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Pollinator diversity increases fruit production in Mexican coffee plantations: The importance of rustic management systems

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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 influenced by the management system applied by farmers, and that such effects may have strong consequences on coffee fruit production.
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UNCORRECTED PROOF
Pollinator diversity increases fruit production in Mexican coffee plantations:
The importance of rustic management systems
Carlos H. Vergara *, Ernesto I. Badano
Departamento de Ciencias Quı
´mico Biolo
´gicas, Escuela de Ingenierı
´a y Ciencias, Universidad de las Ame
´ricas 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 flowering 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
producefruitsandseeds(McGregor, 1976), and these pollina-
tion 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
efficiency 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 agroecosys-
tems may also depend, among other factors, on the population
dynamics (e.g., temporal variability in abundance) of the
pollinator species, pollination efficiency 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).
Mexicoistheworlds5thproducerofcoffeeandthe3rd
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
flow associated with coffee blooming (Labougle and Zozaya,
1986).
Agriculture, Ecosystems and Environment xxx (2008) xxx–xxx
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ARTICLE INFO
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
ABSTRACT
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 where 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 pro duction 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 influenced by the management system applied by farmers, and that such effects may have strong
consequences on coffee fruit production.
ß2008 Published by Elsevier B.V.
* Corresponding author. Tel.: +52 222 229 2415; fax: +52 222 229 2419.
E-mail address: carlosh.vergara@udlap.mx (C.H. Vergara).
G Model
AGEE 3265 1–7
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
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment
journal homepage: www.elsevier.com/locate/agee
0167-8809/$ – see front matter ß2008 Published by Elsevier B.V.
doi:10.1016/j.agee.2008.08.001
UNCORRECTED PROOF
Coffee (Coffea arabica L.) is a self-compatible species, which may
or may not benefit 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). Then, 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 reflecting both the impact of species
richness and the distribution of abundances of the different species
(e.g., the Shannon-Wiener’s index or the Simpson’s index).
Moreover, a diversity of management systems have been identified
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) identified five 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 vegetation of 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 shaded and soil
nitrification; (5) sun coffee, where forest is removed are coffee
plants are directly exposed to sun without vegetation cover.
Gordon et al. (2006) proposed modifications to this system of
classification 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 influence of
management systems on the diversity of insect pollinators and
their associated consequences for coffee production. We specifi-
cally 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 influence 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 flowering 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 classification 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
flowering coffee plant to each point. However, because coffee
flowers usually remain open for 2days but are attractive to
pollinators only during the fist day (Free, 1993), we repeated this
procedure as many times as necessary until founding four plants
with recently open flowers. 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 first 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
considered as pollinators those floral visitors that made contact
with the sexual parts of the flower, including species of Trigona
subgenus Trigona (traditionally considered as floral robbers) that
were collecting nectar or pollen legitimally. All pollinators were
identified 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
system were 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 Dis calculated from Nto 1 individuals.
In our rarefaction analyses, values of S,H
0
and Dwere computed
1000 times for each value of n. After resampling 1000 times the
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C.H. Vergara, E.I. Badano / Agriculture, Ecosystems and Environment xxx (2008) xxx–xxx
2
G Model
AGEE 3265 1–7
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
UNCORRECTED PROOF
value of Sfor each value of n, these 1000 values were averaged to
estimate the mean species richness at each sampling size. The
Shannon-Wiener index for each of the 1000 resamples of size nwas
calculated using natural logarithms as H
0
=
S
p
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 nwere 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 Das the number of
individuals included in the resamples decreases from Nto 1, we
constructed rarefaction curves by plotting the average values of S,
H
0
and Dagainst their respective value of n. Further, to assess
statistical differences in pollinator diversity among management
systems, we calculated the 95% confidence intervals for each
community attribute at each value of n; significant differences
between management systems were assumed if their confidence
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 floral
visitors on the development of fruits, and to determine differences
in these effects among management systems, we made a field
pollination experiment by manipulating the access of pollinators
to flowers. We first selected four coffee plants (different from those
on which we assessed pollinator diversity) at each site by using the
same procedure described above. On each plant, we selected two
branches with floral 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
floral buds on each branch with small plastic flags. After that, one of
the branches was covered with a Nytex
1
mesh bags to exclude
floral 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 floral buds in the respective
branch and the number of developing fruits.
Statistical comparisons among combinations of management
systemspollination treatments were performed with a factorial
ANOVA. Inthis analysis, plantations wereconsidered as independent
replicates; before performing the analysis, we averaged the four
values of fruit set ratio obtained for each pollination treatment at
each plantation (rustic coffee systemopen pollination n=4;
commercial polycultureopen pollinationn= 4; specialized shaded
coffee open pollination n=4;suncoffeeopen pollination n=4;
rustic coffee system pollinator exclusion n= 4; commercial
polycultureopen pollination n=4; specialized shaded coffee
pollinator exclusion n=4;sun coffee pollinator exclusion n=
4). The Tukey’s test was used to assesspost hoc differences between
combinations of management system 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 final 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 significant 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 influenced 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 aregiven above). In the firstregression analysis,the average
fruit set ratio of the open pollination treatment obtained for each
plantation was the dependent variable, the observedspecies 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
influences 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 ArcView 3.2 (ESRI Software,
CA, USA). We later made two multiple regression analysis with
categorical variables (details on this regression analysis are given
above). In the first 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 flowers
were insects (Table 1). The highest richness of pollinator species
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C.H. Vergara, E.I. Badano / Agriculture, Ecosystems and Environment xxx (2008) xxx–xxx
3
G Model
AGEE 3265 1–7
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
UNCORRECTED PROOF
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 flowers. 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 index and species dominanceamong manage-
ment systems only included estimations up to 447 individuals (the
highest number of individuals detected in a treatment with the
lowest abundance—sun 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 significantly 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 significantly
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 significantly lower
values of species dominance than the other two management
systems after 200 individuals were included in rarefaction curves
(Fig. 1C). The highervalues 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 significant 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 significant effect of the interaction between manage-
ment 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 systems pollination
treatments (Fig. 2). Fruit set ratios did not differ among the other
combinations of management systems pollination treatments.
A positive relationship was indicated between fruit retention
rate and fruit set rate of the open pollination treatment (goodness
of fit 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 flowers and both, pollinator
species richness (goodness of fit test ANOVA: F
(7,8)
= 17.153;
p<0.001; R
2
= 0.938) and pollinator species diversity (goodness of
fit 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
system, 2336 m and 3285 m for the commercial polyculture
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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. 69 0 0
Hymenoptera/Halictidae Augochlora sp. 60 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.
C.H. Vergara, E.I. Badano / Agriculture, Ecosystems and Environment xxx (2008) xxx–xxx
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UNCORRECTED PROOF
system, 981 m and 1561 m for the specialized shaded system, and
154 m and 236 m for the full sun exposed plantations. However, for
all management systems, neither species richness (goodness of fit
test ANOVA: F
(7,8)
= 2.815; p= 0.085; R
2
= 0.391) nor the Shannon-
Wiener diversity index (goodness of fit 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 floristically
complex rustic shaded and commercial polyculture systems
showed higher species richness while the other two systems
(specialized-shade 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 reflected 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 plantations. 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
studies on coffee pollinators in Tropical America which have also
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Fig. 1. Average values (
95% confidence 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). Significant differences were assumed if 95% confidence intervals did not
overlap between management systems at a given number of individuals.
Fig. 2. Mean fruit set ratios (
95% confidence 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). Significant differences
between means are indicated with different letters (post hoc Tukey’s test critical
a= 0.05).
C.H. Vergara, E.I. Badano / Agriculture, Ecosystems and Environment xxx (2008) xxx–xxx
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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
UNCORRECTED PROOF
found that honey bees (A. mellifera) are the most abundant
pollinators found on coffee flowers (Roubik, 2002a,b; Ricketts,
2004), in spite of the species richness observed. However, none of
these studies focused on the influence of management systems on
species richness or abundance of coffee pollinators. On the other
hand, we found a low number of flower-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 flower-visiting insects, five of which were bees. This
contrasts with the situation of more equatorial coffee plantations;
for instance, Roubik (2002a) found 22 floral visitors in coffee 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 flowers in Costa Rica;
Veddeler et al. (2008) found 29 morphospecies of bees visiting
coffee flowers 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 flowers in the less
intensively managed systems (rustic shaded and commercial
polyculture) but not for the intensively managed systems. This
difference could be related with the low number 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 finding is in
agreement with the results of Klein et al. (2003b) for highland
coffee (Coffea arabica) in Indonesia, but differs from findings by
Klein et al. (2003c) for lowland coffee (Coffea canephora), where
both diversity and abundance of flower 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 flowers were found in three of the
management systems studied, while a negative correlation was
detected in the 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 floral resources (competition by exploitation). Honey
bees are mass-recruiters, perform rapid visits to flowers, and
harvest pollen almost exclusively from coffee during the major
flowering 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 flowers of
pollen before other insects have the opportunity to visit the flowers
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 floral 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 influenced 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 farm productivity 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 benefit 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 field 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
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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) xxx–xxx
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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
UNCORRECTED PROOF
Dionisio Pe
´rez J; Jessica Contreras, Renata Ferrari, Gabriela
Gutierrez-Zamora, Jovita Paredes and Ivette Macouzet helped
with field work and data collection. This study was supported by a
grant from Mexico’s Environmental Ministry (SEMARNAT-CON-
ACyT 2002-C01-0194) to CV. Two anonymous reviewers con-
tributed to improving the original manuscript.
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plantations: The importance of rustic management systems. Agric Ecosyst Environ (2008), doi:10.1016/j.agee.2008.08.001
... Many following studies reported increases in pollinator diversity and richness as well as coffee yield in fields near forest fragments (e.g. Boreux et al., 2013;Bravo-Monroy et al., 2015;Caudill et al., 2017;De Marco and Coelho, 2004;Klein et al., 2003c;Krishnan et al., 2012;Munyuli, 2014;Ricketts et al., 2004;Saturni et al., 2016;Vergara and Badano, 2009). However, in these studies, forest was often identified on the ground according to local criteria rather than by international standards. ...
... Aristizábal and Metzger, 2019;Classen et al., 2014;Munyuli, 2014;Philpott et al., 2006). Farm management strategies, such as shading, management intensity and pesticide application are also known to impact coffee yields (Hipólito et al., 2018;Munyuli, 2014;Vergara and Badano, 2009). This information was therefore recorded as part of the data collection, if available. ...
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