Hummingbird tongues are elastic
rspb.royalsocietypublishing.org
Research
Cite this article: Rico-Guevara A, Fan T-H,
Rubega MA. 2015 Hummingbird tongues are
elastic micropumps. Proc. R. Soc. B 282:
20151014.
http://dx.doi.org/10.1098/rspb.2015.1014
Received: 29 April 2015
Accepted: 27 July 2015
Subject Areas:
biophysics, biomechanics, behaviour
Keywords:
capillarity, feeding mechanism, fluid dynamics,
hummingbird foraging
Author for correspondence:
Alejandro Rico-Guevara
e-mail: a.rico@uconn.edu
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2015.1014 or
via http://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
3
Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá DC, Colombia
Pumping is a vital natural process, imitated by humans for thousands of
years. We demonstrate that a hitherto undocumented mechanism of fluid
transport pumps nectar onto the hummingbird tongue. Using high-speed
cameras, we filmed the tongue –fluid interaction in 18 hummingbird species,
from seven of the nine main hummingbird clades. During the offloading of
the nectar inside the bill, hummingbirds compress their tongues upon extru-
sion; the compressed tongue remains flattened until it contacts the nectar.
After contact with the nectar surface, the tongue reshapes filling entirely
with nectar; we did not observe the formation of menisci required for the
operation of capillarity during this process. We show that the tongue
works as an elastic micropump; fluid at the tip is driven into the tongue’s
grooves by forces resulting from re-expansion of a collapsed section. This
work falsifies the long-standing idea that capillarity is an important force fill-
ing hummingbird tongue grooves during nectar feeding. The expansive
filling mechanism we report in this paper recruits elastic recovery properties
of the groove walls to load nectar into the tongue an order of magnitude
faster than capillarity could. Such fast filling allows hummingbirds to extract
nectar at higher rates than predicted by capillarity-based foraging models, in
agreement with their fast licking rates.
1. Introduction
Hummingbirds have remarkably high metabolic rates, amazing speed and
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
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
artificial systems [13]. However, during five years of high-speed filming of
free-living hummingbirds, we accrued the most comprehensive dataset of
tongue–nectar interactions reported to date, and both our qualitative and quan-
titative analyses show that capillarity cannot account for either the tongue
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
 (a)
tongue
nectar protrusion
collapsed (c)
tongue
grooves
(b)
cylindrical
nectar flow
tongue grooves
Figure 1. The hummingbird tongue fills with nectar even when only the tip is
immersed. (a) Hummingbirds can drink from flowers with corollas longer than
their bills by extending their bifurcated, longitudinally grooved tongues to reach
the nectar. During protrusion, the tongue is compressed as it passes through
the bill tip, which results in a collapsed configuration of the grooves (cross-
section). (b) Upon reaching the nectar, the tongue tips fringed with lamellae
roll open and spread apart, but some of the grooved portions of the tongue will
never contact the nectar pool. For the grooves to fill with nectar, they must
return to their uncompressed, cylindrical configuration. (c) Coronal cutaway
from a mCT scan showing the bill and tongue architecture. Hummingbird
drawn by K. Hurme. (Online version in colour.)
dynamics, or for the rate at which nectar fills the grooves in
unmanipulated hummingbirds feeding in the wild.
2. Mutually exclusive possibilities
Hummingbirds extract nectar from flowers by licking—they
repetitively protrude their tongue (figure 1a), dip the tip into
the pool of nectar inside a flower (figure 1b), and then retract
the tongue. During protrusion, they use their bill tips to
squeeze the nectar off the tongue grooves inside the bill [14].
Consequently, as the tongue emerges, it is compressed along
the grooves’ entire length [15]. Just exterior to the compression
point (the bill tip), the grooves exhibit a collapsed configur-
ation (figure 1a). Once a given portion of the grooves passes
the compression point, there are two possible, mutually exclu-
sive, outcomes: (i) In the absence of the compression imposed
by the bill tip over the tongue, the grooves could recover their
shape, yielding two empty cylinders soon after the tongue
emerges from the bill and before the tongue tips contact the
nectar; or (ii) the grooves could remain collapsed while traver-
sing the air, either by the force at the compression point being
transferred along the length of the tongue walls or by the thin
layer of liquid remaining inside the flattened grooves acting as
an adhesive, or a combination of both.
The first scenario is compatible with the capillarity hypoth-
esis [7–9]. If the tongue grooves reshape after compression,
they will reach the nectar surface as two open cylinders
(figure 1c) and can fill via capillarity. Since the grooves are
open-sided, rather than complete cylinders, we expect that sur-
face tension in the nectar will tend to ‘zip up’ the gap [8] as the
fluid rises into the grooves. Capillarity (or ‘capillary suction’
sensu [8,9]) is a filling mechanism that operates in a tube or
tube-like structure and which requires that such a structure
contain an empty space that can be filled by a moving
meniscus. This process can be observed quite easily, and the
filling rate can be measured by tracking the moving meniscus.
The expectation of a capillary process in the case of
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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meniscus, and (iii) that the capacity of the whole structure
should remain constant throughout the process. Models [8]
propose that capillary suction fills the (i) empty space in the
grooves in a hummingbird’s tongue by slightly closing the
tongue walls while the (ii) meniscus is passing through. The
only difference in expectation between this and capillarity
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
slightly as it zips up (i.e. the groove closes around the fluid
Proc. R. Soc. B 282: 20151014
as the meniscus passes through). Thus, the capillarity hypoth-
esis predicts that the section of the tongue composed of the
grooves should decrease (or remain unchanged [9]) in thick-
ness after filling, as compared to before contact with the nectar.
Conversely, if tongue grooves remain flattened before filling,
then the condition of the tongue is incompatible with capillarity,
since the rise of nectar into the grooves through capillarity
requires that the grooves reshape into open cylinders before con-
tact with the nectar. If the tongue grooves remain flattened until
the tongue tip reaches the nectar surface, there is no empty cylin-
der and therefore no meniscus formation. In this scenario,
capillarity is precluded by the geometry of the flattened
tongue; if no menisci are formed, then capillarity equations
(which track the velocity of the meniscus) are not applicable.
3. Results
(a) Capillarity is not biologically relevant to feeding
in wild hummingbirds
Analysis of our videos demonstrates that capillarity is not oper-
ating during tongue-filling in free-living hummingbirds. Our
observations and measurements from 96 foraging bouts, com-
prising hundreds of licks, of 32 birds of 18 species (electronic
supplementary material, table S1) show that the tongue grooves
remained collapsed until the tongue tips contacted the nectar
surface (electronic supplementary material, video S1). After con-
tacting the surface, the grooves expanded and filled completely
with nectar (e.g. figure 2a). Formation of a meniscus within the
tongue grooves was almost never observed (see theoretical
versus experimental data section). This result is contrary to
requirements for capillary filling (tongue grooves contacting
the nectar surface as empty cylinders, and formation of a menis-
cus). Furthermore, measured tongue thicknesses did not
conform to that predicted by capillarity filling the grooves;
rather than decreasing (or remaining unchanged) as compared
to before filling, tongue thickness increased (Student’s paired
t-test: p , 0.001, figure 2a, e.g. electronic supplementary
material, videos S1 and S2). We calculated the percentage of
groove expansion out of the final thickness of the groove. This
percentage ranged from 48 to 60% among species (electronic
supplementary material, table S1). All observed licks followed
the same pattern: tongue thickness was stable during protrusion
of the tongue, and rapidly increased after the tongue tips con-
tacted the nectar (electronic supplementary material, video
S2). After complete loading, the grooves filled with nectar
were brought back inside the bill and squeezed for the next
cycle, all in less than a tenth of a second.
Summarizing and contrasting to the mutually exclusive
hypotheses outlined in the introduction, we found that:
 (a)
0 ms 6 ms
10 ms 14 ms
(b)
z=0 z = h(t) z=L
nectar in front position sealed end
Rf
(c)
0.25
apparent radius
0.20
R (mm)
0.15
0.10
0.05 nectar flow
0
0 2 4 6 8 10
distance z (mm)
Figure 2. Expansive filling mechanism. (a) Video frames showing a lateral view
of an Amazilia hummingbird’s tongue being protruded and contacting dyed red
nectar. The full filling of the grooves is completed in 14 ms. Scale bars
(white) ¼ 0.5 mm. (b) A schematic showing the gradually expanded tube
(groove) profiles and the position of the fluid front to be compared with exper-
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,
0.01, 0.1 and 0.5 (black lines), and at 0.7, 1.0 and 2.0 (grey lines) times
the characteristic time scale t ¼ 8mL2 =ðR2f EÞ, with the parameters described
in the text. Black lines describe progressive wave-like behaviour, and grey lines
show the diffusive recovery. (Online version in colour.)
(i) the tongue is, and remains, compressed prior to actual
transport, and there is therefore no empty space within the
tongue available to fill via capillarity; (ii) there is no meniscus
during transport of fluid into the tongue; and (iii) tongue
volume increases during transport, in contradiction of all the
expectations for basic capillarity (e.g. no change in capacity)
and the capillary suction model [8] (e.g. reduction in tongue
volume). Thus, in free-living birds, feeding under realistic con-
ditions, no expectations of either the traditional or the capillary
suction model are met, thus we conclude that free-living birds
are not using capillarity. These results on their own refute the
idea that capillarity is an important component of the process
that occurs while hummingbirds drink nectar.
(b) Novel fluid flow mechanism: a conceptual
explanation
Our results, drawn from an unprecedentedly large and
direct set of observations of the interaction of tongue and
nectar, contradict the capillarity hypothesis [7–9] of drinking
dynamics in hummingbirds. Some other process must
account for the movement of fluid into the tongue grooves.
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
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
capillarity equations that have been used to understand the
energetics and ecology of hummingbird feeding [9 –11].
We suggest that while squeezing nectar off the tongue
during protrusion, the bird is collapsing the grooves and
Proc. R. Soc. B 282: 20151014
loading elastic energy into the groove walls that will be
subsequently used to pump nectar into the grooves. The
collapsed configuration is conserved during the trip of the
tongue across the space between the bill tip to the nectar
pool. Once the tongue tips contact the nectar surface, the
supply of fluid allows the collapsed groove to gradually
recover to a relaxed cylindrical shape until the nectar has
filled it completely; hereafter, we refer to this previously
undocumented mechanism as ‘expansive filling’. The liquid
column has a progressive front within the tongue h(t)
(figure 2b). We modelled a single uptake event by a simpli-
fied tube configuration with a sealed end at the groove
base (figure 2b), and deduced that the fluid motion and
uptake rate can be characterized by short- and long-time pro-
cesses (figure 2c) based on the balance of inertial, elastic,
viscous, and transmural pressure forces. The local effects of
gravity are negligible owing to the small dimension of
the system. The fluid is assumed to be Newtonian and
incompressible in both short- and long-time processes.
(c) Elastohydrodynamic model of expansive filling
Considering a long-time quasi-steady and almost fully devel-
oped nectar flow in the elastic tube (groove) with a length
of about 10– 13 mm and inner diameter of 0.3 –0.4 mm, the
typical viscous incompressible fluid motion within a deform-
able tube is governed by a quasi-Poiseuille flow, which gives
the local volumetric flow rate that is based on a linear
relationship with the pressure gradient:
_ pRðz, tL Þ4 @ pðz, tL Þ
Qðz, tL Þ ≃  , ð3:1Þ
8m @z
where tL indicates that this is a long-time process in which the
inertia of the tube is neglected, the flow is approximately
fully developed, and the elastic recovery of the tube is
quasi-static, R is the apparent local radius of the tube, m is
dynamic viscosity, p is pressure, and the travelling distance
of the liquid column is defined by 0  z  L, where L is the
tube length (much larger than the tube diameter). The flow
rate and various apparent radii along the tube satisfy the
quasi-one-dimensional continuity equation:
@ Rðz, tL Þ2 @ Q
_
p þ ≃ 0: ð3:2Þ
@ tL @z
Similar to a pipetting effect, the negative excess pressure
is assumed proportional to the change of the apparent
cross-sectional area:
" #
Rðz, tL Þ2
pðz, tL Þ ¼ E 1 , ð3:3Þ
R2f
where Rf is the fully recovered tube radius and E is the appar-
ent area modulus of the tube. Both p and E influence the
characteristic time and strength of the elastic recovery.
Combining the above momentum, continuity and the elastic
equations leads to a nonlinear diffusive pressure equation [16]:
 2 @ p
@ p ER2f @  p
¼ þ1 , ð3:4Þ
@ tL 8m @ z E @z
originally proposed to simulate a collapsible blood vessel and
other physiological scenarios [17–19]. The elasticity of, for
example, blood vessels determines the degree of compliance
of the tube wall due to the pressure drop; while in the
tongue of hummingbirds, the elasticity of the groove walls
plays an active pumping role during the recovery of the col-
lapsed configuration. Accordingly, the characteristic length
and diffusive time scale are L and 8mL2 =ðR2f EÞ, respectively.
Here, we define an initial condition for the negative excess
pressure p (z, 0) ¼ 2pa, where pa is a positive constant repre-
senting the adhesive energy provided by the thin liquid film
remaining in the collapsed tube. It is assumed that the liquid
film inside the tongue can temporarily sustain the negative
pressure (tension) without cavitation. The boundary condition
at the inlet (z ¼ 0) has zero gauge pressure, while the pressure
gradient vanishes at the sealed end (z ¼ L). The diffusive
pressure field is featured by the relative contributions of nega-
tive excess pressure and area modulus, essentially the scaled
initial condition, 2pa/E. This is the only dimensionless par-
ameter that we use to estimate the self-similar empirical data
at various tube lengths.
At the very beginning of the process, because local accel-
eration is important when the fluid is suddenly drawn into
the tube while convective acceleration may be negligible
owing to the almost fully developed condition, the above
steady approximation is no longer valid in this short-time
regime. The elastic relaxation is considered fast and the
motion of the tube boundary is much slower than the accel-
erated momentum transport. We therefore decompose the
velocity field for the whole process into transient vz (r, z, t)
and quasi-steady ṽz (r, z, tL) contributions, which correspond
to the short- and long-time processes, respectively. Substitut-
ing the transient and a quasi-steady velocity components,
vz þ ṽz, respectively, into the linear momentum equation
and subtracting the long-time quasi-steady equation by
assuming that the pressure effect primarily balances the
long-time viscous effect, that is, 0  @ p=@ z þ ðm=rÞ@ =
@ rðr@ ~vz =@ rÞ, the quasi-linear transient flow in the short-
time regime can thus be simplified and expressed by the
diffusive momentum equation
 
@ vz m @ 2 vz 1 @ vz
≃ þ , ð3:5Þ
@t r @ r2 r @r
in which the pressure effect vanishes due to the balance with
the long-time viscous effect, and the radial velocity contri-
bution compared to the local acceleration, estimated by the
variation of tube radius DR/Rf, is neglected to facilitate the
analytical solution. This approximation is compatible with
the quasi-steady boundary condition for the radial motion
of the wall. Note that the trial solution of a transient pipe
flow (e.g. [16]) implies that the pressure gradient essentially
remains time-independent from the transient to quasi-
steady processes, and thus for equation (3.5) there is no
need to decompose the pressure to short- and long-time con-
tributions. The initial condition is vz (r, z, 0) ¼ 2 ṽz (r, z, 0). It
is expected that the pressure gradient does not play a role 4
in the first approximation of the local acceleration in
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terms of the transient velocity field vz, and the time depen-
dency of the pressure field only comes from the
deformation of the boundary. The boundary conditions are
finite velocity vz (0, z, t) along the axial line and the no-slip
condition at the wall vz (R(z, tL), z, t) ¼ 0. The analytical
solution for the transient velocity field can be expressed as
X1   ð
t J0 ðbm r=Rf Þ R rJ0 ðbm r=Rf Þ~vz
vz ≃2 exp bm 22
2
dr,
m¼1
rRf =m J1 ðbm R=Rf Þ 0 R2
ð3:6Þ
Proc. R. Soc. B 282: 20151014
where J0 and J1 are the zeroth and first-order Bessel functions,
respectively, and bm are the eigenvalues given by the no-slip
condition J0(bmR/Rf ) ¼ 0. As a correction for the leading-
order approximation, the initial condition in the integral
term here is given by the long-time velocity from the pressure
equation
1 @ pðz, tL Þ 2
~vz ðr, z, t ¼ tL Þ ≃ ½r  R2 ðz, t ¼ tL Þ: ð3:7Þ
4m @ z
Finally, the complete velocity is the summation of both
transient and quasi-steady components, vz þ ṽz. The local
flow rate can also be obtained from the apparent radius
and pressure gradient. Equation (3.7) is obtained by direct
integration of the Stokes equation twice with respect to r,
which preserves the time dependency that comes from the
deformation of the boundary. In this case, the nonlinear
pressure equation is solved numerically before substituting
into the integral solution for the velocity field. Once the
velocity of the progressive moving front of the liquid
column relative to the tongue is computed, the travelling dis-
tance or the filling length can be tracked by a simple
Lagrangian integration. Note that the linear approximation
here is aimed to accommodate the essential multi-scale be-
haviour analytically. Perturbative or numerical computation
of the full momentum equation, specifically the nonlinear
radial velocity contribution in the short-time regime, would
be helpful to justify this approximation.
(d) Theoretical versus experimental data
In order to evaluate our model, we compared the model
output against our empirical results from actual feeding
birds, using the following model parameters: Rf ≃ 0:2 mm,
m ≃ 0:00181 Pa s, r ≃ 1080 kg m3 , pa ¼ 3.3 kPa, E ¼ 4 kPa,
and four tube lengths from 10 to 13.4 mm based on exper-
imental measurements. The self-similar dynamics is
featured by the ratio pa/E, in which pa controls the pump
strength or the peak value of front velocity, while E adjusts
the filling time (figure 3). The ratio and both parameters
are our best-effort selections based on sensitivity tests (e.g.
figure 4) applied to all datasets. The short time scale is on
the order of 1 ms, while the long time scale is about 10 –
20 ms. The Reynolds number is up to an order of 100 at the
peak velocity. The results show a sub-linear increase of the
observable front velocity (figure 3a) and a super-linear increase
of the filling length (equivalent to the front position h(t),
figure 3b). The filling length / tn and filling velocity / tn21,
where 1.0 , n , 1.5, indicate that the inertial force on the
fluid drawn from the nectar pool is more significant than
the result obtained from the inertia-dominated capillarity rise
model [21], where n ¼ 1, and of course than the quasi-steady
 (a) L (mm)
10.0
10.9
11.9
13.4
(b) 14 theoretical and experimental
expansive filling
12
10
filling length (mm)
8 pressure 2pa and area modulus E. The lines are predictions from our elasto-
Bosanquet’s zero
6 contact angle
capillary filling
4
2 experimental
capillary filling
0
0 5 10 15 20
filling time (ms)
Figure 3. Theoretical and experimental data for the filling mechanisms in
hummingbird tongues. (a) Transient velocity of the travelling liquid front
versus time. Data points (black symbols) denote expansive filling data from
four drinking sequences of free-living birds, exemplifying different filling
tube lengths (mm). Lines (black) are predictions from our elastohydrodynamic
model. (b) Transient filling length h versus time at the same tube lengths
shown above. Bosanquet’s [20] capillary model curve corresponds to theoretical
capillary filling, that takes inertial effect into consideration, under a zero contact
angle condition (complete wetting). All parameters used in Bosanquet’s model,
including fluid properties and relaxed tube size, follow the expansive filling
model except that the length of the tube is irrelevant for Bosanquet’s
result. Experimental capillary filling data points (circles at the bottom) represent
our only observation of capillarity, from only one side of the tongue, in a single
lick (electronic supplementary material, video S3). Vertical bars correspond to
95% confidence intervals (CIs) from five repeated measurements of each filling
event. (Online version in colour.)
case, where n ¼ 0.5 based on the Lucas–Washburn model [22].
The duration for the transition from super-linear to sub-linear
increase of the filling length is relatively long compared with
the short time scale; this is perhaps why others have been
led to believe that capillarity (n ¼ 1) is the primary driving
mechanism. This is understandable because capillarity, regard-
less of the contact angle, provides a pulling force very similar
to a pressure drop across the liquid column. However,
comparing with the Bosanquet’s capillary model [20] that
takes inertial effect into account (figure 3b), even under the
largest effective surface tension force, based on contact
angle of zero, the capillarity model cannot match our
fast empirical filling data. Note that Bosanquet’s capillary
model considers the balance of pressure, capillarity, inertial
and viscous effects. The transient equation, initial condi-
tions and the solution for the capillary rise h(t) can be
_
expressed as dðhhÞ=dt _ ¼ B, h(0) ¼ 0 and hhð0Þ
þ AðhhÞ _ ¼ 0,
pa 3.30 kPa, E 4.0 kPa 5
140
140
pa 2.75 kPa, E 4.0 kPa
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120
front velocity (cm s–1)
120
front velocity (cm s–1)
pa 2.75 kPa, E 3.0 kPa
100 100
pa 2.50 kPa, E 3.0 kPa
80 80 experimental data,
60 10 mm filling length
60
40 40
20
20
0
Proc. R. Soc. B 282: 20151014
0 5 10 15 20 25
filling time (ms)
Figure 4. Sensitivity tests for the elastohydrodynamic model of the filling
mechanism in hummingbird tongues. The graph represents the comparison
of calculated front velocity versus time based on various negative excess
hydrodynamic model, and the data points are experimental results for L ¼
10 mm. Vertical bars correspond to 95% CIs from five repeated measurements.
pffiffiffiffiffiffiffiffiffiffiffiffipffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
and hðtÞ ¼ 2B=A t  ð1  eAt Þ=A, respectively, where
A ¼ 8m/rR 2 and B ¼ (2gcosu/R þ p0)/r, and all parameters
involved follow their typical definitions. The gravity effect is
25 neglected in Bosanquet’s analytical result.
In hundreds of licks studied, we observed capillarity only
once and acting in only a single tongue groove (electronic
supplementary material, video S3). In this event, at the initial
stages of tongue protrusion, one of the groove tips adhered to
the feeder wall before the tip reached the surface of the nectar
pool, and the stuck groove tip bent as the tongue continued
to move forward. We surmise that the bending caused the
groove to lose its collapsed configuration and recover its
cylindrical, empty, shape when still outside the nectar.
Before the tongue contacted the liquid surface, the groove
tip slid forward and entered the nectar unbent. Thanks to
this unusual accident, we captured one of the two grooves
being filled by expansive filling (as usual), while the other
was being filled by capillarity, offering a fortuitous opportu-
nity to directly compare the two mechanisms. Our measured
capillary filling rate (circles at the bottom, figure 3b) is an
order of magnitude slower than expansive filling when all
other factors are equal; therefore, capillarity cannot be the
nectar uptake mechanism observed in all the other licks.
Figure 3a shows the front velocity at r ¼ 0 and z ¼ h(t); in
the short time regime, the elastic force overcomes the inertial
effect to pull the nectar into the tube, while at the long time
regime, the elasticity-induced negative excess pressure bal-
ances the fluid viscous effect. The first transition appears at
the peak velocity on the order of 1 m s21, and then decays
as the diffusive pressure wave travels along the tube length
(figure 2c). The second transition that is evident in the mod-
elling results is when the pressure wave reaches the sealed
end of the tube, and the tube profiles diffusively relax to an
equilibrium shape. Considering the case of L ¼ 10 mm, at
the decaying stage, the velocity changes its slope at around
6–7 ms. Because the characteristic time scale t ¼ 8mL 2/
(R2f E)  9 ms, the profile shown in figure 2c at 0.7t  6 –
7 ms explains that such a transition appears when the
dynamic cross-sectional tube profiles transit from wave-like
to diffusive-like behaviours. The various capillarity models
that have been applied to hummingbird feeding are not
able to describe the observed short- to long-time behaviours
and the interesting dynamics at both transitions.
The fit of output from our first-order-only approximation
to our empirical measurements (figure 3) is satisfactory, and
provides support for our conceptual explanation of the micro-
pumping mechanism. Figure 4 shows one of the sensitivity
tests we performed using various negative excess pressure
2pa and area modulus E values. Overall, a larger excess pressure
results in higher peak velocity, while the time scale or width of
the profile is more affected when the E value is modified. Note
that the selection of the parameters pa and E is not arbitrary.
As mentioned earlier, the self-similar dynamics is featured by
the relative contributions of negative excess pressure and area
modulus 2pa/E as the only characteristic number in this
model. Our best fit of pa/E is about 0.83, corresponding to two
cases: pa ¼ 3.3, E ¼ 4.0 that better predicts the peak value of
the front velocity, and pa ¼ 2.5, E ¼ 3.0 that fit better to
the long-time profile. Another two cases with smaller or larger
pa/E value, about 0.69 and 0.92 are not good selections. We
thus choose pa ¼ 3.3, E ¼ 4.0 for all cases in figure 3 to empha-
size the maximum front velocity. The prediction for the long-
time behaviour may be improved by gradually reducing the
thickness of the tube towards the end (taking into account that
hummingbird tongue grooves taper off towards the base).
4. Discussion
Our dataset of direct measurements of tongue/nectar inter-
actions during nectar uptake in free-living wild birds refutes
the century-old paradigm that posits capillary rise as the
main mechanism operating during hummingbird drinking.
Capillary rise is physically possible in hummingbird tongues,
but, in the wild, it simply is not biologically relevant.
Combining the elastohydrodynamic model we present
here with our previous work on the mechanics of fluid trap-
ping at the tongue tips [14], we now have an empirically
supported, mechanistic understanding of nectar intake in
hummingbirds with which to newly interpret their energetics
and ecology. It is noteworthy that at flowers where full
groove immersion is prohibited by corolla length, filling
lengths are usually equivalent to the distances between the
bill tip and the nectar surface. Given that it is only at great fill-
ing lengths (when the bill tip is far from the nectar surface
and full groove immersion is precluded) that a tongue-filling
mechanism besides nectar trapping at the groove tips [14]
would contribute a significant portion of the total load per
lick, we rule out capillarity as an important drinking mechan-
ism in free-living birds feeding at real flowers.
The average flow rate, a measure of interest for ecology and
engineering applications, would be calculated as the volume of
liquid collected per unit time. Given that the end result of both
capillarity and expansive filling is a tongue groove entirely filled
with nectar, the volume would be exactly the same under the
two scenarios. However, a groove would be filled appreciably
slower via capillarity (e.g. figure 3; electronic supplementary
material, video S3). The slow fill speed of capillarity would
therefore limit the hummingbird’s licking rate, and thus their
energy intake rate. This is manifest in the time interval for the
one full lick cycle reported elsewhere as the result of capillarity
[8]: 200 ms, which translates into a licking rate of only 5 Hz.
This is very low when compared to the licking rates registered
for larger samples of birds, under more realistic conditions,
which are around 14 Hz [23]. If the tongue normally worked 6
via capillarity in free-living hummingbirds, we would not
rspb.royalsocietypublishing.org
observe the high licking rates that have been reported (up to
17 Hz [15]). On the other hand, the elastic micropump we
describe here allows for tongue loading at rates that are compa-
tible with previously reported licking rates. Thus, we conclude
that the capillary tongue-filling reported in laboratory studies
(e.g. [8]) is the result of feeding under unnatural conditions,
and therefore is not representative of the processes operating
in wild birds under biologically relevant conditions.
Fluid trapping is the predominant process by which hum-
mingbirds achieve nectar collection at small bill tip-to-nectar
Proc. R. Soc. B 282: 20151014
distances, wherein tongue grooves are wholly immersed in
nectar, or when the nectar is found in very thin layers [14].
Expansive filling accounts for nectar uptake by the portions of
a hummingbird’s tongue that remain outside the nectar pool.
The relative contributions of the two synergistic mechanisms
(fluid trapping and expansive filling) to the rate and volume
of nectar ultimately ingested are determined by the distance
from the bill tip to the nectar surface during the licking process.
Updating feeding efficiency estimates in light of these advances
could provide new insights critical to current evolutionary
debates (e.g. optimal nectar concentrations [9,11,24,25]). In
addition it could also improve our understanding of broad-
scale ecological patterns (e.g. species range limits and compe-
tition in hummingbird assemblages [6], and phenological
shifts with conservation implications [26]).
A reappraisal of preference experiments along gradients of
nectar concentrations [27–32] using these new nectar intake
models and applying recent advances on gustatory discrimi-
nation [33], could shed new light on coevolutionary enigmas.
Several plant lineages have converged on a transition from an
insect-pollinated condition to vertebrate-pollination [34–37],
and vertebrate-pollinated flowers tend to have more dilute
nectars than the insect-pollinated ones [24,38–40]. The new
explanation of the mechanics of nectar uptake we provide
here suggests that physical constraints are the main determi-
nants of the relationship between pollinator type and nectar
concentration, and can guide us through alternative hypoth-
eses [40] of hummingbird–flower coevolution. Our discovery
of this elastic tongue micropump could inspire applications,
and the study of flow, in elastic-walled (flexible) tubes in
both biological [41,42] and artificial [43–46] systems.
5. Methods
(a) Fieldwork
At field sites with existing feeders in seven countries throughout the
Americas, we filmed free-living, never handled, hummingbirds
drinking at modified transparent feeders simulating the nectar
volumes and concentrations of hummingbird-pollinated flowers.
We measured 96 foraging bouts of 32 focal birds belonging to
18 species from seven out of the nine main hummingbird clades
(electronic supplementary material, table S1). We used artificial
nectar (18.6% mass/mass sucrose concentration) and focused on
recording the tongue–fluid interaction using high-speed cameras
(TroubleShooter HR and Phantom Miro ex4) with macro lenses
(Nikon 105 mm f/2.8 VR) running up to 1260 frames per second
(1280  512 pixels). We positioned red flat plastic sheets (to mini-
mize lateral view obstruction) cut in flower shapes at the
entrances of the feeders. The purpose of the flat flowers was two-
fold: to attract and guide wild hummingbirds into our feeders,
and to allow us to control the relative position of the artificial corolla
entrance with respect to the nectar chamber. While filming wild (complete filling), using a two-tailed Student’s paired t-test, after 7
hummingbirds, we noted that every individual, after a couple of testing for normality through a Shapiro–Wilk test. Having good
exploratory visits, would insert its beak as far as possible into the estimates of the position of groove tip and base is important to pro-

feeder in order to reach the nectar. At real flowers, corolla length
limits how close the bird can place the tip of its beak to the surface
of the nectar pool. Controlling the position of the flat flower with
respect to the nectar reservoir, we achieved videos in which there
is enough realistic distance between the bill tip and the nectar sur-
face to study the filling of the tongue portions that never enter the
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
rspb.royalsocietypublishing.org
vide accurate measurements of the groove thickness at comparable
points (semilandmarks) across time, licks, individuals and species.
For these comparative measurements, we used the semi-landmark
no. 12 (near the middle of the grooves) and calculated the percen-
tage, out of the final thickness of the groove, that the expansion
represents (electronic supplementary material, table S1).

Proc. R. Soc. B 282: 20151014

diluted it (down to 18.6% mass/mass concentration).
(b) Velocity and thickness measurements
We limited our measurements to the instances in which we could
confidently track the tongue tip and the groove bases throughout
the entire lick. We calculated tongue tip velocity through time
and estimated fluid displacement velocities using IMAGEJ [47]. To
measure groove thickness at regular length intervals, we delineated
the contour of the tongue in TPSDIG 2.16 [48]. Subsequently, we lim-
ited these outlines between the tip and the base of the grooves and
resampled dorsal and ventral outlines into 20 semi-landmarks
[49,50]. These semi-landmarks allowed us to calculate groove thick-
ness at equally spaced points along the tongue through the licking
cycle, and to quantitatively test predictions from the mutually
exclusive possible outcomes. We tested whether there was a differ-
ence in groove thickness before and after contact with the nectar
Ethics. All filming activities were reviewed and authorized by the
Institutional Animal Care and Use Committee at the University of
Connecticut; Exemption Number E09-010.
Authors’ contributions. A.R.-G. and M.A.R. conceived the project and
designed the experiments. T.-H.F. performed the fluid dynamics
simulations and mathematical modelling. A.R.-G. conducted the
experiments and analysed the data. All authors discussed results
and commented on manuscript.
Competing interests. We declare we have no competing interests.
Funding. A.R.-G. was funded by: UConn EEB Department, CESE, Amer-
ican Ornithologists’ Union, Sigma-Xi and NSF IOS- DDIG 1311443,
and T.-H.F. acknowledges the support from NSF CMMI-0952646.
Acknowledgements. We thank D. Sustaita, C. Elphick, R. Colwell,
K. Schwenk, C. Field, K. Hurme, E. Hurme, H. Brown and the
UConn Ornithological Research Group for feedback. We are grateful
to C. Clark, and D. Altshuler for the loan of high-speed cameras and
logistic support. Finally, we thank L. Rico, A. Morales, L. Cárdenas
and O. Acevedo for fieldwork assistance.

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