Pollinator diversity increases fruit production in Mexican coffee plantations:

The importance of rustic management systems

Carlos H. Vergara *, Ernesto I. Badano
Departamento de Ciencias Qumico Biologicas, Escuela de Ingeniera y Ciencias, Universidad de las Americas Puebla, Ex-Hda. Sta. Catarina Martir,
Cholula 72820, Puebla, Mexico
1. Introduction
Pollination is an ecological process fundamental for the
maintenance of the viability and diversity of owering plants
and provides important ecosystems services to humans (Allen-
Wardell et al., 1998; Daily et al., 1997; Kevan, 1999; Klein et al.,
2007). At a global scale, about one-third of the human food is
obtained from plant species that depend on pollinators to
produce fruits and seeds (McGregor, 1976), and these
pollination services have been valued in 112 billons of American
dollars (Costanza et al., 1997). Introduction of exotic pollinators,
mainly Apis mellifera L., has been useful for increasing crop
production around the world (Allen-Wardell et al., 1998).
However, wild pollinators may provide pollination services,
even with higher efciency than A. mellifera, without incurring
in economic costs (Kearns et al., 1998; Kremen et al., 2002;
Olschewski et al., 2006). Nevertheless, fruit and seed production
in agroecosystems may also depend, among other factors, on the
population dynamics (e.g., temporal variability in abundance)
of the pollinator species, pollination efciency of different
pollinator species, competition between cultivated and wild
plants for pollinators, distance between crops and native
vegetation patches, availability of resources (other than crops)
for pollinators and land management systems used by farmers
(Kevan, 1999).
Mexico is the worlds 5th producer of coffee and the 3rd
exporter of organic coffee (International Coffee Organization,
2006) with more than 1.5 million people economically depend-
ing on this crop (Nolasco, 1985). The state of Veracruz is the
second most important producer of coffee in Mexico, and most
of the cultivation takes place in the central region of the state,
where our study was carried out. Management for pollination is
not common among coffee producers in Mexico and very
often this aspect is not even considered as a management
practice. However, beekeepers usually move many hives of A.
mellifera into coffee plantations to take advantage of the intense
nectar ow associated with coffee blooming (Labougle and
Zozaya, 1986).
Agriculture, Ecosystems and Environment xxx (2008) xxxxxx
A R T I C L E I N F O
Article history:
Received 4 April 2008
Received in revised form 31 July 2008
Accepted 4 August 2008
Available online xxx
Keywords:
Coffee
Me xico
Pollination service
Pollinator diversity
Fruit production
A B S T R A C T
Pollination is an ecological process that provides important services to humans. Pollination service in
agroecosystems depends on several factors, including the land management systems used by farmers.
Here we focused on the effects of insect pollinator diversity on coffee fruit production along a gradient of
management systems in central Veracruz, Mexico. The gradient ranged from low environmental impact
management systems (the native forest is not completely removed) to high environmental impact
management systems (the native forest is completely removed). We hypothesized that pollinator
diversity should be higher in low-impact systems. Then, if fruit production is positively related to
pollinator diversity, plantations with low-impact management systems should display higher fruit
production than plantations with high-impact management systems. We used observational and
experimental data to test this hypothesis. Our results indicated that low-impact management systems
have higher species richness and relative diversity (measured with the Shannon-Wiener diversity index)
of pollinators than high-impact management systems. In all cases, fruit production was positively related
with species richness and diversity of pollinators. Moreover, fruit production was higher in low-impact
than in high-impact management systems. These results suggest that the diversity of insect pollinators
can be inuenced by the management system applied by farmers, and that such effects may have strong
consequences on coffee fruit production.
2008 Elsevier B.V. All rights reserved.
* Corresponding author. Tel.: +52 222 229 2415; fax: +52 222 229 2419.
E-mail address: carlosh.vergara@udlap.mx (C.H. Vergara).
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doi:10.1016/j.agee.2008.08.001
Coffee (Coffea arabica L.) is a self-compatible species, which may
or may not benet from pollination by animals. Nevertheless, in
several instances, it has been reported that increases in the number
of visits by pollinating insects lead to higher fruit set in coffee
plants (Free, 1993; Manrique and Thimann, 2002; Roubik, 2002a,b;
Klein et al., 2003a). Despite the importance that pollinators may
have on coffee production, no previous studies have addressed this
issue in any of the coffee producing regions of Mexico. On the other
hand, most studies on the impact of pollinators on coffee
production focused on the effects of species richness and/or the
abundance of pollinators (Klein et al., 2003a,b; Ricketts, 2004), but
do not integrate these two variables in a single ecological index of
diversity reecting both the impact of species richness and the
distribution of abundances of the different species (e.g., the
Shannon-Wieners index or the Simpsons index). Moreover, a
diversity of management systems have been identied in coffee
farms of this country (see below) but, as far as we are aware, there
are no studies evaluating if management system affects pollinator
diversity and, consequently, coffee production.
Moguel and Toledo (1999) identied ve management systems
in Mexican coffee plantations: (1) rustic shaded coffee, where
plantations are located beneath the canopy of native tropical or
temperate forests after removing vegetationof the lower strata; (2)
traditional shaded coffee, where vegetation of the lower strata is
removed and coffee is grown beneath the native forest canopy
together with several other plant species for local subsistence
(bananas and oranges, among others); (3) commercial polyculture,
where the native forest is completely removed and replaced with a
set of nonnative trees with high economic value (pepper and cedar,
among others) which provide shaded for coffee; (4) specialized
shaded coffee, where native forest is removed and replaced by tree
species only belonging to the family Fabaceae for shade and soil
nitrication; (5) sun coffee, where forest is removed and coffee
plants are directly exposed to sun without vegetation cover.
Gordon et al. (2006) proposed modications to this system of
classication for the coffee farms found in the central region of
Veracruz, some of which were used by us as study sites. These
management systems have quite different consequences on local
biodiversity. For instance, it has been indicated that the rustic
system, mainly employed by indigenous people, retains higher
levels of plant and animal diversity than the other management
systems (Moguel and Toledo, 1999). However, the effects of these
different management systems on pollinator diversity remain
unknown.
The aim of this study was to evaluate the inuence of
management systems on the diversity of insect pollinators
and their associated consequences for coffee production. We
specically focused on four management systems in the hope they
represent a management gradient: rustic shaded coffee,
commercial polyculture, specialized shaded coffee and sun coffee
(see descriptions above). We hypothesized that pollinator diversity
should be higher in rustic shaded coffee plantations because this
management system has lower impacts on natural ecosystems.
Then, if fruit production is positively related with pollinator
diversity, coffee plants from rustic shaded plantations should
display higher number of fruits than those in plantations where the
other management systems are applied. However, because
increases in the distance between plantations and patches of
native vegetation may negatively inuence the diversity of insect
pollinators (Rathcke and Jules, 1993; Klein et al., 2003b), such an
effect may lead to confounding effects when relationships between
fruit production and pollination diversity are assessed. For this
reason, we also evaluated the relationship between pollinator
diversity in plantations and the distance to the closest patch of
native forest.
2. Materials and methods
2.1. Study sites
This study was conducted in the central area of the State of
Veracruz (19812
0
22
00
27
0
29
00
N, 96853
0
04
00
59
0
17
00
W), where an
important proportion of Mexican coffee is produced. In May
2004, during the owering peak of coffee, we selected 16
plantations with different management systems. The study sites
were located between 1040 and 1245 m.a.s.l. We selected four
study sites (plantations) for each management category. Four
plantations belonged to the rustic shaded coffee system (rustic or
traditional shaded coffee), four to the commercial polyculture
system, four to the specialized shaded coffee system and the other
four to the sun coffee system. This classication of management
types follows Gordon et al. (2006).
2.2. Pollinator sampling
To assess pollinator diversity, four coffee plants were randomly
selected at each site. For this, we used points at random directions
and distances from the center of each site and selected the nearest
owering coffee plant to each point. However, because coffee
owers usually remain open for 2 days but are attractive to
pollinators only during the st day (Free, 1993), we repeated this
procedure as many times as necessary until founding four plants
with recently open owers. On each selected plant, we drew an
imaginary observation area including 40% of their branches to
perform pollinator observations. All observations were carried out
on clear sunny days. At each plantation, the four selected coffee
plants were sequentially observed on the same day between 9:00 h
and 15:00 h; the rst plant was observed at 9:00, the second at
11:00, the third at 13:00 and the fourth at 15:00. Each plant was
observed for 25 min and the abundance of each pollinator species
was recorded. Observations of pollinators were started at 9:00
because insect activity was very low earlier in the day. We only
consideredas pollinators thoseoral visitors that madecontact with
the sexual parts of the ower, including species of Trigona subgenus
Trigona (traditionally considered as oral robbers) that were
collecting nectar or pollenlegitimally. All pollinators wereidentied
in situ by a specialist (Carlos H. Vergara). Pollinator data of the four
plants observed at each plantation were pooled to obtain the total
abundance of each pollinator species per plantation.
2.3. Pollinator diversity analyses
To determine whether diversity of pollinator communities
varied among management systems, we estimated the species
richness (S), the index of proportional diversity of Shannon-Wiener
(H
0
) and a dominance index (D) for each system. For this, pollinator
data from the plantations belonging to the same management
systemwere pooled. To avoid biases due to differences in sampling
effort among management systems, we used individual-based
rarefactions to compute these community attributes (Gotelli and
Colwell, 2001). Rarefaction analyses were conducted with the
software EcoSim 7.72 (Gotelli and Entsminger, 2005). These
analyses are based in Monte-Carlo resampling, where community
attributes (S, H
0
and D) are estimated as the sampling size (i.e., the
number of individuals in a resample = n) decreases from a
maximum value determined by the maximum number of
individuals (N) (Gotelli and Colwell, 2001). Then, each value of
S, H
0
and D is calculated from N to 1 individuals.
In our rarefaction analyses, values of S, H
0
and D were computed
1000 times for each value of n. After resampling 1000 times the
value of S for each value of n, these 1000 values were averaged to
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estimate the mean species richness at each sampling size. The
Shannon-Wiener index for each of the 1000 resamples of size n was
calculated using natural logarithms as H
0
= Sp
i
ln(p
i
), were
p
i
= proportion of individuals of the ith species in the sample; these
1000 values of H
0
for each value of n were then averaged to
estimate the mean diversity at each sampling size. The species
dominance index (D) was calculated as the fraction of the
(resampled) collection that was represented by the most common
species at each rarefaction run (Gotelli and Entsminger, 2005), and
was estimated for each sampling size in the same way as described
for H
0
. To assess variations in S, H
0
and D as the number of
individuals included in the resamples decreases from N to 1, we
constructed rarefaction curves by plotting the average values of S,
H
0
and D against their respective value of n. Further, to assess
statistical differences in pollinator diversity among management
systems, we calculated the 95% condence intervals for each
community attribute at each value of n; signicant differences
between management systems were assumed if their condence
intervals did not overlap (Gotelli and Entsminger, 2005). Since N
may vary among treatments (management systems in this case), it
is important to note that statistical comparisons among treatments
are only valid at similar values of n (Gotelli and Colwell, 2001).
2.4. Effects of pollinators on coffee fruit production
To assess the importance of cross-pollination mediated by oral
visitors on the development of fruits, and to determine differences
in these effects among management systems, we made a eld
pollination experiment by manipulating the access of pollinators
to owers. We rst selected four coffee plants (different fromthose
on which we assessed pollinator diversity) at each site by using the
same procedure described above. On each plant, we selected two
branches with oral buds, taking care that these branches were at
the same height in the plant and had approximately the same
length and exposure to sunlight. We then counted and labeled all
oral buds on each branchwith small plastic ags. After that, one of
the branches was covered with a Nytex
1
mesh bags to exclude
oral visitors (pollinator exclusion). The other branch remained
uncovered for the time of the experiment (open pollination). Seven
weeks later, we recorded the number of developing fruits on each
branch and calculated the fruit set rate of each pollination
treatment for each plant. The fruit set rate was calculated as the
ratio between the initial number of oral buds in the respective
branch and the number of developing fruits.
Statistical comparisons among combinations of management
systems pollination treatments were performed with a factorial
ANOVA. In this analysis, plantations were considered as indepen-
dent replicates; before performing the analysis, we averaged the
four values of fruit set ratio obtained for each pollination treatment
at each plantation (rustic coffee system open pollination n = 4;
commercial polyculture open pollination n = 4; specialized
shaded coffee open pollination n = 4; sun coffee open pollina-
tion n = 4; rustic coffee system pollinator exclusion n = 4;
commercial polyculture open pollination n = 4; specialized
shaded coffee pollinator exclusion n = 4; sun coffee pollinator
exclusion n = 4). The Tukeys test was used to assess post hoc
differences between combinations of management system polli-
pollination treatment.
We used the values calculated for fruit set for the previously
described analyses because fruit set is less dependent than fruit
retention or nal fruit production on plant physiological limita-
tions, resource availability and management practices. However, in
order to determine whether the effects of the open pollination
effectively translate into an increase in coffee production, 7
months after the pollination treatments were applied, we
monitored the number of fruits that reached maturity on branches
of coffee plants on which we applied this treatment. We used these
data to calculate the fruit retention rate as the ratio between the
number of mature fruits and the number of fruits initiated per
branch. The four values of fruit retention rate obtained for each
plantation were averaged to proceed with the statistical analysis.
We made a linear multiple regression analysis with categorical
variables to assess whether the fruit retention rate was related
with the fruit set rate, and to determine if these relationships
differed among plantations. In this analysis, the average fruit
retention rate was the dependent variable, the average fruit set
ratio was the continuous predictive variable, and the management
system (rustic, commercial polyculture, specialized shade coffee
and sun coffee) constituted the four levels of the categorical
predictive variable. In the regression model, we also included a
multiplicative interaction term between predictive variables to
account for differences in the slopes of regression functions
obtained for the different levels of the qualitative variable (Neter
et al., 1996). The analysis allows estimating a linear regression
function for each level of the categorical variable, and the
relationships between continuous variables are indicated to differ
between levels of the categorical variable if signicant differences
are detected between estimated parameters (intercepts or slopes)
of linear regression functions. Differences between these regres-
sion parameters were assessed with t-tests (Neter et al., 1996).
2.5. Relationships between pollinator diversity and fruit set
To assess if diversity of pollinator assemblages inuenced fruit
production, and to determine whether these relationships varied
among management systems, we conducted two linear multiple
regression analyses with categorical variables (details on this
analysis are givenabove). Inthe rst regression analysis, the average
fruit set ratio of the open pollination treatment obtained for each
plantationwas thedependent variable, theobservedspecies richness
of pollinators at each plantation was the continuous predictive
variable, and the management system constituted the four levels of
the categorical predictive variable. The second regression analysis
was made in a similar way, but in this case we calculated the
Shannon-Wiener diversity index for pollinator assemblages at each
plantation and used these values as the continuous predictive
variable in the regression analysis instead of species richness.
To determine if the distance to patches of native forest
inuences pollinator diversity in coffee plantation, we calculated
the distance (in meters) between the edge of the plantation and the
closest patch of native forest. These distances were determined by
analyzing high-resolution satellite images (IKONOS-2 one pixel per
square meter) with the software ERDAS IMAGINE 8.4 (ERDAS Inc.,
GA, USA) subsequently processed with ArcView3.2 (ESRI Software,
CA, USA). We later made two multiple regression analysis with
categorical variables (details on this regression analysis are given
above). In the rst analysis, pollinator richness detected at each
plantation was the dependent variable, distance to the closest
forest patch the continuous predictive variable, and management
system indicated the four levels of the categorical predictive
variable. In the second regression analysis the Shannon-Wiener
diversity index for pollinator assemblages at each plantation was
used as dependent variable.
3. Results
3.1. Pollinator diversity
All pollinators recorded during observations of coffee owers
were insects (Table 1). The highest richness of pollinator species
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was observed in rustic shaded sites (12 species), followed by
commercial polyculture sites (11 species). The lowest species
richness was recorded in the specialized shaded coffee plantations,
with 4 insect species. In the sun coffee management system, 5
species were detected during observations of owers. Apis mellifera
was the dominant species in all management systems in terms of
abundance of individuals, representing more than 80% of the
pollinator assemblages (Table 1).
Given that statistical comparisons of community attributes
through rarefaction analyses only make sense if they are conducted
at the same number of individuals (i.e., sampling sizes), the
rarefaction curves made to compare species richness, the Shan-
non-Wiener diversity indexandspecies dominance among manage-
ment systems only included estimations up to 447 individuals (the
highest number of individuals detected in a treatment with the
lowest abundancesun coffee system, in this case). Rarefaction
curves indicated no differences in species richness, diversity and
dominance between the rustic and the commercial polyculture
management systems at any number of individuals (Fig. 1).
However, these two management systems had signicantly higher
numbers of pollinator species than the specialized shaded and sun
coffee plantations after 100 individuals were included in rarefaction
curves (Fig. 1A). Similarly, values of the Shannon-Wiener diversity
index estimated for the rustic and the commercial polyculture
management systems were higher than those estimated for the
specialized shaded and sun coffee systems (Fig. 1B). The specialized
shaded and the sun coffee plantations also differed in terms of
species diversity, with the Shannon-Wiener index signicantly
higher for the sun coffee plantations after 150 individuals were
included in the analysis (Fig. 1B). In contrast to the analyses of
species richness and diversity, the rustic and the commercial
polyculture management systems showed signicantly lower
values of species dominance than the other two management
systems after 200 individuals were included in rarefaction curves
(Fig. 1C). The higher values of species dominance were estimated for
the specialized shaded coffee plantations, while the sun coffee
plantations showed intermediate values (Fig. 1C).
3.2. Effects of pollinators on coffee fruit production
Comparisons of fruit set rates from the pollination experiment
indicated highly signicant differences in fruit set among the
management systems (F
(3,24)
= 9.269; p < 0.001) and between the
two pollination treatments (F
(1,24)
= 22.950; p < 0.001). Moreover,
a highly signicant effect of the interaction between
management systems and pollination treatments was also
indicated (F
(3,24)
= 13.830; p < 0.001). The higher fruit set ratios
belonged to the combinations rustic open pollination and
commercial polyculture open pollination, showing statistical
differences with all other combinations of management system-
s pollination treatments (Fig. 2). Fruit set ratios did not differ
among the other combinations of management systems pollina-
pollination treatments.
A positive relationship was indicated between fruit retention
rate and fruit set rate of the open pollination treatment (goodness
of t test ANOVA: F
(7,8)
= 13.386; p = 0.047; R
2
= 0.921; data not
shown). However, differences were neither detected among slopes
(p > 0.05 in all cases) nor among intercepts (p > 0.05 in all cases) of
regression functions obtained for the different management
systems. These results indicate that higher fruit set rates lead to
higher fruit retention rates, and that these relationships are similar
among management systems.
3.3. Relationships between pollinator diversity and fruit set
Multiple regression analyses indicated strong relationships
between fruit set of open pollinated owers and both, pollinator
species richness (goodness of t test ANOVA: F
(7,8)
= 17.153;
p < 0.001; R
2
= 0.938) and pollinator species diversity (goodness of
t test ANOVA: F
(7,8)
= 8.743; p < 0.001; R
2
= 0.884). However, the
direction of these relationships varied among management
systems. The rustic, commercial polyculture and sun management
systems showed positive relationships between fruit set ratio and
either species richness or diversity (Fig. 3), and no differences were
detected between slopes or intercepts of regression functions
estimated for these management systems (p > 0.05 in all cases). In
contrast, fruit set ratio decreased as pollinator species richness or
diversity increased across the specialized-shade coffee plantations
(Fig. 3), and both the slope and the intercept of the regression
function estimated for this management system differed from
those estimated for the rustic, commercial polyculture and the sun
management systems (p < 0.05 in all cases).
Distance between plantations and the closest forest patch
varied between 273 m and 513 m for the rustic management
Table 1
List of pollinator species recorded during observations made at coffee plantations with the three management systems considered in this study
Order/family Species Management system
Rustic Commercial polyculture Specialized shade Sun
Hymenoptera/Apidae Apis mellifera L. 417 467 557 411
Plebeia frontalis Friese 1 0 1 0
Scaptotrigona mexicana Gue rin 0 0 3 0
T. (Trigona) nigerrima Cresson 2 0 2 0
T. (Trigona) corvina Cockerell 30 6 0 0
Ceratina sp. 6 9 0 0
Hymenoptera/Halictidae Augochlora sp. 6 0 0 0
Hymenoptera/Vespidae Polistinae sp. 1 3 8 0 7
Polistinae sp. 2 5 17 0 0
Diptera Syrphidae sp. 1 15 10 0 0
Syrphidae sp. 2 0 14 0 0
Syrphidae sp. 3 4 8 0 3
Calliphoridae 0 8 0 0
Bibionidae 3 8 0 5
Coleoptera/Melolonthidae Macrodactylus fulvescens Bates 5 3 0 21
Total number of individuals 497 558 563 447
Total species richness 12 11 4 5
All pollinator species were insects. The table indicates the abundance of each species at each management system.
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system, 2336 m and 3285 m for the commercial polyculture
system, 981 m and 1561 m for the specialized shaded system, and
154 mand 236 mfor the full sun exposed plantations. However, for
all management systems, neither species richness (goodness of t
test ANOVA: F
(7,8)
= 2.815; p = 0.085; R
2
= 0.391) nor the Shannon-
Wiener diversity index (goodness of t test ANOVA: F
(7,8)
= 1.551;
p = 0.724; R
2
= 0.161) were related to the distance to the closest
patch of native forest (relationships not shown).
4. Discussion
Our results show that coffee management systems have an
important effect on diversity of insect pollinator communities in
Mexico. In the present study, the more structurally and oristically
complex rustic shaded and commercial polyculture systems
showed higher species richness while the other two systems
(specialized-shaded plantations and sun plantations) harbored
very low numbers of species of pollinators. Few studies have
focused on the relationships between land-use intensity and
pollinator diversity. For instance, Klein et al. (2002) found that
land-use intensity was negatively correlated with the number of
species of social bees and there was no correlation with the
number of species of solitary bees. In our case, the results show
that the management system not only affects the number of
pollinator species, but also seems to have an impact on the species
abundance distributions, which was reected in the Shannon-
Wiener diversity index. Other authors usually do not include in
their analysis these measures of diversity or species dominance
indexes (Klein et al., 2002; Ricketts, 2004). Nevertheless, our study
suggests that such measures should also be included in further
studies.
The fact that there is a difference in pollinator diversity
between rustic shaded and commercial polyculture plantations,
on the one hand, and specialized shaded and sun systems, on the
other hand, indicates that light intensity may not be a good
predictor of pollinator community attributes in coffee planta-
tions. Indeed, specialized shaded plantations displayed the lowest
species richness, the lowest diversity and the highest values for
species dominance, and were statistically indistinguishable in
these aspects from sun coffee. These results concur with previous
Fig. 1. Average values (95% condence intervals) of pollinator species richness (A),
Shannon-Wiener diversity index (B) and species dominance (C) estimated at each
sampling size for the rustic (solid circles), commercial polyculture (empty circles),
specialized shaded coffee (solid triangles) and the sun coffee systems (empty
triangles). Signicant differences were assumed if 95% condence intervals did not
overlap between management systems at a given number of individuals.
Fig. 2. Mean fruit set ratios (95% condence intervals) from the pollination
experiment for each combination between management systems (rustic, commercial
polyculture, specialized shaded coffee and sun coffee) and pollination treatments
(open pollination: solid bars; pollinator exclusion: empty bars). Signicant differences
between means are indicated with different letters (post hoc Tukeys test critical
a = 0.05).
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studies on coffee pollinators in Tropical America which have also
found that honey bees (A. mellifera) are the most abundant
pollinators found on coffee owers (Roubik, 2002a,b; Ricketts,
2004), in spite of the species richness observed. However, none of
these studies focused on the inuence of management systems on
species richness or abundance of coffee pollinators. On the other
hand, we found a lownumber of ower-visiting species (between
5 and 12, depending on the management system), seven of which
were bees (see Table 1). Similarly, in a recent study conducted in
Chiapas, Mexico, Philpott et al. (2006) found a maximum of 14
species of ower-visiting insects, ve of which were bees. This
contrasts with the situation of more equatorial coffee plantations;
for instance, Roubik (2002a) found22oral visitors incoffee farms
in Panama, 21 of which were bees; Klein et al., 2003b found 29 bee
species in coffee farms in Indonesia; Ricketts (2004) found 40
morphospecies of bees visiting coffee owers in Costa Rica;
Veddeler et al. (2008) found 29 morphospecies of bees visiting
coffee owers in Ecuador. The low number of bees detected in
Mexican plantations, as is our case, may also be related with the
response of bees to the loss of natural and semi-natural habitats
(reviewed in Winfree et al., 2008), where bee abundance and/or
species richness decreases with increasing isolation from natural
habitat patches (Aizen and Feinsinger, 1994; Kremen et al., 2002;
Klein et al., 2003a,b; Ricketts, 2004; Chacoff and Aizen, 2006).
Fruit set was higher for open pollinated owers in the less
intensively managed systems (rustic shaded and commercial
polyculture) but not for the intensively managed systems. This
differencecouldberelatedwiththelownumber of pollinator species
found in these management systems and not to low abundance of
pollinators, because the total number of pollinators recorded in the
specialized shade coffee sites was, in fact, higher than in any of the
other management systems. This nding is in agreement with the
results of Klein et al. (2003b) for highland coffee (Coffea arabica) in
Indonesia, but differs from ndings by Klein et al. (2003c) for
lowland coffee (Coffea canephora), where both diversity and
abundance of ower visiting bees increased fruit set. Indeed,
positive relationships between species diversity (measured as
species richness or Shannon-Wiener index) and fruit set in open
pollinated owers were found in three of the management systems
studied, while a negative correlation was detectedinthe specialized
shade coffee sites. This negative correlation could be an effect of the
high abundance of honey bee workers, which may outcompete
insects of other species when collecting oral resources (competi-
tionby exploitation). Honey bees are mass-recruiters, performrapid
visits to owers, and harvest pollen almost exclusively from coffee
during the major owering periods of this plant (Roubik, 2002a,b),
indicating that that there is potential exclusion of other pollen-
collecting insects (social and solitary bees), and they probably
deplete owers of pollen before other insects have the opportunity
to visit the owers to collect pollen.
Contrary to previous studies (Klein et al., 2003b; Ricketts, 2004),
we found that neither species richness nor the Shannon-Wiener
diversity index were related to the distance to the closest patch of
native forest. The most abundant oral visitors found in our study
are managed species (like A. mellifera in hives), species that do not
depend on natural vegetation for nesting (like feral colonies of A.
mellifera), stingless bees adapted to nest in man-made structures
(like S. mexicana) or on branches of cultivated trees (like T. corvina
and the polistine paper wasps). This may also explain the low
species richness found for all the sites, because only species that
can nest and reproduce under disturbed conditions will be found.
In summary, our results suggest that diversity of insect
pollinators can be inuenced by the management system applied
by farmers, and that such effects may have strong consequences on
coffee fruit production. Hence, management measures that favor
pollinator diversity could result in increased farmproductivity and
will enhance biodiversity conservation in coffee growing regions.
In this way, we suggest that an open communication between
ecologists and farmers, like the one already established as a result
of the Proyecto Biocafe , may benet the development of rural
areas of Mexico.
Acknowledgments
We wish to thank Santiago Mario Va zquez Torres, from the
Instituto de Investigaciones Biolo gicas, Universidad Veracruzana
for letting us use a vehicle during the eld season; the coffee
plantation owners and managers for permitting us to include their
plantations in our study: Jorge A. Mu ller Grohmann, Sergio and
Francisco de la Vequia Bernardi, Rau l Monge Villalobos and
Fig. 3. Relationships between fruit set ratio and pollinator species richness (A) and pollinator species diversity (B) across the four management systems of coffee plantations
considered in this study: rustic (solid circles-solid line), commercial polyculture (empty circles-doted line) specialized shaded coffee (solid triangles-long dashed line) and
sun coffee (empty triangles-short dashed line).
C.H. Vergara, E.I. Badano / Agriculture, Ecosystems and Environment xxx (2008) xxxxxx 6
G Model
AGEE-3265; No of Pages 7
Please cite this article in press as: Vergara, C.H., Badano, E.I., Pollinator diversity increases fruit production in Mexican coffee
plantations: The importance of rustic management systems. Agric Ecosyst Environ (2008), doi:10.1016/j.agee.2008.08.001
Dionisio Pe rez J; Jessica Contreras, Renata Ferrari, Gabriela
Gutierrez-Zamora, Jovita Paredes and Ivette Macouzet helped
with eld work and data collection. This study was supported by a
grant from Mexicos Environmental Ministry (SEMARNAT-CON-
ACyT 2002-C01-0194) to CV. Two anonymous reviewers con-
tributed to improving the original manuscript.
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