The evolutionary relationship among beak shape,mechanical advantage,and feeding ecology in modern birds*

Extensive research on avian adaptive radiations has led to a presumption that beak morphology predicts feeding ecology in birds. However, this ecomorphological relationship has only been quantified in a handful of avian lineages, where associations are of variable strength, and never at a broad macroevolutionary scale. Here, we used shape analysis and phylogenetic comparative methods to quantify the relationships among beak shape, mechanical advantage, and two measures of feeding ecology (feeding behavior and semiquantitative dietary preferences) in a broad sample of modern birds, comprising most living orders. We found a complex relationship, with most variables showing a significant relationship with feeding ecology but little explanatory power. For example, diet accounts for less than 12% of beak shape variation. Similar beak shapes are associated with disparate dietary regimes, even when accounting for diet‐feeding behavior relationships and phylogeny. Very few lineages optimize for stronger bite forces, with most birds exhibiting relatively fast, weak bites, even in large predatory taxa. The extreme morphological and behavioral flexibility of the beak in birds suggests that, far from being an exemplary feeding adaptation, avian beak diversification may have been largely contingent on trade‐offs and constraints.     

Gulps, wheezes, and sniffs: how measurement of beak movement in sea turtles can elucidate their behaviour and ecology

This study was performed to assess the extent to which an intermandibular angle sensor (IMASEN) may be used to elucidate the behaviour of six captive loggerhead turtles. The measuring system was glued to the beak of turtles and set to measure the intermandibular distance at 5 Hz while the turtles fed (on anchovies, squid, and live crabs), swam, rested, and breathed. The behaviour of the equipped turtles was filmed and compared afterwards to the sensor readings. The IMASEN output data allowed quantification of the number of food items ingested as well as the time between food seizure and deglutition and the type of food ingested. However, nonfeeding turtles exhibited regular jaw movements with a reduced amplitude of ca. 2.2 mm, which clearly differed from feeding movements and were caused by buccal oscillations. Such movements of the base of the buccal cavity generate a steady flow of water pass the chemosensory organs and were interrupted only during food ingestion, resting, and breathing. Breathing was clearly distinguishable by the IMASEN. The beak sensor is thus a reliable system to investigate a number of behaviours in sea turtles which encompass foraging, buccal oscillation, and respiratory frequency. It has potential for allocating time to different activities in free-ranging sea turtles and thus allows us to gain insight to their foraging and diving strategies.     

The magnetite-based receptors in the beak of birds and their role in avian navigation

Iron-rich structures have been described in the beak of homing pigeons, chickens and several species of migratory birds and interpreted as magnetoreceptors. Here, we will briefly review findings associated with these receptors that throw light on their nature, their function and their role in avian navigation. Electrophysiological recordings from the ophthalmic nerve, behavioral studies and a ZENK-study indicate that the trigeminal system, the nerves innervating the beak, mediate information on magnetic changes, with the electrophysiological study suggesting that these are changes in intensity. Behavioral studies support the involvement of magnetite and the trigeminal system in magnetoreception, but clearly show that the inclination compass normally used by birds represents a separate system. However, if this compass is disrupted by certain light conditions, migrating birds show ‘fixed direction’ responses to the magnetic field, which originate in the receptors in the beak. Together, these findings point out that there are magnetite-based magnetoreceptors located in the upper beak close to the skin. Their natural function appears to be recording magnetic intensity and thus providing one component of the multi-factorial ‘navigational map’ of birds.     

Review: Automated techniques for monitoring the behaviour and welfare of broilers and laying hens: towards the goal of precision livestock farming

There is increasing public concern about poultry welfare; the quality of animal welfare is closely related to the quality of livestock products and the health of consumers. Good animal welfare promotes the healthy growth of poultry, which can reduce the disease rate and improve the production quality and capacity. As behaviour responses are an important expression of welfare, the study of behaviour is a simple and non-invasive method to assess animal welfare. The use of modern technology offers the possibility to monitor the behaviour of broilers and laying hens in a continuous and automated way. This paper reviews the latest technologies used for monitoring the behaviour of broilers and laying hens under both experimental conditions and commercial applications and discusses the potential of developing a precision livestock farming (PLF) system. The techniques that are presented and discussed include sound analysis, which can be an online tool to automatically monitor poultry behaviour non-invasively at the group level; wireless, wearable sensors with radio-frequency identification devices, which can automatically identify individual chickens, track the location and movement of individuals in real time and quantify some behavioural traits accordingly and image processing technology, which can be considered a direct tool for measuring behaviours, especially activity behaviours and disease early warning. All of these technologies can monitor and analyse poultry behaviour, at the group level or individual level, on commercial farms. However, the popularity and adoption of these technologies has been hampered by the logistics of applying them to thousands and tens of thousands of birds on commercial farms. This review discusses the advantages and disadvantages of these techniques in commercial applications and presents evidence that they provide potential tools to automatically monitor the behaviours of broilers and laying hens on commercial farms. However, there still has a long way to go to develop a PLF system to detect and predict abnormal situations.     

Tied hands: synchronism between beak development and feeding-related morphological changes in ommastrephid squid paralarvae

Ommastrephid squid produce some of the smallest cephalopod hatchlings, whose feeding behavior has not been observed. The present study aimed at indirectly filling this knowledge gap by describing ontogenetic changes in beak morphology and morphometry and integrating these results with published datasets on Illex argentinus arm crown morphology and gut contents. Individuals [0.7–15 mm mantle length (ML)] were measured, weighed, and had their buccal mass extracted. Jaw measurements were correlated with ML to determine whether jaw development occurred linearly with ML. For a 10 mm increment in ML, weight increased 430-fold. The jaws of hatchlings were rudimentary, but in larger paralarvae the rostrum protrudes and the jaw features (teeth, slit, groove) disappear. Increases in ML were predicted by beak robustness indices and rostrum protrusion, with growth discontinuities pointing to faster growth in individuals ≤ 2 mm ML. Morphological changes in the beak and arm crown are in synchrony with a transitional event in the feeding ecology of paralarvae: the onset of active predation on crustaceans and masticating their exoskeletons for ingestion. Integration of the results with published data has led to the proposal of a hypothesis of four size-differentiated developmental stages in the feeding ecology of I. argentinus rhynchoteuthions.

     

A geometric morphometric appraisal of beak shape in Darwin's finches

Beak size and shape in Darwin's finches have traditionally been quantified using a few univariate measurements (length, depth, width). Here we show the improved inferential resolution of geometric morphometric methods, as applied to three hierarchical levels: (i) among seven species on Santa Cruz Island, (ii) among different sites on Santa Cruz for a single species (Geospiza fortis), and (iii) between large and small beak size morphs of G. fortis at one site (El Garrapatero). Our results support previous studies in finding an axis of shape variation (long/shallow/pointy vs. short/deep/blunt) that separates many of the species. We also detect additional differences among species in the relative sizes and positions of the upper and lower mandibles and in curvature of the mandibles. Small-scale, but potentially relevant, shape variation was also detected among G. fortis from different sites and between sympatric beak size morphs. These results suggest that adaptation to different resources might contribute to diversification on a single island.     

Smaller beaks for colder winters: Thermoregulation drives beak size evolution in Australasian songbirds

Birds’ beaks play a key role in foraging, and most research on their size and shape has focused on this function. Recent findings suggest that beaks may also be important for thermoregulation, and this may drive morphological evolution as predicted by Allen's rule. However, the role of thermoregulation in the evolution of beak size across species remains largely unexplored. In particular, it remains unclear whether the need for retaining heat in the winter or dissipating heat in the summer plays the greater role in selection for beak size. Comparative studies are needed to evaluate the relative importance of these functions in beak size evolution. We addressed this question in a clade of birds exhibiting wide variation in their climatic niche: the Australasian honeyeaters and allies (Meliphagoidea). Across 158 species, we compared species’ climatic conditions extracted from their ranges to beak size measurements in a combined spatial‐phylogenetic framework. We found that winter minimum temperature was positively correlated with beak size, while summer maximum temperature was not. This suggests that while diet and foraging behavior may drive evolutionary changes in beak shape, changes in beak size can also be explained by the beak's role in thermoregulation, and winter heat retention in particular.     

QTL and quantitative genetic analysis of beak morphology reveals patterns of standing genetic variation in an Estrildid finch

The intra- and interspecific diversity of avian beak morphologies is one of the most compelling examples for the power of natural selection acting on a morphological trait. The development and diversification of the beak have also become a textbook example for evolutionary developmental biology, and variation in expression levels of several genes is known to causally affect beak shape. However, until now, no genomic polymorphisms have been identified, which are related to beak morphology in birds. QTL mapping does reveal the location of causal polymorphisms, albeit with poor spatial resolution. Here, we estimate heritability and genetic correlations for beak length, depth and width and perform a QTL linkage analysis for these traits based on 1404 informative single-nucleotide polymorphisms genotyped in a four-generation pedigree of 992 captive zebra finches (Taeniopygia guttata). Beak size, relative to body size, was sexually dimorphic (larger in males). Heritability estimates ranged from 0.47 for beak length to 0.74 for beak width. QTL mapping revealed four to five regions of significant or suggestive genome-wide linkage for each of the three beak dimensions (nine different regions in total). Eight out of 11 genes known to influence beak morphology are located in these nine peak regions. Five QTL do not cover known candidates demonstrating that yet unknown genes or regulatory elements may influence beak morphology in the zebra finch.     

How does the curvature of the upper beak bone reflect the overlying rhinotheca morphology?

The beak has independently been evolved accompanied by the edentulism in many tetrapod linages, including extant Testudinata and Aves, and its form and function have been greatly diversified. The beak is formed by beak bones and the overlying keratinous cover, although their profiles are different from each other. Therefore, it is difficult to reliably reconstruct the entire profile of the beak in extinct taxa, whose keratinous tissues are rarely preserved. For elucidation of the morphological relationship between beak bone and overlying keratinous cover, we compared the curvature distribution of the culminal profiles of the upper beak bone and the overlying keratinous cover (rhinotheca) with each other using CT‐scan, in 66 extant testudinatan and avian specimens (Aves: 33 genera, 24 families; Testudinata: 12 genera seven families). In both, rhinotheca and beak bone, the curvature of the profile was nearly constant rostral to a certain point, which was defined as the transition point, and the transition points of the rhinotheca and beak bone were close to each other. The profiles of the rhinotheca and beak bone rostral to their transition point were different in curvature and length. However, the ratio between the curvatures of rhinotheca and the beak bone strongly correlated with the arc angle of the rostral culminal profiles of the beak bone. The upper beak profile in extinct taxa is expected to be reconstructed more reliably using the abovementioned relationship between the beak bone and the rhinotheca.     

Region-specific expression of scutate scale type beta keratins in the developing chick beak.

This study shows that different patterns of scutate scale type beta keratins are accumulated in the three adjacent structures of the embryonic chick beak: periderm, egg tooth, and cornified beak. The cornified beak accumulates all of the beta keratins of scutate scale except pp2,3. The periderm, which is the outermost, multilayered covering of the whole embryonic beak, accumulates only beta keratins 2,3, and p2,3 of the scutate scale pattern. The egg tooth, which is the rounded elevation on the dorsal surface of the upper beak, and the embryonic claw accumulate greatly reduced levels of 2,3 and p2,3 compared to scutate scale. Like cornified beak, the claw does not accumulate pp2,3, but both tissues express a potentially new beta keratin, beta keratin 8. Neither the histidine rich "fast" proteins (HRPs), which are expressed in embryonic scutate scales and feathers, nor the avian cytokeratin associated proteins (cap-1 and cap-2), which are expressed in scutate and reticulate scales, are expressed in any of the embryonic beak structures or in the claw. The implications of these findings with regard to regulation of terminal differentiation of avian skin are discussed.     

Elastic instability model of rapid beak closure in hummingbirds

The hummingbird beak, specialized for feeding on floral nectars, is also uniquely adapted to eating flying insects. During insect capture the beak often appears to close at a rate that cannot be explained by direct muscular action alone. Here we show that the lower jaw of hummingbirds has a shape and compliance that allows for a controlled elastic snap. Furthermore, hummingbirds have the musculature needed to independently bend and twist the sides of the lower jaw. According to both our simple physical model and our elastic instability calculation, the jaw can be smoothly opened and then snapped closed through an appropriate sequence of bending and twisting actions by the muscles of the lower jaw.     

From snout to beak: the loss of teeth in birds

All living birds are toothless, constituting by far the most diverse toothless vertebrate clade, and are striking examples of evolutionary success following tooth loss. In recent years, an unprecedented number of Mesozoic birds have been described, illustrating the evolution of dentition reductions. Simultaneously, major advances in experimental embryology have yielded new results concerning avian edentulism. Reviewing these lines of evidence, we propose hypotheses for its causes, with a prominent role for the horny beak during development. A horny beak and a muscular gizzard functionally 'replaced' dentition for food acquisition and processing, respectively. Together with edentulism itself, these features and others contributed to the later success of birds, as a result of their high performance or additional functionality working in concert in these complex organisms.     

Ultraviolet reflecting photonic microstructures in the King Penguin beak

King and emperor penguins (Aptenodytes patagonicus and Aptenodytes forsteri) are the only species of marine birds so far known to reflect ultraviolet (UV) light from their beaks. Unlike humans, most birds perceive UV light and several species communicate using the near UV spectrum. Indeed, UV reflectance in addition to the colour of songbird feathers has been recognized as an important signal when choosing a mate. The king penguin is endowed with several highly coloured ornaments, notably its beak horn and breast and auricular plumage, but only its beak reflects UV, a property considered to influence its sexual attraction. Because no avian UV-reflecting pigments have yet been identified, the origin of such reflections is probably structural. In an attempt to identify the structures that give rise to UV reflectance, we combined reflectance spectrophotometry and morphological analysis by both light and electron microscopy, after experimental removal of surface layers of the beak horn. Here, we characterize for the first time a multilayer reflector photonic microstructure that produces the UV reflections in the king penguin beak.     

Dive and beak movement patterns in leatherback turtles Dermochelys coriacea during internesting intervals in French Guiana

1. Investigating the foraging patterns of free-ranging species is essential to estimate energy/time budgets for assessing their real reproductive strategy. Leatherback turtles Dermochelys coriacea (Vandelli 1761), commonly considered as capital breeders, have been reported recently to prospect actively during the breeding season in French Guiana, Atlantic Ocean. In this study we investigate the possibility of this active behaviour being associated with foraging, by studying concurrently diving and beak movement patterns in gravid females equipped with IMASEN (Inter-MAndibular Angle SENsor). 2. Four turtles provided data for periods varying from 7.3 to 56.1 h while exhibiting continuous short and shallow benthic dives. Beak movement ('b-m') events occurred in 34% of the dives, on average 1.8 +/- 1.4 times per dive. These b-m events lasted between 1.5 and 20 s and occurred as isolated or grouped (two to five consecutive beak movements) events in 96.0 +/- 4.0% of the recorded cases, and to a lesser extent in series (> five consecutive beak movements). 3. Most b-m events occurred during wiggles at the bottom of U- and W-shaped dives and at the beginning and end of the bottom phase of the dives. W-shaped dives were associated most frequently with beak movements (65% of such dives) and in particular with grouped beak movements. 4. Previous studies proposed wiggles to be indicator of predatory activity, U- and W-shaped dives being putative foraging dives. Beak movements recorded in leatherbacks during the first hours of their internesting interval in French Guiana may be related to feeding attempts. 5. In French Guiana, leatherbacks show different mouth-opening patterns for different dive patterns, suggesting that they forage opportunistically on occasional prey, with up to 17% of the dives appearing to be successful feeding dives. 6. This study highlights the contrasted strategies adopted by gravid leatherbacks nesting on the Pacific coasts of Costa Rica, in the deep-water Caribbean Sea and in the French Guianan shallow continental shelf, and may be related to different local prey accessibility among sites. Our results may help to explain recently reported site-specific individual body size and population dynamics.     

Pain issues in poultry

This review highlights the possible pain experienced by layer and broiler poultry in modern husbandry conditions. Receptors which respond to noxous stimulation (nociceptors) have been identified and physiologically characterised in many different part of the body of the chicken including the beak, mouth, nose, joint capsule and scaly skin. Stimulation of these nociceptors produces cardiovascular and behavioural changes consistent with those seen in mammals and are indicative of pain perception. Physiological and behavioural experiments have identified the problem of acute pain following beak trimming in chicks, shackling, and feather pecking and environmental pollution. Chronic pain is a much greater welfare problem because it can last for long periods of time from weeks to months. Evidence for possible chronic pain is presented from a variety of different conditions including beak trimming in older birds, orthopaedic disease in broiler and bone breakage in laying hens. Experiments on pain in the chicken have not only identified acute and chronically painful conditions but also have provided information on qualitative differences in the pain experienced as well as identifying a cognitive component providing evidence of conscious pain perception.     

Mate-guarding in a promiscuous insect: species discrimination influences context-dependent behaviour

Mating strategy is often informed by social context. However, information on social environment may be sensitive to interference by nearby heterospecifics, a process known as reproductive interference (RI). When heterospecific individuals are present in the environment, failures in species discrimination can lead to sub-optimal mating behaviours, such as misplaced courtship, misplaced rivalry behaviours, or heterospecific copulation attempts. All aspects of mating behaviour that are influenced by social context may be prone to RI, including copulatory behaviours associated with mate-guarding in the presence of possible competitors. Here we investigate the effect of three heterospecifics on the mate-guarding behaviour of male Lygaeus equestris seed bugs. We find that, despite previously reported heterospecific mating harassment amongst these species of lygaeid bug, male L. equestris are able to effectively distinguish rival conspecific males from heterospecifics. Thus, heterospecific mating attempts in this group may reflect selection on males to mate opportunistically, rather than a failure of species discrimination.     

Influence of genetic architecture on contemporary local evolution in the soapberry bug,Jadera haematoloma: artificial selection on beak length

Little is known about the influence of genetic architecture on local adaptation. We investigated the genetic architecture of the rapid contemporary evolution of mouthparts, the flight polymorphism and life history traits in the soapberry bug Jadera haematoloma (Hemiptera) using laboratory selection. The mouthparts of these seed‐feeding bugs have adapted in 40–50 years by decreasing in length following novel natural selection induced by a host switch to the seeds of an introduced tree with smaller fruits than those of the native host vine. Laboratory selection on beak length in both an ancestral population feeding on the native host and a derived population feeding on the introduced host reveals genetic variance allowing a rapid response (heritabilities of 0.51–0.87) to selection for either longer or shorter beaks. This selection resulted in reverse evolution by restoring long beaks in the derived population and forward evolution by re‐creating short beaks in the ancestral bugs. There were strong genetic correlations (0.68–0.84) in both populations between beak lengths and the frequency of flight morphs, with short beaks associated with short wings. The results reveal a genetically interrelated set of adaptive multivariate traits including both beak length and flight morph. This suite of traits reflects host plant patchiness and seeding phenology. Weaker evidence suggests that egg mass and early egg production may be elements of the same suite. Reversible or forward evolution thus may occur in a broad set of genetically correlated multivariate traits undergoing rapid contemporary adaptation to altered local environments.     

The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution

The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak''s precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies—a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis—beak depth—was mirrored in the structure of beak''s additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution.     

Evidence of accelerated beak growth associated with avian keratin disorder in black-capped chickadees (Poecile atricapillus)

We recently documented an epizootic of beak deformities in more than 2,000 Blackcapped Chickadees (Poecile atricapillus) and other wild bird species in North America. This emerging avian disease, which has been termed avian keratin disorder, results in gross overgrowth of the rhamphotheca, the outer, keratinized layer of the beak. To test the hypothesis that the beak deformities characteristic of this disorder are associated with accelerated keratin production, we measured rates of beak growth and wear in affected Black-capped Chickadees (n=16) and a control sample of unaffected chickadees (n=14) collected from south-central (61°09'-61°38'N, 149°11' -149°48'W) and interior Alaska (64°51' -64°53'N, 147°49' -147°59'W). Rates of absolute growth were 50-100% higher in affected birds than they were in control birds and exceeded records from other passerine species. These results suggest that abnormally rapid epidermal growth is the primary physical mechanism by which beak deformities develop and are maintained in affected chickadees. Although beak overgrowth typically worsened over time, differential patterns of wear influenced the severity and morphology of deformities. In some cases, the effects of accelerated keratin growth were partially mitigated by frequent breakage of rhamphothecal tips. However, mortalities occurred in 9 of 16 birds (56%) with beak deformities during the study, suggesting that avian keratin disorder results in severe health consequences for affected birds. Additional study of factors that control beak keratin production is needed to understand the pathogenesis of this debilitating disease in wild birds.