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

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Chapter 17 Feeding 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 We start with a general description of the structure of the feeding apparatus in 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 morphology and function. We establish explicit links between form and function, and consequent relations to foraging behaviors. In Sect. 17.3, we systematically explore the 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, USA e-mail: [email protected] D. Sustaita Department of Biological Sciences, California State University San Marcos, 333 S. Twin Oaks Valley Road, San Marcos, CA 92096, USA e-mail: [email protected] S. Gussekloo Department of Animal Sciences, Experimental Zoology Group, P.O. Box 338 6700AH, Wageningen, The Netherlands e-mail: [email protected] A. Olsen Department of Ecology and Evolutionary Biology, Brown University, 171 Meeting St, Box G-B 204, Providence, RI 02912, USA e-mail: [email protected] J. Bright School of Geosciences, University of South Florida, 4202 E. Fowler Avenue, NES 107, Tampa 33620, USA e-mail: [email protected] C. Corbin Department of Biological and Allied Health Sciences, Bloomsburg University, Bloomsburg, PA 17815, USA e-mail: [email protected] R. Dudley Department of Integrative Biology, University of California, 3040 Valley Life Sciences Building # 3140, Berkeley, CA 94720-3140, USA e-mail: [email protected] Smithsonian Tropical Research Institute, Balboa, Republic of Panama © Springer Nature Switzerland AG 2019 643 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_17 644 A. Rico-Guevara et al. 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 they feed. We dedicate a separate Sect. (17.4) to drinking because most birds have to perform this process regardless of their diet, and often using different mechanisms than the ones they use to feed. We then discuss evolutionary forces and patterns in bird feeding (convergences, radiations, trade-offs, etc.), including functions different from handling and ingestion that also act to shape the feeding apparatus in birds (Sect. 17.5).

17.1 Introduction: Anatomical Features of the Avian Feeding 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 critical roles in getting birds to their food, or in getting food to the bird’s beak. The beak is part of an integrated jaw mechanism, whose individual parts (and interactions among them) are more intimately described in Sect. 17.2.2. Here we focus primarily on the morphology of the beak, as the implement that interacts directly with the environment. Over the past 10–15 years we have gained tremendous insights into the genetic bases of beak development (e.g., Abzhanov et al. 2006; Mallarino et al. 2011; Bhullar et al. 2015), and how beak form and function are shaped by the loading patterns they experience (e.g., Herrel et al. 2010; Soons et al. 2010). The evo-devo of bird beaks is beyond the scope of this section (but see Bhullar et al. 2015). However, it is relevant to 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 a great diversity of shapes, sizes, and functions. The bony structure of the beak is dominated by the premaxillary, maxillary, and nasal bones of the upper bill, and the dentary bone of the lower bill (Baumel and Wit- mer 1993;Fig.17.1). Other bony elements connected to these bones (jugal, palatine, pterygoid, articular, and quadrate bones) play important roles in the transmission of forces (Bowman 1961; Soons et al. 2010; Herrel et al. 2010) and kinetic movements (Bock 1964;Zusi1984; Bout and Zweers 2001; Gussekloo et al. 2001), but these are removed from direct contact with food and/or substrates and are treated below (Sect. 17.2.2). The premaxilla is arguably the principle element involved in distributing 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 its ability 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, trabecular densities 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 from Proctor and Lynch (1993), with permission from Yale University Press feeding habits among the species studied. The orientation of the trabeculae seems to correspond to tensile and compression trajectories. Bock (1966) proposed that these trabeculae transmit forces from their points of application along the bill to the load-bearing compact bone of the outer walls, which in turn transmits stresses to the base of the jaw. Species with different bill morphologies appear to be well adapted for specific loading conditions: species that tend to apply forces at the beak tips experience relatively lower bone stresses and higher safety factors under tip-biting loads than those that tend to crush seeds at the beak base (Herrel et al. 2010; Soons et al. 2015). The beak is not all bone, however, and the overlying keratinous rhamphotheca plays an important role in dictating overall beak shape and its feeding performance capabilities (Fig. 17.2). Campàs et al. (2010) found that in Geospiza finches, the keratin layer closely corresponds to the shape of the underlying bone, and these are related by simple scaling transformations. In other groups, however, there is more discordance 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 in those species with strongly curved culmens and hooked beaks, such as parrots and raptors. These, and other, groups display a variety of tomial projections, such as the serrations of piscivorous birds, geese, and hummingbirds, which are thought to play roles in grasping food items, and also in the case of hummingbirds, male–male combat (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;Csermelyetal.1998). These may or may not correspond to underlying bone structures; for example, in shrikes these tomial structures are entirely keratinous (Fig. 17.2), whereas in falcons they are underlain by bone (Schön 1996). The baleen-like projections (lamellae) of many ducks and flamingos that are vital for filter-feeding (Fig. 17.3; Louchart and 646 A. Rico-Guevara et al.

Fig. 17.2 Upper panel: loggerhead shrike (Lanius ludovicianus) showing the hooked beak tip and tomial “tooth” (ventral projections of the rhamphotheca on either side of the tomium of the rostral upper beak). Lower panel: radiograph of a northern shrike (Lanius borealis) beak, showing the underlying bony trabeculae and the overlying keratinous rhamphotheca that formulates the hooked tip (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 a dynamic tissue that continuously grows and wears, beak shape can change plastically over relatively short periods of time (Matthysen 1989; Van Hemert et al. 2012). This could be significant because very small changes in beak size (let alone shape) could have 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 roughly half 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, present that provide tactile information (Berkhoudt 1979). An extreme adaptation has been described for the red knot (Calidris canutus), which uses Herbst corpuscles to detect pressure fields in wet substrates as induced by bill insertion and consequently 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 647

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, Heidweiler et al. 1992), c mallard (Anas platyrhynchos, Kooloos et al. 1989). The top images show the roof of the oropharynx, the bottom images show the ﬂoor of the oropharynx. (1) choanae, (2) papilla choanales, (3) rima infundibuli, (4) papillae linguae caudales, (5) papilla pharyngis caudodorsales, (6) papillae pharyngis caudoventrales, (7) ruga palatina mediana, (8) rugae palatinae laterales (line indicates 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 of the authors. Panels b and c reprinted by permission from Springer Nature, Zoomorphology 648 A. Rico-Guevara et al. reﬂected off buried mollusc prey (Piersma et al. 1998). Although this particular behavior has only been described for the red knot, similar high receptor densities and 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 feeding behavior, other functions affect the rhamphotheca as well (Sect. 17.5.2.3). A number of songbirds (Belding’s sparrow, Passerculus sandwichensis beldingi; Alameda sparrow, Melospiza melodia pusillula; lark bunting, Calamospiza melanocorys)show clear sexual dimorphism and seasonal changes in their bill shape indicating that the bill 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 correlation between bill length and ambient temperature, with shorter bills in colder environments. This shows that the bill might contribute to heat loss and thus can play an important role in the cost of thermoregulation (Symonds and Tattersall 2010).

17.1.2 Morphology and Evolution of the Avian Lingual Apparatus

The tongue is a key evolutionary novelty for terrestrial feeding (Schwenk 2000; Chap. 11), largely overlooked in earlier studies of feeding mechanics (Schwenk and Rubega 2005). Furthermore, the evolution of flight and consequent diversification of feeding ecologies has been recently linked to the elaboration of tongue structure and function (Li et al. 2018). For pragmatic purposes, here we define the avian tongue as the discrete, rostralmost portion of the lingual apparatus (bones, muscles, nerves, epithelia, etc., detailed in Homberger 2017), which is typically rigid, covered by keratinized epithelium, and that is mostly enclosed within the oral cavity (sensu Lucas and Stettenheim 1972); sometimes also called the “free part of the tongue” or lingual body (Homberger and Meyers 1989; Homberger 2017). Avian tongues range from vestigial (e.g., pelicans; McSweeney and Stoskopf 1988) to extensively elaborate (e.g., ducks, Kooloos et al. 1989;Fig.17.3). Bird tongue bones, attached muscles, 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). This is 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 fused into a single structure in adults, which is commonly shaped as an arrow head and it is embedded in the tongue, sometimes with cartilaginous ends; (2) basihyale, normally flattened and allowing the widest range of rotation at the “joints” with the paraglossum and the ceratobranchials; (3) urohyale, in most cases fused to the caudal end of the basihyale in adults, with a cartilaginous end, and sometimes absent altogether; (4) ceratobranchiale, slender, paired and cylindrical, normally ossified (in some cases the only element ossified), and usually the longest elements except 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 649 in birds with extreme tongue protrusion; (5) epibranchiale, paired, cylindrical, and abutting upon the caudal end of the ceratobranchials, they are the elements that, when elongated to allow great protrusion, reach the maximum relative length among birds; (6) pharyngobranchiale, attached to the end of the epibranchials, they are normally cartilaginous, 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 hyobranchial elements have a long list of synonymies; in some cases, these main parts present processes, extensions, accessory elements, and vary from cartilaginous to ossified across 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 tongues lack the intrinsic musculature characteristic of the rest of tetrapods [except some groups that use their tongues to collect and/or manipulate their food, e.g., parrots, (Homberger 1986), and woodpeckers (Bock 1999)]. Avian tongues are comparatively simple among tetrapods regarding internal musculature (Schwenk 2000), yet they can be very sophisticated depending upon their role in the feeding process (intraoral transport, food collection and/or manipulation, etc., Fig. 17.4). The evolution of gizzards in archosaurs released their jaws from food processing (review in Reilly et al. 2001) and bird bills and tongues are exclusively food gathering as opposed to processing 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 “hyobranchial joints”. In addition, the bird hyobranchium and associated musculature appear more rostral when compared to other reptiles (Tomlinson 2000), which is probably linked to the disappearance of the ceratohyals [which are not used in displays like in lepidosaurs (Bels et al. 1994; but see Riede et al. 2015)], and the avian apomorphic paraglossum offers reach and support to the largely keratinous tongue (Tomlinson 2000; Hill et al. 2015). This keratinization and stratification of the lingual epithelium likely evolved during the transition from wet to dry environments in bird ancestors (Iwasaki 2002). We propose that the appearance of cornified tongue tissues, along with the shift from food processing to also gathering, facilitated the development of intricate lingual surface structures and complex structural configurations that allowed some bird groups to excel in specialized niches (e.g., tongues covered with hair-like structures in filter feeders, barbed tongues in penguins, tongues with spear-shaped tips in woodpeckers, tubular tongues in hummingbirds). Avian tongues, although usually hidden, could be considered as diverse and plastic as bills, and have played a key role in the evolution of birds, the group with one of the most morphologically varied array of feeding structures among tetrapods (Rubega 2000). Bird tongues present cases of tremendous specialization and may differ dramatically from one another, however, a general design can be identified for most of them with the following parts (from rostral to caudal): (1) apex linguae, or tongue tip, usually only composed of lamina propria (connective tissue layer) between dorsal and ventral epidermal epithelia, the external keratinized layer of the tongue epithelia at the apex is thicker in the ventral surface, sometimes frayed and in extreme cases 650 A. Rico-Guevara et al.

Fig. 17.4 Avian hyobranchium and tongue. a Idealized dorsal aspect of the tongue bones, or hyobranchium, with the tongue overlaid in gray on top. b Dorsal view of the tongue; the Latin word “linguae” which means “of the tongue” has been removed from all the terms for clarity. See text for definitions of all the components. c Lateral view of the tongue body and root during food transport. d Most birds use their protrusible hyobranchia and tongues to move food to their throats by placing it behind the tongue wings. Cedar waxwing (Bombycilla cedrorum) photographs by Kim Michaels developing as cuticula cornificata linguae (lingual nail); as the first contact point with the food, the apex is modified in a variety of ways, including lance-shaped with lateral barbs, fraying along all edges, sometimes cleft to deeply bifurcated, and others with fringed margins curling to form one to several tube-like grooves; (2) corpus linguae, or tongue body, usually wedge-shaped tapering rostrally, in most cases the paraglossum is the only reinforcing element, although the basihyale could also be partially to completely embedded as well; the tongue body usually contains a variety of lingual glands, connective and adipose tissue, and sometimes corpora cavernosa; (3) dorsum linguae, or dorsal surface, usually made of keratinized epithelium stratificatum squamosum (cornified epidermis), it sometimes presents a median sulcus (longitudinal shallow groove); in the tongue body, the keratinized layer is 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 651 thicker in the dorsal surface (in contrast with the apex); (4) margo linguae, or lateral edges, present most of the papillary projections (besides the papillary crest), modifications include backward-facing serrated margins, spine-like projections, hair-like laterally projected filiform papillae, and forward-facing frayed margins; (5) ventrum linguae, or ventral surface, it is usually convex transversely, smoother, with a thinner epithelial layer and a thicker lamina propria than the dorsal side; the hyoid elements areclosertotheventrum than to the dorsum, and in some cases the ventrum is found on 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 rows of spine-like, sometimes conical, papillae pointing caudally and of varying sizes, which normally follow the caudal contour; sometimes absent; (7) alae linguae,or tongue wings, are also referred to as giant conical papillae, and are largely supported by caudally directed paraglossal projections forming an inverted “V” at the tongue base; sometimes absent altogether; (8) radix linguae, or tongue root, is a distinctive support structure extending from the ventrum; it usually contains the basihyale thus allowing a hinge for the rest of the tongue (Fig. 17.4b, c, Lucas 1895; Zweers 1982; Homberger 1986; Baumel and Witmer 1993; Tomlinson 2000;Erdo˘gan and Iwasaki 2014; Homberger 2017). A list of synonymies of these main lingual components similar to those existing for the hyobranchial skeletal elements and musculature has not been yet provided.

17.1.3 Other Structures of the Oropharynx

Within the avian oropharynx, we find a completely different set of structures that play a role in feeding behavior. In many species, we find papillae on a number of locations and structures inside the oral cavity. The most common locations for papillae are around the choanae, near the base of the tongue, and just caudal to the epiglottis. In some species, such as the chicken, papillae are found on almost the complete roof of the oropharynx. It is assumed that most of these papillae play a role in intraoral food transport, either for holding the food item or for transporting it towards the oesophagus. Salivary glands in the oral cavity also play a role in intraoral transport. These glands are dispersed over the whole oropharynx, although some regions have higher densities and are considered separate glands [see (McLelland 1979)]. In most cases, they provide lubrication for the food (McLelland 1979), which is reflected in the variation among birds with different diets. In general, for birds eating dry food items, such as granivorous birds, the salivary glands are large, whereas in fish-eating birds they are almost absent (Denbow 2015). In birds using the “slide-and-glue” mechanism for intraoral transport (Zweers et al. 1994), such as pigeons (Zweers 1982) and chickens (Van den Heuvel and Berkhoudt 1997), saliva is even more important for intraoral transport as it actually glues smaller food items to the tongue to facilitate transport towards the oesophagus. Information about enzymatic action within the saliva is sparse. 652 A. Rico-Guevara et al.

Although less prominent than in other vertebrates, several taste buds can be found in the oropharynx of birds, sensing all traditional tastes (Roura et al. 2013). An overview 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 even reaches 100,000 (Clark et al. 2015). It must, however, be kept in mind that these are absolute numbers, and the 35,000 taste buds found in an ox is obviously much larger than even the largest bird. The location of the taste buds is mainly in the non-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 they are occasionally also found in the rhamphotheca (Crole and Soley 2015). Birds, in general, 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 among species. Frugivorous and omnivorous birds have more affection for sweet tastes than other trophotypes, with an extreme case in the granivorous chicken that seems to lack the 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 strongly from 0.35% to over 35.0% (Rensch and Neunzig 1925). Analyses of bitter receptor gene clusters showed a number of variations in the receptors indicating that bitter is probably perceived in different ways in different populations and species (Davis et 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 in chickens and little is known from other species. In chickens, the general pattern is that extreme pH values are avoided (Roura et al. 2013). The final taste, umami, has only been predicted based on the fact that in the chicken genome genes have been found 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 and Mason 1990; Moran and Stilborn 1996) but more research is needed to elucidate the actual umami perception of birds. In summary, the oropharynxes of birds show a large number of adaptations to specific feeding behaviors, including prey detection, food capture, food assessment, and the intraoral transport of the food.

17.2 From Feeding Apparatus Morphology to Feeding Biomechanics

17.2.1 The Study of Bird Feeding

Bird bills come in a truly astonishing variety of shapes and sizes. This variation is often associated with specific feeding behaviors that exert strong selective pressures on cranial architecture (Grant and Grant 1993), and with this relationship so immediately apparent, it is perhaps unsurprising that few studies have bothered to 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 653 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 bird feeding. The first was a bias in phylogenetic sampling, with the majority of work heavily focused on model groups such as Darwin’s finches, convenient domestic birds, or species whose unusual behavior or morphology made them of particular interest. The second was that many studies make functional assertions based on morphology alone, and lack explicit hypotheses. Birds are rife with many-to-one and one-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 to many 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 be difficult to define, needing clear differentiation between colloquially interchangeable but 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 statistical power. Consequently, we know very little about how bill shape responds to feeding selection versus other factors, such as phylogenetic relatedness, development, and sexual selection. Indeed, many non-feeding functions and behaviors, such as preening (Clayton et al. 2010), competition and territoriality (Rico-Guevara and Araya-Salas 2015), thermoregulation (Tattersall et al. 2009), and vocalization (Huber and Podos 2006; Giraudeau et al. 2014) impose other selective pressures in ways we are only beginning to understand. In addition to in vivo experimentation, a range of modeling methods may be employed to investigate the function of avian feeding structures. The most appropriate method will depend on the hypothesis being tested, but all models will be grounded in a knowledge of anatomy. Information on shape may be supplemented by muscle data from traditional (Baumel et al. 1993) or digital dissection (Lautenschlager et al. 2014; Quayle et al. 2014), electromyography (Zweers 1974), and kinematic data from high-speed video (Rico-Guevara and Rubega 2011; Sustaita et al. 2018b), Roentgen stereophotogrammetry (Gussekloo et al. 2001) and X-ray Reconstruction Of Moving Morphology (XROMM, Dawson et al. 2011). This provides valuable physiological brackets for the model input parameters. Models need not be overly complicated. Despite their simplicity, lever diagrams and bar linkages are immensely useful tools for calculating crucial performance metrics such as bite force (Sustaita 2008) and mechanical advantage (Sakamoto 2010; Olsen and Westneat 2017). Even simple physical paper models can prove to be remarkably illustrative, paving the way for more complex numerical modeling to explain their features (Smith et al. 2011). To date, the most complicated modeling approach applied to bird feeding has been Finite Element Analysis (FEA). FEA is an engineering technique capable of calculating deformation (strain) and mechanical stresses in structures with complex geometries, loading regimes, or distributions of material. The method works by subdividing the structure into a large number of bricks (“elements”) of simple shape joined at their corners by nodes to form a mesh. This model is then solved by applying loads of 654 A. Rico-Guevara et al.

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), and indicate where the structure is most likely to fail. The flexible zone of rhynchokinetic bending is clearly highlighted by higher stresses in this model. Figure reproduced from Cuff et al. (2015) under CC 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 simultaneous equations. Results are visualized as contour plots over the structure or queried at individual 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 particular strength or weakness, has obvious applications for functional morphologists [see Rayfield (2007) for a review]. In particular, hypotheses about biomechanical function as it relates to form through evolution can be readily quantified due to the ability to manipulate and modify said form in silico. In birds, FEA has been used to demonstrate performance differences that correspond to beak shape and the preferred mode 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 (Soons et al. 2012) by allowing the bill to act as a sandwich foam: a thin, stiff shell of keratin encloses a closed-cell “foam” of trabecular bone, conferring high stiffness and resistance to buckling for low weight (Seki et al. 2005, 2006). This is particularly important for birds with large bills relative to their body size. In comparison to other theropod dinosaurs, bird skulls show an evolutionary trend towards an exceptionally high degree of fenestration. By using FEA to demonstrate the load-bearing role of the postnasal bars during feeding, Gussekloo et al. (2017) suggest that the loss of these structures in palaeognathous birds may explain why palaeognaths have failed 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 655 to explore the disparity of beak shapes seen in neoganthous birds (who retain these structures). Finally, FEA offers the unique opportunity to perform functional analyses of extinct birds (e.g., Degrange et al. 2010). A caveat of this is that 3D preservation is required (rare in the avian fossil record), but the successful retrodeformation and analysis 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 bird feeding. This is partially due to high start-up barriers in cost, computer power, and necessary 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 studies (Bright 2014), and bird skulls present several unique challenges regarding their incredibly thin and highly pneumatized bones, multiple moving parts in the quadrates and palate, flexible bending zones, and the presence of a rhamphotheca. So far, the only 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 broadly possible to replicate strain patterns, but performance values are generally unreliable. This is likely due to an incomplete understanding of model input parameters, and for the time being limits studies to those that are purely comparative (Bright 2014). For- tunately, several comparative questions present themselves in the under-quantified realm of bird feeding functional morphology, and though in its infancy in birds, comparative and hypothetico- deductive FEA (sensu Rayfield 2007) is already yielding interesting 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 bones posterior 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 manipulation and Roentgen stereophotogrammetry (e.g., Gussekloo et al. 2001), computational simulation (e.g., Van Gennip and Berkhoudt 1992; Meekangvan et al. 2006;Olsen and Westneat 2017), and in vivo XROMM (e.g., Dawson et al. 2011). In most birds, such as mallards (Anas platyrhynchos;Dawsonetal.2011) and sparrows (Hoese and Westneat 1996), the upper beak rotates like a hinge, termed prokinesis (Bühler 1981), 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 beak bends at ﬂexion zones more rostrally along the beak, termed rhynchokinesis (Zusi 1984). These ﬂexion zones can be relatively short, allowing just the tip of the beak to rotate, as in hummingbirds (Yanega and Rubega 2004) and shorebirds (Estrella and Masero 2007), or relatively long, causing broad bending of the beak, as in palaeognathous birds (Gussekloo and Bout 2005). Variability in the quadrate-neurocranium 656 A. Rico-Guevara et al. articulation also affects quadrate kinematics, ranging from allowing a full range of quadrate rotation as a single condyle in mallards (Dawson et al. 2011,Fig.1)or constraining quadrate rotation to a single axis of rotation, as two separate, widely spaced condyles in owls (Olsen and Westneat 2017, Fig. 2). The variably present pterygoid-neurocranium joint, sometimes accompanied by a basipterygoid process on the neurocranium, is thought to function primarily in stabilizing skull forces in palaeognathous birds (Elzanowski 1977; Gussekloo and Bout 2005), although its function in neognathous birds remains unclear. Cranial kinesis is actuated by seven muscles that interconnect all the mobile cranial bones, except the jugal and upper beak (Fig. 17.6; Zweers 1974). Studies that have recorded activity of the avian jaw muscles (i.e., by electromyography) either during feeding or drinking are few and limited to four species: mallards (Anas platyrhynchos; Zweers 1974), chickens (Gallus gallus domesticus; Van den Heuvel 1992), pigeons (Columba livia; Bermejo et al. 1992; Bout and Zeigler 1994), and Java sparrows (Padda oryzivora; van der Meij and Bout 2008). In general, the depressor mandibulae (DM) and protractor quadrati et pterygoidei (PQP) muscles act as jaw openers, with the former depressing the lower bill (Bout and Zeigler 1994; Zweers

Fig. 17.6 The main skeletal components and muscles in the bird skull. Most elements are connected by 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 not present in all bird lineages (dotted line). Muscles (red lines) attach to various skeletal elements, with some muscles connecting more than two elements (corresponding labels are located at the ﬁlled circle end of each line or lines) 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 657

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 function in “unlocking” the lower bill through a mechanism involving the quadrate and the postorbital ligament, which extends from the neurocranium to the lower bill (Zusi 1967). After DM and PQP activity, the adductor and pseudotemporalis muscles generally 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 a ﬁxed lower bill, shows the most variable activity. In some cases, PT activity is similar to adductor activity (Van den Heuvel 1992) whereas at other times it is active at various 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 functions dually as a closer of the upper and lower bill, and that upper and lower bill motions are often slightly out of phase (Zweers 1974;Dawsonetal.2011) or independent of one 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 is opening (depressing) and closing (elevating). Depressing the lower jaw is facilitated by gravity and the mandibular depressor muscles, originating on the paroccipital process on the posterior skull and inserting on the caudal fossa of the posterior mandible (Bühler 1981; Baumel and Witmer 1993; Vanden Berge and Zweers 1993;Fig.17.6). Total gape is increased by elevating the upper bill (modeled by Hoese and Westneat 1996; and see rhynchokinesis portion of this chapter), or increasing the mediolateral volume (see below). Closing the lower jaw is accomplished by two main muscle groups. The ﬁrst is the pterygoideus, originating on palatine and pterygoid bones of the cranium and inserting on the caudomedial aspect of the mandible. The second group includes the mandibular adductors, originating on the skull caudal and ventral to the orbit and inserting on the mandible (Fig. 17.6). Passive components of opening and closing are facilitated with a series of ligaments (e.g., occipitomandibular, postorbital) linking attachment sites that are similar to associated musculature (Bock 1964; and see Baumel and Raikow 1993). Marked variation in force and velocity of closing is thought to be a result of a number of different biomechanical strategies including 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 adductor mandibulae muscle groups have independent attachment sites and lie at oblique angles to one another anterioposteriorly and lateromedially (Fig. 17.6),birdsmay protrude and retract the lower jaw (see Bühler 1981) and exhibit lateral excursions. These movements are important in the food manipulation capacities of icterids (orioles and allies) that roll seeds over palatine blades (Beecher 1951), rhamphastids (toucans) that position fruit before ballistic feeding (Baussart et al. 2009), and psittacids 658 A. Rico-Guevara et al.

(parrots), which may undergo a complex oral handling of food items prior to swallowing (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) their mandibular rami (Böker 1938; Meyers and Myers 2005). This action is mediated by special hinge zones along each ramus (Smith et al. 2011;Zusi2013), and a twisting, rotating action causing the distal portion of the mandible to bend downward (Zusi 2013), and the intraramal space to increase dramatically. Increasing the gape in this way is used in precopulatory behaviors and territorial displays (i.e., exposing the inner mouth; Snow 1974; Stiles and Wolf 1979; Rico-Guevara and Araya-Salas 2015), obtaining aerial, and submerged prey items (increasing net-size; Bühler 1970; Burton 1977; Yanega and Rubega 2004; Meyers and Myers 2005), and obtaining buried prey items (Judin 1961).

17.2.2.3 Integration of Mechanisms

Feeding behavior comprises foraging, food acquisition, and digestion (Zweers et al. 1994). Here we will focus on food acquisition only, which includes the whole process from the movement 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 is impossible to name them all. The most commonly observed form, and probably the ancestral 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 by intraoropharyngeal transport and a final swallowing movement by retraction of the larynx (Zweers 1982; Vanden Heuvel and Berkhoudt 1997). The first grasp-phase and final swallowing are very similar among species, but the intraoropharyngeal transport varies depending on both food size and species. The simplest form is the so-called cranio-inertial, or “throw and catch” behavior (e.g., Fig. 17.4c), in which the bird accelerates its head back and/or upwards while holding the food item, then releasing the food item, followed by a head movement in the opposite direction resulting in relative displacement of the food item in the direction of the oesophagus. This behavior is recorded for large ratites such as rheas and ostriches, and in long billed frugivorous birds such as toucans and hornbills, but is also employed by pigeons and chickens when eating large food items (Zweers 1982; Van den Heuvel and Berkhoudt 1997; Tomlinson 2000; Gussekloo and Bout 2005; Baussart et al. 2009; Baussart and 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 with saliva after which the tongue is retracted. After retraction, the food item is pressed against the palate, after which a second cycle might take place (Zweers 1982; Vanden Heuvel and Berkhoudt 1997). The use of the tongue for transport is observed in many other species (e.g., Fig. 17.4d), but is often more complex than the slide-and-glue mechanism and linked to special morphological features. A well-described example is 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 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 659 the lateral side of the tongue are used for transport in the caudal direction (Kooloos 1986). It is assumed that from the general pecking feeding behavior several other feeding behaviors have evolved such as filter feeding and probing behavior (Zweers 1991; Zweers et al. 1994). Filter feeding in ducks probably evolved from a grasping ancestor and can be seen as an adaptation from lingual transport as it fully depends on the craniocaudal movement of the tongue for both the transport of water and the filtered food particles (Kooloos et al. 1989; Zweers and Vanden Berge 1997). Adaptations to probing behavior are an elongation of the bill to increase probing depth, increased sensitivity in the bill tip for sensing buried prey, and the presence of rhynchokinesis (Zweers and Gerritsen 1996; Zweers and VandenBerge 1997). Rhyn- chokinesis is a special form of cranial kinesis, and currently the only form of avian cranial kinesis for which clear functional advantages are recognized. In rhynchokinesis 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 when opening their bill while catching prey. In addition, by curving the bill tip behind the food item, there is less chance of losing the food item during its extraction from the substrate (Zweers and Gerritsen 1996). Further intraoropharyngeal transport can be done 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 the wide diversity of other feeding behaviors and the large radiation we observe in modern birds. As shown by the adaptive radiation in Darwin’s finches, food availability is a strong 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 shape accordingly varies according to diet is generally accepted as a truism. However, this tenet is belied by two important points: (1) most birds of any given species opportunistically consume a variety of food types, despite any ostensible adaptations for a particular diet, and (2) beaks also play essential roles in other functions, such as in thermoregulation (Greenberg et al. 2012), vocalization (Podos 2001), and ectoparasite control (Clayton et al. 2005). As a result, contemporary views are shifting toward a more holistic understanding of the feeding apparatus, in recognition of the fact that birds, like other vertebrates, are not necessarily adapted to speciﬁc diets, but rather to the mechanical demands of consuming different types of food (Schwenk 2000; Schwenk and Rubega 2005; Gailer et al. 2017). Accordingly, this section focuses on the diversity of the modes of feeding (e.g., Fig. 17.7), and not necessarily on the diversity of avian diets. A comprehensive review of avian food habits is beyond the scope of this chapter and would take several volumes to ﬁll. Nevertheless, there are excellent 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 660 A. Rico-Guevara et al.

Fig. 17.7 Birds have evolved to exploit resources in terrestrial, aquatic, and aerial niches; as shown here they have a diversity of feeding tactics that have shaped not only their food acquisition and processing 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 face while 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 attributes with 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 dismantles and 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 lower bills and held in place with the tongue. The lower mandible is then pushed forward 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 661

(towards the tip of the bill) and the outer coat is separated, generally along natural margins of the seed coat (Van der Meij and Bout 2006).Thelowerbillmaybe moved side-to-side in order to further separate the coat from the seed. Seed-cracking is employed by larger birds (e.g., parrots; Homberger 2003), birds with relatively large bills (e.g., grosbeaks), or birds with plates or keels in the mouth (e.g., blackbirds). Cracking is similar to husking, where the seed is crushed or opened but not necessarily along its natural margin, or alternatively the seed may be rolled along the edge of a keel formed from the palatine bones, as seen in blackbirds (see Beecher 1951). 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 repeatedly hitting the object with its bill.

17.3.1.2 Folivores

Phytophagy, referring to the consumption of leaves (as in folivory) or other vegetative plant structures, is a restricted dietary strategy in birds, characterizing only about 3% of extant taxa. Because the energy density of leaves is low compared to that of plant reproductive structures and of animal tissue, a greater mass investment is required of the avian digestive system to process such material, along with a larger gut volume (Morton 1978; Dudley and Vermeij 1992). In turn, energetic costs of flight are disproportionately increased, rendering folivory a challenging nutritional strategy for 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) also correlates 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 process such food, including the use of gizzard stones or of crushing ridges in the crop (e.g., doves, hoatzin). Transient folivory, particularly among frugivorous taxa such as tanagers, may be more common than is currently realized (e.g., Munson and Robinson 1992), but seems to be driven by seasonal scarcity of more preferred energy- rich fruits, thereby illustrating the ecological limitations of folivory as a dedicated nutritional 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. Most frugivorous birds eat the fruits whole, using catch and throw behavior for intraoral transport (Baussart et al. 2009; Baussart and Bels 2011). Very few birds actually take 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 662 A. Rico-Guevara et al. of these families, only a few species eat fruit, and those species often only eat fruit occasionally, but it does show the preference for this food source. This review also shows that birds use all types of fruits, from soft to hard, and forage for fruit attached to the plant or fallen to the ground. Also, the extent of the use of fruit varies among species. Many species pass seeds intact through the intestinal tract, whereas others crush 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 role in fruit selection in birds, but color is an important factor, with birds favoring red and 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;Berman1984; Symes and Downs 2001).

17.3.1.4 Nectarivores

Nectar is exploited facultatively by a plethora of bird species with varied morphologies (e.g., Cecere et al. 2011; Dalsgaard et al. 2017). Yet there are some birds whose subsistence depends on feeding efficiently on nectar, and consequently, their feeding apparatus has adapted to reach, extract, and swallow small amounts of liquid rapidly. Most specialized nectarivores access nectar chambers by traversing long corollas with slender and elongated bills; protruding their tongues far past their bill tips and gathering nectar with brushed and/or tube-like tongue tips. These “anthophilic” (Stiles 1981) morphofunctional adaptations vary with the fluid collection and intraoral transport mechanism of each particular group. For instance, hummingbirds use surface tension trapping (Rico-Guevara and Rubega 2011) and elastic pumping (Rico-Guevara et al. 2015) to fill their bi-tubular, fringed tongues, and use their flexible bills and tongue wings to move nectar backwards hydraulically (Rico-Guevara 2014). Sun- birds with comparable bills and tongues (e.g., Schlamowitz et al. 1976;Downs2004) may employ similar mechanisms. Honeyeaters with multi-tubular, brushed tongues could employ capillary wetting both within and between their distal splits (Gadow 1883; Paton and Collins 1989; Collins 2008). All of these birds squeeze their tongues with their bill tips between licks, but other specialized nectarivores have to feed with their bills open. Among these, lorikeets (Trichoglossus spp.) exhibit lingual apical filiform papillae that form nectar-collecting brushes (reviewed by Homberger 1980; Gartrell 2000) that can be discharged at the palate. Flowerpiercers (genera Diglossa and Diglossopis) have inverted bi-tubular tongues with the openings of the tube-like grooves on the ventral side (Moller 1931; Schondube 2003), capable of sustained flow 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 species number, individuals, and total volume, so it is not surprising that invertebrates are an 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 663 important food source for birds. Given that invertebrates are so morphologically and behaviorally diverse, birds have evolved many different feeding behaviors, varying from 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 buried invertebrates (molluscs, insects, worms) are often probers, which means that they insert 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 (Gerritsen and Meiboom 1985; Piersma et al. 1998). Additionally, almost all probers show rhynchokinesis (Zusi 1984), which helps reduce the total resistance encountered from the substrate while opening their bill tips beneath it. Other aquatic invertebrates can be obtained by efficient filter feeding as observed in spoonbills and flamingos (Zweers et al. 1995). At the other extreme are the aerial insectivores, which require extreme high-speed flying and agility to capture prey on the wing (below). Other groups of birds feed on arthropods living in, or on, plants. Birds that get their food from inside the bark of trees include woodpeckers. Woodpeckers peck holes in the bark of trees and subsequently remove insects using their long-barbed tongue, sticky with a special 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 hammering into wood (Gibson 2006; Yoon and Park 2011; Lee et al. 2014). For an overview of other 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 that probe 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 as adaptations seen in insectivorous Darwin’s finches, shows that the avian body plan can easily adapt to different types of insectivory (Tebbich et al. 2004; Claramunt 2010).

17.3.1.6 Feeding on Vertebrates

Feeding on vertebrates is a very different endeavor from feeding on invertebrates because vertebrates are usually larger prey items, both absolutely and relative to predator body size. Vertebrates are arguably more challenging for predators to phys- ically subdue, dispatch, and dismember for ingestion. The foraging behavior of meat- eating birds (diurnal raptors and owls) has traditionally been dichotomized by “sit and wait” ambushing versus active searching and pursuit strategies (Jaksi´c and Carothers 1985), 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 feed on, such as birds, mammals, or lepidosaurs. The quintessential “raptorial” features of 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 bill and deep mandibular symphysis) and scavengers (e.g., long, narrow, highly curved 664 A. Rico-Guevara et al.

“meathook” upper bill). Despite clear indications of the effects of diet on beak form and function, body size (i.e., allometry), in association with constraints imposed by cranial integration (coordinated development of parts) and phylogeny (i.e., shared ancestry) have recently been identified as more important drivers of the variation in beak shape observed across the diurnal raptors (Bright et al. 2016). As previously mentioned in regards to some frugivores (e.g., parrots) and granivores (e.g., tits), the feet constitute an important component of the feeding apparatus in these birds (Clark 1973). Birds that tend to grasp and carry prey items show greater relative development of the deep (distally inserted) digital flexor muscles (Backus et al. 2015;Fig.17.8aversusFig.17.8b). The hypertrophied talons (particularly that of the second digit) of most raptorial birds vary considerably in size and shape (e.g., degree of curvature) (Fowler et al. 2009;Csermelyetal.2012). Variation in claw size has been linked to dietary differences among taxa, with those that take fish and large (relative to body size) mammals tending toward larger (relative to toe length) talons, and those that feed on birds and smaller mammals tending toward relatively smaller 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 the ground 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 are finely tuned to differences in feeding behavior (Hertel 1994), but as a group vultures tend to have less muscle mass and area allocated to the digital muscles than do pursuit predators (Hertel et al. 2015). Some vultures, such as the lammergeier (Gypaetus barbatus), process bones by dropping them from great heights in order to break them into pieces on the rocks below (Ferguson-Lees and Christie 2001). Furthermore, raptors and owls are not the only carnivorous birds, as there is a variety of primarily insectivorous or omnivorous taxa that feed opportunistically on small (but perhaps large relative to their body sizes) vertebrates. They include butcherbirds, shrikes, puffbirds, jacamars, frogmouths, and corvids (ravens, crows, and jays), to name just a few. In some cases, these birds may possess formidable killing implements, but perhaps not the whole “suite.” For example, shrikes have sharply hooked beaks with tomial teeth as do falcons (Fig. 17.2), but lack the talons of these more exclusive carnivores (Cade 1995; Schön 1996). Shrikes employ clever killing maneuvers (Sus- taita et al. 2018b) and impaling (Yosef and Pinshow 2005) to compensate for the lack of these additional predatory weapons. Piscivores (fish-eaters) have a very different array of adaptations given the disparate challenges of locating and capturing fish under water (see below). 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 665

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 experience downward-directed forces from grasping and carrying objects (e.g., raptors; left) and b birds that tend 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), under Royal 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 simply staying stationary and waiting for food to come to them. Also called “sit-and- wait”, or “ambush” foraging, this search-minimizing technique has ramifications in evolutionary ecology research [see the central place foraging hypothesis of Orians and Pearson (1979)]. Sally-hawking is a behavior in which a bird will wait at a perch for a suitable prey item, fly out to capture it and return to the same or a dif- 666 A. Rico-Guevara et al. ferent perch for consumption (Fitzpatrick 1980). This behavior has evolved many times and is generally associated with particular morphological characteristics, such as a relatively wide bill and long rictal bristles (Fitzpatrick 1980; Corbin 2008). Passerine sally-hawking specialists include species from different families of flycatchers (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 and bee-eaters. Also, hummingbirds acquire much of their protein via sally-hawking behaviors (Stiles 1995; Yanega and Rubega 2004). An extension of sally-hawking is seen in the pouncing behaviors of some flycatchers (Sayornis spp., phoebes), bluebirds and thrushes (Sialia spp. and Turdus spp.; Corbin et al. 2013), and terrestrial foraging kingfishers (e.g., East and South African Halcyon; Corbin and Kirika 2002). The energetic considerations of landing to capture a prey item rather than staying airborne 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 rapid maneuvers (i.e., torsional agility; see Dudley 2002). Although aerial insect fauna is abundant, cruising flight, for which long and slender wings are most efficient, is necessary to capture sufficient prey. Such wings have a high moment of inertia, however, which impedes rapid rotations of the body, and there is thus a conflict between the demands of energy efficiency and capture success (Warrick 1998). Aerodynamic studies have demonstrated the biomechanical underpinnings to such simultaneous abilities. 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 used to capture insects (Lentink et al. 2007). Caprimulgiforms and swallows presumably engage in similar behaviors, but have not yet been investigated. Aerial insectivory by hummingbirds, by contrast, typically occurs at low speeds or while hovering, and involves primarily body rotations coupled with rapid beak snapping (Yanega and Rubega 2004).

17.3.2.3 Bird- and Bat-Eaters

In addition to the array of vertebrate-eating adaptations described above, raptors that specialize on volant prey (e.g., birds and/or bats), include falcons and accipiter hawks. They exhibit a few key behavioral and morphological modiﬁcations. These raptors tend to possess relatively long toes (particularly the middle toe), which are thought to increase the probability of contacting airborne prey items (Payne 1962; Wattel 1973; Bierregaard 1978;Csermelyetal.1998; Einoder and Richardson 2007). Similarly, Csermely et al. (1998) suggested that talons may have evolved as a mechanism to 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 667 elongate the toes in kestrels to increase the surface area for contacting prey. Those species 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 Christie 2001).

17.3.3 Catching Aquatic Prey

17.3.3.1 Surface Feeders

To feed on surficial prey, prey located on or near the surface of water, different species of waders have developed specialized mechanisms. For example, spoon-billed and other calidrid sandpipers, as well as oystercatchers, employ a tactile method termed “stitching”, which consists of inserting the bill down to a centimeter under the surface and performing rapid up and down “sewing” movements (Burton 1971; Hulscher 1976; Kelsey and Hassall 1989). Such tactile feeding is mainly used under poor light conditions, but it could also explain the widened bill tips of the spoon-billed sandpiper (Calidris pygmaea;Burton1971; Mouritsen 1993). Phalaropes and other shorebirds use surface tension transport (Rubega and Obst 1993; Rubega 1997), a feeding mechanism that takes advantage of the adhesion of water drops to the inner bill surfaces to move prey proximad through quick opening and closing (see also Zweers 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, and organic detritus found as a cohesive, densely packed mat (i.e., “biofilm”) layered on mudflat surfaces (Elner et al. 2005; reviewed by Jardine et al. 2015). It has been proposed that small tongue spines found in biofilm feeders are used to collect bits off this layer (Elner et al. 2005; Kuwae et al. 2008, 2012). However, the spines are not restricted to just the tip (Elner et al. 2005), and the limited tongue protrusion abilities in these birds (Kuwae et al. 2008) suggests that the tongue is more involved in filtration of food particles.

17.3.3.2 Filter Feeders

The simplest form of filtering prey from water or mud has been proposed for slender- billed shearwaters (Ardenna tenuirostris), which by opening and closing their bills suck in and retain small prey between overlapping projections in the palate and dorsal lingual surface. This surface acts as a filtering mesh, and the surplus water is discarded 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 minute prey may be used by some penguins and auks (Olson and Feduccia 1980). A different filtering method 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 668 A. Rico-Guevara et al. extensible pouch, controls the pumping of water in and out the beak to catch prey along 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 different depths are found in flamingos. Flamingo beaks are strongly decurved to maintain the lid-like maxilla perpendicular to the filtering substrate while they rock their heads back-and-forth (Zweers et al. 1995). Water and food particle inflow is controlled by depressing and retracting the tongue, which functions like a piston, while expanding the gular region. The expulsion of water occurs by reversing the tongue movements (Jenkin 1957; Zweers et al. 1995). Flamingos possess spine-like soft projections along the maxillary tomia that exclude large particles during inflow, and palatal and mandibular lamellae that retain food particles upon outflow. The final mesh size is fine-tuned by the degree of bill opening, and two rows of lingual projections aid transport of food particles to the throat (Zweers et al. 1995; Mascitti and Kravetz 2002). 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 most elaborate tongues and internal bill structures in birds. Inflow and outflow are driven by 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 lamellae covering the maxillary and mandibular internal lateral margins. Food moves through the maxillary lamellae and longitudinal grooves, and, upon tongue retraction, lingual soft brush-like projections sweep the particles backwards (Zweers et al. 1977). Selection of food particle size is achieved by modifying the maxillary and mandibular lamellar distance (i.e., by regulating gape size; Dubbeldam 1984), and by controlling the 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 down into the water column. Recurvirostrids, such as stilts, for example, perform visual underwater pecking and nonvisual scything (Pierce 1985). Scything is a tactile method performed by recurvirostrids and some Tringa spp. waders that disturbs the water and underlying substrate, during which prey are detected by the sensitive bill tips. Upon capture, a combination of surface tension and inertial and lingual transport 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 and incline their heads upwards until their recurved bill tips are horizontal near the substrate, and sweep their slightly opened bills toward the leading foot, usually swinging only 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 spoonbills the behavior is less stereotyped than in avocets, and the arc length and distance from 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 669 the substrate are more variable. Furthermore, sweeps are not coordinated with steps in spoonbills, several arcs are completed before lifting the head, and the intraoral transport mechanism is entirely inertial (Weihs and Katzir 1994; Swennen and Yu 2005, 2008). The broadened and sensitive tips of the characteristic spoon-shaped bill are thought to improve detection and prey trapping (Swennen and Yu 2004). Furthermore, ﬂattening minimizes drag and turbulence during sweeping (Swennen and Yu 2004, 2008; but see Weihs and Katzir 2008). Finally, the spatulate tips act as hydrofoils that create vortices that lift small prey off the bottom (Weihs and Katzir 1994, 2008).

17.3.3.4 Surface Fishers

For reasons that may include social and energetic benefits, organisms such as fish may aggregate near the surface of water. This provides excellent opportunity for avian predation and examples of ecosystem energy transfer, but may impose special challenges due to refraction and reflection of light (see Casperson 1999). There is a relatively large body of literature associated with these predator–prey interactions (see Pitcher et al. 1988, or Gotceitas and Godin 1993 and their references for examples). We define surface fishing as a bird taking prey items just at or slightly below the surface of a body of water. Surface fishing is further classified according to the mode of capture. First, birds such as darters or herons spear or stab fish with their bills (see Recher and Recher 1968). This behavior is coupled to a relatively long spear-like bill, quick flexion of a streamlined head and neck (Owre 1967), and panoramic 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). Many species [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 curved claws (Fowler et al. 2009) and possibly modified scales (e.g., those of osprey) which are excellent for grasping slippery fish. Another strategy of surface fishing is that of “tactile fishing”. Rather than being dependent on sight for prey detection, birds may 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 categorized by their primary modes of accessing prey from the air above the water, or from the surface of the water. They include “plunge divers” (e.g., pelicans, tropicbirds, boobies and gannets), who dive from the air, “foot-propelled divers” (e.g., loons, grebes, cormorants, and mergansers) who dive from the surface, and “wing-propelled divers”, who hunt beneath the water surface (e.g., penguins) and air (auks, puffins, murres, 670 A. Rico-Guevara et al. 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 of raptors, these categories can be quite fluid, and some species adopt different strategies depending on the circumstances: Australasian gannets plunge dive for subsurface fish, but “pursuit dive” to reach deeper fish on the move (Machovsky Capuska et al. 2011). Furthermore, these groupings do not necessarily reflect ecological adaptations. For example, an Antarctic procellariform community described by Moreno et al. (2017) consists of four heterospecific assemblages or “guilds”, distinguished by their focus on crustaceans, small or large fish and squid, or carrion. Although most seabirds have serrated or hooked beaks to maintain purchase of slippery prey, there are other morphological differences among taxa that are thought to provide a basis for partitioning of resources in the pelagic environment (Ashmole 1971). Differences in wing shape are associated with differences in flight (Brewer and Hertel 2007) and foraging (Hertel and Ballance 1999) behavior among taxa. Seabirds tend to be opportunistic, but the patchy distribution of resources of the pelagic environment selects for a variety of more or less specialized foraging tactics, such as foraging nocturnally, in flocks, along fronts, associating with other marine predators (e.g., dolphins), or simply patrolling large ocean 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 fluid through the beak (beak transport) and through the pharynx (pharyngeal transport). The first phase of drinking is achieved in two distinct ways. Birds either keep their bills immersed in the water or make a scooping motion with their head. Intrapharyngeal transport is either achieved by laryngeal motion or by using gravity (Zweers 1992). Pigeons were the first bird species observed by fluoroscopy as they drank (Zweers 1982) and are the only bird species in which muscle activity has been recorded during drinking (Bermejo et al. 1992; Bout and Zeigler 1994). Pigeons use cyclical motion of the tongue and beak to generate suction for beak transport followed by cyclical motion of the larynx to generate suction for pharyngeal transport; during both phases the beak remains immersed in water with the head tipped down (Zweers 1982). Drinking in estrildid finches resembles that in pigeons, with the tongue and beak driving beak transport, the larynx driving pharyngeal transport, and no tipping up of the head (Fisher et al. 1972; Heidweiller and Zweers 1990). Fluid transport in finches is achieved by “scooping” (Heidweiller and Zweers 1990) of the tongue and larynx, rather than suction. Suction or scooping by the tongue and larynx may be common among several bird orders: drinking without tipping up of the head has been observed in parakeets (Fisher et al. 1972), tanagers, sparrows (Moermond 1983), and mousebirds (Cade and Greenwald 1966). Mallards (Kooloos and Zweers 1989) and chickens (Heidweiller et al. 1992)also use suction to drink, driven by motion of the beak, tongue, and (in chickens) the 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 671 larynx. For pharyngeal transport, both species tip up the head so that gravity and cyclical motion of the larynx direct water into the oesophagus. Tongue scooping or suction followed by gravity-based pharyngeal transport is also been observed in sandgrouse (Cade et al. 1966). For drinking, rheas use “beak scooping” followed by gravity-based flow for pharyngeal transport (Gussekloo and Bout 2005). Beak scooping may also be used for drinking in several families of songbirds, including manakins, flycatchers, thrushes, and grosbeaks (Moermond 1983). A pecking action for 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 water is limited (Gussekloo and Bout 2005). For beak transport of nectar, hummingbirds use their tongue tips as a fluid traps (Rico-Guevara and Rubega 2011), the base of the 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 behavior of beak transport is likely used for drinking water (Fisher et al. 1972)butthe pharyngeal transport mechanism remains unclear (Rico-Guevara 2014). There is much we do not know about how birds drink and why birds have evolved different drinking strategies. Capillary action has been proposed to play some role in 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). This hypothesis requires scrutiny using more sophisticated techniques (e.g., Rico-Guevara et al. 2015). Similarly, the relative contributions of scooping versus suction during drinking in many birds remain unclear. New imaging and simulation techniques will clarify the relative contributions of these different mechanisms and maybe even reveal additional mechanisms of fluid capture by birds (Prakash et al. 2008). Addi- tionally, the independent evolution of the same drinking behaviors in birds, the dual functionality of the beak and tongue in feeding and drinking, and the relationship between a bird’s diet and how frequently it needs to drink (Bartholomew and Cade 1963) all point to a strong evolutionary association between drinking and feeding. Yet, we still do not understand the trade-offs and mutual compatibilities between these behaviors. New observations of drinking in previously unstudied clades will likely 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 (BirdLife International 2015). Closely related species may have strikingly disparate bills, and indeed Darwin’s finches (Grant and Grant 1993), Hawaiian honeycreepers (Lovette et 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 672 A. Rico-Guevara et al. to be driven by rapid morphological evolution in response to ecological opportunity (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 often associated with islands, where the opportunity to invade new niches should encour- age rapid morphological evolution. High rates also occurred on branches leading up to early radiating families with unusual bill morphologies (e.g., hummingbirds, anseriforms), suggesting that adaptations to unlock novel feeding strategies facilitate the evolution of disparate phenotypes. One must take care to note that high rates of morphological evolution do not necessarily imply high rates of speciation, and vice versa: many explosive radiations of birds are not associated with high bill disparity (e.g., white-eyes; Moyle et al. 2009). In these instances, high speciation rates may be driven instead by other functional traits, sexual selection, geographic factors, 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 evolution and a number of hypothesized evolutionary drivers (e.g., range size, occupation of islands, environmental mutagens, and other factors) in 5,551 avian species, 80% of the variation in species-specific rates could not be explained. Thus it may be that many of the ‘classic’ adaptive radiations in birds are actually quite exceptional. Genetic studies have determined that the major 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, allometric, and phylogenetically conserved patterns that imply developmental constraints on bill and skull shape (Bhullar et al. 2012; Bright et al. 2016; Cooney et al. 2017). For many birds, the bill represents a compromise between development and an array of functions. In order to untangle these different signals, we need well-defined hypotheses and methods that quantify both form and function. A range of tools is now available for investigating beak evolution. Morphology has traditionally been quantified with linear measurements, but the emergence of landmark-based geometric morphometrics methods (Zelditch et al. 2012; Adams et al. 2013) allows much more detailed analyses to take place. In birds, in which the structures of interest can be elaborate and highly curved and thus missed by linear metrics, this is a useful tool. Briefly, geometric morphometrics requires placement of homologous “landmarks” on every specimen, which are then aligned to remove the differences in specimen scale, position, and rotation (that is, all the geometric data that are not related to shape) using Generalized Procrustes Analysis. The Procrustes aligned coordinates may then be used to describe the nature of shape variation in the sample. A typical first step is a principal component (PC) analysis to determine the major axes of morphological variation, and to generate visualization aids, such as thin-plate spline warps and morphospace plots of the PC scores (Klingenberg 2013;Fig.17.9). In birds, geometric morphometrics data has been used to look at differences associated with biogeography (Foster et al. 2008), and diet or feeding behavior (e.g., Si et al. 2015; Bright et al. 2016;Olsen2017), and regression of shape on 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 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 673

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 and craniofacial integration in several families of birds, with larger bird species tending to occupy positive values on PC1. Figure reproduced from Bright et al. (2016) they often describe a relative lengthening of the rostrum with increasing size, and are often associated with strong signals of integration between the bill and the rest of the 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). If selection aligns with an allometric trajectory, then allometry underpinned by integration may represent an evolutionary line of least resistance that allows birds to diversify relatively quickly (see theoretical models of Marroig et al. 2009; Villmoare 2013; Goswami et al. 2014). One may also test for any phylogenetic similarities underlying the shape data (Klingenberg and Marugán-Lobón 2013; Bright et al. 2016; Cooney et al. 2017), or investigate rates of phenotypic evolution (Cooney et al. 2017;Chira et al. 2018).

17.5.1.2 Convergences and Parallelisms in Avian Feeding Behaviors and Structures

Convergent morphologies and feeding mechanics among phylogenetically distant groups of birds have always attracted the attention of biologists. These outcomes are most striking in the context of intercontinental and hemispheric comparisons; the similarly shaped beaks and convergent transport mechanics of the frugivorous New World toucans and the Old World hornbills, for example, presumably reflect common functional demands for reaching, manipulating, and consuming fruits (Baus- sart et al. 2009; Baussart and Bels 2011). Additional and non-mutually exclusive selective pressures on beak morphology can include use in inter- and intrasexual selection, visual displays to heterospecifics, and use in thermoregulation. Functional convergence in specialized hunting behavior is similarly impressive, as characterizes 674 A. Rico-Guevara et al. ballistic plunge-diving in gannets, tropicbirds, terns, and many kingfishers. Feeding on carrion and carcasses has elicited morphological convergence in vulture morphologies worldwide (Hertel 1994, 1995). Granivory by sandgrouse and seedsnipes, ground-litter insectivory by monias and thrashers, and the aerial insectivory of swifts and swallows further exemplify the evolution of anatomical and functional similarities driven by comparable diets. Nectarivory represents a powerful example of convergence in the feeding apparatus, given the mutualistic coevolution with nectar-bearing flowers that has elicited comparable beak and lingual morphologies among avian clades from different conti- nents and island groups (i.e., the New World hummingbirds, the Old World sunbirds and their allies, the Australo-pacific honeyeaters, and many of the Hawaiian drepani- ids, cf. Paton and Collins 1989). Because feeding from floral corollae requires specific actions of lapping and pumping of sugar-rich viscous solutions, bill and tongue morphology are strongly influenced by the biomechanics of nectar extraction (Rico- Guevara and Rubega 2011; Rico-Guevara et al. 2015). Bill length and curvature are potentially variable according to specialization on particular flowers or plant groups, but dedicated nectar-feeders are easily recognized worldwide. Partial or opportunistic nectarivory also characterizes many bird groups (e.g., many orioles and tanagers, including the New World honeycreepers). Most nectarivores perch on vegetative structures while feeding, and only hummingbirds have evolved the capacity for sustained hovering during nectar extraction. By contrast, diets may converge among different avian taxa but the specific morphological and behavioral adaptations for feeding remain distinct. Piscivory, for example, characterizes plunge-divers, surface-scavenging eagles, and foot-propelled surface divers such as grebes, loons, and cormorants, but is carried out by these groups using very different locomotor behaviors and mechanisms of capture. Granivory is a widespread feeding mode but involves a diversity of methods of seed acquisition and processing according to taxon and ecological context (e.g., crossbills versus dabbling ducks). Similarly, frugivory is widespread among many taxa and involves feeding from a large taxonomic range of fruits, varying most prominently in size. Sequen- tial ingestion of many small fruits, for example, differs mechanically from repeated pecking at the pulp of larger fruits. In part, broad-brush dietary categorizations such as frugivory may simply reflect linguistic ambiguity about the mechanics of feeding, and a more finely resolved description of the actual process will be necessary to quantify patterns of convergence.

17.5.1.3 Convergent Behaviors with Differing Morphologies

There are several examples of birds having evolved convergent feeding behaviors with both convergent and divergent feeding morphologies. Filter feeding has evolved 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 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 675 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): in ratites (Milton et al. 1994; Wood et al. 2008), landfowl (Sedinger 1997), at least seven times in waterfowl (Olsen 2015), in hoatzins (Grajal et al. 1989), in Gruiformes (Mills and Mark 1977), in Psittaciformes (Trewick 1996), and in Passeriformes (Munson and Robinson 1992; Bucher et al. 2003). Beak shapes among herbivorous birds take many different forms and thus there is no single beak shape critical for cropping behavior. Underwater pursuit diving has also evolved many times; in diving petrels, loons, grebes, cormorants (Grémillet et al. 2006), penguins (Cannell and Cullen 1998), alcids (Sanford and Harris 1967), and mergansers. Most underwater pursuit divers have relatively narrow and elongate beaks but the presence of a “hook” or downward curvature at the end of the beak is present in some lineages (e.g., diving petrels, cormorants, mergansers) and absent in others (e.g., grebes, loons, alcids).

17.5.2 Evolutionary Processes in Bird Feeding: Natural Selection’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. For instance, nectarivorous hummingbirds also feed on a variety of arthropods (reviews in Stiles 1995; Yanega 2007; Rico-Guevara 2008), sap and other plant fluids, even fruits (reviews in Kevan and Baker 1983; Estades 2003; Ruschi 2014). In addition to meeting their primary energetic demands through the carbohydrates of floral nectar, hummingbirds are also highly specialized arthropod hunters, often catching small flying 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). Use of 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 not opposing forces of selection may act on anatomical and biomechanical features of these two feeding modes. In general, recognition of diverse functional roles for the same structure can force a more quantitative description of their varied uses as well as frequencies of occurrence, as opposed to a simplified and qualitative semantic characterization of diet. 676 A. Rico-Guevara et al.

17.5.2.2 Feeding Trade-Offs

Given the variety of food items that birds consume and their dietary flexibility, it is common to find morphological and functional constraints, as well as trade-offs between 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 biophysical challenges are dissimilar. For instance, different species of Flowerpiercers (Diglossa spp. and Diglossopis spp.) exhibit bill hooks of various lengths which are correlated with the efficiency of feeding on fruit versus nectar (Schondube and Martinez del Rio 2003). Experiments modifying the hook length showed that birds with small hooks feed more efficiently on fruit, but were less efficient at robbing nectar; the opposite was true for birds with intact bills presenting long hooks (Schondube and Martinez del Rio 2003). Flowerpiercers use their maxillary hooks to hold the base of a flower and pierce it with their mandible, creating a hole through which they extract nectar with their tubular tongues. Below we provide two additional feeding trade-offs examples in waterfowl and finches. Waterfowl face at least two major trade-offs in feeding mechanics. The first is a predicted trade-off between prey size selection and water filtration rate during filter feeding, 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;Van der Leeuw et al. 2003). Waterfowl with more duck-like beaks (e.g., mallard) show relatively high filtering performance and relatively low grazing performance whereas those with more goose-like beaks [e.g., white-fronted goose (Anser albifrons)] show higher grazing performance and lower filtering performance. Yet, waterfowl with intermediate beak shapes [e.g., Eurasian wigeon (Mareca penelope)] appear not to experience a deficit in either filtering or grazing performance (Van der Leeuw et al. 2003). Some birds can close their jaws with more force than other birds. A classic example of this variation can be measured in Geospiza Finches (Herrel et al. 2009) where bite forces in G. magnirostris are around 10–15X that of its congeners. In birds with higher bite forces, the coronoid process and associated ramus (insertion surfaces for adductor musculature) on the mandible may be relatively robust and close to the anterior tip of the bill. On the other hand, velocity of closing may be a beneficial trait, particularly in those birds catching aerial prey items (e.g., flycatchers). High bill tip closing speeds can be achieved either by lengthening the bill or moving adductor attachment sites closer to the jaw joint (Corbin et al. 2015). Although predicted by a number of kinematic and muscle biology studies (see Lorenz and Campello 2012), the interplay between optimizing closing force or closing velocity or some other aspect of feeding performance (i.e., seed husking time; see van der Meij and Bout 2006;sit and wait versus wide foraging, see McBrayer and Corbin 2007), probably is not a simple trade-off. Changes in overall body or head size, possibly an evolutionary line of least resistance (Marroig et al. 2005), may accomplish the same goal as modifying the in-lever to out-lever ratio (Corbin et al. 2015). 17 Feeding in Birds: Thriving in Terrestrial, Aquatic … 677

17.5.2.3 Additional Selective Pressures Acting on the Feeding Apparatus

Avian bills can be used in a variety of non-feeding roles that may select for additional features of anatomical and physiological design of the feeding apparatus. Widespread use 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 in thermoregulation (Tattersall et al. 2009). Maxillary overhang has been demonstrated experimentally to enhance ectoparasite removal by pigeons (Clayton et al. 2005), whereas overly long bills may impair the ability to autogroom (Clayton and Cotgreave 1994). Bite forces and torques, as influenced by both size and shape of the beak, can influence its use in hetero- and conspecific interactions (Herrel et al. 2009). Of this latter class of behaviors, the forces of sexual selection may be particularly powerful relative to diverse features of beak size and shape. The spectral composition of avian vocalizations can be influenced by beak morphology, and in turn influence speciation dynamics (e.g., Podos and Nowicki 2004). Bills can also serve as visual signals in territorial and mating displays. They can be used as tools of combat, as suggested anatomically when sexually dimorphic (e.g., Babbitt and Frederick 2007), and in some cases documented behaviorally. One species of hermit hummingbirds possesses a dagger-like modification to the bill tip, which is sexually dimorphic, that serves as a weapon during inter-male aerial combat (Rico-Guevara and Araya-Salas 2015). Overall, diverse and sometimes conflicting forces of both natural and sexual selection serve to mold avian bill anatomy, feeding behavior, and functional capacity. This conclusion will come as no surprise to any field biologist who routinely observes birds in the wild, but focal experimental studies on particular feeding modes may not encompass alternative interpretations for any particular morphological feature. Given the range of food items consumed by any given bird species, the underlying and often variable biomechanics necessary to capture and process such items, and the presence of supplemental selective forces, many more interesting and unexpected aspects of avian feeding behavior are likely to be described in the future.

17.6 Conclusion

Although our understanding of the avian feeding system has improved dramatically over recent years, there are many questions to ask. For instance, how does performance vary along particular axes of bill shape evolution? How does this correspond with competing selection pressures? How is performance modiﬁed by peculiar family-speciﬁc novelties like casques or de novo muscles? And to what extent does the wide range of naso-frontal hinge and palate morphologies modify kinesis and stress patterns? This last question opens up numerous opportunities for further work with contrast-enhanced computed tomography scanning (Lautenschlager et al. 2014; Gignac et al. 2016), muscle modeling techniques such as Multibody Dynamics Anal- 678 A. Rico-Guevara et al. 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 detailed ecological (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 for studying not just functional morphology, but how it operates within a macroevolutionary framework, are enormous.

Acknowledgements We are grateful to Margaret Rubega and Gregor Yanega, who have profoundly shaped 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 ﬁnal stages of editing.

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