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One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill-flower matching, with a strong focus on the benefits to the hummingbird and how to quantify them. Explanations for the coevolution of bill-flower matching include 1) that the evolution of traits by bird-pollinated plants, such as long and thin corollas, prevents less efficient pollinators (e.g., insects) from accessing the nectar, and 2) that increased matching, as a result of reciprocal adaptation, benefits both the bird (nectar extraction efficiency) and the plant (pollen transfer). In addition to nectar feeding, we discuss how interference and exploitative competition also play a significant role in the evolution and maintenance of trait matching. We present hummingbird-plant interactions as a model system to understand how trait matching evolves and how pollinator behavior can modify expectations based solely on morphological matching, and discuss the implications of this behavioral modulation for the maintenance of specialization. While this perspective piece directly concerns hummingbird-plant interactions, the implications are much broader. Functional trait matching is likely common in coevolutionary interactions (e.g., in predator-prey interactions), yet the physical mechanisms underlying trait matching are understudied and rarely quantified. We summarize existing methods and present novel approaches that can be used to quantify key benefits to interacting partners in a variety of ecological systems.
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Bene“fit” Assessment in Pollination Coevolution: Mechanistic
Perspectives on Hummingbird Bill–Flower Matching
Alejandro Rico-Guevara ,*
Kristiina J. Hurme,* Rosalee Elting*
and Avery L. Russell
*Department of Biology, University of Washington, 24 Kincaid Hall, Seattle, WA 98105, USA;
Division of Ornithology,
Burke Museum of Natural History and Culture, 4300 15th Ave NE, Seattle, WA 98105, USA;
Department of Biology,
Missouri State University, 910 S John Q Hammons Pkwy, Springfield, MO 65897, USA
From the symposium “Physical mechanisms of behavior” presented at the virtual annual meeting of the Society for
Integrative and Comparative Biology, January 3– 7, 2021.
Synopsis One of the reasons why flowering plants became the most diverse group of land plants is their association
with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and,
in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide
variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small
caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and
efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent
traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of
bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected
benefits from bill–flower matching, with a strong focus on the benefits to the hummingbird and how to quantify them.
Explanations for the coevolution of bill–flower matching include (1) that the evolution of traits by bird-pollinated plants,
such as long and thin corollas, prevents less efficient pollinators (e.g., insects) from accessing the nectar and (2) that
increased matching, as a result of reciprocal adaptation, benefits both the bird (nectar extraction efficiency) and the plant
(pollen transfer). In addition to nectar-feeding, we discuss how interference and exploitative competition also play a
significant role in the evolution and maintenance of trait matching. We present hummingbird–plant interactions as a
model system to understand how trait matching evolves and how pollinator behavior can modify expectations based
solely on morphological matching, and discuss the implications of this behavioral modulation for the maintenance of
specialization. While this perspective piece directly concerns hummingbird–plant interactions, the implications are much
broader. Functional trait matching is likely common in coevolutionary interactions (e.g., in predator–prey interactions),
yet the physical mechanisms underlying trait matching are understudied and rarely quantified. We summarize existing
methods and present novel approaches that can be used to quantify key benefits to interacting partners in a variety of
ecological systems.
Introduction to plant–pollinator
functional trait matching
A fundamental question in ecology is how speciali-
zation evolves and is maintained. Plant–pollinator
mutualisms are a model system for the study of spe-
cialization and both plants and their animal pollina-
tors can vary from being highly generalized to being
strongly specialized. For example, plants with a gen-
eralist pollination strategy might receive pollination
services from a wide range of pollinator taxa (e.g.,
Fig. 1A; Hern
andez-Conrique et al. 2007), while
highly specialized plants often restrict access to a
few pollinator taxa (e.g., Fig. 1B; Sargent and
Vamosi 2008;Soteras et al. 2018). Specialization on
the part of the plant is thought to arise due to the
costs of associating with less efficient visitors and
selection by the most effective pollinator (Pauw et
al. 2020). Animals vary in their effectiveness as
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Integrative and Comparative Biology
Integrative and Comparative Biology, pp. 1–15
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pollinators and visits by ineffective pollinators can
carry heavy fitness costs for a plant, including exces-
sive pollen loss (the male plant gamete), increased
heterospecific pollen transfer (Ashman and Arceo-
omez 2013), consumption of nutritive food
rewards (e.g., nectar) without pollinating (i.e., rob-
bing), and even cause damage to the flower (Rojas-
Nossa et al. 2021). These costs might drive the evo-
lution of floral traits that filter less effective pollina-
tors. Similarly, more effective pollinators (e.g.,
transporting more conspecific pollen) shape selection
for floral traits that further enhance their effective-
ness as pollinators. In some cases, highly specialized
plants are pollinated by animals that have in turn
specialized to feed on that plant’s food rewards
(Brown and Kodric-Brown 1979;Serrano-Serrano
et al. 2017). Such interactions, where both plant
and pollinator are reciprocally specialized, create a
tighter coevolutionary association that frequently
involves the evolution of specialized traits that fur-
ther enhance specialization (Proctor et al. 1996).
Specialized traits that enhance reciprocal speciali-
zation are often matched between plant and pollina-
tor (i.e., “trait matching”). At broad taxonomic
scales, selection favors similarity in traits across
groups of pollinators and plants (Johnson and
Anderson 2010;Medeiros et al. 2018), and trait
matching is frequently studied in the context of pair-
wise interactions between plant and pollinator spe-
cies. For example, the length of hawkmoth tongues
may closely match the length of floral tubes
(Johnson et al. 2017) in a community of hawkmoths
pollinating long-tubed flowers. A classic case of pair-
wise trait matching occurs between Angraecum ses-
quipedalia, a Madagascaran orchid with an extremely
long nectar spur, and its presumed coevolved spe-
cialist pollinator, the long-tongued sphinx moth,
Xanthopan morganii (Darwin 1862;Johnson and
Anderson 2010;Arditti et al. 2012). Trait-matching
is often inferred through comparing the morphology
of plant and pollinator, and is assumed to be func-
tional (Castellanos et al. 2003;Maglianesi et al. 2014;
Weinstein and Graham 2017). That is, trait matching
is predicted to simultaneously improve the precision
of pollen placement on the pollinator and subse-
quent deposition on the stigma and enhance the ex-
traction of floral rewards by pollinators (Castellanos
et al. 2003). In addition, trait-matching may limit
interspecific competition, both for the pollinator,
by limiting which plant species a given pollinator
may profitably visit, and simultaneously for the
plant, by reducing heterospecific pollen transfer
(Waser and Fugate 1986;Ashman and Arceo-
omez 2013;Maglianesi et al. 2014;Fonseca et al.
2016). From the plant’s perspective, important fac-
tors to consider include sequence of plants/flowers
visited by the pollinator, the visitation timing and
distance between those flowers, the number of pol-
linators and their morphologies, the adhesive prop-
erties, size, and amount of pollen grains deposited
per floral visit, and the degree of reproductive in-
compatibility of the plant species involved. When a
pollinator visits a flower, it can already be carrying
and could deposit heterospecific pollen (which has
the potential to reduce plant fitness, Waser and
Fugate 1986;Fonseca et al. 2016). Furthermore,
any heterospecific pollen left on the pollinator’s
body can reduce space available for pollen from a
conspecific plant, reducing pollination probability.
Finally, conspecific pollen can be lost and wasted
by pollinator delivery to a heterospecific plant
(Morales and Traveset 2008).
Avian adaptations to collect floral nectar have
been summarized in the appropriately named
“syndrome of anthophily” (Stiles 1981). Features of
this syndrome include a bill that is usually slender
(e.g., Fig. 1), often long and/or curved, and a bifur-
cated tongue tip (grooved, fringed, and/or capable of
rolling into a tube) that is extendable beyond the bill
tip. In contrast with other nectar-feeding animals
(like some bats that store their long tongues deeper
inside their bodies; Muchhala 2006), specialized nec-
tarivorous birds not only have evolved elongated
tongues to reach the nectar, but also long bills to
hold them and allow them to be inserted inside
the nectar chamber with enough precision to collect
the liquid reward efficiently (Stiles 1981). In fact, bill
length and shape are considered key to functional
trait matching, because while tongues may extend
far beyond the bill tip, in most birds, tongues have
motion control only at their base and are too flimsy
to traverse barriers within the flower on their own
(e.g., Rico-Guevara et al. 2019). Here, we focus on
hummingbirds, the most speciose group of anthoph-
ilous vertebrates. Hummingbirds exhibit a wide array
of traits associated with their dependence on nectar-
feeding (Stiles 1981;Fleming and Muchhala 2008),
which allow them to feed on flowers well enough to
make their living out of small volumes of nectar.
Presumed adaptations to nectarivory in humming-
birds range from the traditionally recognized ones
(such as elongated bills) that evolved more than 30
million years ago (Mayr 2004), to specialized tongue
elastic properties described recently (Rico-Guevara et
al. 2015). Hummingbird feeding apparatus present a
variety of minute structures at their tips that are
believed to be adaptations to improve the collection
and transport of nectar (Rico-Guevara and Rubega
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2011,2017). We discuss the evolution of presumed
functional trait matching between hummingbird bills
and flowers and propose tools to study this interac-
tion from biomechanical and behavioral perspectives.
Similar to their pollinators, hummingbird-
pollinated plants have repeatedly evolved a suite of
traits that characterize them as throchiliphilous
(plants that use hummingbirds as pollination vec-
tors). Such convergent traits deviate to varying
degrees from the ancestral states of entomophilous
(insect-pollinated) plants and include larger flowers,
increased correspondence with the bills of the hum-
mingbirds that are pollinating those flowers, fine-
tuned placement of reproductive organs to contact
hummingbird surfaces (different areas in the bill,
head, and throat), larger volumes of more dilute
nectar, overall larger caloric rewards, reduced or ab-
sent nectar amino acids, reddish coloration, reduced
scent cues, and in some cases, hanging (pendant)
flowers that are reached via hovering, or inflorescen-
ces shaped to support the weight of clinging birds
(Stiles 1978; Mart
ınez del Rio et al. 2001;Rocca and
Sazima 2010;Pauw 2019). Some species may explore
other food sources when there is intense competi-
tion, for example, recent studies have shown that
hummingbirds include nonthrochiliphilous plants
in their diet (e.g., Bee hummingbirds: Dalsgaard et
al. 2008,2009;Waser et al. 2018;Wessinger et al.
2019), demonstrating the importance of studying be-
havioral plasticity and expanding studies to all the
potential sources of nectar in a given environment.
Throchiliphilous plants (approximately 7,000 spp.)
have likely independently evolved hundreds of times
across 68 families (Thomson and Wilson 2008;
Abrahamczyk and Renner 2015), highlighting the
importance of hummingbirds as pollinators in a va-
riety of ecosystems.
Traits that are likely involved in functional trait
matching, such as bill and floral morphologies are
well characterized. Similarly, the interactions between
a hummingbird and ornithophilous plant species in
pollination networks are also well known. The key
gap in our knowledge is understanding how the
expected benefits from functional trait matching
are achieved. In this perspective piece, we discuss
how hummingbird behavior and morphological
matching between the feeding apparatus of hum-
mingbirds and the floral structures of plants interact
and modulate the benefits for both the plant and
pollinator. From the hummingbird perspective, we
discuss adaptations that enhance the extraction of
floral rewards, focusing on nectar drinking efficiency,
as this is the most prominent link between the evo-
lution of nectarivory in birds and coevolution with
ornithophilous plants. To understand the general
benefits of trait matching, we present novel methods
that could allow researchers to quantify the benefits
of trait matching. The tools we present provide a
window into how the hummingbirds interact with
the flowers at the moment of the floral visit,
highlighting the importance of considering behavior
as an integral part of the study of trait matching
between hummingbirds and the plants they pollinate.
Evolution of trait matching in
hummingbird–plant interactions
Determining whether trait matching is functional
(i.e., benefits both hummingbird and plant) depends
in part on understanding how mutualists may be
driving coevolution. The close physical match be-
tween slender hummingbird bills and the elongated
and narrow-entranced corollas of hummingbird pol-
linated plants is frequently interpreted as sufficient
evidence of reciprocal adaptation between these two
mutualist groups (see Cronk and Ojeda 2008).
Indeed, there is a strong evidence that hummingbird
pollination drives the diversification of
hummingbird-pollinated plants and the evolution
of their floral morphology (Temeles et al. 2002;
Pauw 2019;Wessinger et al. 2019).
Fig. 1. Strategies in hummingbird–plant coevolutionary systems.
(A) Generalist Indigo-capped hummingbird (Saucerottia cyanifrons)
visiting a flower of a leguminous tree (Calliandra spp.), a plant that
also exhibits a generalist strategy (Hern
andez-Conrique et al.
2007). (B) Specialist Black-throated mango (Anthracothorax nigri-
collis) visiting a specialized throchiliphilous plant (Aphelandra spp.).
Photos taken at the Colibr
ı Gorriazul Research Station, near
a, Colombia, courtesy of Ricardo Zarate.
Bene“fit” in bill–corolla coevolution 3
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However, floral traits that appear to be matched
with hummingbird pollination may also be to some
extent a consequence of historical contingency,
rather than having evolved to match exclusively
within the plant–hummingbird association.
Hummingbird pollination is thought to be rarely an-
cestral and transitions from insect pollination to
hummingbird pollination are the norm (Tripp and
Manos 2008;Serrano-Serrano et al. 2017;Dellinger
et al. 2019;Wessinger et al. 2019). In transitions to
hummingbird pollination, morphological traits asso-
ciated with hummingbird pollinated flowers might
therefore evolve as a function of increasing exclusion
of less efficient insect pollinators (and release from
the interspecific competition via heterospecific pollen
transfer) when hummingbird pollination is assured
(Arcos et al. 2018). Experimental studies provide
substantial support for this interpretation (Mackin
et al. 2021). Elongated and narrow-entranced corol-
las reduce the efficiency of insects as pollinators and
also reduce insect pollinator preference for these
flowers, making them less able to handle the flower
and extract nectar (Castellanos et al. 2004;Gegear
et al. 2017;Arcos et al. 2018). Similarly, transitions
from hummingbird pollinated to insect pollinated or
to mixed pollination systems exhibit shifts toward
shorter and wider-entranced corollas that enhance
insect pollination but have no effect on humming-
bird pollination effectiveness (Tripp and Manos
2008;Arcos et al. 2018).
Altogether, the evidence suggests that the match
between hummingbird bills and corollas may be
driven in large part not by coevolution between
hummingbirds and throchiliphilous plants (in which
both bill and flower shape evolve to match each
other) but by selection on floral shape to filter out
less effective insect pollinators (evolving narrow and
long corollas and other filtering mechanisms).
Hummingbirds are more effective pollinators even
of many insect-pollinated plants (Thomson and
Wilson 2008), and so selection favors floral mor-
phology that excludes insect visitors when more ef-
fective hummingbird pollinators are present. In turn,
these elongated flowers with narrow entrances drive
selection on hummingbird bills to be thinner and
longer to match floral morphology. Once this prom-
inent hummingbird hallmark, the slender bill,
evolved, it became a historical contingency that was
likely perpetuated through “guild coevolution” (see
below). Insect exclusion seems to have driven the
evolution of narrow flowers and subsequent slender
bills; however, it seems unlikely that plants that have
recently transitioned to rely on hummingbird polli-
nators exert strong selection on hummingbird bill
shape. Instead, it is more likely that associated flow-
ers evolve to “fit the bill” (Wilson et al. 2006;Arcos
et al. 2018), although rare cases of strong pairwise
coevolution undoubtedly occur (Stein 1992;
Abrahamczyk et al. 2014;Lagomarsino 2015).
Most hummingbird species have bills likely capa-
ble of extracting nectar from most trochiliphilous
plants, regardless of shared coevolutionary history
(aka guild coevolution) (Cotton 1998). For example,
the Green-backed firecrown (Sephanoides sephanio-
des) a hummingbird only found in South American
latitudes, would be able to feed on the flowers of
plants that originated and coevolved with North
American hummingbird species, due to similar selec-
tive pressures where both hummingbirds and thro-
chiliphilous plants occur. In all hummingbird–plant
assemblages, there are common inefficient pollina-
tors (like short-tongued bees) that need to be re-
stricted from crawling inside the flower to access
the nectar. This is the consensus explanation for
why tubular flowers have narrow entrances (too nar-
row for insect bodies) and elongated corollas (too
long for insect mouthparts to access e.g.,
es and Llandres 2008;Dalsgaard
et al. 2009). While there are many other insect pol-
linators that could potentially still reach the nectar,
hummingbird-pollinated plants have additional bar-
riers at the entrance of the nectar chamber that pre-
vent even long insect mouthparts from accessing the
nectar. For example, microtrichia on internal flaps
projecting from the internal corolla walls require suf-
ficient physical strength to be surpassed; humming-
birds, but not insects, can push their mouthparts
through, specifically, their bill tips (Wolf et al.
In addition, independent appearances of trochi-
liphily among plants (see Introduction to plant–pol-
linator functional trait matching section) are
common (Wessinger et al. 2019). Plant clades that
switch to be hummingbird-pollinated frequently
evolve with local hummingbirds feeding on other
co-occurring trochiliphilous plants (Serrano-Serrano
et al. 2017). These new trochiliphilous clades con-
verge on similar floral traits to take advantage of
existing hummingbird pollinators, thus also resulting
in selection for these hummingbirds to maintain
existing bill morphology to sustain efficient nectar
extraction. This pattern of evolution seems to be
the norm in hummingbird–plant assemblages
(Temeles et al. 2002;Maglianesi et al. 2014;
Weinstein and Graham 2017). Nonetheless, extreme
cases of bill–corolla matching do occasionally occur,
in which hummingbirds have evolved uncommon
bill morphologies that often match the lengths and
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curvatures of the flowers they feed on. Examples of
this include the Sword-billed hummingbird (Ensifera
ensifera) with an exceptionally long bill that matches
the elongated corolla of the Passion flowers
(Passiflora spp.) they visit (Lindberg and Olesen
2001;Abrahamczyk et al. 2014), and the Sicklebill
hummingbirds (Eutoxeres spp.) with exceptionally
curved bills that match the curvature of the
Heliconia and Centropogon flowers they feed on
(Stein 1992;Lagomarsino 2015). These extreme cases
of bill–corolla matching are likely cases of runaway
reciprocal exploitation, in which coevolutionary
trends of functional trait matching go beyond what
is strictly required to reduce competition on both
the bird and the plant sides, if the benefits from a
tighter match among the assemblage of species con-
tinue to be advantageous.
Physical components of hummingbird–
plant trait matching and pollination
Our understanding of the selective forces at play
during the evolution of bill–corolla matching is
greatly improved by considering the physical mech-
anisms that determine the benefits of stronger
matching (Box 1 ). While in this section, we primar-
ily consider trait-matching benefits at the level of
isolated bird–plant coevolution, in the next section,
we discuss interference competition and its potential
to influence bill shape evolution (thus also affecting
coevolutionary processes, see Behavioral components
of hummingbird–plant trait matching section). Thus,
the mechanistic principles we describe here can be
transferred to the level of an assemblage of compet-
ing pollinators and plants, providing a more com-
prehensive explanation for how trait matching
Part of the rationale behind the bill–corolla
matching coevolution explanation is that humming-
bird individuals of a given species (or sex) should
obtain higher net energy gain while feeding on flow-
ers matching their bill length and shape. One com-
plication of this explanation comes from the fact that
hummingbirds have tongues that can be extended up
to two times their bill length (Rico-Guevara 2017),
and it is unknown to which degree this protrusion
ability varies across species, especially during nectar
feeding. For example, of the two coexisting species in
which one has a bill that is half as long as the other
(or three-fourths as long as in Fig. 1), an individual
from the short-billed species, by extending its
tongue, could potentially reach the nectar in flowers
that “match” the long-bill species better. In fact,
many species of hummingbirds visit flowers with
corollas longer than their bills (Dalsgaard et al.
2021). Which begs the question, is the difference in
bill length sufficient to result in niche partitioning?
Three factors need to be considered here. (1)
Hummingbird tongues are mostly inert structures
that only have motion control at their base (e.g.,
Rico-Guevara et al. 2019); thus, when the tongue is
extended inside the flower, it behaves like a thread
that could get stuck to one of the sides of the co-
rolla, bent among floral reproductive structures, and
other vicissitudes. Hummingbird bills are rigid struc-
tures that guide the tongue through the length of the
corolla. (2) Along the same line, many hummingbird
pollinated flowers have nectar chamber barriers that
need to be passed to access the liquid reward.
Hummingbird tongues are too flimsy to transverse
these obstacles on their own, therefore, bill tips also
provide the final push to access the nectar deep in-
side the flower. Finally, (3) longer bills, by probing
deeper inside corollas, achieve smaller distances be-
tween bill tips and nectar than shorter bills. Smaller
bill tip–nectar distances yield greater licking rates
(Ewald and Williams 1982) because the tongue needs
to travel a shorter distance while reciprocating to
collect the liquid, and this, in turn, results in higher
nectar extraction efficiency (Hainsworth 1973;
Hainsworth and Wolf 1976;Montgomerie 1984;
Grant and Temeles 1992;Temeles and Roberts
1993;Temeles 1996). Under this lens, with every-
thing else being equal, bills with a higher match to
the flower shape are expected to be more efficient in
terms of nectar intake rate (Wolf et al. 1972;Temeles
and Kress 2010). However, tests of this hypothesis
have produced conflicting results. For example, we
would expect that long-billed species are more effi-
cient on long-tubed flowers and short-billed hum-
mingbirds are more efficient on short-tubed
flowers, but experimental results do not support
the second prediction (e.g., Hainsworth 1973;
Montgomerie 1984;Temeles and Roberts 1993;
Temeles 1996). In fact, under experimental condi-
tions, longer-billed birds feed more quickly from
longer flowers than shorter-billed birds, but
shorter-billed birds do not feed more quickly from
shorter flowers than longer-billed ones (Temeles
1996;Temeles et al. 2002,2009). If long bills can
also reach the rewards inside short corollas, mini-
mizing bill tip—nectar distances, and achieving
higher energy intake rates (Montgomerie 1984),
why does not selection always favor longer bills?
Drawbacks associated with longer bills include
that longer-billed hummingbirds make more inser-
tion errors when feeding in short, narrow flowers
compared to shorter-billed hummingbirds (Temeles
Bene“fit” in bill–corolla coevolution 5
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1996). Insertion errors would increase the total time
required per floral visit and therefore reduce net en-
ergy gain per visit. Similarly, wielding long bills
might reduce control of fine adjustments that are
required to properly position the bill tip and tongue
to transverse the internal floral barriers (when pre-
sent) that prevent easy access to the nectary and
reaching all folds containing nectar. Additionally,
longer bills may require longer intraoral transport
times given that after offloading the nectar near
the bill tip, the liquid needs to be actively trans-
ported to the throat (Rico-Guevara 2014). Shorter
bills reduce the distance between the body of the
bird and substrate surfaces that could be used for
support (e.g., feeding while clinging or on the
ground). Employing substrates for weight support
greatly reduces energy expenditure (hovering is en-
ergetically expensive), and thus many hummingbirds
regularly perch to perform several consecutive visits,
even from the same perching position (e.g., in
Asteraceae inflorescences Stiles 2008). Finally, by be-
ing closer to the flower, hummingbirds with short
bills can more easily perforate the corolla near the
nectary to reach the nectar and more easily exploit
existing holes in the corolla made by other visitors
(Lara and Ornelas 2001).
Although we have focused on bill length, a suite of
traits are involved in bill–corolla trait matching; for
example, bill curvature shows trait matching with
flower shape (Maglianesi et al. 2014). The extremes
of these trait-matching axes (length and curvature)
are reflected in their morphological diversification
into a novel range of bill shapes (Cooney et al.
on et al. 2021). To showcase morpholog-
ical extremes, compare the short straight beaks
(7 mm) of Purple-backed thornbills
(Ramphomicron microrhynchum) to the extremely
long (100 mm) and slightly recurved bills (poten-
tially enhancing visits to pendulous flowers, Stiles
2008) of Sword-billed hummingbirds, to the 90de-
curved bills of Sicklebill hummingbirds, matching
their preferred flowers (Stein 1992). While hum-
mingbird assemblages are often composed of species
with more modest differences in bill shape (but see
Rico-Guevara 2008), it is an open question whether
there is typically sufficient morphological diversity
for trait-derived niche partitioning to develop.
Other factors such as phenological and microhabitat
Here we present the parameters that would ideally be measured to evaluate the benefits to the hummingbird from trait matching
via quantification of hummingbird nectar extraction performance in the wild (Fig. 2). When a hummingbird feeds on a flower that matches
its bill shape, it would be expected to obtain a larger net energy gain (calories acquired minus invested) than when feeding on a flower with a
poorer match. For example, the hummingbird might be able to more efficiently insert its bill into the flower, reducing its time to access nectar
(handling time minus licking time), increase extraction efficiency, and collect a larger reward. By measuring the amount of nectar in the
flower and the licking rate, we can calculate the volumetric extraction efficiency (ll/s), and with a range of potential values for nectar
concentration in a particular flower, we can estimate the energy intake rate (cal/s). While it is not possible to measure the precise nectar
concentration consumed in a given floral visit without disturbing the system, the best approximation involves measuring the nectar con-
centration on the same lower but at a different time, or at the same time from adjacent flowers, or by characterizing nectar concentration
variation among flowers and across the relevant temporal scale (e.g. daily fluctuation). Nectar concentration is commonly measured via a
refractometer, following extraction of nectar from ‘bagged’ flowers (preventing visitors from extracting nectar) via microcapillary tubes.
nectar concentration = cal/μl
licking rate
Fig. 2. Variables for quantification of hummingbird drinking per-
formance during visits to wild flowers. Energy intake rate (cal/s)
¼extraction efficiency (ml/s)nectar concentration (cal/ml). See
text for a discussion of licking rate and handling time.
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overlap, abundance (e.g., V
azquez et al. 2009), and
type of competitive interactions (see Behavioral com-
ponents of hummingbird–plant trait matching sec-
tion) need to be considered to achieve a full
understanding of the magnitude of the importance
of functional trait-matching in determining hum-
mingbird–plant networks. Similar to bill length, bill
curvature shows trait matching with flower shape
(Maglianesi et al. 2014). Even if corolla and bill
length correspond, if curvature differs, benefits
from the length match will be greatly reduced or
even nullified for plant and hummingbird.
Similarly, benefits will not be fully realized if bill–
corolla curvature, but not lengths, match [see discus-
sion on curvature measurement methods in (Rico-
Guevara and Araya-Salas 2015)]. Finally, the corolla
and nectar chamber entrances restrict access also
based on bill and tongue thickness (see Evolution
of trait matching in hummingbird–plant interactions
section), and the depth to which the bill can pene-
trate the corolla depends on its internal configura-
tion. For example, a thicker bill tip and/or tongue
could prevent deep access inside the flower because
of corollar internal diameter constraints and/or the
presence of reproductive structures (stigma and/or
anthers) that reduce the bill tip mobility (Smith et
al. 1996). The actual bill tip space required for effec-
tive drinking is determined by the bill tip thickness
when the bill is opened to receive the tongue full of
nectar. Therefore, the thicker the tongue, the larger
the opening has to be to allow for access to the fully
loaded tongue (Grant and Temeles 1992). Given the
suite of physical traits that have to be considered to
characterize bill–corolla functional trait matching, a
thorough experimental and quantitative exploration
of the reciprocal benefits determined by matching
hummingbird bill–flower morphospaces is war-
ranted. Imperfect bill–corolla match does not neces-
sarily restrict access to the nectar of throchiliphilous
plants (or even other plants e.g., Waser et al. 2018),
and so hummingbirds can feed on a variety of floral
resources. Characterizing the costs and benefits of
physical trait matching, while considering the behav-
ioral and ecological context will be a key to under-
standing how they might drive coevolution.
While we have focused primarily on the pollina-
tor’s perspective, from the plant’s perspective, the
benefits for an individual plant from increased bill–
flower matching come from enhanced pollen depo-
sition on pollinator surfaces that ultimately contact a
conspecific flower’s stigma (cross-pollination, e.g.,
Betts et al. 2015). In terms of trait matching, there
is strong selection on floral morphology that forces
the pollinator into a position in which pollen is
picked up through contact with the anthers (from
the male perspective) and that effectively deposits
conspecific pollen onto the stigma (from the female
perspective). Reduced bill–flower fit might either re-
sult in lower chances of pollen dispersal because the
flower becomes a less desirable resource for the pol-
linator (if it experiences low net energy gain), or in
nectar extraction by the pollinator without proper
pollen transfer (e.g., robbing or mismatch between
floral reproductive organ surfaces and pollinator sur-
faces, e.g., Betts et al. 2015). The effects on pollen
deposition and actual transport (how much of it can
remain) on a given surface (e.g., forehead) of a pol-
linator, especially in the face of multiple consecutive
deployments, need to be documented to better un-
derstand the influence of foraging circuits (see
Behavioral components of hummingbird–plant trait
matching section) and mechanisms influencing pol-
lination outcomes. There are many open questions
regarding the underlying physical mechanisms in-
volved in successful pollen transfer. For example,
by pressing against the pollinator, does the anther
remove previously deposited pollen? Are different
structural and/or chemical properties of pollen adap-
tive in terms of pollen deposition and transport on
the pollinator and transfer to the stigma? Are partic-
ular pollinator surfaces adapted for pollen dispersal
(e.g., feathers)? Does preening/cleaning remove pol-
len and how often does this behavior occur between
floral visits (e.g., bill rubbing against branches)?
These are just a few of the many possible questions
relating to mechanisms potentially enhancing or dis-
rupting trait matching, but they stress the impor-
tance of quantifying both physical mechanisms and
behavioral components.
Behavioral components of
hummingbird–plant trait matching
While we have considered functional trait matching
mostly as a consequence of physical mechanisms,
animal behavior at multiple scales plays a powerful
role in determining the degree to which physical
components contribute to functional trait matching.
For example, at the level of individual floral visits,
cognitive flexibility and behavioral plasticity in hum-
mingbird lapping rate (e.g., Roberts 1995) and
tongue protrusion distance (Rico-Guevara 2017)
could enable hummingbirds to functionally adjust
their match to different flowers. Thus, even when
bill and flower seem morphologically matched, be-
havioral plasticity could expand the range of matches
to some degree. In addition, learning and cognition
generally (recently reviewed by Gonz
omez and
Bene“fit” in bill–corolla coevolution 7
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Araya-Salas 2019), preference (related to particular
behavioral strategies), and competition (related to
abundance of both resources and competitors e.g.,
Simmons et al. 2019) are potentially powerful behav-
ioral components of functional trait matching evo-
lution. Here, we focus on behavioral strategies at the
level of landscape (defense and movement among
floral resources) and its consequences for the evolu-
tion of bill–flower matching in hummingbird–plant
assemblages. Optimal foraging theory predicts that
hummingbirds should attempt to balance costs and
benefits associated with finding and extracting better
quality nectar rewards (Heinrich 1975;Stiles 1975;
Pyke 2019;Blem et al. 2000). However, to achieve
a net positive energy gain, hummingbirds might con-
ceivably visit flowers that are a poor functional
match to their bills. As long as the hummingbird
achieves a net positive energy gain, a hummingbird
may, for example, prefer to visit flowers that are
close together to reduce costs associated with search-
ing, even if the bill–corolla match for some of those
flowers is poor. In addition, trochiliphilous flowers
frequently conceal their nectar deep within the nec-
tary, lacking visual, olfactory, or electrostatic cues
associated with the reward (Rocca and Sazima
2010;Lunau et al. 2020;Pauw et al. 2020), unlike,
for example, bee-pollinated plants (Clarke et al.
2013;Russell et al. 2018). Consequently, achieving
a net positive energy gain from flowers is a proba-
bilistic game that has multiple successful behavioral
strategies (Feinsinger and Colwell 1978).
Here, we provide new terms to focus on two
widely observed and presumably mutually exclusive
behavioral strategies thought to maximize net energy
gain, and which have consequences for plant repro-
ductive success: (1) stationary interference (formerly
“territoriality”), in which individuals stay within a
resource patch and use aggressive behaviors to inter-
fere with attempts of different nectarivores to access
the patch and (2) traveling exploitation (formerly
“traplining”), in which individuals forage on resour-
ces scattered across the landscape, traveling among
foraging areas in a particular sequence (e.g., Stiles
1975;Feinsinger and Colwell 1978;Tello-Ramos et
al. 2015, see Kamath and Wesner 2020;Sargent et al.
2021) for a discussion on the controversies and
semantic problems with the prior terms). These
new terms describe both the predominant
landscape range and the type of competition
associated with these ends of the spectrum of
behavioral strategies. A stationary interference
strategy is expected to be used when tolerating
other nectarivores is costly, such as when floral
nectar is readily accessible to a diverse assemblage
of pollinators (Stiles 1975). This is because
interfering with the foraging of competitors is most
useful when competitors can access the resource as
easily as the interferer, resulting in agonistic
interactions collectively known as interference
competition (Rico-Guevara et al. 2019). Conversely,
when foraging on a specific plant species carries a
net positive benefit for only well-matched nectari-
vores, the focal pollinator is released from the need
to defend nectar resources from all possible nectar-
ivores (see Sargent et al. 2021). The net energy gain
is thus maximized by visiting only flowers with a
good match, regardless of their spatial proximity
and thus a traveling exploitation strategy may be
favored, in which pollinators visit plants scattered
across a broad range (Ohashi and Thomson 2009;
Buatois and Lihoreau 2016). Note that this is differ-
ent from how the term traplining has been applied
to foraging circuits independent of the scale at which
they occur (Tello-Ramos et al. 2015). From this per-
spective, traplining can also be performed by a sta-
tionary interferer while visiting the flowers in a given
patch, while also defending it (Tello-Ramos et al.
2015). In our new terminology, a traveling exploiter,
by definition, does not stay in an area to defend the
resources within.
When hummingbirds restrict access to resource
patches via stationary interference, this strategy can
shift the realized hummingbird–plant interactions
from what would be expected given the fundamental
niche distribution based only upon bill–corolla
matching. Stationary interference is linked to aggres-
sive behavior, which can also be a strong selective
force on hummingbird bill morphology, and thus
indirectly drive selection on flower shape and other
aspects of a plant’s reproductive strategy via coevo-
lution. Indeed, agonistic behaviors are associated
with at least some bill traits in the context of intra-
sexual competition and evolution of intrasexually se-
lected weapons (Rico-Guevara and Araya-Salas 2015;
Rico-Guevara and Hurme 2019), and have been pro-
posed to be associated with interspecific competition
(Rico-Guevara et al. 2019). For example, physical
confrontations in which the bill is used to contact
the opponent could select for (1) longer beaks that
provide increased reach to stab an opponent before
getting stabbed, (2) straighter beaks that transmit the
force from bill base to tip better, (3) thicker beaks
that can withstand higher axial loadings, (4) sharper
bill tips that can pierce with less applied force, and
(5) stronger bill tips that resist bending forces while
biting (e.g., to pluck feathers or physically displace
8A. Rico-Guevara et al.
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Stationary interference and traveling exploitation
strategies may also influence the benefits for the
plant, beyond simple differences in conspecific pollen
transfer. For example, stationary interference is likely
to reduce pollen dispersal of the defended plants,
assuming that displacing other pollinators reduces
floral visitation rate, and could also increase hetero-
specific pollen transfer when interferers visit multiple
plant species in the same area (Ashman and Arceo-
omez 2013). In addition, stationary interference is
likely to reduce outcrossing, as pollen will be mostly
transferred among the defended plants (Torres-
Vanegas et al. 2019). Traveling exploitation on the
other hand involves the pollinator visiting flowers in
a discrete sequence across the landscape, thus shap-
ing the direction of pollen movement. As a result,
one plant in the visitation sequence may always serve
as a pollen donor, while another in the sequence
may always serve as a pollen recipient, even if the
individual plants are widely separated (e.g., Ohashi
and Thomson 2009, but see Torres-Vanegas et al.
2019). Traveling exploitation and stationary interfer-
ence lie at the extremes of a continuum between
exploitative and interference competition (Rico-
Guevara et al. 2019) that can select for a variety of
behavioral and morphological traits that can directly
impact pollination. In an assemblage of spatiotem-
porally coexisting hummingbirds and hummingbird-
visited plants (a pollinator interaction network, see
Approaches to studying hummingbird–plant (bill–
corolla) trait matching section), the foraging links
between particular plants and birds, as well as their
strength (e.g., the proportion of visits for both par-
ties), depend on pollinator behavior. Similarly, plant
and hummingbird abundance and phenology can
also affect the links between them and thus the
strength of selection (V
azquez et al. 2009). At the
community level, additional evolutionary processes
need also to be considered to link mechanisms and
patterns at different ecological scales. For example,
character displacement on hummingbirds feeding on
coexisting plants can partially explain their astonish-
ing diversity in bill shape and size (Maglianesi et al.
2014). Similarly, intersexual floral resource partition-
ing is thought to at least in part explain sexual di-
morphism in bill morphology (Temeles et al. 2000,
2010). Furthermore, character displacement likely
drives the evolution of diverse floral morphologies
and pollen deposition and collection strategies
among plants (e.g., different lengths of anthers aim-
ing at different body surfaces, lever mechanisms, ex-
plosive pollen release, modified petals, etc. (Aluri
and Reddi 1995;Rengifo et al. 2006;Temeles and
Rankin 2011;LoPresti et al. 2020)).
Approaches to studying hummingbird–
plant (bill–corolla) trait matching
Inferences about reciprocal specialization between
hummingbird bills and the flowers they pollinate
are frequently drawn from research on humming-
bird–plant interaction networks (examples in
Supplementary Table S1). These studies establish
which hummingbird and plant species interact and
can generate hypotheses for putative benefits of bill–
corolla trait matching (e.g., Maglianesi et al. 2014).
While plant–pollinator networks suggest that func-
tional trait matching maintains links among species,
the determinants of both pollination and nectarivory
at the level of the floral visits are poorly understood.
Moreover, evaluating the inferred benefits or draw-
backs of particular interactions for plants and polli-
nators requires a detailed look at what happens
during a floral visit. Therefore, to help guide future
research, we provide a comparison of different net-
work building methods (Supplementary Table S1)
used to characterize benefits to hummingbird and
plant and thus assess the mechanisms enabling pu-
tative bill–corolla coevolution. We focus in particular
on the value of video, because while some methods
effectively characterize which plants and humming-
birds are interacting, as well as the strength of these
interactions (e.g., number of visits, their frequency,
and the amount of pollen found on the pollinator),
only video recordings enable precise characterization
of hummingbird behavior on flowers and the inter-
action between floral reproductive organs and the
hummingbird. Recent video footage of plant–polli-
nator interactions has unveiled pollinator fidelity to
their resources even in times of low abundance and a
relatively high occurrence of nectar-robbing
(Weinstein and Graham 2017), as well as highlighted
the influence of spatial distributions in trait-
matching and resulting morphotypes (Sonne et al.
In addition to the importance of quantifying pol-
lination network interactions, it is necessary to un-
derstand how they are modulated through a
common currency: net energy gain. The main pro-
posed benefit of bill–corolla matching from the pol-
linator’s perspective is an increase in net energy gain
(Box 1), which is a consequence of (1) nectar accu-
mulation in specialized flowers (if competitors can-
not access or are morphologically discouraged from
accessing the reward, Behavioral components of
hummingbird–plant trait matching section), (2) re-
duced access time to the flower entrance and nectary
(Physical components of hummingbird–plant trait
matching and pollination section), and (3) increased
Bene“fit” in bill–corolla coevolution 9
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nectar intake efficiency. Measuring nectar replenish-
ment (without affecting floral visitation) and feeding
performance in wild flowers was practically impossi-
ble until recent technological advances, thus, nectar
drinking has been mostly studied under artificial
conditions (e.g., Roberts 1995;Collins 2008;Rico-
Guevara et al. 2019). In particular, advances in vid-
eography capabilities and affordability (see discus-
sion about costs in Rico-Guevara and Mickley
2017) have been a game changer. Video recordings
are comprehensive in capturing both successful and
unsuccessful attempts to extract nectar from focal
flowers and enabling characterization of alternative
behaviors such as nectar robbing. Similarly, in com-
bination with field data (e.g., nectar concentration
and flower dimensions) they can provide the means
to quantify performance variables involved in evalu-
ating how bill–corolla match shapes net energy gain
(e.g., Fig. 2). We present an overview of the video
techniques that would be applicable to the study of
plant–pollinator and other ecological interactions,
and we finish with an example of one out of the
many possible combinations of those techniques.
To capture hummingbird fast behaviors (e.g., lick-
ing rates up to 17 Hz, Ewald and Williams 1982), we
need high-speed video; to resolve movement and
contact with the floral sex organs or nectar inside
small flowers and tiny nectaries (e.g., the exclusion
of insect pollinators or the movement of the bill
inside the corolla), we need macro-photography;
and to mitigate the influence of the camera on hum-
mingbird behavior, we need tele-photo capabilities
(Supplementary Table S2). Solving these challenges
is possible with specialized and field-friendly cameras
(e.g., Rico-Guevara and Mickley 2017). We present a
combination of backlit-filming, long duration, and
high-speed recording techniques that allows us to
measure rates of nectar depletion and replenishment
in wild flowers. This is key, because to the best of
our knowledge, until this point researchers have not
had a way to measure nectar extraction, which
requires knowing both the uptake rate and the pre-
existing volume of nectar in the flower. Backlit film-
ing allows estimation of the nectar volume without
physically manipulating the flower (e.g., extracting
nectar manually) and thus does not affect floral vis-
itation or damage floral tissues (Fig. 3;
Supplementary Table S2). We performed volumetric
estimations (Supplementary Table S3) of the nectar
through the visualization of the liquid inside the
flower (Supplementary Video S1) and floral dissec-
tions to calculate the internal dimensions of the nec-
tar chamber (Supplementary Fig. S1). Measuring
nectar extraction in unmanipulated wild flowers
takes us a step closer to directly testing the bill–co-
rolla matching benefits from the hummingbird’s
Concluding remarks and implications
for the study of other coevolutionary
Half a century of research on floral foraging by hum-
mingbirds has provided us with a wealth of knowl-
edge about hummingbird nectar preferences
(Hainsworth and Wolf 1976;Stiles 1976;Calder
1979;Tamm and Gass 1986;Mart
ınez del Rio
1990;Stromberg and Johnsen 1990;Roberts 1996;
Blem et al. 1997,2000;Fleming et al. 2004;
Chalcoff et al. 2008), nectar extraction efficiency
(Houston and Krakauer 1993;Roberts 1995;Collins
2008), the role of cognition (Healy and Hurly 2013;
omez and Araya-Salas 2019), and optimi-
zation of foraging and energetics (DeBenedictis et al.
1978;Hixon and Carpenter 1988;Gass and Roberts
1992;Shankar et al. 2019). Despite the breadth of
this literature, we still lack a good understanding of
the mechanisms underlying bill–corolla matching
and their role in maintaining hummingbird–plant
interactions as well as driving coevolution.
Therefore, we endeavored to elucidate these gaps in
our knowledge via a discussion of the evolution and
physical and behavioral components of bill–corolla
matching. To help move this field forward, we
have highlighted key questions and methods that
we hope will facilitate and expand characterization
of functional trait matching for both plant and pol-
linator (Supplementary Tables S1 and S2).
In particular, we emphasize taking a mechanistic
perspective when considering the drivers of adapta-
tions in hummingbird–trochiliphilous plant interac-
tions. Specialized videography is uniquely suited to
characterize the physical interactions between floral
reproductive structures and pollinator surfaces, mak-
ing it possible to quantify the benefits of trait match-
ing for the plant (Physical components of
hummingbird–plant trait matching and pollination
section; Supplementary Table S2). Similarly, video
of hummingbirds drinking from flowers makes it
possible to quantify key parameters needed to deter-
mine costs and benefits for the birds (Fig. 2), such as
energy intake efficiency (Fig. 3), which is one of the
drivers of foraging decisions (Behavioral components
of hummingbird–plant trait matching section) and
thus reciprocal adaptation. Similarly, a combination
of methods (Supplementary Table S1) can be used to
characterize the interaction networks resulting from
those foraging decisions. In addition, with
10 A. Rico-Guevara et al.
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videography we can document visits by different
hummingbirds to focal flowers and hummingbirds
preventing competitors from accessing those flowers,
thus revealing the interplay between exploitative and
interference competition. In other words, videogra-
phy permits us to contrast null expectations of
plant–hummingbird interactions based exclusively
on bill–corolla matching, with the actual interactions
occurring in natural communities and thus the con-
ditions influencing bill–corolla coevolution. Finally,
by combining videography and quantification of
nectar extraction performance with the wealth of
knowledge about hummingbird aerodynamics and
energetics in the context of floral foraging (Sargent
et al. 2021, it becomes possible to quantify net en-
ergy gain, the key benefit of trait matching for the
hummingbird. Altogether, these quantitative and
mechanistic approaches make hummingbird–plant
interactions a model system for studying the benefits
of functional trait matching for both plant and pol-
linator and, more generally, the drivers of
Our proposed framework unites theoretical
expectations and empirical observations to improve
our understanding of the mechanisms constraining
functional trait matching and its evolution. While
the methods and framework presented here concern
the biomechanics and energetics of hummingbird–
flower interactions, they hopefully serve as a tem-
plate for quantifying costs and benefits in other
plant–pollinator systems and ecological interactions.
For example, some of the questions asked about
hummingbird–plant interactions, like bill–corolla
length-matching, are equivalent to questions asked
in bumble bee–plant interactions (tongue-corolla
length-matching e.g., Miller-Struttmann et al.
2015). Similarly, with slight modifications—such as
infrared lights and recording capabilities—equivalent
measurements could be collected for a variety of di-
urnal (e.g., other anthophilous birds, butterflies,
bees) and nocturnal (e.g., bats and moths) nectari-
vores, that sometimes even feed on the same flowers
(e.g., Fig. 1A). Additionally, while behavioral plastic-
ity in flower feeding mechanisms potentially strongly
affects functional trait matching, we have barely
scratched the surface of this subject in a variety of
pollination systems, including anthophilous birds,
rodents, bats, and butterflies (but see work on moths
e.g., Goyret and Raguso 2006;Goyret and Kelber
2011; and work on bees e.g., Russell et al. 2017,
2018;Wei et al. 2020). Finally, biomechanics per-
spectives are often incompletely developed in other
coevolutionary systems, such as the snake–newt–te-
trodotoxin system (e.g., feeding biomechanics that
potentially influences the costs of prey consumption)
and the anemone–anemonefish system (e.g., anemo-
nefish biomechanics that potentially benefits the
host). All in all, the study of physical mechanisms
of behavior is an important avenue for reintegrating
biological sciences and will be an active field of re-
search for years to come.
We thank Patrick Green for organizing the Physical
Mechanisms of Behavior Symposium. We thank
many field assistants and researchers for their sup-
port and discussions in the development of filming
techniques. We are grateful to Patrick Green and
Melissa Morado for their extensive support in man-
uscript preparation and review, and to Derrick
Groom and Alyssa Sargent for discussions. We thank
two anonymous reviewers for their excellent
This work was supported by the Walt Halperin
Endowed Professorship and the Washington
Research Foundation as Distinguished Investigator
(to A.R-G.), and by The Company of Biologists
and the Society of Integrative and Comparative
Conflicts of interest
The authors declare no conflicts of interest.
Extraction Rate (µl/s)
Nectar In Flower (µl)
Time (s)
Fig. 3 Nectar depletion (in blue, left axis, and circles) and ex-
traction rate (in magenta, right axis, and triangles) for a single
visit of a Speckled hummingbird (Adelomyia melanogenys)toa
flower of Palicourea sp. (Supplementary Video S1). Measurements
of nectar pool depletion were performed after every lick
(Supplementary Table S3). Our methods allow for the assess-
ment of feeding performance, at the flower visit level, quantifying
variables that have not been possible to measure to date in the
wild (e.g., maximum bill insertion, access times, licking rates,
liquid collection rates, etc.; Fig. 2).
Bene“fit” in bill–corolla coevolution 11
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Animal ethics statement
Activities are covered by UW IACUC protocol 4498-
Data availability statement
All the data presented and used in graphs are in-
cluded in the supplement.
Supplementary data
Supplementary Data available at ICB online.
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... Hummingbird bill shape is thought to have coevolved with tubular floral corollas (Cotton, 1998;Feinsinger & Colwell, 1978;Leimberger et al., 2022;Rico-Guevara et al., 2021) and hummingbirds have been consistently shown to visit flowers that match their bill shape (e.g., Maglianesi et al., 2014Maglianesi et al., , 2015Weinstein & Graham, 2017). ...
... bill, a segmented tongue, a tendency toward a small body size, and reduced intestinal length (Table 1). More taxa need to be examined for many traits (e.g., kidney morphology, (Pyke, 1980;Rico-Guevara et al., 2021) while honeyeaters have access to open, cup-shaped flowers and flowers with relatively large nectar volumes (Franklin & Noske, 2000;Pyke, 1980), such that nectar is easier to access and extensive tongue protrusion may not be essential for efficient feeding. ...
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.
... 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]. ...
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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.
... However, a high number of feeds with lower space is consistent with expectations under exclusionary competition for resources and is distinct from a feeding strategy with higher space use [53]. Furthermore, the spectrum of behaviours we describe here is well documented in hummingbirds [53,64], and exclusionary competition is conspicuously evident by watching white-necked jacobins interact at both natural and artificial food sources in the wild. ...
Female-limited polymorphisms, where females have multiple forms but males have only one, have been described in a variety of animals, yet are difficult to explain because selection typically is expected to decrease rather than maintain diversity. In the white-necked jacobin (Florisuga mellivora), all males and approximately 20% of females express an ornamented plumage type (androchromic), while other females are non-ornamented (heterochromic). Androchrome females benefit from reduced social harassment, but it remains unclear why both morphs persist. Female morphs may represent balanced alternative behavioural strategies, but an alternative hypothesis is that androchrome females are mimicking males. Here, we test a critical prediction of these hypotheses by measuring morphological, physiological and behavioural traits that relate to resource-holding potential (RHP), or competitive ability. In all these traits, we find little difference between female types, but higher RHP in males. These results, together with previous findings in this species, indicate that androchrome females increase access to food resources through mimicry of more aggressive males. Importantly, the mimicry hypothesis provides a clear theoretical pathway for polymorphism maintenance through frequency-dependent selection. Social dominance mimicry, long suspected to operate between species, can therefore also operate within species, leading to polymorphism and perhaps similarities between sexes more generally.
... They are highly specialised pollinators in the Neotropics (Stiles, 1981;Zanata et al., 2017) with a well-developed visual system (Hickman and Robert, 1993;Pritchard et al., 2017;Tyrrell et al., 2018 and references therein). Indeed, there is experimental evidence that hummingbirds recognise specific floral shapes and prefer visiting those associated to their bill shape and size (Maglianesi et al., 2015;Rico-Guevara et al., 2021). As florivory implies damage to the flowers, which affects flower integrity and shape, we expect that these changes per se could be enough to interfere in the visual communication between flowers and hummingbirds, causing hummingbirds to neglect damaged flowers. ...
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Many flowers are fed on by florivores, but we know little about if and how feeding on flowers affects their visual and chemical advertisement and nectar resource, which could disrupt pollination. Here, we investigated if damages caused by florivores compromise a Neotropical hummingbird pollination system, by modifying the floral advertisements and the nectar resource. We surveyed natural florivory levels and patterns, examined short-term local effects of floral damages caused by the most common florivore, a caterpillar, on floral outline, intra-floral colour pattern and floral scent, as well as on the amount of nectar. Following, we experimentally tested if the most severe florivory pattern affected hummingbird pollination. The feeding activity of the most common florivore did not alter the intra-floral colour pattern, floral scent, and nectar volume, but changed the corolla outline. However, this change did not affect hummingbird pollination. Despite visual floral cues being important for foraging in hummingbirds, our results emphasise that changes in the corolla outline had a neutral effect on pollination, allowing the maintenance of florivore–plant–pollinator systems without detriment to any partner.
... Nectarivory has evolved in a variety of ecological contexts, from tight coevolutionary relationships (e.g. some hummingbirds, Rico-Guevara et al., 2021) to more generalized systems (e.g. honeyeaters, Fleming and Muchhala, 2008;Zanata et al., 2017). ...
Nectar-feeding birds employ unique mechanisms to collect minute liquid rewards hidden within floral structures. In recent years, techniques developed to study drinking mechanisms in hummingbirds have prepared the groundwork for investigating nectar feeding across birds. In most avian nectarivores, fluid intake mechanisms are understudied or simply unknown beyond hypotheses based on their morphological traits, such as their tongues, which are semi-tubular in sunbirds, frayed-tipped in honeyeaters and brush-tipped in lorikeets. Here, we use hummingbirds as a case study to identify and describe the proposed drinking mechanisms to examine the role of those peculiar traits, which will help to disentangle nectar-drinking hypotheses for other groups. We divide nectar drinking into three stages: (1) liquid collection, (2) offloading of aliquots into the mouth and (3) intraoral transport to where the fluid can be swallowed. Investigating the entire drinking process is crucial to fully understand how avian nectarivores feed; nectar-feeding not only involves the collection of nectar with the tongue, but also includes the mechanisms necessary to transfer and move the liquid through the bill and into the throat. We highlight the potential for modern technologies in comparative anatomy [such as microcomputed tomography (μCT) scanning] and biomechanics (such as tracking BaSO4-stained nectar via high-speed fluoroscopy) to elucidate how disparate clades have solved this biophysical puzzle through parallel, convergent or alternative solutions.
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Wild animals and plants have developed a variety of adaptive traits driven by adaptive evolution, an important strategy for species survival and persistence. Uncovering the molecular mechanisms of adaptive evolution is the key to understanding species diversification, phenotypic convergence, and inter-species interaction. As the genome sequences of more and more non-model organisms are becoming available, the focus of studies on molecular mechanisms of adaptive evolution has shifted from the candidate gene method to genetic mapping based on genome-wide scanning. In this study, we reviewed the latest research advances in wild animals and plants, focusing on adaptive traits, convergent evolution, and coevolution. Firstly, we focused on the adaptive evolution of morphological, behavioral, and physiological traits. Secondly, we reviewed the phenotypic convergences of life history traits and responding to environmental pressures, and the underlying molecular convergence mechanisms. Thirdly, we summarized the advances of coevolution, including the four main types: mutualism, parasitism, predation and competition. Overall, these latest advances greatly increase our understanding of the underlying molecular mechanisms for diverse adaptive traits and species interaction, demonstrating that the development of evolutionary biology has been greatly accelerated by multi-omics technologies. Finally, we highlighted the emerging trends and future prospects around the above three aspects of adaptive evolution.
Johnson gives an overview of bird pollinators and the plant species they pollinate.
The function of flower orientation is much debated, with adaptation to pollinator mouthparts being a particularly compelling explanation, but also one that has lacked empirical support from broad-scale comparative studies. The two families of long-proboscid fly pollinators show similar hovering behaviour while feeding on nectar but differ in the biomechanics of their proboscides which can be up to 80 mm in length: Tabanidae have a fixed forward-pointing proboscis while Nemestrinidae can swivel their proboscis downwards. We predicted that this difference has implications for the evolution of flower orientation. We established the flower angles of 156 South African plant species specialised for pollination by long-proboscid flies. Using a phylogenetically corrected analysis, we found that flowers pollinated by Tabanidae tend to be horizontally orientated, while those pollinated by Nemestrinidae tend to be more variable in orientation and more often vertically orientated. These results confirm the importance of pollinator biomechanics for the evolution of floral traits and highlight a potential mechanism of reproductive isolation between sympatric plant species pollinated by different long-proboscid fly families.
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The Andean bellflowers comprise an explosive radiation correlated with shifts to specialized pollination. One diverse clade has evolved with extremely curved floral tubes and is predicted to be pollinated exclusively by one of two parapatric species of sicklebill hummingbirds (Eutoxeres). In this study, we focused on the floral biology of Centropogon granulosus, a bellflower thought to be specialized for pollination by Eutoxeres condamini, in a montane cloud forest site in southeastern Peru. Using camera traps and a pollination exclusion experiment, we documented E. condamini as the sole pollinator of C. granulosus. Visitation by E. condamini was necessary for fruit development. Flowering rates were unequivocally linear and conformed to the “steady‐state” phenological type. Over the course of >1800 h of monitoring, we recorded 12 E. condamini visits totaling 42 s, indicating traplining behavior. As predicted by its curved flowers, C. granulosus is exclusively pollinated by buff‐tailed sicklebill within our study area. We present evidence for the congruence of phenology and visitation as a driver of specialization in this highly diverse clade of Andean bellflowers. Specialized pollination is thought to drive niche partitioning in plants and hummingbirds. Floral curvature is one mode by which specialization is thought to operate, but many pollinator species are elusive and understudied. In this study, we document, for the first time, specialized pollination in the rarely seen buff‐tailed sicklebill hummingbird and the Andean bellflower Centropogon granulosus. Photograph taken by Gloria Jilahuanco (Asociación para la Conservación del Valle de Kosñipata, APCONK). Photo used with permission.
The ecological co-dependency between plants and hummingbirds is a classic example of a mutualistic interaction: hummingbirds rely on floral nectar to fuel their rapid metabolisms, and more than 7000 plant species rely on hummingbirds for pollination. However, threats to hummingbirds are mounting, with 10% of 366 species considered globally threatened and 60% in decline. Despite the important ecological implications of these population declines, no recent review has examined plant–hummingbird interactions in the wider context of their evolution, ecology, and conservation. To provide this overview, we (i) assess the extent to which plants and hummingbirds have coevolved over millions of years, (ii) examine the mechanisms underlying plant–hummingbird interaction frequencies and hummingbird specialization, (iii) explore the factors driving the decline of hummingbird populations, and (iv) map out directions for future research and conservation. We find that, despite close associations between plants and hummingbirds, acquiring evidence for coevolution (versus one-sided adaptation) is difficult because data on fitness outcomes for both partners are required. Thus, linking plant–hummingbird interactions to plant reproduction is not only a major avenue for future coevolutionary work, but also for studies of interaction networks, which rarely incorporate pollinator effectiveness. Nevertheless, over the past decade, a growing body of literature on plant–hummingbird networks suggests that hummingbirds form relationships with plants primarily based on overlapping phenologies and trait-matching between bill length and flower length. On the other hand, species-level specialization appears to depend primarily on local community context, such as hummingbird abundance and nectar availability. Finally, although hummingbirds are commonly viewed as resilient opportunists that thrive in brushy habitats, we find that range size and forest dependency are key predictors of hummingbird extinction risk. A critical direction for future research is to examine how potential stressors – such as habitat loss and fragmentation, climate change, and introduction of non-native plants – may interact to affect hummingbirds and the plants they pollinate.
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Evolutionary variation in ontogeny played a central role in the origin of the avian skull. However, its influence in subsequent bird evolution is largely unexplored. We assess the links between ontogenetic and evolutionary variation of skull morphology in Strisores (nightbirds). Nightbirds span an exceptional range of ecologies, sizes, life-history traits and craniofacial morphologies constituting an ideal test for evo-devo hypotheses of avian craniofacial evolution. These morphologies include superficially ‘juvenile-like’ broad, flat skulls with short rostra and large orbits in swifts, nightjars and allied lineages, and the elongate, narrow rostra and globular skulls of hummingbirds. Here, we show that nightbird skulls undergo large ontogenetic shape changes that differ strongly from widespread avian patterns. While the superficially juvenile-like skull morphology of many adult nightbirds results from convergent evolution, rather than paedomorphosis, the divergent cranial morphology of hummingbirds originates from an evolutionary reversal to a more typical avian ontogenetic trajectory combined with accelerated ontogenetic shape change. Our findings underscore the evolutionary lability of cranial growth and development in birds, and the underappreciated role of this aspect of phenotypic variability in the macroevolutionary diversification of the amniote skull.
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Changes in the pollinator assemblage visiting a plant can have consequences for reproductive success and floral evolution. We studied a recent plant trans-continental range expansion to test whether the acquisition of new pollinator functional groups can lead to rapid adaptive evolution of flowers. In Digitalis purpurea, we compared flower visitors, floral traits and natural selection between native European populations and those in two Neotropical regions, naturalised after independent introductions. Bumblebees are the main pollinators in native populations while both bumblebees and hummingbirds are important visitors in the new range. We confirmed that the birds are effective pollinators and deposit more pollen grains on stigmas than bumblebees. We found convergent changes in the two new regions towards larger proximal corolla tubes, a floral trait that restricts access to nectar to visitors with long mouthparts. There was a strong positive linear selection for this trait in the introduced populations, particularly on the length of the proximal corolla tube, consistent with the addition of hummingbirds as pollinators. Synthesis. The addition of new pollinators is likely to happen often as humans influence the ranges of plants and pollinators but it is also a common feature in the long-term evolution of the angiosperms. We show how novel selection followed by very rapid evolutionary change can be an important force behind the extraordinary diversity of flowers. © 2021 The Authors. Journal of Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society
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Functional traits can determine pairwise species interactions, such as those between plants and pollinators. However, the effects of biogeography and evolutionary history on trait‐matching and trait‐mediated resource specialization remain poorly understood. We compiled a database of 93 mutualistic hummingbird‐plant networks (including 181 hummingbird and 1,256 plant species), complemented by morphological measures of hummingbird bill and floral corolla length. We divided the hummingbirds into their principal clades and used knowledge on hummingbird biogeography to divide the networks into four biogeographical regions: Lowland South America, Andes, North & Central America, and the Caribbean islands. We then tested: (i) whether hummingbird clades and biogeographical regions differ in hummingbird bill length, corolla length of visited flowers and resource specialization, and (ii) whether hummingbirds’ bill length correlates with the corolla length of their food plants and with their level of resource specialization. Hummingbird clades dominated by long‐billed species generally visited longer flowers and were the most exclusive in their resource use. Bill and corolla length and the degree of resource specialization were similar across mainland regions, but the Caribbean islands had shorter flowers and hummingbirds with more generalized interaction niches. Bill and corolla length correlated in all regions and most clades, i.e. trait‐matching was a recurrent phenomenon in hummingbird‐plant associations. In contrast, bill length did not generally mediate resource specialization, as bill length was only weakly correlated with resource specialization within one hummingbird clade (Brilliants) and in the regions of Lowland South America and the Andes in which plants and hummingbirds have a long co‐evolutionary history. Supplementary analyses including bill curvature confirmed that bill morphology (length and curvature) does not in general predict resource specialization. These results demonstrate how biogeographical and evolutionary histories can modulate the effects of functional traits on species interactions, and that traits better predict functional groups of interaction partners (i.e. trait‐matching) than resource specialization. These findings reveal that functional traits have great potential, but also key limitations, as a tool for developing more mechanistic approaches in community ecology.
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Nectarivorous insects generally adopt suction or lapping to extract nectar from flowers and it is believed that each species exhibits one specific feeding pattern. In recent literature, large groups of nectarivores are classified as either 'suction feeders', imbibing nectar through their proboscis, or 'lappers', using viscous dipping. Honeybees (Apis mellifera) are the well-known lappers by virtue of their hairy tongues. Surprisingly, we found that honeybees also employ active suction when feeding on nectar with low viscosity, defying their classification as lappers. Further experiments showed that suction yielded higher uptake rates when ingesting low-concentration nectar, while lapping resulted in faster uptake when ingesting nectar with higher sugar content. We found that the optimal concentration of suction mode in honeybees coincided with the one calculated for other typical suction feeders. Moreover, we found behavioural flexibility in the drinking mode: a bee is able to switch between lapping and suction when offered different nectar concentrations. Such volitional switching in bees can enhance their feeding capabilities, allowing them to efficiently exploit the variety of concentrations presented in floral nectars, enhancing their adaptability to a wide range of energy sources.
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• The large body of work on the adaptation of plants to pollinators is still somewhat incomplete because most studies focus on one‐to‐one interactions. How will adaptation proceed in a multi‐pollinator environment? According to Stebbins’ Most Effective Pollinator Principle, “the characteristics of the flower will be molded by those pollinators that visit it most frequently and effectively”. • To test this hypothesis, we studied the pollination biology of Pelargonium incrassatum (Geraniaceae) in the Namaqualand Region of Southern Africa. The species has a long floral tube and we expected its most important pollinator to have a long proboscis. • Contrary to expectations the most important pollinator was a short proboscid fly (a new species of Prosoeca ), while Prosoeca peringueyi , which had a proboscis that matched the floral tube length, was a rare visitor. Consistent with the high degree of trait mismatching, we did not detect selection on tube length at most sites. • The paradox of mismatching traits can be resolved by considering the strength of the trade‐off involved. Adaptation to the rare species can apparently occur without incurring the cost of reduced pollination by the abundant species. Generally, species may often evolve specialized morphology if they do not incur the cost of ecological specialization.
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Nectar is the most common floral reward for flower-visiting flies, bees, bats and birds. Many flowers hide nectar in the floral tube and preclude sensing of nectar by flower-visitors from a distance. Even in those flowers that offer easily accessible nectar, the nectaries are mostly inconspicuous to the human eye and the amount of nectar is sparse. It is widely accepted that many flowers display nectar guides in order to direct flower-visitors towards the nectar. Using false colour photography, covering ultraviolet, blue and green ranges of wavelength, revealed a yet unknown conspicuousness of nectar, nectaries and false nectaries for bees due to concordant reflection in the ultraviolet range of wavelength. Nectars, many nectaries and false nectaries have glossy surfaces and reflect all incident light including UV-light. In most cases, this is not particularly conspicuous to the human eye, but highly visible for UV-sensitive insects, due to the fact that the glossy areas are often positioned in UV-absorbing central flower parts and thus produce a strong UV-signal. The optical contrast produced by the glossiness of small smooth areas in close proximity to nectar holders represents a widespread yet overlooked floral cue that nectarivorous flower-visitors might use to locate the floral nectar.
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Animal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective pollination services, potentially reducing the number of realized pollinators and increasing the cryptic specialization of pollination networks. Thus, there is a need to understand how different functional groups of pollinators influence pollination success. Here, we examined whether patterns of contemporary pollen-mediated gene flow in Heliconia tortuosa are consistent with the foraging strategy of its territorial or traplining hummingbird pollinators. Territorial hummingbirds defend clumps of flowers and are expected to transfer pollen locally. In contrast, traplining hummingbirds forage across longer distances, thereby increasing pollen flow among forest fragments, and are thought to repeatedly visit particular plants. If trapliners indeed visit the same plants repeatedly along their regular routes, this could lead to a situation where neighboring plants sample genetically distinct pollen pools. To test this hypothesis, we genotyped 720 seeds and 71 mother plants from 18 forest fragments at 11 microsatellite loci. We performed TwoGener analysis to test pollen pool differentiation within sites (among neighboring plants within the same forest fragment: Φ SC ) and between sites (among forest fragments: Φ CT ). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (Φ SC = 0.0506), and weaker, statistically significant differentiation among sites (Φ CT = 0.0285). We interpret this pattern of hierarchical pollen pool differentiation as the landscape genetic signature of the foraging strategy of traplining hummingbirds, where repeatable, long-distance, and high-fidelity routes transfer pollen among particular plants. Although H. tortuosa is also visited by territorial hummingbirds, our results suggest that these pollinators do not contribute substantially to successful pollination, highlighting differences in realized pollination efficiency. This cryptic reduction in the number of realized pollinators potentially increases the vulnerability of pollination success to the decline of populations of traplining hummingbirds, which have been shown to be sensitive to forest fragmentation. We conclude that maintaining habitat connectivity to sustain the foraging routes of trapliners may be essential for the maintenance of pollen-mediated gene flow in human-modified landscapes.
Hummingbirds have two main foraging strategies: territoriality (defending a patch of flowers) and traplining (foraging over routine circuits of isolated patches). Species are often classified as employing one or the other. Not only have these strategies been inconsistently defined within the behavioral literature, but this simple framework also neglects the substantial evidence for flexible foraging behavior displayed by hummingbirds. Despite these limitations, research on hummingbird foraging has explored the distinct avenues of selection that proponents of either strategy presumably face: trapliners maximizing foraging efficiency, and territorialists favoring speed and maneuverability for resource defense. In earlier studies, these functions were primarily examined through wing disc loading (ratio of body weight to the circular area swept out by the wings, WDL) and predicted hovering costs, with trapliners expected to exhibit lower WDL than territorialists and thus lower hovering costs. While these pioneering models continue to play a role in current research, early studies were constrained by modest technology, and the original expectations regarding WDL have not held up when applied across complex hummingbird assemblages. Current technological advances have allowed for innovative research on the biomechanics/energetics of hummingbird flight, such as allometric scaling relationships (e.g., wing area–flight performance) and the link between high burst lifting performance and territoriality. Providing a predictive framework based on these relationships will allow us to reexamine previous hypotheses, and explore the biomechanical trade-offs to different foraging strategies, which may yield divergent routes of selection for quintessential territoriality and traplining. With a biomechanical and morphofunctional lens, here we examine the locomotor and energetic facets that dictate hummingbird foraging, and provide a) predictions regarding the behavioral, biomechanical, and morphofunctional associations with territoriality and traplining; and b) proposed methods of testing them. By pursuing these knowledge gaps, future research could use a variety of traits to help clarify the operational definitions of territoriality and traplining, to better apply them in the field.
Nectar robbers are animals that extract nectar through holes made in floral tissues. This behaviour has a wide spectrum of consequences for the plant that range from negative, to neutral, to positive according to life history traits of the interacting organisms and the ecological mechanisms involved. Lonicera etrusca has long tubular flowers producing large quantities of nectar and undergoing high levels of nectar robbing. Despite this, robbing seems to have neutral effects on the reproduction of the species. The aim of this work is to understand why this pollinator-dependent plant is not affected by an interaction that is commonly detrimental for plants. To achieve this goal we try to answer two questions: 1) do nectar robbers deposit suitable pollen for plant reproduction after a visit? And, 2) is the visitation rate of legitimate visitors affected by nectar robbing? We experimentally studied the details of the reproductive compatibility system of the plant and compared pollen tube growth after single visits of the main nectar robbers. We made observations on plants of three populations to study the effect of robbers on the visitation rates of legitimate foragers. The results revealed that nectar robbers effectively perform cross-pollination. Visitation rates of legitimate visitors are reduced by nectar robbing. The net neutral effect observed for L. etrusca is the result of two processes: on one side the direct positive effect of nectar robbers acting as pollinators, and on the other, a negative indirect effect caused by the decrease in visitation rates of legitimate visitors. Since the number of ovules in this species is low, both legitimate visitors and robbers contribute to an efficient cross-pollination. This example illustrates how neutral effects for the plant can arise as the final result of a complex interaction between plants, legitimate visitors and robbers.
Territoriality is central to animal behaviourists' understanding of many facets of animal behaviour, including resource acquisition, space use behaviour, communication and mating systems. However, the term itself, how it is conceptualized and defined, has long been nebulous and contentious. Here, we ask whether juxtaposing debates about territoriality from animal behaviour with parallel discussions of territoriality from the social sciences can offer a historically and sociologically informed path out of the conceptual gridlock in which animal territoriality has been located for decades. We delineate two key problems with territoriality identified in the animal behaviour literature: First, that it focuses on how animals are expected to behave rather than how they actually behave and, second, that it assumes rather than demonstrates the function of, and specific relationships among, individuals. We then link these problems to social scientists' theorizations of the difference between property and access: whereas property is focused on how people are expected to behave under juridical–legal rules governing resource use, access focuses on a wide array of means by which people actually access resources. We thus argue that longstanding problems with animal territoriality have arisen due to implicitly embedded notions of property and ownership. Our juxtaposition raises two further problems with territoriality: first, it unwarrantedly serves to attribute authority to individuals described as territory ‘owners’ and casts others (‘intruders’, ‘sneakers’) as transgressors and, second, conceiving of ownership is unfeasible in animal societies lacking the particular juridical–legal institutions that establish and enforce property rights. Instead, we advocate for an access-based approach that will obviate these problems. Ultimately, we argue that the theory of access, as developed in social science literatures on spatial and relational resource use, will allow for a fuller and more nuanced understanding of variation in animal behaviour than that afforded by current dominant notions of territoriality.