Feeding in Birds: Approaches and Opportunities

C H A P T E R

12 Feeding in Birds: Approaches and Opportunities MARGARET RUBEGA Department of Ecology and Evolutionary Biology University of Connecticut Storrs, Connecticut 06268

covered a previously unknown feeding mechanism, surface tension transport (STT) (Fig. 12.2), in phalaropes (Phalaropus), despite decades of previous study on their foraging (e.g.. Bent, 1927; Tinbergen, 1935; Mercier and Gaskin, 1985; Jehl, 1986). Similarly, Piersma et ah (1998) demonstrated the existence of a previously unknown prey detection mechanism in red knots {Calidris canutus). Quite aside from our interest in the evolution of feeding mechanisms per se, this lack of understanding has important consequences for the evolutionary and ecological study of birds. First, without an informed understanding of feeding mechanisms, we may seriously err in our ideas about the dietary and energetic strategies available to birds, and hence about one of the most fundamental aspects of the selective regimes they operate, and evolve, under. Note that I am distinguishing here (and hereafter) between our (frequently extensive) information about what birds eat, and our relatively poor understanding of how they eat it ("food acquisition'' sensu Zweers et ah 1994) , and of how bill morphology influences the latter. Second, our knowledge of avian feeding mechanics circumscribes our ability to understand how foraging relates to other behaviors. Prey intake rates are an important component of many behavioral and energetic models of the process of habitat choice (Krebs and Davies, 1991; Sutherland, 1996). Indeed, much of optimal foraging theory was built upon studies of avian subjects (Stephens and Krebs, 1986). Yet because we rarely understand the functional relationship of feeding movements in birds to actual ingestion rate, our data frequently constitute estimates of intake rates with unknown error terms. Often we are unable even to distinguish the specific prey being taken.

I. INTRODUCTION 11. PATTERNS OF ANALYSIS A. Systematics and Choice of Taxa B. Inferring Function from Structure versus Tests of Hypotheses C. Statistical Analysis, Sample Sizes, and the Importance of Variation III. CONCLUSION References

L INTRODUCTION The feeding structures of birds are probably more diverse than those in any animals except insects (Fig. 12.1). This dramatic modification of the feeding structures in birds has attracted a good deal of attention, historically, on the basis of the idea that where there is a crossbill, there must be an interesting feeding mechanism. In addition, bird beaks and their workings have long been attractive subjects because students of evolution reasonably presume that extreme modification of structures as fundamental to survival as mouthparts is likely the result of strong selection. Indeed, Darwin's (1859) ideas about evolution by natural selection were influenced by variation in beak size and shape in Galapagos finches (Geospizinae). Studies of the influence of this variation on survival via the ability to crack hard seeds in hard times remain a classic demonstration of evolution in the wild (Boag and Grant, 1981; Grant, 1985). Nonetheless, to a great degree, avian feeding mechanics and functional morphology remain poorly understood. For example, Rubega and Obst (1993) disFEEDING (K. Schwenk, ed.)

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no review that examines the entire published literature with a view specifically toward identifying areas where new efforts are liable to produce new insights into the evolution of avian feeding mechanisms. Rather than merely repeat an overview of the existing literature, this chapter aims to (1) identify patterns in the nature of past and present work on avian feeding mechanics and (2) suggest areas where new investigations might be particularly informative, and approaches which I believe will be especially productive.

IL PATTERNS OF ANALYSIS A. Systematics and Choice of Taxa A survey of the literature (see earlier list of reviews) reveals that feeding structure and/or mechanisms have been investigated in a wide variety of avian taxa, but opportunities for significant new contributions are abundant. The majority of the published analyses I could locate are single species ("idiographic"; see Chapter 1) studies, and I have used the term "analysis" very broadly. In a large number of cases, the analysis consisted of an examination of beak morphology and the subsequent generation of (frequently untested) hypotheses about the functional significance of features of the beak (see Section II,B), rather than direct examinations of feeding patterns and mechanics.

FIGURE 12.1. Diversity of feeding structures in birds. (A) Hyacinth macaw (Anodorhynchus hyacinthinus), (B) southern giant petrel {Macronectes giganteus), (C) parakeet auklet {Aethia psittacula), (D) wrybill (Anarhynchus frontalis), (E) Andean avocet (Recurvirostra andina), (F) whippoorwill {Caprimulgus vociferus), and (G) African spoonbill {Platalea alba). Feeding structures and feeding mechanics of these species are unstudied. Drawings by M. J. Spring.

Because of the long history of interest in feeding in birds, there is a large literature, with multiple reviews published since the mid-1980s. Gottschaldt (1985) reviewed sensory receptors in the bill; Berkhoudt (1985) summarized information on taste receptors; Zusi (1984) presented a detailed review and analysis of avian rhynchokinesis; Vanden Berge and Zweers (1993) reviewed the myology of the avian feeding apparatus; and Zweers et al. (1994) reviewed behavioral aspects of feeding mechanisms. To date, however, there has been

FIGURE 12.2. Surface-tension feeding in phalaropes. Small invertebrate prey are seized in the tips of the jaws and are transported in the water that adheres to the bill. Water is adhesive to the surface of the bill; by spreading its jaws the bird stretches the drop. The increase in potential energy resulting from the increase in the surface area of the drop drives the drop and prey along the bird's bill into the buccal cavity. Reproduced from Rubega (1997), with permission.

12. Feeding in Birds Throughout the remainder of this chapter I refer only to feeding analyses of the following types: (1) detailed anatomical descriptions of the feeding apparatus [e.g., Homberger's (1986) now-classic treatment of the tongue in the African grey parrot, Psittacus erithacus], (2) experimental (or at least controlled) examinations of motor patterns and feeding mechanisms in live animals (e.g., Tomlinson's analysis of cranioinertial feeding in paleognaths. Chapter 11), or (3) studies that combine the two [e.g., Zweers et al.'s (1977) brilliant and comprehensive analysis of feeding and the feeding apparatus in mallards. Anas platyrhynchos]. I specifically exclude uni- or bidiraensional comparisons of bill size [e.g., tables of bill lengths, commonly found in, but not restricted to, identification guides, such as Prater et al.'s (1984) guide to Holarctic waders], casual observations of free-living birds, and untested speculation about feeding mechanisms based on either. Species in approximately 19 of 25 orders have been the subject of some form of feeding analysis. Although this may seem like rather extensive coverage of the class, it should be noted that the majority of bird families remain completely unexamined. Published work to date covers only about 49 of 158 families, i.e., details of feeding structure and mechanics are unknown for almost 70% of all families of birds. Table 12.1 identifies the orders and families of birds for which no published work on the details of either bill morphology or feeding mechanism could be located. It can be assumed that I have failed to locate every published feeding study on birds. Also, my assessment of the degree to which we are uninformed about avian feeding depends on the classification of birds used. I have used a traditional classification (Morony et ah, 1975; del Hoyo et ah, 1992), rather than a newer, still controversial classification (Sibley et ah, 1988, Sibley and Ahlquist, 1990) with fewer orders and families (see Section II,C). Nonetheless, even if my estimate of the number of published studies was doubled, my overall conclusion would not change: there are about 9000 extant species of birds, and we know little or nothing about feeding structure and mechanics for the majority of them. This survey reveals that the field lacks a phylogenetic strategy with respect to the taxa investigated. In a few cases, systematic and purposeful within-clade comparative work has been done [e.g., passerines, Passeriformes (Bock, 1960); waterfowl, Anatidae (Goodman and Fisher, 1962); woodpeckers, Piciformes (Spring, 1965); kingfishers and allies, Coraciiformes (Burton, 1984)]; however, most of the literature on avian feeding seems to have been largely driven by (a) convenience [e.g., the investigator works with a common, or commonly available, species such as

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chickens, Gallus domesticus (e.g., Calhoun, 1933; White, 1968; Lucas and Stettenheim, 1972; McClelland, 1979; Bhattacharyya, 1980; Berkhoudt, 1985; Homberger and Meyers, 1989; Van den Fleuvel, 1992), or domestic pigeons, Columba livia (e.g., Lucas and Stettenheim, 1972; Zeigler et al, 1980; Zweers, 1982a,b, 1985; Bermejo et al, 1989), thus each of these are disproportionally well known relative to their phylogenetic importance]; (b) serendipity, in which the investigator is studying something else and makes a chance observation [e.g., observations leading to the discovery of surface tension feeding in phalaropes (Rubega and Obst, 1993) were made during the making of an educational film (University of California 1985)]; or (c) the allure of the extreme [e.g., flamingo, Phoenicopteriformes, feeding mechanisms have been much more intensively studied (e.g., Jenkin, 1957; Kear and Duplaix-Hall, 1975; Zweers et al, 1995) than those of tyrant flycatchers, Tyrannidae, for example, which are far more speciose (~ 374 species: del Fioyo et ah 1992) and widely distributed)]. To be sure, these criteria have produced a wealth of information about the diverse ways in which birds capture and process their food. Yet available data are so thinly scattered across taxa that it would be impossible to confidently assert anything about the higher-level evolution of avian feeding systems (Table 12.1). In fact, to date the field not only lacks a widely accepted general theory explaining the evolution and diversity of avian feeding mechanisms (Lauder, 1989), but lacks a core group of plausible hypotheses, which are being systematically evaluated. For example, in the context of attempting to construct a general theory, Zweers (1991a,b) has stated that pecking mechanisms occur in all modern birds, and thus pecking is the ancestral condition (Zweers et ah, 1994; Zweers and Gerritsen, 1997; Zweers and Vanden Berge, 1997). This assertion is intuitively attractive, but made in the absence of information about the feeding mechanics in two-thirds of the families of birds, its accuracy remains to be demonstrated. The hypothesis is certainly true if pecking is defined sufficiently broadly. This is not mere hairsplitting; if defined sufficiently broadly, pecking is present in all reptiles as well. What, if anything, makes avian pecking characteristically avian, as opposed to reptilian in nature? Is there only one kind of avian pecking, arising from one conserved motor pattern underlying this approach to food grasping? This would be an interesting and impressive finding. If not, how many kinds of pecking are there, how are they distributed among taxa, and what is their relationship to the diversity of feeding structures in birds? An even more compelling question is what, if anything, makes avian feeding, as a whole, characteristically avian?

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Margaret Rubega TABLE 12.1

Unstudied Orders and Families in the Class Aves''

Common name

Approx. no. of species in family

Order

Family

Struthioniformes

Struthionidae Rheae Casuariidae Dromaiidae Apterygidae

Ostrich Rheas Cassowaries Emu Kiwis

Tinamiformes

Tinamidae

Tinamous

47

Sphenisciformes Gaviiformes

Spheniscidae Gaviidae

Penguins Loons (divers)

17 4

Podicipediformes

Podicipedidae

Grebes

22

Diomedeidae Procellariidae Hydrobatidae Pelecanoididae Phaethontidae Pelicanidae Sulidae Phalacrocoracidae Anhingidae Fregatidae

Albatrosses Petrels, shearwaters Storm petrels Diving petrels

14 70 20 4

Tropic birds Pelicans Gannets, boobies Cormorants Darters Frigate birds

3 7 9 39 2 5

Ardeidae Scopidae Ciconiidae Balaencipitidae Threskiornithidae

Herons Hamerkop Storks ShoebiU Ibises, spoonbills

60 1 19 1 32

Procellariformes

Pelecaniformes

Ciconiiformes

Phoenicopteriformes

1 2 3 1 3

Order

Family

Common name

Approx. no. of species in family 8 2 1 7 1 13 9

Charadriidae Scolopacidae Thinocoridae Chionididae Stercorariidae Laridae Rynchopidae Alcidae

Jacanas Painted snipe Crab plover Oystercatchers Ibisbill Avocets, stilts Thick knees Coursers, pratincoles Plovers Sandpipers, snipe Seedsnipe Sheathbills Skuas Gulls, terns Skimmers Auks

Columbiformes

Pteroclididae Columbidae

Sandgrouse Pigeons, doves

16 283

Psittaciformes

Loriidae Cacatuidae Psittacidae

Lories Cockatoos Parrots

55 18 271

Cuculiformes

Musophagidae Cuculidae

Turacos Cuckoos

19 130

Strigiformes

Tytonidae Strigidae

Barn owls "Typical" owls

12 134

Caprimulgiformes

Steatornithidae Podargidae Nyctibiidae Aegothelidae Caprimulgidae

Oilbird Frogmouths Potoos Owlet-nightj ars Nightjars

1 13 5 8 76

Apodidae Hemiprocnidae Trochilidae

Swifts Tree swifts Hummingbirds

82 4 338

Charadriiformes

16 64 86 4 2 5 90 3 23

Phoenicopteridae

Flamingoes

Anseriformes

Anhimidae Anatidae

Screamers Ducks, geese, swans

Falconiformes

Cathartidae Pandionidae Accipitridae Sagittariidae

7 New World vultures, Osprey 1 217 Hawks, eagles Secretary bird 1

Apodiformes

Coliiformes

Coliidae

Mousebirds

Galliformes

Megapodiidae Cracidae

Trogoniformes

Trogonidae

Trogons

37

Coraciiformes

Phasianidae Opisthicomidae

Megapodes Guans, chachalacas. currasows Pheasants, grouse Hoatzin

44 213 1

Mesitornithidae Turnicidae Pedionomidae Gruidae Aramidae Psophiidae Rallidae Heliomithes Rhynochetidae Eurypygidae Cariamidae Otididae

Mesites Button quails Plains wanderer Cranes Limpkin Trumpeters Rails, coots Finfoots Kagu Sunbittern Seriemas Bustards

3 14 1 15 1 3 133 3 1 1 2 24

Alcedinidae Todidae Motmotidae Meropidae Coraciidae Brachypteraciidae Leptosomatidae Upupidae Phoeniculidae Bucerotidae

Kingfishers Todies Motmots Bee eaters Rollers Ground rollers Cuckoo roller Hoopoe Woodhoopoes Hornbills

90 5 9 21 11 5 1 1 8 44

Piciformes

Galbulidae Bucconidae Capitonidae Indicatoridae Ramphastidae Picidae

Jacamars Puffbirds Barbets Honeyguides Toucans Woodpeckers

17 34 81 14 33 204

Gruiformes

5

Jacanidae Rostratulidae Dromadidae Haematopodidae Ibidorhynchidae Recurvirostridae Burhinidae Glareolidae

3 147

12

6

(continues)

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12. Feeding in Birds TABLE 12.1 (continued)

Order

Family

Passeriformes

Eurylaimidae Dendrocolaptidae Furnariidae Formicariidae Conopophagidae Rhinocryptidae Cotingidae Pipridae Tyrannidae Oxyruncidae Phytotomidae Pittidae Xenicidae Philepittidae Menuridae Atrichornithidae Alaudidae Hirundinidae Motacillidae Campephagidae Pycnonotidae Irenidae Laniidae Vangidae Bombycillidae Dulidae Cinclidae Troglodytidae Mimidae Prunellidae Muscicapidae

Common name

Approx. no. of species in family

14 Broadbills 52 Woodcreepers Ovenbirds 218 Antbirds 228 Gnateaters 11 Tapaculos 30 Cotingas 79 57 Manakins Tyrant flycatchers 374 Sharpbill 1 Plantcutters 3 Pittas 24 New Zealand wrens 4 Asities 4 Lyrebirds 2 Scrub birds 2 Larks 77 Swallows, martins 80 Wagtails, pipits 54 Cuckooshrikes 70 Bulbuls 123 Leafbirds, ioras. fairy bluebirds 14 Shrikes 74 Vanga shrikes 13 Waxwings 8 Palmchat 1 Dippers 5 Wrens 59 Mockingbirds, thrashers 31 Accentors 12 Thrushes and allies 1423

Order Passeriformes (continued)

Family Aegithalidae Remizidae Paridae Sittidae Certhiidae Rhabdornithidae Climacteridae Dicaiedae Nectariniidae Zosteropidae Meliphagidae Emberizidae Parulidae Drepanididae Vireonidae Icteridae Fringillidae Estrilididae Ploceidae Sturnidae Oriolidae Dicruridae Callaeidae Grallinidae Artamidae Cracticidae Ptilonorhynchidae Paradisaeidae Corvidae

Common name

Approx. no. of species in family

Long-tailed tits Penduline tits Tits, chickadees Nuthatches Treecreepers Philippine creepers Australian creepers Flowerpeckers Sunbirds White eyes Honeyeaters Buntings, cardinals. tanagers New World warblers Hawaiian honeycreepers Vireos New World blackbirds Finches Waxbills Weavers, sparrows Starlings Orioles Drongos Wattlebirds Magpie-larks Woodswallows Butcherbirds Bowerbirds Birds of paradise Crows, jays

8 10 27 25 6 2 6 58 116 83 171 558 126 23 43 95 122 127 143 111 28 20 3 4 10 8 18 42 105

^Taxa for which I could identify no published studies of the functional morphology of the feeding structures or feeding mechanics are bold faced. Classification is traditional and follows del Hoyo et al (1992) and Morony et ah (1975).

Progress currently is hampered by our lack of focus, phylogenetically speaking. A long list of authors have persuasively stated the case for a phylogenetic approach to understanding the evolution of complex behaviors and their ecological relevance (see citations summarized in Brooks and McClennan, 1991; Losos and Miles, 1994). It is therefore striking to note that the modern study of feeding mechanics in all vertebrates, except birds (and possibly mammals), is proceeding within an explicitly evolutionary framework, using phylogenetic tools and approaches (see other chapters in this book). What factors have prevented investigators of avian

feeding mechanisms from following suit? As with other groups of vertebrates, the bulk of all work to date was done prior to the rise of phylogenetic methods. More recently, ornithologists have been hampered by the lack of a rigorous phylogeny for the class. The ordinal level relationships of birds are still poorly understood (Raikow, 1985; Cracraft, 1988). The development of a phylogeny for the class is impeded by an insufficient inventory of cladistic characters (Cracraft, 1988). Such a phylogeny is essential to understanding the evolution of avian feeding mechanisms, as a basis for the generation of sampling schemesn, and for mapping character states.

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Margaret Rubega

This is not to say that no higher-level phylogenetic analyses exist; Sibley and associates have provided a phylogenetic hypothesis for the whole class (Sibley et ah, 1988; Sibley and Ahlquist, 1990). Unfortunately, their characters, methods, and assumptions have serious weaknesses and have been widely criticized (e.g., Krajewski, 1991; O'Hara, 1991; Raikow, 1991; Lanyon, 1992). It has been argued, however, that this phylogeny at least presents us with a working hypothesis (O'Hara, 1991), and thus a starting place, and an opportunity for tests of hypotheses about the evolution of feeding mechanisms. To date, there are no alternative higherlevel phylogenies for the whole class. Nonetheless, ornithologists have been among the most active vertebrate systematists, and phylogenies below the ordinal level now are available for many groups of birds. A shortage of phylogenies, of course, is not the only factor preventing a shift toward phylogenetic (cladistic) methods. Some of the most active investigators of avian feeding methods and evolution have deliberately eschewed a phylogenetic approach in order to pursue alternate strategies of investigation. Zweers and colleagues, the most prolific and productive group currently working on avian feeding mechanics, have been developing an approach that deduces likely pathways of phenotypic transformation in avian feeding systems (Zweers, 1991a,b; Zweers and Vanden Berge, 1997; Zweers and Gerrittsen, 1997). They use functional optimality as the criterion for morphological and mechanistic change in order to generate testable ideas about the domain of all possible feeding mechanisms and evolutionary pathways to those mechanisms (see Chapter 1). In other words, they are using mechanical principles to generate ideas about how feeding mechanisms and bill morphology might have evolved, rather than looking at the distribution of feeding characters on a phylogeny, and then inferring the direction and nature of evolution. This approach shows some promise as a tool for generating hypotheses, but suffers from potential circularity. (The choice of optimal morphologies and mechanisms is unavoidably drawn from extant examples, which are then mapped onto the resulting transformation scheme, and are found to match.) Such a method will ultimately require grounding in a phylogenetic framework if it is to serve as a tool for understanding the actual evolution of existing feeding mechanisms. For instance, Zweers and associates (Zweers, 1991a,b; Zweers et al, 1994; Zweers and Gerritsen, 1997; Zweers and Vanden Berge, 1997) have proposed that avian filter-feeding mechanisms arose via modification of a charadriiform-like bill structure, and of the motor patterns associated with pecking. This idea posits the following sequence of events: (1) Shorebird-like bill structures are a modification of a more generalized

(pigeon-like) ancestral beak. In this first modification, elongation and slenderization contributed to improved probing performance. (2) Surface-tension transport, a mechanism by which birds transport prey along the bill using the physical properties of water droplets (Rubega and Obst, 1993; Rubega, 1997), arose as an epiphenomenon of this change in bill morphology. (3) Further modification of the bill structure and motor patterns arose as a consequence of specialization. (4) Modifications that increased the volume of prey and water processed in one feeding cycle led to flamingo- and duck-like bill morphologies, and hence to filter-feeding mechanisms. The initial generation of these ideas took place in a strictly biomechanical rather than phylogenetic context, and thus was not accompanied by the directed sampling of feeding structure and mechanism necessary to test most of the resultant hypotheses. An additional problem is that trophic mechanisms or morphologies are not coded in a manner that would lend itself to cladistic analysis. Zweers and Vanden Berge (1997) do provide a phenogram in which key trophic mechanisms and transitions are overlaid with the names of taxa that putatively have the mechanisms (Fig. 12.3), and then compare their scheme of "trophic radiation" to available phylogenetic analyses. Unfortunately, their phenogram includes many taxa for which detailed analysis of feeding mechanisms have not been conducted (e.g., stone curlew, Burhinus oedicnemus; spoonbill sandpiper, Eurynorhynchus pygmeus; crab plover. Dramas ardeola; ruff, Philomachus pugnax; Eurasian curlew, Numenius arquata; the screamers Anhimidae), or can never be done (e.g., Preshyornis, a fossil bird with a duck-like head and a shorebird-like axial skeleton). Also, they fail to map their character states (mechanisms or morphologies) directly onto existing phylogenies. Thus, it is difficult to evaluate their conclusion that their scheme of phenotypic transformation is largely congruent with cladistically produced phylogenies. Nonetheless, this detailed set of hypotheses can provide a basis for designing a sampling scheme that would contribute to our understanding of the evolution of feeding mechanisms in the shorebirds (Charadriiformes). There are a number of explicit predictions resulting from the Zweers model that can be tested. First, the model postulates that the ability to use surface-tension prey transport is simply a consequence of the basic shorebird bill structure. If true, then the capacity to employ this feeding mechanism should be found not only in the species in which it was discovered, the highly aquatic red-necked phalarope {Phalaropus lohatus), but in every shorebird with a straight, needlelike bill. Initial steps in a survey of the whole shorebird clade indicate that surface-tension transport of prey is indeed available to other phalaropes (Wilson's phala-

401

12. Feeding in Birds

organic ooze scraping mechanism

t

catching fish I shoveling shells 1 ^ grazing m's \ 1 A dabbling m's

\lt/

scaling of filter-feeding mechanisms

scaling of filter-feeding mechanisms

\t/

\t/

scaling of remote touch mechanisms stretching curved beak curving beak ^ combined vertical wedge mechanism \ remote 1 touch & \ 1 penetration filter-feeding m.

stab & crunch/ split & cut mechanisms

M

size & hardness recording touch mechanism: along jaw rami

L- , « , . back & forth pump mechanism

at jaw tips

M e r g u s (merganser)

Polysticta Somateria (eider) Aythya (scaup)

Limnodromus (dowitcher) Scolopax (woodcock) Calidris (stint, sandpiper) Gallinago (snipe) T r i n g a (shank)

A n a s (wigeon)

L i m o s a (godwit) Numenius (curlew) Philomachus (ruff)

\u

\

grubbing '^'''®^^ ^^^^^^ hunting m's horizontal wedge mechanism curving/scaling/widening' mechanism

\\t

t suction pressure pump mechanism

grazing & filter-feeding (water) hole inspection mechanism mechanisms A T / scaling curved beak / probing mechanisms i ^

substrate penetration mechanisms

deep probe-hunting mechanism

grasp-pump graze-filter

\f fetch and carry mechanism

^ »-

inspection/ turn-over/ chase m's

combined sight-peck & touch-probe m.

sit-watch & run-peck m. & superficial-probe m. stretch-catch m. & scaling , ^ _ ® T walk & peck mechanism top-soil breaking m. , ^ ^ fastened ingestion m. I sight-peck mechanism

f grasp mechanism shores/ wetlands

Ciconidae (storks) Ardeidae (herons)

Burhinidae (stone curlews) shorebird-like ancestor

G a l l i f o r m e s (fowl) C o l u m b i f o r m e s (doves) pecking ancestor

FIGURE 12.3. A hypothesis of phenotypic transformations of avian feeding systems resulting in probing and filter feeding. (A) The branching pattern and the mechanisms along it were deduced by modifications of a pecking mechanism, optimized for probing and filter-feeding functions. (B) A phenogram of hypothetical evolutionary change in avian feeding systems, produced by overlaying taxa with appropriate feeding systems on (A). Reproduced from Zweers and Vanden Berge (1997), with permission.

rope, P. tricolor), as well as other species of shorebirds, including western {Calidris mauri) and least (C. minutilla) sandpipers (Rubega, 1997). The latter two species generally feed by probing in sandy or muddy substrates, hence it is unlikely that STT is a specialization for an aquatic lifestyle. Second, it follows from the optimization criteria used by Zweers that character states within the shorebirds that deviate from this basic needle-like bill morphology are derived and thus will be accompanied by improved performance of some other (new) feeding mechanism. The physical model for STT requires that deviations from a straight needle-like bill will result in a reduction in performance of surface-tension feeding (Rubega and

Obst, 1993). Some evidence for intra- and interspecific STT performance variation exists (Rubega, 1996,1997), but sampling of a broader array of shorebird bill morphologies would be informative. One interesting observation points to the importance of detailed and quantitative performance testing: American avocets {Recurvirostra americana) hatch with a needle-like bill that subsequently develops into a structure that is markedly dorsoventrally flattened and recurved. Hatchlings employ surface-tension transport throughout the transition from one morphology to another (Harker, Rubega, and Oring, unpublished observation). Field observations indicate that mean feeding performance increases as chicks grow (i.e., during

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Margaret Rubega

the transition from a needle-shaped bill to one that is dorsoventrally flattened and recurved) (Harker and Rubega, unpublished observation). This appears to contradict the prediction that STT performance should decrease with deviations from a needle-shaped bill. These field observations, however, cannot distinguish improved performance at the individual level from improvements in the mean performance of age classes, which could result from the elimination of poorly performing individuals from the population by selection. Only quantitative measures of clearly defined performance characters under controlled conditions (i.e., in the laboratory) allow us to test directly the relationships between variation in morphology and feeding mechanics (e.g., Rubega, 1996). A third prediction of Zweers' model for the evolution of filter feeding is that character transformations, including increased bill volume, a tongue-based water pump, and straining structures, lead to a filter-feeding mechanism (Zweers et al., 1994). In its general outline of progression from a simple bill with low internal volume to a higher-volume, complex bill with filtering structures, this model is plausible, even compelling. As a phylogenetic hypothesis for the evolution of filter feeding in extant birds, the model is at odds with phylogenetic information, as it appears to suggest that the Anseriformes (the avian lineage in which filter feeding is most widespread and developed) arose from a shorebird (charadriiform) ancestor (Zweers and Vanden Berge, 1997; see Fig. 12.3B). All available evidence points to a sister-group relationship between the Anseriformes and Galliformes, which together form a clade that is the sister group of all other neognaths, with no special relationship to the charadriiform clade (Ho et al, 1976; Sibley et al, 1988; Cracraft, 1988). Nonetheless, it is conceivable that, despite their galliform relationship, anseriform ancestors had a simple, plover-like bill, which might have been subsequently modified for filter feeding. There is no paleontological evidence for or against this idea. With the proper sampling opportunities, however, we could test Zweers' ideas about the evolution of filter feeding within the Anseriformes. Although there are no anseriform extant taxa with Zweers' hypothesized ancestral plover-like (simple) bill morphology, the basic ideas of the model may be testable within the charadriiform lineage instead. For example, red phalaropes {Phalaropus fulicaria), which are so closely related to red-necked phalaropes as to be virtually indistinguishable genetically (Dittman et al, 1989; Dittman and Zink, 1991), have a bill that is wider and deeper (i.e., has a larger internal volume). Red phalaropes also have small internal bill structures that may be simple filtering systems (personal observation). Evidence shows that they select prey within

a rather narrow size range (Dodson and Egger, 1980; Mercier and Gaskin, 1985), as would be expected if filter size limits prey-capture performance. Red phalaropes thus provide a putative intermediary in which to examine the mechanistic predictions of the Zweers model for the evolution of filter feeding. If these predictions appear to be supported, it would be of interest to consider what factors may have prevented further evolution of filter feeding, which is otherwise not known to be present among the shorebirds. B. Inferring Function from Structure versus Tests of Hypotheses Possibly no group of vertebrates has a richer history of anatomical description than birds. Beginning with Aristotle, a long line of investigators has been carefully dissecting and describing birds in an attempt to understand their anatomy. From the 16th century onward, the detailed description oLanatomy was particularly important, second only to plumage descriptions (which were frequently all an investigator had, prior to the discovery of methods to preserve tissues) as a means of classification (Stresemann, 1975). When binoculars became widely available early in the 20th century, the focus of mainstream ornithology shifted to avian behavior, but beautiful and useful anatomical descriptions continued to be produced, particularly among German and Dutch investigators (e.g., Fiirbringer, 1922). While the anatomical descriptions in these studies were masterful and comprehensive, they constituted only the first step in understanding the role morphological structures play in avian feeding. Attempts to understand the anatomy they were describing naturally led investigators to formulate hypotheses about the function and evolutionary significance of various structures and structural complexes. Unfortunately, there has been a tendency in the ornithological literature to elevate such hypotheses to the status of fact. Nowhere has this practice been more evident than in the description of the avian feeding apparatus. Because of the obvious and dramatic modifications of the bill, there has been much speculation on the functional relationship between bill structures and feeding mechanics. In the most common approach, feeding mechanics are inferred from morphological features revealed by anatomical dissection, rather than directly observed or experimentally verified (see discussion in Chapter 1). This approach, dubbed "adaptive storytelling" in Gould and Lewontin's (1979) now-famous "Spandrels" paper and extensively criticized since, has been slow to fade in the avian literature and is still surprisingly common. An examination of the beaks of different birds that feed on the same prey provides

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12. F e e d i n g in Birds

ample demonstration that many tools can do one job (Fig. 12.4) and implies that they are unlikely to do the job in simple, easily predicted ways. It seems likely that adaptive storytelling about feeding in birds is driven more by what is already known about the diets of birds than by informed understanding about the relationship between feeding structures and function. Occasionally, the storytelling approach is given a veneer of experimentalism via manipulation of specimens in ways meant to reveal the functional relationship among structures (e.g., pulling on a muscle to see if the mouth opens). The weakness of this approach is nicely illustrated by Dial's (1992) study of the avian flight apparatus, which showed clearly that flapping flight in birds is powered by different muscles, firing at different times, than anatomical description and manipulation of dead specimens had led investigators to believe. The frequency of the earliest adaptive storytelling is not surprising, not least because many of the hypotheses generated by anatomists would have been difficult or impossible to test without modern technology. Nonetheless, adaptive storytelling appears to have persisted for a series of obvious and not-so-obvious reasons. First, it is, quite simply, easier to formulate a hypothesis than it is to test it. Even in the post-Spandrel era, when most investigators have learned to label clearly untested hypotheses as speculation, such hypotheses are often untested. For example, Zusi (1984) pointed out that hypotheses concerning cranial kinesis arising from his anatomical analysis of bony hinges in bird skulls should be tested against observations of bill movement in living birds. It appears they never have been. Sometimes this failure to follow-up tends to occur because our ideas about the relationship between form and function in avian feeding have not been translated into formalized, falsifiable null and alternative hypotheses, and thus are weak generators of testable predictions. For instance, ornithologists have long guessed that the unique spinning behavior of phalaropes serves to "stir u p ' ' prey from the bottoms of ponds and lakes where they were feeding, but this idea failed to explain why birds spin while at sea over water many fathoms deep. It was only when this idea was formalized into testable hypotheses about the specific patterns of water flow generated by spinning that it became possible to show that spinning by phalaropes does draw prey to the surface, but by creating an upwelling rather than by stirring {Ohstetal,1996). As in other vertebrates, it often is difficult even to guess how intricate structural complexes might function (e.g., there are many unanswered questions about the functioning of the avian tongue in feeding and drinking; Homberger, 1988), hence it is difficult to generate clear, testable predictions about the relation-

K ^ ^ . l } . . . . , "I rry

F I G U R E 12.4. An example of the diversity of feeding structures associated with feeding on a single prey type. All these species eat fish. (A) Brown pelican {Pelecanus occidentalis), (B) horned puffin {Fratercula comiculata), (C) common loon (Gavia immer), (D) shoebill {Balaeniceps rex), and (E) red-breasted merganser {Mergus senator). Drawings by M. J. Spring.

ship between parts and feeding mechanics. There appears to be no cure for this problem but creativity and empiricism.

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To some extent, untested hypotheses based only on descriptions of structure have also accumulated because birds are uniquely vagile organisms, thus the range of feeding circumstances is huge, and the opportunities for observation (much less manipulation) of live, feeding birds are limited. Taxa that feed in midair (e.g., flycatchers, see discussion later) or underwater (e.g., penguins, Spheniscidae, and auks, Alcidae) are particularly poorly known. Even when observation is possible and good hypotheses exist, in many cases there are significant technical barriers to testing hypotheses directly, e.g., the feeding event happens too rapidly to be discernable with the naked eye. For example, in rednecked phalaropes, surface tension transport can be completed in as little as 0.002 sec (Rubega and Obst, 1993) and would have been undetectable without the aid of high-speed videography. Occasionally, we fail even to discard hypotheses that have been falsified. For example, ornithologists have long guessed that the brush-like array of rictal bristles (feathers modified into fine, rather stiff, whiskers; Fig. 12.IF) present around the mouth margins of many species of fly-catching birds function to funnel prey into the gape. Lederer (1972) presented strong evidence that this is unlikely, and Conover and Miller's (1980) study of willow flycatchers {Empidonax traillii) clearly demonstrated that this is not the case. Birds caught prey equally well both before and after rictal bristles had been removed. Yet textbooks continue to assert that rictal bristles function as insect nets (e.g.. Gill, 1995). This may simply be a demonstration of the difficulty inherent to the dissemination of results at a time when investigators are more overwhelmed with new literature than ever before. Alternatively, this example may merely demonstrate that we are fonder of a good story than of the facts. This is unfortunate, as the facts generally are more interesting than any story we could make up. What are rictal bristles for? They are present to a greater or lesser extent in many birds (Lederer, 1972) (including birds such as kiwis, Dinornithiformes, flightless birds, which forage in leaf litter), but dense, basketlike arrays of them around the margins of the mouth have apparently arisen independently more than once in birds. A partial list of birds with prominent rictal bristles includes New World flycatchers (Tyrannidae), Old World flycatchers (Muscicapidae), shrikes (Lannidae), and frogmouths (Caprimulgidae). In all cases, insect capture on the wing is a significant part of the feeding biology. Conover and Miller (1980) presented evidence that rictal bristles may function to protect the eyes from strikes by missed prey or from parts of prey that may break up when seized. Increased emphasis on experimentalism and availability of new tools (e.g.. X-ray cineradiography and high-speed film and video) have contributed to a wel-

come and growing tendency to approach avian feeding with formalized hypothesis testing. Some recent examples include Benkman's elegant analysis of crossbill {Loxia sp.) feeding (Benkman, 1987,1988; Benkman and Lindholm, 1991); the impressive body of work amassed by Zweers and associates on greater flamingoes Phoenicopterus ruber (Zweers et al, 1995), pigeons (Zweers, 1982), ducks {Anas platyrhynchos, A. clypeata, and Ay thya fuligula) (Zweers et ah, 1977; Kooloos et ah, 1989), and sandpipers (Calidris sp.) (Gerritsen et ah, 1983; Gerritsen and van Heezik, 1985; Gerritsen and Meiboom, 1986); my own work on feeding mechanics in phalaropes (Rubega and Obst, 1993; Rubega, 1996,1997); Hulscher and Ens's (1991) analysis of the functional significance of bill shape in Eurasian oystercatchers {Haematopus ostralegus), and the clever experimental work of Piersma et al. (1998) on red knot prey detection mechanisms. In all these cases, real progress in our understanding of feeding in birds was achieved by the observation of live animals at close range under controlled (i.e., laboratory) conditions, inventive experimental approaches, the application of appropriate technology to reveal details of feeding mechanics, or all three. Most importantly, all these tools were employed in the deliberate testing of formalized, falsifiable hypotheses about the relationship of feeding structures to mechanisms of food capture and processing. C. Statistical Analysis, Sample Sizes, and the Importance of Variation Historically, investigators of feeding in birds have tended to base their studies on observations of few individuals. In some situations this is acceptable, but most of our understanding of avian feeding mechanisms is hampered by reliance on small sample sizes. Studies of avian feeding can be broken down into (1) those that primarily describe phenomena and (2) those that compare groups of organisms. Descriptions of phenomena do not require large sample sizes. A sample of one is sufficient to demonstrate that a structure or mode of feeding exists. Even in these studies, however, assessing whether the phenomenon occurs in more than one or two individuals is important to ensure that the observations are not aberrant. When one wants to compare groups (e.g., comparing structure among species or trying to relate performance to variation in morphology), a rigorous statistical analysis becomes important (Shaffer and Lauder, 1985a,b). Results of statistical analyses are only meaningful when applied to appropriate sample sizes. The vast majority of published studies of the feeding apparatus and feeding function, however, are based on fewer than five in-

12. Feeding in Birds dividuals (I am guilty of this myself: Rubega and Obst, 1993,1997); in many cases, the sample size is one. Why do avian feeding specialists persist in presenting results from such small samples? One of the most obvious reasons for this problem is the difficulty in obtaining, and keeping, sufficient numbers of live, healthy specimens. This problem is not unique to birds, but perhaps uniquely complicated by their volant nature. Birds can be much more difficult to catch than fish, lizards, or small mammals. Once caught, all but the smallest species of birds also require significantly more space and attention for captive maintenance. Experimental feeding setups for some species of birds (e.g., pursuit diving birds) can be too demanding of space and resources anywhere outside of a zoological park. Birds held in zoos are only rarely available for manipulative experiments. These problems are real, but by no means sufficient to explain the widespread lack of statistical rigor in the field. For example, warblers are completely unstudied with respect to feeding mechanics. Yet many species are widespread, abundant, easily caught in nets (as evidenced by the thousands banded yearly for studies of movement patterns), and require no more space for captive maintenance than a typical lizard or snake. The same is true for many other families of passeriform birds. Our failure to direct our attention to the opportunities present in these taxa is probably due to patterns identified earlier (see Section II,A). An important contributor to the lack of statistical rigor in the field is that journal editors and reviewers have continued to allow investigators of avian feeding mechanics to publish with small samples. This appears to be due, at least in part, to a tradition of belief that feeding patterns are "hardwired" (genetically inherited, rather than learned, and therefore largely invariant), thus a sample of one is as representative, and as informative, as a larger sample. As I have repeatedly pointed out, we actually have very little detailed information on the feeding process in birds, but we have enough to know that the notion of feeding patterns as invariant within a species must be at least partly false. First, although there is certainly a genetic component to control of the feeding process and development of the feeding apparatus in birds, it would be surprising in the extreme to find complete genetic fixation for most traits in the feeding complex. The huge range of variance in bill shape and feeding patterns across the class Aves attests, at a minimum, to the historical availability of population-level variation in feeding structures and selection for their modification. Further, evidence shows that extrinsic factors may influence adult bill morphology (and presumably feeding performance, if not pattern) via developmental plasticity James (1983) and NeSmith (1984; cited in Travis,

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1994), for example, showed that variation in temperature and humidity induces variation in bill shape of nestling red-winged blackbirds {Agelaius phoeniceus). The existence and importance of interspecific feeding variation have mostly been assumed on the basis of observed variation in bill morphology among related species or inferred from observations of differential habitat use and diets. Few direct comparisons of multiple species employing a common feeding mechanism on a standard food type have been conducted. Exploratory analyses (of data from a small sample of individuals) indicate that there is significant interspecific variation among four species of shorebird (red-necked phalarope, Wilson's phalarope, western sandpiper, and least sandpiper) in the performance of surface-tension feeding. Motor patterns are similar, but vary quantitatively among species (Rubega, 1997). Variance in feeding structures, process, and performance clearly exists within species as well. For example, it has been demonstrated repeatedly that juvenile birds exhibit poor feeding performance (usually expressed as feeding efficiency, or the catch-to-attack ratio; poor performance is also inferred from diet restricted to prey that is presumed to be less preferred) relative to their adult conspecifics (for reviews, see Marchetti and Price, 1989; Wunderle, 1991). Increasing age is associated with improved feeding performance. Explanations offered for this pattern of an ontogenetic feeding shift include learning, physical maturation of the feeding apparatus, variance in the nutritional status of juveniles relative to adults, and competitive suppression of juvenile feeding by adults. To date, none of these have been accompanied by formalized, testable hypotheses linking them to the feeding mechanism itself. Additional explanations that are well worth pursuing include the effects of neurological maturation, the possibility that juveniles may exhibit superior performance (relative to adults) of "juvenile" feeding mechanisms, and the likelihood that the perceived improvement in mean feeding performance with age is due to the elimination of poorly performing individuals from the population due to selection. Finally, significant variation in feeding within groups (among individuals) has also been demonstrated. Red-necked phalaropes exhibit significant among-individual variation in the performance of surface-tension feeding as a function of morphological variation of the inside of the upper jaw (Rubega, 1996). It should be apparent by this point in this chapter that, aside from the importance of accounting for variability when assessing the generality of our conclusions about avian feeding mechanisms, variance in avian feeding structures and mechanics is (or should be), in itself, a statistic of interest to us. This is especially true given the extreme degree of variation in feeding in birds overall relative to other vertebrates. In any group of

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vertebrates, variation (especially at the individual level) is the basis for selection and thus reflects the opportunity for, and outcome of, the evolution of feeding mechanics. In particular, attention to individual-level variation may be revealing with respect to the direction of selection, which in turn may provide us with clues as to which aspect of function is selectively most important.

III. C O N C L U S I O N The exceptional degree of variation in the avianfeeding apparatus has stimulated a large and interesting literature on beak and tongue morphology, feeding mechanics, and behavioral aspects of foraging. Much, however, remains to be done. I have tried to show that opportunities for significant new contributions to our understanding of feeding in birds are abundant. There is no widely accepted general theory explaining evolution of the observed diversity in avian feeding mechanisms. This is at least partly due to the complete lack of information about many species of birds: detailed analyses of feeding structures and function are lacking for more than half of all families of birds. To date our choice of taxa has been largely opportunistic. Significant advances will be made only when a phylogenetic strategy is applied to the problem of choosing study taxa. Further advances will also require the controlled testing of formal hypotheses about the relationship of feeding structures to some aspect of function or performance, and coding of feeding mechanisms in ways that allow cross-taxa comparisons. Although the difficulties inherent in maintaining birds in captivity are not trivial, our confidence in the outcome of comparative studies will depend on statistically appropriate sample sizes, however difficult they may be to attain. Some of the tools required to achieve these goals (such as high-speed video cameras and family-level phylogenetic hypotheses) are increasingly available. Widely and properly applied, they could produce a renaissance in the study of avian feeding. Even in the absence of a renaissance, we stand to learn a great deal more about feeding in birds. References Benkman, C. W. (1987) Crossbill foraging behavior, bill structure, and patterns of food profitability. Wilson Bull. 99:351-368. Benkman, C. W. (1988) On the advantages of crossed mandibles: an experimental approach. Ibis 130:288-293. Benkman, C. W., and A. K. Lindholm (1991) The advantages and evolution of a morphological novelty. Nature 349:519-20.

Bent, A. C. (1927) Life histories of North American shore birds. Order Limicolae (Part I). U. S. National Museum Bulletin 142. Berkhoudt, H. (1985) Structure and function of avian taste receptors. In: Form and Function in Birds, Vol. 3. A. S. King and J. McClelland (eds). Academic Press. Bermejo, R., R. W. Allan, D. Houben, J. D. Deich, and H. P Zeigler. (1989) Prehension in the pigeon. I. Descriptive analysis. Exp. Brain Res. 75:569-576. Bhattacharyya, B. N. (1980) The morphology of the jaw and tongue musculature of the common pigeon, Columba livia, in relation to its feeding habit. Proc. Zool. Soc. Calcutta 31:95-127. Boag, P. T, and P. R. Grant (1981) Intense natural selection in a population of Darwin's finches (Geospizinae) in the Galapagos. Science 214:82-85. Bock, W. J. (1960) The .palatine process of the premaxilla in the Passere. Bull. Mus. Comp. Zool. 122(8):361-488. Burton, P. J. K. (1984) Anatomy and evolution of the feeding apparatus in the avian orders Coraciiformes and Piciformes. Bull. Brit. Mus. (Nat. Hist.) 47(6): 331-443. Brooks, D. R., and D. A. McLennan. (1991) Phylogeny, Ecology and Behavior; a Research Program in Comparative Biology. University of Chicago, Chicago. Calhoim, M. L. (1933) The microscopic anatomy of the digestive tract of Gallus domesticus. Iowa State Coll. J. Sci. 7:261-382. Conover, M. R., and D. E. Miller (1980) Rictal bristle function in willow flycatcher. Condor 82:469-471. Cracraft, J. (1988) The major clades of birds. In: The Phylogeny and Classification ofTetrapods, Vol. 1. M. J. Benton (ed). Systematics Association Special Volume No. 35A. Clarendon Press, Oxford. Darwin, C. 1859. On the Origin of Species hy Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London. Del Hoyo, J., A. Elliott, and J. Sargatal (eds.) (1992) Handbook of the Birds of the World Vol. 1. Lynx Edicions, Barcelona. Dial, K. P. (1992) Avian forelimb muscles and nonsteady flight: can birds fly without using the muscles in their wings? Auk 109: 874-885. Dittman, D. L., and R. M. Zink (1991) Mitochondrial DNA variation among phalaropes and allies. Auk 108:771-779. Dittman, D. L., R. M. Zink, and J. A. Gerwin. (1989) Evolutionary genetics of phalaropes. Auk 106:326-331. Dodson, S. I., and D. L. Egger. (1980) Selective feeding of red phalaropes on zooplankton of Arctic ponds. Ecology 61:755-763. Fiirbringer, M. (1922) Das Zungenbein der Wirbeltiere insbesondere der Reptilien und Vogel. Abhandlungen der Heidelberger Akademie, math.-nathurw. Kl. Abt.B 11:1-164. Gerritsen, A. F. C , and A. Meijboom (1986) The role of touch in prey density estimation by Calidris alba. Neth. J. Zool. 36:530-562. Gerritsen, A. F. C , and Y. M. van Heezik (1985) Substrate preference and substrate related foraging behavior in three Calidris species. Neth. J. Zool. 35:671-692. Gerritsen, A. R C , Y. M. van Heezik, and C. Sweenen (1983) Chemoreception in two further Calidris species: Calidris maritima and C. canutus; a comparison of the relative importance of chemoreception during foraging in Calidris species. Neth. J. Zool. 33: 485-496. Gill, R B. (1995) Ornithology, 2nd Ed. Rreeman, New York. Goodman, D. C , and H. I. Fisher (1962) Functional Anatomy of the Feeding Apparatus in Waterfowl (Aves: Anatidae). Southern Illinois University Press, Carbondale, IL. Gottschaldt, K. M. (1985) Structure and function of avian somatosensory receptors. In: Form and Function in Birds, Vol. 3. A. S. King and J. McClelland (eds). Academic Press, New York. Gould, S. J., and R. C. Lewontin (1979) The spandrels of San Marco

12. Feeding in Birds and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B 205:581-598. Grant, P. R. (1985) Selection on bill characters in a population of Darwin's finches: Geospiza conirostris on Isla Genovesa, Galapagos. Evolution 39:523-532. Ho, C. Y.-K., E. M. Prager, A. C. Wilson, D. T. Osuga, and R. E. Feeney (1976) Penguin evolution: protein comparisons demonstrate phylogenetic relationships to flying aquatic birds. J. Mol. Evol. 8: 271-82. Homberger, D. G. (1986) The Lingual Apparatus of the African Grey Parrot Psittacus erithacus Linne (Aves: Psittacidae): Description and Theoretical Mechanical Analysis. Ornithological Monograph No. 39. American Ornithologists' Union, Washington. Homberger, D. G. (1988) Comparative morphology of the avian tongue. In: Acta XIX Congressus Internationalis Ornithologici, Vol. II. H. Ouellet (ed). University of Ottawa Press, Ottawa. Homberger, D. G., and R. A. Meyers (1989) Morphology of the lingual apparatus of the domestic chicken, Gallus gallus, with special attention to the structure of the fasciae. Am. J. Anat. 186:217-257. Hulscher, J. B., and B. J. Ens (1991) Somatic modifications of feeding system structures due to feeding on different foods with emphasis on changes in bill shape in Oystercatchers. Acta XX Congr. Inter. Ornith. Symposium 13:889-896. James, F. C. (1983) Environmental component of morphological differentiation in birds. Science 221:184-186. Jehl, J. R. (1986) Biology of the red-necked phalarope (Phalaropus lobatus) at the western edge of the Great Basin in fall migration. Great Basin Nat. 46:185-197. Jenkin, P. M. (1957) The filter feeding and food of flamingoes (Phoenicopteri). Phil. Trans. Roy. Soc. Lond. B 240:401-493. Kear, J. and N. Duplaix-Hall (1975) Flamingos. Poyser, Berkhamsted, UK. Kooloos, J. G. M., A. R. Kraaijeveld, G. E. J. Langenbach, and G. A. Zweers (1989) Comparative mechanics of filter feeding in Anas platyrhynchos, Anas clypeata, and Aythya fuligula (Aves, Anseriformes). Zoomorphology 108:269-290. Krajewski, C. (1989) Phylogeny and classification of birds: a study in molecular evolution. Auk 108:987-990. Krebs, J. R., and N. B. Davies (1991) Behavioural Ecology: An Evolutionary Approach. Blackwell, Oxford. Lanyon, S. M. (1992) Phylogeny and classification of birds: a study in molecular evolution. Condor 94:304-307. Lauder, G. V. (1989) How are feeding systems integrated, and how have evolutionary innovations been introduced? In: Complex Organismal Functions: Integration and Evolution in Vertebrates. D. B. Wake and G. Roth (eds). Wiley, Chichester. Lederer, R. J. (1972) The role of avian rictal bristles. Wilson Bull. 84: 193-197. Losos, J. B., and D. B. Miles (1994) Adaptation, constraint, and the comparative method: phylogenetic issues and methods. In: Ecological Morphology, P. C. Wainwright and S. M. Reilly (eds). University of Chicago, Chicago. Lucas, A. M., and P. R. Stettenheim (1972) Avian Anatomy, Integuement. Agricultural Handbook No. 362. U. S. Government Printing Office, Washington, DC. Marchetti, K., and T. Price (1989) Difference in the foraging of juvenile and adult birds: the importance of developmental constraints. Biol. Rev. 64:51-70. McClelland, J. (1979) Digestive system. In: Form and Function in Birds, Vol. 1. A. S. King and J. McClelland (eds). Academic Press, New York. Mercier, F., and D. E. Gaskin (1985) Feeding ecology of migrating red-necked phalaropes {Phalaropus lobatus) in the Quoddy region. New Brunswick, Canada. Can. J. Zool. 63:1062-1067

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Zweers, G. A. (1991b) Pathways and space for evolution of feeding mechanisms in birds. In: The Unity of Evolutionary Biology, E. C. Dudley (ed). Dioscorides Press, Portland. Zweers, G. A., H. Berkhoudt, and J. C. Vanden Berge (1994) Behavioral mechanisms of avian feeding. Pp. 241-279, In: Advances in Comparative and Environmental Physiology, Vol. 18. V. L. Bels, M. Chardon, and P. Vandewalle (eds.). Springer-Verlag, Berlin. Zweers, G. A., F. de Jong, H. Berkhoudt, and J. C. Vanden Berge (1995) Filter feeding in flamingos (Phoenicopterus ruber). Condor 97:297-324. Zweers, G. A., and A. F. C. Gerritsen (1997) Transitions from pecking to probing mechanisms in waders. Neth. J. Zool. 47:161-208. Zweers, G. A., A. F. C. Gerritsen, and P. J. van Kranenburg-Vood (1977) Mechanics of feeding of the mallard (Anas platyrhynchos L.; Aves, Anseriformes). Contrib. Vert. Evol, Vol. 3. Karger, Basel. Zweers, G. A., and J. C. Vanden Berge (1997) Evolutionary transitions in the trophic system of the wader-waterfowl complex. Neth. J. Zool. 47:255-287.