Nectar feeding beyond the tongue: hummingbirds drink using phase-shifted bill opening, flexible tongue flaps and wringing at the tips

Abstract

Hummingbirds are the most speciose group of vertebrate nectarivores and exhibit striking bill variation in association with their floral food sources. To explicitly link comparative feeding biomechanics to hummingbird ecology, deciphering how they move nectar from the tongue to the throat is as important as understanding how this liquid is collected. We employed synced, orthogonally positioned, high-speed cameras to describe the bill movements, and backlight filming to track tongue and nectar displacements intraorally. We reveal that the tongue base plays a central role in fluid handling, and that the bill is neither just a passive vehicle taking the tongue inside the flower nor a static tube for the nectar to flow into the throat. Instead, we show that the bill is actually a dynamic device with an unexpected pattern of opening and closing of its tip and base. We describe three complementary mechanisms: (1) distal wringing: the tongue is wrung out as soon as it is retracted and upon protrusion, near the bill tip where the intraoral capacity is decreased when the bill tips are closed; (2) tongue raking: the nectar filling the intraoral cavity is moved mouthwards by the tongue base, leveraging flexible flaps, upon retraction; (3) basal expansion: as more nectar is released into the oral cavity, the bill base is open (phase-shifted from the tip opening), increasing the intraoral capacity to facilitate nectar flow towards the throat.

Macroevolutionary drivers of morphological disparity in the avian quadrate

“…and/or that the morphology and function of other areas of the head like the tongue (including the hyoid skeleton) and/or the upper and lower jaws are simply more closely linked to nectar feeding than the quadrate is [48]. These results echo recent studies that have demonstrated that, at broad phylogenetic scales, avian evolution is characterised by complex relationships between skeletal morphology and ecology.…”

Macroevolutionary drivers of morphological disparity in the avian quadrate

“…Many-to-one (different shapes associated with the same ecology) and oneto-many (similar shapes associated with disparate ecologies) relationships between quadrate morphology and function are apparent from our results (figures 3 and 4). For instance, nectarivory, a highly specialized feeding ecology, is represented in our dataset by several distantly related species which all 4b), perhaps reflecting different mechanisms of nectar feeding associated with distinct phylogenetic histories [49], and/or that the morphology and function of other areas of the head like the tongue (including the hyoid skeleton) and/or the upper and lower jaws are simply more closely linked to nectar feeding than the quadrate is [50]. These results echo recent studies that have demonstrated that, at broad phylogenetic scales, avian evolution is characterized by complex relationships between skeletal morphology and ecology.…”

“…For instance, nectarivory, a highly specialized feeding ecology, is represented in our dataset by several distantly related species which all exhibit highly divergent quadrate shapes (i.e. many-to-one relationship of morphology and function; figure 4 b ), perhaps reflecting different mechanisms of nectar feeding associated with distinct phylogenetic histories [ 49 ], and/or that the morphology and function of other areas of the head like the tongue (including the hyoid skeleton) and/or the upper and lower jaws are simply more closely linked to nectar feeding than the quadrate is [ 50 ]. These results echo recent studies that have demonstrated that, at broad phylogenetic scales, avian evolution is characterized by complex relationships between skeletal morphology and ecology.…”

El efecto de la concentración del néctar sobre las estrategias de forrajeo entre colibríes (Aves: Trochilidae) en bebederos artificiales

“…Las diferencias en el tiempo de consumo de estas especies pudieron también estar relacionadas con su comportamiento oportunista (Mendonca & Anjos 2005, Gómez-Rosas et al 2013, por medio del cual tratan de compensar el hecho que son frecuentemente atacadas por especies dominantes; por este motivo en los datos VIN, estas especies presentaron disminución en la proporción de visitas respecto a los datos sin competidores (VEL). Por el contrario, algunas especies de mayor tamaño corporal tendieron a visitar los bebederos durante más tiempo (e.g., hembras de A. nigricollis, machos de C. buffoni y C. delphinae), la duración de consumo mayor en algunas especies de pico largo pudo estar sujeta a que estos colibríes tardan más en trasportar el néctar en la sección intraoral, ya que el líquido atraviesa distancias superiores que en picos cortos (Rico-Guevara et al 2023). Entre las especies de mayor tamaño, A. nigricollis y las especies del género Colibri, se presentaron diferencias en el tiempo de visita y cantidad de tomas, esto ocurre entre competidores con requerimientos semejantes, pues la competencia es más intensa (Lyon 1976, Araújo-Silva & Bessa 2010 y resulta conveniente optar por diferentes estrategias de forrajeo.…”