RESUMEN
We investigated the kinematics and biomechanics of nectar feeding in five species of honeyeater (Phylidonyris novaehollandiae, Acanthagenys rufogularis, Ptilotula penicillata, Certhionyx variegatus, Manorina flavigula). There is abundant information on honeyeater foraging behaviors and ecological relationships with plants, but there has never been an examination of their nectar-feeding from kinematic and biomechanical perspectives. We analyzed high-speed video of feeding in captive individuals to describe the kinematics of their nectar feeding, with specific focus on describing tongue movements and bill-tongue coordination, and to characterize the mechanism of nectar uptake in the tongue. We found clear interspecific variation in kinematics and tongue filling mechanics. Species varied in lick frequency, tongue velocity, and protrusion and retraction duration, which, in some cases, are relevant for differences in tongue filling mechanisms. We found support for the use of capillary filling in Certhionyx variegatus only. By contrast, Phylidonyris novaehollandiae, Acanthagenys rufogularis, Ptilotula penicillata, and Manorina flavigula employed a modified version of the expansive filling mechanism seen in hummingbirds, as there was dorsoventral expansion of the tongue body, even the portions that remain outside the nectar, once the tongue tip entered the nectar. All species use fluid trapping in the distal fimbriated portion of the tongue, which supports previous hypotheses describing the honeyeater tongue as a "paintbrush."
Asunto(s)
Passeriformes , Néctar de las Plantas , Humanos , Animales , Conducta AlimentariaRESUMEN
Nectar-feeding birds provide an excellent system in which to examine form-function relationships over evolutionary time. There are many independent origins of nectarivory in birds, and nectar feeding is a lifestyle with many inherent biophysical constraints. We review the morphology and function of the feeding apparatus, the locomotor apparatus, and the digestive and renal systems across avian nectarivores with the goals of synthesizing available information and identifying the extent to which different aspects of anatomy have morphologically and functionally converged. In doing so, we have systematically tabulated the occurrence of putative adaptations to nectarivory across birds and created what is, to our knowledge, the first comprehensive summary of adaptations to nectarivory across body systems and taxa. We also provide the first phylogenetically informed estimate of the number of times nectarivory has evolved within Aves. Based on this synthesis of existing knowledge, we identify current knowledge gaps and provide suggestions for future research questions and methods of data collection that will increase our understanding of the distribution of adaptations across bodily systems and taxa, and the relationship between those adaptations and ecological and evolutionary factors. We hope that this synthesis will serve as a landmark for the current state of the field, prompting investigators to begin collecting new data and addressing questions that have heretofore been impossible to answer about the ecology, evolution, and functional morphology of avian nectarivory.
Asunto(s)
Aves , Néctar de las Plantas , Animales , Aves/anatomía & histología , FilogeniaRESUMEN
Frog larvae (tadpoles) undergo many physiological, morphological and behavioral transformations throughout development before metamorphosing into their adult form. The surface tension of water prevents small tadpoles from breaching the surface to breathe air (including those of Xenopus laevis), forcing them to acquire air using a form of breathing called bubble sucking. With growth, tadpoles typically make a behavioral/biomechanical transition from bubble sucking to breaching. Xenopus laevis tadpoles have also been shown to transition physiologically from conforming passively to ambient oxygen levels to actively regulating their blood oxygen. However, it is unknown whether these mechanical and physiological breathing transitions are temporally or functionally linked, or how both transitions relate to lung maturation and gas exchange competency. If these transitions are linked, it could mean that one biomechanical breathing mode (breaching) is more physiologically proficient at acquiring gaseous oxygen than the other. Here, we describe the mechanics and development of air breathing and the ontogeny of lung morphology in X. laevis throughout the larval stage and examine our findings considering previous physiological work. We found that the transitions from bubble sucking to breaching and from oxygen conforming to oxygen regulation co-occur in X. laevis tadpoles at the same larval stage (Nieuwkoop-Faber stages 53-56 and 54-57, respectively), but that the lungs do not increase significantly in vascularization until metamorphosis, suggesting that lung maturation, alone, is not sufficient to account for increased pulmonary capacity earlier in development. Although breach breathing may confer a respiratory advantage, we remain unaware of a mechanistic explanation to account for this possibility. At present, the transition from bubble sucking to breaching appears simply to be a consequence of growth. Finally, we consider our results in the context of comparative air-breathing mechanics across vertebrates.
Asunto(s)
Pipidae , Animales , Larva/fisiología , Metamorfosis Biológica , Oxígeno , Respiración , Xenopus laevis/fisiologíaRESUMEN
Nectar-feeding birds employ unique mechanisms to collect minute liquid rewards hidden within floral structures. In recent years, techniques developed to study drinking mechanisms in hummingbirds have prepared the groundwork for investigating nectar feeding across birds. In most avian nectarivores, fluid intake mechanisms are understudied or simply unknown beyond hypotheses based on their morphological traits, such as their tongues, which are semi-tubular in sunbirds, frayed-tipped in honeyeaters and brush-tipped in lorikeets. Here, we use hummingbirds as a case study to identify and describe the proposed drinking mechanisms to examine the role of those peculiar traits, which will help to disentangle nectar-drinking hypotheses for other groups. We divide nectar drinking into three stages: (1) liquid collection, (2) offloading of aliquots into the mouth and (3) intraoral transport to where the fluid can be swallowed. Investigating the entire drinking process is crucial to fully understand how avian nectarivores feed; nectar-feeding not only involves the collection of nectar with the tongue, but also includes the mechanisms necessary to transfer and move the liquid through the bill and into the throat. We highlight the potential for modern technologies in comparative anatomy [such as microcomputed tomography (µCT) scanning] and biomechanics (such as tracking BaSO4-stained nectar via high-speed fluoroscopy) to elucidate how disparate clades have solved this biophysical puzzle through parallel, convergent or alternative solutions.
Asunto(s)
Conducta Alimentaria , Passeriformes , Animales , Fenómenos Biomecánicos , Néctar de las Plantas , Microtomografía por Rayos XRESUMEN
We investigated the functional morphology of lingual prey capture in the blue-tongued skink, Tiliqua scincoides, a lingual-feeding lizard nested deep within the family Scincidae, which is presumed to be dominated by jaw-feeding. We used kinematic analysis of high-speed video to characterize jaw and tongue movements during prey capture. Phylogenetically informed principal components analysis of tongue morphology showed that, compared to jaw-feeding scincids and lacertids, T. scincoides and another tongue-feeding scincid, Corucia zebrata, are distinct in ways suggesting an enhanced ability for hydrostatic shape change. Lingual feeding kinematics show substantial quantitative and qualitative variation among T. scincoides individuals. High-speed video analysis showed that T. scincoides uses significant hydrostatic elongation and deformation during protrusion, tongue-prey contact, and retraction. A key feature of lingual prey capture in T. scincoides is extensive hydrostatic deformation to increase the area of tongue-prey contact, presumably to maximize wet adhesion of the prey item. Adhesion is mechanically reinforced during tongue retraction through formation of a distinctive "saddle" in the foretongue that supports the prey item, reducing the risk of prey loss during retraction.
Asunto(s)
Lagartos/anatomía & histología , Lagartos/fisiología , Conducta Predatoria/fisiología , Lengua/anatomía & histología , Animales , Fenómenos Biomecánicos , Femenino , Masculino , Filogenia , Análisis de Componente Principal , Factores de Tiempo , Lengua/fisiologíaRESUMEN
We describe air-breathing mechanics in gray tree frog tadpoles (Hyla versicolor). We found that H. versicolor tadpoles breathe by 'bubble-sucking', a breathing mode typically employed by tadpoles too small to break the water's surface tension, in which a bubble is drawn into the buccal cavity and compressed into the lungs. In most tadpoles, bubble-sucking is replaced by breach breathing (breaking the surface to access air) at larger body sizes. In contrast, H. versicolor tadpoles bubble-suck throughout the larval period, despite reaching body sizes at which breaching is possible. Hyla versicolor tadpoles exhibit two bubble-sucking behaviors: 'single bubble-sucking', previously described in other tadpole species, is characterized by a single suction event followed by a compression phase to fill the lungs; 'double bubble-sucking' is a novel, apparently derived form of bubble-sucking that adds a second suction event. Hyla versicolor tadpoles transition from single bubble-sucking to double bubble-sucking at approximately 5.7â mm snout-vent length (SVL), which corresponds to a period of rapid lung maturation when they transition from low to high vascularization (6.0â mm SVL). Functional, behavioral and morphological evidence suggests that double bubble-sucking increases the efficiency of pulmonary gas exchange by separating expired, deoxygenated air from freshly inspired air to prevent mixing. Hyla versicolor, and possibly other hylid tadpoles, may have specialized for bubble-sucking in order to take advantage of this increased efficiency. Single and double bubble-sucking represent two- and four-stroke ventilation systems, which we discuss in the context of other anamniote air-breathing mechanisms.