Digest: Evolution of shape and leverage of bird beaks reflects feeding ecology,but not as strongly as expected*

Is feeding ecology the main driver of beak diversification in modern birds? Taking a broad‐scale interspecific comparative approach, Navalón et al. (2019) found a relationship between feeding ecology (diet and feeding behavior) and beak morphology (shape and leverage), although much of the observed variation remained unexplained. This low explanatory power may suggest that variation in the multitude of nonfeeding functions of the beak also influences its evolution.     

Is Beak Morphology in Darwin’s Finches Tuned to Loading Demands?

One of nature''s premier illustrations of adaptive evolution concerns the tight correspondence in birds between beak morphology and feeding behavior. In seed-crushing birds, beaks have been suggested to evolve at least in part to avoid fracture. Yet, we know little about mechanical relationships between beak shape, stress dissipation, and fracture avoidance. This study tests these relationships for Darwin''s finches, a clade of birds renowned for their diversity in beak form and function. We obtained anatomical data from micro-CT scans and dissections, which in turn informed the construction of finite element models of the bony beak and rhamphotheca. Our models offer two new insights. First, engineering safety factors are found to range between 1 and 2.5 under natural loading conditions, with the lowest safety factors being observed in species with the highest bite forces. Second, size-scaled finite element (FE) models reveal a correspondence between inferred beak loading profiles and observed feeding strategies (e.g. edge-crushing versus tip-biting), with safety factors decreasing for base-crushers biting at the beak tip. Additionally, we identify significant correlations between safety factors, keratin thickness at bite locations, and beak aspect ratio (depth versus length). These lines of evidence together suggest that beak shape indeed evolves to resist feeding forces.     

Messy eaters: Swabbing prey DNA from the exterior of inconspicuous predators when foraging cannot be observed

Complex coevolutionary relationships among competitors, predators, and prey have shaped taxa diversity, life history strategies, and even the avian migratory patterns we see today. Consequently, accurate documentation of prey selection is often critical for understanding these ecological and evolutionary processes. Conventional diet study methods lack the ability to document the diet of inconspicuous or difficult‐to‐study predators, such as those with large home ranges and those that move vast distances over short amounts of time, leaving gaps in our knowledge of trophic interactions in many systems. Migratory raptors represent one such group of predators where detailed diet studies have been logistically challenging. To address knowledge gaps in the foraging ecology of migrant raptors and provide a broadly applicable tool for the study of enigmatic predators, we developed a minimally invasive method to collect dietary information by swabbing beaks and talons of raptors to collect trace prey DNA. Using previously published COI primers, we were able to isolate and reference gene sequences in an open‐access barcode database to identify prey to species. This method creates a novel avenue to use trace molecular evidence to study prey selection of migrating raptors and will ultimately lead to a better understanding of raptor migration ecology. In addition, this technique has broad applicability and can be used with any wildlife species where even trace amounts of prey debris remain on the exterior of the predator after feeding.     

Historical contingency and animal diets: the origins of egg eating in snakes

Evolutionary changes in animal diets must often begin through the inclusion of a novel food type as a minor component of the diet. An aspect of this initial change that has rarely been studied is the relationship between the existing diet and the use of specific novel foods. We used comparative analyses to test the hypothesis that, in snakes, feeding on squamate (lizard and snake) eggs or bird eggs--items that represent evolutionarily derived and, in most cases, minor components of the diet--is associated with feeding on squamates or birds, respectively. Phylogenetic concentrated-changes tests indicate a significant tendency for predation on eggs to arise in snake lineages characterized by feeding on the corresponding animals. These results also generally hold for analyses including only snake species that are likely to encounter eggs and are large enough to ingest them. The inferred histories of specialized egg eaters also support the hypothesis. Because snakes often use chemical cues to recognize prey, the observed phylogenetic patterns might be explained by chemical similarities between eggs and adult animals. Our results suggest broad effects of predispositions on snake diets and thus illustrate how historical contingencies can shape the ecology of organisms.     

Coos,booms, and hoots: The evolution of closed‐mouth vocal behavior in birds

Most birds vocalize with an open beak, but vocalization with a closed beak into an inflating cavity occurs in territorial or courtship displays in disparate species throughout birds. Closed‐mouth vocalizations generate resonance conditions that favor low‐frequency sounds. By contrast, open‐mouth vocalizations cover a wider frequency range. Here we describe closed‐mouth vocalizations of birds from functional and morphological perspectives and assess the distribution of closed‐mouth vocalizations in birds and related outgroups. Ancestral‐state optimizations of body size and vocal behavior indicate that closed‐mouth vocalizations are unlikely to be ancestral in birds and have evolved independently at least 16 times within Aves, predominantly in large‐bodied lineages. Closed‐mouth vocalizations are rare in the small‐bodied passerines. In light of these results and body size trends in nonavian dinosaurs, we suggest that the capacity for closed‐mouth vocalization was present in at least some extinct nonavian dinosaurs. As in birds, this behavior may have been limited to sexually selected vocal displays, and hence would have co‐occurred with open‐mouthed vocalizations.     

Dietary breadth of frugivorous birds in relation to their feeding strategies in the lowland forests of central Honshu,Japan

Variation in the dietary breadth of frugivorous birds, i.e. variation in the degree of dietary specialization, is a key factor for understanding the construction of the architecture of diffused fruit–bird interactions. However, little information is available on the dietary breadth of frugivorous birds in a community and the avian attributes influencing it. In this study, we evaluated and compared the dietary breadth of 23 frugivorous birds (including both seed dispersers and seed predators) in relation to their feeding strategies (depending on which the birds were categorized into four types as gulpers, grinders, crushers and peckers) and other avian attributes. In particular, we hypothesized that feeding types with long fruit‐handling time (i.e. crushers and peckers) have a narrow dietary breadth. Our analysis was based on the data obtained through long‐term volunteer monitoring in the lowland forests of Kanagawa prefecture, Japan. We evaluated the dietary breadth of the birds while controlling for differences in sampling efforts and seasonal variation in the available fruit assemblages among the birds. Our analysis revealed that there was a large variation in dietary breadth among the birds, even after controlling for differences in sampling efforts and seasonal variation in the available fruit assemblages. Feeding strategies of the birds defined their dietary breadth to some degree, but we found little support for the hypothesis that fruit handling determines dietary breadth. We also observed a large variation in dietary breadth among the gulpers, which act mainly as seed dispersers for plants, and this variation could not be explained fully by other avian attributes. Our results showed that variation in the dietary breadth of frugivorous birds is partly determined by their feeding strategies and suggested that other unknown factors may play a role in determining dietary breadth variation and in structuring fruit–bird interaction networks.     

Does morphology predict behavior? Correspondence between behavioral and morphometric data in a Tyrant‐flycatcher (Tyrannidae) assemblage in the Santa Marta Mountains,Colombia

ABSTRACT Morphology is commonly used as a predictor of ecological relationships among species when studying local assemblages of Neotropical birds. Nevertheless, most evidence supporting ecomorphological correspondence in birds comes from studies of communities and not from local assemblages and, moreover, from temperate latitudes. To increase our understanding of ecomorphological correspondence in Neotropical assemblages, we used three multivariate approaches to evaluate correspondence between morphological and foraging behavior data in a tyrant‐flycatcher assemblage (N= 12 species) in the Santa Marta Mountains in Colombia. Principal components analyses revealed similar species ordinations when using morphological measurements (beak size and shape, tarsus length, wing length, and tail length) or behavioral data (behavioral types of searching for prey and prey capture) separately. Discriminant function analyses tested the ability of morphological traits to predict foraging behavior, showing that more than 90% of all measured individuals (N= 267) were correctly classified in previously defined categories of search and attack behavior. Finally, Canonical correlation analyses revealed a significant correlation between morphological data and two independent datasets of search and attack behavior. Our results demonstrate that morphology can accurately predict ecology in an assemblage of Neotropical tyrannids, and similar results have been reported in previous studies of temperate Tyrant‐flycatchers. Our results also show that bill size and shape, wing length, and tarsus length are the best predictors of foraging behavior in this assemblage. Testing for ecomorphological correspondence in other Neotropical taxa would help identify subsets of phenotypic traits that could be used for a practical, but reliable, determination of ecological relationships within different assemblages.     

Skull shape variation in extant and extinct Testudinata and its relation to habitat and feeding ecology

Turtles (Testudinata) are a diverse group of reptiles that conquered a broad set of habitats and feeding ecologies over the course of their well‐documented evolutionary history. We here investigate the cranial shape of 171 representatives of the turtle lineage and the relationship of shape to different habitat and diet preferences using two‐dimensional geometric morphometrics. The skull shape of extant turtles correlates with both ecological proxies, but is more affected by habitat than diet. However, the application of these correlations to extinct turtles produces mostly flawed results, as least when compared to external data such as sedimentary environment, highlighting that the morphospace held by extant turtles is not necessarily the optimal location in tree space for a particular ecology. The inability of this study to correctly predict the ecology of extinct turtles is likely related to the fact that the shape of turtle skulls is dominated by the emarginations and jaw closure mechanisms, two shape features unrelated to habitat or feeding ecology. This indicates that various specializations that are apparent in the skull only contribute little to overall shape.     

Evolution of tooth crown shape in Mesozoic birds,and its adaptive significance with respect to diet

Both the evolution of tooth morphology and the relationship between dental features and diet in toothed birds have long been studied. Here we quantify variation in tooth crown shape in 28 key Mesozoic bird species, and examine differences in dental morphology among birds belonging to different taxonomic groupings and inferred to have had different diets. Using geometric morphometric methods (GMM) and phylogenetic comparative methods (PCM), we found few clear differences in tooth crown shape between different taxonomic and ecological categories, and our analysis provides little support for many dietary inferences drawn in previous studies. However, the Solnhofen Archaeopteryx, Jeholornis, Protopteryx, Pengornis, Longipteryx, Tianyuornis, Mengciusornis, Ichthyornis and Hesperornis all were found to possess relatively specialized tooth crown shapes, perhaps reflecting specialized diets such as insectivory, granivory, piscivory and consumption of soft-shelled arthropods. Similarity in tooth crown shape across many Mesozoic birds may indicate the lack of dietary specialization, and the association between tooth form and diet may have been weakened in any case by ‘functional replacement’ of the dentition by a horny beak and, in many cases, gastroliths.     

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.     

Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test

Many male birds use carotenoid pigments to acquire brilliant colors that advertise their health and condition to prospective mates. The direct means by which the most colorful males achieve superior health has been debated, however. One hypothesis, based on studies of carotenoids as antioxidants in humans and other animals, is that carotenoids directly boost the immune system of colorful birds. We studied the relationship between carotenoid pigments, immune function, and sexual coloration in zebra finches (Taeniopygia guttata), a species in which males incorporate carotenoid pigments into their beak to attract mates. We tested the hypotheses that increased dietary carotenoid intake enhances immunocompetence in male zebra finches and that levels of carotenoids circulating in blood, which also determine beak coloration, directly predict the immune response of individuals. We experimentally supplemented captive finches with two common dietary carotenoid pigments (lutein and zeaxanthin) and measured cell-mediated and humoral immunity a month later. Supplemented males showed elevated blood-carotenoid levels, brighter beak coloration, and increased cell-mediated and humoral immune responses than did controls. Cell-mediated responses were predicted directly by changes in beak color and plasma carotenoid concentration of individual birds. These experimental findings suggest that carotenoid-based color signals in birds may directly signal male health via the immunostimulatory action of ingested and circulated carotenoid pigments.     

Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus

The development of molecular genetic screening techniques for avian blood parasites has revealed many novel aspects of their ecology, including greatly elevated diversity and complex host-parasite relationships. Many previous studies of malaria in birds have treated single study populations as spatially homogeneous with respect to the likelihood of transmission of malaria to hosts, and we have very little idea whether any spatial heterogeneity influences different malaria lineages similarly. Here, we report an analysis of variation in the prevalence and cytochrome b lineage distribution of avian malaria infection with respect to environmental and host factors, and their interactions, in a single blue tit (Cyanistes caeruleus) population. Of 11 Plasmodium and Haemoproteus cytochrome b lineages found in 997 breeding individuals, the three most numerous (pSGS1, pTURDUS1 and pBT7) were considered separately, in addition to analyses of all avian malaria lineages pooled. Our analyses revealed marked spatial differences in the prevalence and distribution of these lineages, with local prevalence of malaria within the population ranging from over 60% to less than 10%. In addition, we found several more complex patterns of prevalence with respect to local landscape features, host state, parasite genotype, and their interactions. We discuss the implications of such heterogeneity in parasite infection at a local scale for the study of the ecology and evolution of infectious diseases in natural populations. The increased resolution afforded by the combination of molecular genetic and geographical information systems (GIS) tools has the potential to provide many insights into the epidemiology, evolution and ecology of these parasites in the future.     

Dietary correlates of temporomandibular joint morphology in New World primates

Previous analyses of the masticatory apparatus have demonstrated that the shape of the temporomandibular joint (TMJ) is functionally and adaptively linked to variation in feeding behavior and diet in primates. Building on previous research, this study presents an analysis of the link between diet and TMJ morphology in the context of functional and dietary differences among New World primates. To evaluate this proposed relationship, I used three-dimensional morphometric methods to quantify TMJ shape across a sample of 13 platyrrhine species. A broad interspecific analysis of this sample found strong relationships among TMJ size, TMJ shape, and diet, suggesting that both size and diet are significant factors influencing TMJ morphology in New World primates. However, it is likely that at least some of these differences are related to a division of dietary categories along clade lines.A series of hypotheses related to load resistance capabilities and range of motion in the TMJ were then tested among small groups of closely related taxa with documented dietary differences. These pairwise analyses indicate that some aspects of TMJ morphology can be used to differentiate among closely related species with different diets. However, not all of my predictions were upheld. The anteroposterior dimensions of the TMJ were most strongly consistent with hypothesized differences in ingestive/masticatory behaviors and jaw gape, whereas the predictions generated for variation in entoglenoid and articular tubercle height were not upheld. These results imply that while some features can be reliably associated with increased load resistance and facilitation of wider jaw gapes in the masticatory apparatus, other features are less strongly correlated with masticatory function.     

Variability in seed size selection by granivorous passerines: effects of bird size,bird size variability,and ecological plasticity

The niche variation hypothesis predicts a direct relationship between intraspecific variability in feeding ecology and the variability of the morphological traits related to feeding behaviour. The following study tests this prediction by measuring in captivity the seed size preferences and the morphology of 9–11 individuals of seven specialized granivorous bird species. The average seed size preferences of these birds have previously been shown to be related to components of bill size. The ranges of seed sizes selected were related to the mean bill sizes of birds in a way that paralleled the patterns found when analysing average values. Bill and body size variability were not related, however, to the range of seed preferences after controlling for the significant mean-variance relationship showed by morphological traits. Thus, results do not support the niche variation hypothesis. the significant effect of average bill size on diet variability was consistent with the direct relationship between bird size and ecological plasticity expected on the basis of the shape of the family of functions relating seed size and seed profitability for different-sized birds. These findings suggest morphological mechanisms for ecological plasticity whose generality and evolutionary significance merit further research.     

Fruit-eating in brids and its nutritional consequences

Fruits comprise a large protion of the diet in many bird species. Several species switch diet composition seasonally, from a diet consisting almost entirely of invertebrates to one that comprises even exclusively fruits, and vice versa. The adaptive significance of these dietary shifts has rarely been investigated. The present article reviews some recent data revealing much evidence that seasonal frugivory is highly adaptive, and that fruits may be an adequate food to satisfy the birds' daily nutritional demands. There is further evidence that fruits may provide particular nutritional qualities to meet particular demands. Secondary plant metabolites considered to act as feeding deterrents seem to be less detrimental to avian frugivores than observed in many herbivores. The birds appear to be able to counteract the detrimental effects of secondary compounds taken with their fruit diets. In addition, there is evidence that secondary plant compounds may even stimulate food intake and metabolism in avian frugivores, although the mechanisms of counteradaptation need to be clarified.     

Microanatomy of passerine hard‐cornified tissues: Beak and claw structure of the black‐capped chickadee (Poecile atricapillus)

The microanatomy of healthy beaks and claws in passerine birds has not been well described in the literature, despite the importance of these structures in avian life. Histological processing of hard‐cornified tissues is notoriously challenging and only a few reports on effective techniques have been published. An emerging epizootic of beak deformities among wild birds in Alaska and the Pacific Northwest region of North America recently highlighted the need for additional baseline information about avian hard‐cornified structures. In this study, we examine the beak and claw of the Black‐capped Chickadee (Poecile atricapillus), a common North American passerine that is affected by what has been described as “avian keratin disorder.” We use light and scanning electron microscopy and high‐magnification radiography to document the healthy microanatomy of these tissues and identify features of functional importance. We also describe detailed methods for histological processing of avian hard‐cornified structures and discuss the utility of special stains. Results from this study will assist in future research on the functional anatomy and pathology of hard‐cornified structures and will provide a necessary reference for ongoing investigations of avian keratin disorder in Black‐capped Chickadees and other wild passerine species. © 2011 Wiley Periodicals, Inc.     

The skull evolution of oviraptorosaurian dinosaurs: the role of niche partitioning in diversification

Oviraptorosaurs are bird‐like theropod dinosaurs that thrived in the final pre‐extinction ecosystems during the latest Cretaceous, and the beaked, toothless skulls of derived species are regarded as some of the most peculiar among dinosaurs. Their aberrant morphologies are hypothesized to have been caused by rapid evolution triggered by an ecological/biological driver, but little is known about how their skull shapes and functional abilities diversified. Here, we use quantitative techniques to study oviraptorosaur skull form and mandibular function. We demonstrate that the snout is particularly variable, that mandibular form and upper/lower beak form are significantly correlated with phylogeny, and that there is a strong and significant correlation between mandibular function and mandible/lower beak shape, suggesting a form–function association. The form–function relationship and phylogenetic signals, along with a moderate allometric signal in lower beak form, indicate that similar mechanisms governed beak shape in oviraptorosaurs and extant birds. The two derived oviraptorosaur clades, oviraptorids and caenagnathids, are significantly separated in morphospace and functional space, indicating that they partitioned niches. Oviraptorids coexisting in the same ecosystem are also widely spread in morphological and functional space, suggesting that they finely partitioned feeding niches, whereas caenagnathids exhibit extreme disparity in beak size. The diversity of skull form and function was likely key to the diversification and evolutionary success of oviraptorosaurs in the latest Cretaceous.     

Review: Key tweaks to the chicken's beak: the versatile use of the beak by avian species and potential approaches for improvements in poultry production

The avian beak is a multipurpose organ playing a vital role in a variety of functions, including feeding, drinking, playing, grasping objects, mating, nesting, preening and defence against predators and parasites. With regards to poultry production, the beak is the first point of contact between the bird and feed. The beak is also manipulated to prevent unwanted behaviour such as feather pecking, toe pecking and cannibalism in poultry as well as head/neck injuries to breeder hens during mating. Thus, investigating the beak morphometry of poultry in relation to feeding and other behaviours may lead to novel insights for poultry breeding, management and feeding strategies. Beak morphometry data may be captured by advanced imaging techniques coupled with the use of geometric morphometric techniques. This emerging technology may be utilized to study the effects of beak shape on many critical management issues including heat stress, parasite management, pecking and feeding behaviour. In addition, existing literature identifies several genes related to beak development in chickens and other avian species. Use of morphometric assessments to develop phenotypic data on beak shape and detailed studies on beak-related behaviours in chickens may help in improving management and welfare of commercial poultry.     

Ecological correlates of trophic status and frugivory in neotropical primates

Primates are among the most observable and best studied vertebrate order in tropical forest regions, with widespread attention dedicated to the feeding ecology of wild populations. In particular, primates play a key role as frugivores and seed‐dispersal agents for a myriad of tropical plants. Sampling effort by primatologists, however, has been unequally distributed, hampering quantitative comparisons of primate diets. We provide the first systematic review of primate diets, with an emphasis on frugivory, using a comprehensive compilation of 290 unique primate dietary studies from 164 localities in 17 countries across the entire Neotropical realm. We account for sampling effort (standardised as hours) in comparing the richness of fruiting plants recorded in primate diets, and the relative contribution of frugivory to the overall diet in relation to key life‐history traits, such as body mass. We find strong support for the long‐held hypothesis, based on Kay's Threshold, that body size imposes an upper limit on insectivory and a lower limit on folivory, and therefore that frugivory is most important at intermediate body sizes. However, the upper body mass limit of extant neotropical primates, truncated by the post‐Pleistocene megafaunal overkill, has implications for the extent of the frugivory–folivory continuum in extinct lineages. Contemporary threats faced by the largest primates serve as a further warning that the feeding ecology and diet of all neotropical primates remain severely undersampled with regard to the composition and richness of fruits consumed. Indeed, frugivorous primates expected to have the most species‐rich plant diets are amongst those most poorly sampled, exposing implications for our current understanding of primate–plant interaction networks.     

The evolution of the modern avian digestive system: insights from paravian fossils from the Yanliao and Jehol biotas

The avian digestive system, like other aspects of avian biology, is highly modified relative to other reptiles. Together these modifications have imparted the great success of Neornithes, the most diverse clade of amniotes alive today. It is important to understand when and how aspects of the modern avian digestive system evolved among neornithine ancestors in order to elucidate the evolutionary success of this important clade and to understand the biology of stem birds and their closest dinosaurian relatives: Mesozoic Paraves. Although direct preservation of the soft tissue of the digestive system has not yet been reported, ingested remains and their anatomical location preserved in articulated fossils hint at the structure of the digestive system and its abilities. Almost all data concerning direct evidence of diet in Paraves comes from either the Upper Jurassic Yanliao Biota or the Lower Cretaceous Jehol Biota, both of which are known from deposits in north-eastern China. Here, the sum of the data gleaned from the thousands of exceptionally well-preserved fossils of paravians is interpreted with regards to the structure and evolution of the highly modified avian digestive system and feeding apparatus. This information suggests intrinsic differences between closely related stem lineages implying either strong homoplasy or that diet in each lineage of non-ornithuromorph birds was highly specialized. Regardless, modern digestive capabilities appear to be limited to the Ornithuromorpha, although the complete set of derived feeding related characters is restricted to the Neornithes.