Bills Of Birds Research Articles

Variable foraging and flower probing behaviour of sunbird pollinators of the South African Pelargonium fulgidum

ABSTRACT Whether foraging sunbird pollinators hover or perch, the type of perch used, and the direction of flower probing are generally thought to be determined by matching shapes of decurved bird bills and curved flower tubes, as well as inflorescence architecture. However, few studies have objectively quantified aspects of sunbird foraging behaviour to test predictions based on adaptive trait matching. I investigated sunbird foraging in a population of Pelargonium fulgidum, a species with slightly upcurved flowers borne on upward-oriented peduncles, which grows along the west coast of South Africa. Long-range photographs revealed that Cinyris chalybeus, a sunbird species with a slightly decurved bill, hovers or perches during foraging, and uses both the inflorescence and alternative vegetation structures as perch. Contrary to previous suggestions, both male and female sunbirds probe flowers from either of two alternative directions (sternotribic versus nototribic) in more or less equal proportions, and frequently display flexibility in both foraging behaviour and flower probing direction. Predominant or complete sternotribic and nototribic flower probing were explained by hovering versus use of an inflorescence perch respectively, whereas use of an alternative perch resulted in similar proportions of each mode of flower probing. The number of flowers per visited inflorescence and number and proportion of probed flowers did not vary with foraging behaviour or flower probing direction. Although certain foraging behaviours resulted in predictable flower probing directions, variation in foraging behaviour and the presence of many alternative perches provided by vegetation surrounding P. fulgidum plants resulted in variability in flower probing direction that appears not to affect foraging efficiency. Relatively weak reciprocal curvature of flower tube and sunbird bill, resulting in easy access to nectar from multiple feeding directions, likely facilitates flexible foraging. This study shows that environmental context may facilitate more complex foraging behaviour than that predicted by adaptive trait matching.

Natural history of pollination of an Asian bignoniaceous tree: The long-tubed flower and the not-so-long bird bill

Bird pollination is well-established in New World Bignoniaceae, but studies of species with floral traits suggestive of bird pollination in the Old World are lacking. Here we studied the pollination ecology of Mayodendron igneum to test the prediction of pollination by specialist flower-visiting birds. Observations from multiple sites showed that both the Streaked Spiderhunter (Arachnothera magna) and pollen-collecting bees were floral visitors. However, almost no fruit was produced if birds were excluded, suggesting that bees do not play a role in pollination, and that pollination is performed almost exclusively by birds in this self-incompatible tree. Measurements of floral traits revealed a typical bird pollination syndrome, and the nectar concentration and volume were both within the proposed ranges based on other flowers pollinated by specialist birds. However, the rather low level of sucrose (less than 2 %) in nectar sugar contradicts the expectation for nectar of flowers pollinated by specialist nectar-feeding birds. Although the Streaked Spiderhunter is among the longest-billed flower-visiting birds in Asia, its bill is only 2/3 of the corolla tube in length, suggesting that the bird can extend the tongue to access nectar. This study is the first to experimentally confirm bird pollination in the Old World Bignoniaceae. It also indicates aspects that are possibly characteristic of spiderhunter pollination systems, i.e. high degrees of specialization, unusual nectar sugar composition, and floral tubes much longer than bird bills.

Birds are better at regulating heat loss through their legs than their bills: implications for body shape evolution in response to climate.

Endotherms use their appendages-such as legs, tails, ears and bills-for thermoregulation by controlling blood flow to near-surface blood vessels, conserving heat when it is cold, and dissipating heat in hot conditions. Larger appendages allow greater heat dissipation, and appendage sizes vary latitudinally according to Allen's rule. However, little is known about the relative importance of different appendages for thermoregulation. We investigate physiological control of heat loss via bird bills and legs using infrared thermography of wild birds. Our results demonstrate that birds are less able to regulate heat loss via their bills than their legs. In cold conditions, birds lower their leg surface temperature to below that of their plumage surface, retaining heat at their core. In warm conditions, birds increase their leg surface temperature to above that of their plumage surface, expelling heat. By contrast, bill surface temperature remains approximately 2°C warmer than the plumage surface, indicating consistent heat loss under almost all conditions. Poorer physiological control of heat loss via bird bills likely entails stronger selection for shorter bills in cold climates. This could explain why bird bills show stronger latitudinal size clines than bird legs, with implications for predicting shape-shifting responses to climate change.

Ecological predictors of interspecific variation in bird bill and leg lengths on a global scale.

Bills and legs are two vital appendages for birds, and they exhibit huge interspecific variation in form and function, yet no study has examined the global predictors of this variation. This study examined global gradients in the relative lengths of bird bills and tarsi (i.e. exposed leg parts) to body size across non-migratory birds, while accounting for phylogeny. We found that relative bill length and tarsus length were related to diet, habitat density, latitude, annual mean temperature, temperature variability and hand-wing index (HWI), a proxy for birds' flight efficiency. Among these factors, diet played a primary role in predicting bill length, with nectar-feeding pollinators, vertivores, invertivores and omnivores having longer bills; HWI emerged as the predominant predictor of tarsus length, wherein species with higher HWI had shorter tarsi. However, the effects of these factors differed between passerines and non-passerines, with some temperature-related effects exhibiting opposite trends between these two groups. Our findings highlight the compromise in adaptations for feeding, thermoregulation and flight performance between the two distinct appendages.

A century of comparative biomechanics: emerging and historical perspectives on an interdisciplinary field.

A century of comparative biomechanics: emerging and historical perspectives on an interdisciplinary field.

Effects of climate on bill morphology within and across Toxostoma thrashers

Bird bills possess an important thermoregulatory function as they are a site for environmental heat exchange. Previous studies have demonstrated that birds in warmer climates have larger bills than those living in colder climates, as larger bills can dissipate more heat. Because this dry heat transfer does not incur water loss, it may be additionally advantageous in water‐restricted habitats. Here, we examine the influence of climate on bill morphology in Toxostoma thrashers, a group of 10 North American species that varied in bill morphology and occupied climate niche, with several species inhabiting arid climates. Past examinations of thrasher bill morphology have only considered foraging, leaving unanswered the role of climate in morphological divergence within this group. We photographed 476 Toxostoma museum specimens encompassing all 10 species and calculated bill measurements from the photos using a MATLAB‐based program. For each species, we calculated occupied climate niche using data from WorldClim describing temperature and precipitation. We found no reliable significant relationships between climate variables and bill morphology across species, suggesting that other factors such as foraging behavior may be more important in shaping bill morphology in this genus. Within species, we found three Toxostoma species have significant relationships between bill morphology and climate that follow Allen's rule. However, we also found the relationships between climate and bill morphology varied in strength and direction across species. Notably, we found a negative relationship between maximum temperature of the hottest month and bill surface area in LeConte's thrasher, which occupies the hottest and most arid climates of the thrashers. This adds to the evidence that Allen's rule may reverse in extremely hot climates when the bill may become a heat sink instead of a heat radiator. These results demonstrate the importance of considering the generality of ecogeographical rules across lineages that occupy extreme climates.

Bene"fit" Assessment in Pollination Coevolution: Mechanistic Perspectives on Hummingbird Bill-Flower Matching.

One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill-flower matching, with a strong focus on the benefits to the hummingbird and how to quantify them. Explanations for the coevolution of bill-flower matching include (1) that the evolution of traits by bird-pollinated plants, such as long and thin corollas, prevents less efficient pollinators (e.g., insects) from accessing the nectar and (2) that increased matching, as a result of reciprocal adaptation, benefits both the bird (nectar extraction efficiency) and the plant (pollen transfer). In addition to nectar-feeding, we discuss how interference and exploitative competition also play a significant role in the evolution and maintenance of trait matching. We present hummingbird-plant interactions as a model system to understand how trait matching evolves and how pollinator behavior can modify expectations based solely on morphological matching, and discuss the implications of this behavioral modulation for the maintenance of specialization. While this perspective piece directly concerns hummingbird-plant interactions, the implications are much broader. Functional trait matching is likely common in coevolutionary interactions (e.g., in predator-prey interactions), yet the physical mechanisms underlying trait matching are understudied and rarely quantified. We summarize existing methods and present novel approaches that can be used to quantify key benefits to interacting partners in a variety of ecological systems.

Object manipulation without hands.

Our current understanding of manipulation is based on primate hands, resulting in a detailed but narrow perspective of ways to handle objects. Although most other animals lack hands, they are still capable of flexible manipulation of diverse objects, including food and nest materials, and depend on dexterity in object handling to survive and reproduce. Birds, for instance, use their bills and feet to forage and build nests, while insects carry food and construct nests with their mandibles and legs. Bird bills and insect mandibles are much simpler than a primate hand, resembling simple robotic grippers. A better understanding of manipulation in these and other species would provide a broader comparative perspective on the origins of dexterity. Here we contrast data from primates, birds and insects, describing how they sense and grasp objects, and the neural architectures that control manipulation. Finally, we outline techniques for collecting comparable manipulation data from animals with diverse morphologies and describe the practical applications of studying manipulation in a wide range of species, including providing inspiration for novel designs of robotic manipulators.

Are superior ovaries damaged by the bills of flower-visiting birds and does this preclude adaptation to bird pollinators?

A biological trait may promote adaptation to particular pollinators, and this may be a major factor governing the variation of pollination systems among angiosperm taxa. For instance, one long-standing hypothesis is that compared with superior ovaries, inferior ovaries of angiosperm flowers may be protected from damage by visiting bird bills and, therefore, inferior ovaries may be associated more frequently with bird pollination. To test this hypothesis, we explored the pollination ecology of two Cerasus spp. (Rosaceae) with superior ovaries and investigated the potential damage to superior ovaries by bird bills, because such damage must be predicted by the hypothesis. To test whether there is a general relationship between ovary position and bird pollination, we examined published community-level studies involving bird pollination. Cerasus cerasoides is more inclined to bird pollination than C. conradinae in floral syndrome and pollination experiments, whereas damage to the ovaries or decline in fruit set after bird visitation was not detected in either species. The birds extended their tongues longer than the ovaries, demonstrating why the predicted damage was absent. Bird pollination was not less frequent in plants with superior ovaries in reviewed studies. Our findings did not support the prediction that superior ovaries are damaged by flower-visiting birds and overall the frequency of bird pollination varies with ovary position. These results highlight the complexity in predicting how floral traits affect plant adaptation to pollinators.

Habitat-specific divergence of air conditioning structures in bird bills

ABSTRACT We used high precision computed tomography (CT) and traditional radiography to study the nasal conchae, complex structures within the nasal cavity that condition air via countercurrent heat exchange. Air conditioning in the conchae assists thermoregulation and water balance, both of which pose challenges for many birds. We hypothesized that hot and water-limited environments would select for larger or more complex conchae to maximize moisture recapture during exhalation and in turn cause the evolution of deeper and wider bills. We provide the first intraspecific comparison of concha size and structure in birds based on CT scans of 15 individuals and radiographs of 39 individuals of 2 subspecies of Song Sparrow (Melospiza melodia) that inhabit climatically distinct habitats. CT scans revealed that middle and rostral conchae filled the nasal cavities and had larger surface areas in individuals with larger nasal cavities. The subspecies that inhabits hot and dry coastal dunes (M. m. atlantica) had r...

Bills as daggers? A test for sexually dimorphic weapons in a lekking hummingbird

One way in which secondary sexual traits can influence differential reproductive success is by playing a key role in the outcome of direct physical contests for mates. Here we describe an undocumented trait in a species of hummingbird with a lek mating system, the Long-billed hermit (LBH, Phaethornis longirostris). The trait under consideration is a dagger-like structure at the bill tip, which we hypothesize is a secondary sexual trait that functions as a sexually dimorphic weapon. We tested our hypothesis by examining 5 leks during 4 consecutive years, and by employing morphological analyses, performance experiments, and behavioral observations. We found that 1) adult male bill tips were longer and pointier than their counterparts in females and juvenile males, 2) juvenile males acquired dagger-like tips during their transition to adulthood, 3) variation in bill tip morphology reflected puncture capability, and 4) males with larger and pointier bill tips were more successful in achieving lek territory tenure. Our study provides the first evidence of sexually dimorphic weapons in bird bills and stands as one of the few examples of male weaponry in birds. Our results suggest a role of sexual selection on the evolution of overall bill morphology, an alternative hypothesis to the prevailing ecological causation explanation for bill sexual dimorphism in hummingbirds.

Neural Correlates of a Magnetic Sense

Many animals rely on Earth's magnetic field for spatial orientation and navigation. However, how the brain receives and interprets magnetic field information is unknown. Support for the existence of magnetic receptors in the vertebrate retina, beak, nose, and inner ear has been proposed, and immediate gene expression markers have identified several brain regions activated by magnetic stimulation, but the central neural mechanisms underlying magnetoreception remain unknown. Here we describe neuronal responses in the pigeon's brainstem that show how single cells encode magnetic field direction, intensity, and polarity; qualities that are necessary to derive an internal model representing directional heading and geosurface location. Our findings demonstrate that there is a neural substrate for a vertebrate magnetic sense.

High summer temperature explains bill size variation in salt marsh sparrows

Physiological factors are rarely proposed to account for variation in the morphology of feeding structures. Recently, bird bills have been demonstrated to be important convective and radiant heat sinks. Larger bills have greater surface area than smaller bills and could serve as more effective thermoregulatory organs under hot conditions. The heat radiating function of bills should be more important in open habitats with little shade and stronger convective winds. Furthermore, as a means of dumping heat without increasing water loss through evaporation, bills might play a particularly important thermoregulatory role in heat loss in windy habitat where fresh water is limited. North American salt marshes provide a latitudinal gradient of relatively homogeneous habitat that is windy, open, and fresh‐water limited. To examine the potential role of thermoregulation in determining bill size variation among ten species or subspecies of tidal marsh sparrows, we plotted bill size against maximum summer and minimum winter temperatures. Bill surface areas increases with summer temperature, which explained 82–89% of the variance (depending upon sex) when we controlled for genus membership. Latitude alone predicted bill surface area much more poorly than summer temperature, and winter temperatures explained < 10% of the variance in winter bill size. Tidal marsh sparrow bill morphology may, to a large degree, reflect the role of the bill in expelling excess body heat in these unbuffered, fresh‐water‐limited environments. This new example of Allen's rule reaffirms the importance of physiological constraints on the evolution of vertebrate morphologies, even in bird bills, which have conventionally been considered as products of adaptation to foraging niche.

Geographical Variation in Bill Size across Bird Species Provides Evidence for Allen’s Rule

Allen's rule proposes that the appendages of endotherms are smaller, relative to body size, in colder climates, in order to reduce heat loss. Empirical support for Allen's rule is mainly derived from occasional reports of geographical clines in extremity size of individual species. Interspecific evidence is restricted to two studies of leg proportions in seabirds and shorebirds. We used phylogenetic comparative analyses of 214 bird species to examine whether bird bills, significant sites of heat exchange, conform to Allen's rule. The species comprised eight diverse taxonomic groups-toucans, African barbets, Australian parrots, estrildid finches, Canadian galliforms, penguins, gulls, and terns. Across all species, there were strongly significant relationships between bill length and both latitude and environmental temperature, with species in colder climates having significantly shorter bills. Patterns supporting Allen's rule in relation to latitudinal or altitudinal distribution held within all groups except the finches. Evidence for a direct association with temperature was found within four groups (parrots, galliforms, penguins, and gulls). Support for Allen's rule in leg elements was weaker, suggesting that bird bills may be more susceptible to thermoregulatory constraints generally. Our results provide the strongest comparative support yet published for Allen's rule and demonstrate that thermoregulation has been an important factor in shaping the evolution of bird bills.

Nectar bat stows huge tongue in its rib cage

Bats of the subfamily Glossophaginae (family Phyllostomidae) are arguably the most specialized of mammalian nectarivores, and hundreds of neotropical plants rely on them for pollination. But flowers pollinated by bats are not known to specialize for bat subgroups (unlike flowers that have adapted to the length and curvature of hummingbird bills, for example), possibly because the mouthparts of bats do not vary much compared with the bills of birds or the probosces of insects. Here I report a spectacular exception: a recently-described nectar bat that can extend its tongue twice as far as those of related bats and is the sole pollinator of a plant with corolla tubes of matching length.

VARIATION IN THE TARSUS LENGTH OF BIRDS IN ISLAND AND MAINLAND REGIONS.

The biological significance of variation in such complex morphological characters as the bills of birds is open to question. Van Valen (1965) has argued that variation in bill width is adaptive in itself, and is not part of the genetic or phenotypic load. Soule and Stewart (1970) have argued against this interpretation, and have suggested instead that a large degree of variation indicates a transient release of variation associated with a deterioration of canalization. This happens, they argue, in small isolated populations living in simplified environments, as on islands. The difference might be resolved if it was known whether populations on islands generally exhibit a large degree of variation. It is difficult to anticipate whether they do or do not from a consideration of either the generation or maintenance of variation. If an island is colonized by one or a few individuals from a mainland region the island population starts with only a portion of the total genetic variety of the mainland population, because not all of the alleles are present in the island population. If this reduced genetic variety is translated into a reduced phenotypic variance, one might anticipate that the island population exhibits less morphological variation than its mainland counterpart, even after it has reached an equilibrium population size in the island environment. However, as Lewontin (1965, p. 481) has pointed out, the genetic variance upon which selection acts will not be substantially lower in the island population than in the mainland population. Indeed, while the population on the island is increasing, considerable genetic variation due to recombination and mutation might appear if selection is weaker here than on the mainland. But this is a temporary phenomenon. How might selection act when the population has reached equilibrium size? Again it is not easy to make an a priori judgment on the basis of ecological considerations. On the one hand the diversity of habitats and food is less on islands than on the mainland, conditions which might lead one to anticipate reduced morphological variation on islands as a result of selection. On the other hand the diversity of competitors and predators is less on islands than mainland, which might allow for greater ecological and morphological variation in a population on an island. In the face of such uncertainty it is helpful to proceed empirically. Amadon (1950) and Lack (1947) noted that morphological variation in birds from oceanic islands was approximately the same as that in distantly related species of birds from continents. The populations of six species Van Valen (1965) studied were from mainland and island regions. With one predictable exception, all the island populations exhibited greater morphological variation than did the mainland populations. However this result cannot be used to make a general statement about variation in birds on islands and mainland, because the examples were carefully selected on the basis of pre-existing information on the relative size of the ecological niche of each species in the island and mainland regions, and because the mainland areas were far from the closest point to the islands. Grant (1965a, 1967) attempted to discover if morphological variation was larger or smaller on islands than on mainland by using data from most of the 34 land bird species on the Tres Marias Islands and on the adjacent mainland of western Mexico. Variation in length of wing, tail, tarsus and