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Língua Do Beija-Flor - Física Da Microbomba
Língua Do Beija-Flor - Física Da Microbomba
rspb.royalsocietypublishing.org micropumps
Alejandro Rico-Guevara1,3, Tai-Hsi Fan2 and Margaret A. Rubega1
1
Department of Ecology and Evolutionary Biology, and 2Department of Mechanical Engineering, University
of Connecticut, Storrs, CT 06269, USA
Research 3
Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá DC, Colombia
1. Introduction
Author for correspondence: Hummingbirds have remarkably high metabolic rates, amazing speed and
Alejandro Rico-Guevara superb aeronautic control. All these traits result from the ability of humming-
birds to feed on nectar efficiently enough to fuel an extreme lifestyle out of a
e-mail: a.rico@uconn.edu
sparse, but energetically dense, resource. Therefore, the way in which they
feed on nectar determines the peaks and span of their performance, and thus
their behaviour (and evolutionary trajectory), across a range of environmental
axes. Accordingly, the details of their feeding ecology and coevolution with
flowers have been the subject of intense study for over 40 years [1–6]. Half a
century’s worth of coevolutionary theory, as understood through humming-
birds as an example, depends on obtaining an empirical and mechanistic
understanding of the nectar collection process.
The hypothesis that capillarity moves the nectar inside hummingbird tongues
has been proposed as an inference arising from their anatomy (e.g. [7]) and fairly
limited in vivo experimental data [8]. The idea that capillarity is important in
nectar feeding is intuitively attractive and understandable, but lacks evidence
in extensive field investigations. The tongue of a hummingbird features paired
longitudinal grooves running from near the tip to mid-tongue (figure 1); these
grooves in their relaxed state resemble open cylinders, which is the reason
why meniscus-driven (capillarity) equations have been invoked. Capillarity
equations have been used to infer optimal concentrations in the nectar produced
by bird-pollinated plants [9–11], optimization in drinking behaviours of nectar-
feeding animals [12] and fluid transport optimality in a variety of natural and
Electronic supplementary material is available artificial systems [13]. However, during five years of high-speed filming of
free-living hummingbirds, we accrued the most comprehensive dataset of
at http://dx.doi.org/10.1098/rspb.2015.1014 or
tongue–nectar interactions reported to date, and both our qualitative and quan-
via http://rspb.royalsocietypublishing.org. titative analyses show that capillarity cannot account for either the tongue
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
(a) hummingbirds requires, therefore: (i) the existence, prior to fill- 2
ing, of an empty space in the tongue, (ii) an observable
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tongue meniscus, and (iii) that the capacity of the whole structure
nectar protrusion should remain constant throughout the process. Models [8]
propose that capillary suction fills the (i) empty space in the
collapsed (c) grooves in a hummingbird’s tongue by slightly closing the
tongue tongue walls while the (ii) meniscus is passing through. The
grooves only difference in expectation between this and capillarity
(b) occurring in small glass tubes is that the walls of hummingbird
tongue grooves are not static, but flexible, and the (iii) expec-
tation is that the capacity of the structure should decrease
cylindrical
nectar flow slightly as it zips up (i.e. the groove closes around the fluid
tongue grooves
3. Results
2. Mutually exclusive possibilities
Hummingbirds extract nectar from flowers by licking—they
(a) Capillarity is not biologically relevant to feeding
repetitively protrude their tongue (figure 1a), dip the tip into in wild hummingbirds
the pool of nectar inside a flower (figure 1b), and then retract Analysis of our videos demonstrates that capillarity is not oper-
the tongue. During protrusion, they use their bill tips to ating during tongue-filling in free-living hummingbirds. Our
squeeze the nectar off the tongue grooves inside the bill [14]. observations and measurements from 96 foraging bouts, com-
Consequently, as the tongue emerges, it is compressed along prising hundreds of licks, of 32 birds of 18 species (electronic
the grooves’ entire length [15]. Just exterior to the compression supplementary material, table S1) show that the tongue grooves
point (the bill tip), the grooves exhibit a collapsed configur- remained collapsed until the tongue tips contacted the nectar
ation (figure 1a). Once a given portion of the grooves passes surface (electronic supplementary material, video S1). After con-
the compression point, there are two possible, mutually exclu- tacting the surface, the grooves expanded and filled completely
sive, outcomes: (i) In the absence of the compression imposed with nectar (e.g. figure 2a). Formation of a meniscus within the
by the bill tip over the tongue, the grooves could recover their tongue grooves was almost never observed (see theoretical
shape, yielding two empty cylinders soon after the tongue versus experimental data section). This result is contrary to
emerges from the bill and before the tongue tips contact the requirements for capillary filling (tongue grooves contacting
nectar; or (ii) the grooves could remain collapsed while traver- the nectar surface as empty cylinders, and formation of a menis-
sing the air, either by the force at the compression point being cus). Furthermore, measured tongue thicknesses did not
transferred along the length of the tongue walls or by the thin conform to that predicted by capillarity filling the grooves;
layer of liquid remaining inside the flattened grooves acting as rather than decreasing (or remaining unchanged) as compared
an adhesive, or a combination of both. to before filling, tongue thickness increased (Student’s paired
The first scenario is compatible with the capillarity hypoth- t-test: p , 0.001, figure 2a, e.g. electronic supplementary
esis [7–9]. If the tongue grooves reshape after compression, material, videos S1 and S2). We calculated the percentage of
they will reach the nectar surface as two open cylinders groove expansion out of the final thickness of the groove. This
(figure 1c) and can fill via capillarity. Since the grooves are percentage ranged from 48 to 60% among species (electronic
open-sided, rather than complete cylinders, we expect that sur- supplementary material, table S1). All observed licks followed
face tension in the nectar will tend to ‘zip up’ the gap [8] as the the same pattern: tongue thickness was stable during protrusion
fluid rises into the grooves. Capillarity (or ‘capillary suction’ of the tongue, and rapidly increased after the tongue tips con-
sensu [8,9]) is a filling mechanism that operates in a tube or tacted the nectar (electronic supplementary material, video
tube-like structure and which requires that such a structure S2). After complete loading, the grooves filled with nectar
contain an empty space that can be filled by a moving were brought back inside the bill and squeezed for the next
meniscus. This process can be observed quite easily, and the cycle, all in less than a tenth of a second.
filling rate can be measured by tracking the moving meniscus. Summarizing and contrasting to the mutually exclusive
The expectation of a capillary process in the case of hypotheses outlined in the introduction, we found that:
(a) Based on our observations of the tongue –fluid interactions 3
in our videos, we offer here an alternative conceptual expla-
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nation, and a quantitative model (below), for the nectar
uptake mechanism in hummingbirds. We incorporate the
0 ms 6 ms
elastic recovering force on the grooves into a new nectar
flow model, which correctly predicts the empirical data
from feeding birds. The model, although with the limitations
of any first approximation, provides a replacement for the
10 ms 14 ms
capillarity equations that have been used to understand the
(b) energetics and ecology of hummingbird feeding [9 –11].
z=0 z = h(t) z=L We suggest that while squeezing nectar off the tongue
nectar in front position sealed end during protrusion, the bird is collapsing the grooves and
0.15
undocumented mechanism as ‘expansive filling’. The liquid
0.10
column has a progressive front within the tongue h(t)
0.05 nectar flow
(figure 2b). We modelled a single uptake event by a simpli-
0
0 2 4 6 8 10 fied tube configuration with a sealed end at the groove
distance z (mm) base (figure 2b), and deduced that the fluid motion and
uptake rate can be characterized by short- and long-time pro-
Figure 2. Expansive filling mechanism. (a) Video frames showing a lateral view cesses (figure 2c) based on the balance of inertial, elastic,
of an Amazilia hummingbird’s tongue being protruded and contacting dyed red viscous, and transmural pressure forces. The local effects of
nectar. The full filling of the grooves is completed in 14 ms. Scale bars gravity are negligible owing to the small dimension of
(white) ¼ 0.5 mm. (b) A schematic showing the gradually expanded tube the system. The fluid is assumed to be Newtonian and
(groove) profiles and the position of the fluid front to be compared with exper- incompressible in both short- and long-time processes.
imental data. During the nectar filling process, the groove is wider near the
liquid and thinner near the bill tip, the inverse of what would be expected
if capillarity were filling the groove. (c) Axi-symmetric modelling results show-
ing the transient profiles (apparent groove radius along its length) at 0.001, (c) Elastohydrodynamic model of expansive filling
0.01, 0.1 and 0.5 (black lines), and at 0.7, 1.0 and 2.0 (grey lines) times Considering a long-time quasi-steady and almost fully devel-
the characteristic time scale t ¼ 8mL2 =ðR2f EÞ, with the parameters described oped nectar flow in the elastic tube (groove) with a length
in the text. Black lines describe progressive wave-like behaviour, and grey lines of about 10– 13 mm and inner diameter of 0.3 –0.4 mm, the
show the diffusive recovery. (Online version in colour.) typical viscous incompressible fluid motion within a deform-
able tube is governed by a quasi-Poiseuille flow, which gives
(i) the tongue is, and remains, compressed prior to actual the local volumetric flow rate that is based on a linear
transport, and there is therefore no empty space within the relationship with the pressure gradient:
tongue available to fill via capillarity; (ii) there is no meniscus
_ pRðz, tL Þ4 @ pðz, tL Þ
during transport of fluid into the tongue; and (iii) tongue Qðz, tL Þ ≃ , ð3:1Þ
8m @z
volume increases during transport, in contradiction of all the
expectations for basic capillarity (e.g. no change in capacity) where tL indicates that this is a long-time process in which the
and the capillary suction model [8] (e.g. reduction in tongue inertia of the tube is neglected, the flow is approximately
volume). Thus, in free-living birds, feeding under realistic con- fully developed, and the elastic recovery of the tube is
ditions, no expectations of either the traditional or the capillary quasi-static, R is the apparent local radius of the tube, m is
suction model are met, thus we conclude that free-living birds dynamic viscosity, p is pressure, and the travelling distance
are not using capillarity. These results on their own refute the of the liquid column is defined by 0 z L, where L is the
idea that capillarity is an important component of the process tube length (much larger than the tube diameter). The flow
that occurs while hummingbirds drink nectar. rate and various apparent radii along the tube satisfy the
quasi-one-dimensional continuity equation:
@ Rðz, tL Þ2 @ Q
_
p þ ≃ 0: ð3:2Þ
(b) Novel fluid flow mechanism: a conceptual @ tL @z
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characteristic time and strength of the elastic recovery. terms of the transient velocity field vz, and the time depen-
Combining the above momentum, continuity and the elastic dency of the pressure field only comes from the
equations leads to a nonlinear diffusive pressure equation [16]: deformation of the boundary. The boundary conditions are
2 @ p finite velocity vz (0, z, t) along the axial line and the no-slip
@ p ER2f @ p
¼ þ1 , ð3:4Þ condition at the wall vz (R(z, tL), z, t) ¼ 0. The analytical
@ tL 8m @ z E @z
solution for the transient velocity field can be expressed as
originally proposed to simulate a collapsible blood vessel and X1 ð
t J0 ðbm r=Rf Þ R rJ0 ðbm r=Rf Þ~vz
other physiological scenarios [17–19]. The elasticity of, for vz ≃2 exp bm 22
2
dr,
m¼1
rRf =m J1 ðbm R=Rf Þ 0 R2
example, blood vessels determines the degree of compliance
of the tube wall due to the pressure drop; while in the ð3:6Þ
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10.9 120
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The fit of output from our first-order-only approximation observe the high licking rates that have been reported (up to
to our empirical measurements (figure 3) is satisfactory, and 17 Hz [15]). On the other hand, the elastic micropump we
provides support for our conceptual explanation of the micro- describe here allows for tongue loading at rates that are compa-
pumping mechanism. Figure 4 shows one of the sensitivity tible with previously reported licking rates. Thus, we conclude
tests we performed using various negative excess pressure that the capillary tongue-filling reported in laboratory studies
2pa and area modulus E values. Overall, a larger excess pressure (e.g. [8]) is the result of feeding under unnatural conditions,
results in higher peak velocity, while the time scale or width of and therefore is not representative of the processes operating
the profile is more affected when the E value is modified. Note in wild birds under biologically relevant conditions.
that the selection of the parameters pa and E is not arbitrary. Fluid trapping is the predominant process by which hum-
As mentioned earlier, the self-similar dynamics is featured by mingbirds achieve nectar collection at small bill tip-to-nectar
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feeder in order to reach the nectar. At real flowers, corolla length vide accurate measurements of the groove thickness at comparable
limits how close the bird can place the tip of its beak to the surface points (semilandmarks) across time, licks, individuals and species.
of the nectar pool. Controlling the position of the flat flower with For these comparative measurements, we used the semi-landmark
respect to the nectar reservoir, we achieved videos in which there no. 12 (near the middle of the grooves) and calculated the percen-
is enough realistic distance between the bill tip and the nectar sur- tage, out of the final thickness of the groove, that the expansion
face to study the filling of the tongue portions that never enter the represents (electronic supplementary material, table S1).
liquid (e.g. electronic supplementary material, video S4). To
improve visualization of the filling front, while filming Amazilia
hummingbirds (Amazilia amazilia) in Ecuador, we used humming-
bird nectar concentrate (Petcow), which comes tinted red, and we
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