Oecologia (2001) 128:263–273
DOI 10.1007/s004420100640
Carlos Lara · Juan Francisco Ornelas
Preferential nectar robbing of flowers with long corollas: experimental
studies of two hummingbird species visiting three plant species
Received: 29 September 2000 / Accepted: 28 December 2000 / Published online: 28 February 2001
© Springer-Verlag 2001
Abstract Long flower tubes have been traditionally
viewed as the result of coevolution between plants and
specialized, legitimate, long billed-pollinators. However, nectar robbers may have played a role in selection
acting on corolla length. This study evaluated whether
hummingbirds are more likely to rob flowers with longer corollas from which they cannot efficiently extract
nectar with legitimate visits. We compared two hummingbird species with similar bill lengths (Lampornis
amethystinus and Colibri thalassinus) visiting floral arrays of artificial flowers with exaggerated corolla
lengths, and also evaluated how the birds extract nectar
rewards from medium to long corollas of three hummingbird-pollinated plants (Salvia mexicana, S. iodantha and Ipomoea hederifolia). The consequences of
foraging for plant fitness were evaluated in terms of
seed production per flower. Variation in seed production
after legitimate visits of hummingbird-pollinated plants
was mostly explained by differences in pollinator effectiveness. Seed production did not increase with the
number of legitimate visits to a flower, except in I. hederifolia. We found that birds were more likely to rob
both artificial and natural flowers with long corolla
tubes. Nectar robbing was not observed on short-corolla
flowers of Salvia spp., but robbing negatively affected
seed production of long-tubed flowers of I. hederifolia.
Significant differences between hummingbird species in
the use of this behavior were observed, but males and
females behaved alike. We suggest that short-billed
hummingbirds with enlarged bill serrations (the edge of
both tomia finely toothed) may have an advantage in
illegitimately feeding at long-corolla flowers. This
raises the possibility of counter-selection on increasing
corolla length by nectar robbers.
C. Lara · J.F. Ornelas (✉)
Departamento de Ecología y Comportamiento Animal,
Instituto de Ecología, A.C., Apdo. Postal 63, Xalapa,
91000 Veracruz, México
e-mail: [email protected]
Tel.: +52-28-421800 ext. 4125, Fax: +52-28-187809
Keywords Colibri thalassinus · Lampornis
amethystinus · Nectar robbing · Corolla length · Seed
production
Introduction
Long floral tubes (corollas) have been traditionally
viewed as a floral adaptation for pollination by longtongued and long-billed pollinators (Darwin 1859, 1877;
Feinsinger and Colwell 1978; Stiles 1981; Feinsinger
1983). In this view, longer corollas are favored because pollinators remove more pollen grains from them
(Darwin 1862; Wolf et al. 1976; Nilsson 1988; Fenster
1991). However, this situation may be complicated by
visitors that extract nectar by piercing floral tissues without contacting the anther and stigma (nectar robbing;
Feinsinger et al. 1987; Ornelas 1994; Navarro 1999;
Maloof and Inouye 2000). Short-billed hummingbirds
often obtain the nectar of flowers by making perforations
at the base of the corolla tube or using a hole already
made by insects and birds (e.g., Beal 1880; Ridgway
1890; Grant 1952; Skutch 1954, 1973; Kodric-Brown
and Brown 1979; Inouye 1983; Kodric-Brown et al.
1984; Feinsinger et al. 1987; Ornelas 1994, 1998;
Navarro 1999; but see Colwell et al. 1974). Insofar as
birds preferentially rob flowers with longer corollas,
from which they cannot efficiently extract nectar through
the corolla mouth, they may have played a role as a selective force countering corolla elongation. Other floral
traits such as chemical deterrents (Guerrant and Fiedler
1981), dilute nectar (Bolten and Feinsinger 1978), protective floral bracts (Inouye 1983; Ornelas 1996), thickening of floral tissue (Inouye 1983; McDade 1984;
Ornelas 1998), shifts from diurnal to nocturnal nectar
production (Haber and Frankie 1982), and alliances
with protective ants (Becerra and Venable 1989; Oliveira
et al. 1999) may also be the result of selection by nectarrobbing species.
Nectar robbing by insects and passerines occurs commonly on flowers adapted for hummingbird pollination
264
(Barrows 1976; McDade and Kinsman 1980; Willmer
and Corbet 1981; Inouye 1983; Arizmendi et al. 1996;
Bittrich and Amaral 1996; Irwin and Brody 1998, 1999;
Navarro 1999; Maloof and Inouye 2000). In particular,
long-tubed hummingbird flowers are exploited regularly by various robbers that significantly reduce the
floral nectar available to pollinators (e.g., McDade and
Kinsman 1980; Snow 1981; Pleasants 1983; Arizmendi
et al. 1996; Irwin and Brody 1998; Traveset et al. 1998;
Navarro 1999; Lara and Ornelas 2001).
Skutch (1954) stated that nectar robbing is quite a
rare behavior among tropical hummingbirds, but species
of Aglaiocercus, Anthracothorax, Chalybura, Chlorostilbon, Chrysolampis, Colibri, Eulampis, Eupherusa,
Heliothryx, Thalurania, and Trochilus are consistently
reported to act as nectar robbers (ffrench 1973; Skutch
1973; Feinsinger et al. 1979; McDade and Kinsman
1980; Snow and Snow 1980; Snow 1981; Berry 1982;
Ruschi 1982; Kodric-Brown et al. 1984; McDade 1984;
Stiles 1985; Feinsinger et al. 1987; Gill 1987; Ornelas
1994, 1995; Navarro 1999). Yet, the behavior, ecology
and evolution of nectar robbing by hummingbirds has
rarely been studied (Colwell 1973; McDade and
Kinsman 1980; Feinsinger et al. 1987; Ornelas 1994;
Navarro 1999).
Hummingbirds may extract nectar illegitimately by
(1) actively piercing the base of typically long corollas
and leaving a slit in the floral tissue (primary nectar robbers); (2) using the hole left in flowers already pierced
by other species (secondary nectar robbers); (3) visiting
flowers morphologically adapted for pollination by insects or bats (nectar thieves); and (4) by reaching between the petals of polypetalous flowers (nectar thieves)
(Ornelas 1994, 1995). Ornelas (1994) found that 28 genera (23% of hummingbird genera) have species with enlarged tomial serrations (a variable number of serrations
in the terminal portion of the maxillary and mandibular
tomia). He hypothesized that enlarged bill serrations may
enhance the exploitation of resources such as long-tubed
corollas and tough-tissue corollas by facilitating access
to protected nectaries, the grasping of tough and waxy
blooms, and the cutting of flower tissue. Serrate, shortbilled hummingbirds pierce the corolla tubes near the
base to extract nectar, leaving a conspicuous slit in the
floral tissues (Ornelas 1994; Navarro 1999). These robbing behaviors have been categorized based on how
hummingbirds handle flowers to extract nectar (Inouye
1983), however, the dichotomy between legitimate and
illegitimate visitation is more useful when trying to document facultative nectar robbing. Of particular interest is
the observation that a hummingbird can behave as either
a legitimate pollinator or a robber of the same plant
species (e.g., McDade and Kinsman 1980; Soberón and
Martínez del Rio 1985; Ornelas 1994), or a legitimate
pollinator of one plant species and a robber of another
(McDade and Kinsman 1980; Soberón and Martínez del
Rio 1981; Inouye 1983). The outcomes of presumably
mutualistic interactions between a plant and its diverse
array of floral visitors are conditioned by the degree of
morphological matching between the flower and visitor,
but also by the individual behavior of the pollinator, in
particular, the mode, sequence and frequency of visitation to single flowers.
The aim of our study was to determine how individuals of two hummingbird species with relatively short
bills behave on flowers with contrasting corolla lengths.
We asked to what extent natural and experimental variation in corolla length affects (1) the frequency of robbing
visits to artificial and natural floral arrays and (2) the behavior of individual hummingbirds during each visit. We
also evaluated seed production of experimental plants.
We predicted that robbing should be more common on
longer corollas and would negatively affect seed production. To our knowledge, this is the first experimental
study of facultative nectar robbing and its causes and
consequences.
Materials and methods
Study site
Fieldwork was conducted from November to March 1992 and
from July to October 1993 at the Laboratorio Natural Las Joyas
field station (19°35′–19°37′N, 103°15′–104°37′W; at 1592 m
a.s.l.; Arizmendi et al. 1996). This 1245-ha preserve is located in
the Sierra de Manantlán Biosphere Reserve, in the Mexican states
of Jalisco and Colima. Mean annual precipitation is 1610 mm
(Jardel 1991), most of it falling between June and October when
hurricanes occur. A short dry season extends from March to May.
Mean annual temperature is 14.6°C, with freezing temperatures
occurring only for a few days during the winter (November to
February; Arizmendi et al. 1996). The reserve has a heterogeneous
topography (Jardel 1991), and the vegetation is a mosaic of wet
coniferous, pine-oak, and fragments of cloud forest along ravines,
and secondary vegetation (Vázquez et al. 1995).
Hummingbird species
Our study focused on 2 of the 21 hummingbird species recorded at
Las Joyas (Ornelas and Arizmendi 1995), the amethyst hummingbird (Lampornis amethystinus) and green violet-ear (Colibri
thalassinus), a resident and an altitudinal migrant in the study
area, respectively. Amethyst hummingbirds have straight, smooth,
medium-sized bills (mean±SD=20.72±0.10 mm, n=48 males;
mean±SD=22.30±0.10 mm, n=41 females; Ornelas 1995). Green
violet-ears have slightly curved, medium-sized bills with enlarged
bill serrations (see Ornelas 1994) (mean±SD=21.02±0.11 mm,
n=17 males; mean±SD=20.90±0.12 mm, n=19 females; Ornelas
1995). Green violet-ears nest at the field station at the end of the
rainy season and during this time feed mostly on the introduced
bee-pollinated runner bean, Phaseolus coccineus (Leguminoseae).
Amethyst hummingbirds breed early in the rainy season; during
this time, they feed mostly from flowers of Ipomoea hederifolia
(Convolvulaceae) and Crusea coccinea (Rubiaceae) (Ornelas
1995; Ornelas and Arizmendi 1995). Both species feed from
flowers that range in corolla length from 10 to 33 mm at our study
site (Arizmendi 1994; J.F. Ornelas, unpublished work).
Field procedures
A total of 120 adult hummingbirds were captured in the field for
this study. Before trials, hummingbirds were housed individually
for 1–2 days in field-collapsible cages (61×61×61 cm). These
cages were placed in a room with ambient light and temperature.
265
shown in Fig. 1. Original vegetation was not removed, to give a
more natural setting for the bird being tested. A perch was placed
inside the aviary 3 m away from the observer.
Hummingbirds were released one by one into the aviary to visit the artificial flowers for 1 h and then removed. We noted for
each hummingbird (1) the type of visit (legitimate or illegitimate),
and (2) the number of times it probed each type of flower. Because
plastic flowers cannot be pierced, probing illegitimately at the
base of artificial flowers was considered as a robbing attempt
(hereafter robbing visits). Observations were conducted from 0800
to 1200 hours and we used hummingbirds as we netted them.
Nectar robbing on natural flowers
Fig. 1 Diagram showing the arrangement of artificial flowers.
Four groups of long (58 mm) and four groups of short (33 mm) artificial flowers were placed alternately in groups of three flowers
as illustrated, with the corolla opening either facing up, down, or
horizontally
Hummingbirds had free access to 20% (by mass) sugar solution,
and ≈20 live Drosophila flies introduced to the cage two or three
times a day. Most hummingbirds acclimated to captivity within
1 day (Ornelas 1995; Lara and Ornelas 1998). We found no effect
of pre-trial housing on the hummingbird's foraging performance.
Nectar robbing on artificial flowers
We first looked for effects of corolla length and flower angle on
nectar robbing behavior using arrays of artificial flowers. We hypothesized that robbing should be more likely on longer corollas
when legitimate visitation takes a greater effort for the rewards
that can be obtained. For this part of our study 15 individuals of
each hummingbird species (8 males and 7 females) were used. We
manipulated corolla length using conical plastic micropipet tips of
33 and 58 mm length and simulated “petals” with red plastic material (Fig. 1). The lengths of corollas correspond to the range of
long-tubed, hummingbird-pollinated flowers normally encountered at Manantlán (Arizmendi 1994; J.F. Ornelas, unpublished
work). Each flower was filled with c. 20 µl of 20% (by mass)
sugar solution (Ornelas 1995) based on the 2–18 µl nectar production range known for the species studied (Arizmendi et al. 1996;
J.F. Ornelas, unpublished work). Artificial flowers were placed inside a portable, outdoor aviary (4×8×2 m). The flowers were hung
along a wire across the aviary at 1.7 m height and at a distance of
5 m from the observer. The whole floral array consisted of eight
groups with three artificial flowers each (4 groups with 33-mm
flowers and 4 groups with 58-mm flowers) 20 cm apart from each
other. To manipulate flower angle within each size group, one
flower was attached with the corolla opening facing up (0°), one
flower facing down (180°), and the third facing horizontally (90°).
To minimize the effect of treatment position, we placed the floral
arrays so as to alternate groups of small and large flowers as
We chose the most common hummingbird plant species during the
study period with contrasting corolla lengths that range from 18 to
30 mm (Lara 1995) to test whether nectar robbing is facultative on
corolla length. Preliminary observations in the study area showed
that flowers of Salvia mexicana L., S. iodantha Fernald (Labiatae),
and Ipomoea hederifolia L. (Convolvulaceae) are visited by
C. thalassinus and L. amethystinus (Arizmendi 1994; J.F. Ornelas,
unpublished work).
S. mexicana and S. iodantha are commonly found in successional areas of burned pine forest and less frequently in patches
of cloud forest (Arizmendi 1994). Their flowers are visited by 12
hummingbird species (C. thalassinus, Hylocharis leucotis, Amazilia beryllina, A. rutila, A. violiceps, L. amethystinus, Eugenes
fulgens, Tilmatura dupontii, Atthis heloisa, Stellula calliope,
Selasphorus platycercus, and S. rufus; Arizmendi 1994; J.F.
Ornelas, personal observations) and commonly pierced by
passerine Diglossa baritula (Arizmendi et al. 1996). Arizmendi
(1994) reported that more than 50% of Salvia flowers are pierced
by D. baritula under natural conditions. While it is not known
which hummingbird species are the most effective pollinators of
these Salvia species, short-billed hummingbirds (e.g., Selasphorus
spp.) are likely candidates, since they are very abundant during
winter flowering and pollen is deposited abundantly on their foreheads during a flower visit (Arizmendi 1994). Flowers of
S. mexicana, with relatively short purple corolla tubes
(mean±SD=18.7±0.02 mm, n=40; Lara 1995), are hermaphroditic,
self-compatible, and last 4 days (Arizmendi et al. 1996). Mean
numbers of seeds produced by flowers range from 0.1±0.4 (SD)
seeds by automatic self-pollination, 1.4±1.3 (SD) after a single
visit by the long-billed, least efficient pollinator (Eugenes
fulgens), to 2.5±1.2 (SD) by the short-billed, most efficient
pollinator (Hylocharis leucotis) (Arizmendi et al. 1996). Flowers
of S. iodantha, with medium-sized maroon corolla tubes
(mean±SD=21.3±0.23 mm, n =30; Lara 1995), are also hermaphroditic, self-compatible, and also last 4 days (M.C. Arizmendi,
personal communication). Both species bloom from December to
March (J.F. Ornelas, unpublished work).
I. hederifolia is a woody vine commonly growing in pine and
pine-oak forests (Arizmendi 1994). Its solitary, 1-day flowers
(Chemas-Jaramillo 1995) are visited by several hummingbird species but mostly by Eugenes fulgens and L. amethystinus, and
several species of butterflies (Chemas-Jaramillo 1995; J.F.
Ornelas, personal observations); Trigona bees and D. baritula
frequently rob its flowers (Arizmendi 1994; Chemas-Jaramillo
1995). Arizmendi (1994) reported that less than 30% of its flowers
are pierced by D. baritula under natural conditions. While it is not
known which hummingbird species are the most effective pollinators of this species, long-billed E. fulgens are likely candidates because pollen is deposited abundantly on their foreheads during a
flower visit (Arizmendi 1994). Flowers are hermaphroditic and
self-incompatible (Chemas-Jaramillo 1995) with long orangeyellow corolla tubes (mean±SD=30.2±0.32 mm, n=30; Lara
1995). Blooming occurs asynchronously year-round, but peaks
from July to September (J.F. Ornelas, unpublished work).
The remaining 90 captured hummingbirds were used in this
part of the experiment. We presented 15 hummingbirds of each
species (8 males and 7 females) with each of the three selected
266
plant species. The same aviary was used as an enclosure and
placed over naturally growing clumps of flowering plants to ensure hummingbird visitation. Clumps were formed by about eight
plants of one of the plant species displaying numerous developed
buds and open flowers. Salvia flowers last >1 day, so it was necessary to have newly opened flowers and flowers >1 day old in our
experimental sample to ensure outcrossed pollination. Inside the
aviary, flowers on plants were bagged and unbagged with bridal
netting, as needed, to control hummingbird visitation. Vegetation
surrounding plants was removed to facilitate observations.
To begin behavioral observations, we unbagged 30 open
flowers at anthesis and then introduced a hummingbird. Only one
hummingbird at a time was released into the aviary. All observations were conducted from 0800 to 1200 hours when hummingbirds are more active foraging and nectar production is high
in these plants (Arizmendi et al. 1996). For each individual
hummingbird we observed (1) whether its floral visits on each
flower were legitimate (flower visited by its entrance), illegitimate
(flower probed at the base), or robbed (flower actively pierced by
any way), and (2) how often it visited each flower within a foraging bout. Hummingbirds typically visited all 30 flowers at least
once during a session of behavioral observations, however, some
flowers were revisited and fewer not visited at all. Behavioral observations ended before anthesis of the 30 open flowers was finished. Then we released the hummingbird, inspected the flowers
for any damage, and then bagged them until seed production.
Lastly, a group of 30 non-manipulated flowers (unbagged and
outside the aviary) of each plant species was monitored until seed
set to estimate seed production under open conditions of pollination.
All statistical analyses were run using General Linear Modeling with StatView and SuperANOVA (Abacus Concepts 1989,
1996).
Results
Foraging behavior on artificial flowers
Both hummingbird species made the same number of legitimate visits to artificial flowers, independent of corolla
length and flower angle, except that individuals of
L. amethystinus made more legitimate visits on average
than C. thalassinus to short flowers facing up and to
long flowers facing horizontally (Table 1, Fig. 2). As predicted, the number of robbing visits was statistically
higher among long corolla tubes (58 mm; Table 1)
and C. thalassinus made significantly more robbing visits
than L. amethystinus, independent of flower angle (Fig. 2).
Statistical analyses
Artificial flowers
We used two-way ANOVAs to evaluate variation in the number
and type of visits to artificial flowers by individuals of the two
hummingbird species (Zar 1984). In the model, hummingbird species and sex, and their interaction were fixed main factors, and the
number of legitimate and robbing visits were dependent variables.
Next, a three-way ANOVA (Zar 1984) with fixed factors of hummingbird species, corolla length and flower angle, and all interactions, was used to explore responses to features of the artificial
flowers. Post hoc mean comparisons (Games-Howell procedure)
were conducted to examine differences between hummingbird
species in visiting (legitimately and robbing attempts) short and
long artificial flowers.
Natural flowers
The same two-way ANOVA model was used to evaluate variation
in number of visits to flowers of S. mexicana, S. iodantha, and
I. hederifolia, and the effects of hummingbird species and number
of visits on seed production variation of flowers of these species
receiving legitimate visits.
Because some flowers of all plant species ended up being revisited by hummingbirds, it was necessary to control for these differences in the analysis, as they might otherwise obscure the effect
that floral visitors have on seed production. We analyzed the relationship between seed production and hummingbird visitation
with ANCOVA (Zar 1984). In the model, hummingbird species
was a fixed factor, number of visits to a flower was a covariate,
and seed production was the dependent variable. The same analysis was used for legitimate and legitimate with robbing or illegitimate probes. Robbing visits were not analyzed this way because
of small sample sizes. Post hoc mean comparisons (GamesHowell procedure) were conducted to examine the data for differences in seed production among flowers visited legitimately, legitimately visited and then robbed or illegitimately probed, and only
robbed by the two hummingbird species.
Fig. 2 Variation in number of a legitimate and b robbing visits to
short and long artificial flowers offered at various angles to individuals of Colibri thalassinus and Lampornis amethystinus. Asterisks indicate significance after post hoc mean comparisons
(**P=0.001, ***P=0.0001). The two hummingbird species differed significantly in number of visits to artificial flowers (legitimate visits F1,176=13.45, P<0.001, robbing visits F1,176=13.88,
P<0.001), but males and females did not differ from each other
(legitimate visits F1,176=0.85, P>0.05, robbing visits F1,176=0.80,
P>0.05). In all cases the species×sex interaction was not significant (legitimate visits F1,176=1.33, P>0.05; robbing visits
F1,176=0.25, P>0.05)
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Table 1 Results of three-way
ANOVAs of number of visits to
artificial flowers as a function
of hummingbird species, corolla
length, and flower angle for
legitimate visits and robbing
visits
Source
Legitimate visits
Hummingbird species
Corolla length
Flower angle
Hummingbird species×Corolla length
Hummingbird species×Flower angle
Corolla length×Flower angle
Hummingbird species×Corolla
length×Flower angle
Residual
Robbing visits
Hummingbird species
Corolla length
Flower angle
Hummingbird species×Corolla length
Hummingbird species×Flower angle
Corolla length×Flower angle
Hummingbird species×Corolla
length×Flower angle
Residual
Fig. 3a–c Variation in number
of visits to flowers of Salvia
mexicana, S. iodantha, and Ipomoea hederifolia by individuals
of C. thalassinus and L. amethystinus. Asterisks indicate
significance after one-way
ANOVAs (*P=0.01,
**P=0.001, ***P=0.0001).
No differences in the number
of visits between males and
fe-males were observed for
S. mexicana (Table 2). For
S. iodantha, males of L. amethystinus made significantly
more visits (mean±SE
1.52±0.05) to individual
flowers than females (mean±SE
1.34±0.04) (post hoc mean
contrasts, F=3.97, P<0.05).
Females of C. thalassinus
made more visits (mean±SE
1.63±0.07) to individual flowers than males (mean±SE
1.48±0.60), but this difference
was not significant (post hoc
mean contrasts, F=2.77,
P>0.05). In all cases, no differences between males and females were observed in I. hederifolia, and the species×sex interaction was not significant
(Table 2)
Sum of
squares
df
Mean
square
F
P
14.975
7.561
13.736
0.699
0.350
1.974
1.647
<0.001
<0.01
<0.001
NS
NS
NS
NS
22.130
60.380
5.297
30.151
0.443
1.176
0.128
<0.001
<0.001
<0.01
<0.001
NS
NS
NS
108.422
54.742
198.902
5.058
5.071
28.591
23.847
1
1
2
1
2
2
2
108.422
54.742
99.451
5.058
2.536
14.295
11.924
1216.360
168
7.240
45.371
123.791
21.719
61.816
1.817
4.822
0.527
1
1
2
1
2
2
2
45.371
123.791
10.860
61.816
0.908
2.411
0.263
344.435
168
2.050
268
Table 2 Results of two-way
ANOVAs of number of visits
by males and females of two
hummingbird species to flowers of Salvia mexicana,
S. iodantha and Ipomoea
hederifolia for number of legitimate visits, legitimate with
robbing visits, and robbing
visits only
Source
Sum of squares
df
Mean square
Legitimate visits
Salvia mexicana
Hummingbird species
Sex
Hummingbird species×Sex
Residual
10.454
0.100
0.253
1078.858
1
1
1
896
10.454
0.100
0.253
1.204
8.757
0.083
0.210
<0.01
NS
NS
Salvia iodantha
Hummingbird species
Sex
Hummingbird species×Sex
Residual
3.552
0.056
5.758
768.740
1
1
1
896
3.552
0.056
5.758
0.858
4.140
0.065
6.711
0.042
NS
<0.01
Ipomoea hederifolia
Hummingbird species
Sex
Hummingbird species×Sex
Residual
28.315
0.223
1.208
1127.582
1
1
1
671
28.315
0.233
1.028
1.680
16.849
0.133
0.719
<0.001
NS
NS
Legitimate with robbing visits
Ipomoea hederifolia
Hummingbird species
Sex
Hummingbird species×Sex
Residual
0.121
0.553
0.050
44.633
1
1
1
178
0.121
0.533
0.050
0.251
0.483
2.205
0.199
NS
NS
NS
Robbing visits only
Ipomoea hederifolia
Hummingbird species
Sex
Hummingbird species×Sex
Residual
1.263
0.211
0.211
22.386
1
1
1
35
1.263
0.211
0.211
0.640
1.975
0.330
0.330
NS
NS
NS
Foraging behavior on natural flowers
No nectar robbing was observed in S. mexicana and
S. iodantha. All flowers were legitimately visited at least
once by C. thalassinus and L. amethystinus. In S. mexicana, individuals of C. thalassinus made significantly
more legitimate visits on average than L. amethystinus
(Fig. 3). In S. iodantha, we observed a marginal difference between hummingbird species in the number of legitimate visits (Fig. 3, Table 2).
Nectar robbing was observed in I. hederifolia. Individuals of C. thalassinus actively pierced the base of the
flowers (21% of the flowers), with no apparent damage
to the ovaries but leaving a slit at the base of the flowers.
In contrast, individuals of L. amethystinus did not pierce
but probed at the base of the flowers. Although no apparent damage was left at the base of the flower or to
the ovaries, we interpreted this behavior as illegitimate,
facultative nectar robbing.
Nine flowers of Ipomoea hederifolia were not visited
(6 out of 450 presented to C. thalassinus and 3 out of
450 presented to L. amethystinus). Most flowers were
legitimately visited at least once by C. thalassinus and
L. amethystinus (64.4 and 83.7%, respectively), and the
remaining were legitimately visited but then robbed or
only robbed by C. thalassinus (25.1 and 9.5%, respectively), and legitimately visited but then probed at the
F
P
base or only probed at the base by L. amethystinus (14
and 2.3%, respectively). We then compared the number
of visits of both hummingbird species according to these
behavioral categories, separately. Individuals of L. amethystinus made more legitimate visits and legitimate
visits with robbing than C. thalassinus (Fig. 3), but the
number of robbing visits to flowers of I. hederifolia was
not statistically different between species (Fig. 3).
Pollinator effectiveness
In all cases, open pollination (unbagged flowers) resulted in a higher seed production than flowers legitimate
visits by either hummingbird species (Fig. 4). C. thalassinus was significantly more effective in pollinating
S. mexicana than L. amethystinus (F1,886=9.73, P<0.01).
Both hummingbird species were equally effective in pollinating S. iodantha (F1,887=0.61, P>0.05) and I. hederifolia (F1,662=0.753, P>0.05). The number of seeds
was not affected by the number of legitimate visits in
the Salvia species (S. mexicana F7, 886=0.56, P>0.05;
S. iodantha F6,887=0.381, P>0.05), but in I. hederifolia
the effectiveness of both hummingbird species significantly increased up to full seed set after two visits to a
flower (F1,662=101.24, P<0.001; Fig. 5). In Salvia spp,
the species×number of visits interactions were not signif-
269
Fig. 4 Variation in number of seeds produced by S. mexicana,
S. iodantha, and I. hederifolia under open conditions of pollination and after legitimate and illegitimate visitation by C. thalassinus and L. amethystinus. Asterisks indicate significance after post
hoc mean comparisons (***P=0.0001)
Fig. 5 Relationship between number of legitimate visits and number of seeds produced after hummingbird visitation. Numbers
above bars indicate flowers visited a given number of times.
Asterisks indicate significance after post-hoc mean comparisons
(*P=0.01, **P=0.001, ***P=0.0001)
icant (S. mexicana F5,886=1.87; P>0.05; S. iodantha
F1,887=0.18, P>0.05), but it was significant in I. hederifolia (F5,662=4.43, P<0.001).
significant differences between hummingbird species
(F1, 897 =11.22, P<0.001). That is, the number of legitimate visits affects seed production. In I. hederifolia, the
number of legitimate visits also affected seed production
(Table 3). Because the F-value for the hummingbird species×number of visits interaction was not significant, it
was removed from the model. After removing such an
effect, the F-value for hummingbird species was significant (F1, 673 =4.22, P<0.05).
Effect of number of legitimate visits on seed production
Variation in S. mexicana seed production was not
affected by the number of legitimate visits (Table 3).
There were no significant differences between species,
and the hummingbird species×number of visits interaction was significant (Table 3). Similar results were observed in S. iodantha, except that hummingbird species×number of visits interaction was not significant
(Table 3). We removed it from the model and found
Effect of number of robbing visits on seed production
As expected, nectar robbing was not observed in
short-tubed flowers (S. mexicana and S. iodantha), so
270
Table 3 Results of ANCOVAs for the regression of the mean
number of seeds against the number of visits by the two hummingbird species in flowers of S. mexicana, S. iodantha and I. hederifo-
lia. A low P-value for hummingbird species×number of visits interaction, indicates that the number of visits (covariate) was useful
in predicting seed production for legitimate visits and legitimate
with robbing visits
Source
Sum of squares
df
Legitimate visits
Salvia mexicana
Hummingbird species
Number of visits
Hummingbird species ×Number of visits
Residual
2.049
2.223
8.050
1443.305
1
1
1
896
2.049
2.233
8.050
1.611
1.272
1.386
4.997
NS
NS
<0.05
Salvia iodantha
Hummingbird species
Number of visits
Hummingbird species ×Number of visits
Residual
2.610
0.134
0.001
743.204
1
1
1
896
2.610
0.134
0.001
0.829
3.147
0.161
0.001
NS
NS
NS
Ipomoea hederifolia
Hummingbird species
Number of visits
Hummingbird species ×Number of visits
Residual
0.247
51.218
0.003
109.743
1
1
1
672
0.247
51.218
0.003
0.163
1.514
313.627
0.016
NS
<0.0001
NS
Legitimate with robbing visits
Ipomoea hederifolia
Hummingbird species
Number of visits
Hummingbird species ×Number of visits
Residual
0.000
6.648
0.435
29.586
1
1
1
174
0.000
6.648
0.435
0.170
0.000
39.096
2.556
NS
<0.0001
NS
they are not analyzed further. In contrast, some longtubed flowers of I. hederifolia were robbed after a
number of legitimate visits, and other flowers were
only robbed. We analyzed these two categories separately.
Flowers legitimately visited and then robbed by
C. thalassinus produced significantly fewer seeds than
those legitimately visited and then illegitimately probed
by L. amethystinus (Fig. 4). Results of ANCOVA
showed that seed production in I. hederifolia is also
affected by number of legitimate visits with robbing
(Table 3). After removing the non-significant hummingbird species×number of visits interaction, the F-value for
hummingbird species was significant (F1,175 =6.58,
P<0.05). Number of visits was useful in predicting seed
production (P<0.001). Flowers that were only robbed by
C. thalassinus produced almost no seeds and those only
probed at the base by L. amethystinus produced no seeds
(Fig. 4).
There was a statistical difference in seed production
between flowers legitimately visited by C. thalassinus,
and those legitimately visited and then robbed by the
same hummingbird species (one-way ANOVA,
F1,414=14.03, P<0.001), suggesting that robbing negatively affected seed set in this species (Fig. 4). In contrast, no differences in seed set were observed between
flowers legitimately visited by L. amethystinus and those
legitimately visited and then probed at the base by the
same hummingbird species (P>0.05; Fig. 4).
Mean square
F
P
Discussion
Pollinator effectiveness
Within hummingbird species, individuals visited flowers
legitimately and robbed, sometimes simultaneously, and
in other cases as separate activities. Nectar robbers are
generally assumed not to pollinate (Inouye 1983); however, we have shown that pollination effectiveness depends on corolla length, frequency, and mode of nectar
robbing.
Reduced seed set in flowers of all three species compared to those under open conditions of pollination may
be because flowers were excluded from other more
effective pollinators (Arizmendi 1994) than the ones we
studied, and/or received fewer visits. There are three
possible explanations for the increase in seed production
of I. hederifolia with the number of visits: (1) hummingbirds used in this comparative study transfer and deposit
pollen loads inefficiently, (2) the plant is resource and/or
pollen limited, and/or (3) the plant is obligately outcrossed. Although our study was not designed to distinguish among these non-mutually exclusive explanations,
the among-plant variation we found in the number of
seeds produced by each flower depending on the number
of visits and the pollinator (Fig. 5), suggests that the
number and origin of pollen grains deposited on the stigma may play an important role in determining seed set.
The differences in the number of times a hummingbird
271
visits a given flower means that bill and floral morphological attributes can not solely account for the variation
we observed on I. hederifolia reproductive success, but
that flowers need more than one visit to reach full seed
set. On the other hand, differences between Salvia
species in seed set can be solely interpreted in terms of
differences in pollinator effectiveness (morphological
mismatch between hummingbird beaks and flowers).
Although we cannot distinguish between those seeds
sired as a result of hummingbird visitation from those
that resulted by selfing (Salvia flowers visited only once
produced the same number of seeds as those visited
more times), it seems that individuals of C. thalassinus
are more effective pollinators of S. mexicana flowers and
those of L. amethystinus are more effective pollinators of
S. iodantha and I. hederifolia flowers. Nevertheless, pollinator effectiveness was diminished by the intensity and
the mode of nectar robbing by C. thalassinus because
I. hederifolia flowers produced fewer seeds when legitimately visited and then robbed or only robbed, than
those that were only legitimately visited (Fig. 4). Robbing of Ipomoea by Colibri yields some seeds, but
robbing by Lampornis did not. Also, the fact that Lampornis robbing yields zero seed set whereas legitimate
visits yields seed set is evidence for a cost of robbing in
this species. It is possible that Colibri does some pollination during what looks like an illegitimate visit, that is,
by piercing the corolla some pollen grains dropped onto
the stigma.
Studies looking at the negative effect of nectar robbers on seed set have shown contradictory results (see
Maloof and Inouye 2000 for a review). The assumption
that nectar robbing carries both male and female fitness
costs to plants is based on the correlative evidence that
robbed flowers have fewer seeds than flowers visited
legitimately (Roubik et al. 1985; Reddy et al. 1992; Irwin and Brody 1998, 1999; Traveset et al. 1998; Navarro
1999; this study). In nature, however, robbed flowers
might receive further visits that were legitimate, even
when flowers were emptied of nectar by robbers, and
therefore one legitimate visit might suffice to produce
the full seed set. In contrast, robbed flowers would set
fewer or no seeds if long-billed hummingbirds were less
efficient in pollinating or avoided them because they are
empty of nectar (less attractive) than those non-robbed
flowers (see also Irwin and Brody 1998, 1999). There is
some evidence that hummingbirds discriminate against
robbed flowers (Gass and Montgomerie 1981; Irwin and
Brody 1998), but whether legitimate pollinators are less
efficient with robbed flowers remains to be investigated.
Flowers that receive further legitimate visits after robbing might have a real fitness cost when nectar taken by
the robbers is replaced by additional secretion. New
nectar production may impose a high cost on the plant
(Southwick 1984; Pyke 1991). Navarro (1999) showed
that flowers of Macleania bullata (Ericaceae) produced
more nectar as a consequence of nectar robbing by shortbilled hummingbirds. This additional nectar secretion
entailed an energetic cost that reduced fruit set.
The effects of corolla length
Legitimate pollinators may select for long corollas and
colors (and other floral traits), but the role of nectar robbers as agents of selection on flower morphology has
mostly been ignored (Maloof and Inouye 2000). Robbing
may represent a counter selective force that counter balance selection for longer corollas by specialist pollinators. Some floral traits, including variation in corolla
length among populations (Waser 1979; Roubik et al.
1985), flower location (Colwell et al. 1974; Traveset
et al. 1998; Arizmendi et al. 1996), and high rates of nectar production (Pyke 1981; Navarro 1999), may be the
consequence of nectar robbing. Floral characters such as
corolla length, curvature, and flower angle vary considerably among hummingbird-pollinated plants, and this affects foraging efficiency of the birds. It has been shown
that hummingbirds take more time to extract nectar
from long-tubed flowers than from short-tubed flowers
(e.g., Hainsworth 1973; Hainsworth and Wolf 1976;
Montgomerie 1984; Hainsworth et al. 1983). Earlier studies have compared foraging behavior of hummingbird
species that differed in bill lengths (Wolf et al. 1972;
Hainsworth 1973; Hainsworth and Wolf 1976; Ewald and
Williams 1982; Montgomerie 1984; Temeles and Roberts
1993; Temeles 1996), and have shown that birds with
longer bills have greater maximum extraction depths and
faster handling times at relatively long flowers than birds
with shorter bills. We were unable to quantify handling
times and nectar volume extracted by the birds; however,
our experimental approach showed that short-billed hummingbirds used nectar robbing as an alternative to forage
from long-tubed flowers. We found that the longer of the
three species (Ipomoea) (and the longer of the artificial
flowers) receive illegitimate probes, as has been commonly observed in nature (e.g., Grant 1952; Skutch 1954;
Colwell et al. 1974; Kodric-Brown and Brown 1979;
Stiles 1981; Inouye 1983; Kodric-Brown et al. 1984;
Feinsinger et al. 1987; Ornelas 1994; Navarro 1999).
Although flower angle may also play an important role
in explaining flower-handling variation (Montgomerie
1984), our results for nectar robbing on long-tubed flowers were not confounded by this factor by design. In
short, we have shown that facultative robbing behavior in
both hummingbird species is most likely if corollas are
longer. This suggests that selection will not unilaterally
favor longer corollas – facultative (and obligate) robbers
may select in the opposite direction from non-robbers,
that is, robbers may select for shorter corollas. However,
a formal demonstration of such selection would require
establishment of a relationship between corolla length
and seed set within a plant species and show that this is
related to robbing.
Nectar robbing among short-billed hummingbirds
We found significant variation between hummingbird
species in use of robbing behavior. It is possible that the
272
variation among individuals in nectar robbing is a result
of their previous foraging experience. A higher incidence
of illegitimate feeding by males has been observed as a
result of their having shorter bills (Bertin 1982; Temeles
and Roberts 1993). However, we found that males and
females for either hummingbird species in I. hederifolia
used legitimate and robbing behaviors similarly, although both species are sexually dimorphic in bill length
(Ornelas 1995). Here, we have documented that individuals of both species of hummingbirds are indeed facultative in robbing behavior, and that this presumably opportunistic behavior of C. thalassinus, which has a serrated
bill, negatively affected seed production of long corollas.
Additional research is needed to determine whether
nectar robbing is most likely to evolve among shortbilled hummingbirds (Ornelas 1994).
Because we found no visible evidence of physical
damage to the ovaries and corolla tubes of the examined
flowers, we think that the decreased fertility of flowers
robbed by both hummingbird species may be due to effects on pollinator visitation, rather than to destruction of
plant reproductive parts (see also Irwin and Brody 1999).
However, individuals of C. thalassinus with enlarged
tomial serrations had the highest negative effect on I. hederifolia seed production. Further studies should explore
the role bill serrations play in perforating and handling
long-tubed flowers. If the function of bill serrations were
to hold the flowers in some fashion and then rob them,
one would expect the act of legimate visitation and flower piercing to be somewhat slower than that of nectar
robbery. A high-speed video analysis would show
whether the flowers are stabbed, grasped, and/or sawed,
and one could compare floral handling (e.g., foraging
time) between nectar robbers with bill serrations and
nectar thieves with smooth bills.
In conclusion, we have shown that both of the two
species of hummingbirds are more likely to rob artificial
flowers with long rather than short corollas. Furthermore, the hummingbird with the shorter bill was more
likely to rob than the species with the longer bill. In the
field, only the plant species with a long corolla experienced nectar robbing, and this had a negative impact on
seed set. Our experimental results suggest that nectar
robbing may favor short corollas.
Acknowledgements Comments by María del Coro Arizmendi,
William A. Calder, Phyllis D. Coley, Barbara Ditsch, Astrid Eben,
Theodore H. Fleming, Myriam Mermoz, Jorge López Portillo,
Joan E. Maloof, Carlos Martínez del Rio, Victor Rico-Gray, Nick
Waser and three anonymous reviewers greatly improved an earlier
draft of this paper. We also thank R. Iorente Adame, C. Ortíz
Arrona, G. Zavala, J. Sandoval, and L.I. Iñiguez for their help during fieldwork, and the staff of Las Joyas field station for the facilities to conduct our research. This research was supported by a
doctoral scholarship (No. 56254) from the Consejo Nacional de
Ciencia y Tecnología (CONACyT) and the James R. Silliman
Memorial Research Grant to J.F.O.
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