chapter 17 feeding in birds: thriving in terrestrial

Chapter 17Feeding in Birds: Thriving in Terrestrial,Aquatic, and Aerial Niches

Alejandro Rico-Guevara, Diego Sustaita, Sander Gussekloo, Aaron Olsen,Jen Bright, Clay Corbin and Robert Dudley

Abstract Westartwith a general description of the structure of the feeding apparatusin birds (Sect. 17.1), then we describe the biomechanics of those parts (Sect. 17.2),including a review of contemporary approaches to the study of bird feeding mor-phology and function. We establish explicit links between form and function, andconsequent relations to foraging behaviors. In Sect. 17.3, we systematically explorethe vast diversity of bird feeding environments by grouping foraging (searching) and

A. Rico-Guevara (B)Department of Integrative Biology, University of California, Berkeley, CA 94720, USAe-mail: [email protected]

D. SustaitaDepartment of Biological Sciences, California State University San Marcos, 333 S.Twin Oaks Valley Road, San Marcos, CA 92096, USAe-mail: [email protected]

S. GusseklooDepartment of Animal Sciences, Experimental Zoology Group, P.O. Box 338 6700AH,Wageningen, The Netherlandse-mail: [email protected]

A. OlsenDepartment of Ecology and Evolutionary Biology, Brown University,171 Meeting St, Box G-B 204, Providence, RI 02912, USAe-mail: [email protected]

J. BrightSchool of Geosciences, University of South Florida, 4202 E. Fowler Avenue, NES 107, Tampa33620, USAe-mail: [email protected]

C. CorbinDepartment of Biological and Allied Health Sciences,Bloomsburg University, Bloomsburg, PA 17815, USAe-mail: [email protected]

R. DudleyDepartment of Integrative Biology, University of California,3040 Valley Life Sciences Building # 3140, Berkeley, CA 94720-3140, USAe-mail: [email protected]

Smithsonian Tropical Research Institute, Balboa, Republic of Panama

© Springer Nature Switzerland AG 2019V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates,Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_17

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feeding (handling—consumption) mechanisms that birds use on land, air, and water.Each one of these subsections addresses not only what birds eat, but also how theyfeed. We dedicate a separate Sect. (17.4) to drinking because most birds have toperform this process regardless of their diet, and often using different mechanismsthan the ones they use to feed. We then discuss evolutionary forces and patterns inbird feeding (convergences, radiations, trade-offs, etc.), including functions differ-ent from handling and ingestion that also act to shape the feeding apparatus in birds(Sect. 17.5).

17.1 Introduction: Anatomical Features of the AvianFeeding Apparatus

17.1.1 General Functional Morphology of the Beak

The beak is the obvious place to begin to describe the avian feeding apparatus,although many other post-cranial features, such as the wings and feet, play criticalroles in getting birds to their food, or in getting food to the bird’s beak. The beak ispart of an integrated jawmechanism, whose individual parts (and interactions amongthem) are more intimately described in Sect. 17.2.2. Here we focus primarily on themorphology of the beak, as the implement that interacts directly with the environ-ment. Over the past 10–15 years we have gained tremendous insights into the geneticbases of beak development (e.g., Abzhanov et al. 2006;Mallarino et al. 2011; Bhullaret al. 2015), and how beak form and function are shaped by the loading patterns theyexperience (e.g., Herrel et al. 2010; Soons et al. 2010). The evo-devo of bird beaks isbeyond the scope of this section (but see Bhullar et al. 2015). However, it is relevantto note that distinct sets of genes guiding the development of the prenasal cartilages(e.g., Bmp4, CaM) and premaxillary bones (TGFβIIr, β-catenin, and Dkk3) ulti-mately control different dimensions (Mallarino et al. 2011), and thereby enable agreat diversity of shapes, sizes, and functions.

The bony structure of the beak is dominated by the premaxillary, maxillary, andnasal bones of the upper bill, and the dentary bone of the lower bill (Baumel andWit-mer 1993; Fig. 17.1). Other bony elements connected to these bones (jugal, palatine,pterygoid, articular, and quadrate bones) play important roles in the transmissionof forces (Bowman 1961; Soons et al. 2010; Herrel et al. 2010) and kinetic move-ments (Bock 1964; Zusi 1984; Bout and Zweers 2001; Gussekloo et al. 2001), butthese are removed from direct contact with food and/or substrates and are treatedbelow (Sect. 17.2.2). The premaxilla is arguably the principle element involved indistributing and dissipating forces (Mallarino et al. 2011), and the internal scaffold-ing (trabeculae; Fig. 17.2) plays a key role in transmitting forces and in dictating itsability to withstand external loads (Bock 1966; Genbrugge et al. 2012; Seki et al.2005, 2006). Genbrugge et al. (2012) found that, among Darwin’s finches, trabeculardensities of the upper bill vary according to the loading regimes imposed by different

17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 645

Fig. 17.1 Illustration of the lateral view of a rock pigeon (Columbia livia) skull. Reproduced fromProctor and Lynch (1993), with permission from Yale University Press

feeding habits among the species studied. The orientation of the trabeculae seemsto correspond to tensile and compression trajectories. Bock (1966) proposed thatthese trabeculae transmit forces from their points of application along the bill to theload-bearing compact bone of the outer walls, which in turn transmits stresses to thebase of the jaw. Species with different bill morphologies appear to be well adaptedfor specific loading conditions: species that tend to apply forces at the beak tipsexperience relatively lower bone stresses and higher safety factors under tip-bitingloads than those that tend to crush seeds at the beak base (Herrel et al. 2010; Soonset al. 2015).

The beak is not all bone, however, and the overlying keratinous rhamphothecaplays an important role in dictating overall beak shape and its feeding performancecapabilities (Fig. 17.2). Campàs et al. (2010) found that in Geospiza finches, thekeratin layer closely corresponds to the shape of the underlying bone, and these arerelated by simple scaling transformations. In other groups, however, there is morediscordance between the shape of the rostrum maxillare (union of the bony premax-illae) and that of the overall rhamphotheca (Urano et al. 2018). This is evident inthose species with strongly curved culmens and hooked beaks, such as parrots andraptors. These, and other, groups display a variety of tomial projections, such asthe serrations of piscivorous birds, geese, and hummingbirds, which are thought toplay roles in grasping food items, and also in the case of hummingbirds, male–malecombat (Rico-Guevara and Araya-Salas 2015; Rico-Guevara and Hurme 2019). The“tomial teeth” of falcons, shrikes (Fig. 17.2) and possibly those of some barbets,are thought to be important for prey-processing (Cade 1995; Csermely et al. 1998).These may or may not correspond to underlying bone structures; for example, inshrikes these tomial structures are entirely keratinous (Fig. 17.2), whereas in falconsthey are underlain by bone (Schön 1996). The baleen-like projections (lamellae) ofmany ducks and flamingos that are vital for filter-feeding (Fig. 17.3; Louchart and


Fig. 17.2 Upper panel: loggerhead shrike (Lanius ludovicianus) showing the hooked beak tip andtomial “tooth” (ventral projections of the rhamphotheca on either side of the tomium of the rostralupper beak). Lower panel: radiograph of a northern shrike (Lanius borealis) beak, showing theunderlying bony trabeculae and the overlying keratinous rhamphotheca that formulates the hookedtip (a) and tomial “tooth” (b) of the upper bill (Images are not shown to scale)

Viriot 2011), are made of keratin and not underlain by bone. Because keratin is adynamic tissue that continuously grows andwears, beak shape can change plasticallyover relatively short periods of time (Matthysen 1989; Van Hemert et al. 2012). Thiscould be significant because very small changes in beak size (let alone shape) couldhave profound functional and fitness consequences (Newton 1967; Benkman 2003).In addition to its role in effecting size and shape, the rhamphotheca contributes sub-stantially to the structural integrity of the bill. Even though keratin exhibits roughlyhalf the stiffness (i.e., Young’s modulus) of bone (Seki et al. 2006; Soons et al. 2012;Lee et al. 2014), the layering of keratin, cortical, and cancellous bone acts syner-gistically to absorb more energy in stress dissipation than they would independently(Seki et al. 2006; Soons et al. 2012, 2015).

Not only does the rhamphotheca provide the tools for feeding (and preening),but there are also mechanosensors, such as Herbst and Grandry corpuscles, presentthat provide tactile information (Berkhoudt 1979). An extreme adaptation has beendescribed for the red knot (Calidris canutus), which uses Herbst corpuscles todetect pressure fields in wet substrates as induced by bill insertion and consequently


Fig. 17.3 Oropharynx of three different species with increasing feeding apparatus complexity.a Greater rhea (Rhea americana, Gussekloo and Bout 2005), b chicken (Gallus gallus, Heidweileret al. 1992), c mallard (Anas platyrhynchos, Kooloos et al. 1989). The top images show the roofof the oropharynx, the bottom images show the floor of the oropharynx. (1) choanae, (2) papillachoanales, (3) rima infundibuli, (4) papillae linguae caudales, (5) papilla pharyngis caudodorsales,(6) papillae pharyngis caudoventrales, (7) ruga palatina mediana, (8) rugae palatinae laterales (lineindicates left one), (9) papillae palatinae, (10) lamellae rostri (maxillary/mandibulary lamellae), (11)alae linguae, (12) torus linguae, (13) torus palatina, (14) papillae linguae lateralis, (15) sulci palatini,(16) papillae pharynges, (17) radix linguae, and (18) glottis. Panel a reprinted with permission ofthe authors. Panels b and c reprinted by permission from Springer Nature, Zoomorphology


reflected off buried mollusc prey (Piersma et al. 1998). Although this particularbehavior has only been described for the red knot, similar high receptor densitiesand associated adaptations in the brain have been observed in other probing birds(Cunningham et al. 2013).

Although it seems clear that the rhamphotheca mainly shows adaptations to feed-ing behavior, other functions affect the rhamphotheca aswell (Sect. 17.5.2.3). A num-ber of songbirds (Belding’s sparrow, Passerculus sandwichensis beldingi; Alamedasparrow,Melospizamelodia pusillula; lark bunting, Calamospizamelanocorys) showclear sexual dimorphism and seasonal changes in their bill shape indicating that thebill plays a role in the sexual display (Chaine and Lyon 2008; Greenberg et al. 2013).In addition, the study of a wide range of avian species has shown a strong correlationbetween bill length and ambient temperature, with shorter bills in colder environ-ments. This shows that the bill might contribute to heat loss and thus can play animportant role in the cost of thermoregulation (Symonds and Tattersall 2010).

17.1.2 Morphology and Evolution of the Avian LingualApparatus

The tongue is a key evolutionary novelty for terrestrial feeding (Schwenk 2000;Chap. 11), largely overlooked in earlier studies of feeding mechanics (Schwenk andRubega 2005). Furthermore, the evolution of flight and consequent diversificationof feeding ecologies has been recently linked to the elaboration of tongue struc-ture and function (Li et al. 2018). For pragmatic purposes, here we define the aviantongue as the discrete, rostralmost portion of the lingual apparatus (bones, muscles,nerves, epithelia, etc., detailed in Homberger 2017), which is typically rigid, coveredby keratinized epithelium, and that is mostly enclosed within the oral cavity (sensuLucas and Stettenheim 1972); sometimes also called the “free part of the tongue”or lingual body (Homberger and Meyers 1989; Homberger 2017). Avian tonguesrange from vestigial (e.g., pelicans; McSweeney and Stoskopf 1988) to extensivelyelaborate (e.g., ducks, Kooloos et al. 1989; Fig. 17.3). Bird tongue bones, attachedmuscles, and innervation are derived from the ancestral gill arch (branchial) skeleton,as in all tetrapods (reviews in Schwenk 2000; Iwasaki 2002; Hill et al. 2015). Thisis why the group of “tongue bones” is referred to as the apparatus hyobranchialis(or hyobranchium). In birds, this hyoid skeleton is composed of six main elements(arranged rostrally to caudally): (1) paraglossum, a paired element usually fusedinto a single structure in adults, which is commonly shaped as an arrow head and itis embedded in the tongue, sometimes with cartilaginous ends; (2) basihyale, nor-mally flattened and allowing the widest range of rotation at the “joints” with theparaglossum and the ceratobranchials; (3) urohyale, in most cases fused to the cau-dal end of the basihyale in adults, with a cartilaginous end, and sometimes absentaltogether; (4) ceratobranchiale, slender, paired and cylindrical, normally ossified(in some cases the only element ossified), and usually the longest elements except


in birds with extreme tongue protrusion; (5) epibranchiale, paired, cylindrical, andabutting upon the caudal end of the ceratobranchials, they are the elements that, whenelongated to allow great protrusion, reach the maximum relative length among birds;(6) pharyngobranchiale, attached to the end of the epibranchials, they are normallycartilaginous, and in some cases are reduced or absent (Fig. 17.4a; Lucas 1895;Zweers 1982; Homberger 1986; Baumel and Witmer 1993; Tomlinson 2000; Gen-brugge et al. 2011; Rico-Guevara 2014; Homberger 2017). These main hyobranchialelements have a long list of synonymies; in some cases, these main parts presentprocesses, extensions, accessory elements, and vary from cartilaginous to ossifiedacross bird clades (e.g., Bock and Morony 1978; Zweers 1982; Homberger 1986;Homberger and Meyers 1989; Tomlinson 2000).

Similar to amphibians (Chap. 12) and crocodilians (Chap. 15), most avian tongueslack the intrinsic musculature characteristic of the rest of tetrapods [except somegroups that use their tongues to collect and/or manipulate their food, e.g., parrots,(Homberger 1986), andwoodpeckers (Bock 1999)]. Avian tongues are comparativelysimple among tetrapods regarding internal musculature (Schwenk 2000), yet theycan be very sophisticated depending upon their role in the feeding process (intrao-ral transport, food collection and/or manipulation, etc., Fig. 17.4). The evolution ofgizzards in archosaurs released their jaws from food processing (review in Reillyet al. 2001) and bird bills and tongues are exclusively food gathering as opposed toprocessing tools, which is an important factor in mammalian jaw evolution (Chaps.18–21). During this transition, birds have compensated for the diminished manipu-lative capabilities of a non-fleshy tongue by developing truly mobile “hyobranchialjoints”. In addition, the bird hyobranchium and associated musculature appear morerostral when compared to other reptiles (Tomlinson 2000), which is probably linkedto the disappearance of the ceratohyals [which are not used in displays like in lep-idosaurs (Bels et al. 1994; but see Riede et al. 2015)], and the avian apomorphicparaglossum offers reach and support to the largely keratinous tongue (Tomlinson2000; Hill et al. 2015). This keratinization and stratification of the lingual epitheliumlikely evolved during the transition from wet to dry environments in bird ancestors(Iwasaki 2002). We propose that the appearance of cornified tongue tissues, alongwith the shift from food processing to also gathering, facilitated the development ofintricate lingual surface structures and complex structural configurations that allowedsome bird groups to excel in specialized niches (e.g., tongues covered with hair-likestructures in filter feeders, barbed tongues in penguins, tongues with spear-shapedtips in woodpeckers, tubular tongues in hummingbirds). Avian tongues, althoughusually hidden, could be considered as diverse and plastic as bills, and have playeda key role in the evolution of birds, the group with one of the most morphologicallyvaried array of feeding structures among tetrapods (Rubega 2000).

Bird tongues present cases of tremendous specialization and may differ dramati-cally from one another, however, a general design can be identified for most of themwith the following parts (from rostral to caudal): (1) apex linguae, or tongue tip,usually only composed of lamina propria (connective tissue layer) between dorsaland ventral epidermal epithelia, the external keratinized layer of the tongue epitheliaat the apex is thicker in the ventral surface, sometimes frayed and in extreme cases


Fig. 17.4 Avian hyobranchium and tongue. a Idealized dorsal aspect of the tongue bones, orhyobranchium, with the tongue overlaid in gray on top. b Dorsal view of the tongue; the Latinword “linguae” which means “of the tongue” has been removed from all the terms for clarity. Seetext for definitions of all the components. c Lateral view of the tongue body and root during foodtransport. dMost birds use their protrusible hyobranchia and tongues to move food to their throatsby placing it behind the tongue wings. Cedar waxwing (Bombycilla cedrorum) photographs by KimMichaels

developing as cuticula cornificata linguae (lingual nail); as the first contact pointwith the food, the apex is modified in a variety of ways, including lance-shapedwith lateral barbs, fraying along all edges, sometimes cleft to deeply bifurcated, andothers with fringed margins curling to form one to several tube-like grooves; (2)corpus linguae, or tongue body, usually wedge-shaped tapering rostrally, in mostcases the paraglossum is the only reinforcing element, although the basihyale couldalso be partially to completely embedded as well; the tongue body usually containsa variety of lingual glands, connective and adipose tissue, and sometimes corporacavernosa; (3) dorsum linguae, or dorsal surface, usually made of keratinized epithe-lium stratificatum squamosum (cornified epidermis), it sometimes presents a mediansulcus (longitudinal shallow groove); in the tongue body, the keratinized layer is


thicker in the dorsal surface (in contrast with the apex); (4) margo linguae, or lateraledges, present most of the papillary projections (besides the papillary crest), modi-fications include backward-facing serrated margins, spine-like projections, hair-likelaterally projected filiform papillae, and forward-facing frayed margins; (5) ventrumlinguae, or ventral surface, it is usually convex transversely, smoother, with a thinnerepithelial layer and a thicker lamina propria than the dorsal side; the hyoid elementsare closer to the ventrum than to the dorsum, and in some cases the ventrum is foundon the dorsal side of the tongue due to lingual folding; (6) papillae linguae caudales,or the papillary crest at the tongue base, consists of one or more transverse rowsof spine-like, sometimes conical, papillae pointing caudally and of varying sizes,which normally follow the caudal contour; sometimes absent; (7) alae linguae, ortongue wings, are also referred to as giant conical papillae, and are largely supportedby caudally directed paraglossal projections forming an inverted “V” at the tonguebase; sometimes absent altogether; (8) radix linguae, or tongue root, is a distinctivesupport structure extending from the ventrum; it usually contains the basihyale thusallowing a hinge for the rest of the tongue (Fig. 17.4b, c, Lucas 1895; Zweers 1982;Homberger 1986; Baumel and Witmer 1993; Tomlinson 2000; Erdogan and Iwasaki2014; Homberger 2017). A list of synonymies of these main lingual componentssimilar to those existing for the hyobranchial skeletal elements and musculature hasnot been yet provided.

17.1.3 Other Structures of the Oropharynx

Within the avian oropharynx, we find a completely different set of structures thatplay a role in feeding behavior. In many species, we find papillae on a numberof locations and structures inside the oral cavity. The most common locations forpapillae are around the choanae, near the base of the tongue, and just caudal to theepiglottis. In some species, such as the chicken, papillae are found on almost thecomplete roof of the oropharynx. It is assumed that most of these papillae play arole in intraoral food transport, either for holding the food item or for transporting ittowards the oesophagus.

Salivary glands in the oral cavity also play a role in intraoral transport. Theseglands are dispersed over the whole oropharynx, although some regions have higherdensities and are considered separate glands [see (McLelland 1979)]. In most cases,they provide lubrication for the food (McLelland 1979), which is reflected in thevariation among birds with different diets. In general, for birds eating dry fooditems, such as granivorous birds, the salivary glands are large, whereas in fish-eatingbirds they are almost absent (Denbow 2015). In birds using the “slide-and-glue”mechanism for intraoral transport (Zweers et al. 1994), such as pigeons (Zweers1982) and chickens (Van den Heuvel and Berkhoudt 1997), saliva is even moreimportant for intraoral transport as it actually glues smaller food items to the tongueto facilitate transport towards the oesophagus. Information about enzymatic actionwithin the saliva is sparse.


Although less prominent than in other vertebrates, several taste buds can be foundin the oropharynx of birds, sensing all traditional tastes (Roura et al. 2013). Anoverview of seven bird species shows a taste bud number varying from 5 to 400,whereas in mammals it ranges from 473 to 35,000 and in catfish this number evenreaches 100,000 (Clark et al. 2015). It must, however, be kept in mind that theseare absolute numbers, and the 35,000 taste buds found in an ox is obviously muchlarger than even the largest bird. The location of the taste buds is mainly in thenon-keratinized roof and floor of the oropharynx and on the root of the tongue,and often in close proximity to the salivary glands (Berkhoudt 1985), although theyare occasionally also found in the rhamphotheca (Crole and Soley 2015). Birds, ingeneral, seem to have receptors for all five tastes (sweet, salt, bitter, sour, and umami)(Roura et al. 2013; Clark et al. 2015), but the actual ratio among them can vary amongspecies. Frugivorous and omnivorous birds have more affection for sweet tastes thanother trophotypes, with an extreme case in the granivorous chicken that seems to lackthe sweet taste receptor completely (Lagerström et al. 2006; Shi and Zhang 2006).Salt is detected by a large variety of birds, but rejection thresholds vary stronglyfrom 0.35% to over 35.0% (Rensch and Neunzig 1925). Analyses of bitter receptorgene clusters showed a number of variations in the receptors indicating that bitteris probably perceived in different ways in different populations and species (Daviset al. 2010). Because bitterness is often an indicator for toxic substances in the food(Davis et al. 2010), birds tend to reject food with a bitter taste (Roura et al. 2013;Clark et al. 2015). The behavioral reactions to sour have been mainly investigated inchickens and little is known from other species. In chickens, the general pattern isthat extreme pH values are avoided (Roura et al. 2013). The final taste, umami, hasonly been predicted based on the fact that in the chicken genome genes have beenfound similar to the umami receptor genes in other vertebrates (Shi and Zhang 2006).Affinity to umami tastes have been shown in a few experiments (e.g., Espaillat andMason 1990; Moran and Stilborn 1996) but more research is needed to elucidate theactual umami perception of birds.

In summary, the oropharynxes of birds show a large number of adaptations tospecific feeding behaviors, including prey detection, food capture, food assessment,and the intraoral transport of the food.

17.2 From Feeding Apparatus Morphology to FeedingBiomechanics

17.2.1 The Study of Bird Feeding

Bird bills come in a truly astonishing variety of shapes and sizes. This variationis often associated with specific feeding behaviors that exert strong selective pres-sures on cranial architecture (Grant and Grant 1993), and with this relationship soimmediately apparent, it is perhaps unsurprising that few studies have bothered to


quantitatively link bill shape and function. Rubega (2000) identified the danger here,pointing out three key areas that needed to be addressed in future studies of birdfeeding. The first was a bias in phylogenetic sampling, with the majority of workheavily focused on model groups such as Darwin’s finches, convenient domesticbirds, or species whose unusual behavior or morphology made them of particularinterest. The second was that many studies make functional assertions based on mor-phology alone, and lack explicit hypotheses. Birds are rife with many-to-one andone-to-many mapping (Lauder 1995) between diet and bill structure; for example,one bill shape in omnivorous birds such as crows (Corvus sp.) permits access tomany different food items, and conversely, many different bill shapes (e.g., pelicans,puffins, kingfishers) are adapted for catching fish. Thus, when considering feeding,the diet of the bird may be of less importance than the way that the food is obtained,and precise biomechanical hypotheses and predictions are necessary. These can bedifficult to define, needing clear differentiation between colloquially interchangeablebut scientifically precise terminology surrounding function, performance, and role(Homberger 1988; Lauder 1995). Finally, and associated with the first two problems,many bird feeding studies are limited by small sample sizes and a lack of statisticalpower. Consequently, we know very little about how bill shape responds to feedingselection versus other factors, such as phylogenetic relatedness, development, andsexual selection. Indeed,manynon-feeding functions and behaviors, such as preening(Clayton et al. 2010), competition and territoriality (Rico-Guevara and Araya-Salas2015), thermoregulation (Tattersall et al. 2009), and vocalization (Huber and Podos2006; Giraudeau et al. 2014) impose other selective pressures in ways we are onlybeginning to understand.

In addition to in vivo experimentation, a range of modeling methods may beemployed to investigate the functionof avian feeding structures. Themost appropriatemethod will depend on the hypothesis being tested, but all models will be groundedin a knowledge of anatomy. Information on shape may be supplemented by muscledata from traditional (Baumel et al. 1993) or digital dissection (Lautenschlager et al.2014;Quayle et al. 2014), electromyography (Zweers 1974), and kinematic data fromhigh-speed video (Rico-Guevara and Rubega 2011; Sustaita et al. 2018b), Roentgenstereophotogrammetry (Gussekloo et al. 2001) andX-ray Reconstruction OfMovingMorphology (XROMM, Dawson et al. 2011). This provides valuable physiologicalbrackets for the model input parameters. Models need not be overly complicated.Despite their simplicity, lever diagrams and bar linkages are immensely useful toolsfor calculating crucial performance metrics such as bite force (Sustaita 2008) andmechanical advantage (Sakamoto 2010; Olsen and Westneat 2017). Even simplephysical paper models can prove to be remarkably illustrative, paving the way formore complex numerical modeling to explain their features (Smith et al. 2011). Todate, themost complicatedmodeling approach applied to bird feeding has been FiniteElement Analysis (FEA). FEA is an engineering technique capable of calculatingdeformation (strain) and mechanical stresses in structures with complex geometries,loading regimes, or distributions of material. The method works by subdividing thestructure into a large number of bricks (“elements”) of simple shape joined at theircorners by nodes to form a mesh. This model is then solved by applying loads of


Fig. 17.5 Validated finite element model of an ostrich (Struthio camelus) cranium under non-physiological loading. Warm colors indicate higher values of Von Mises Stress (in MPa), andindicate where the structure is most likely to fail. The flexible zone of rhynchokinetic bending isclearly highlighted by higher stresses in this model. Figure reproduced fromCuff et al. (2015) underCC BY 4.0

known force or displacement alongside constraints where displacement is set to zero,then calculating deformation at each node in the mesh as part of several simultaneousequations. Results are visualized as contour plots over the structure or queried atindividual nodes or elements (Fig. 17.5).

The ability to calculate performance metrics like stress, strain, reaction forces,and strain energy density throughout a structure, and identify “hot-spots” of par-ticular strength or weakness, has obvious applications for functional morphologists[see Rayfield (2007) for a review]. In particular, hypotheses about biomechanicalfunction as it relates to form through evolution can be readily quantified due to theability to manipulate and modify said form in silico. In birds, FEA has been used todemonstrate performance differences that correspond to beak shape and the preferredmode of beak use in Darwin’s finches (Herrel et al. 2010; Soons et al. 2010, 2015).The keratinous rhamphotheca plays an important functional role in biting (Soonset al. 2012) by allowing the bill to act as a sandwich foam: a thin, stiff shell of ker-atin encloses a closed-cell “foam” of trabecular bone, conferring high stiffness andresistance to buckling for low weight (Seki et al. 2005, 2006). This is particularlyimportant for birds with large bills relative to their body size. In comparison to othertheropod dinosaurs, bird skulls show an evolutionary trend towards an exceptionallyhigh degree of fenestration. By using FEA to demonstrate the load-bearing role ofthe postnasal bars during feeding, Gussekloo et al. (2017) suggest that the loss ofthese structures in palaeognathous birds may explain why palaeognaths have failed


to explore the disparity of beak shapes seen in neoganthous birds (who retain thesestructures). Finally, FEAoffers the unique opportunity to perform functional analysesof extinct birds (e.g., Degrange et al. 2010). A caveat of this is that 3D preservationis required (rare in the avian fossil record), but the successful retrodeformation andanalysis of partially crushed dinosaur skulls provides optimism for future studies(Lautenschlager et al. 2013; Cuff and Rayfield 2015).

Despite its potential, FEA has yet to really take hold as a method to study birdfeeding. This is partially due to high start-up barriers in cost, computer power, andnecessary expertise, but also because of specific concerns surrounding how to con-struct valid models of avian skulls. Model validity is of critical concern in FE stud-ies (Bright 2014), and bird skulls present several unique challenges regarding theirincredibly thin and highly pneumatized bones, multiplemoving parts in the quadratesand palate, flexible bending zones, and the presence of a rhamphotheca. So far, theonly attempts to experimentally validate entire skulls (Cuff et al. 2015) or mandibles(Rayfield 2011) have reiterated results from FE models of other taxa: it is broadlypossible to replicate strain patterns, but performance values are generally unreliable.This is likely due to an incomplete understanding of model input parameters, and forthe time being limits studies to those that are purely comparative (Bright 2014). For-tunately, several comparative questions present themselves in the under-quantifiedrealm of bird feeding functional morphology, and though in its infancy in birds, com-parative and hypothetico- deductive FEA (sensu Rayfield 2007) is already yieldinginteresting and informative results (e.g., Soons et al. 2015; Gussekloo et al. 2017).

17.2.2 Functioning of the Avian Feeding Apparatus

17.2.2.1 Cranial Kinesis

Most, if not all birds, can move their upper beak through the motion of cranial bonesposterior to the beak (Fig. 17.6; Fisher 1955; Bock 1964; Bout and Zweers 2001).The motion of these bones, referred to generally in vertebrates as cranial kinesis,has been studied through a variety of approaches, including passive manipulationand Roentgen stereophotogrammetry (e.g., Gussekloo et al. 2001), computationalsimulation (e.g., Van Gennip and Berkhoudt 1992; Meekangvan et al. 2006; Olsenand Westneat 2017), and in vivo XROMM (e.g., Dawson et al. 2011). In most birds,such as mallards (Anas platyrhynchos; Dawson et al. 2011) and sparrows (Hoeseand Westneat 1996), the upper beak rotates like a hinge, termed prokinesis (Bühler1981), at a highly localized region between the upper beak and neurocranium. How-ever, in other birds the upper beak-neurocranium joint is fused and the upper beakbends at flexion zones more rostrally along the beak, termed rhynchokinesis (Zusi1984). These flexion zones can be relatively short, allowing just the tip of the beak torotate, as in hummingbirds (Yanega and Rubega 2004) and shorebirds (Estrella andMasero 2007), or relatively long, causing broad bending of the beak, as in palaeog-nathous birds (Gussekloo and Bout 2005). Variability in the quadrate-neurocranium


articulation also affects quadrate kinematics, ranging from allowing a full range ofquadrate rotation as a single condyle in mallards (Dawson et al. 2011, Fig. 1) orconstraining quadrate rotation to a single axis of rotation, as two separate, widelyspaced condyles in owls (Olsen and Westneat 2017, Fig. 2). The variably presentpterygoid-neurocranium joint, sometimes accompanied by a basipterygoid processon the neurocranium, is thought to function primarily in stabilizing skull forces inpalaeognathous birds (Elzanowski 1977; Gussekloo and Bout 2005), although itsfunction in neognathous birds remains unclear.

Cranial kinesis is actuated by sevenmuscles that interconnect all themobile cranialbones, except the jugal and upper beak (Fig. 17.6; Zweers 1974). Studies that haverecorded activity of the avian jaw muscles (i.e., by electromyography) either duringfeeding or drinking are few and limited to four species: mallards (Anas platyrhyn-chos; Zweers 1974), chickens (Gallus gallus domesticus; Van den Heuvel 1992),pigeons (Columba livia; Bermejo et al. 1992; Bout and Zeigler 1994), and Javasparrows (Padda oryzivora; van der Meij and Bout 2008). In general, the depressormandibulae (DM) and protractor quadrati et pterygoidei (PQP) muscles act as jawopeners, with the former depressing the lower bill (Bout and Zeigler 1994; Zweers

Fig. 17.6 Themain skeletal components andmuscles in the bird skull.Most elements are connectedby joints that allow some mobility (solid line). This mobility has been lost in some lineages of birds(dashed line). Some articulations that appear to function in stabilizing the skeletal element are notpresent in all bird lineages (dotted line). Muscles (red lines) attach to various skeletal elements, withsome muscles connecting more than two elements (corresponding labels are located at the filledcircle end of each line or lines)


1974) and the latter elevating the upper bill (Zweers 1974; Van den Heuvel 1992).However, PQP is usually active before DM, indicating a potential additional functionin “unlocking” the lower bill through a mechanism involving the quadrate and thepostorbital ligament, which extends from the neurocranium to the lower bill (Zusi1967). After DM and PQP activity, the adductor and pseudotemporalis muscles gen-erally act as jaw closers (Zweers 1974; Bermejo et al. 1992; Van den Heuvel 1992;Bout and Zeigler 1994). Relative to the other jaw muscles, the pterygoideus (PT)muscle, which can both elevate the lower bill and depress the upper bill relative to afixed lower bill, shows the most variable activity. In some cases, PT activity is similarto adductor activity (Van den Heuvel 1992) whereas at other times it is active at var-ious points during both jaw opening and closing (Zweers 1974; Bermejo et al. 1992;Bout and Zeigler 1994). This may be due to the fact that the PT muscle functionsdually as a closer of the upper and lower bill, and that upper and lower bill motionsare often slightly out of phase (Zweers 1974; Dawson et al. 2011) or independent ofone another (Van den Heuvel 1992; Hoese and Westneat 1996).

17.2.2.2 Lower Beak Biomechanics

Depression/elevation. The most obvious movement in the lower jaws of birds isopening (depressing) and closing (elevating). Depressing the lower jaw is facilitatedby gravity and themandibular depressor muscles, originating on the paroccipital pro-cess on the posterior skull and inserting on the caudal fossa of the posterior mandible(Bühler 1981; Baumel andWitmer 1993; Vanden Berge and Zweers 1993; Fig. 17.6).Total gape is increased by elevating the upper bill (modeled by Hoese and Westneat1996; and see rhynchokinesis portion of this chapter), or increasing the mediolateralvolume (see below). Closing the lower jaw is accomplished by two main musclegroups. The first is the pterygoideus, originating on palatine and pterygoid bones ofthe cranium and inserting on the caudomedial aspect of the mandible. The secondgroup includes the mandibular adductors, originating on the skull caudal and ventralto the orbit and inserting on the mandible (Fig. 17.6). Passive components of open-ing and closing are facilitated with a series of ligaments (e.g., occipitomandibular,postorbital) linking attachment sites that are similar to associated musculature (Bock1964; and see Baumel and Raikow 1993). Marked variation in force and velocity ofclosing is thought to be a result of a number of different biomechanical strategiesincluding muscle physiology (pennation angles, cross-sectional areas, fiber types,etc.) and in-lever to out-lever ratios (see Corbin et al. 2015).

Protrusion/retraction/lateral motion. Because the pterygoideus and adductormandibulae muscle groups have independent attachment sites and lie at obliqueangles to one another anterioposteriorly and lateromedially (Fig. 17.6), birds mayprotrude and retract the lower jaw (see Bühler 1981) and exhibit lateral excursions.These movements are important in the food manipulation capacities of icterids (ori-oles and allies) that roll seeds over palatine blades (Beecher 1951), rhamphastids (tou-cans) that position fruit before ballistic feeding (Baussart et al. 2009), and psittacids


(parrots), which may undergo a complex oral handling of food items prior to swal-lowing (Demery et al. 2011).

Intramandibular flexion. Some birds (i.e., hummingbirds, pelicans, goat-suckers),exhibit streptognathism to widen and heighten their gape: they bow (mediolaterally)theirmandibular rami (Böker 1938;Meyers andMyers 2005). This action ismediatedby special hinge zones along each ramus (Smith et al. 2011; Zusi 2013), and atwisting, rotating action causing the distal portion of the mandible to bend downward(Zusi 2013), and the intraramal space to increase dramatically. Increasing the gapein this way is used in precopulatory behaviors and territorial displays (i.e., exposingthe inner mouth; Snow 1974; Stiles and Wolf 1979; Rico-Guevara and Araya-Salas2015), obtaining aerial, and submerged prey items (increasing net-size; Bühler 1970;Burton 1977; Yanega and Rubega 2004; Meyers and Myers 2005), and obtainingburied prey items (Judin 1961).

17.2.2.3 Integration of Mechanisms

Feeding behavior comprises foraging, food acquisition, and digestion (Zweers et al.1994). Here wewill focus on food acquisition only, which includes thewhole processfrom themovement of the head towards the food item up to ingestion and deglutition.Within birds, a wide variety of different feeding behaviors can be observed and it isimpossible to name them all. The most commonly observed form, and probably theancestral behavior, is pecking as observed in pigeons and chickens (Zweers 1991).This behavior consists of picking the food item up between the bill tips followed byintraoropharyngeal transport and a final swallowing movement by retraction of thelarynx (Zweers 1982;VandenHeuvel andBerkhoudt 1997). Thefirst grasp-phase andfinal swallowing are very similar among species, but the intraoropharyngeal transportvaries depending on both food size and species. The simplest form is the so-calledcranio-inertial, or “throw and catch” behavior (e.g., Fig. 17.4c), in which the birdaccelerates its head back and/or upwards while holding the food item, then releasingthe food item, followed by a head movement in the opposite direction resultingin relative displacement of the food item in the direction of the oesophagus. Thisbehavior is recorded for large ratites such as rheas and ostriches, and in long billedfrugivorous birds such as toucans and hornbills, but is also employed by pigeons andchickens when eating large food items (Zweers 1982; Van denHeuvel and Berkhoudt1997; Tomlinson 2000; Gussekloo and Bout 2005; Baussart et al. 2009; Baussartand Bels 2011). When the latter two feed on small food items, they show the so-called slide-and-glue mechanism in which the food item is stuck to the tongue withsaliva after which the tongue is retracted. After retraction, the food item is pressedagainst the palate, after which a second cyclemight take place (Zweers 1982; Van denHeuvel and Berkhoudt 1997). The use of the tongue for transport is observed inmanyother species (e.g., Fig. 17.4d), but is often more complex than the slide-and-gluemechanism and linked to special morphological features. A well-described exampleis the transport mechanism observed in mallards, where several lingual structures,such as lingual ears, are used to keep food items in place and lingual scrapers on


the lateral side of the tongue are used for transport in the caudal direction (Kooloos1986). It is assumed that from the general pecking feeding behavior several otherfeeding behaviors have evolved such as filter feeding and probing behavior (Zweers1991; Zweers et al. 1994). Filter feeding in ducks probably evolved from a graspingancestor and can be seen as an adaptation from lingual transport as it fully dependson the craniocaudal movement of the tongue for both the transport of water and thefiltered food particles (Kooloos et al. 1989; Zweers and Vanden Berge 1997).

Adaptations to probing behavior are an elongation of the bill to increase probingdepth, increased sensitivity in the bill tip for sensing buried prey, and the presence ofrhynchokinesis (Zweers andGerritsen 1996; Zweers andVandenBerge 1997). Rhyn-chokinesis is a special form of cranial kinesis, and currently the only form of aviancranial kinesis for which clear functional advantages are recognized. In rhynchoki-nesis only the very tip of the upper bill can rotate relative to the rest of the cranium,which means that birds only have to displace a very small volume of substrate whenopening their bill while catching prey. In addition, by curving the bill tip behind thefood item, there is less chance of losing the food item during its extraction from thesubstrate (Zweers and Gerritsen 1996). Further intraoropharyngeal transport can bedone either by slide-and-glue or cranio-inertial transport (Gerritsen 1988). Unfortu-nately, very little is known about the evolutionary forces that have resulted in thewidediversity of other feeding behaviors and the large radiation we observe in modernbirds. As shown by the adaptive radiation in Darwin’s finches, food availability is astrong selective force and bill morphology in birds is highly adaptive (Grant 1999),but more research is needed to see the full potential of avian trophic adaptation.

17.3 A Review of the Main Feeding Modes in the Class Aves

Birds eat just about everything (Rubega 2000; Fig. 17.7), and that their beak shapeaccordingly varies according to diet is generally accepted as a truism. However, thistenet is belied by two important points: (1) most birds of any given species oppor-tunistically consume a variety of food types, despite any ostensible adaptations fora particular diet, and (2) beaks also play essential roles in other functions, such as inthermoregulation (Greenberg et al. 2012), vocalization (Podos 2001), and ectopara-site control (Clayton et al. 2005). As a result, contemporary views are shifting towarda more holistic understanding of the feeding apparatus, in recognition of the fact thatbirds, like other vertebrates, are not necessarily adapted to specific diets, but ratherto the mechanical demands of consuming different types of food (Schwenk 2000;Schwenk and Rubega 2005; Gailer et al. 2017). Accordingly, this section focuseson the diversity of the modes of feeding (e.g., Fig. 17.7), and not necessarily on thediversity of avian diets. A comprehensive review of avian food habits is beyond thescope of this chapter and would take several volumes to fill. Nevertheless, there areexcellent sources of dietary information available for the vast majority of avian taxa(del Hoyo et al. 2014; Wilman et al. 2014). Below we outline the major types of


Fig. 17.7 Birds have evolved to exploit resources in terrestrial, aquatic, and aerial niches; as shownhere they have a diversity of feeding tactics that have shaped not only their food acquisition andprocessing tools (e.g., beaks, tongues, and feet), but also their locomotor and sensory structures,and associated behavioral strategies. This is exemplified by the variety of challenges that birds facewhile trying to subsist on tiny invertebrates, airborne insects, large mammals, elusive fish and birds,and specialized floral nectar resources. Photos by Dave Furseth

feeding tactics, describe some of the key morphological and behavioral attributeswith which they are associated, and feature the avian taxa that best exemplify them.

17.3.1 Obtaining Food on Land

17.3.1.1 Granivores

Granivory (eating seeds or seed parts) is exhibited in birds by at least four modes:swallowing whole (see frugivory below), husking, cracking, and hammering. Husk-ing is a behavior common to finches and sparrows. During husking, a bird dismantlesand discards the outer coat, and subsequently eats the calorically rich seed (cotyle-don and embryo). Initially, the whole seed is positioned between the upper and lowerbills and held in place with the tongue. The lower mandible is then pushed forward


(towards the tip of the bill) and the outer coat is separated, generally along natu-ral margins of the seed coat (Van der Meij and Bout 2006). The lower bill may bemoved side-to-side in order to further separate the coat from the seed. Seed-crackingis employed by larger birds (e.g., parrots; Homberger 2003), birds with relativelylarge bills (e.g., grosbeaks), or birds with plates or keels in the mouth (e.g., black-birds). Cracking is similar to husking, where the seed is crushed or opened but notnecessarily along its natural margin, or alternatively the seed may be rolled along theedge of a keel formed from the palatine bones, as seen in blackbirds (see Beecher1951). Hammering involves a bird stabilizing a seed (e.g., titmice; Corbin et al. 2015)or cone (e.g., nutcrackers; Tomback 1998) using its feet or substrate and repeatedlyhitting the object with its bill.

17.3.1.2 Folivores

Phytophagy, referring to the consumption of leaves (as in folivory) or other vegetativeplant structures, is a restricted dietary strategy in birds, characterizing only about3% of extant taxa. Because the energy density of leaves is low compared to thatof plant reproductive structures and of animal tissue, a greater mass investment isrequired of the avian digestive system to process suchmaterial, alongwith a larger gutvolume (Morton 1978; Dudley and Vermeij 1992). In turn, energetic costs of flightare disproportionately increased, rendering folivory a challenging nutritional strategyfor active fliers. Gut transit time can be increased at the cost of digestive efficiency(as in the case of geese), but in general, the few avian folivores tend to be aquatic(e.g., various Anseriformes) or transient fliers [e.g., grouse, tinamous, and hoatzin(Opisthocomus hoazin)]. Reduction of flight capacity (including flightlessness) alsocorrelates with folivory, as in many ratites (see Olsen 2015). Because leaves, stems,buds, roots, and other vegetative material are often mechanically defended (e.g.,phytolith inclusion in grasses), additional structural investment is required to processsuch food, including the use of gizzard stones or of crushing ridges in the crop(e.g., doves, hoatzin). Transient folivory, particularly among frugivorous taxa suchas tanagers, may be more common than is currently realized (e.g., Munson andRobinson1992), but seems tobedrivenby seasonal scarcity ofmore preferred energy-rich fruits, thereby illustrating the ecological limitations of folivory as a dedicatednutritional strategy.

17.3.1.3 Frugivores

Fruit-eating birds have an important biological role in the dispersion of seeds (Gon-zales et al. 2009), and therefore fruits are attractive for many bird species. Mostfrugivorous birds eat the fruits whole, using catch and throw behavior for intraoraltransport (Baussart et al. 2009; Baussart and Bels 2011). Very few birds actuallytake bites out of soft fruits, although this may be true for most parrots (Corlett 1998;Collar 2017). In a review on frugivorous species in the Indomalayan region, fruit-eating birds were reported from over 40 families (Corlett 1998). In a large number


of these families, only a few species eat fruit, and those species often only eat fruitoccasionally, but it does show the preference for this food source. This review alsoshows that birds use all types of fruits, from soft to hard, and forage for fruit attachedto the plant or fallen to the ground. Also, the extent of the use of fruit varies amongspecies. Many species pass seeds intact through the intestinal tract, whereas otherscrush the seeds in the gizzard. Species that eat large fruits, such as hornbills, regur-gitate the largest seeds. Very little is known about the exact factors that play a rolein fruit selection in birds, but color is an important factor, with birds favoring redand black colors even when this is not correlated with energy content (Corlett 2011;Duan et al. 2014). In addition, in some frugivores such as parrots and mousebirds,the feet play a role in handling, manipulating, and processing food prior to ingestion(Berman and Raikow 1982; Berman 1984; Symes and Downs 2001).

17.3.1.4 Nectarivores

Nectar is exploited facultatively by a plethora of bird species with varied morpholo-gies (e.g., Cecere et al. 2011; Dalsgaard et al. 2017). Yet there are some birds whosesubsistence depends on feeding efficiently on nectar, and consequently, their feedingapparatus has adapted to reach, extract, and swallow small amounts of liquid rapidly.Most specializednectarivores access nectar chambers by traversing long corollaswithslender and elongated bills; protruding their tongues far past their bill tips and gath-ering nectar with brushed and/or tube-like tongue tips. These “anthophilic” (Stiles1981)morphofunctional adaptations varywith the fluid collection and intraoral trans-portmechanismof eachparticular group. For instance, hummingbirds use surface ten-sion trapping (Rico-Guevara and Rubega 2011) and elastic pumping (Rico-Guevaraet al. 2015) to fill their bi-tubular, fringed tongues, and use their flexible bills andtongue wings to move nectar backwards hydraulically (Rico-Guevara 2014). Sun-birds with comparable bills and tongues (e.g., Schlamowitz et al. 1976; Downs 2004)may employ similar mechanisms. Honeyeaters with multi-tubular, brushed tonguescould employ capillary wetting both within and between their distal splits (Gadow1883; Paton and Collins 1989; Collins 2008). All of these birds squeeze their tongueswith their bill tips between licks, but other specialized nectarivores have to feed withtheir bills open. Among these, lorikeets (Trichoglossus spp.) exhibit lingual apicalfiliform papillae that form nectar-collecting brushes (reviewed by Homberger 1980;Gartrell 2000) that can be discharged at the palate. Flowerpiercers (genera Diglossaand Diglossopis) have inverted bi-tubular tongues with the openings of the tube-likegrooves on the ventral side (Moller 1931; Schondube 2003), capable of sustainedflow through a cohesive pulling mechanism (Rico-Guevara 2014).

17.3.1.5 Feeding on Invertebrates

The paraphyletic group invertebrates are the largest group of animals in speciesnumber, individuals, and total volume, so it is not surprising that invertebrates are an


important food source for birds. Given that invertebrates are so morphologically andbehaviorally diverse, birds have evolved many different feeding behaviors, varyingfrom diving to catch sedentary molluscs as observed in eiders, to catching high-velocity flying insects, as seen in swifts and some raptors. Birds that feed on buriedinvertebrates (molluscs, insects, worms) are often probers, which means that theyinsert their beaks into mud to extract their prey. These probers, including shorebirds,ibises, and kiwis, often have a large number of sensory pits on the tip of the bill(Nebel et al. 2005; Cunningham et al. 2013) that are used to detect prey (Gerritsenand Meiboom 1985; Piersma et al. 1998). Additionally, almost all probers showrhynchokinesis (Zusi 1984),which helps reduce the total resistance encountered fromthe substrate while opening their bill tips beneath it. Other aquatic invertebrates canbe obtained by efficient filter feeding as observed in spoonbills andflamingos (Zweerset al. 1995). At the other extreme are the aerial insectivores, which require extremehigh-speed flying and agility to capture prey on the wing (below). Other groupsof birds feed on arthropods living in, or on, plants. Birds that get their food frominside the bark of trees include woodpeckers. Woodpeckers peck holes in the bark oftrees and subsequently remove insects using their long-barbed tongue, sticky with aspecial kind of saliva (Bock 1999). Getting into the bark demands a suite of shock-resisting and stress-dissipating modifications of the skull and beak for hammeringinto wood (Gibson 2006; Yoon and Park 2011; Lee et al. 2014). For an overview ofother feeding types, we can consider the diverse group of South American ovenbirds(Furnariidae). Within this group, several different feeding behaviors can be found,including woodpecker-like behavior, birds that split twigs to get to insects, birds thatprobe in tree bark crevices, and birds that search for insects in dead or live foliage(Remsen and Parker 1984; Fjeldså et al. 2005). A study of the last group, as well asadaptations seen in insectivorous Darwin’s finches, shows that the avian body plancan easily adapt to different types of insectivory (Tebbich et al. 2004; Claramunt2010).

17.3.1.6 Feeding on Vertebrates

Feeding on vertebrates is a very different endeavor from feeding on invertebratesbecause vertebrates are usually larger prey items, both absolutely and relative topredator body size. Vertebrates are arguably more challenging for predators to phys-ically subdue, dispatch, and dismember for ingestion. The foraging behavior ofmeat-eating birds (diurnal raptors and owls) has traditionally been dichotomized by “sit andwait” ambushing versus active searching and pursuit strategies (Jaksic and Carothers1985), although this is really more of a continuum than a strict categorization. Rap-tors are often secondarily categorized by the primary types of prey they tend to feedon, such as birds, mammals, or lepidosaurs. The quintessential “raptorial” featuresof meat-eating birds are the sharply hooked beak and large talons. Indeed, beak(and cranial) shape has been shown to vary with diet type in raptors (Hertel 1995),with the greatest differences occurring between bird-eaters (short, wide upper billand deep mandibular symphysis) and scavengers (e.g., long, narrow, highly curved


“meathook” upper bill). Despite clear indications of the effects of diet on beak formand function, body size (i.e., allometry), in association with constraints imposed bycranial integration (coordinated development of parts) and phylogeny (i.e., sharedancestry) have recently been identified as more important drivers of the variation inbeak shape observed across the diurnal raptors (Bright et al. 2016).

As previously mentioned in regards to some frugivores (e.g., parrots) and grani-vores (e.g., tits), the feet constitute an important component of the feeding apparatusin these birds (Clark 1973). Birds that tend to grasp and carry prey items show greaterrelative development of the deep (distally inserted) digital flexor muscles (Backuset al. 2015; Fig. 17.8a versus Fig. 17.8b). The hypertrophied talons (particularly thatof the second digit) of most raptorial birds vary considerably in size and shape (e.g.,degree of curvature) (Fowler et al. 2009; Csermely et al. 2012). Variation in clawsize has been linked to dietary differences among taxa, with those that take fish andlarge (relative to body size) mammals tending toward larger (relative to toe length)talons, and those that feed on birds and smaller mammals tending toward relativelysmaller talons (Einoder and Richardson 2007). The hypertrophied talons of the first(hallux) and second toes are used as an aid to body weight for “pinning” prey to theground in raptors that more exclusively use their feet to subdue and dispatch prey(e.g., accipitrid hawks and eagles) (Fowler et al. 2009).

Meat-eating does not always require the complete arsenal of killing and prey-processing implements. Among vultures, differences in skull (and beak) shape arefinely tuned to differences in feeding behavior (Hertel 1994), but as a group vulturestend to have less muscle mass and area allocated to the digital muscles than do pur-suit predators (Hertel et al. 2015). Some vultures, such as the lammergeier (Gypaetusbarbatus), process bones by dropping them from great heights in order to break theminto pieces on the rocks below (Ferguson-Lees and Christie 2001). Furthermore, rap-tors and owls are not the only carnivorous birds, as there is a variety of primarilyinsectivorous or omnivorous taxa that feed opportunistically on small (but perhapslarge relative to their body sizes) vertebrates. They include butcherbirds, shrikes,puffbirds, jacamars, frogmouths, and corvids (ravens, crows, and jays), to name justa few. In some cases, these birds may possess formidable killing implements, butperhaps not the whole “suite.” For example, shrikes have sharply hooked beaks withtomial teeth as do falcons (Fig. 17.2), but lack the talons of these more exclusivecarnivores (Cade 1995; Schön 1996). Shrikes employ clever killing maneuvers (Sus-taita et al. 2018b) and impaling (Yosef and Pinshow 2005) to compensate for the lackof these additional predatory weapons. Piscivores (fish-eaters) have a very differentarray of adaptations given the disparate challenges of locating and capturing fishunder water (see below).


Fig. 17.8 Schematic showing the relative size contributions of the deep, distally inserted (red)and superficial, proximally inserted (blue) digit flexor muscles in a birds that tend to experiencedownward-directed forces from grasping and carrying objects (e.g., raptors; left) and b birds thattend to experience more upward-directed forces from terrestrial locomotion and perching (e.g.,grounddwelling birds and songbirds; right). Figure reproduced from Backus et al. (2015), underRoyal Society Open Science CC-BY open access license

17.3.2 Catching Airborne Prey

17.3.2.1 Sally-Hawkers (Insectivores)

Many organisms minimize the energy expenditure associated with searching by sim-ply staying stationary and waiting for food to come to them. Also called “sit-and-wait”, or “ambush” foraging, this search-minimizing technique has ramifications inevolutionary ecology research [see the central place foraging hypothesis of Oriansand Pearson (1979)]. Sally-hawking is a behavior in which a bird will wait at aperch for a suitable prey item, fly out to capture it and return to the same or a dif-


ferent perch for consumption (Fitzpatrick 1980). This behavior has evolved manytimes and is generally associated with particular morphological characteristics, suchas a relatively wide bill and long rictal bristles (Fitzpatrick 1980; Corbin 2008).Passerine sally-hawking specialists include species from different families of fly-catchers (Tyrannidae, Monarchidae, and Muscicapidae), silky-flycatchers, drongos,New World warblers [e.g., American redstarts (Setophaga ruticilla)] and solitaires(Myadestes spp.). Non-passerine sally-hawkers are the Coraciiform mot-mots andbee-eaters. Also, hummingbirds acquire much of their protein via sally-hawkingbehaviors (Stiles 1995; Yanega and Rubega 2004). An extension of sally-hawking isseen in the pouncing behaviors of some flycatchers (Sayornis spp., phoebes), blue-birds and thrushes (Sialia spp. and Turdus spp.; Corbin et al. 2013), and terrestrialforaging kingfishers (e.g., East and SouthAfricanHalcyon; Corbin andKirika 2002).The energetic considerations of landing to capture a prey item rather than stayingairborne is a ripe avenue for further research.

17.3.2.2 Flying-Hawkers (Insectivores)

Catching airborne insect prey is a dedicated feeding strategy in some clades (e.g.,swallows, swifts, treeswifts, nightjars), and a facultative strategy in others (e.g.,many hummingbirds; see Stiles 1995), but requires both fast linear flight and rapidmaneuvers (i.e., torsional agility; see Dudley 2002). Although aerial insect faunais abundant, cruising flight, for which long and slender wings are most efficient, isnecessary to capture sufficient prey. Such wings have a high moment of inertia, how-ever, which impedes rapid rotations of the body, and there is thus a conflict betweenthe demands of energy efficiency and capture success (Warrick 1998). Aerodynamicstudies have demonstrated the biomechanical underpinnings to such simultaneousabilities. By variably sweeping their wings forward and backward at different air-speeds, swifts can effect both high-speed gliding flight as well as the rapid turns usedto capture insects (Lentink et al. 2007). Caprimulgiforms and swallows presumablyengage in similar behaviors, but have not yet been investigated. Aerial insectivoryby hummingbirds, by contrast, typically occurs at low speeds or while hovering, andinvolves primarily body rotations coupled with rapid beak snapping (Yanega andRubega 2004).

17.3.2.3 Bird- and Bat-Eaters

In addition to the array of vertebrate-eating adaptations described above, raptors thatspecialize on volant prey (e.g., birds and/or bats), include falcons and accipiter hawks.They exhibit a few key behavioral and morphological modifications. These raptorstend to possess relatively long toes (particularly the middle toe), which are thought toincrease the probability of contacting airborne prey items (Payne 1962; Wattel 1973;Bierregaard 1978; Csermely et al. 1998; Einoder and Richardson 2007). Similarly,Csermely et al. (1998) suggested that talons may have evolved as a mechanism to


elongate the toes in kestrels to increase the surface area for contacting prey. Thosespecies that tend to hunt bats (e.g., bat hawks and bat falcons), are more crepuscular,active at dawn and dusk, in their foraging behavior (Ferguson-Lees and Christie2001).

17.3.3 Catching Aquatic Prey

17.3.3.1 Surface Feeders

To feed on surficial prey, prey located on or near the surface ofwater, different speciesof waders have developed specialized mechanisms. For example, spoon-billed andother calidrid sandpipers, as well as oystercatchers, employ a tactile method termed“stitching”, which consists of inserting the bill down to a centimeter under the surfaceand performing rapid up and down “sewing” movements (Burton 1971; Hulscher1976; Kelsey and Hassall 1989). Such tactile feeding is mainly used under poorlight conditions, but it could also explain the widened bill tips of the spoon-billedsandpiper (Calidris pygmaea; Burton 1971; Mouritsen 1993). Phalaropes and othershorebirds use surface tension transport (Rubega and Obst 1993; Rubega 1997), afeeding mechanism that takes advantage of the adhesion of water drops to the innerbill surfaces to move prey proximad through quick opening and closing (see alsoZweers and Vanden Berge 1997; Estrella et al. 2007; Sustaita et al. 2018a). Lastly,a number of small sandpipers feed on micro and meiofauna, algae, bacteria, andorganic detritus found as a cohesive, densely packed mat (i.e., “biofilm”) layeredon mudflat surfaces (Elner et al. 2005; reviewed by Jardine et al. 2015). It has beenproposed that small tongue spines found in biofilm feeders are used to collect bitsoff this layer (Elner et al. 2005; Kuwae et al. 2008, 2012). However, the spines arenot restricted to just the tip (Elner et al. 2005), and the limited tongue protrusionabilities in these birds (Kuwae et al. 2008) suggests that the tongue is more involvedin filtration of food particles.

17.3.3.2 Filter Feeders

The simplest form of filtering prey fromwater or mud has been proposed for slender-billed shearwaters (Ardenna tenuirostris), which by opening and closing their billssuck in and retain small prey between overlapping projections in the palate anddorsal lingual surface. This surface acts as a filtering mesh, and the surplus water isdiscarded through special channels at the base of the bill (Morgan and Ritz 1982;Zweers et al. 1994; Lovvorn et al. 2001). A similar method for feeding on minutepreymay be used by some penguins and auks (Olson and Feduccia 1980). A differentfilteringmethod in seabirds is performed by some species of prions (Pachyptila spp.),which lack palatal and lingual spines but exhibit a series of densely packed comb-like projections just inside the maxillary tomia. A muscular tongue, aided by an


extensible pouch, controls the pumping of water in and out the beak to catch preyalong the combs (Morgan and Ritz 1982; Harper 1987; Prince and Morgan 1987;Klages and Cooper 1992; Cherel et al. 2002).

More specialized bills, tongues, and even body shapes to filter feed at differentdepths are found in flamingos. Flamingo beaks are strongly decurved to maintain thelid-like maxilla perpendicular to the filtering substrate while they rock their headsback-and-forth (Zweers et al. 1995). Water and food particle inflow is controlled bydepressing and retracting the tongue, which functions like a piston, while expandingthe gular region. The expulsion of water occurs by reversing the tongue movements(Jenkin 1957; Zweers et al. 1995). Flamingos possess spine-like soft projectionsalong the maxillary tomia that exclude large particles during inflow, and palatal andmandibular lamellae that retain food particles upon outflow. The final mesh size isfine-tuned by the degree of bill opening, and two rows of lingual projections aidtransport of food particles to the throat (Zweers et al. 1995; Mascitti and Kravetz2002).

The Anatidae, ducks, geese, and swans, comprises that largest number of filter-feeding species. Filter-feeding ducks have specialized flow-through mechanisms(reviewed by Zweers and Vanden Berge 1997) and have evolved some of the mostelaborate tongues and internal bill structures in birds. Inflow and outflow are drivenby alternating movements of lateral lingual bulges and the caudal lingual cushion(torus linguae, Fig. 17.3), and the filtering mesh is formed by long and hard lamellaecovering the maxillary and mandibular internal lateral margins. Food moves throughthe maxillary lamellae and longitudinal grooves, and, upon tongue retraction, lin-gual soft brush-like projections sweep the particles backwards (Zweers et al. 1977).Selection of food particle size is achieved bymodifying themaxillary andmandibularlamellar distance (i.e., by regulating gape size; Dubbeldam 1984), and by controllingthe flow vortices (i.e., the inertial impact deposition mechanism; Kooloos et al. 1989;but see Gurd 2007).

17.3.3.3 Subsurface Feeders

Some birds take advantage of added bill length and curvature to reach farther downinto the water column. Recurvirostrids, such as stilts, for example, perform visualunderwater pecking and nonvisual scything (Pierce 1985). Scything is a tactilemethod performed by recurvirostrids and some Tringa spp. waders that disturbsthe water and underlying substrate, during which prey are detected by the sensitivebill tips. Upon capture, a combination of surface tension and inertial and lingualtransport is used to swallow the catch (Becker et al. 2002, Rico-Guevara, pers. obs.).Avocets scythe, or sweep their bill, more often and stereotypically. They lower andincline their heads upwards until their recurved bill tips are horizontal near the sub-strate, and sweep their slightly opened bills toward the leading foot, usually swingingonly once per step followed by lifting the head (Hamilton 1975; Becker et al. 2002).A similar scythe-like sweeping is performed by spoonbills. However, in spoonbillsthe behavior is less stereotyped than in avocets, and the arc length and distance from


the substrate are more variable. Furthermore, sweeps are not coordinated with stepsin spoonbills, several arcs are completed before lifting the head, and the intraoraltransport mechanism is entirely inertial (Weihs and Katzir 1994; Swennen and Yu2005, 2008). The broadened and sensitive tips of the characteristic spoon-shapedbill are thought to improve detection and prey trapping (Swennen and Yu 2004).Furthermore, flattening minimizes drag and turbulence during sweeping (Swennenand Yu 2004, 2008; but see Weihs and Katzir 2008). Finally, the spatulate tips act ashydrofoils that create vortices that lift small prey off the bottom (Weihs and Katzir1994, 2008).

17.3.3.4 Surface Fishers

For reasons that may include social and energetic benefits, organisms such as fishmay aggregate near the surface of water. This provides excellent opportunity foravian predation and examples of ecosystem energy transfer, but may impose spe-cial challenges due to refraction and reflection of light (see Casperson 1999). Thereis a relatively large body of literature associated with these predator–prey interac-tions (see Pitcher et al. 1988, or Gotceitas and Godin 1993 and their references forexamples). We define surface fishing as a bird taking prey items just at or slightlybelow the surface of a body of water. Surface fishing is further classified accordingto the mode of capture. First, birds such as darters or herons spear or stab fish withtheir bills (see Recher and Recher 1968). This behavior is coupled to a relativelylong spear-like bill, quick flexion of a streamlined head and neck (Owre 1967), andpanoramic field of view in the frontal plane (Martin and Katzir 1994). Alternatively,fish may be caught in an open bill such as in “beak-fishing” gulls and kingfishers.This behavior has evolved multiple times within Aves, even among close relatives(e.g., Alcedinidae; see the character evolution analysis in Moyle et al. 2007). Manyspecies [e.g., eagles and osprey (Pandion haliaetus)] of birds utilize “foot-fishing”behavior, in which prey items are captured with a foot that exhibits highly curvedclaws (Fowler et al. 2009) and possibly modified scales (e.g., those of osprey) whichare excellent for grasping slippery fish. Another strategy of surface fishing is thatof “tactile fishing”. Rather than being dependent on sight for prey detection, birdsmay feel for prey that hit or touch the bill, and the bill is snapped shut quickly (e.g.,skimmers, spoonbills; see above).

17.3.3.5 Divers

Birds that must go to greater depths to capture fish are often coarsely categorizedby their primary modes of accessing prey from the air above the water, or from thesurface of thewater. They include “plunge divers” (e.g., pelicans, tropicbirds, boobiesand gannets), who dive from the air, “foot-propelled divers” (e.g., loons, grebes,cormorants, andmergansers)whodive from the surface, and “wing-propelled divers”,who hunt beneath the water surface (e.g., penguins) and air (auks, puffins, murres,


and diving petrels) (Ashmole 1971; del Hoyo et al. 1992; Sustaita et al. 2018a).As mentioned above with respect to the ambush versus pursuit foraging modes ofraptors, these categories can be quite fluid, and some species adopt different strategiesdepending on the circumstances: Australasian gannets plunge dive for subsurfacefish, but “pursuit dive” to reach deeper fish on the move (Machovsky Capuska et al.2011). Furthermore, these groupings donot necessarily reflect ecological adaptations.For example, an Antarctic procellariform community described by Moreno et al.(2017) consists of four heterospecific assemblages or “guilds”, distinguished bytheir focus on crustaceans, small or large fish and squid, or carrion.

Although most seabirds have serrated or hooked beaks to maintain purchase ofslippery prey, there are other morphological differences among taxa that are thoughtto provide a basis for partitioning of resources in the pelagic environment (Ashmole1971). Differences in wing shape are associated with differences in flight (Brewerand Hertel 2007) and foraging (Hertel and Ballance 1999) behavior among taxa.Seabirds tend to be opportunistic, but the patchy distribution of resources of thepelagic environment selects for a variety of more or less specialized foraging tactics,such as foraging nocturnally, in flocks, along fronts, associating with other marinepredators (e.g., dolphins), or simplypatrolling largeocean expanses (e.g., albatrosses)(Ballance and Pitman 1999).

17.4 Drinking in Birds

Drinking movement in birds can be divided into two phases: the motion of fluidthrough the beak (beak transport) and through the pharynx (pharyngeal transport).Thefirst phase of drinking is achieved in twodistinctways.Birds either keep their billsimmersed in the water or make a scooping motion with their head. Intrapharyngealtransport is either achieved by laryngeal motion or by using gravity (Zweers 1992).Pigeons were the first bird species observed by fluoroscopy as they drank (Zweers1982) and are the only bird species in which muscle activity has been recordedduring drinking (Bermejo et al. 1992; Bout and Zeigler 1994). Pigeons use cyclicalmotion of the tongue and beak to generate suction for beak transport followed bycyclical motion of the larynx to generate suction for pharyngeal transport; duringboth phases the beak remains immersed in water with the head tipped down (Zweers1982). Drinking in estrildid finches resembles that in pigeons, with the tongue andbeak driving beak transport, the larynx driving pharyngeal transport, and no tippingup of the head (Fisher et al. 1972; Heidweiller and Zweers 1990). Fluid transport infinches is achieved by “scooping” (Heidweiller and Zweers 1990) of the tongue andlarynx, rather than suction. Suction or scooping by the tongue and larynx may becommon among several bird orders: drinking without tipping up of the head has beenobserved in parakeets (Fisher et al. 1972), tanagers, sparrows (Moermond 1983), andmousebirds (Cade and Greenwald 1966).

Mallards (Kooloos and Zweers 1989) and chickens (Heidweiller et al. 1992) alsouse suction to drink, driven by motion of the beak, tongue, and (in chickens) the


larynx. For pharyngeal transport, both species tip up the head so that gravity andcyclical motion of the larynx direct water into the oesophagus. Tongue scoopingor suction followed by gravity-based pharyngeal transport is also been observed insandgrouse (Cade et al. 1966). For drinking, rheas use “beak scooping” followedby gravity-based flow for pharyngeal transport (Gussekloo and Bout 2005). Beakscooping may also be used for drinking in several families of songbirds, includingmanakins, flycatchers, thrushes, and grosbeaks (Moermond 1983). A pecking actionfor transporting fluid directly into the pharynx has been observed in chicken hatch-lings (Heidweiller and Zweers 1992), and in rheas, when the surface area of wateris limited (Gussekloo and Bout 2005). For beak transport of nectar, hummingbirdsuse their tongue tips as a fluid traps (Rico-Guevara and Rubega 2011), the base ofthe tongue grooves as elastic pumps (Rico-Guevara et al. 2015), and their beak to“squeeze” out the trapped fluid (Rico-Guevara and Rubega 2017). The same behav-ior of beak transport is likely used for drinking water (Fisher et al. 1972) but thepharyngeal transport mechanism remains unclear (Rico-Guevara 2014).

There is much we do not know about how birds drink and why birds have evolveddifferent drinking strategies. Capillary action has been proposed to play some rolein fluid flow during drinking in waterfowl (Kooloos and Zweers 1989), chickens(Heidweiller et al. 1992), and nectarivores (e.g., Collins 2008; Kim et al. 2012). Thishypothesis requires scrutiny usingmore sophisticated techniques (e.g., Rico-Guevaraet al. 2015). Similarly, the relative contributions of scooping versus suction duringdrinking in many birds remain unclear. New imaging and simulation techniqueswill clarify the relative contributions of these different mechanisms and maybe evenreveal additional mechanisms of fluid capture by birds (Prakash et al. 2008). Addi-tionally, the independent evolution of the same drinking behaviors in birds, the dualfunctionality of the beak and tongue in feeding and drinking, and the relationshipbetween a bird’s diet and how frequently it needs to drink (Bartholomew and Cade1963) all point to a strong evolutionary association between drinking and feeding.Yet, we still do not understand the trade-offs and mutual compatibilities betweenthese behaviors. New observations of drinking in previously unstudied clades willlikely provide insights into feeding/drinking relationships.

17.5 Evolutionary Forces Shaping Bird Feeding

17.5.1 Patterns in Bird Feeding

17.5.1.1 Adaptive Radiations

Birds are the most diverse tetrapod class, with over 10,000 extant species (BirdLifeInternational 2015). Closely related species may have strikingly disparate bills, andindeed Darwin’s finches (Grant and Grant 1993), Hawaiian honeycreepers (Lovetteet al. 2002), and Malagasy vangas (Jønsson et al. 2012) are often cited as text-book examples of macroevolution in action. Such adaptive radiations are presumed


to be driven by rapid morphological evolution in response to ecological opportu-nity (Givnish 2015). In a study of over 2,000 bird genera, Cooney et al. (2017)demonstrated that the fastest rates of bill shape evolution within clades are oftenassociated with islands, where the opportunity to invade new niches should encour-age rapid morphological evolution. High rates also occurred on branches leadingup to early radiating families with unusual bill morphologies (e.g., hummingbirds,anseriforms), suggesting that adaptations to unlock novel feeding strategies facil-itate the evolution of disparate phenotypes. One must take care to note that highrates of morphological evolution do not necessarily imply high rates of speciation,and vice versa: many explosive radiations of birds are not associated with high billdisparity (e.g., white-eyes; Moyle et al. 2009). In these instances, high speciationrates may be driven instead by other functional traits, sexual selection, geographicfactors, or some combination of these factors (Jetz et al. 2012). Chira et al. (2018)report that when considering the correlations between rates of beak shape evolutionand a number of hypothesized evolutionary drivers (e.g., range size, occupation ofislands, environmental mutagens, and other factors) in 5,551 avian species, 80% ofthe variation in species-specific rates could not be explained. Thus it may be thatmany of the ‘classic’ adaptive radiations in birds are actually quite exceptional.

Genetic studies have determined that themajor axes of bill shape variation (height,width, and depth) are controlled by relatively few genes (Abzhanov et al. 2004, 2006;Mallarino et al. 2011).Morphological studies have identified heterochronic, allomet-ric, and phylogenetically conserved patterns that imply developmental constraints onbill and skull shape (Bhullar et al. 2012; Bright et al. 2016; Cooney et al. 2017). Formany birds, the bill represents a compromise between development and an array offunctions. In order to untangle these different signals, we need well-defined hypothe-ses and methods that quantify both form and function.

A range of tools is now available for investigating beak evolution. Morphologyhas traditionally been quantified with linear measurements, but the emergence oflandmark-based geometric morphometrics methods (Zelditch et al. 2012; Adamset al. 2013) allows much more detailed analyses to take place. In birds, in which thestructures of interest can be elaborate and highly curved and thus missed by linearmetrics, this is a useful tool. Briefly, geometric morphometrics requires placement ofhomologous “landmarks” on every specimen, which are then aligned to remove thedifferences in specimen scale, position, and rotation (that is, all the geometric datathat are not related to shape) using Generalized Procrustes Analysis. The Procrustesaligned coordinates may then be used to describe the nature of shape variation inthe sample. A typical first step is a principal component (PC) analysis to determinethe major axes of morphological variation, and to generate visualization aids, suchas thin-plate spline warps and morphospace plots of the PC scores (Klingenberg2013; Fig. 17.9). In birds, geometric morphometrics data has been used to look atdifferences associated with biogeography (Foster et al. 2008), and diet or feedingbehavior (e.g., Si et al. 2015; Bright et al. 2016; Olsen 2017), and regression of shapeon size or age data has been used to investigate the effects of allometry, ontogeny,and heterochrony (Kulemeyer et al. 2009; Bhullar et al. 2012; Marugán-Lobón et al.2013). Furthermore, when allometric patterns have been identified within families


Fig. 17.9 Phylomorphospace plot showing shape changes among the skulls of diurnal raptors.Shape changes along PC1 are typical of the variation associated with trajectories of allometry andcraniofacial integration in several families of birds, with larger bird species tending to occupypositive values on PC1. Figure reproduced from Bright et al. (2016)

they often describe a relative lengthening of the rostrum with increasing size, andare often associated with strong signals of integration between the bill and the rest ofthe skull based on partial least squares analysis and tests of modularity/integration(Klingenberg and Marugán-Lobón 2013; Bright et al. 2016; Young et al. 2017). Ifselection aligns with an allometric trajectory, then allometry underpinned by integra-tionmay represent an evolutionary line of least resistance that allows birds to diversifyrelatively quickly (see theoretical models of Marroig et al. 2009; Villmoare 2013;Goswami et al. 2014). One may also test for any phylogenetic similarities underlyingthe shape data (Klingenberg and Marugán-Lobón 2013; Bright et al. 2016; Cooneyet al. 2017), or investigate rates of phenotypic evolution (Cooney et al. 2017; Chiraet al. 2018).

17.5.1.2 Convergences and Parallelisms in Avian Feeding Behaviorsand Structures

Convergent morphologies and feeding mechanics among phylogenetically distantgroups of birds have always attracted the attention of biologists. These outcomes aremost striking in the context of intercontinental and hemispheric comparisons; thesimilarly shaped beaks and convergent transport mechanics of the frugivorous NewWorld toucans and the Old World hornbills, for example, presumably reflect com-mon functional demands for reaching, manipulating, and consuming fruits (Baus-sart et al. 2009; Baussart and Bels 2011). Additional and non-mutually exclusiveselective pressures on beak morphology can include use in inter- and intrasexualselection, visual displays to heterospecifics, and use in thermoregulation. Functionalconvergence in specialized hunting behavior is similarly impressive, as characterizes


ballistic plunge-diving in gannets, tropicbirds, terns, and many kingfishers. Feedingon carrion and carcasses has elicited morphological convergence in vulture mor-phologies worldwide (Hertel 1994, 1995). Granivory by sandgrouse and seedsnipes,ground-litter insectivory by monias and thrashers, and the aerial insectivory of swiftsand swallows further exemplify the evolution of anatomical and functional similari-ties driven by comparable diets.

Nectarivory represents a powerful example of convergence in the feeding appa-ratus, given the mutualistic coevolution with nectar-bearing flowers that has elicitedcomparable beak and lingual morphologies among avian clades from different conti-nents and island groups (i.e., the NewWorld hummingbirds, the Old World sunbirdsand their allies, the Australo-pacific honeyeaters, and many of the Hawaiian drepani-ids, cf. Paton and Collins 1989). Because feeding from floral corollae requires spe-cific actions of lapping and pumping of sugar-rich viscous solutions, bill and tonguemorphology are strongly influenced by the biomechanics of nectar extraction (Rico-Guevara and Rubega 2011; Rico-Guevara et al. 2015). Bill length and curvature arepotentially variable according to specialization on particular flowers or plant groups,but dedicated nectar-feeders are easily recognized worldwide. Partial or opportunis-tic nectarivory also characterizes many bird groups (e.g., many orioles and tanagers,including the New World honeycreepers). Most nectarivores perch on vegetativestructures while feeding, and only hummingbirds have evolved the capacity for sus-tained hovering during nectar extraction.

By contrast, diets may converge among different avian taxa but the specific mor-phological and behavioral adaptations for feeding remain distinct. Piscivory, forexample, characterizes plunge-divers, surface-scavenging eagles, and foot-propelledsurface divers such as grebes, loons, and cormorants, but is carried out by these groupsusing very different locomotor behaviors and mechanisms of capture. Granivory is awidespread feeding mode but involves a diversity of methods of seed acquisition andprocessing according to taxon and ecological context (e.g., crossbills versus dabblingducks). Similarly, frugivory is widespread among many taxa and involves feedingfrom a large taxonomic range of fruits, varying most prominently in size. Sequen-tial ingestion of many small fruits, for example, differs mechanically from repeatedpecking at the pulp of larger fruits. In part, broad-brush dietary categorizations suchas frugivory may simply reflect linguistic ambiguity about the mechanics of feeding,and a more finely resolved description of the actual process will be necessary toquantify patterns of convergence.

17.5.1.3 Convergent Behaviors with Differing Morphologies

There are several examples of birds having evolved convergent feeding behav-iors with both convergent and divergent feeding morphologies. Filter feeding hasevolved at least three times independently in birds: in waterfowl (Kooloos et al. 1989;Gurd 2006), flamingos (Zweers et al. 1995), and prions (Klages and Cooper 1992).Although some aspects of the feeding apparatus are striking in their convergence(e.g., each lineage has evolved keratinous lamellae along the beak margins, with


interlamellar spacing between 0.2 and 2.0 mm), other morphological features (e.g.,beak shape differences between waterfowl and flamingos) are strikingly divergent.Herbivory also evolved independently several times among birds (Morton 1978): inratites (Milton et al. 1994;Wood et al. 2008), landfowl (Sedinger 1997), at least seventimes inwaterfowl (Olsen 2015), in hoatzins (Grajal et al. 1989), inGruiformes (Millsand Mark 1977), in Psittaciformes (Trewick 1996), and in Passeriformes (Munsonand Robinson 1992; Bucher et al. 2003). Beak shapes among herbivorous birds takemany different forms and thus there is no single beak shape critical for croppingbehavior. Underwater pursuit diving has also evolved many times; in diving petrels,loons, grebes, cormorants (Grémillet et al. 2006), penguins (Cannell and Cullen1998), alcids (Sanford and Harris 1967), and mergansers. Most underwater pursuitdivers have relatively narrow and elongate beaks but the presence of a “hook” ordownward curvature at the end of the beak is present in some lineages (e.g., divingpetrels, cormorants, mergansers) and absent in others (e.g., grebes, loons, alcids).

17.5.2 Evolutionary Processes in Bird Feeding: NaturalSelection’s Tug of War

17.5.2.1 Dietary Flexibility

Avian diets are often multifaceted and seasonally variable, but even taxa character-ized as dietary specialists routinely consume very different kinds of resources. Forinstance, nectarivorous hummingbirds also feed on a variety of arthropods (reviewsin Stiles 1995; Yanega 2007; Rico-Guevara 2008), sap and other plant fluids, evenfruits (reviews in Kevan and Baker 1983; Estades 2003; Ruschi 2014). In addition tomeeting their primary energetic demands through the carbohydrates of floral nectar,hummingbirds are also highly specialized arthropod hunters, often catching smallflying insects and spiders for their own protein and lipid demands, and also for regur-gitation to the young by incubating females (Stiles 1995; Rico-Guevara 2008). Useof the beak in aerial insectivory (Yanega and Rubega 2004; Smith et al. 2011) is func-tionally very different from the small distal opening motions during nectar extraction(Rico-Guevara 2014), and more research is necessary to determine whether or notopposing forces of selection may act on anatomical and biomechanical features ofthese two feeding modes. In general, recognition of diverse functional roles for thesame structure can force a more quantitative description of their varied uses as wellas frequencies of occurrence, as opposed to a simplified and qualitative semanticcharacterization of diet.


17.5.2.2 Feeding Trade-Offs

Given the variety of food items that birds consume and their dietary flexibility, itis common to find morphological and functional constraints, as well as trade-offsbetween traits enhancing one feeding mode versus an opposing one. In several cases,the evolution of traits increasing feeding performance in a particular kind of food,hinder the birds’ efficiency to feed on a different item for which the biophysicalchallenges are dissimilar. For instance, different species of Flowerpiercers (Diglossaspp. and Diglossopis spp.) exhibit bill hooks of various lengths which are correlatedwith the efficiency of feeding on fruit versus nectar (Schondube and Martinez delRio 2003). Experiments modifying the hook length showed that birds with smallhooks feed more efficiently on fruit, but were less efficient at robbing nectar; theopposite was true for birds with intact bills presenting long hooks (Schondube andMartinez del Rio 2003). Flowerpiercers use their maxillary hooks to hold the baseof a flower and pierce it with their mandible, creating a hole through which theyextract nectar with their tubular tongues. Below we provide two additional feedingtrade-offs examples in waterfowl and finches.

Waterfowl face at least two major trade-offs in feeding mechanics. The first is apredicted trade-off between prey size selection and water filtration rate during filterfeeding, due to the need to separate detritus from food particles (Gurd 2007; 2008).The second is a trade-off between filter feeding and grazing (Kooloos et al. 1989; Vander Leeuw et al. 2003). Waterfowl with more duck-like beaks (e.g., mallard) showrelatively high filtering performance and relatively low grazing performancewhereasthose with more goose-like beaks [e.g., white-fronted goose (Anser albifrons)] showhigher grazing performance and lower filtering performance. Yet, waterfowl withintermediate beak shapes [e.g., Eurasian wigeon (Mareca penelope)] appear not toexperience a deficit in either filtering or grazing performance (Van der Leeuw et al.2003).

Somebirds can close their jawswithmore force than other birds.Aclassic exampleof this variation can be measured inGeospiza Finches (Herrel et al. 2009) where biteforces in G. magnirostris are around 10–15X that of its congeners. In birds withhigher bite forces, the coronoid process and associated ramus (insertion surfaces foradductor musculature) on the mandible may be relatively robust and close to theanterior tip of the bill. On the other hand, velocity of closing may be a beneficialtrait, particularly in those birds catching aerial prey items (e.g., flycatchers). High billtip closing speeds can be achieved either by lengthening the bill or moving adductorattachment sites closer to the jaw joint (Corbin et al. 2015). Although predicted by anumber of kinematic andmuscle biology studies (seeLorenz andCampello 2012), theinterplay between optimizing closing force or closing velocity or some other aspectof feeding performance (i.e., seed husking time; see van der Meij and Bout 2006; sitand wait versus wide foraging, see McBrayer and Corbin 2007), probably is not asimple trade-off. Changes in overall body or head size, possibly an evolutionary lineof least resistance (Marroig et al. 2005), may accomplish the same goal as modifyingthe in-lever to out-lever ratio (Corbin et al. 2015).


17.5.2.3 Additional Selective Pressures Acting on the FeedingApparatus

Avian bills can be used in a variety of non-feeding roles that may select for additionalfeatures of anatomical and physiological design of the feeding apparatus.Widespreaduse of the feeding apparatus in radiating heat has only recently been recognized(Tattersall et al. 2017; Homberger 2017). Large bills may have an important role inthermoregulation (Tattersall et al. 2009). Maxillary overhang has been demonstratedexperimentally to enhance ectoparasite removal by pigeons (Clayton et al. 2005),whereas overly longbillsmay impair the ability to autogroom (Clayton andCotgreave1994). Bite forces and torques, as influenced by both size and shape of the beak, caninfluence its use in hetero- and conspecific interactions (Herrel et al. 2009). Of thislatter class of behaviors, the forces of sexual selection may be particularly powerfulrelative to diverse features of beak size and shape. The spectral composition ofavian vocalizations can be influenced by beak morphology, and in turn influencespeciation dynamics (e.g., Podos and Nowicki 2004). Bills can also serve as visualsignals in territorial and mating displays. They can be used as tools of combat, assuggested anatomically when sexually dimorphic (e.g., Babbitt and Frederick 2007),and in some cases documented behaviorally. One species of hermit hummingbirdspossesses a dagger-like modification to the bill tip, which is sexually dimorphic, thatserves as a weapon during inter-male aerial combat (Rico-Guevara and Araya-Salas2015).

Overall, diverse and sometimes conflicting forces of both natural and sexual selec-tion serve to mold avian bill anatomy, feeding behavior, and functional capacity. Thisconclusion will come as no surprise to any field biologist who routinely observesbirds in the wild, but focal experimental studies on particular feeding modes may notencompass alternative interpretations for any particularmorphological feature.Giventhe range of food items consumed by any given bird species, the underlying and oftenvariable biomechanics necessary to capture and process such items, and the presenceof supplemental selective forces, many more interesting and unexpected aspects ofavian feeding behavior are likely to be described in the future.

17.6 Conclusion

Although our understanding of the avian feeding system has improved dramati-cally over recent years, there are many questions to ask. For instance, how doesperformance vary along particular axes of bill shape evolution? How does this corre-spondwith competing selection pressures? How is performancemodified by peculiarfamily-specific novelties like casques or de novo muscles? And to what extent doesthe wide range of naso-frontal hinge and palate morphologies modify kinesis andstress patterns? This last question opens up numerous opportunities for further workwith contrast-enhanced computed tomography scanning (Lautenschlager et al. 2014;Gignac et al. 2016), muscle modeling techniques such asMultibody Dynamics Anal-


ysis (Curtis 2011), and in vivo kinematic data such as that produced by XROMM(e.g., Dawson et al. 2011). When such quantitative data are coupled with detailedecological (Wilman et al. 2014) and phylogenetic (Jetz et al. 2012; Jarvis et al. 2014;Prum et al. 2015) information now openly available for birds, the possibilities forstudying not just functional morphology, but how it operates within a macroevolu-tionary framework, are enormous.

Acknowledgements Weare grateful toMargaret Rubega andGregorYanega,who have profoundlyshaped our understanding of feeding birds. Comments by Fritz Hertel and Juan Pablo Gailer sub-stantially improved the manuscript. Special thanks to Katherine Shaw for assistance with the finalstages of editing.

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chapter 17 feeding in birds: thriving in terrestrial

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