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Salisbury University, Department of Biological Sciences, Salisbury, Maryland 21801 USA and Rocky Mountain Biological Laboratory, Crested Butte, Colorado 81224 USA
Received for publication January 2, 2001. Accepted for publication May 25, 2001.
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ABSTRACT |
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Key Words: Bombus • community ecology • Corydalis • flight distances • nectar robbing • outcrossing • robbers
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INTRODUCTION |
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.
However, researchers who closely examined the effects of nectar
robbers often found that the robbers were behaving as pollinators by
moving pollen onto the stigma as a result of their movements during
pollen or nectar gathering (Koeman-Kwak, 1973
;
Waser, 1979
;
Higashi et al., 1988
;
Guitán, Guitán, and Navarro, 1993
;
Guitán, Sánchez, and Guitán, 1994
;
Navarro, 2000
). A
new terminology has developed to describe animals that behave in this
way: robberlike pollinators (Higashi et al., 1988
).
These robberlike pollinators often have positive effects on the
reproductive success of the plants they visit.
In addition to enhancing reproductive success directly through
pollination, robbers may also influence reproductive success
indirectly by causing changes in the behavior of the legitimate
pollinators either through scent marking, changes in nectar
volume, or both. Reduced nectar volume has been shown to cause
bumble bees to increase interplant flight distances (Heinrich,
1983
;
Zimmerman and Cook, 1985
) and
to visit fewer flowers on the same inflorescence (Pyke, 1982
;
Heinrich, 1983
;
Hodges, 1985
;
Johnson and Nilsson, 1999
).
Both of these behaviors can reduce geitonogamy (the fertilization of
flowers by pollen from other flowers on the same plant), increase
pollen flow distances, and thereby increase outcrossing rates (see de
Jong, Waser, and Klinkhamer, 1993
;
Barrett and Harder, 1996
).
Higher rates of outcrossing often lead to increased seed set and
improved survival rates of seedlings (e.g., Charlesworth and
Charlesworth, 1987
;
Fenster, 1991
).
It seems likely then that robbers, by reducing nectar volume,
might change pollinator behavior and consequently affect pollen
transfer. Holsinger (1996)
states
that "identifying the factors that affect the patterns of pollen
transfer should probably be the overriding goal of future empirical
research in pollination and mating system biology." But to date, only
two studies have attempted to measure the effects of robbers on
pollinator foraging behavior (Zimmerman and Cook, 1985
;
Irwin and Brody, 1998
). Zimmerman and Cook (1985)
artificially robbed flowers of Impatiens capensis by
making a hole in the spur of the corolla and removing nectar with a
syringe. The authors concluded that "the presence of nectar-robbers
in the system does not alter the general pollination behavior, but it
does induce foragers to fly longer distances thus further promoting
outcrossing." Irwin and Brody (1998)
artificially robbed experimental arrays of Ipomopsis
aggregata. They found that the legitimate pollinator, a
hummingbird, visited fewer plants and fewer flowers per plant in the
heavily robbed arrays, thus decreasing fruit set and seed set and
having a negative effect on plant fitness.
In both of these studies, the flowers were "artificially" robbed,
meaning that humans mimicked the actions of real nectar robbers
by cutting holes in the flowers and extracting nectar. Evidence
is accumulating, however, that bumble bees (one of the most
prevalent nectar robbers, and the robbers in both of these systems)
may scent-mark flowers while foraging and detect the scent-markings
of previous visitors (see Goulson, Hawson, and Stout, 1998
). In a number of instances these scent markings have been
shown to change the behavior of foraging bumble bees (Schmitt
and Bertsch, 1990
;
Goulson, Hawson, and Stout, 1998
;
Williams, 1998
). In one study the bumble bees were apparently able to
discern scents created by human fingerprints on floral surfaces
(Marden, 1984
).
Therefore, if we wish to examine the effect of bumble bee nectar
robbers on legitimate pollinators, we should consider the possibility
that scent marking plays a role in this interaction and design our
experiments accordingly.
In this study I have examined the interactions among a plant species (Corydalis caseana subsp. brandegei), its nectar robber (a bumble bee, Bombus occidentalis), and its pollinator (a bumble bee, Bombus appositus). Specifically I have addressed the following questions: (1) At what age are the flowers generally robbed? (2) Is there a difference in fruit set or seed set between the robbed and the unrobbed flowers? (3) Do robbers pollinate the flowers they visit? (4) How much nectar is removed by the robbers? (5) Do robbers change the behavior of the legitimate pollinators by changing the number of bees attracted, the number of inflorescences visited per bee, the number of flowers visited per inflorescence, or the flight distances between inflorescences?
To allow for the possibility that scent marking plays some role in the effect of nectar robbers, all robbing in this study was done by Bombus occidentalis, the natural robber of the plant species. This study represents the first time the effect of nectar robbers on the behavior of the legitimate pollinator has been tested experimentally using real nectar robbers.
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MATERIALS AND METHODS |
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).
Young plants have only a single stem, but older plants (>7 yr)
have numerous stems (2–25) arising from a single large root. Each
mature stem is topped by a terminal racemose inflorescence bearing up
to 70 flowers; stems also have numerous side inflorescences with 5–40
flowers each. It was sometimes difficult, without digging up the
plants, to determine if stems in close proximity were from the same,
or different, individuals. For that reason, the behavioral
studies were done at the level of the inflorescence.
The flower (Fig. 1) has a
long nectar spur (12–16 mm; Ownbey, 1947
), and
only long-tongued visitors, such as Bombus appositus, can
reach the nectar through the front. Short-tongued, nectar-robbing
bumble bees bite holes in the spur-shaped petal to reach the nectar.
In the absence of visitors, nectar, with an average sugar
concentration of 35%, accumulates in the flowers at a rate of  1960_files/sim.gif){kind=small}
1 µL per
day. Flowers remain in good condition for 4 d before they begin to
wilt. Corydalis caseana is self-compatible, yet it is
dependent upon insect visitors for pollination. When compared with
open-pollinated and outcross-pollinated flowers, self-pollinated
flowers produced fewer fruits, fewer seeds per fruit, and smaller
seeds, suggesting lower fitness due to inbreeding depression. (For
additional information on the distribution and reproductive biology
of C. caseana see Maloof, 2000b
.)
|
Pollination study
The aim of this study was to determine
if B. occidentalis robbers pollinate C. caseana.
Monospecific patches of C. caseana plants were temporarily
enclosed in tents 3.9 m wide x 2.7 m deep
x 2 m high. The walls of the tents
were made of fine mesh and the roofs were made of opaque
polyethylene. The tents prevented legitimate pollinators from gaining
access to the experimental plants and kept robbers contained inside
with the plants during the experimental treatments. Commercially
raised colonies of Bombus occidentalis robbers were used in
these studies (suppliers: 1997, Bees West, Freedom, California, USA;
1998, Koppert Biological Systems, Romulus, Michigan, USA). Each
colony contained 80 bees.
Commercially supplied pollen pellets were freely administered
to the colonies, but no supplemental nectar was available to
them during the course of the experiments. Prior to the initiation
of the experiments, the bees were allowed to forage freely in
enclosures for a few hours a day. This "training period" gave
the bees an opportunity to learn how to collect nectar from
C. caseana by robbing. None of the bees foraged legitimately
or collected pollen from the flowers. After 1 wk, all foraging
workers were robbing nectar from flowers. Thus, the foraging
behavior of the commercial bees was the same as the behavior of
the naturally occurring B. occidentalis.
After foraging, whether for training or experimental purposes, the bees were returned to the colony box by adjusting the nest entrance so that returning bees could enter but not leave and by capturing any remaining foragers in plastic vials and returning them to the nest.
For this experiment, eight inflorescences in each tent (experimental and control) were protected with netting while the flowers were still in bud. When the inflorescences were in peak bloom, the netting was removed and the pedicels of all open flowers on the test inflorescences were marked with permanent ink. (Pilot studies showed that fruits and seeds developed normally when the pedicels were marked in this way.) Immediately after marking, the colony of robbers was allowed to forage for 4 h inside the experimental tent. No robbers were released into the control tent. After 4 h the bees were removed from the experimental tent and the open and robbed flowers on each inflorescence were counted. The inflorescences were rebagged and checked for fruit set after 16 d.
The experiment was repeated four times (17, 19, 21, and 23 July)
in a crossover design that alternated the experimental (with
robbers) treatment and the control (without robbers) treatment.
Previous research had shown that C. caseana would not set
fruit if all visitors were excluded (Maloof, 2000a)
;
therefore, fruit set in the experimental inflorescences would
indicate pollination by the robbers.
Nectar removal
To determine how much nectar a robber
removes from a filled flower, a tent protected plants from visitors
for 4 d. On the fifth day (16 July 1997) the robbers were allowed to
forage in the tent. When a flower was robbed, it was collected,
along with an adjacent (same-age) unvisited flower from the same
inflorescence. The nectar volume in both flowers was measured
immediately by using a 10-µL microcapillary tube to extract the
nectar and a digital micrometer (Mitutoyo, Utsunomiya-shi, Japan)
to measure the filled length of the tube. Length measurements
were converted to volume.
Effect on pollinator behavior
To determine if B.
occidentalis robbers changed the behavior of B. appositus
(the legitimate pollinator) a pair of tents was erected a minimum of
5 m apart over a naturally occurring C. caseana patch. I
attempted to match the densities of the inflorescences in both tents.
Tents were left in place for 3–4 d. On the morning of the experiment,
a colony of B. occidentalis was allowed to forage freely in
one of the tents. All foragers collected nectar by robbing. After 4
h, the colony was removed from the tent. Immediately following the
removal of the robber, the footprints of the tents were outlined
using plastic tagging tape and the tents were removed. To avoid
disturbing any possible scent marks, flowers were not handled. Three
researchers were stationed by each outlined patch. Both patches were
observed simultaneously by the three-person teams. When a B.
appositus (pollinator) bee entered the patch it was identified
and its movements were followed. Observers noted the number of
flowers visited on an inflorescence and the distance flown to the
next inflorescence. Distances were estimated visually to the
nearest cm with the assistance of a meter rule. Bees were followed
until they flew out of the patch. If the distance of the final
flight, which took the bee out of the patch, could be determined,
that flight distance was recorded as well. It was rare for
visitors besides B. appositus to enter the patch, but if they
did, they were brushed out. The experiment could not be conducted as
a blind test, because robbing holes in the flowers were evident
to the observers. After 1 h, the observers exchanged patches in
order to eliminate any bias in estimation and continued observations
for a second hour. This process was repeated on 20, 23, and 27
July 1998 with the tents in a new location for each trial.
Data analysis
To eliminate differences in fruit set or
seed set that could be caused by genetic and/or environmental
factors, the fate of robbed and unrobbed flowers on the same
inflorescence were compared by paired t test. Nectar volumes
from robbed and unrobbed flowers on the same inflorescence were also
compared by paired t test.
To determine if there was any relationship between the initial nectar volume and the amount of nectar removed, the volumes removed from the robbed flowers (determined by subtracting the nectar volume remaining in the robbed flower from the nectar volume in its unrobbed counterpart) were compared with the nectar volumes in unrobbed flowers by linear regression.
Pollinator behavior was analyzed on a per bee basis. Because
marking the bees could interfere with their normal behavior, I
did not mark them. Consequently, it is possible that a bee could have
left the plot and then reentered at a later time without being
recognized as a previous visitor. The number of inflorescences
visited per bee, the number of flowers visited per inflorescence per
bee, and the distance flown between inflorescences were compared for
the two treatments (robbed and unrobbed; treatment = fixed, date =
random) by the General Linear Method procedure in SPSS 8.0 (Norusis,
1998
).
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RESULTS |
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Nectar removal
As expected, robbers reduced the
availability of nectar in C. caseana (P < 0.0005; Fig. 4). The
unrobbed flowers contained a mean (± 2 SE) nectar volume of 4.8 µL
(±1.74, N = 28), and the robbed flowers contained a mean
nectar volume of 1.0 µL (±0.74, N = 28). It is important to
note, however, that these observations were made on flowers
previously protected from visitors. The natural standing crop nectar
values were lower (e.g., 0.60 ± 0.73 µL, mean ± SD;
Maloof, 2000b)
, and
it has not been determined exactly how robbers influence nectar
volume or variation in the flowers under open field conditions. In
the previously protected flowers of this experiment, not all the
nectar was drained by the robbers. In the 28 pairs of flowers tested
(assuming that the robbed flowers began with a nectar level similar
to the unrobbed flowers) the robbers removed an average of 79.7% of
the available nectar, leaving behind a mean of 1 µL of nectar. There
was a significant relationship between the amount of nectar in the
unrobbed flowers and the amount of nectar presumably removed from the
robbed flowers (F1, 27 = 134.8, P <
0.0005, r 2 = 0.838; nectar removed = 0.37 + 0.72
original nectar in flower). In other words, the robbers did not
remove a fixed volume of nectar; the more nectar that was contained
in a flower, the more nectar they removed, though still leaving
behind an average of 20% of the original nectar volume.
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DISCUSSION |
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The natural place to look for effects is in fruit set and seed
set. Darwin (1872)
assumed that robbers had negative fitness effects, but in a
recent survey (Maloof and Inouye, 2000)
robbers were equally as likely to have positive or neutral
effects, as they were to have negative effects. In this study I
have found that the robber has no discernable negative effect on
fruit set or seed set.
In other studies, where robbers had positive effects on reproductive
success (Koeman-Kwak, 1973
;
Waser, 1979
;
Higashi et al., 1988
;
Guitián, Sánchez, and Guitán, 1994
;
Navarro, 2000
), the
robbers were pollinating in the process of nectar robbing. In this
study, I have determined that the robbers do not pollinate C.
caseana. This result was somewhat surprising because earlier
experiments showed that C. caseana is self-compatible, with no
spatial or temporal separation of male and female function (Maloof,
2000a)
. I
suspected that the activity of the robbers would result in
fertilization, as in Corydalis ambigua (Higashi et al., 1988
), but
experiments proved that this was not so. To my knowledge this is the
first study in which a controlled experiment showed that the robbers
were not pollinating. More studies of this type would greatly aid our
understanding of robbers.
Although the robbers removed a substantial proportion of the nectar from the previously protected flowers, it is noteworthy that in most cases some nectar was left in the flowers. Additional studies should be done comparing nectar volumes and variance for naturally occurring (unprotected) robbed and unrobbed flowers. In a study on Impatiens capensis the standing crop of nectar in robbed flowers was lower than the standing crop of nectar in unrobbed flowers, because robbers could reach more of the nectar (H. Young, Middlebury College, personal communication).
Corydalis caseana requires a pollinator visit for reproduction
(Maloof, 2000a)
, and
the consistently high rate of fruit set in my study plots between
1996 and 1999 (>80%), despite robbing rates of 39–87% (Maloof,
2000b
, and
unpublished data), indicates that nectar removal by robbers may not
be consequential enough to cause the legitimate pollinators to switch
their foraging to another species. Also, complex flowers, such as
C. caseana, take longer for pollinators to learn how to handle
and bees are more likely to be constant to complex flowers once
they have learned to handle them (Laverty, 1994
).
Similarly, Stout, Allen, and Goulson (2000)
found
that despite nectar robbing levels of 96%, the pollinator bumble bees
continued visiting the complex flowered species they studied,
Linaria vulgaris.
The tent studies showed that pollinating bumble bees did not avoid
the experimental robbed plots by comparing pollinator visitation to
these plots to visitation within the experimental unrobbed plots.
This indicates that the bees either cannot tell from a distance which
flowers are robbed or that they do not discriminate between robbed
and unrobbed flowers. Stout, Allen, and Goulson (2000)
also
observed no discrimination by bumble bee pollinators between robbed
and unrobbed flowers. In both their study and this study, there was
no difference in seed set between robbed and unrobbed flowers, most
likely because of equal pollinator visitation to robbed and unrobbed
flowers. Similarly, Rust (1979)
and
Hodges (1995)
found
that manipulating the nectar volume did not change the number of
pollinators arriving at plants. Hummingbird pollinators, however, may
avoid robbed flowers (Irwin and Brody, 1998
).
Measuring avoidance, or its contrary, attraction, is important
because if pollinators avoid robbed flowers, then robbers would have
negative fitness effects on plants, albeit indirectly.
Once the pollinators (B. appositus) are in the experimentally
robbed plot, one would expect them to visit fewer flowers on an
inflorescence and fewer inflorescences before moving out. Although
these are the responses produced by lowered nectar levels in other
studies (see Kadmon and Shmida, 1992
;
Johnson and Nilsson, 1999
), the
pollinators in this study did not show those behaviors: they visited
similar numbers of flowers per inflorescence and a similar number of
inflorescences before they left the experimental robbed plot. The one
difference I did detect between the robbed plots and the unrobbed
plots was that B. appositus tended to fly longer distances
between foraging bouts in the robbed plots. A pollinator flying
longer distances between visits to the same plant species when total
visit numbers are not reduced might have positive effects on the
fitness of the plant through increased pollen flow distances. In
previous studies on C. caseana, outcross-pollinated flowers
produced more fruits and more seeds than self-pollinated flowers
(Maloof, 2000a)
. In
plants with numerous stems and numerous inflorescences, such as C.
caseana, longer flight distances could minimize the possibility
of geitonogamy and the resulting effects of inbreeding.
Both the bumble bee nectar robber and the bumble bee pollinator
are necessary for the indirect positive fitness effect of increased
outcross pollination due to longer flight distances. Flowers
visited by both robbing and nonrobbing bumble bees are not uncommon.
Willis and Burkill (1903)
mention this combination of visitors on Arctostaphylos
uva-ursi, Erica cinerea, Vicia sepium, and Oxytropis
campestris. A number of species in the vicinity of the Rocky
Mountain Biological Laboratory are also visited by both robbing
bumble bees and nonrobbing bumble bees: Delphinium nuttallianum,
D. barbeyi, Aconitum columbianum, Mertensia ciliata, Lathyrus
leucanthus (D. Inouye, University of Maryland, personal
communication) and Linaria vulgaris (personal observation).
Further research is needed to determine if longer flight distances
by the pollinators, such as those found in this study, are a
typical result of these three-species interactions.
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FOOTNOTES |
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Funding was provided by Earthwatch and its Research Corps, and an
NSF Research Training Grant in the Biology of Small Populations,
DBI-9602266.  1960_files/back.gif){kind=small}
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LITERATURE CITED |
|---|
| TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE
CITED |
|---|
Charlesworth D., B. Charlesworth, 1987 Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-237[ISI]
Colorado Natural Heritage Program. 1996 Colorado's natural heritage: rare and imperiled animals, plants, and natural communities. 2: 42
Darwin C., 1872 The effects of cross and self fertilisation in the vegetable kingdom. Murray, London, UK
de Jong T. J., N. M. Waser, P. G. L. Klinkhamer, 1993 Geitonogamy: the neglected side of selfing. Trends in Ecology and Evolution 8: 321-321
Fenster C. B., 1991 Gene flow in Chamaecrista fasciculata (Leguminosae). Evolution 45: 398-398[ISI]
Goulson D., S. A. Hawson, J. C. Stout, 1998 Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Animal Behaviour 55: 199-199[ISI][Medline]
Guitián J., J. M. Sánchez, P. Guitián, 1994 Pollination ecology of Petrocoptis grandiflora Rothm. (Caryophyllaceae); a species endemic to the north-west part of the Iberian Peninsula. Botanical Journal of the Linnean Society 115: 19-19[ISI]
Guitián P., J. Guitián, L. Navarro, 1993 Pollen transfer and diurnal versus nocturnal pollination in Lonicera etrusca. Acta Oecologica 14: 219-219[ISI]
Heinrich B., 1983 Insect foraging energetics. In C. E. Jones and R. J. Little [eds.], Handbook of experimental pollination biology, 187–214. Van Nostrand Reinhold, New York, New York, USA
Higashi S., M. Ohara, H. Arai, K. Matsuo, 1988 Robber-like pollinators: overwintered queen bumblebees foraging on Corydalis ambigua. Ecological Entomology 13: 411-411[ISI]
Hodges C. M., 1985 Bumble bee foraging: the threshold departure rule. Ecology 66: 179-179[ISI]
Hodges S. A., 1995 The influence of nectar production on hawkmoth behavior, self pollination, and seed production in Mirabilis multiflora (Nyctaginaceae). American Journal of Botany 82: 197-197[ISI]
Holsinger K. E., 1996 Pollination biology and the evolution of mating systems in flowering plants. Evolutionary Biology 29: 107-107[ISI]
Irwin R. E., A. K. Brody, 1998 Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116: 519-519[ISI]
Johnson S. D., L. A. Nilsson, 1999 Pollen carryover, geitonogamy, and the evolution of deceptive pollination systems in orchids. Ecology 80: 2607-2607[ISI]
Kadmon R., A. Shmida, 1992 Departure rules used by bees foraging for nectar: a field test. Evolutionary Ecology 6: 142-142[ISI]
Koeman-Kwak M., 1973 The pollination of Pedicularis palustris by nectar thieves (short-tongued bumblebees). Acta Botanica Neerlandica 22: 608-608[ISI]
Laverty T. M., 1994 Bumble bee learning and flower morphology. Animal Behaviour 47: 531-531[ISI]
Maloof J. E., 2000a Reproductive biology of a North American subalpine plant: Corydalis caseana A. Gray ssp. brandegei (S. Watson) G. B. Ownbey. Plant Species Biology 15: 281-281
Maloof J. E., 2000b The ecological effects of nectar robbers, with an emphasis on the reproductive biology of Corydalis caseana. Ph.D. dissertation, University of Maryland, College Park, Maryland, USA
Maloof J. E., D. W. Inouye, 2000 Are nectar robbers cheaters or mutualists?. Ecology 81: 2651-2651[ISI]
Marden J. H., 1984 Remote perception of floral nectar by bumblebees. Oecologia 64: 232-232[ISI]
Navarro L., 2000 Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators. American Journal of Botany 87: 980-980[Abstract/Full Text]
Norusis M. J., 1998 SPSS advanced statistics 8.0. SPSS, Chicago, Illinois, USA
Ownbey G. B., 1947 Monograph of the North American species of Corydalis. Annals of the Missouri Botanical Garden 34: 187-187
Pyke G. H., 1982 Foraging in bumblebees: rule of departure from an inflorescence. Canadian Journal of Zoology 60: 417-417[ISI]
Rust R., 1979 Pollination of Impatiens capensis: pollinators and nectar robbers. Journal of the Kansas Entomological Society 52: 297-297
Schmitt U., A. Bertsch, 1990 Do foraging bumblebees scent-mark food sources and does it matter?. Oecologia 82: 137-137[ISI]
Stout J. C., J. A. Allen, D. Goulson, 2000 Nectar robbing, forager efficiency and seed set: bumblebees foraging on the self incompatible plant Linaria vulgaris (Scrophulariaceae). Oecologia 21: 277-277
Waser N. M., 1979 Pollinator availability as a determinant of flowering time in ocotillo (Fouquieria splendens). Oecologia 39: 107-107[ISI]
Williams C. S., 1998 The identity of the previous visitor influences flower rejection by nectar-collecting bees. Animal Behaviour 56: 673-673[ISI][Medline]
Willis J. C., I. H. Burkill, 1903 Flowers and insects in Great Britain. III. Annals of Botany 17: 539-539[ISI]
Zimmerman M., S. Cook, 1985 Pollinator foraging, experimental nectar-robbing and plant fitness in Impatiens capensis. American Midland Naturalist 113: 84-84[ISI]
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= 7/20/98;
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= 7/23/98;
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= 7/27/98.
The closed symbol ( 1960_files/diams.gif){kind=small}
)
represents the mean of the means for all bees over all trials. (A)
Total bees attracted. (B) Mean number of inflorescences visited per
bee in each plot (no significant difference). (C) Mean number of
flowers visited per bee per inflorescence (no significant
difference). (D) Mean flight distance per bee (differences are
significant, GLM; N = 75, P = 0.021)