AMER. ZOOL., 19:1115-1127 (1979).
Competition Between Distantly Related Taxa In the Coevolution
of Plants and Pollinators
ASTRID KODRIC-BROWN AND JAMES H. BROWN
Department of Ecology and Evolutionary Biology, University of Arizona,
Tucson, Arizona 85721
SYNOPSIS. Competition among distantly related plants for pollinators and among distantly
related animals for pollen and nectar plays a potentially important role in the organization of
ecological communities and the coevolution of plant-pollinator relationships. Plants which
rely on animals to disperse their pollen potentially compete for pollinators by processes
similar to interference and exploitative competition. Coexisting plant species may evolve to
avoid or reduce such competition by character displacement in floral morphology and/or
phenology. One important difference between competition for pollinators and most other
kinds of competition is that pollinator resources are not used up and made absolutely
unavailable to competitors. Consequently, plant species can potentially overlap completely
in their utilization of pollinators. The disadvantages of competing apparently are sometimes
outweighed by the advantages of sharing pollinators, because distantly related plant species
frequently show evolutionary convergence in floral morphology, blooming time and nectar
rewards to utilize the same pollinators.
Distantly related animal taxa may compete for floral nectar and pollen by both interference and exploitation. The mechanisms of such competition depend primarily on the
energetic costs and benefits of foraging and aggression. Exploitative competition is very
important because nectar feeders of small body size and low energy requirements can forage
economically and reduce nectar availability to levels that will not support larger animals.
Thus small nectarivores often can exclude larger competitors from flowers to which both
taxa have equal access. Plants may evolve to influence the outcotre of competition among
animal visitors and favor species that provide the best pollination services. Thus flowers
specialized for pollination by large animals often show morph >logical or phenological
specializations which make rewards unava'lable to smaller animals. Interference is adaptive
only when the benefits of exclusive use of a resource outweig.i the costs of defending it.
Because distantly related kinds of flower visitors often differ in body size and energetic
requirements, interference competition among them is probably rare although it is often
important among closely related nectarivores.
The community level consequences of competition in the ecology and evolution of
plant-pollinator associations are still poorly understoood. Competition among distantly
related pollinators for plant floral rewards appears to play a major role, but competition
among plants for pollinator services may be only a weak force. Although the basic interaction
between plant and pollinator usually is a mutualistic one, certain species of both plants and
animals parasitize this interaction and compete with the mutualists for limited resources.
Thus some animals rob nectar and pollen and compete with legitimate pollinators without
providing pollination services. Similarly, some plants offer no floral rewards but obtain
pollinator services by mimicing rewardingflowersof other species. The effects of these kinds
of interactions on the organization of communities of plants and pollinators provide a
fertile area for future research.
INTRODUCTION
H. w. Bond and T. G. whittam participated in all
Pollination biologists have been slow to
phases of the research on C.linearis and R. pinetorum. recognize the importance of Competition,
We thank E. L. charnov, T. c. Gibson, N. M. Waser in large part because they have been priand many others for valuable discussions, C. C. Smith m a r U c o n c e r n e d w i t h t h e mutualistic COadand N. M. Waser tor helpful comments on the manu•
• ,
,
,
r
r
script, and D. F. Gori and R. Vestal for assistance. a Ptatlons of particular pairs of plant and
This work was supported in part by NSF Grants GB animal species (e.g., Faegn and van d e r Pijl,
39260 and DEB 76-09499.
1966; van der Pijl and Dodson, 1967; Proc1115
1116
A. KODRIC-BROWN AND J. H. BROWN
tor and Yeo, 1972), the behavior and energetics of pollinator foraging (e.g., Heinrich
and Raven, 1972; Wolf, et al., 1972; Feinsinger and Chaplin, 1975; Hainsworth and
Wolf, 1976; Heinrich, 1976a; Gould, 1978;
Pyke, 1978), and the effects of pollinator
activity on plant breeding systems (e.g.,
Baker, 1961, 1963; Grant and Grant, 1965;
Levin, 1972; Heinrich, 1975a; Cruden,
1976; Lack, 1976; Solbrig, 1976; Janzen,
1977; Price and Waser, 1979; Feinsinger,
1978). It is only when pollination systems
are studied as multi-species ecological
communities that the importance of competition becomes apparent. Most plantpollinator associations are based on mutualism. Plants provide nectar or pollen
which attracts foraging animals, which in
turn transport male gametes between individual plants. Since several plant species
often share the services of the same pollinators and several animal species commonly forage from the same flowers, there
is potentially competition among plants for
pollinators and among animals for nectar
and pollen.
Competition between distantly related
taxa of both plants and pollinators plays a
potentially important role in the ecology
and evolution of these communities. Nectar, which flowers have evolved specifically
to attract pollinators, is rich in sugars and
sometimes other nutrients (Hainsworth
and Wolf, 1972, 1976; Baker and Baker,
1973, 1975). Some pollen also is highly nutritious and particularly rich in protein
(Brian, 1950; Doull, 1966; Howell, 1974;
Gilbert, 1972). Only a few distantly related
taxa of animals have specialized to harvest
these floral resources; these include several
groups of insects, birds, and mammals
(Baker, 1961; Grant and Grant, 1968;
Heinrich, 1979; Heithaus et al., 1975;
Sussman and Raven, 1978). A growing literature suggests that nectar and pollen
feeders are often limited by availability of
food resources and consequently they have
evolved strategies for efficient foraging
(Grant, 1950; Stiles, 1971; Wolf et al.,
1972; Feinsinger and Chaplin, 1975; Heithaus et al., 1975; Heinrich, 1976a; Pyke,
1978; Kodric-Brown and Brown, 1978). In
such a situation not only may distantly related animals compete for floral resources,
but also, to the extent that they differ in effectiveness as pollinators, these foragers
may select for patterns of floral display and
nectar and pollen provision which influence pollinator specificity and competition
with other plant species. Variants in floral
characteristics which experience increased
reproductive success through more efficient pollination will tend to increase in frequency. Such changes, together with analogous ones in pollinator attributes which
increase foraging efficiency, result in the
interrelated evolution of plant and pollinator which we call coevolution.
The present paper has two primary purposes. First, we shall examine the extent
and mechanisms of competition among distantly related plants for pollinators and
among distantly related animals for nectar
and pollen. Second, we shall assess the role
of this competition in the coevolution of
particular plant-pollinator associations and
in the structure of communities. This is a
promising, but as yet largely untapped,
area of investigation. Our viewpoint is
based on a few direct studies of competition
in pollination systems and much indirect,
circumstantial evidence. Many of our conclusions are tenuous and controversial, but
we hope they will focus attention on interesting problems and stimulate future research.
COMPETITION AMONG DISTANTLY RELATED
PLANTS FOR POLLINATORS
The process
Consider the role of pollinators as a resource for plants. Movement of foraging
animals between flowers on the same plant
and between individual plants of the same
species determines in large part the nature
of the breeding system in animal-pollinated
plants. During these movements pollinators transport male gametes from the anthers of a donor flower to the sigma of a
recipient. Some proportion of the pollen
may be distributed to flowers on the donor
COMPETITION BETWEEN DISTANTLY RELATED TAXA
plant, which may result in self-fertilization
if the plant is self-compatible. However, we
assume that some degree of outcrossing
(transport of pollen to plants other than the
donor) must be advantageous for animal
pollination to have evolved and be maintained. Animal-pollinated plants apparently invest substantial resources in the
production of floral attractants (odors and
brightly colored petals) and rewards (nectar
and pollen), and these structures and substances are reduced in completely self-fertilized species, of which the extreme examples have cleistogamous (small, cryptic,
never-opening) flowers. Many animal pollinated plants are self incompatible (Grant
and Grant, 1965; Proctor and Yeo, 1972;
Cruden, 1976), so that movement of pollinators between individuals is required for
sexual reproduction. Clearly plant reproductive success is potentially limited by the
availability and movement patterns of pollinators.
To what extent might pollinators be limiting so that plants might compete interspecifically for their services? In much of the
pollination literature it is assumed that seed
production is limited by the availability of
pollinators. The best evidence comes from
agricultural crops, where fruit and seed set
can be increased artificially by providing
suitable pollinators (Blake, 1958; Hawkins,
1961; Free, 1968, 1970). However, mass
flowering of crop plants presents an unnatural situation which may overwhelm
non-coevolved native pollinators. Evidence
that pollinators normally limit seed production under natural conditions is less convincing (but see Cruden, 1976; Wyatt, 1976;
Waser, 1978a, 1979; Schaffer and Schaffer,
1979). Recently Charnov (1979) has argued
that application of Bateman's principle of
sexual investment to hermaphroditic (perfect flowered, i.e., with both anthers and
pistil in the same flowers) plants suggests
that female function (seed set) should
usually be resource limited, whereas male
function (pollen flow) should be pollinator
limited. If this is correct, plants should compete for pollinators to disperse their pollen,
even under conditions where pollinator
availability does not affect seed set.
1117
We can imagine two ways that plants
might compete interspecifically for pollinators (see also Waser, 19786; Brown and
Kodric-Brown, 1979; and included references). These are somewhat analogous to
interference and exploitative competition
among animals. In the first case, sharing of
a pollinator between two plant species
might result in interference with pollen
transport. On the one hand, deposition of
heterospecific pollen on stigmas might
occlude the receptive surface, prevent pollination, and reduce seed set. However, in
support of Charnov's argument, stigmatic
surfaces frequently appear to be able to
hold far more compatible pollen than they
normally receive and to receive more than
enough to fertilize all ovules (Willson and
Rathcke, 1974; G. S. Byers, personal communication; Brown and Kodric-Brown,
unpublished). On the other hand, loss of
pollen on heterospecific stigmas clearly
represents a loss to male function, since that
pollen is unavailable to fertilize compatible
plants. Plants might also compete interspecifically simply to attract pollinators. If
flower species fhare pollinators, the visitation rate to ?ny single species will be less
than if a specific pollinator had to obtain
food at the same rate from that species
alone.
Character displacement in floral characteristics, so that coexisting plant species differ in utilization of pollinators, may evolve
in response to both kinds of competition.
Interference competition may be reduced
by adaptations to use different parts of the
pollinator's body to transport pollen. In this
way the plants can continue to use the same
pollinator simultaneously. Both interference and exploitative competition can be
reduced by adaptations which promote exclusive use of different pollinators. This can
be accomplished either directly, by specializations which result in species-specific
foraging behavior, or indirectly by evolving
to bloom at different times or in different
habitats.
In attempting to evaluate the role of
competition among plant species for pollinators, it is important to realize that such
competition is fundamentally different
1118
A. KODRIC-BROWN AND J. H. BROWN
from interspecific competition for most
other resources. Unlike these other resources, pollinators are not used up and
made absolutely unavailable to competitors. One consequence of this difference is
that outcrossing pollination occurs even
though plants may compete intraspecifically for pollinators (Schaffer and Schaffer, 1979). A second consequence is that it is
possible for two plant species to overlap
completely in their utilization of pollinators, without competitive exclusion (Brown
and Kodric-Brown, 1979). Competition for
pollinators, especially if it operates primarily through male function, might reduce
fitness of coexisting plant species sufficiently to select for character displacement without significantly affecting seedling recruitment and population density.
The patterns
Most of the evidence that plants compete
for pollinators is circumstantial. Differences among coexisting species in floral
morphology and phenology which result in
differential utilization of pollinators have
been interpreted as adaptations to avoid
competition. From such patterns of character displacement pollination biologists have
inferred that competition plays an important role in structuring plant communities;
similarly ecologists have interpreted differences in trophic structures among coexisting animal species as evidence of competition for food resources {e.g., Brown and
Wilson, 1956; Hutchinson, 1959; Diamond,
1975).
Coexisting plant species achieve differential utilization of pollinators both directly
by specializations which promote pollinator
specificity and indirectly by flowering at different times or in different habitats. As in
most cases of character displacement, such
patterns are particularly apparent among,
but not restricted to, closely related species.
Simultaneously flowering species often differ in floral shape and color, which have
been interpreted as adaptations to attract
different pollinators (Levin and Anderson,
1970; Levin, 1972; Heinrich, 1975ft, 1976ft;
Inouye, 1976; Whalen, 1978). Heinrich
(1976a) recently has described a special case
of differential pollinator utilization which
often involves distantly related species.
Flowers blooming simultaneously in the
same habitats in Maine often differ in color,
shape, and nectar rewards. Each of these
species is visited specifically by individual
bumblebees which have learned to forage
efficiently from their "major" flower species. By taking advantage of the bees' learning ability and providing a specific search
image, these plant species are able to promote pollinator constancy of individual
bees while other individuals of the same
species and even of the same colony may
forage on other kinds of flowers. Flowers of
similar shape and color often bloom at different seasons, and such temporal displacement in phenology results in differential utilization of snared pollinators
(Robertson, 1895; Mosquin, 1971; Chase
and Raven, 1975; Heinrich, 19756; Stiles,
1975). These patterns have long been interpreted as adaptations to avoid competition, and Waser (1978a) recently has provided experimental evidence to support
this view.
Although many plant species appear to
avoid competition by adaptations to promote pollinator specificity, other species
bloom simultaneously and share the same
pollinators. While these species do not
avoid exploitative competition for pollinators, they sometimes show apparent
adaptations to avoid interference with pollen transport. In some cases these species
differ in the orientation of anthers and
stigma so that pollen is transported on different parts of the pollinator's body (Howell, 1977; Brown and Kodric-Brown, 1979).
Some plant taxa disperse their pollen in
compact masses called pollinia, and they
possess specialized adaptations for depositing and picking up pollinia on particular
parts of a pollinator. While much of the
evolution of pollinia might be interpreted
as resulting from selection to promote pollination efficiency even in the absence of
interspecific competition, some patterns
suggest that competition has played a significant role. Pollinia often are characteristic of plant taxa which occur at low density
{e.g., orchids, van der Pijl, and Dodson,
COMPETITION BETWEEN DISTANTLY RELATED TAXA
1967) so that they must share pollinators
with more common flower species. Orchids
which use the same species of insect pollinator, characteristically place their pollinia on different parts of its body (van der
Pijl and Dodson, 1967).
It is our impression that interspecific
competition for pollinators by itself is a relatively weak force in the ecology of plant
communities, although it may lead to significant adaptations over evolutionary time.
Evidence to support this view comes from
studies of associations of hummingbirdpollinated flowers (Grant and Grant, 1968;
Brown and Kodric-Brown, 1979). In local
areas in western North America it is not
uncommon to find two, three, or more
flower species of similar shape and color,
blooming at the same time, and sharing the
pollination services of the same individual
hummingbird (Fig. 1). Usually these flowers belong to different genera and often
different families and represent convergent evolution of hummingbird pollination. Competition for pollinators among
these distantly related taxa apparently has
not been sufficient to prevent convergence
and sharing of pollinators. This pattern
suggests that these species are able to
coexist because of their abilities to compete
for and utilize differentially, resources (e.g.,
sunlight, water, and nutrients) other than
pollinators, and when this is the case it may
actually be advantageous to share pollinators. Character displacement in orientation of reproductive structures among
these coexisting hummingbird-pollinated
flowers suggests that interference with pollen transport has resulted in coadaptations
over evolutionary time, although there is no
evidence that it significantly affects coexistence in ecological time. In the light of these
observations it would seem appropriate to
reexamine cases of character displacement
among closely related flower species which
have been interpreted as resulting from
selection to avoid competition for pollinators. In these cases pollinator specificity
may represent an adaptation to avoid the
disadvantageous genetic consequences of
hybridization between closely related species rather than to avoid ecological competition.
1119
COMPETITION AMONG DISTANTLY RELATED
ANIMALS FOR NECTAR AND POLLEN
The process
Competition among animals for nectar
and pollen is generally similar to competition for other limited food resources. Floral
nectar typically is a solution containing
moderate to high concentrations of sugars
and sometimes other solutes such as amino
acids (Baker and Baker, 1973, 1975). It
represents a rich, easily assimilated source
of energy and sometimes other nutrients.
While the nectar constituents of particular
plant species may coevolve to attract specific
pollinators, in general nectar represents a
valuable food resource which is in short
supply and potentially exploitable by many
animal taxa. Pollen is not so universally attractive as nectar. Pollen usually contains
high concentrations of amino acids and
other important nutrients, but digestive
specializations appear to be required to
break down the pollen grains and assimilate
efficiently their contents (e.g., Howell,
1974). Pollen can be a limiting resource for
those animals which are specialized to
utilize it, but fewer taxa potentially compete
for pollen than for nectar. While competition among distantly related pollen feeders
(including some bats, birds, bees and butterflies) is potentially important, it is virtually unstudied. The following discussion
will be limited to competition for nectar,
although many of the principles might also
apply to interactions among pollen feeders.
Animals may compete for floral nectar by
both interference and exploitative means.
The mechanisms and outcome of such
competition depends largely on the economics of foraging and defense. In general,
animals of small body size and low energy
requirements can forage porfitably when
the quantity of nectar per flower is inadequate to support larger nectar feeders
(Heinrich and Raven, 1972; Heinrich, 1975;
Cruden, 1976; Brown, Kodric-Brown, Whitham and Bond, unpublished). If they are
sufficiently abundant, small nectar feeders can potentially maintain low standing
crops of nectar and exploitatively exclude
larger animals. Large nectar feeders are
1120
A. KODRIC-BROWN AND J. H. BROWN
/pom ops is
aggregate/
Penstemon
barbatus
Castilleja
Integra
Aquilegia
triternata
Lonicera
arizonica
Castilleja
austromontana
Silene
laciniata
Echinocereus
triglochidia tus
Lobelia
cardinalis
FIG. 1. Scale drawings of the nine species of red,
hummingbird pollinatedflowerswhich bloomed in the
White Mountains in eastern Arizona. Note the convergence in size and form.
able to coexist with smaller competitors
only when flowers maintain sufficiently
high standing crops to permit economical
foraging. Three characteristics of floral
resources may support large nectar feeders in the face of competition from small
ones: 1) Temporal or spatial patterns of
nectar availability may temporarily or locally overwhelm small nectarivores and
permit accumulation of sufficient rewards
to support larger animals; 2) Nectar may be
secreted at times of day when small nectar
COMPETITION BETWEEN DISTANTLY RELATED TAXA
feeders are inactive, because most small
nectar-feeding insects are least active at
night and at low environmental temperatures; and 3) Floral characteristics, such as
shape, odor and color, may conceal nectar
rewards from small animals or physically
prevent them from collecting it, while still
making nectar available to large animals.
Nectar feeders (including closely related
species) of similar body size and energy requirements may also compete and exclude
each other by exploitative means, but in
such cases the outcome depends on more
subtle differences in foraging economics.
Many nectarivorous animals utilize aggressive behavior to defend floral resources
against competitors. We expect such behavior to occur only when the benefits of
defending food resources outweigh the
costs of excluding competitors (Brown,
1964). Whereas aggressive interference
among closely related nectarivorous species
is well documented (e.g., stingless bees,
Johnson and Hubbell, 1974; hummingbirds, Pitelka, 1942; Colwell, 1973; Kodric-Brown and Brown, 1978), we would
not expect this to be a common mechanism
of interaction among distantly related taxa.
As already pointed out, competition among
nectarivores potentially is particularly severe from animals of smaller body size, but
the costs of defending floral resources
against such competitors may outweigh the
benefits of exclusive use of nectar.
The patterns
We know of only a few anecdotal examples of interference competition among distantly related nectarivores. Most cases involve aggression between hummingbirds
and large insects (e.g., bumblebees, Lyon
and Chadek, 1971; skipper butterflies,
Primack and Howe, 1975; carpenter bees,
Boyden, 1978). Because these organisms
are not too different in body size, the aggressor may benefit energetically from defending floral resources.
Exploitative competition undoubtedly is
widespread among distantly related taxa of«
nectar feeders and has played a major role
in plant-pollinator coevolution. Like most
cases of competition between distantly re-
1121
lated taxa, documented examples are few,
but this is only because pollination biologists have devoted little attention to the
problem. Recently we have obtained direct
evidence that hummingbirds and insects
compete for the nectar of two species of
shrubs (Ribes pinetorum, Greene and Chilopsis linearis, Sweet) in the southwestern United States (Brown, Kodric-Brown, Whitham
and Bond, unpublished). Both species secrete sufficient quantities of nectar to
attract hummingbirds but their floral morphology is such that their nectar is also
accessible to several insect taxa. Ribes pinetorum blooms in early spring at high elevations where ambient temperatures are low
except at midday. We observed that this
species accumulated sufficient quantities of
nectar to attract foraging hummingbirds in
the morning and evening when insects were
inactive, but at midday insects foraged
heavily on the flowers, reduced the standing crop of nectar, and excluded hummingbirds (Fig. 2). Chilopsis linearis, which
bloomed at lower elevations where temperatures were higher, attracted some hummingbird foragers early in its blooming season when insects were scarce and good
standing crops of nectar accumulated, but
as the flowering season progressed and
more insects were attracted, they reduced
the standing crop of nectar and hummingbirds were excluded (Fig. 3). Carpenter (1979) describes another example of
competition between hummingbirds and
insects.
Patterns of body size among distantly related taxa of nectarivores provide indirect
evidence for competitive interaction. Brown
etal. (1978) examined correlates and consequences of body size in nectar-feeding
birds. Although avian nectarivores include
the smallest birds, there is little evidence
that absolute physiological constraints limit
minimum size in birds. The lower limit of
size in avian nectarivores appears in part to
reflect increasing competition with insects
as body size decreases. This interpretation
is supported by the work of Inouye (1977)
who noted that in northern Europe, where
there are no nectarivorous birds, there is a
species of bumblebee which attains larger
size and has a longer proboscis than any
1122
A. KODRIC-BROWN AND J. H. BROWN
Ribes pinetorum
Hummingbird Feeders
May 11-13, 1974
May 23, 1974
0600 0800 1000 1200 1400 1600" 1800 " 2000 0600 0800 1000 1200 1400 1600 1800 2000
TIME OF DAY
FIG. 2. Daily patterns of nectar availability, ambient
temperature, and animal visits for Ribes pinetorum, and
hummingbird visits to feeders in the same area. Plotted values represent means for more than 100 flowers
and total number of animal visits for the days indicated. Standard errors in nectar availability are 0.26 ml
when nectar levels are high and < 0.1 ml when they are
low. Note that when a continous supply of food is
provided, there is no midday depression in the foraging activity of hummingbirds, as observed atflowersof
species in North America where bumblebees coexist and potentially compete with
hummingbirds. Where they occur together
bumblebees and hummingbirds commonly
forage from the same flower species (Waser,
1978a; Brown, Kodric-Brown, Whitham
and Bond, unpublished) Inouye's interpretation is that in the absence of competing
birds, European bumblebees are able to use
a class of floral resources not available to
them in North America.
Additional circumstantial evidence for
competition among distantly related pollinators comes from studies of coevolution
of floral characteristics and specific pollinators and from observations of nectar
robbers. These will be discussed in the next
section.
COMPETITION, COEVOLUTION, AND COMMUNITY
STRUCTURE
Ribes pinetorum.
Coevolution
The mutualistic nature of plant-pollinator interactions allows each element in
these systems to coevolve in response to
competition among its partners. Thus an
individual plant species may respond by
adaptive changes in floral characteristics so
as to favor one of several competing species
of animal foragers which provides the best
or most efficient pollination services. Similarly foraging animals will tend to visit
differentially and thereby enhance the reproductive success of one of several coexisting plant species which provides the best
rewards. These potentially complex in-
1123
COMPETITION BETWEEN DISTANTLY RELATED TAXA
Chilopsis linearis
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May 18-19,1974-,
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TIME OF DAY
FIG. 3. Daily patterns of nectar availability, ambient nectar availability are always < 0.24 ml. Note the large
temperature and animal visits for Chilopsis linearis. number of bumblebee visits, rapid decline in available
Plotted values for nectar quantities represent means of nectar, and low frequency of hummingbird and honsamples of more than 100flowers,and total numberof eybee visits on 27 May, eight days after the first meaanimal visits for the days indicated. Standard errors in surements.
teractions can play an important role in
plant-pollinator coevolution and, as a result, in the structure and function of communities. The response of plants to competition among distantly related pollinators is
suggested by the observation that changes
in major classes of pollinators have occurred frequently and independently in the
phylogeny of plant taxa. The most frequently cited case probably is Grant and
Grant's (1965) study of pollination in the
phlox family (Polemoneacae), but there are
many other examples. Hummingbird-pollinated forms have evolved independently
from insect-pollinated ancestors at least 6
times in the evolution of the genus Penstemon (family Scrophulariaceae), which contains about 230 species in western North
America (F. S. Crosswhite, personal communication). Grant and Grant (1968) list 19
genera of flowers from the western United
States which contain species specialized for
both insect and hummingbird pollination.
In fact we suspect that many cases of geographic variation in floral phenotype which
classically have been interpreted as hybridization resulting from secondary contact after geographic isolation actually represent a response to local selection to utilize
different pollinators (e.g., see Straw, 1955;
Chase and Raven, 1975; Grant, 1976).
Although changes in pollinators have occurred frequently in many plant groups,
such shifts may be complicated by competition among potential pollinators. As mentioned earlier, most bird-pollinated flowers
1124
A. KODRIC-BROWN AND J. H. BROWN
have a syndrome of adaptations which prevent insects from detecting and exploiting
their rich nectar rewards. How do plants
evolve from insect to bird pollination? As
increased nectar secretion makes the flowers more attractive to birds, what prevents
competing insects from harvesting the nectar and negating this advantage? One possibility is that the whole syndrome of bird
pollinated characters evolves simultaneously. A more likely alternative is that a high
degree of bird specificity is attained by some
simple phenotypic change, and other characteristics of the ornithophilic syndrome
evolve gradually at a later time. Thus Ribes
pinetorum in the southwestern United Staes
has a morphologically unspecialized flower
whose nectar is readily accessible to both
hummingbirds and insects, but it attains a
high degree of hummingbird specificity by
secreting its nectar at times of day (morning
and evening) when low ambient temperatures inhibit insect foraging (Brown, Kodric-Brown, Whitham and Bond, unpublished). Such a strategy may represent an
intermediate stage in the evolution of specialized bird-pollinated flowers from generalized insect-pollinated ancestors. In this
regard it probably is not coincidental that
the highest diversities of ornithophilous
flowers occur at intermediate to high elevations (Cruden, 1972; Stevens, 1976) where
morning and evening temperatures are
low enough to inhibit the foraging of many
insects.
Much of the diversity in floral morphology, phenology, and attractants among
coexisting plant species apparently represents adaptations to subdivide visitation by
nectar and pollen-feeding animals in order
to obtain the benefits of relatively specific pollinations. Floral phenotypes have
evolved to attract desirable pollinators and
exclude undesirable competitors for floral
rewards. Earlier we suggested that insects
of small body size and low energy requirements represent potentially important
competitors of vertebrate pollinators. In
this regard some social bees, because of
their capacity to recruit to rich nectar
sources, are particularly severe competitors. It is interesting to note that most
vertebrate-pollinated flowers either possess
morphological adaptations to deny bees
and other insects access to their nectar, or
else they bloom at times when bees are inactive or in habitats and geographic areas
(e.g., Australia, North American deserts)
where native social bees are rare or absent.
Convergence
Whereas competition for floral rewards
among distantly related animal taxa has
had a major influence on plant-pollinator
coevolution and community structure,
there is little direct evidence that competition for pollinators among distantly related
plant taxa has played a similar role (but see
Waser, 1978a and included references).
While distantly related animals often differ
in body size and other characteristics which
result in utilization of different kinds of
food resources, community patterns suggest that distantly related plant species frequently have converged so that they share
the services of the same kinds of pollinators.
For example, Grant and Grant (1968) list
129 plant species from western North
America, belonging to 39 genera and 18
families, which have converged in floral
characteristics to utilize hummingbirds as
pollinators. Often several of these species
bloom simultaneously in the same local area
and share pollination services of the same
individual bird (Brown and Kodric-Brown,
1979). While this example is particularly
dramatic and well studied, the existence of
generalized pollination syndromes (Faegri
and van der Pijl, 1966; Proctor and Yeo,
1972) and other community patterns of
floral characteristics (Oster and Harper,
1978) suggest that similar convergence
characterizes plant taxa that utilize other
kinds of pollinators.
Apparently in these situations the benefits of converging to share pollinators outweigh the costs of competition. Earlier we
pointed out that interspecific competition
for pollinators probably is a weak selective
force acting on plant populations, particularly when the plant species differ in their
requirements for other resources. The prevalence of convergence suggests that in some
cases plants may benefit mutualistically
from sharing pollinators. We (Brown and
COMPETITION BETWEEN DISTANTLY RELATED TAXA
Kodric-Brown, 1979) have pointed out the
resemblance of this interaction to Mullerian mimicry. Just as distantly related, distasteful prey species may benefit from converging toward a common phenotype to
take advantage of the learning behavior of
common predators, so may distantly related plant species benefit from converging
in floral characteristics to provide similar
search images and rewards to common pollinators.
1125
and legitimate pollinators would seem to
play a potentially important role in plantpollinator coevolution.
CONCLUDING REMARKS
Although much of the evidence presently
available is circumstantial, competition
among distantly related taxa of nectar and
pollen feeders appears to be extremely important in the ecology and evolution of
plant-pollinator associations. Competition
for food resources occurs at all taxonomic
Cheaters and robbers
levels within and between the three classes
In some cases convergence in floral char- of animals (insects, birds and mammals)
acteristics functions to deceive pollinators which contain species specialized for foragand is detrimental to some plant species. ing from flowers. Because these diverse
Some plant species might be compared to animals are not equally effective as polBatesian mimics; they attract pollinators linators, and some rob nectar and pollen
because of their resemblance to other without accomplishing any pollination at
species, but they provide no reward (Ma- all, their foraging activities exert potentially
cior, 1971; Proctor and Yeo, 1972; Hein- important selective pressures on plant
rich, 1975a; Brown and Kodric-Brown, populations. Plants will tend to evolve in
1979). These mimics should compete with response to competition among flower
reward-producing flowers for pollinator foragers by increases in characteristics
which encourage the best pollinators
services.
There are also several kinds of animals and/or exclude ineffective ones. While this
which have specialized to take advantage of can be inferred from existing data, much
the mutualistic relationships between additional research will be required to
plants and their pollinators. Several kinds clarify the ecological mechanisms and evoof insects and birds rob nectar or pollen lutionary consequences of these interacfrom flowers without pollinating them. tions.
Some of the best examples are provided by
Even less is known about competition
those robbers which steal the rich nectar among distantly related plant species for
rewards from specialized, bird pollinated common pollinators. In contrast to the esflowers by cutting through the tube without tablished view, we have suggested that
contacting the anthers and stigma (Baker competition for shared pollinators has relaand Cruden, 1971). Several kinds of birds tively weak influence on the ecology and
and bees employ this strategy (bananaquits, evolution of distantly related, coexisting
honey creepers, flower piercers, verdins, plant species. Numerous examples of dishoneybees, carpenter bees, euglossine bees). tantly related flowers which have conThese robbers not only compete directly verged to utilize the same pollinators imply
with legitimate pollinators for floral re- that advantages of providing a common
wards, but in so doing they also reduce the search image often outweigh any disadvaneffectiveness of pollinators. In some cases tages resulting from competition. Some of
the incidence of robbery is amazingly high: these systems are strikingly analogous to
In some populations of hummingbird- associations of Mullerian and Batesian
pollinated flowers in Puerto Rico the fre- mimics.
quency of blossoms robbed by carpenter
Pollination biologists have just begun to
bees (Xylocopa brazilianorum) bananaquits (aappreciate the intricacies and complexity of
passerine bird, Coroebaflaveola)exceeded pollination ecology and plant pollinator
90% (Kodric-Brown and Brown, unpub- coevolution. Because many of the interaclished). Competition between these robbers tions involve several distantly related spe-
1126
A. RODRIC-BROWN AND J. H. BROWN
cies of both plants and pollinators, it is
necessary to study these systems as ecological communities where the ecology and
evolution of each species is affected by its
relationships to the others. Competition between distantly related taxa is only one of
the processes that influences the structure
and function of these communities.
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