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Comparative Efficiency of Nannotrigona perilampoides, Bombus impatiens (Hymenoptera: Apoidea), and Mechanical Vibration on Fruit Production of Enclosed Habanero Pepper

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Abstract

The native bee Nannotrigona perilampoides Cresson (Apidae: Meliponini) has been evaluated with promising results in greenhouse pollination of Solanaceae in Mexico. However, no comparison has been done with imported bumble bees (Apidae: Bombini), which are the most common bees used for greenhouse pollination. We compared the foraging activity and fruit production of habanero pepper. Capsicum chinense Jacquin, by using N. perilampoides and Bombus impatiens Cresson in pollination cages. Both bee species collected pollen on a similar number of ßowers per unit time, but N. perilampoides visited signiÞcantly more ßowers per trip, lasted longer on each ßower, and spent more time per foraging trip. Ambient temperature and light intensity signiÞcantly affected the foraging activity of N. perilampoides. Light intensity was the only environmental variable that affected B. impatiens. Except for the fruit set, there were not signiÞcant differences in the quality of fruit produced by both bee species; however, N. perilampoides and B. impatiens performed better than mechanical vibration for all the variables measured. The abortion of fruit caused the low fruit set produced by B. impatiens, and we speculate it might be due to an excessive visitation rate. Pollination efÞciency per visit (SpearÕs pollination efÞciency index) was similar for both bee species in spite of the signiÞcantly lower amount of pollen removed by N. perilampoides. We suggested that the highest number of ßowers visited per foraging trip coupled with adequate amounts of pollen transported, and transferred between ßowers, could explain the performance of N. perilampoides as a good pollinator of habanero pepper. Our experiments conÞrm that N. perilampoides could be used as an alternative pollinator to Bombus in hot pepper under tropical climates.
HORTICULTURAL ENTOMOLOGY
Comparative Efficiency of Nannotrigona perilampoides,Bombus impatiens
(Hymenoptera: Apoidea), and Mechanical Vibration on Fruit Production
of Enclosed Habanero Pepper
GERARDO PALMA,
1
JOSE
´JAVIER G. QUEZADA-EUA
´N,
1,2
VIRGINIA MELE
´NDEZ-RAMIREZ,
1
JAVIER IRIGOYEN,
1
GUSTAVO R. VALDOVINOS-NUN
˜EZ,
3
AND MANUEL REJO
´N
1
J. Econ. Entomol. 101(1): 132Ð138 (2008)
ABSTRACT The native bee Nannotrigona perilampoides Cresson (Apidae: Meliponini) has been
evaluated with promising results in greenhouse pollination of Solanaceae in Mexico. However, no
comparison has been done with imported bumble bees (Apidae: Bombini), which are the most
common bees used for greenhouse pollination. We compared the foraging activity and fruit production
of habanero pepper. Capsicum chinense Jacquin, by using N.perilampoides and Bombus impatiens
Cresson in pollination cages. Both bee species collected pollen on a similar number of ßowers per unit
time, but N.perilampoides visited signiÞcantly more ßowers per trip, lasted longer on each ßower, and
spent more time per foraging trip. Ambient temperature and light intensity signiÞcantly affected the
foraging activity of N.perilampoides. Light intensity was the only environmental variable that affected
B.impatiens. Except for the fruit set, there were not signiÞcant differences in the quality of fruit
produced by both bee species; however, N.perilampoides and B.impatiens performed better than
mechanical vibration for all the variables measured. The abortion of fruit caused the low fruit set
produced by B.impatiens, and we speculate it might be due to an excessive visitation rate. Pollination
efÞciency per visit (SpearÕs pollination efÞciency index) was similar for both bee species in spite of
the signiÞcantly lower amount of pollen removed by N.perilampoides. We suggested that the highest
number of ßowers visited per foraging trip coupled with adequate amounts of pollen transported, and
transferred between ßowers, could explain the performance of N.perilampoides as a good pollinator
of habanero pepper. Our experiments conÞrm that N.perilampoides could be used as an alternative
pollinator to Bombus in hot pepper under tropical climates.
KEY WORDS crop pollination, bees, greenhouse, Yucata´n
Bombus impatiens Cresson (Apidae: Bombini) is the
most widely used bumble bee species for commercial
green house pollination in Me´xico (Palma et al. 2004,
Velthuis and van Doorn 2006). However, this species
is nonnative to this part of North America (Velthuis
and van Doorn 2006), and if not properly handled,
individuals can escape and possibly act as disease vec-
tors to wild populations or, alternatively, become es-
tablished and start competing with the native apifauna
(Hingston and McQuillan 1999, Delaplane and Mayer
2000, Colla et al. 2006). Also, if interbreeding with
native species, genetic pollution might occur (Cuad-
riello-Aguilar and Salinas-Navarrete 2006, Velthuis
and van Doorn 2006). Due to these potential negative
effects, importation of exotic bumble bees may be
restricted in Me´xico as has occurred in other Latin
American countries (Cuadriello-Aguilar and Salinas-
Navarrete 2006), thus affecting current methods of
greenhouse crop production.
In the Neotropics, there are numerous native pol-
linators that could be used commercially (Free 1993,
Mele´ndez 1997, Can-Alonzo et al. 2005). Stingless bees
(Apidae: Meliponini) have recently gained attention
as potential pollinators of greenhouse cultivars (Mala-
godi-Braga et al. 2000; Slaa et al. 2000, 2006; Macõ´as et
al. 2001). In Me´xico, the most common stingless bee
species is Nannotrigona perilampoides Cresson, occur-
ring across tropical and subtropical areas of the coun-
try, and reaching further north than any other stingless
bee species (Ayala 1999). Colonies of this species
consists of a few thousand workers headed by a single
laying queen; workers are small and robust, measuring
4.1Ð4.2 mm in length (Ayala 1999, Slaa et al. 2000).
The Yucata´n Peninsula is the major producer of
habanero pepper, Capsicum chinense Jacquin, world-
wide with 1,000 ha cultivated and 3,700 tons har-
vested annually (Herrera 2001, Montes-Herna´ndez
2002). The ßowers of Capsicum are self fertile and in
open Þeld, fertilization occur by wind, but in covered
conditions the cultivars need pollinating agents for
1
Departamento de Apicultura, Facultad de Medicina Veterinaria y
Zootecnia, Universidad; Auto´noma de Yucata´n, Apdo. Postal 4-116,
Me´rida, Yucata´n, Me´xico, 97100.
2
Corresponding author, e-mail: qeuan@tunku.uady.mx.
3
CICATA-IPN Ave, Legaria 694 Col. Irrigacio´n Deleg, Miguel
Hidalgo CP, Me´xico D.F. 11500.
0022-0493/08/0132Ð0138$04.00/0 2008 Entomological Society of America
adequate fruit setting and quality (Shipp et al. 1994,
Cauich et al. 2006). Habanero pepper is an annual
plant, its ßowering period can extend up to 16 mo, but
commercial production only lasts a maximum of 4Ð6
mo (Cauich 2006).
N. perilampoides has demonstrated good efÞciency
as pollinator for greenhouse tomato and pepper com-
pared with mechanical vibration (Cauich et al. 2006).
However, it is important to document how this species
compares to other pepper pollinators in the same
environment, such as bumble bees or honey bees
(Cauich et al. 2004). Bumble bees have advantageous
features for pollinating crops, such as their large bod-
ies and tongues that enable them contacting the sexual
parts of ßowers with deep corollas and carry larger
pollen loads (Free 1993). Bumble bees exhibit the
buzz-pollinate behavior or sonication (high-fre-
quency muscle vibrations to shake the pollen off the
ßowers) that increases pollen release in ßowers with
poricidal anther structures such as those of peppers
(Banda and Paxton 1991, Free 1993, Pressman et al.
1999). Colonies of N. perilampoides also have advan-
tages for using them in enclosed crops, surviving long
periods in greenhouses (Cauich et al. 2004) and easily
adapting to managed conditions in wooden hives, so
colonies may be readily available for transporting and
establishment elsewhere (Quezada-Eua´n et al. 2001).
We compared the foraging activity and pollination
efÞciency of N. perilampoides and B. impatiens for fruit
production of habanero pepper in tropical Yucata´n.
The aim was to provide pepper growers with local
alternative pollinators, especially if restriction is im-
posed on the importation of exotic bumble bee colo-
nies in the future.
Materials and Methods
Study Site and Species. The study was conducted at
the Faculty of Veterinary Medicine of the Universidad
Auto´noma de Yucata´ninMe´rida (2110N, 8927W)
between October and December 2003. The climate in
this region is classiÞed as subtropical. The annual av-
erage temperature is 26.5C (range 17Ð 42C) and rain-
fall is 940 mm (Garcõ´a 1988).
In the Yucata´n peninsula, commercial pollination
houses usually consist of an iron frame, covered by
anti-aphid mesh with a plastic roof (Palma 2006). We
used three pollination cages (4 by 4 by 3 m) built to
scale to resemble those commercial pollination houses
in Yucatan.
ÔCreoleÕ habanero pepper plants were grown using
local seed from the Technological Institute for Agri-
culture number two in Conkal Yucata´n, which is pres-
ently conducting a rescue program of habanero local
varieties (Trujillo-Aguirre 2002). Forty plants were
sown in each cage by using the management recom-
mended for this crop (Soria-Fragoso et al. 2002).
Bee Colonies and Experimental Design. One col-
ony of N. perilampoides and one colony of B. impatiens
were used during the experiments. The colony of N.
perilampoides had 1,200 workers, and the B. impa-
tiens colony had 60 workers. The B. impatiens colony
was purchased to Koppert Me´xico (Municipio El
Marque´s, Queretaro, Mexico).
Management of the colonies, before and after the
introduction to the cages, for N. perilampoides was as
described in Cauich et al. (2004, 2006), and for B.
impatiens as recommended by Natupol, Me´xico. The
B. impatiens colony was fed with the sugar syrup sup-
plied by Natupol, and every 3 d, with5goffresh pollen
collected from colonies of the stingless bee Melipona
beecheii Bennet kept at the faculty. The N. perilam-
poides colony was fed with 5 ml of honey every 3 d, or
before, if the feeder was empty; no pollen was supplied
to this colony because it had had large pollen stores.
Water was supplied in one 5-liter bucket placed 1 m
in front of the colony, because N. perilampoides col-
lects water in hot days presumably for temperature
regulation (Cauich et al. 2004).
We only used one colony of each species that was
rotated between cages. After 1 wk in a cage, the col-
onies were removed. A period of 3 d elapsed before
the colonies were introduced to a different cage for
another week, because3distheperiod of maximum
receptivity of habanero ßowers (G.P., personal obser-
vations). This was done three times, so that within
each cage pepper ßowers were exposed to the three
treatments. Mechanical vibration was used as a control
treatment because comparatively low quality of fruit
had been obtained in former work (Cauich et al.
2006). Vibration was conducted by means of an elec-
tronic pollinator II (HGI Worldwide Inc., Colorado
Springs, CO). Mechanical vibration was performed
every3dbyvibrating each truss for 5Ð7 s every hour
between 0800 and 1100 hours.
The fruit that were produced with each treatment
were labeled using ribbons of different colors per
treatment and tags were attached to them to avoid
mixing of the data. An estimation of the number of new
ßowers that opened per day was obtained by counting
them on 10 plants at the start of the experiment. The
counts were made on 7 d.
Foraging Behavior. For all the variables related to
foraging behavior, both bees were evaluated at the
same time on the same days. The foraging activity of
the colonies was evaluated using the following four
variables: 1) number of ßowers visited per plant in 5
min, 2) total number of ßowers visited during a whole
foraging trip, 3) time spent on a single ßower, and 4)
the duration of the trip. These variables were obtained
by marking 10 bees of each species with different
colors on the thorax and by following them across the
cage during their foraging trips between 8 and 16 h in
2 d per repetition. As additional information, the num-
ber of bees entering the hive for 5 min every hour and
the number of bees foraging on the ßowers of 10 plants
was estimated during 6 d (across 8 h and in 2 d per
repetition), but these variables were not subject to
statistical comparison between bee species given the
different population sizes. During the recordings of
the last two variables, the temperature, humidity, wind
speed, and light intensity were recorded using a ther-
mohygrometer (Sato Keiryoki MFG Co.), an ane-
February 2008 PALMA ET AL.: POLLINATION OF HOT PEPPERS WITH BEES 133
mometer (Turbo meter-Davis instrumental) and a
luxometer (Luton Lx), respectively.
Pollination Efficiency. We evaluated pollination ef-
Þciency by using three approaches. First, the fruit
produced in 20 plants per cage was evaluated for the
following variables: fruit set, weight, size of polar di-
ameter, size of equatorial diameter, and total number
of seeds.
Second, we used SpearÕs pollination efÞciency index
(Spears 1983) for which the visits to ßowers by each
pollinator were controlled to obtain the seed and com-
pare them. SpearÕs pollination efÞciency index is a
method for evaluating the relative importance of dif-
ferent visitors to a plantÕs pollination by allowing vir-
gin ßowers to be visited by one visitor and monitoring
the subsequent fruit, seed, or nut set (Spears 1983).
The values of the index range from 0, when no con-
tribution by a given pollinator is observed, to 1, when
the production of seed or fruit by a given pollinator is
equal to that in ßowers that received unrestricted
visits by pollinators. The index is calculated as follows:
pollinator efÞciency (PE) (P
i
Z)/(U Z),
where: P
i
is average number of seeds in the fruit that
received one visit by pollinator i, Z is average number
of seeds in the fruit that received no visits, and U is
average number of seeds in the fruits that received
unrestricted visits.
To obtain the seed under controlled conditions, in
each cage 90 ßowers were randomly selected before
anthesis. Thirty of these ßowers were marked and left
open; 30 ßowers were isolated with cotton bags and
allowed only one bee visit, after which were rebagged;
and 30 ßowers remained bagged to eliminate bee visits
in each repetition. The ßowers were located in dif-
ferent plants and were all of the same age. After 1 wk,
when ßowers had senesced, all bags were opened and
fruit was allowed to develop. The fruit was harvested
between 35 and 40 d after the ßowers were visited.
A third indicator of the efÞciency of both bees was
the amount of pollen removed from the ßower. For
this, pollen counts were obtained on Þve ßowers on
the day they opened when no treatment was con-
ducted in each pollination cage (counts were done on
six different days). The anthers were carefully abs-
cised with a pair of Þne scissors and immediately
deposited in an Eppendorf tube with 1 ml of 70%
ethanol. The tube was centrifuged at 10 gfor 5 min
after which 5
l of methyl blue was added to stain the
pollen grains. Seven 5-
l aliquots were separately
counted in a Neubauer chamber for hematite screen-
ings, and an average number of pollen grains was
calculated for the whole 1 ml. Twenty single visits
ßowers by N. perilampoides and 20 by B. impatiens also
were analyzed in the same manner to have estimations
of the number of pollen grains that were removed by
each visitor after only one visit.
Data Analysis. All variables related to foraging ac-
tivity were log
10
transformed to improve normality.
The variables were then compared by a twoÐway anal-
ysis of variance (ANOVA) by using the linear model
(GLM) procedure of SAS (SAS Institute 1990). Dun-
can multiple comparison test were applied to separate
the means when signiÞcant differences were indicated
by the GLM procedure. Pearson correlations were
used to analyze the effect of the environmental vari-
ables on the number of bees entering the hive and the
number of bees on the ßowers using the PROC CORR
procedure (SAS Institute 1990).
Data of seed number were log
10
transformed. A
KruskalÐWallis test was used to compare pollination
treatments for fruit set followed by a nonparametric
Tukey-type multiple comparison. Comparisons be-
tween treatments for all other variables related to
pollination efÞciency were made using a twoÐway
ANOVA followed by Duncan tests (SAS Institute
1990).
Results
Foraging Behavior. The average number of ßowers
that opened per plant each day was 37.3 6.7 (n10
plants). Thus, there were, on average, 1,400 Ð1,500 new
ßowers each day in a cage.
The onset of foraging started earlier for B. impatiens
compared with N. perilampoides, which only started to
increase after 10 a.m. (Fig. 1). Foraging behavior dif-
fered between both bee species (Table 1). Although
the number of ßowers visited in one plant in 5 min was
similar between both bee species (F4.75; df 1, 169;
P0.01), the time spent on a single ßower was longest
0
2
4
6
8
10
12
14
time of day
Number of bees
N. perilampoides B. impatiens
08:00 09:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00
Fig. 1. Comparative foraging activities of B.impatiens
and N.perilampoides observed in a 5-min period on the
ßowers of habanero pepper during 6 d.
Table 1. Pearson’s correlation coefficients of two estimations
of foraging activity in N. perilampoides and B. impatiens with the
environmental variables inside the pollination cages (n48 for all
cases)
Variable N. perilampoides B. impatiens
No. of bees entering the hive
Temp 0.0258 0.1270
Relative humidity 0.2447 0.0822
Light intensity 0.4199*0.2642
Wind speed 0.2245 0.2025
No. of bees on ßowers
Temp 0.6491*0.2192
Relative humidity 0.0536 0.2127
Light intensity 0.3042*0.5667*
Wind speed 0.1007 0.1270
134 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 101, no. 1
for N. perilampoides (F25.05; df 1, 85; P0.01),
as well as duration of a foraging trip (F14.34; df
1, 63; P0.01) and the number of visits per foraging
trip (F13.1; df 1, 37; P0.05).
For B. impatiens, some individuals were seen fre-
quently displacing others B. impatiens on the same
ßower. Also, B. impatiens foragers frequently left the
hive with the pollen loads of the former trip and ßew
among the plants without collecting pollen.
The temperatures registered in the greenhouse
were, on average, 27 7.2C(n48), and the relative
humidity was 63 16.7% (n48). Light intensity was
14,067.8 8,699 (n48) luxes and wind speed was
0.02 0.088 m/s (n48).
PearsonÕs correlation showed that there was a sig-
niÞcant association between light intensity and the
number of bees entering the hive in N. perilampoides
(Table 2). All other environmental variables had no
correlation with the number of bees entering the hive
either of N. perilampoides or B. impatiens. However,
there were signiÞcant correlations between the num-
bers of ßowers visited in 5 min with light intensity in
B. impatiens. The same relationship was observed in N.
perilampoides, and for this variable, temperature also
had a signiÞcant effect (Table 2).
Pollination Efficiency. SigniÞcant difference in the
percentage of fruit set between treatments was found
with the KruskalÐWallis and the multiple comparison
tests (
2
84.67, df 2, P0.001). However, the
SpearÕs pollination efÞciency index showed that there
were no signiÞcant differences in the pollination ef-
Þciency of N. perilampoides and B. impatiens (Table
3). Also, there were differences for the other four
variables (i.e., polar and equatorial diameter, weight,
and seed number) measured in those fruit produced
by both bee species and those produced by mechan-
ical vibration (Table 3).
An estimation of the number of pollen grains in
habanero pepper ßowers revealed an average of
70.6 1.08 10
3
. Out of this count, a single indi-
vidual of N. perilampoides removed an average of
5.34 2.93 10
3
pollen grains or 7% in a single
visit. However, B. impatiens removed more grains in a
single visit 29.8 4.4 10
3
or 40%. Both species
were signiÞcantly different for this variable (F13.53;
df 1, 50; P0.001).
Discussion
Foraging Behavior. Bumble bees have been recog-
nized as efÞcient pollinators of peppers with a wide
use in greenhouses in Me´xico (Meisels and Chiasson
1997, Dag and Kammer 2001, Velthuis and van Doorn
2006). More recently, N. perilampoides has been suc-
cessfully used in enclosed pepper pollination in Yu-
catan (Cauich et al. 2006). The current study is the
Þrst where both pollinators have been compared un-
der tropical conditions. We showed that the quality of
individual habanero fruit produced in greenhouses
was similar in cages using both bee species and that
both species were comparatively better than pollina-
tion performed through mechanical vibration. In our
study, an average of 37 new ßowers opened daily per
plant, which meant that 1,500 new ßowers were
available per day. Given such results, we can consider
that effective pollination occurred by both pollinators
using a single colony per 40 plants.
The number of bees attracted to the ßowers of a
particular crop is one of the main limitations for its
adequate pollination (Free 1993, Ish-Am and Eisikow-
itch 1998). In our study, the number of individual bees
working on the ßowers of habanero peppers was not
a limitation for the pollination of the crop because
both bee species visited a high number of ßowers per
plant and per foraging trip. Moreover, because haban-
ero ßowers only produce minute amounts of nectar
(G.P., personal observations), we could be sure that
bees were attracted to collect the pollen of this crop,
thus favoring pollination.
Table 2. Comparison of four indicators of foraging activity between B. impatiens and N. perilampoides on habanero pepper
Variable Species P
B. impatiens N. perilampoides
No. of ßowers visited in 5 min 10.1 7.23 (n81) 8.1 3.33 (n90) 0.078
Duration of a foraging trip (min) 13.4 7.14 (n25) 25.7 15.5 (n40) 0.001
Time spent on a ßower (s) 8.1 4.5 (n40) 36.3 17.3 (n47) 0.001
No. visits per trip 19.9 6.8 (n19) 42.4 18.3 (n20) 0.002
Averages (SD) not followed with the same letter are signiÞcantly different (P0.05; two-way ANOVA).
*P0.01.
Table 3. Pollination efficiency of B. impatiens, N. perilampoides, and mechanical vibration on fruit production of habanero pepper
Treatment Fruit
set (%)
Polar diam
(mm)
Equatorial
diam (mm) Wt (g) Seed no. per
fruit
SpearÕs pollination
efÞciency index
N. perilampoides (n171) 84.9a 34.77 0.48a 23.5 0.41a 4.98 0.14a 51.1 0.41a 0.784
B. impatiens n 105 51.3c 33.18 0.6a 22.93 0.53a 4.78 0.18a 49.72 0.32a 0.712
Mechanical vibration (n122 ßowers) 74.8b 31.56 0.56b 20.6 0.51b 4.63 0.17b 42.61 0.27b
SpearÕs pollination efÞciency index is a method for evaluating the relative importance of visitors to ßowers; it was not calculated for mechanical
vibration. Different letters in the same column indicate signiÞcant differences (P0.05; chi-square).
February 2008 PALMA ET AL.: POLLINATION OF HOT PEPPERS WITH BEES 135
When numbers of foragers on the crop is not a
limitation, other factors related to the bees are con-
sidered to estimate their potential for pollination, such
as the number of visits per unit time and the balance
between pollen removed and deposited on the ßowers
(Thomson and Goodell 2001).
Both B. impatiens and N. perilampoides visited sim-
ilar numbers of ßowers per plant in 5 min. However,
fewer ßowers were visited by B. impatiens during a
single foraging trip compared with N. perilampoides;
this may confer an advantage to the latter species
because more ßowers can receive multiple visits
(Goodell and Thomson 1997). The value of a partic-
ular pollinator depends on how many visits are ex-
pected to different ßowers and also how much pollen
is left behind to be taken by later visitors that, in turn,
would increase the chances for delivering it to other
ßowers (Goodell and Thomson 1997). In N. perilam-
poides, the number of visits was signiÞcantly higher
and this coupled with fewer pollen grains being re-
moved in each visit could contribute to a better op-
portunity for pollination of a larger number of ßowers,
especially in conÞned crops.
The foraging speed was higher in B. impatiens; how-
ever, the number of ßowers visited per foraging trip
was lower compared with N. perilampoides. Moreover,
B. impatiens foragers remained longer inside their
nests; thus, much more the time elapsed between
foraging trips compared with N. perilampoides.
The environmental variables that affected foraging
activity were temperature and light intensity for N.
perilampoides and light intensity for B. impatiens. We
do not know about the absorbance of UV light by the
mesh we used in our experiments, but the plastic used
in the roofs could have a dispersing effect on the UV
light entering the structure due to its absorbance, and
this may reduce foraging activity of stingless bees and
bumble bees (Parra-Canto 1998, Malagodi-Braga 2002,
Dyer and Chittka 2004). Thus, more light intensity is
needed for an adequate orientation of the bees in such
types of greenhouses. In the case of temperature,
stingless bees foraging set after 9 a.m., and it increased
throughout the day. Perhaps warming up is needed
before foraging is established (Moo-Valle et al. 2000,
Cauich et al. 2006). However, bumble bees started
foraging earlier and continued constantly foraging
during the period of observation, although it was ob-
served that at high temperatures (28C), their for-
aging was reduced. Although in our study the effect of
temperature was not signiÞcant on bumble bees, this
limitation should be considered when these bees are
used in greenhouses under tropical conditions (Kwon
and Saeed 2003).
Pollination Efficiency. N. perilampoides and B. im-
patiens showed similar pollination efÞciency (as esti-
mated with the SpearÕs pollination efÞciency index) in
spite of a lower number of pollen grains that were
removed in single visits by the former. Therefore, it
seems that the number of pollen grains transported by
N. perilampoides was sufÞcient for adequate pollina-
tion of habanero pepper. Moreover, N. perilampoides
visited more ßowers per foraging trip, and this could
also compensate for the lower amount of pollen trans-
ported after single visits and still act as efÞcient pol-
linators (Heard 1994). It has been reported that al-
though pollen collection and deposition may increase
with body size, small bees can deposit as much or
sometimes more pollen compared with larger species,
as has been found comparing andrenid bees with
bumble bees in apple (Malus spp.) pollination studies
(Kendall and Solomon 1973) or stingless bees with
honey bees in macadamia (Macadamia spp.) (Heard
1994). This could in part be explained by the fact that
even though pollen foragers can remove considerable
amounts of pollen, if this pollen is mainly transferred
to the pollen baskets, the deposit of grains on the
ßowers can be comparatively low.
In single visits, B. impatiens removed almost one
third of the amount of pollen produced by habanero
pepper ßowers. It was evident that bumble bees could
remove larger amounts of pollen, probably due to their
larger size coupled with their sonication behavior,
although we do not know whether C. chinense requires
buzz-pollination for adequate pollination (Banda and
Paxton 1991, Free 1993, Shipp et al. 1994, Slaa et al.
2006, Velthuis and van Doorn 2006). This difference
may signify a higher deposition of pollen in the stigma.
In our study, pollination efÞciencies suggested decent
pollen transfer for both bee species, but for B. impa-
tiens it is necessary to consider that pollen depletion
could be a problem at high densities of foragers per
ßower because these bees remove a large proportion
of the pollen in the Þrst visits.
We did not quantify the deposition of pollen on the
stigmas. The amount of pollen deposited on the stigma
could possibly have been a better way of estimating
fertilization. Moreover, an estimation of the amount of
pollen removed relative to the amount deposited be-
tween both bee species would provide a better indi-
cation of pollinator superiority (Thomson and Good-
ell 2001). A study of the effect of this variable in
habanero pepper would be recommended.
All values for quality of fruit were higher for both
bee species compared with mechanical vibration.
Fruit set was also higher for N. perilampoides com-
pared with mechanical vibration. This is in contrast
with the high percentage of fruit set obtained in ha-
banero pepper by Cauich et al. (2006) by using me-
chanical vibration. However, in the present experi-
ment, vibration was only conducted three times
between 8 a.m. and 11 a.m., whereas in Cauich et al.
(2006) it was carried out Þve times more, each hour
until 4 p.m. This suggests that mechanical vibration is
recommended for a longer period for an adequate fruit
set in habanero pepper. Nevertheless, it seems that
mechanical vibration is not a good option for habanero
pepper, because we corroborated (see Cauich et al.
2006) that the quality of the fruit obtained was better
by using bees.
For B. impatiens, it is also necessary to point out that
abortion of habanero fruit was frequent, and this may
be the main factor explaining the signiÞcantly lower
percentage of fruit set compared with the other two
treatments (Table 3). We speculate that pollen de-
136 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 101, no. 1
pletion of some ßowers visited by B. impatiens may
have caused more visits to them and subsequent dam-
age and abortion of their fruit. Indeed, we observed
that some ßowers lost the petals and that areas of the
stigma and ovary were necrotic after intense visitation.
Our study is the Þrst, to our knowledge, that registers
overpollination caused by bumble bees to hot pepper
ßowers (Velthuis and van Doorn 2006). In Korea, in a
study with 150 plants of Capsicum annuum L. with an
average of 9.5 ßowers per plant (1,500 ßowers per
day, similar to what we had in C. chinense) by using a
colony of B. impatiens (60 workers), no damage to
the ßowers was reported by Kwon and Saeed (2003).
In tomato, excessive visitation of bumble bees to the
ßowers can be detrimental to the crop by damaging
the ßowers and reducing fruit set (Cribb 1990, Jones
1998, Morandin et al. 2001). Perhaps the ßowers of C.
chinense are more sensitive to damage after intense
visitation. It is recommended that growers consider
potential damage if bumble bees were to be used as
pollinators of this crop. Alternatively, this result may
suggest that one colony of B. impatiens could be used
to pollinate more plants and ßowers than those in the
present experiment and could probably be more ben-
eÞcial at higher plant densities than N. perilampoides,
but this would need to be veriÞed in a larger green-
house.
Stingless bees have been recently considered good
pollinator candidates in conÞned systems (Maeta et al.
1992, Slaa et al. 2006). Our results show that the species
N. perilampoides was similar to bumble bees in its
efÞciency as a pollinator of hot pepper and that they
could be a good alternative for the latter under trop-
ical conditions. Nevertheless, more research is needed
on the foraging behavior of stingless bees to provide
estimations for the densities of colonies necessary to
adequately pollinate different types of Capsicum cul-
tivars. Mass breeding techniques also are needed to
supply the commercial demand and thus prevent po-
tential negative impacts on native populations.
Acknowledgments
We thank Manuel Cocom, Humberto Moo-Valle, and Raul
Concha-Viera for data collection. We thank Drs. Alfonso
Velazquez and Luis Rodriguez for statistical advice. Two
anonymous reviewers made valuable comments that helped
to improve the manuscript. We thank Consejo Nacional de
Ciencia y Tecnologia (CONACYT)-Sisierra and Fundacio´n
Produce Yucata´n for funding this research. G.P. thanks
CONACYT for an M.S. grant during which this study was
conducted.
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138 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 101, no. 1
... In Mexico, the pollination effectiveness of the native Nannotrigona perilampoides (a stingless bee) was compared to that of the exotic Bombus impatiens (the common eastern bumblebee from northern North America) on habanero peppers, Capsicum chinense (Palma et al. 2008). A single visit by the exotic B. impatiens removed 40% of pollen grains from anthers, whereas N. perilampoides removed only 7%. ...
... However, fruit set was lower for flowers pollinated by B. impatiens (51%) than for those pollinated by N. perilampoides (85%), even though seed number per fruit was similar for both the exotic and native bees. Palma et al. (2008) argued that foraging behavior allowed N. perilampoides to overcome the differences in pollen removal. Bombus impatiens visited 10 flowers in a 5-min period, whereas N. perilampoides visited eight. ...
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The flowering characteristics, contribution of self versus cross pollination and bee visitation were studied in 'criollo' avocado cultivars in Yucatan, Mexico. The pattern of pistillate and staminate stages (I and II, respectively), stigma receptiveness and the production of fruit in bagged and open panicles was followed in two commercial orchards. The number of bee visits across the day and the number of pollen grains on the body of workers of honey bees and two native stingless bee species were compared. Environmental variables were also recorded to determine their influence on bee visit rates. Few stigmas were morphologically receptive during the second day of opening of individual flowers (stage II). There was no overlapping between stages I and II. Open panicles produced significantly more fruit (60% on average) than bagged ones. Bee visits to flowers of both type A and B cultivars were significantly more frequent during the pistillate stage than during the staminate stage. Apis mellifera had an overall higher frequency of visits compared with the other two species. The number of pollen grains on the bees was not statistically different between A. mellifera (1644 ± 90.1 [s.d.]) and Trigona nigra (1356 ± 71.3) but it was significantly less in Nannotrigona perilampoides (781 ± 16.1). Environmental humidity had an influence on the visits of A. mellifera (r = -0.88) and N. perilampoides (r = 0.92) but not on T. nigra. It is concluded that self pollination is of limited influence in fruit production in avocado cultivars in subtropical Mexico and that both native stingless bees and honey bees potentially are efficient pollinators of this crop.
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Intranidal temperature fluctuation was studied in colonies of Melipona beecheii, an economically important stingless bee from Yucatan, Mexico. Two feral colonies nesting in tree cavities were used in the experiments. The brood and storage pots inside the nests were monitored for temperature changes using a telethermometer. Ambient temperatures immediately outside the logs were recorded simultaneously with thermohygrometers. Temperatures were recorded every hour for 24 h on four non-consecutive days. Differences between ambient temperatures and temperatures within nests were noted during the day and night. In all cases temperatures in brood and storage pots area were different from the ambient temperature (P < 0.01). There was no significant relationship between intranidal and ambient temperatures during the day (09.00 h to 20.00 h) on all days of measurement (P > 0.01). However, during lower ambient temperatures at night (21.00 h to 08.00 h) intranidal and ambient temperatures were significantly correlated (P < 0.01). These findings indicate that temperatures inside natural nesting colonies of M. beecheii remain relatively stable during the day, but tend to vary at night. Colony temperatures at night may lag from 5-6 h behind ambient temperatures. Active temperature control in nests of M. beecheii thus seems unlikely, and therefore the ability to ensure stable temperatures within the nest might be an important factor limiting the successful adaptation of this species to hive culture.
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Avocado in the Western Galilee region of Israel was found to be dependent on honeybees for fruit set. A significant initial fruit set required a density of at least five bees per tree during the female stage of flowering. The early-blooming avocado cultivars were visited by enough honeybees on fewer than one-third of their blooming days. Because they were visited mostly at the end of their blooming season, and due to rainy days, not more than 5% of their entire season's flowers were exposed to sufficient pollination to set fruit. The late-blooming cultivars however, were visited by many bees and exhibited high initial fruit set. The attractiveness to honeybees of various avocado cultivars and some other plant species, which were found to compete for pollination, was measured by the coefficient 'r' obtained from correlations between bee density and reward measures of these plants, over the course of a day or season. At the beginning of the blooming season, the avocado flowers competed for nectar-foraging bees mainly with flowers of Citrus spp., and for pollen foragers with Brassicaceae and Fabaceae, all of which were more attractive to the bees. Since pollination was carried out only by nectar-collecting bees, Citrus spp. flowers presented the main limiting factor for initial fruit set in avocado. However, toward the end of its blooming season, the avocado competed with Poaceae, Asteraceae and Apiaceae flowers, and its relative attractiveness increased.
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The efficiency of an electric bee in pollinating tomatoes grown in an unheated greenhouse was compared with that of bumble bees. Two years of experiments show that under the moderate climatic conditions of autumn and early winter, the two methods had similar effects on fruit set, seed number, fruit size and yield. Under more severe winter conditions, however, bumble bees were more efficient than the common agricultural practice of using the electric bee 2-3 times a week. Even in the presence of relatively low amounts of pollen grains per flower, a high percentage of fruit set was obtained by the bees. Under these adverse climatic conditions, flower vibration with the electric bee and with bumble bees achieved equal degrees of fruit set, only when the electric bee was operated every day. It may be concluded, therefore, that bumble bees are efficient pollinators as long as the flower organs are functional and a minimum number of pollen grains is available. For achieving similar pollination efficacy with an electric bee, one should adjust the frequency of its use according to the circumstances, with daily operation under unfavourable conditions.
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The amount of pollen (of the appropriate species) borne on the body of an insect is presumed to be an important factor influencing its value as a pollinator. Some 700 insects of more than seventy species were collected from the blossoms of apple trees at Long Ashton, and estimates made of the quantities of pollen carried on their bodies (excluding that in the pollen baskets of bees). The species (and sexes and castes of wild bees) are listed in Table 2 in descending order of the geometric mean number of fruit pollen grains on the body. The precise order of the taxa in the list is not significant; the significance, or otherwise, of the differences between taxa represented by five or more specimens is indicated in the table. The specimens were collected at different times and at various phases of blossom and weather in 1969 and 1970. If the mean pollen counts are nevertheless taken at face value, females of Andrena haemorrhoa and A. coitana and workers of Bombus terrestris+ lucorum bore significantly more fruit pollen (over 15 000 grains) than honeybee workers (mean about 4000), a number of other wild bees, and some of the larger and hairier syrphid flies. Insects with significantly less fruit pollen than this group included a few wild bees and the majority of syrphid flies. A number of small or smooth insects, including various flies and beetles, bore very few pollen grains.