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

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.

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.

Intrasexually selected weapons.

We propose a practical concept that distinguishes the particular kind of weaponry that has evolved to be used in combat between individuals of the same species and sex, which we term intrasexually selected weapons (ISWs). We present a treatise of ISWs in nature, aiming to understand their distinction and evolution from other secondary sex traits, including from 'sexually selected weapons', and from sexually dimorphic and monomorphic weaponry. We focus on the subset of secondary sex traits that are the result of same-sex combat, defined here as ISWs, provide not previously reported evolutionary patterns, and offer hypotheses to answer questions such as: why have only some species evolved weapons to fight for the opposite sex or breeding resources? We examined traits that seem to have evolved as ISWs in the entire animal phylogeny, restricting the classification of ISW to traits that are only present or enlarged in adults of one of the sexes, and are used as weapons during intrasexual fights. Because of the absence of behavioural data and, in many cases, lack of sexually discriminated series from juveniles to adults, we exclude the fossil record from this review. We merge morphological, ontogenetic, and behavioural information, and for the first time thoroughly review the tree of life to identify separate evolution of ISWs. We found that ISWs are only found in bilateral animals, appearing independently in nematodes, various groups of arthropods, and vertebrates. Our review sets a reference point to explore other taxa that we identify with potential ISWs for which behavioural or morphological studies are warranted. We establish that most ISWs come in pairs, are located in or near the head, are endo- or exoskeletal modifications, are overdeveloped structures compared with those found in females, are modified feeding structures and/or locomotor appendages, are most common in terrestrial taxa, are frequently used to guard females, territories, or both, and are also used in signalling displays to deter rivals and/or attract females. We also found that most taxa lack ISWs, that females of only a few species possess better-developed weapons than males, that the cases of independent evolution of ISWs are not evenly distributed across the phylogeny, and that animals possessing the most developed ISWs have non-hunting habits (e.g. herbivores) or are faunivores that prey on very small prey relative to their body size (e.g. insectivores). Bringing together perspectives from studies on a variety of taxa, we conceptualize that there are five ways in which a sexually dimorphic trait, apart from the primary sex traits, can be fixed: sexual selection, fecundity selection, parental role division, differential niche occupation between the sexes, and interference competition. We discuss these trends and the factors involved in the evolution of intrasexually selected weaponry in nature.