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One way in which secondary sexual traits can influence differential reproductive success is by playing a key role in the outcome of direct physical contests for mates. Here we describe an undocumented trait in a species of hummingbird with a lek mating system, the Long-billed hermit (LBH, Phaethornis longirostris). The trait under consideration is a dagger-like structure at the bill tip, which we hypothesize is a secondary sexual trait that functions as a sexually dimorphic weapon. We tested our hypothesis by examining 5 leks during 4 consecutive years, and by employing morphological analyses, performance experiments, and behavioral observations. We found that 1) adult male bill tips were longer and pointier than their counterparts in females and juvenile males, 2) juvenile males acquired dagger-like tips during their transition to adulthood, 3) variation in bill tip morphology reflected puncture capability, and 4) males with larger and pointier bill tips were more successful in achieving lek territory tenure. Our study provides the first evidence of sexually dimorphic weapons in bird bills and stands as one of the few examples of male weaponry in birds. Our results suggest a role of sexual selection on the evolution of overall bill morphology, an alternative hypothesis to the prevailing “ecological causation” explanation for bill sexual dimorphism in hummingbirds.
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Original Article
Bills as daggers? Atest for sexually dimorphic
weapons in a lekking hummingbird
AlejandroRico-Guevaraa and MarceloAraya-Salasb
aDepartment of Ecology and Evolutionary Biology, University of Connecticut, 75 N Eagleville Rd.
U-3043, Storrs, CT 06269, USA; bDepartment of Biology, New Mexico State University, Foster Hall,
MSC 3AF, Las Cruces, NM 88003, USA
Received 13 May 2014; revised 1 September 2014; accepted 11 September 2014; Advance Access publication 18 October 2014.
One way in which secondary sexual traits can influence differential reproductive success is by playing a key role in the outcome of
direct physical contests for mates. Here we describe an undocumented trait in a species of hummingbird with a lek mating system,
the Long-billed hermit (LBH, Phaethornis longirostris). The trait under consideration is a dagger-like structure at the bill tip, which
we hypothesize is a secondary sexual trait that functions as a sexually dimorphic weapon. We tested our hypothesis by examin-
ing 5 leks during 4 consecutive years, and by employing morphological analyses, performance experiments, and behavioral observa-
tions. We found that 1)adult male bill tips were longer and pointier than their counterparts in females and juvenile males, 2)juvenile
males acquired dagger-like tips during their transition to adulthood, 3)variation in bill tip morphology reflected puncture capability, and
4)males with larger and pointier bill tips were more successful in achieving lek territory tenure. Our study provides the first evidence
of sexually dimorphic weapons in bird bills and stands as one of the few examples of male weaponry in birds. Our results suggest a
role of sexual selection on the evolution of overall bill morphology, an alternative hypothesis to the prevailing “ecological causation”
explanation for bill sexual dimorphism in hummingbirds.
Key words: animal weaponry, bill morphology, ecological causation, intrasexual competition, male combat, secondary sexual
traits, sexual dimorphism, trochilidae.
Secondary sexual traits are usually selected for through mate choice,
for example, ornaments (Endler 1990), or intrasexual competition,
for example, weapons (Emlen 2008). Here we describe a previously
unnoticed bill trait in a lekking species, the long-billed hermit (P.lon-
girostris, Figure 1, Supplementary Movie A1), and test if this trait
is a secondary sexual one and if it could be considered a sexually
dimorphic weapon. In order to consider a given feature as a second-
ary sexual trait, it has to: 1)be present or enlarged (relative to body
size) in members of one of the sexes, usually in males (Andersson
1994), and 2)appear or become enlarged during puberty (Radford
and du Plessis 2004). In order to establish the conditions under
which to consider a trait a sexually dimorphic weapon, we first
need to point out that in general terms, sexually dimorphic weap-
onry in animals has evolved through sexual selection in the form of
intraspecific fighting (e.g., male-male combat; Emlen 2008). Under
this framework, sexual dierences that have evolved to provide an
advantage during a battle, and ultimately act to influence fitness
(through enhanced mating opportunities), could be considered part
of that organism’s sexually dimorphic weaponry. Sometimes a trait
that has not evolved specifically for fighting can show strong sexual
dimorphism, for example, elongated and stronger arms in male
Kangaroos (Warburton etal. 2013), or larger male canine teeth in
some primates (Leigh etal. 2008; Plavcan 2012). In this case, it is
the dierence in muscle mass and/or bone structure rather than the
presence of the trait itself (arms or teeth) that makes these examples
of sexually dimorphic weapons. To formalize this notion, we con-
sider sexually dimorphic weapons to be structures that are 1)used to
inflict damage during intrasexual agonistic encounters (Andersson
1994), and 2) traits that increase dominance and subsequently the
bearer’s mating success (Darwin 1871; Székely etal. 2000).
Here, we describe a needle-shaped bill tip in long-billed her-
mits (P. longirostris), a type of structure never before reported in
birds. Sexual dimorphism in bill tip morphology of few species
of hummingbirds has been known for a long time (Ramphodon,
Androdon and Glaucis: Salvin 1892), but in those cases the males
have hooked bill tips. For Phaethornis, or any other hummingbird,
the dagger-shaped bill tip has not been reported (cf. Delattre 1843;
Address correspondence to A.Rico-Guevara. E-mail:
A. Rico-Guevara and M.Araya-Salas contributed equally to this paper.
Editor’s choice
Behavioral Ecology (2015), 26(1), 21–29. doi:10.1093/beheco/aru182
Behavioral Ecology
Salvin 1892; Hinkelmann 1996; Hinkelmann and Schuchmann
1997; Hinkelmann and van den Elzen 2002; Piacentini 2011).
We assessed the variation in bill morphology and functional per-
formance (puncture capability) of the bill tip among adult males,
adult females, and juveniles. Since P. longirostris is a lek-breeding
hummingbird, we examined the relationship between male bill tip
morphology, puncture capability, and their ability to defend a ter-
ritory in the lek. Among territorial males, there is still controversy
over whether females prefer males in central territories to males
in peripheral ones (Apollonio et al. 1992) or show no such pref-
erence (Clutton-Brock etal. 1989). Nonetheless, it is clear that in
species in which a lekking system has evolved, males holding lek
territories will have a reproductive advantage over males incapable
of holding territories (Balmford et al. 1992; Andersson 1994) in
the absence of alternative reproductive strategies, that is, sneaker
males (Sinervo and Zamudio 2001). In fact, in lek-breeding spe-
cies, 10–20% of the males often obtain 70–80% of the mating
events (Wiley 1991). In lekking hummingbirds, territory tenure
gives priority or exclusive access to females (e.g., Stiles and Wolf
To test our hypothesis that the structure described here is a sec-
ondary sexual trait and a sexually dimorphic weapon, we evalu-
ated 4 specific predictions: 1) the trait is more developed or only
present in male hummingbirds; 2)it becomes enlarged and better
developed (pointier bill tips) when juvenile males reach adulthood;
3)males with enlarged and pointier bill tips have a potential fight-
ing advantage, in the form of enhanced puncture capability; and
4)males with enlarged and pointier bill tips are more successful in
defending lek territories.
Behavioral observations
Fieldwork was carried out at 5 long-billed hermit leks at La
Selva Biological Station, Costa Rica during the breeding seasons
(~December–August) from 2009 to 2012 (for details of the lek sites
see Araya-Salas and Wright 2013). To perform focal sampling, we
individually marked males capturing birds in the lek and surround-
ing areas (including feeding territories), determining the sex via dis-
criminant function analysis, and attaching color-coded back-tags.
We captured birds using standard 6 and 12 m mist nets (19 mm
mesh size), and ringed all captured hummingbirds with numbered
bands. Long-billed hermits do not exhibit obvious plumage sexual
dimorphism, but individuals can be sexed by a discriminant func-
tion analysis on standard measurements (Stiles and Wolf 1979).
We used a cross-validation discriminant function analysis by creat-
ing several functions using published morphological data for 204
individuals of this species (Stiles and Wolf 1979), and selecting the
function that provided the best classification of sexes (>90% for
each sex); which included wing chord length (flattened), bill length
(exposed culmen), and body mass. Stiles and Wolf (1979) only pro-
vided sample size, mean and standard deviation for each of the
measurements mentioned above. Thus, for each sex we created 100
normally distributed cases using the mean, variation and sample
size reported by Stiles and Wolf (1979) to generate the dataset for
the discriminant function analysis. When applied to an independent
dataset from specimens at the Museum of Zoology of Universidad
de Costa Rica 100% of females (N=5) and 77% of males (N=13)
were correctly classified. In the field, we measured bill and right
tarsus lengths, flattened wing chord length, and body mass using
a digital caliper (±0.005 mm), a stopped wing ruler (±0.1 mm),
and a digital scale (±0.01 g). Individuals classified as males in the
field by the discriminant function analysis (using a field laptop)
were marked with plastic stripes that had unique 3-color combina-
tions attached to the back of the bird with nontoxic eyelash glue,
LashGrip-Ardell® (Stiles and Wolf 1973; Baltosser 1978; González
and Ornelas 2009; Kapoor2012).
We observed marked individuals at leks using binoculars (and
video cameras when possible) from 5:00 to 11:00 h and from 14:00
to 17:00 h, encompassing the previously reported peaks of activ-
ity for this species (Stiles and Wolf 1979). We used focal observa-
tions and territory mapping to ensure that all males in a lek were
sampled in a given period and the status of the males was correctly
assessed (territorial vs. floater). We identified adult males as “ter-
ritorial” when they defended a set of perches at the lek and sang
from them during the observation period (>5days per male in all
cases). Conversely, we identified individuals as non-territorial lek-
king males or “floaters” when they were observed at least 2 times
within the lek during a single season, but were unable to defend
perches from other males. These floaters were seen intermittently
on perches defended by other males but were always displaced from
them (>5days per male), that is, they did not hold territories. We
confidently classified these males as floaters since we did not observe
them holding a territory in any lek. Perches of singing males were
mapped using a 20 × 20 m grid system as reference. Then, a map
of lek territories based on an initial observation period was used
to identify areas for further intensive netting and observations until
we marked and mapped all territorial males on each lek. Aperch
was considered to belong to a given male’s territory when it was
repeatedly and successfully defended during the observation period
(>5days per male). We measured the distance (using a rangefinder)
Long-billed hermit (P.longirostris). Photo by M. Aliaga.
Rico-Guevara and Araya-Salas • Hummingbird bills as daggers
and angle of the perches to the closest landmark. Perch locations
were plotted using ArcGIS 9.3 creating a minimum convex poly-
gon (Zach and Falls 1979; Smith and Shugart 1987)describing the
shape, size and location of each territory.
Morphological analyses
We made a photographic catalogue of the lateral view of bills
(e.g., Supplementary Figure A1a) and bill tips including all the
hummingbirds captured. Bill tip pictures were taken by coupling
a digital camera (Nikon D5100) to a field dissecting microscope
(30× magnification) with a built-in scale and millimeter paper
background (Supplementary Figure A1b). Using these field macro-
photographs, we measured bill tip length as the extension of the
maxillary rhamphotheca (keratinous covering of the maxilla) tip
beyond the mandibular rhamphotheca tip in lateral view. This is
a conservative estimate, given that both maxillary and mandibular
tips seem to be elongated and pointier in adult males. However, we
limited our analyses to the maxillary tip because as it extends past
the mandibular tip, it would be the first point of contact if the bill
were used as a weapon. We assessed the reliability of bill tip elonga-
tion measurements by comparing the length obtained from lateral
and ventral photos from the same individual using linear regres-
sions. We also determined the relationship between the discrimi-
nant function scores used to sex individuals and bill tip elongation
using linear regressions. Ahigh correlation between bill tip length
and discriminant scores would have rendered the comparison of
bill tip elongation between the sexes redundant.
We outlined the contour of the most distal 2 mm of the bill tip
from lateral photos using the program tpsDig version 2.16 (Rohlf
2010). We subsampled the outline of the bill tip obtaining 50 semi-
landmarks (Bookstein 1997; details in Mitteroecker and Gunz 2009),
which were used to evaluate pointiness. To do this, we calculated the
area of dierent sections of the bill tip using the package PBS map-
ping in R (R Development Core Team 2013). Pointier objects, from
a bi-dimensional perspective, have a smaller area in the tip when
compared to a section of similar length in the base of the object.
Hence, we defined our pointiness index as the ratio of the area
enclosed by the distal 20 semi-landmarks to the area of the basal
20 semi-landmarks, from our 2-millimeter long tip outline. We sub-
tracted these values from 1 in order to match higher pointiness to
higher index values. Lastly, we evaluated dierences in bill tip length
and pointiness between sexes and age classes. In the field, humming-
birds were aged based on bill characteristics: juveniles have clear dis-
tinguishable corrugations covering a large extent of the maxillary
rhamphotheca (upper bill), whereas adult males show corrugations
in less than 10% of the upper bill, near its base (Ortiz-Crespo1972).
To examine dierences in overall bill shape, we calculated a bill
curvature index as the arc:chord ratio of exposed culmen (maxillary
curvature; Stiles 1995). Arc length was measured following the dor-
sal profile of the bill from the feathered base to the tip, and chord
was measured as a straight-line distance from the feathered base
to the tip. These measures were taken on the lateral photographs
of complete bills using ImageJ (Schneider et al. 2012). We used
the maxillary curvature index because it provided the most con-
servative estimate, based on Berns and Adams’ (2010) comparison
among several methods. More subtle dierences can be uncovered
with the mandibular curvature index (Paton and Collins 1989), the
reciprocal of the radius (Temeles etal. 2009), and landmark-based
geometric morphometrics (Berns and Adams 2010). By using the
most conservative index (maxillary curvature), we ensure that any
signal we obtain is more apt to convey biological relevance.
We assessed whether bill measurements dier among sexes and
age classes using 2-way analysis of variance (ANOVA). Tukey HSD
or univariate tests were used a posteriori for assessing the relation-
ship to single factors. Multivariate analysis of variance (MANOVA)
was used to assess the eect of sex and age in bill shape variables.
MANOVA was also used to compare changes in overall bill shape
in 2 consecutive years, with “year” as a fixed eect. Paired t-tests
were used as post-hoc tests for individual variables. For birds that
were recaptured and measured in dierent years, only the first mea-
surements were included in order to increase the sample size for
juveniles. Dierences between floaters and territorial males were
assessed using ANOVAs to emphasize comparisons between these
groups within the same leks/years. We used a logistic regression
to evaluate the relationship between bill tip length and territory
Functional assessment
We experimentally estimated bill puncture capability by mea-
suring the force needed for the bill to puncture a Polyvinyl
chloride film (12.5 μm) placed taut on top of a tubular plastic
vial (31.8 mm diameter). We held each hummingbird up to its
bill base, in a similar way as they are held to measure exposed
culmen, in order to ensure that the bill tip contacted the film
at the approximate centre and at a 90-degree angle (maximiz-
ing compression and minimizing fracture-risk forces, cf. Bock
1966). We positioned the vial with the film on a digital scale
(AWS-100 ± 0.01 g) and moved the bill downwards until the bill
tip punctured the film (Supplementary Figure A1c). When the
bill tip contacted the film, the mass readings started to increase
and reached a maximum right before the film was punctured.
We converted maximum mass measurements, recorded with a
digital camera (Fujifilm FinePix HS 10, 120 f/s), to milliNewtons
of force. This technique allowed us to evaluate the capacity of
the whole bill to transfer force from the body to the bill tip, as is
expected in nature. Bills with sharper tips are expected to punc-
ture the film (or the skin of an opponent) at lower force values.
We performed trials on both living birds and museum specimens.
The results did not dier between museum and field experiments
(Nested ANOVA: F1,43 =0.039, P = 0.844), allowing us to pool
the data for further analyses. The eects of sex and age were
tested using females, juvenile males and adult males. Dierences
in force were analyzed with a nested ANOVA, with puncture trial
nested within individual.
Behavioral observations
During our field observations, we recorded chases and ago-
nistic encounters during disputes for perches and territory
supremacy. We placed cameras in front of defended perches and
documented aerial displays that sometimes escalated to mount-
ing attempts and/or chases (e.g., Supplementary Movie A1). We
recorded agonistic interactions involving physical contact dem-
onstrating the use of bills as weapons by males. Specifically, we
observed males stabbing their opponents with their bills (e.g.,
attack in the throat, Supplementary Movie A2). We also observed
territorial males perching in front of each other and pecking
their opponent repeatedly in the throat before a struggle (e.g.,
Supplementary Movie A3). Finally we observed copulations
when females approached territorial males (e.g., Supplementary
Movie A4).
Behavioral Ecology
Bill tip variation with sex, age, size, and
We captured and measured a total of 159 individuals in 5 leks.
Using a cross-validation discriminant function analysis on morpho-
logical measurements in situ, we determined that 144 were males
and 15 were females. These unbalanced sample sizes for each sex
are due to the fact that we concentrated our mist-netting eorts
within lek boundaries, where males move frequently and females
are rare visitors (Stiles and Wolf 1979). La Selva Biological Station
is located at the tip of a narrow biological corridor and it is sur-
rounded by farmland unsuitable for lekking arenas (McDade etal.
1994). We thoroughly scouted the study area and consider unlikely
that there were leks that we did not detect, in agreement with pre-
vious studies (Stiles and Wolf 1979). Only 4.1% of the males cap-
tured were found in 2 dierent leks, and 31% of the males were
floaters. These observations support the inference that there are
males without territories attending regularly at the leks (i.e., true
floaters); these are not just territorial males visiting from other leks
(i.e., erroneously classified as floaters).
We report a hitherto unknown sexually dimorphic trait for hum-
mingbirds: in adult males only, the tip of the upper bill becomes
elongated, and conical (Figure 2a). Given that, bill tip elongations
measured in lateral and ventral views across individuals were highly
correlated (R= 0.92, degrees of freedom [df] = 65, P<0.0001), in
subsequent analyses we used only elongation measured in lateral views.
Tip elongation diered significantly between sexes (F1,156 = 10.39,
P=0.0015) and age classes (F1,156=38.33, P <0.0001, Figure 2b).
Post-hoc analysis revealed that adult males have significantly longer
bill tips (Tukey HSD test: P<0.02 in all cases; Figure2b). Adult males
showed significantly pointier bill tips than juveniles (F2,77 = 4.69,
P = 0.012). When all adult males (without discriminating between
territorial and floaters) were included and compared to females,
pointiness did not dier between sexes (F1,77= 0.15, P = 0.69); how-
ever, when males were subdivided by territoriality, territorial males
showed significantly pointier bill tips than both females and floaters
(F2,76=5.03, P = 0.009; Tukey HSD test: P < 0.001 in both cases;
Figure 2c). Pointiness index was positively correlated to tip elonga-
tion in males (F1,65= 21.41, R2 =0.236, P<0.0001; Supplementary
Figure A2). Bill tip elongation also diered between lekking males
(Figure 3a). Territorial individuals showed significantly longer bill
tips than floaters (F1,119= 10.04, P = 0.002; Figure 3b), and bill tip
length significantly predicts the probability of holding a lek territory
(X2=10.58; df=1; P=0.003); this test result remained significant
after excluding juveniles and duplicated (present in more than 1 lek/
year) individuals (X2=6.67; df=1; P=0.023).
We tracked the bill tip development in 20 males during con-
secutive years and found that bill tip length significantly increased
through time (Paired t-test: t=−2.53, df=19, P=0.020; Figure4a).
Such result is influenced by the fact that bill tip length increased in
all juvenile males included in the analysis; juvenile males acquired
longer bill tips when they reached adulthood (points inside squares,
Figure4a). When focusing on the males that we captured for more
than 2 consecutive years however, we found that in some males the
bill tip always increased in length, in some it always decreased, in
some the bill tip first increased and then decreased, and in some
it first decreased and then increased (Supplementary Figure A3).
To test for the influence of body size over bill tip length, we used
a log10-log10 transformation on the data and estimated allometric
lines using the standardized major axis tests and routines package
(SMATR: Warton etal. 2012). We did not find any significant fit
between bill tip length against weight (Supplementary Figure A4),
tarsus length, exposed culmen, and wing chord (P > 0.1 in all cases).
Bill morphology in relation to sex, age, size, and
Sex and age classes also diered in overall bill morphology when
compared on 3 parameters: height, length and curvature (sex: Pillai’s
Trace=0.336, F3,156=26.33, P<0.0001; age: Pillai’s Trace=0.094,
F3,156 = 5.44, P = 0.0013). Females showed significantly shorter bill
heights (F1,158 = 8.17, P = 0.005) and more curved bills than males
(F1,158=22.53, P< 0.0001). Bill curvature was significantly correlated
to bill length, although bill length explained only 3.4% of the variation
in curvature (F1,160= 6.59, R2: 0.034, P= 0.014). Adults showed lon-
ger bills (F1,158=9.51, P=0.002) and greater bill height (F1,158=4.65,
0.2 0.3 0.4 0.5
Elongation (mm)
Juvenile Adult Juvenile Adult
Females Males
0.34 0.38 0.42
Pointiness index
Females FloaterTerritorial
(a) Female
Sexual dimorphism in bill tip length (elongation) and pointiness, subdivided
by age and territory class, respectively. (a) Field macro-photographs
of the bill tips of a representative individual of each sex. Scale bars
(white)=0.5 mm. (b) Length of the maxillary elongation measured in lateral
view (mean ± SE) for sexes and age classes in long-billed hermits. Letters
represent significant dierences after post-hoc tests. (c) Pointiness index
(mean ± SE) for females and males (by territory tenure). Letters represent
significant dierences after post-hoc tests.
Rico-Guevara and Araya-Salas • Hummingbird bills as daggers
P=0.032) than juveniles, but did not dier in curvature (F1,158=0.34,
P = 0.55). Bill shape changed through time in males measured in
consecutive years (Pillai’s Trace = 0.33, F3,32 = 4.93, P = 0.007);
bill curvature decreased (Paired t-test: t = 3.35, df = 16, P =0.004;
Figure4b), but not bill length (Paired t-test: t=0.71, df=16, P=0.48)
or height (Paired t-test: t=1.17, df=16, P=0.26). Using the SMATR
package for allometric trends, we did not find any significant fit
between bill length against weight, tarsus length, exposed culmen, and
wing chord (Supplementary Figure A5, P > 0.05 in all cases).
Functional assessment
Bill puncture capability analyses revealed significant dierences
between adult males, juvenile males, and females (F2,33 = 69.23,
P< 0.0001). Adult male bills required less force to perforate the film
than those of juvenile males or females (Tukey pos-hoc test: P<0.001
in both cases; Figure5a). In addition, we noted that bill tips in adult
males were stier to the touch than those of females and juveniles,
which tended to bend slightly when gently touched. Bill curvature and
bill tip pointiness (interaction) explained together (Multiple regression:
F2,29 = 4.23, R2 = 0.17, P = 0.024, Figure 5b), but not individually
(curvature: P=0.083; pointiness: P=0.073), a significant proportion
of the variation in puncture force. Bill curvature was positively cor-
related with force (β=2208) while a negative relationship was found
between pointiness and force (β=−353). Bootstrap subsampling tests
supported the results in all unbalanced comparisonsabove.
The role of sexual selection in hummingbird bill
We found supporting evidence for the hypothesis that the dagger-
like bill tip in the long-billed hermit is a secondary sexual trait and
0.2 0.3 0.4 0.5
Elongation (mm)
FloatersTerritorial males
(a) Floater
Territorial male
Bill tip length dierences between floaters and territorial males. (a) Field
macro-photographs of the bill tips of a representative floater and a
territorial male. Scale bars (white) = 0.5 mm. (b) Length of maxillary
elongation measured in lateral view (mean ± SE) for floaters and territorial
males. Sample sizes are given above.
Curvature index
Elongation (mm)
1st year 2nd year
Ontogenetic change in overall bill morphology and bill tip length in male
long-billed hermits. (a) Change in bill tip length (mean ± SE, N = 20)
for males measured in 2 consecutive years. Points around means show
individual bill tip lengths. Points inside squares denote lengths for individuals
that were juveniles when the first measurement was taken. (b) Change in bill
curvature (mean ± SE, N=20) for males measured in 2 consecutive years.
−0.02 0.00 0.02 −0.4 0.0 0.4
Juvenile Adult
Force (mN)
100 150 250
Force (residuals)
-0.5 0.0 1.0
Results of puncture assessment experiments, and the roles of bill tip
curvature and pointiness for explaining dierences in performance. (a)
Applied force (mean ± SE) required to perforate the experimental film by
sex and age classes (among males). Sample sizes are given above. Letters
represent significant dierences after post-hoc tests. (b) Partial regression
plots showing the eect of bill curvature (left) and pointiness index (right)
on the force required to puncture the experimental film. Plots represent the
eect of each variable after correcting by the other (interaction is significant,
see Results: Functional assessment).
Behavioral Ecology
a sexually dimorphic weapon. All our predictions were met: 1)lon-
ger and pointier bill tips were only present in males and were most
developed in adults; 2)fully developed bill tips were acquired during
the transition to male adulthood; 3)variation in bill tip morphology
reflected puncture capability (i.e., pointier bill tips pierced with less
force than the non-pointed bill tips); and 4)males with larger and
pointier bill tips were more successful in defending lek territories.
Our hypothesis is further supported by our behavioral observations
during 4 years: we recorded the displays described by Stiles and
Wolf (1979) that usually escalated to chases (e.g., Supplementary
Movie A1) or led to copulations (e.g., Supplementary Movie A4).
We also observed males using their bills while fighting; confirm-
ing the use of the bill tip as a functional weapon, specifically for
stabbing rivals (e.g., Supplementary Movie A2). Overall, our
results support the hypothesis that this secondary sexual trait is
the first documented sexually dimorphic weapon in humming-
birds. Interestingly, hooked bill tips and serrated tomia have been
shown to be sexually dimorphic in the tooth-billed hummingbird
(Androdon: Gould 1863) and the saw-billed hermit (Ramphodon: Elliot
1879). The function of these dimorphic bill tips has puzzled scien-
tists for over a century, and it might be explained under our theory
of sexually dimorphic weapons.
In some males, bill tip length decreased from 1year to the next,
and even during 3 consecutive years. Hence, although the acqui-
sition of a dagger-like bill tip is delayed until adulthood, older
males do not necessarily possess longer bill tips. Similar results have
been found in male Mandrills; canines become longer with age
up to a point, but then decrease again in the oldest males (Leigh
et al. 2008). Teeth in diphyodont vertebrates (most mammals) are
not replaced during adulthood (review in Wang et al. 2014) then
once they stop growing they would decrease in size due to wear.
However, in birds the rhamphotheca continues to grow even in
adult individuals (e.g., Lüdicke 1933; Hieronymus and Witmer
2010), therefore the interplay between growth and wear may ulti-
mately determine the final size of the bill tip. Among the individu-
als in which we tracked bill tip length across years, we did not find
any consistent pattern (Supplementary Figure A3) besides the fact
that the juvenile males that did not have elongated maxillary tips
(bill tip length ~0.0 mm) when captured for the first time, acquired
elongated bill tips in subsequent years, once they became adults
(Figures 4a and Supplementary Figure A3). We surmise that in such
a dynamic system, the dierences between territorial and floaters
are not mere age-related byproducts. We did not notice any dam-
age to the bill tips of the males included in the analyses of bill tip
length dierences between years, thus discarding the possibility of
broken tips confounding our results. We excluded from these analy-
ses one male in which we clearly observed a broken maxillary tip
the second time it was captured (the following year). This male had
lost his territory by the time of the second capture, but regained
territory tenure by the time of the third capture (about a year after
the second capture) when its bill tip had grown back close to its
original size and shape thus reinforcing the connection between bill
tip length and form, and territory tenure (cf. Figures 2c and 3b).
In a similar manner, if the dierences in bill tip morphology were
due simply to overall body size (larger males having longer bill tips),
one would expect an isometric scaling in maxillary and mandibular
tips. Such isometry would yield proportional lengthening of both
mandibular and maxillary rhamphothecae, roughly preserving the
distance between upper and lower bill tips (i.e., no maxillary elon-
gation). Isometric scaling by definition would preserve the shape
of the structures involved, in this case, bill tips. What we found,
however, was a drastic change in shape between juvenile and adult
males, and significant shape dierences between floaters and ter-
ritorial males. When testing for allometric scaling on the bill traits
(e.g., Supplementary Figures A4 and A5), we did not find signifi-
cant trends using bivariate line-fitting methods (Warton etal. 2012;
but see Martin etal. 2005). The absence of significant isometry or
allometry in our data could be explained by the lack of a robust
estimate of body size in hummingbirds; weight is highly variable
due to their small size, tarsus length is susceptible to proportionally
large measurement error using calipers, wing chord could be sub-
ject to variation in the final stages of moulting and due to selection
under varying aerodynamic requirements (related to displays and
chases), and exposed culmen is a circular proxy because it includes
the bill tip. Since bill tips do not necessarily grow longer with age
(Supplementary Figure A3) or body size (e.g., Figure A4), and since
there is a strong correlation between bill tip length/shape and terri-
tory tenure (Figures 2c and 3), our findings support the importance
of the maxillary tip morphology (elongation and sharpness) per se as
a determinant of successful territoriality.
We found that adult males have pointier, longer and straighter
bills, and that curvature and pointiness partially explain the lower
force adult males need for puncturing (Figure 5b). Therefore, an
adult male bill will inflict more damage during an attack with its
bill, compared to a female or a juvenile. Male LBHs have longer
bills than females (present study; Stiles and Wolf 1979; Temeles
etal. 2010), which could be advantageous to win bill-sparring con-
tests, as has been shown for Ibises (Babbitt and Frederick 2007).
We found that females have more curved bills than males, agreeing
with Temeles etal. (2010) in this and other species of large hermits
(using a dierent curvature index). Moreover, we found that juvenile
males transitioned from curved to straighter bills (Figure 4b) and
acquired longer bill tips (Figure4a) once they reached adulthood.
Straight elongated structures (e.g., slender beams) are mechani-
cally more resistant to buckling, when loaded axially, than curved
ones (Kuo and Yang 1991; Dahlberg 2004). Bending is disadvanta-
geous for a stabbing weapon since it results in less force applied at
the tip, and hence less damage to an opponent. In hummingbirds,
straighter bills transmit more force without bending, and pointier
bills transform that force into perforation capacity (cf. Figure5). We
also found that males have bills that are thicker (greater bill heights)
at the base, potentially providing increased support to resist bend-
ing forces at the bill base when stabbing. The arguments above pro-
vide an alternative explanation to intersexual resource partitioning
or ecological causation for sexual dimorphism in hummingbird bills
(see below).
Sexual selection, in the form of female choice, has been pro-
posed as an explanation for sexual dimorphism in hummingbird
bills (Stiles 1995). Female choice has been shown as a driver of
sexual dimorphism in some species of birds (e.g., Olsen et al.
2013). We observed some territorial males pecking the throat of
recently arrived birds (e.g., Supplementary Movie A3). We hypoth-
esize that this could function as a courtship display and/or a
warning signal and weapon assessment. However, in the interac-
tions that led to copulations (e.g., Supplementary Movie A4) we
did not observed pecking. Although female choice does not seem
to be a plausible mechanism for the evolution of dagger like bill
tips given the courtship behavior in this species (Stiles and Wolf
1979, Supplementary Movie A4), sexually dimorphic weapons in
other animals function both as armaments and ornaments (e.g.,
deer: Goss 1983; fiddler crabs: Allen and Levinton 2007; but see
Callander etal. 2013).
Rico-Guevara and Araya-Salas • Hummingbird bills as daggers
Alternative hypotheses
Sharp bill tips could be useful in nectar thievery (cf. Ornelas 1994),
which has been reported predominantly in short-billed humming-
birds (reviews in Ornelas 1994; Irwin etal. 2010). All the species of
Phaethornis that have been reported robbing nectar, in fact, are small
(<4 g) and have short bills (<25 mm): P.longuemareus (LBH) (McDade
and Kinsman 1980), P. striigularis (Schuchmann 1999), P. ruber
(Lopes et al. 2002, among others). Additionally, species of small
Phaethornis exhibit reduced (or absent) sexual dimorphism in bill
curvature when compared to large Phaethornis (Temeles etal. 2010).
In multiple studies P. longirostris (LBH) has always been reported to
visit flowers legitimately (account in Schuchmann 1999). Floral lar-
ceny usually emerges when a nectarivore cannot access the nectar
in the usual way (Irwin etal. 2010). LBHs, with bills of ~41 mm,
have no trouble legitimately accessing flowers. Nonetheless, if there
were evolutionary pressure to adapt to a nectar robbing strategy,
it would most likely aect the sex with shorter bills, in this case,
females. Conversely, we found the needle-like bill tips to be present
in adult males only. We thus consider nectar theft an unlikely expla-
nation for this sexually dimorphic trait in hummingbirds.
Sexually dimorphic traits in hummingbird bills have been tra-
ditionally explained through the intersexual resource partition-
ing (IRP) hypothesis (Darwin 1871; Temeles and Roberts 1993;
Bleiweiss 1999; Temeles et al. 2000, 2010). In some species of
hermits, it has been shown that males and females feed on dier-
ent plant species (e.g., Temeles etal. 2010), but it is unclear if the
hummingbirds have adapted to the plants or vice versa. If sharp bill
tips were advantageous for feeding on flowers (e.g., to prop open
closed corollas), there is no a priori reason to speculate that such a
trait would favor males but not females. In the cases in which inter-
sexual resource partitioning has been shown, both sexes forage on
very similar flowers (dierent species of the same plant genus; e.g.,
Heliconia: Temeles etal. 2010), and feed in the same way (i.e., no dif-
ferential robbing between sexes). Furthermore, dierences in floral
resource use between sexes of P. longirostris have not been reported
(cf. Temeles etal. 2010). Given that the dagger-like bill tips that
we describe in this paper do not seem to convey any gender-biased
foraging advantage, nor to be related to dierential feeding strate-
gies between the sexes, we infer that this sexually dimorphic trait in
hummingbird bills does not fit the IRP explanation regarding floral
A related hypothesis is that IRP explains sexual dimorphism
in bill traits with respect to arthropod capture. Female humming-
birds need to acquire the necessary protein for egg production
and nurturing of hatchlings during the breeding season (Wolf
and Stiles 1970; Remsen etal. 1986; Chavez-Ramirez and Dowd
1992). Consequently, females spend more time hunting for arthro-
pods, targeting prey at higher trophic levels (higher nitrogen con-
tent; e.g., spiders: Rico-Guevara 2008; Hardesty 2009). Among
hummingbirds, hermits have been shown to rely more heavily on
substrate prey (Stiles 1995). Since longer bills could be advanta-
geous for gleaning prey such as spiders (longer reach, Stiles 1995),
increased bill length would be expected in females, who hunt
and successfully capture prey more frequently than males (Stiles
1995; Rico-Guevara 2008; Hardesty 2009). Nevertheless, in large
Phaethornis bills have been found to be longer in males than in
females (Stiles 1995; Colwell 2000; Rodríguez-Flores and Stiles
2005; Temeles etal. 2010). For those reasons, predictions of bill
sexual dimorphism as a result of arthropod foraging contradict
the observed pattern.
As a final alternative hypothesis, modifications of the bill
tip could be useful for grooming. Maxillary overhangs in birds
have been hypothesized (Clayton and Walther 2001) and proven
(Clayton etal. 2005) to enhance preening, which is the first line of
defense against ectoparasites. Although preening behavior per se has
not been found to be sexually selected (Griggio and Hoi 2006), it
appears to maintain feather colors that may signal male condition
to females (Griggio etal. 2010). It would be plausible then that sex-
ually dimorphic bill tip overhangs evolved to enhance male preen-
ing abilities. We discard this alternative hypothesis by pointing out
the morphological and mechanical dierences between the “max-
illary overhang” used for preening (Clayton and Walther 2001;
Clayton et al. 2005) and the “maxillary elongation” described in
this paper. The preening bill overhang consists of a curved, flat-
tened extension of the maxillary rhamphotheca over the mandibu-
lar tip (see Figure3a in Clayton and Walther 2001). This contrasts
with the maxillary elongation we describe here, which is a straight,
conical extension of the maxillary tip beyond the mandibular tip.
A flattened, curved overhang generates a shearing force (su-
cient to damage ectoparasites) when the mandible moves forward
and scrapes the inside of the overhang (Clayton etal. 2005). The
larger the internal area of the maxillary overhang, before a critical
break point, the better the ectoparasite removal (Figures 1 and 4 in
Clayton etal. 2005). Conversely, the maxillary elongation we found
in LBHs becomes conical at the tip, oering less shearing surface
area. Additionally, since the elongation in LBH bill tips is straight
rather than curved, it would exert a comparatively weaker verti-
cal force (Figure3b in Clayton and Walther 2001) detrimental for
preening purposes.
Having considered alternative hypotheses for the existence of a
needle tipped bill of male LBHs, we argue that it is likely that more
than one selective force could operate synergistically in the evolu-
tion of a sexually dimorphic trait (Hedrick and Temeles 1989). For
instance, for the species in which a correlation between bill sexual
dimorphism and nectar foraging has been shown (e.g., Temeles
etal. 2010), both IRP and sexual selection could play a role in the
existence and maintenance of such dimorphism. We argue, how-
ever, that IRP would be restricted to particular species-poor com-
munities, in which interspecific competition is decreased (Hedrick
and Temeles 1989). We expect that sexual selection in the form of
male-male combat is most important in species with high levels of
aggressive physical interactions (e.g., lekking hummingbirds).
Sexually dimorphic weaponry
Most of the animal weaponry studied to date is found in arthro-
pods or non-avian vertebrates (Emlen 2008) and the documented
examples of bird sexually dimorphic weapons are restricted to leg
spurs in Phasianids and wing spurs in 5 families of aquatic birds
(Rand 1954; Davison 1985). Leg spurs have been suggested to
evolve due to competition for females or for resources attractive to
females (Andersson 1994). There have been previous suggestions of
male birds using their bills in physical combat against conspecifics
(Babbitt and Frederick 2007; Chaine and Lyon 2008; Navarro etal.
2009; Greenberg and Olsen 2010; Greenberg etal. 2013), but there
have been no previous descriptions of sexually dimorphic weap-
ons in bird bills. In Emlen’s 2008 comprehensive review of animal
weapons, there is not a single reference to birds’ weaponry high-
lighting the importance of studying armaments in such a diverse
group. This study stands as one of the few unambiguous examples
of sexually dimorphic weapons inbirds.
Behavioral Ecology
Hummingbirds’ extremely pugnacious nature has been
acknowledged since they first marveled pioneering naturalists (cf.
Wallace 1878), but only now have we started to appreciate its eco-
logical and evolutionary implications, for example, fighting and
the presence of weapons. Our discovery of a new sexually dimor-
phic weapon encourages future comparative studies and reinter-
pretations of sexual dimorphism of bill traits in hummingbirds.
Additionally, this sexually dimorphic weapon in hummingbirds is a
direct modification of the feeding apparatus; possessing a weapon
is advantageous in the mating process but may be disadvanta-
geous for feeding (e.g., salmon: Darwin 1859; Witten and Hall
2002). Hummingbirds feed on nectar by extruding the liquid from
the tongue using their bill tips (Ewald and Williams 1982; Rico-
Guevara and Rubega 2011), the bill tip modifications described
in this paper would impose a functional trade-o between fight-
ing ability and feeding performance. Comparative studies to
understand and quantify the costs (or lack thereof e.g., beetles:
McCullough and Emlen 2013) of sexually dimorphic weapons
in nature, and studies on sexual dierences in feeding eciency
in species with sexually dimorphic weapons (e.g., fiddler crabs:
Weissburg 1993; Mokhlesi etal. 2011) are warranted.
Supplementary material can be found at http://www.beheco.
This work was supported by the Organization for Tropical Studies;
Department of Ecology and Evolutionary Biology at University of
Connecticut National Science Foundation (IOS- DDIG 1311443);
College of Arts and Science and Biology Department at New
Mexico State University; National Geographic Society (CRE
9169-12); and Animal Behavior Society. All of the activities were
reviewed and authorized by the Institutional Animal Care and Use
Committee at the New Mexico State University, IACUC 2011-020,
and were performed under the research permits 152-2009-SINAC
and 063-2011-SINAC.
We thank G.Stiles, W.Eberhard and G.Barrantes for stimulating discus-
sion of ideas on early stages of this manuscript, K. Wells, J. Velotta, D.
Sustaita, P.Allen, P.González-Gómez, C.Clark, and anonymous reviewers
for comments on the manuscript, and M.Rubega, K.Schwenk, T. Wright,
B. Ryerson, and the participants in the Vertebrate Biology Seminar at
UConn for debates on various hypotheses. Special thanks to J.Rack and
K. Hurme for grammar and style advice. Finally we thank S. Ehlman,
X. Sanloz, O. Kolodny, D. Boyce, W. Tsai, D. Sanchez, D. Ocampo
and M. Percy for fieldwork assistance, and the Museum of Zoology of
Universidad de Costa Rica for logistic support.
Handling editor: Paco Garcia-Gonzalez
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... Consequently, though the evolution of sexually dimorphic traits is the result of differential forces acting individually on either sex, the resulting difference provides valuable insight into the forces shaping trait evolution. One captivating example of sexually dimorphic traits evolving under both sexual and natural selection are avian bills shaped by plant-pollinator coevolution [8], while simultaneously used in physical combat as intrasexually selected weapons [7,9]. ...
... Within birds, the hummingbirds (Trochilidae) are a morphologically, colourfully and acoustically diverse family, which are monophyletic [40], species-rich, and occur in many different environments across the Americas. In this family, several morphological and locomotion-related traits have been extensively studied, showing that wing, bill and tail traits are involved in intra-and inter-sexual interactions [14,[41][42][43], but are also under natural selection for access to resources through interference and exploitative competition [8,9,14,44]. Hummingbird coloration is highly diverse and has been associated with both sexual selection for mate attraction [45][46][47], selection for social dominance [27,48,49] and camouflage [45,46]; similarly, hummingbirds also display a wide range of diversity in song structure [50,51]. ...
... Hence, it is important for future studies to account for habitat structure on altitudinal effects on morphology. We showed that differences in overall body size extend to other traits such as bill shape, which may be associated with resource specialization [8,88], and intrasexual competition and aggressive interactions [7,9]. By contrast, dimorphism in tail length was not affected by either altitude or habitat structure, which supports that the main selective regime affecting this trait in hummingbirds is sexual selection [43]. ...
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Traits that exhibit differences between the sexes have been of special interest in the study of phenotypic evolution. Classic hypotheses explain sexually dimorphic traits via intra-sexual competition and mate selection, yet natural selection may also act differentially on the sexes to produce dimorphism. Natural selection can act either through physiological and ecological constraints on one of the sexes, or by modulating the strength of sexual/social selection. This predicts an association between the degree of dimorphism and variation in ecological environments. Here, we characterize the variation in hummingbird dimorphism across ecological gradients using rich databases of morphology, colouration and song. We show that morphological dimorphism decreases with elevation in the understorey and increases with elevation in mixed habitats, that dichromatism increases at high altitudes in open and mixed habitats, and that song is less complex in mixed habitats. Our results are consistent with flight constraints, lower predation pressure at high elevations and with habitat effects on song transmission. We also show that dichromatism and song complexity are positively associated, while tail dimorphism and song complexity are negatively associated. Our results suggest that key ecological factors shape sexually dimorphic traits, and that different communication modalities do not always evolve in tandem.
... The remarkable morphological diversity and multi-functionality of the avian bill render it uniquely suited to address these biomechanical questions of form and function. Involved in numerous functions such as feeding, territorial defense and thermoregulation, bills are subject to a host of selective pressures on their shape and structure [4][5][6][7][8]. In addition to these functions, many birds use their bills to manipulate substrate, from light to physically difficult manoeuvres. ...
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Organisms are subject to physical forces that influence morphological evolution. Birds use their bills as implements to perform various functions, each exerting unique physical demands. When excavating cavities, bird bills must resist a range of mechanical stresses to prevent fracture. However, the contribution of bill geometry and material composition to excavation stress resistance remains poorly understood. Here, we study the biomechanical consequences of bill diversification in the cavity-excavating palaeotropical barbets. Using finite-element models and beam theory, we compare excavation performance for two loading regimes experienced by barbet bills during cavity excavation: impact and torsion. We find that deeper and wider maxillae perform better for impact loads than for torsional loads, with the converse for narrower maxillae. This results in tradeoffs between impact and torsion resistance imposed by bill geometry. Analytical beam models validate this prediction, showing that this relationship holds even when maxillae are simplified to solid elliptical beams. Finally, we find that composite bill structures broadly exhibit lower stresses than homogeneous structures of the same geometry, indicating a functional synergy between the keratinous rhamphotheca and bony layers of the bill. Overall, our findings demonstrate the strong link between morphological evolution, behaviour and functional performance in organisms.
... Their mating system is polygamous; males do not participate in nesting and brood care. Accordingly, several species exhibit sexual dimorphism in body size [11,12], colors [13] and sometimes even in bill structure [14]. ...
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We documented the presence/absence of the eggs of Trochiloecetes, Trochiliphagus, and Leremenopon lice on over 50,000 hummingbird specimens (representing 348 species plus 247 additional subspecies) in four museums in the USA. (i) We provide sample estimates of infestation prevalence. (ii) Sample estimates of parasite genus richness increased with increasing host sample size. (iii) Host body mass did not correlate with parasite genus richness, even when controlled for sample size effects. (iv) The prevalence of Trochiliphagus and Trochiloecetes infestations did not correlate with host body mass, while the prevalence of Leremenopon exhibited a marginally significant positive correlation with host body mass. (v) The prevalence of Trochiliphagus and Leremenopon infestations correlated strongly and positively across host taxa (i.e., species or subspecies). (vi) The co-occurrence of Trochiliphagus and Trochiloecetes within the few largest host samples-i.e., within particular host taxa-was significantly more frequent than expected by chance. This latter association might indicate a true ecological relationship or, alternatively, might have emerged as an artifact of our sampling method. (vii) We found no relationship between host sexual size dimorphism and the prevalence of any of the three louse genera, contrary to the interspecific prediction of the Hamilton-Zuk hypothesis.
The field of comparative biomechanics examines how form, mechanical properties and environmental interactions shape the function of biological structures. Biomechanics has advanced by leaps and bounds as rapid technological progress opens up new research horizons. In this Review, I describe how our understanding of the avian bill, a morphologically diverse multifunctional appendage, has been transformed by employing a biomechanical perspective. Across functions from feeding to excavating hollows in trees and as a vocal apparatus, the study of the bill spans both solid and fluid biomechanics, rendering it useful to understand general principles across disciplines. The different shapes of the bill across bird species result in functional and mechanical trade-offs, thus representing a microcosm of many broader form-function questions. Using examples from diverse studies, I discuss how research into bird bills has been shaped over recent decades, and its influence on our understanding of avian ecology and evolution. Next, I examine how bill material properties and geometry influence performance in dietary and non-dietary contexts, simultaneously imposing trade-offs on other functions. Following an examination of the interactions of bills with fluids and their role as part of the vocal apparatus, I end with a discussion of the sensory biomechanics of the bill, focusing specifically on the bill-tip mechanosensory organ. With these case studies, I highlight how this burgeoning and consequential field represents a roadmap for our understanding of the function and evolution of biological structures.
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Interspecific dominance interactions have consequences for behavior, ecology, and the stability of species coexistence. Determinants of the outcomes of these interspecific interactions are therefore of great interest. However, few large-scale comparative works have demarcated the potential behavioral and morphological traits that explain dominance between species. To delineate which traits may influence species dominance, we rely on a newly established dominance ranking of bird species in North America. We pair these dominance rankings with phylogenetic analysis and incorporate social, morphological, and natural history variables to determine how morphological and social traits contribute. Like previous studies, we find that body mass is a positive predictor of dominance, but we also find that after controlling for body mass, bill length positively predicts a species’ rank in the hierarchy. In addition to morphological traits, we find that species that engage in proportionally more intraspecific fights tend to be less interspecifically dominant. Consequently, both morphological and social variables influence the interspecific dominance rank of a species. Such effects may have downstream consequences for the acquisition of foraging resources and the evolution of a species.
Organisms are subject to a host of physical forces that influence morphological evolution. Birds, for instance, use their bills as implements to perform various functions, each exerting unique physical demands and selective influences on bill morphology. For example, birds that use their bills to excavate nesting or roosting cavities must resist a range of mechanical stresses to prevent fracture. However, the contribution of bill geometry and material composition to excavation stress resistance remains poorly understood. Here, we study the biomechanical consequences of bill diversification in two clades of cavity-excavating, frugivorous birds, the paleotropical barbets. Using multilayered finite element models and beam theory, we compare the excavation performance of different maxillary geometries for two loading regimes experienced by barbet bills during cavity excavation- dorsoventral impact and torsion. We find that deeper and wider maxillae perform better for impact loads than for torsional loads, with the converse for narrower maxillae. This results in a tradeoff between impact and torsion resistance imposed by bill geometry. Analytical beam models validate this prediction, showing that this relationship holds even when maxillae are simplified to solid elliptical beams. Finally, we find that composite bill structures broadly exhibit lower stresses than homogenous structures of the same geometry, indicating a functional synergy between the keratinous rhamphotheca and bony layers of the bill. Overall, our findings demonstrate the strong link between morphological evolution, behavior, and functional performance in organisms.
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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. This article is protected by copyright. All rights reserved.
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Among size-dimorphic animals, a few clades such as hummingbirds show “reversed” sexual size dimorphism: females tend to be the larger sex. What selects for this pattern? Sexual selection for flight performance could drive the evolution of smaller, more agile males, either for male-male combat or female choice for aerial courtship displays. Alternately, natural selection can select for female fecundity (e.g., egg size influences female body size), or sex differences in foraging niche could favor body size differences. The sexual selection hypotheses predict that dimorphism extends to other aspects of flight morphology (e.g., flight muscle size) whereas the natural selection hypotheses predict that male and female flight morphologies are isometric, and the niche differentiation hypothesis predicts that bill dimorphism is correlated with size dimorphism. We tested these predictions through phylogenetic comparative analyses of flight morphology, wingbeat frequency, and courtship behaviors, focused on 30 species within the “bee” hummingbird clade (tribe Mellisugini). There is no correlation between bill morphology and dimorphism. Relative to females, males tend to be smaller, have proportionately shorter wings and higher hovering wingbeat frequencies, but also longer keels and larger flight muscles. Male wingbeat frequencies are greatly elevated during aerial displays, and the species with the greatest wingbeat frequencies have the greatest dimorphism. Of the four hypotheses for dimorphism, the data best support the hypothesis that female choice for courtship displays has selected for aerial agility and small size in male hummingbirds.
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According to Rensch’s rule, in species where males are the larger sex, increasing body size is coupled with increased sexual size dimorphism (SSD), whereas in species where females are larger, SSD decreases with body size. We describe the variation in SSD for body mass and its fit to Rensch´s rule in 45 species of Costa Rican hummingbirds. We examine SSD in body mass, bill length, and wing size and their fit to Rensch´s rule in nine species of hummingbirds for which we have detailed data. We expected that physiological constraints will limit the variation in SSD since hummingbirds have high metabolic rates, high dependence on energy-dense food, and high costs imposed by small size and hovering flight; these factors scale with body size and elevation. Large species should be physiologically capable of withstanding greater variation in SSD compared to small species, which are more energetically limited. Hummingbirds showed mixed allometry and fit Rensch's rule (slope of the RMA regression male vs female body mass = 0.8630). Eighty percent of the species showed male-biased allometry for SSD in body mass. Average variation in SSD was 12% and varied regardless of size. Physiological limitations act on hummingbirds as a group affecting SSD, independently of body size. SSD differences in body size, bill length, and wing area could influence ecological performance, sexual displays, food resource access, and foraging behavior. The SSD mixed allometry, and the positive relationship between the standard deviation of body mass, wing chord, and wing area with hummingbird size found only in males (9 species), suggests that selective pressures act differentially on the sexes and influence sexual niche segregation. Future research should examine intersexual variation in morphology, and quantify intersexual habitat use, niche segregation, and interspecific and intraspecific competitive interactions, targeting species located at the extremes of the Rensch's rule scatterplot.
In many species that fight over resources, individuals use specialized structures to gain a mechanical advantage over their rivals during contests (i.e. weapons). Although weapons are widespread across animals, how they affect the probability of winning contests is still debated. According to theory, understanding weapon function during contests is essential to: (i) understanding its importance in determining the winner, and (ii) identifying what weapon traits (e.g. weapon length versus shape versus performance) are most relevant for contest success. However, quantitative evaluations of how weapon function affects the extent to which weapon traits influence contest success are still lacking. Here, we first develop an individual‐based model to evaluate how increasing the influence of the weapon in determining the winner translates to differences between winners and losers. Then, we use a meta‐analysis to identify: (i) whether different weapon measures influence contest outcome differently; (ii) how animals use their weapons during fights – i.e. weapon function; and (iii) if weapon function correlates to how weapons influence contest outcome. Our model showed that, as weapons increased the chance of determining the winner, the mean difference between winners and losers also increased. Therefore, in our meta‐analysis we used the mean trait difference between winners and losers as a proxy for the extent to which weapons influence contest success. The literature search identified 49 suitable studies, containing information for 52 species, totalling 107 effect sizes. Four main patterns emerged. First, most of the literature focuses on linear measures of weapons, while performance measures are concentrated on Crustacea and Squamata; other types of measures were rare. Second, differences between winners and losers in linear measurements were greater than differences in performance measurements when all species were combined (and when we used only a subset). Third, species that bear weapons almost always perform visual/tactile displays before engaging in physical contact. And fourth, while the way individuals display their weapons did not influence the importance of weapon size on contest outcomes, fighting style predicted when differences between winners and losers would be higher. Species that used their weapons to push or lift (even when combined with other functions) showed greater differences between winners and losers when compared to species that used their weapons to impact, pierce, pull or squeeze. Overall, our results show that we have an incomplete understanding of animal weapons built mostly on weapon size and a few select taxa. Thus, we should start focusing on measuring weapons according to how they are used during contests and in a wider diversity of species. One way forward is to conduct studies that integrate weapon morphology to weapon function to ensure we are measuring the most ecologically relevant variables.
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Sexual size dimorphism occurs throughout the animal kingdom, and its ecological and evolutionary causes and implications have been intensively studied. Sex-specific differences in bill curvature are known in several species of birds, including some tropical hummingbirds. Despite the importance of bill shape for foraging, comparative studies of sexual dimorphism of bill shape are few. We quantified bill shape in two temperate hummingbird species, Black-chinned Hummingbird (Archilocus alexandri) and Ruby-throated Hummingbird (A. colubris) and compared patterns of sexual shape dimorphism. Several commonly used bill-curvature indices yielded contrasting results; one found differences between species and sexes, a second identified no differences in curvature, and a circle-curvature approach revealed shape differences between species and between the sexes. By contrast, landmark-based geometric morphometric methods identified significant differences in sexual shape dimorphism and also revealed that Ruby-throated Hummingbirds exhibited significant sexual differences in shape, whereas Black-chinned Hummingbirds did not. Female Ruby-throated Hummingbirds exhibited relatively greater bill curvature than males, a pattern consistent with observations of some tropical hummingbirds. Although the causes of differences in bill-shape dimorphism between Black-chinned and Ruby-throated hummingbirds remain unclear, we hypothesize that it may be attributable to differences in the structure of the community in which each species breeds and the interplay between inter- and intraspecific competition for resources in these communities. Finally, we recommend that future studies of bill shape include geometric morphometric approaches because they are better suited than univariate approaches for identifying more complex shape differences within and among species.
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Adult male Green Woodhoopoes (Phoeniculus purpureus) are only 5-8% larger than adult females in most linear measures but have 36% longer bills. Such sexual dimorphism may result from sexual selection, reproductive role division, or ecological separation. Here, we show that there is little evidence that sexual selection is currently acting on bill dimorphism in the Green Woodhoopoe. (1) Breeding males did not have longer bills than nonbreeding males. (2) There was no significant relationship between bill length and reproductive success of breeding males. (3) Although there was greater variation in male than in female bill length, the coefficient of variation (5.3%) fell within the range of those for naturally selected traits. (4) Although male bill length was found to be positively allometric with body mass, female bill length followed a similar relationship and there was no significant difference between the allometric slopes of the two sexes. Maintenance of the bill dimorphism by reproductive role division also seems unlikely when considering the nesting and provisioning characteristics of the species. We therefore conclude that the extreme sexual dimorphism in Green Woodhoopoe bill length is maintained by ecological separation to reduce foraging competition. We cannot, however, rule out the possibility that the sexual dimorphism initially evolved as a consequence of sexual selection.
In the study presented here, the problem of calculating deflections of curved beams is addressed. The curved beams are subjected to both bending and torsion at the same time. The Castigliano theorem, taught in many standard courses in Strength of Materials, Mechanics of Solids, and Mechanics of Materials, is used to determine the beam deflections. Using the methodology presented here, beam deflections that cannot be found in handbooks or textbooks can be calculated without too much effort. The Castigliano theorem and a numerical integration algorithm from the MATLAB package have been used. The examples investigated in this paper deal with elliptically curved beams. The beams are either statically determinate or statically indeterminate. Limiting cases of the elliptical beam are bending of straight beams and bending and torsion of a circular beam. Beam deflections obtained in the limiting cases are compared with handbook formulae.
Hummingbirds rely on the sugars in nectar to meet their high metabolic requirements, but most nectars are extremely low in nitrogen. As a result, the birds must also consume arthropods to meet their protein requirements. In many hummingbird species, males use nectar resources differently from females. I hypothesized that the sexes might also differ in their use of arthropods, because breeding females have higher protein requirements. I used Δ15N isotopes in feathers and blood to demonstrate that females feed at higher trophic levels than males and adults at higher levels than juveniles, respectively. Females captured during the breeding season were also feeding at higher trophic levels than those captured outside of the breeding season, though the sample sizes were small. I also found a slight but unanticipated increase in Δ15N values in feathers with elevation in one species.