Ornithol Sci 3: 119–124 (2004)
ORIGINAL ARTICLE Notes on feeding structures of the Black-faced Spoonbill Platalea minor
Cornelis SWENNEN#,* and Yat-tung YU
Department of Ecology and Biodiversity, University of Hong Kong, Pokfulam Road, Hong Kong
Abstract The bills of the spoonbills differ from the bills of most birds by being ORNITHOLOGICAL wider near the downward curved tip than in the middle, and having the mandibles SCIENCE dorso-ventrally extremely flattened. The mandibles have rounded lateral borders and © The Ornithological Society lack cutting edges. The inward directed sides have a dense cover of thin parallel of Japan 2004 ridges on the distal parts and rows of teeth-like tubercles in the proximate parts. Their skeletons have numerous small pits in the distal parts especially along the edges and the insides. These pits are similar to the spaces for sensory corpuscles for touch in the bills of Scolopacidae (sandpipers, snipes) and are presumed to have the same function in spoonbills. The bill seems adapted for tactile feeding with lateral movements (sweeping) and for pecking, but not for probing into sediments. The wide gape with gular pouch allows the swallowing of rather large food items. The muscular layer of the gizzard is weakly developed and the gizzard is more a digestive pocket than a chewing organ such as occurs for grinding hard shells and grains in molluscivorous and granivorous birds. The long legs are laterally flattened, perhaps for minimising resistance and not-disturbing prey when walking in water during feeding; the partly webbed feet with long toes allow walking over soft mud bottoms.
Key words Bill, Black-faced Spoonbill, Digestive tract, East Asia, Leg, Platalea minor
Spoonbills (Ciconiiformes, Threskiornithidae) are ment or water as can be done by the bills of ducks is large wading birds of 1–2 kg with long legs, necks, already rejected by Allen (1942) who showed that the and bills. Their bills are remarkably widened at the bill lacks the necessary rows of lamellae for sieving. tip and not pointed such as in most birds. The six Vestjens (1975) has tried to relate some relative size spoonbill species are very similar in shape and differences between the bills of the Royal Spoonbill behaviour, mainly differing in size, colour of legs, P. regia and Yellow-billed Spoonbill P. flavipes and bills and other bare parts, and in distribution (del suggested that the longer bill of the latter was more Hoyo et al. 1992). Spoonbills are considered to be suited for probing. Different speculations about the tactile feeders that feed by walking in shallow water function of knobs or teeth in the mandibles were meanwhile sweeping their bills from side to side made by Allen (1942) and Vestjens (1975). That the through the water (Kushlan 1978; Hancock et al. bill can act as suction apparatus to disturb and moves 1992). The bill is the morphological structure that is benthic prey items has been suggested by Weihs and used for collecting food. In this respect, the atypical Katzir (1994) for which they specifically assumed bill of a spoonbill looks clumsy compared to the bill that the upper mandible is convex in cross section. of a chicken or egret. This has given reasons for spec- All in all, however, the mandibles have never been ulations that the shape has a specific function without described in some detail, the specific feeding method studying the morphology of the whole bill. That the of spoonbills is not well understood and there is con- bill can be used for sieving small prey out of sedi- fusion about their food. Food lists in the usual hand- books (Cramp & Simmons 1977; del Hoyo et al. (Received 20 November 2003; Accepted 12 August 2004) 1992) give the impression that spoonbills are omniv- # Corresponding author, E-mail: [email protected] * Present address: Doolhof 7, 1792 CM Oudeschild, Texel, The orous, but the morphology of the alimentary tract in Netherlands which the food items are processed and the legs,
119 C. SWENNEN and Y. YU which are as well of importance for the way the food RESULTS can be captured are neglected in studies about the food of spoonbills. An accurate description of the 1) Bill morphological structures used in collecting and pro- Bill length of Black-faced Spoonbills wintering cessing food is an indispensable base for studying in Hong Kong is 181.7 13.0 mm (163–207 mm) and understanding the feeding of any organism. (mean SD and range; N 22), while the width of the In this paper, we study these aspects in some detail. spoon is 51.0 2.2 mm (47–55 mm). In lateral view, We focus on the Black-faced Spoonbill Platalea the bill looks thin, is bent down near the tip and minor, which is the spoonbill species present in our shows a 2–4 mm wide gap in the central part study area. Its distribution is confined to East Asia (Fig. 1a). In dorsal view the mandibles are wide where they mainly breed around the North and East (Fig. 1b). The upper mandible of the bill is wider Coast of the Yellow Sea and winter from South Korea than the lower in the distal part, but the lower to Vietnam (Kennerley 1990; del Hoyo et al. 1992; mandible is wider than the upper in the proximal part Hancock et al. 1992). We give a description of the (Fig. 1b,c). The slit-like external nostrils are close to morphology of the main feeding organs (bill, intes- the head in a suture that runs more or less parallel to tinal tract, and legs). The feeding method and the the border of the upper mandible. The nail on the tip potential foods of the species and of spoonbills in of the upper mandible is small and not pronounced general will be deduced from these morphological data.
MATERIALS AND METHODS Live specimens handled were wintering Black- faced Spoonbills that had been caught in the Mai Po Marshes Nature Reserve (Hong Kong) in the winters of 1998–99 and 1999–2000, where they were marked for a migration study (Melville et al. 1999). We have discriminated first winter birds from older ones by having a pale coloured bill, totally brown iris, and the presence, distribution and size of black on the wing feathers. In adults the bill is black, the iris red, and black on the wing feathers is lacking. Intermediate specimens were considered in their second winter. Before releasing the birds, measurements were taken of morphological characteristics from adult birds of unknown sex. Length of legs were measured from the ankle (intertarsal joint) and the feathers on the belly straight to the floor in the natural stand. Bill length was measured as the shortest distance between the tip and the start of the feathering over the length axis of the upper mandible. Further details of the bill were studied from some skulls of preserved adult speci- mens in private collections in Hong Kong and Tai- Fig. 1. (a) Lateral view of the bill showing the gap and the wan, and of two fledglings in a private collection in flatness of the mandibles. Drawn from a photograph. (b) Bill South Korea. One preserved alimentary canal was in dorsal view. (c) Cross sections of the mandibles (at the given to us in Hong Kong, it originated from a win- same scale). The position of the sections is indicated in the tering specimen that was found freshly dead. left drawing. (d) Comb-like incisions at the tip of the bill. A: Border of upper mandible in frontal view. B: Border of lower mandible dorsal view. (e) Parallel ridges on the ventral side of the lower mandible. lm: lower mandible, na: nail, no: nostril, sp: spoon, su: suture, tu: tubercles, um: upper mandible.
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(Fig. 1b). The mandibles are rigid to lateral forces, and only slightly flexible to dorso-ventral forces. Both mandibles are dorso-ventrally extremely flattened. The thickness of the spoons is 2 mm, gradually increasing proximally and reaching 7.6 0.3 mm (mean SD, N 10) in the upper mandible and 5.5 0.4 mm in the lower mandible at the distal part of the nostrils (Fig. 1a, c). The epidermal layer is thin over the whole length of the mandibles, slightly thicker along the distal borders of the mandibles where both show a series of comb-like incisions on both sides of the median line (Fig. 1d A, B). A few short and inconspicuous parallel ridges are found on the outside of the lower mandible (Fig. 1e). The insides of the mandibles are densely covered by minute ( 0.5 mm high) seemingly parallel, epi- dermal ridges in the distal parts (Fig. 2a). The ridges split and unite during their course, and the distance between their crests varies between about 0.3 mm where they converge near the tip and 1 mm where Fig. 2. (a) Inside of the bill. A: Upper mandible in ventral they diverge in the widest part of the spoon. Rows of view. B: Lower mandible in dorsal view. (b) Tongue of Black- minute depressions can be seen with the help of a faced Spoonbill in dorsal view. gp: gular pouch, pr: parallel magnifying glass on and between the dried ridges, ridges, tu: tubercles. between the comb-like incisions, and in the smooth outer sides of the spoons of dry preserved specimens. lower mandible to the spoons and branch there. These probably indicate sites of sensory corpuscles in the dermal layer. The central parts of the insides of 2) Alimentary tract the mandibles show two longitudinal rows of widely The alimentary tract from a fresh carcass found in spaced, less than 1 mm high teeth-like cuticular Hong Kong had deep longitudinal folds in the about tubercles (Fig. 2a). These tubercles are lacking in 27 cm long oesophagus. The proventriculus was fledglings, and develop during the first winter. The rather solid, about 5 cm long, 3 cm wide, and could lateral sides of the mandibles are rounded and lack easily be expanded. The wall mainly existed of a any sign of tomia, i.e. sharp cutting edges (Fig. 1c). layer of tubular glands (Fig. 3c D); the inside showed The two bony bars of the lower mandible are con- several ( 30 per cm2) small openings of the glands. nected by soft, elastic tissue, which may expand to a The ventriculus (gizzard) was about 7 cm long, gular pouch when swallowing large prey. This pouch 5.5 cm high and 4.5 cm wide (Fig. 3c A). The muscu- is longitudinally folded; its colour is black in all age lar layer was 9 mm thick on the dorsal side and 2 mm classes (Fig. 2a). The short tongue is triangular; the on the ventral and lateral sides (Fig. 3c C). Locally, it proximate side is thinly fimbriated (Fig. 2b). was a little thicker near the passage to the duodenum. The surface of the bony skeleton of the bill shows The wrinkled touch lining of the lumen was about fields with small pits in the distal parts. These pits are 5.9 mm thick along the sides and about 3 mm on the generally wider than the holes for the blood vessels. top and bottom. The intestine was 132 cm long; it had They are most dense along the sides of the mandibles two short and narrow caeca with lumens of about from the tip up to over half of the bill length, on the 2.5 mm deep. insides and the outsides of the widened distal parts (Fig. 3a A, B, C, D). Most pits have an oval aperture 3) Leg varying in size between 0.4 0.5 mm and 0.7 Tarsus and tibia are laterally compressed with di- 1.1 mm, and a few are round with a diameter varying mensions in cross sections of 6.5 0.2 mm (mean between 0.3 and 0.4 mm. (Fig. 3b). Two major nerve SD; N 4) and 12.6 0.1 mm, and 7.5 0.2 mm and branches run up through the bones of upper and 13.5 0.1 mm, respectively. The three frontal toes are
121 C. SWENNEN and Y. YU
and transporting food into the oesophagus. Foods of birds differ between species and so do the bills and methods of collecting food items. The other functions such as a structure for drinking, feather preening, nest building, and defence can be conducted with all dif- ferent kind of bills. Therefore we concentrate on the aspects of food collecting. The spoonbill usually feed by sweeping its bill in turbid water and preferentially at dusk and dawn (Yu & Swennen 2004a, b). We deduce that the extreme flatness of the mandibles will minimise drag and turbulence during the lateral movement while searching for prey in water. This will be mainly intended to avoid disturbing potential prey in advance because tactile feeding means that prey has to be touched by the bill and caught at once; a disturbed prey will flee from the source of distur- Fig. 3. (a) Distribution and relative density of pits in the bance and will be difficult to locate without visual bony skeleton of the mandibles of the Black-faced Spoonbill. clues. The pits are shown as small dots. A: Upper mandible dorsal The bill allows also grasping of visible food items, view. B: Upper mandible ventral view. C: Lower mandible dor- which is rarely noted in the Royal and Yellow-billed sal view. D: Lower mandible ventral view. (b) Detail photo- Spoonbill (Vestjens 1975) and Eurasian Spoonbill graph of pits in the bone of the ventral side of the upper (Stienen & Brenninkmeijer 1993; Weihs & Katzir mandible. The photographed part measures 4.1 3.2 mm. (c) Stomach of a Black-faced Spoonbill. A: Ventriculus (gizzard). 1994). Feeding by probing is mentioned in the litera- B: Proventriculus. C: Cross section of ventriculus. D: Cross ture for the African Spoonbill (del Hoyo et al. 1992) section of proventriculus. The position of the cross sections is and Yellow-billed Spoonbill (Vestjens 1975), but it is indicated by dotted lines. (d) Feet of Black-faced Spoonbill in not clear what is meant. The bill shape shows that ventral view. L: Left foot, R: Right foot. du: opening to duode- probing into sediment is not an option for any spoon- num, oe: oesophagus, tg: tubular glands, cl: cuticle layer, ml: bill, because the wide and curved tip would receive muscular layer. much resistance during penetration as well as during retraction, but when the frontal parts can be pushed partially webbed (Fig. 3d); the hind toe is relatively into sediment the wide tip can not be opened or long and has a slightly raised base, but still makes a closed for grasping a burrowing prey, because the full print in muddy sediments. The span from the tip upper mandible has no flexible area that allows an ac- of the nail of the middle toe to the nail of the hind toe tively upward bending of the distal part (rhynchoki- is 141 1.9 mm (mean SD; N 4), that between the nesis) such as occurs in snipes (Scolopacidae) and tips of the nails of left and right toes about 119 some other bird groups. 1.0 mm. In the standing leg, the distance between foot The numerous pits in the skeleton are most likely sole and ankle is 130.2 14.7 mm and to the belly spaces for the sensory receptors. Similar pits occur in 225 22.6 mm (N 10). the better-studied bills of Scolopacidae (snipes, sand- Inspection of preserved specimens in the collection pipers), but in a slightly different position (Bolze of the National Museum of Natural History, Leiden 1968; Piersma et al. 1998). Scolopacid shorebirds (The Netherlands) demonstrated that the bills and make sewing movements and probe into sediments legs of the Eurasian, Royal, Roseate, and Yellow- for food; they have the pits for sensory corpuscles billed Spoonbill show the same details as described densest on the dorsal and ventral sides of the tips of above for the Black-faced Spoonbill. They mainly the mandibles. Spoonbills make lateral feeding move- differ in length, relative width of the distal part, and ments with the bill open; they have the pits relatively colour. most dense on the lateral and insides of the bill (Fig. 3b). The most common Herbst corpuscles have DISCUSSION a length of 0.05–0.2 mm (Schwartzkopff 1973), the pits are large enough to lodge a whole series of them The main function of a bill is collecting, tasting, similar as has been found in Red Knots (Piersma et
122 Feeding structures of the Black-faced Spoonbill al. 1998). Histological evidence is still lacking, but it shelled molluscs (McLelland 1979). This means that is supported by the presence of major nerves embed- Black-faced Spoonbills can only digest meat of mol- ded in the skeleton. The ordering of the pits differs luscs that have a thin shell or no shell at all. Food from the rows of supposed sensory corpuscles that lists of spoonbills given in del Hoyo et al. (1992) are visible in the epidermis of dry preserved bills. contain in variable detail several taxa including mol- The occurrence of such a density of supposed sensory luscs and plants, which may largely be based on elements agrees with the tactile way of feeding recognisable fragments in stomach contents. Shellfish (Kushlan 1978). is named in the second place as food of the Black- The dense covering with low cuticular ridges on faced Spoonbill, but their anatomical structure does the insides of the distal parts of the mandibles may not support the eating of molluscs, which was also have a function in keeping hold of a slippery prey. doubted for other reasons by Hsueh et al. (1993). All these details lead to the conclusion that the pecu- Fragments of shells in a stomach may have been liar widening of the tips is necessary for improving swallowed accidentally and do not represent food the chance of catching moving food items that are intake. sensed between the mandibles. This is correlated with The length of the legs up to the belly determines their way of feeding in turbid water (Yu & Swennen the water depth in which a spoonbill can feed (Yu & 2004a) during twilight (Yu & Swennen 2004b) which Swennen 2004a). The long partly webbed toes allow prevent a visual detection of food items in the normal walking on rather soft mud, and the lateral flattening feeding situation. of the legs may reduce resistance and agitation when The tongue is too small for a function in the feeding in water which may be important for not-dis- upward transport of food, its role may be in covering turbing prey. up the glottis during swallowing and perhaps in taste. The rudimentary tongues of large fish-eaters such as ACKNOWLEDGEMENTS occurring in the Pelicaniformes and Ciconiiformes are often considered an adaptation allowing bulky This study was funded by the Agriculture, Fisheries and foods to be swallowed whole and quickly (McLelland Conservation Department of the Hong Kong SAR Govern- 1979). The transport of food through the bill will be ment for the research in Hong Kong via WWF Hong Kong, and by the Dutch Society for the Protection of the Wadden Sea conducted via catch-and-throw movements. The two and the Van der Hucht Fund for the research in Taiwan and rows of tooth-like projections more proximal in the South Korea. We are indebted to private collectors in Taiwan mandibles seem suited for holding a prey during and South Korea, and the Kadoorie Farm and Botanic Garden, transport to the throat, and thus replace the function Hong Kong for permission to examine the Black-faced Spoon- of the cutting edges which give hold on a prey in bill materials in their collections. Thanks are also due to other fish-eating birds. Vestjens (1975) states that C. Smeenk of the National Museum of Natural History, Leiden these tubercles in Royal and Yellow-billed Spoonbills (The Netherlands) and O. Overdijk for permission to study materials of other species in their collections. This study could are also used for chewing larger food items. This is not have been conducted without their co-operation. We unlikely, as the projections do not have a molar-shape sincerely thank R. Corlett for his helpful comments and for in any spoonbill species, and their positions in the improving our English. upper and lower mandible do not match (Figs. 1c, 2a A, B). Allen (1942) suggests that these projections may contain specific sensory receptors; however, no REFERENCES indications of sensory elements are visible in the Allen RP (1942) The Roseate Spoonbill. Research Re- dried skin on and around the tubercles and there are port 2. Natl Audubon Soc, New York. also no sensory pits or perforations for nerves in the Bolze G ( 1968) Anordnung und Bau der Herbstlichen skeleton below the tubercles (Fig. 3a B, C). Körperchen in Limicolen Schnäbeln im Zusammen- The rudimentary tongue, gular pouch and wide, hang mit der Nahrungsfindung (Arrangement and folded oesophagus indicate that rather large food structure of Herbst’s corpuscles in bills of Limicolae items can be swallowed. The spoonbill ventriculus in relation to food finding). Zool Anz 181: 313–355 (Fig. 3c C) is a wide pocket for digestion suited for (in German). feeding on fish or meat. It lacks the thick muscular Cramp S & Simmons KEL (eds) (1977). The birds of layer of a gizzard for grinding or cracking hard foods the western palearctic, Vol 1, Oxford University such as occurs in birds swallowing hard seeds or Press, Oxford.
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