Feducciaand M. A. Rubegafor discussingparts of this work; and Drs. J. on top-soil filter feeding of uniformly sized par- Wattel, J. Rooth and G. Mees for making available titles has driven the development along the de- dissection’ material and skullsof severalPhoenicopte- duced lines. rus and Phoeniconaiasspecies. Van der Leeuw and GZ (d) Fourth, widened and lengthened, straight kindly provided us with the model for filter feeding as beaks, and an enlarged tongue that acts as piston developed for geese.We acknowledgethe assistanceof S. Zeilstra who dissectedthe trigeminal branchesin the and valve in a suction-pressure pump mecha- inws -I----. nism are deduced for a different, parallel line of increasing the water flow capacity. The lingual bulges may add to food retention, but primarily LITERATURE CITED lamellae in the outflow sieve particles by inertial ALLEN,R. P. 1956. The flamingos: their life history impact and a vortex mechanism. Filtered food and survival. Res. Rep. 5, National Audubon So- is transported laterally along the tongue (later- ciety, New York. BATH, W. 1906. Die Geschmacksorganeder Vogel oventral to the lingual cushion) into the pharynx. und Krokodille. Arch. Biontologie 1:5-47. This configuration, the through-pump (13) is the BAUM, D. A., ANDA. LARSON. 1991. Adaptation re- last branch along the pump-line. It is present in viewed: a phylogenetic methodology for studying Anas (Zweers et al. 1977, Kooloos et al. 1989). character microevolution. Syst. Zool. 40: l-l 8. BAUMEL, J. J., A. S. KING, J. E. B~EAZILLE,H. E. EVANS, For an evolutionary interpretation, we assume AND J. C. VANDENBERGE. 1993. Handbook of that a wide trophic diversification has occurred avian anatomy: Nomina anatomica avium. Publ. once this verv effective multi-nurnose_ _ mecha- 23, Publications of Nuttal Omithol. Club. Cam- nism had been developed, since it was easily scal- bridge,MA. able, and compromizable to a variety of other BAUMEL,J. J., ANDL. M. WITMER. 1993. Osteologia, p. 45-132. In J. J. Baumel [ed.], Handbook of requirements. avian anatomy:Nomina anatomicaavium. Publ. We recognize that only bony elements are 23. Publicationsof Nuttal Omithol. Club, Cam- known from Presbyornis.We therefore follow the bridge,MA. suggestion of Feduccia (1980) and Olson and BERKHOUDT,H. 1976. The epidennal structureofthe bill tip organin ducks.Neth. J. Zool. 26:561-566. Feduccia (1980) to consider the Presbyornisfeed- BERKHOUDT,H. 1977. Taste budsin the bill of the ing type an offshoot(12) closeto, but earlier, than Mallard (Anusplatyrhynchos L.). Their morphol- ducks. ogy, distribution and functional significance.Neth. Several studies have led to phylogenetic hy- J. Zool. 27:31C-331. potheseswhich include the above filter feeding BERKHOUDT,H. 1985. Structureand functionof avi- an tastereceptors, p. 463496. In A. S. King and taxa (Feduccia 1976,1987,1980; Olson and Fe- J. McLelland [eds.],Form and function in birds. duccia 1980a, 1980b; Olson 1985). They de- Vol. 3. AcademicPress, . scribe phylogenetic relationships that were based BILJXTEIN,K. L. 1993. White , wetlandwanderer. partly on the fossil record and partly on feeding SmithsonianInstitution Press,Washington, DC. Bock, W. J. 1988. The nature of explanationsin mechanisms. Sibley and Ahlquist (1990) devel- morphology.Amer. Zool. 28:205-2 15. oped cladistic analyses at the DNA level to for- w W. J. 1991, Bxnlanationsin Konstmktions- mulate phylogenetical relationships, and Cra- morphologie and evolutionary morphology, p. 9- FILTER FEEDING IN FLAMINGOS 323

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