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Convergence, Competition, and Mimicry in a Temperate Community of HummingbirdPollinated Flowers
Author(s): James H. Brown and Astrid Kodric-Brown
Source: Ecology, Vol. 60, No. 5 (Oct., 1979), pp. 1022-1035
Published by: Ecological Society of America
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Ecology, 60(5), 1979, pp. 1022-1035
? 1979 by the Ecological Society of America
CONVERGENCE, COMPETITION, AND MIMICRY IN
A TEMPERATE COMMUNITY OF
HUMMINGBIRD-POLLINATED FLOWERS'
JAMES H. BROWN AND ASTRID KODRIC-BROWN
Department of Ecology and Evolutionary Biology, University of Arizona,
Tucson, Arizona 85721 USA
Abstract. We studied the pollination ecology of nine species of red, tubular flowers which bloom
together in different combinations in the White Mountains of Arizona, USA. All species were strikingly convergent in floral color, size, and shape. Hummingbirds, the primary pollinators, usually did
not visit flower species selectively, and individual birds often simultaneously carried four or more
species of pollen. Flowers may have competed interspecifically for these shared pollinators, but
competition was reduced because character displacement in orientation of anthers and stigma resulted
in some species using different parts of the bird to transport their pollen. Most flower species secreted
nectar at similar rates, particularly when they bloomed together in mixed stands. A population of
Lobelia cardinalis secreted no nectar; it attracted hummingbirds by mimicing more abundant, nectarproducing species. This temperate flower community, which resembles some associations of convergent Mullerian and Batesian mimics, appears to have evolved its characteristic convergent structure
because the advantages of using similar signals and rewards to share the same hummingbird pollinators
outweigh the advantages of diverging to reduce interspecific competition.
Key words: coevolution; coexistence; community; competition; convergence;flowers; hummingbirds; mimicry; nectar; pollination.
INTRODUCTION
Two processes produce the mutualistic relationship
between plants and pollinators and determine the
course of their coevolution. Transport of pollen between individual plants by foraging animals results in
outcrossing, and production of nectar or pollen provides a food resource which attracts pollinators to
flowers. In most natural situations, this mutualistic relationship is complicated by interspecific competition
among plants for pollinators and among pollinators for
nectar and pollen. Coexisting flower species often differ in morphology, odor, color, flowering time, and
nectar and pollen rewards, and these patterns have
been interpreted as adaptations to reduce competition
for pollinators by promoting specific plant-pollinator
associations (e.g., Robertson 1895, Free 1970, Levin
and Anderson 1970, Mosquin 1971, Heithaus 1974,
Heinrich 1976a, Lack 1976, Waser 1978).
An apparent exception to this general pattern of
competition, character displacement, and pollinator
specificity was described by Grant and Grant (1968)
in their monograph on hummingbirds and the flowers
which they pollinate. The Grants noted that hummingbird-pollinated flowers in western North America
are characterized by striking convergence in shape and
color and are pollinated by one of several similar hummingbird species. They report that such convergence
extends to those plant species which bloom simultaneously in the same habitats, producing (p. 92) i. . .
a regional ecosystem consisting, on the one hand, of
I Manuscript received 29 August 1978; accepted 22 January
1979.
several hummingbird species able to feed equally well
on any native species of hummingbird flower, and on
the other hand, of numerous species of bird flowers
which can be pollinated successfully by any species
of hummingbird"
and that this situation,
". . . with
broad standardization and interchangeability of parts
between different species of birds and plants, prevails
in western North America." The Grants described
morphological, biogeographic, and systematic attributes of temperate hummingbirds and flowers to document this convergent pattern, but they did not obtain
sufficient data on nectar rewards and pollen transport
to understand the ecological processes responsible for
the coevolution and maintenance of these communities.
This paper examines interactions among coexisting
hummingbird-pollinated plant species in the mountains
of eastern Arizona. Relationships among the hummingbirds have been reported in an earlier paper (Kodric-Brown and Brown 1978). In the present study, we
have verified the striking convergence in floral shape
and color described by Grant and Grant (1968), but in
addition, we have obtained detailed quantitative data
on spatial and temporal distribution of flowers, rates
of nectar secretion, and patterns of pollen transport in
order to determine how these flower species interact
with each other and with their pollinators. Our results
suggest that the flowers compete for pollinators, that
floral adaptations reduce deleterious effects of this
competition, and that the convergent organization of
this community represents a stable condition typical
of coevolved associations of hummingbirds and plants
in temperate habitats.
TEMPERATE HUMMINGBIRD FLOWERS
October 1979
METHODS
Study area
We studied different associations of plant species at
many specific localities, but all work was done within
a 30-km radius of Alpine in the White Mountains of
east central Arizona. Elevation was 1800-3000 m.
Habitats include chaparral, riparian forest, and pinonjuniper woodland at the lowest elevations, through
open forests of pine and oak at intermediate altitudes,
to dense forests of mixed conifers at the highest elevations. At all altitudes, there were patches of open
habitat with few if any trees; these included natural
meadows, talus slopes and cliffs, as well as man-made
meadows and roadsides. Artificially disturbed habitats
often supported large populations of flowers and were
convenient study sites. However, all disturbed areas
studied were comparable in habitat structure, species
composition, and flower density to natural sites nearby.
Most of the study was conducted from June through
August, 1973-1975, but we spent short periods on the
study area in 1972, 1976, and 1977. In each of these
years, we also visited similar habitats in the southern
Rocky Mountains and the isolated mountain ranges of
southern Arizona and New Mexico, where many of
the same flower species also occur. Observations in
these areas were an invaluable source of comparative
information which enable us to be more confident of
the generality of the results reported here.
Characteristics of flowers, nectar, and pollen
Our work centered around local habitats where red,
tubular, hummingbird-pollinated flowers were in
bloom. We concentrated on sites where each species
was sufficiently abundant to measure conveniently floral and nectar characteristics, but we also searched
over the range of habitats and elevations in the study
area to document distributions and to observe plantpollinator interactions where densities were low. Densities of flowers of each species were recorded using
an arbitrary scale which ranged from one (<0.05 inflorescences/m2) to five (>5 inflorescences/m2). Specimens of each species were obtained to verify identification and to obtain reference pollen samples.
Not all flower species were studied with equal intensity. We tried to obtain basic data on distribution,
flowering time, floral morphology, and 24-h nectar secretion rates for all species. We made particularly detailed measurements on three species, Ipomopsis aggregata, Penstemon barbatus, and Castilleja integra,
which were of particular interest because they often
bloomed together in dense mixed stands. Most measurements of these species, as well as data on hummingbirds foraging on them, were obtained in the immediate vicinity of a single large meadow, 6 km
northeast of Nutrioso, Arizona at 2300 m elevation.
Several characteristics of flowers were measured,
including length of the constricted floral tube (corolla
1023
of most species), which permits insertion of only the
bill and tongue of a foraging hummingbird. Life of
flowers was determined by removing all existing blossoms from a plant, marking individual flowers as they
opened, and recording when these were dropped. Importance of animal pollination was assessed by covering individual plants with fine (3-mm) mesh nylon
bags and leaving them in place for the entire blooming
season. The mesh was sufficiently fine to exclude all
animal visitors except the smallest insects. Adjacent
plants of similar size, marked at the time of bagging
but left uncovered, served as controls. Bagged and
control plants were collected at the end of the flowering season when number of inflorescences, aborted
flowers, fruits, and seeds were counted.
Nectar secretion and availability were measured by
collecting nectar from individual flowers in calibrated
microcapillary tubes. Nearly all samples were taken
at the same time of day (1400-1600) to standardize for
daily variation in nectar secretion and hummingbird
foraging. To measure rates of nectar secretion, plants
were covered with nylon mesh bags to exclude nectar
feeders. After flowers had been bagged for 24 h, accumulated nectar was measured, and amount of nectar
in control flowers, measured at the time of bagging,
was subtracted to calculate secretion rates. This method does not take into account those flowers which
opened and began secreting nectar during the 24-h period of measurement. However, when the life of flowers is known, it is possible to correct measurements
of nectar secretion rates for the proportion of newly
opened flowers that have not been secreting for the
full 24 h. Nectar concentration was measured with a
hand-held, temperature-compensated refractometer.
This measures nectar concentration in terms of equivalent percent sucrose and gives an accurate estimate
of its caloric value to hummingbirds (Hainsworth and
Wolf 1972).
Because rates of nectar secretion per flower are
small, it is difficult to measure accurately daily patterns of nectar secretion. However, we were able to
estimate these patterns for I. aggregate and P. barbatus in 1974 when hummingbirds were so dense in
relation to floral resources that their foraging kept the
standing crop of available nectar per flower at very
low levels. At standard times throughout the day
(0600, 0900, 1200, 1500, 1800), we measured the volume of nectar in half of the flowers on sample plants,
then immediately bagged the remaining flowers on
sample plants, left the bags in place for 2 h, and then
measured nectar volume in these flowers. Secretion of
nectar during the 2-h period was determined by subtracting the mean initial volumes prior to bagging from
the mean final volumes after bagging. By using the
same technique, but leaving bags in place either from
0600-2000 or from 2000-0600, we also measured secretion during daytime and overnight periods, respectively.
1024
JAMES H. BROWN AND ASTRID KODRIC-BROWN
Pollen samples were collected from mist-netted
birds by pressing the sticky side of clear plastic tape
against the bird and then sticking the tape to a clean
white paper or glass slide. Separate samples were taken from the bill, crown, sides (cheeks), and chin.
These samples were returned to the laboratory where
number and species of pollen grains were counted under a microscope. If a sample contained fewer than
100 grains, all were counted; otherwise, the first 100
grains in arbitrarily selected fields were counted.
Flower stigmas were collected, prepared under clear
plastic tape, and the adhering pollen grains were later
counted under a microscope. Pollen of P. barbatits
collapsed and became difficult to detect when it had
germinated on nonspecific stigmas, so counts of P.
barbatus stigmas provide only a very conservative estimate of the quantity of nonspecific pollen present.
Length and width of pollen grains were measured with
an ocular micrometer.
RESULTS AND DiSCUSSION
Spatial anal temporal distribution
of'fl()
ers
Nine species of red, tubular flowers, representing
eight genera and seven families, bloomed within 30 km
of Alpine, Arizona (Table 1). These plants are herbaceous perennials, except for Lonicera arizonica,
which is a trailing, somewhat woody perennial vine,
and Ipomopsis aggregate,
which is a biennial herb.
Distribution of the flower species varied spatially
with habitat and elevation (Table 1). Penstenon barbatiis and I. aggregate were abundant and widespread. They occurred in many habitats and over a
wide range of altitudes. They attained their highest
densities in open or disturbed habitats such as meadows, cliffs, eroded hillsides, and banks of temporary
watercourses, where they often bloomed profusely in
mixed stands which sometimes exceeded densities of
20 inflorescences and 250 flowers/m2. The two species
of Castilleja also were abundant, but they were segregated by habitat: C. integra occurred in dry meadows and open piflon-juniper woodland below 2500 m,
whereas C. austromnontana was common in the herbaceous understory of aspen and conifer forests above
2500 m. Lonicera arizonica and Echinocerelis triglochidiatus were restricted to mesic talus slopes and
bare rock outcrops, respectively, but sometimes they
were dense in appropriate habitat. Aquilegia triternata
and Si/ene laciniata were found only at low densities
in a few mesic habitats at high elevations. Lobelia
cardlinalis was known only from one population of
100 individuals growing along the outflow of a small
spring at 2000 m.
Distribution of these flowers also varied temporally,
both within a growing season and from year to year.
Most species bloomed for long periods (6-12 wk)
wherever they occurred. Although there was some
tendency for the peak flowering of some coexisting
Ecology, Vol. 60, No. 5
species to be displaced (Table 1; Kodric-Brown and
Brown 1978), the overall pattern of flowering phenology was such that there was much interspecific overlap and hummingbird flowers bloomed in most habitats
throughout the summer. In arid habitats at low elevations, E. triglochidiatus and C. integra bloomed
first, followed by P. barhatus and then by I. aggregata, but there was much overlap. In more mesic habitats higher in the mountains, there was somewhat
more separation; A. triternata, Lonicera arizonica and
E. triglochidiatus were replaced later in the season by
P. barbatus, I. aggregate, C. austromontana, and S.
laciniata. Lobelia (ardlinalis did not bloom until near
the end of the season, overlapping the end of the flowering period of P. barbatus and I. aggregate, which
bloomed in drier habitats nearby.
Amount and seasonal pattern of precipitation varied
greatly from year to year, and this had great effect on
the local abundance and distribution of flowers. Normally precipitation falls primarily in winter (November
to April) and summer (July to August); the spring and
fall are dry. In 1974 and 1977, winter precipitation was
far below average, and the light snow cover melted
early in the spring. Because of the ensuing drought
most flower species suffered widespread mortality and
failure to bloom. The effect was most pronounced at
lower elevations. At 2300 m, fewer than 1% of the
flowers blooming in 1972, 1973, 1975, and 1976 were
present in 1974 and 1977. In places where hillsides had
been covered with dense stands (>5 inflorescences/
mi2) during normal years, it was impossible to find a
single flower during the droughts. During the drought
years, hummingbirds competed for nectar with incredible intensity. Their frequent frequent foraging resulted in extremely low levels of nectar (standing crops)
available in individual flowers (Table 2). During 1974
and 1977, only a small fraction of the birds which normally bred on or migrated through the study area could
be supported there; many birds emigrated, but many
others undoubtedly died of starvation (Kodric-Brown
and Brown 1978).
Our earlier paper (Kodric-Brown and Brown 1978)
gave detailed data on seasonal flowering phenology
and the exact number of flowers of each species within
hummingbird territories at the primary study site.
While that paper should be consulted for details (see
especially Fig. 1 and Table 2), the major patterns will
be summarized briefly here. In 1975, P. barbatus and
C. integra flowered profusely from early July to midAugust. Ipomnopsisaggregate began blooming in midJuly, reached a peak in mid-August, and probably continued to flower well into September. We counted
flowers in 47 mapped hummingbird territories, 23 in
the period from July 20-31, 1975, and 24 from August
4-6, 1976. Number of flowers per territory ranged
from 302 to 1699. Relative proportions of the three
species varied widely from virtually pure stands of P.
barbatus and L. aggregate to approximately evenly
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1026
JAMES H. BROWN AND ASTRID KODRIC-BROWN
Ecology, Vol. 60, No. 5
2. Year-to-year variation in quantity of nectar available in two flowers on our study area in late July and early August.
Note that in the drought year of 1974, flowers contained a small fraction of the amount in other years. Since the flowers
produced nectar at similar rates in all years, this difference reflects increased rate of hummingbird visitation in 1974 when
the number of flowers blooming was < 1% of the number in flower in the other years. Values in parentheses are sample
sizes.
TABLE
x Available nectar/flower (gl)
Flower species
1973
1974
1975
1976
Penstemon barbatus
Ipomopsis aggregate
1.57 (159)
1.61 (283)
0.26 (150)
0.20 (300)
1.43 (1000)
2.14 (800)
1.14 (401)
1.60 (828)
mixed two- and three-species stands. We did not map
any territories which contained only C. integra, but
there were several such territories within 0.5 km.
These broad interspecific overlaps in space and time
are characteristic of hummingbird-pollinated flowers
throughout our entire study area.
Floral morphology and nectar
The nine species had convergent floral morphologies
(Fig. 1). All were predominantly bright red, had generally tubular shapes, and in all species except E. triglochidiatus the tube was constricted so as to admit
only the bill and tongue of a foraging hummingbird. In
seven species the tube was of similar length (20-25
mm, Table 1). Since most species belong to different
genera and families and have close relatives which are
strikingly different in appearance and are insect pollinated (Grant and Grant 1968), the similarities must
be attributed to convergence toward a common hummingbird-pollinated form. As is often true in evolutionary convergence, these species have achieved similar appearance and function by different means. For
example, most species had petals fused to form a
thickened corolla tube, but S. laciniata had thin, sep-
arate petals held in a functional tube by a tubular calyx, and A. triternata had long, tubular spurs on the
petals which contained nectaries at the bases. In the
two species of Castilleja, most of the red color was
owing to coloration of the stout bracts which surrounded the rather fragile, colorless perianth. In some
species the convergent similarity involved not only the
individual flower, but also extended to the arrangement of blossoms on the inflorescence. The most striking example was provided by I. aggregate, P. barbatus, and Lobelia cardinalis; these species displayed
their flowers on loose spikes having similar numbers
and spacing of open blossoms (Table 3).
We might expect these flower species also to have
converged to provide similar nectar rewards; otherwise, hummingbirds might learn to discriminate
against those flowers which secrete less sugar than
others (Hainsworth and Wolf 1976). Unfortunately the
problem is more complicated, because the costs of
hummingbird foraging vary with flower density, environmental temperature, intensity of competition
with other birds, and other factors. In order to be similarly attractive, flowers should provide similar net,
rather than gross, rewards, and we might expect sig-
3. Characteristics of the three species of hummingbird-pollinated flowers which were studied in detail where they
bloomed in mixed stands, 6 km northeast of Nutrioso, Arizona. Values of 24-h nectar accumulation in bagged flowers
measured in 1975 were used to calculate nectar secretion, corrected for differences between species in the proportion of
new flowers opening each day. Note that this method results in all three species showing higher and more similar rates of
nectar secretion than the values presented in Table 1. Sample sizes are given in parentheses.
TABLE
Species
Arrangement of flowers on plant
Mean nectar
Mean life of concentrations
flower (d)
(% sucrose)
Mean 24-h
nectar secretion*
(pA)
(mg
sucrose)
Ipomopsis
aggregate
Loose, branched inflorescence; usually
1-4 inflorescences/plant and 5-15 open
flowers/inflorescence
1.81 (104)
27.54 (52)
8.59 (100)
2.37
Penstemon
barbatus
Loose, branched inflorescence; usually
1-6 inflorescences/plant and 4-12 open
flowers/inflorescence
2.96 (89)
33.89 (41)
7.55 (100)
2.56
Castilleja
integra
Tight, unbranched inflorescence; usually
2-7 inflorescences/plant and 2 receptive
flowers/inflorescence
2.00 (33)
41.75 (31)
4.98 (96)
2.08
* 24-h nectar secretion (y) was calculated from the equation A
py/2 + (I - p)(x + y), where A = 24-h accumulation in
bagged flower, x = amount of nectar in control flower at time of bagging, and p = proportion of new flowers opening each
day. Values of p used were 0.5, 0.33 and 0.5 for I. aggregate, P. barbatus and C. integra. respectively.
October 1979
1027
TEMPERATE HUMMINGBIRD FLOWERS
Ipomopsis
uggregatf
Penstemon
burbafus
Cast//fe/u
infegru
Aqul/egia
triternato
Lonicera
arizonica
Castif/e/u
austromontana
Silence
Eclinocereus
Lobe li
triglochidiatuls
card/na//s
Gciftiatf
FIG. 1. Scale drawings of the nine species of red, hummingbird-pollinated flowers which bloomed on the study area. Note
the convergence in size and form.
nificant local variation in rates of sugar secretion. Over
our entire study area, most flowers secreted 1-8 gl of
nectar, which varied in concentration from 20-45%
sucrose; this amounts to secretion rates of 0.5-2.5 mg
of sucrose/d (Table 1). A conspicuous exception was
Lobelia cardinalis, which secreted no nectar and appears to be mimetic. Although the five-fold variation
in nectar secretion rates may not appear to make a
convincing case for convergence, it is much less than
the 40-fold variation recorded for nonconvergent hummingbird-pollinated flowers in Puerto Rico (Brown and
Kodric-Brown, personal observation) and the almost
1000-fold variation among morphologically dissimilar
bumblebee-pollinated flowers which bloom together in
the same habitats in Maine (Heinrich 1975).
A better test for convergence in nectar secretion
rates is degree of similarity when flowers bloom simultaneously in mixed species stands, because costs
6 --60
4. Effects of bagging flowers to exclude pollinators
on fruit and seed set in two species of hummingbird-pollinated plants. Note that bagged plants produced approximately as many inflorescences and flowers, but far fewer
fruits and seeds than unbagged controls.
TABLE
PENSTEMON BARBATUS
4 -
c?I
-40
0
2~~~~~~~0
2
2
2
z~~~~~~~~~
0~~~~~~~~~
C)
Ecology, Vol. 60, No. 5
JAMES H. BROWN AND ASTRID KODRIC-BROWN
1028
00<
0~~~~~~~~~
LAJ~~~~~~~~~~~~~~~~~~~~~~~~~~L
z~~~~~~~~~
Inflorescences/
Plants plant
Bagged
Control
10
10
Bagged
Control
8
8
Fruits/
plant
Seeds/
fruit
Penstemon harhatus
6.40
50.10
2.60
35.00
58.10
2.70
6.48
30.35
Ipoinopsis
2.75
2.50
Flowers/
plant
aggregat(1
236.13
188.00
13.50
105.75
3.76
5.97
I. aggregate and P. barbattus, but these do not suggest
any strong displacement in daily patterns of nectar
secretion (Fig. 2). Although there is some tendency
for P. barbatus to secrete more nectar at night and in
z
the early morning and for I. aggregate to secrete most
O
?QOQO
HbJI a
Z
0
~~~~~~~~0
of its nectar in the afternoon, in general the two
=?
Nspecies show broadly overlapping patterns of secreP
o
0.0
tion throughout the daylight hours. Furthermore, comparisons of standing crops of nectar in flowers measured at the same time of day (Table 2) suggest that
aggregatea during the day, measured by bagging flowers for these two species make nectar available to humming2-h periods during the day, as well as during the entire day- birds at comparable rates throughout the day. Obserlight period (0600-2000). overnight (2000-0600). and for 24
hummingbirds foraging in mixed species
h. Values are means of accumulated nectar minus amounts vation of
stands suggested that they visited flower species in the
in control flowers measured at the time of bagging. Nectar
order and proportions that they encountered them
concentrations as percent sucrose are also given.
(Kodric-Brown and Brown 1978).
An unexpected result of this study was the discovto the hummingbirds should be similar, particularly ery of an apparently mimetic population of hummingwhen the flowers have similar densities and spatial bird-pollinated flowers. Whereas the Lobelia cardiarrangements on inflorescence. WhereI.
<ggrgata, nalis on our study area conformed in other respects
P. barbatuls, and C. integra bloomed together on the to the convergent pattern of the other hummingbird
primary study area, they secreted sucrose at very sim- flowers, they secreted no nectar (Table 1). Although
ilar rates (Table 3). Ipomopsis aggregate and P. bar- we bagged large numbers of plants in two different
batuls were particularly similar in floral morphology summers, we were unable to obtain nectar from a sinand display, and foraging hummingbirds often visited gle flower. Plants transplanted to our garden near Tucthese species indiscriminately in the sequence and son bloomed profusely, but also secreted no nectar.
proportions in which the flowers were encountered
We observed several hummingbirds visiting these
(Kodric-Brown and Brown 1978). It is perhaps addi- flowers, both in their natural habitat and in our garden,
tional evidence of convergence that these two species and we found pollen of L. (cardinalis on birds captured
provided nectar to the hummingbirds at similar rates, in the immediate vicinity of this population in its nateven though they differed in floral lifespan and hence ural habitat.
in the total amount of sucrose secreted by a flower
Distribution o( pollen
during its life. What matters to the hummingbirds is
the rate at which sucrose can be harvested, and we
Animal pollinators were required for fruit and seed
take the near identity of secretion rates (Table 3) and set in these flowers, and hummingbirds were the only
quantities of available nectar per flower (Kodricimportant pollinators. Plants of Ipoinopsis aggregate
Brown and Brown 1978) as evidence thatgthes species and P. barbatus. which were bagged to exclude all
have converged to offer similar rewards at least when animal visitors, produced as many inflorescences and
they bloom together in mixed stands.
flowers as unbagged control plants, but set less than
It is possible that flowers which are otherwise sim- 10%,as many seeds (Table 4). Very few insects were
ilar in morphology and nectar rewards might secrete seen visiting the flowers. Butterflies (Papilio glaucius),
nectar at different times of day. We have data only for hawkmoths (Celerio lineata), and small solitary bees
4-
o
--40
-
o
Z>
0
October 1979
1029
TEMPERATE HUMMINGBIRD FLOWERS
5. Distribution of pollen on three species of hummingbirds on the study area in 1975. Values are mean numbers of
pollen grains per bird, counting only those birds with pollen on some part of the head. Note that Pensternon and Castilleja
pollen is transported primarily on the crown and bill, whereas Ipomopsis pollen is carried mainly on the chin.
TABLE
Hummingbird
species
Selasphorus rufus
(N =63)
Pollen
species
Penstemon
harbatus
Castelleja
sp.
Ipomopsis
aggregata
Pollen
location
Bill
Crown
Sides
Chin
34.4
74.2
29.5
28.2
4.6
14.0
5.9
5.9
0.8
1.0
9.1
18.9
Archilochus alexandri
(N =2)
Selasphorus platycercus
(N
9)
Penstemon
Other harbatus
4.2
2.7
1.6
2.0
Castilleja
sp.*
Ipomopsis
aggregata
5.0
11.3
2.6
3.3
0.1
0.4
1.3
4.0
51.9
79.4
19.4
17.9
Penstemon
Other harbatus
2.6
3.1
0.8
4.5
15.0
77.5
16.0
3.0
Castilleja
sp.*
Ipomopsis
aggregata
Other
2.5
21.5
8.5
0.0
0.0
0.0
0.0
0.0
0.0
1.0
2.0
0.0
* Most of this pollen undoubtedly is from Castilleja integra, the most abundant species of Castilleja where these birds
were captured. Pollen from different species of Castilleja could not be distinguished.
visited flowers in a manner that might have resulted
in some pollination, but these accounted for much less
than 5% of all animal visits which we observed. Bumblebees (Bomnbussp.) robbed nectar from flowers of
I. aggregate and P. barbatus in some localities, but
they cut through the corolla at the base without contacting the anthers and stigma.
We observed literally hundreds of hummingbirds
foraging at thousands of flowers on the study area, and
we recorded hummingbird visits to all flower species
(Table 1). At least two species of hummingbirds visited
each flower species, and we are confident that resident
hummingbirds visited all flower species within their
territories. In addition to territorial residents, nonterritorial individuals moved through the study area,
sneaking into territories and visiting flowers defended
by resident birds (Kodric-Brown and Brown 1978).
From data on numbers of flowers and amounts of nectar per flower on hummingbird territories, it is clear
that hummingbirds were the only animals which re-
moved significant amounts of nectar from I. aggregate
and P. barbatiis on our primary study area (KodricBrown and Brown 1978).
Some coexisting flower species differed conspicuously in the placement of anthers and stigma (Table
1). This suggested that flowers might use different
parts of the hummingbird head to transport pollen.
This was confirmed by analysis of pollen collected
from hummingbirds (Table 5). Penstemon barbatuts
and C. integra, which have dorsally located reproductive structures, placed most of their pollen on the
crown and top of the bill, whereas I. aggregate, which
has ventrally located anthers and stigma, deposited its
pollen primarily on the chin. The distribution of pollen
of P. barbatus and C. integra might have been more
segregated than is apparent from our data. Pollen of
both species was white and could not be distinguished
with the naked eye. In the San Francisco peaks about
200 km west of our study site, Castille a conflisa
bloomed together with P. barbatus and had a distinc-
6. Distribution of pollen of different plant species on stigmas of three species of hummingbird-pollinated flowers on
the study area in 1975. Note that half or more of the stigmas have some grains of heterospecific pollen and about 20% of
all stigmas had more heterospecific than conspecific pollen.
TABLE
Stigmas of
With pollen of
Penstetnon barbatus
Castilleja sp.*
Ip(mopsis aggregate
Other
With some heterospecific pollen
Penstemnon barbatist
(N = 111)
Castilleja integra
(N
75)
Ipomopsis aggregate
(N
80)
Number
107
28
4
36
(96.4)
(25.2)
(3.6)
(32.4)
Number
19
65
34
18
(%)
(25.3)
(86.7)
(45.3)
(24.0)
Number
21
18
77
3
(S)
(26.3)
(22.5)
(96.3)
(3.8)
55
(49.5)
48
(64.0)
46
(57.5)
(Cc)
With more grains of heterospecific
than nonspecific pollen
21
(18.9)
17
(22.7)
18
(22.5)
* Most of this pollen undoubtedly is from Castilleja integra, but pollen from different species of Castilleja could not be
distinguished.
t Quantity of P. harbatus pollen on nonspecific stigmas is underestimated because grains of this species collapse. and are
difficult to detect once they have germinated on compatible stigmas.
1030
JAMES H. BROWN AND ASTRID KODRIC-BROWN
Ecology, Vol. 60, No. 5
tive yellow-orange pollen; its pollen was carried by TABLE 7. Means and standarddeviations of body weights
and bill lengths of the three common species of humminghummingbirds at the base of the bill and the front of
birds on the study area. Sample sizes are given in parenthe crown, farther forward on the head than most poltheses.
len of P. barbatus.
Despite displacement of reproductive structures
Bill length
Body weight*
(mm)
(g)
among some species so that pollen tends to be trans- Species
ported on different parts of the bird, much interspe- Selasphorus rufus
cific pollen transfer occurred. About half of all flower
15.7 ? 0.6
3.48 + 0.41
(118)
(13)
stigmas sampled had some heterospecific pollen, and
almost 20W had more heterospecific than nonspecific
16.7 ? 0.8
3.45 + 0.35
(97)
(13)
pollen (Table 6). This is not surprising in view of the
indiscriminate foraging of hummingbirds among these Selasphorus platycercus
flower species. Of 119 hummingbirds sampled, the av16.9 ? 0.7
3.44 + 0.32
(12)
erage bird was carrying 3.2 species, and 34% of the
(39)
birds had four or more species of pollen. Since pollen
17.1 ? 1.1
3.76 + 0.32
9$
(31)
(21)
of all species is generally similar in size, shape, and
consistency, competition for pollen transport is poten- Archilochus alexandri
tially severe and appears to favor coexisting species
17.8 ? 0.5
? 0.21
dSd3.12
(17)
which deposit pollen on different parts of the bird. The
(15)
20.2 + 0.6
best evidence for character displacement in placement
9 $?
3.34 + 0.21
(3)
(16)
of reproductive structures comes from I. aggregate.
Ipomopsis and the closely related genus Gilia have
* Datafrom sources indicatedin Kodric-Brownand Brown
basically radially symmetrical flowers (Grant and (1978, Table 3).
t Length of exposed culmen measuredon birds captured
Grant 1965), but some populations have secondarily
in this study.
evolved either dorsal or ventral placement of anthers
and stigmas. Ventral orientation in our population of
I. aggregate is achieved by downward curvature of
GENERAL DISCUSSION
the style and differential exertion of the lower anthers.
Convergence, competition, and
This condition contrasts with the symmetrical oriencharacter displacement
tation of reproductive structures in Ipomopsis tenuiWe have documented convergence of the hummingtuba (Brown and Kodric-Brown, personal observations). a hawkmoth-pollinated form which occurs bird-pollinated flowers on our study area. Several cotogether and hybridizes with I. aggregate in the existing species are convergent not only in size, shape,
mountains of Arizona. Ventral displacement of repro- and color, but also in nectar rewards and arrangement
ductive structures in I. aggregate causes pollen to be of flowers on the inflorescence. The convergence is
transported primarily on the chin of hummingbirds and particularly marked in those species which bloom toreduces competition with coexisting P. barbatus and gether in mixed stands. The similar appearance and
Castilleja species which place their pollen on the bill nectar rewards result in generally nonselective foraging by all of the hummingbird species on the study
and crown (Table 5).
Although we quantified pollen loads collected from area on all of the flower species. These hummingbirds
many hummingbirds and flower stigmas, we could de- are all extremely similar in body size and bill length
tect no systematic relationship between species com- (Table 7; Kodric-Brown and Brown 1978). Undoubtposition of these pollen samples and species compo- edly floral convergence increases the probability that
a flower will be visited by a hummingbird and insures
sition of the flowering plants in the immediate vicinity.
There was a general correspondence on a large scale; that any hummingbird can serve as a pollinator, but
it also increases the likelihood and intensity of interfor example, hummingbirds captured long distances
from the nearest flowers of a particular species rarely specific competition for pollinators.
A rapidly increasing literature presents evidence of
carried that kind of pollen. However, pollen loads
from hummingbirds or stigmas collected in a mixed competition for pollinators among coexisting plant
species stand were highly variable and did not corre- species (e.g., Robertson 1895, Free 1968, 1970, Grant
spond closely to the species composition of flowers in and Grant 1968, Levin 1968, 1972, Macior 1970, Mosthe stand. We suspect that this is because pollen carry- quin 1971, Heithaus 1974, Heinrich 1975, 1976, Stiles
over from one plant to the next is limited, so that 1975, Lack 1976, Feinsinger 1978, Waser 1978).
pollen loads reflect the pattern of immediately pre- Much of the evidence consists of: (1) character
displacement in habitat or flowering phonology so that
vious pollinator visits and these are highly stochastic.
Detailed investigations of pollinator movements and the same kinds of pollinators are shared but not utipollen dispersal in stands of varying species compo- lized simultaneously, (2) divergence in floral characteristics which promote species-specific pollinator forsition clearly are warranted.
October 1979
TEMPERATE HUMMINGBIRD FLOWERS
1031
aging, and (3) character displacement in orientation of be limited by energy and/or other resources, but not
anthers and stigma so that pollen is transported on by availability of pollen or pollinators. However, male
different parts of the body of shared pollinators. Most function (pollen dispersal) should be limited by comstudies infer the role of competition from circumstan- petition to fertilize the limited number of ovules that
tial evidence and do not attempt to describe the un- will ultimately develop into seeds, and hence should
derlying mechanisms or to quantify their effects on be limited by availability of pollinators. If this view is
individual fitness and population size. The problem of correct, it suggests that virtually all competition
estimating the magnitude and mechanism of competi- among plants for pollinators must occur through limtion for pollinators is complicated by the fact that itation of male function. It also provides another reaplants do not compete for pollinators in the same way son why competition for pollinators may affect plant
that animal and plant populations compete for most fitness and result in coevolution without significantly
other limited resources. Unlike competition for light, affecting population size. The only reliable data that
water, and nutrients among plants or for food and we have bearing on Charnov's hypothesis are for Ipospace among animals, competition for pollinators does mopsis aggregate. This species set 56% of its flowers
not use up the limited resource and make it absolutely as fruit and an average of six seeds per fruit (Table 4),
unavailable to other individuals. In fact outcrossing is but 47 (59%) of 80 stigmas had six or more nonspecific
accomplished only because the potentially limited pol- pollen grains. The latter probably underestimates the
linators are shared at least among some intraspecific real situation, because we could not see all of the stigcompetitors. A consequence of this difference in the matic surface when counting grains and we may have
mechanism of competition is that complete interspe- collected some stigmas before the plants had been
cific overlap in utilization of pollinators need not result completely pollinated. On the other hand, some of the
in competitive exclusion or even significant reductions grains may have been incompatible pollen from the
in population density among competing plant species.
same plant. The observation that seveval stigmas had
We suspect that coexistence among plant species, par- more than 40 grains suggests that interference comticularly among distantly related taxa such as the hum- petition for space on the stigmatic surface rarely, if
mingbird-pollinated flowers studied here, depends pri- ever, limits seed set. While these data are not definimarily on subdivision of edaphic requirements. While tive and experimental tests of Charnov's hypothesis
competition for pollinators may not be sufficiently in- are urgently needed, we suspect that these plants comtense to have large, direct effects on population size pete for pollinators primarily, if not exclusively,
and coexistence, it apparently reduces fitness suffi- through male function. If this is true, competition
ciently to act as an important selective agent in plant- among species for shared pollinators is probably a
pollinator coevolution, and thereby to influence the weak force in influencing plant-community structure
structure of plant communities.
in ecological time, although it can lead to significant
Coexisting plant species might compete for shared adaptive change over evolutionary time.
pollinators in two ways. One is by interfering with the
Interspecific interference with pollen transport aptransfer of pollen to nonspecific stigmas. Limited stig- pears to be important in the coevolution of commumatic surfaces may be occluded with heterospecific nities of plants and pollinators which share each othpollen, preventing fertilization of female gametes.
er's services. Significant quantities of pollen are
Also pollen deposited on heterospecific stigmas rep- actually deposited on heterospecific stigmas. Flower
resents loss of male gametes capable of fertilizing species have evolved to reduce this form of competiovules. Coexisting plant species might also compete tion by character displacement in orientation of the
simply to attract pollinators. Even in the absence of anthers and stigmas so that pollen is transported on
interference with pollen transport, it would be advan- different parts of the bird (see also Grant and Grant
tageous to have a species-specific pollinator, which 1968). Apparently once interference competition
would visit more nonspecific flowers and produce among these flower species has been reduced to some
more outcrossing than a nonselective one. Plants tolerable level, the advantages of converging to use
potentially can avoid both interference with pollen the same pollinators outweigh the disadvantages of
transport and exploitative competition for shared pol- diverging to coevolve species-specific associations. In
linators by coevolving specific plant-pollinator asso- this respect temperate communities of hummingbirds
ciations, either directly or indirectly by flowering at and flowers differ from two other plant-pollinator asdifferent times and in different places. Interference sociations that have been well studied. Not only are
with pollen transport potentially can be avoided by temperate hummingbird-pollinated flowers convercharacter displacement in location of reproductive gent, but also the hummingbird species which utilize
structures, but plants which diverge only in this re- them are strikingly similar in body size and bill length
spect might still compete to attract shared pollinators. (Table 7). Tropical communities of hummingbird flowRecently Charnov (in press) has suggested that in ers typically vary greatly in size, shape, and nectar
outcrossed, hermaphroditic (with perfect flowers) rewards and are visited selectively by hummingbird
plants such as these, female function (seed set) should species which differ in body size and in length and
1032
JAMES H. BROWN AND ASTRID KODRIC-BROWN
pomopsts aggregate
,--'
Archi/ochus co/ubrys
?
ftL1 Archi/ochus
Ecology, Vol. 60, No. 5
alexandri
*enslemon
arba/us
.
Calyple0cosine
=3
Calypte
y
Se/osphorus
*
-
' Ste//u/n
.- -
.b
p/otycercus
Se/osphorus ru/us
Se/osphorus
,s+
-
sos/n
calliope
E1
.r"
Coste/le/a
in/egro
Coste//eta
austromontona
Lan/cern arizoni-co
tri'terno:to
~~~~~~~~~~~~~~~~~~~~~Aquil
Si/ene Inciniato
EchlOnocereus
trig/och/dioltus
Lobe/ia cardinal/s
FiG. 3. Approximate geographic ranges of the eight hummingbird species which are widely distributed north of Mexico
(left), and of the nine flower species which coexist on our study site (0) in eastern Arizona (right). Note that there is no
correspondence between the distributions of particular hummingbird and plant species.
shape of the bill (Snow and Snow 1972, Stiles 1975,
Feinsinger 1976, Wolf et al. 1976, Feinsinger and Colwell 1978). Temperate bumblebee-pollinated flowers are diverse in morphology and color, and individual species tend to be visited specifically by bee
species with appropriate tongue lengths and by individual bees that have learned to forage efficiently from
them (Heinrich 1975, 1976a, 1976b, Inouye 1976). Why
are temperate hummingbird-plant communities characterized by convergence and nonspecific plant-pollinator associations?
We suggest that there is no simple answer to this
question. Because competition for pollinators need not
result either in divergence in utilization or in competitive exclusion, sharing of pollinators represents only
a relative disadvantage which can be outweighed by
net benefits of convergence. The situation is complicated because the optimal strategy of the plants depends not only on inherent characteristics of their pollinators, but also on the capacity of these resources to
coevolve. The following characteristics of temperate
hummingbirds and hummingbird-pollinated plants all
appear to be important in the coevolutionary convergence in community structure:
1) Geographic ranges of individual hummingbird and
plant species appear to be independent of each oth-
er (Fig. 3). Temperate hummingbirds are migratory,
and their extensive breeding, wintering, and migratory ranges include many flower species. Ranges of
hummingbird flowers appear to be limited primarily
by edaphic conditions and competition from nonhummingbird-pollinated plant species. Thus it is
advantageous for any hummingbird species to recognize and forage from any sufficiently rewarding
flowers within its range, and it is likewise advantageous for hummingbird-pollinated plants over all
of western North America to employ similar signals
and rewards to attract whatever hummingbirds are
locally available (Grant 1966).
2) Temperate hummingbirds tend to be intra- and interspecifically territorial (Pitelka 1942, Armitage
1955, Cody 1968, Dunford and Dunford 1972, Stiles
1973, Gas et al. 1976, Yeaton and Laughrin 1976,
Kodric-Brown and Brown 1978), so that often only
one resident avian nectarivore is reliably available
to serve as a pollinator within a local area. This
makes it highly advantageous for all bird-pollinated
plant species to be able to share the same individual
pollinator.
3) Abundance and species composition of hummingbird-pollinated plants vary greatly between local
areas and between seasons (Table 3; Kodric-Brown
and Brown 1978). This variation in the competitive
TEMPERATE HUMMINGBIRD FLOWERS
October 1979
environment means that only some local populations in some seasons may compete intensely for
pollinators.
4) Plants which usually grow at low densities potentially have much to gain from hummingbird pollination, because the birds' high-energy requirements and vagility result in foraging patterns which
promote long-distance pollen transport. However,
these rare species may have difficulty attracting and
sustaining avian pollinators unless they share them
with other plant species which will supply some of
the foraging and maintenance costs.
5) Because hummingbirds hover while foraging, their
position relative to flowers is highly predictable,
and it is possible to avoid much interference competition for pollen transport by displacement in
orientation of anthers and stigmas. Once such interference is reduced, deleterious effects of competing to attract pollinators may be small.
The convergent structure of temperate communities
of hummingbirds and flowers is a stable condition
which has evolved because of mutual advantages to
both plants and pollinators. The combination of factors which selects for this convergence in temperate
hummingbird-plant associations does not occur in
either tropical hummingbird-flower or temperate bumblebee-flower associations. Tropical hummingbirds
are nonmigratory, and some species have different
strategies for using and defending space which permit
local coexistence (Feinsinger and Colwell 1978).
At least one of these strategies, "traplining," appears
to represent a coevolutionary adaptation to forage
from and pollinate flower species which occur at low
densities. In addition there probably is less year-toyear variation in local availability of flowers in most
tropical habitats.
Bumblebees are neither migratory nor territorial.
Since several species and many individuals may have
broadly overlapping foraging areas, it is possible for
coexisting flower species to develop species-specific
pollinator relationships with particular bumblebee
species and individuals (Heinrich 1975, 1976a, 1976b,
Inouye 1976). Also, because bees are relatively small,
have well-developed pollen-gathering and grooming
behavior, and crawl into flowers, it may be difficult
for bumblebee-pollinated flowers to avoid interference
competition by orienting reproductive structures to
use different parts of the bee to transport pollen.
Nectar secretion
and mimicry
Hummingbird flowers attract pollinators because
the birds find it profitable to forage for the sugars contained in floral nectar. Thus it would seem that morphological convergence of flower species to attract and
use the same pollinators must be accompanied by coevolution of convergent nectar rewards. Otherwise,
birds would discriminate against less rewarding
1033
species and select for distinctive signals by which the
more productive species would advertise their superior rewards. The virtually identical secretion rates of
the three species which bloomed together profusely at
the primary study site (Table 2) indicate that these
coexisting, morphologically convergent flower species
apparently have also converged to offer similar nectar
rewards. Nectar secretion rates should vary in response to foraging and maintenance costs of their pollinators. Thus bird-pollinated flowers typically secrete
more sugars than coexisting or closely related insectpollinated species (Heinrich and Raven 1972, Brown
et al. 1978). We would also expect variation in
secretion rates among hummingbird-pollinated flowers
as, for example, colder climate increased the metabolic cost of thermoregulation, or more sparsely distributed flowers required the pollinator to fly greater
distances. Our data indicate significant intra- and interspecific variation in nectar secretion rates between
local areas (Table 1). Although data are too few to
make a rigorous case, it is our impression that secretion rates increase with increasing elevation (colder
climate) and decreasing flower density, as we would
expect from increasing pollinator costs.
The population of Lobelia cardinalis on our study
area appears to be mimetic. Flowers of these plants
do not secrete nectar to reward their pollinators, but
instead, obtain sufficient hummingbird visits because
of their resemblance to other hummingbird-pollinated
flowers which produce significant quantities of nectar.
This population of L. cardinalis possesses several attributes which are consistent with its apparent role as
a mimic: (1) It is rare. We know of only one population, numbering perhaps 100 plants, on our study area.
(2) It closely resembles I. aggregate and P. barbatus,
which are probably the most important models because they are common in adjacent habitats. There is
close resemblance among these species not only in
floral color, size, and shape, but also in arrangement
of flowers on loose, spike-like inflorescences. (3) This
population of L. cardinalis blooms in late August and
September when most of the hummingbirds present
are juvenile migrant Selasphorus rufus. These birds
should be generally inexperienced and, when they first
arrive from their breeding grounds in the northern
Rocky Mountains and Coast Ranges, totally unfamiliar
with the local flora. (4) Lobelia cardinalis has a very
large stigmatic surface. Not only is the receptive surface of the stigma large, but it is densely covered with
long sticky papillae which serve further to increase
surface area and to which many pollen grains adhere.
Such a large surface may be advantageous in avoiding
competition for space on the stigma from pollen grains
of more numerous model species. Of 16 Lobellia stigmas, 8 had heterospecific pollen (primarily of P. barbatus), but all 16 had some L. cardinalis pollen and
many had hundreds of grains.
Lobelia cardinalis is probably the most widely dis-
1034
JAMES H. BROWN AND ASTRID KODRIC-BROWN
tributed hummingbird-pollinated flower in North
America, and most populations probably are not mimetic. We have discovered (Brown and KodricBrown, personal observation) one other population of
this species (near Montezuma Well National Monument about 250 km west of our study area) which appears to secrete no nectar. On the other hand, Baker
(1975) records values of nectar concentration for a
population grown in Berkeley, California (original
source not indicated). We have obtained (Brown and
Kodric-Brown, personal observation) amounts and
concentrations of nectar typical of other hummingbird
flowers from a population of L. cardinalis in the Chiricahua Mountains of southeastern Arizona, about 200
km south of our study site. Presumably the mimetic
populations save sufficient energy by not secreting
nectar to compensate for visits lost by not rewarding
the pollinators. Such a strategy should be advantageous only for rare flowers which occur where there
are sufficient inexperienced pollinators and nectarproducing model flowers. A number of other flower
species, particularly orchids, appear to be mimetic and
to achieve pollination by deceit without offering rewards (van der Pijl and Dodson 1967, Proctor and Yeo
1972).
Our observations on hummingbird-pollinated flowers suggest that analogs to both Mullerian and Batesian mimicry may be found in plant-pollinator interactions (also see Grant 1966, Macior 1974, Wiens 1978).
In some cases flower species may find it mutually beneficial to resemble each other and be treated
identically by shared pollinators. Then they should
converge to present similar signals and attractants in
much the same way that Mullerian mimics benefit by
adopting similar signals to advertise their distastefulness to shared predators. If a plant species is sufficiently rare, it can adopt an alternative strategy, dispense with nectar secretion, and parasitize the
coevolved relationship between more common, nectar-producing flowers and their pollinators. In much
the same way, Batesian mimics take advantage of the
warning signals of more common distasteful species
to avoid predators. Wickler (1968) describes sets of
coexisting insect species which have superficially similar, convergent morphologies and color patterns, and
which consist of a mixture of Mullerian and Batesian
mimics. Similarly the present community of hummingbird-pollinated flowers might be viewed as consisting of nine convergent species, eight "Mullerian"
mimics and one "Batesian" mimic.
ACKNOWLEDGMENTS
We thank R. Vestal and C. L. Smith for assistance with
pollen counts and data analysis, and L. Arnow for checking
flower identifications.A. C. Gibson, D. Inouye and P. Feinsinger criticallyreviewed the manuscript.Kevin and Karen
Brown provided help and companionshipin the field. Numerousstudentsand colleagues suppliedencouragementand
critical discussion, but W. M. Schaffer and N. M. Waser
Ecology, Vol. 60, No. 5
deserve special mention. The work was supported in part by
National Science Foundation Grants GB 39260 and DEB 7609499.
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TEMPERATE HUMMINGBIRD FLOWERS
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