Taxonomic and Functional Diversity of Flower-Visiting Insects in Coffee Crops
by
, , ,
Juan Diego Maldonado-Cepeda
1,
Jesús Hernando Gómez
1,
Pablo Benavides
1,
Juliana Jaramillo
2 and
Zulma Nancy Gil
1,* 1
Department of Entomology, National Coffee Research Center—Cenicafé, Manizales 170009, Colombia
2
Theme Lead Regenerative Agriculture, Rainforest Alliance, De Ruyterkade 6, 1013 BG Amsterdam, The Netherlands
*
Author to whom correspondence should be addressed.
Insects 2024, 15(3), 143; https://doi.org/10.3390/insects15030143
Submission received: 10 January 2024
/
Revised: 7 February 2024
/
Accepted: 16 February 2024
/
Published: 21 February 2024
(This article belongs to the Collection Insects on Pollination Ecology)
Abstract
:Simple Summary
Floral-visiting insects and pollinators play an important role in ecosystem services, and consequently, their identification and study are essential to their adequate preservation and management in crops of agricultural interest. Coffee is a worldwide commodity; however, the diversity of insects that visit its flowers has been little studied. The objective of this research was to quantify the abundance, richness, and functional diversity of coffee floral-visiting insects, especially bees. The results showed that coffee crops host a wide diversity of flower visitors, especially bees, which could be beneficial for productivity and contribute to the maintenance of plant species that accompany coffee cultivation.
Abstract
Despite the important role that flower-visiting insects play in agricultural production, none of the previous studies of coffee pollinators in Colombia have incorporated functional diversity into their analysis. Therefore, this study aimed to quantify the abundance, richness, and functional diversity of insects that visit flowers in coffee crops. Twenty-eight plots were selected among five sites in the north, center, and south of Colombia. In each plot, coffee flower insect visitors were collected and recorded on 90 trees at eight-minute intervals per tree, at three different times over three days. All sampling was carried out during two flowering events per year, over three years, resulting in a total of 1240 h of observations. Subsequently, the insects were taxonomically identified, and the number of individuals and species, as well as the diversity of the order q, were estimated. Functional diversity was also characterized in the bee community. The results: (a) 23,735 individuals belonging to 566 species were recorded; of them, 90 were bees, with the native species being the most abundant during 10:30 and 13:00 h; (b) bees formed five functional groups, with corbiculate and long-tongued non-corbiculate bees being the most abundant and occupying the largest regions of functional space; (c) potential pollinators in coffee crops are Apis mellifera, Nannotrigona gaboi, Tetragonisca angustula, Geotrigona cf. tellurica, and Partamona cf. peckolti. Coffee crops host a wide diversity of flower visitors, especially bees, which could be beneficial for productivity and contribute to the maintenance of plant species that accompany coffee cultivation.
1. Introduction
Insects form an important part of ecosystems as they provide different services, particularly pollination. According to Ollerton et al. [1], 87.5% of angiosperms are pollinated by animal vectors, most of which are insects.
For this reason, it is essential to study the taxonomic and functional diversity of flower-visiting insects. Because insect richness and density are the most important crop yield predictors [2,3], it is fundamental to study the taxonomic diversity of flower-visiting insects [2,3]. According to Klein et al. [4], there are three ways to use this information to increase crop yield: (1) random inclusion of the most efficient and effective species in pollination; (2) complementary pollination among species; and (3) facilitation, as several species could facilitate the permanence or role of others as pollinators of a given crop, and a better understanding of the taxonomic diversity of flower visitors can serve to successfully adjust the estimates of insects present in a given region or crop.
Additionally, functional diversity provides a valuable understanding of the role of species and allows the incorporation of characteristics that influence their performance and processes in the ecosystem [5]. In addition, it allows us to know the response of species to climate change [6]. Coffee is an important agricultural commodity, produced in about 80 tropical countries, with an estimated 125 million people depending on it for their livelihoods. In Colombia, coffee (Coffea arabica L., Rubiaceae) is of particular interest to researchers, mainly because of its contribution to the national economy and because it is the livelihood of almost half a million coffee-growing families nationwide [7]. Coffee, a self-pollinated plant, grows best between 1200 and 1800 m above sea level and at temperatures between 18 and 21 °C [8]. Flowers open in the morning hours and can last one or two days after being pollinated. Non-pollinated flowers can last up to five days [9].
Despite the autogamy of C. arabica, several groups of flower visitors are known to visit coffee crops [2]. Studies to identify the main flower visitors of coffee crops carried out in Brazil, Costa Rica, Ecuador, Indonesia, and Mexico revealed that social bees belonging to the tribes Meliponini and Apini were the most important in the pollination of C. arabica, in particular those of the genus Apis [9]. Moreaux et al. [10] also performed a global analysis of the value of biotic pollination in C. arabica. In the studies they reviewed, bees were found to represent an average of 70% of all recorded species and 87% of all individuals. Based on these results, bees are believed to be the main pollinators of coffee [10].
Jaramillo [11] evaluated the diversity and abundance of bees in C. arabica crops in the department of Antioquia, Colombia, and found three (Apidae, Halictidae, and Megachilidae) of the five families reported for the country, distributed in twenty genera and fifty species. Of these, 45% were solitary bees and 19% were stingless social bees from the tribe Meliponini, with the family Apidae being the most abundant. Subsequently, a second study by Cepeda et al. [12] evaluated the diversity of coffee-visiting bees in the department of Cundinamarca, Colombia. They found thirteen species of the same three families found by [11]. The family with the highest richness was Apidae, with nine species, particularly in the genus Trigona. The species representing the highest number of visits to coffee were Apis mellifera and Paratrigona eutaeniata Camargo & Moure, 1994 (Hymenoptera: Apidae) [12]. Although bees are the most abundant flower visitors in coffee, the literature reports other groups of insects, for example, species of Syrphidae (Diptera) [13,14], Hesperiidae, and Nymphalidae (Lepidoptera), Dictyoptera, and Coccinellidae (Coleoptera) [13,15], and several wasps of the Hymenoptera.
There are no known studies on functional diversity in coffee; however, several studies have been carried out on other crops. Garibaldi et al. [16] found that bee species with functional traits adjusted to the requirements of flowers were the best pollinators in 33 crops evaluated. It is also important to mention the meta-analysis carried out by Woodcock et al. [17] in canola Brassica napus L. (Brassicaceae), where the complementary pollination among species was corroborated, indicating a community presenting non-overlapping traits favors the pollination service. Considering that only a few studies have been conducted on insect diversity in C. arabica flowers and that it is important to identify which insects visit coffee flowers and the role they play within the crop, the present study focused on estimating and characterizing the taxonomic and functional diversity of flower-visiting insects in coffee crops.
2. Materials and Methods
2.1. Study Sites
This study was carried out at five sites corresponding to experiment stations of Colombia’s National Coffee Research Center (Cenicafé, its Spanish acronym), located in northern (Cesar and Santander departments), central (Caldas and Quindío departments), and southern (Cauca department) Colombia (Table 1, Figure 1).
2.2. Methodology
2.2.1. Taxonomic Diversity
Twenty-eight coffee plots of Coffea arabica var. Castillo® were selected in five locations in northern, central, and southern Colombia (Table 1). They were sampled between 2019 and 2022 as follows: two at Pueblo Bello Experiment Station, four at San Antonio Experiment Station (northern), eight at Paraguaicito Experiment Station, ten at Naranjal Experiment Station (central), and four at Manuel Mejía Experiment Station (southern). All coffee plots were grown in places exposed to the sun, except at the Pueblo Bello Experimental Station, where coffee was grown in the shade. In Colombia, coffee plots are surrounded by areas of natural vegetation, patches of secondary forest, and other crops (for example, see Figure 2).
In each coffee plot, ninety coffee plants were randomly selected, and for three consecutive days, all flower-visiting insects were collected from thirty plants per day of flowering. During the samplings, flower-visiting insects were observed and recorded at three different times (7:00 to 9:30, 10:30 to 13:00, and 14:00 to 16:30 h) at 8-min intervals for each plant, totaling 1240 h of observation. No captures were made for Apis mellifera L. (Hymenoptera: Apidae), given its abundance and ease of identification directly from the field.
The collected insects were placed and tagged in glass vials. Bees were dry-preserved to analyze pollen load, but other taxonomic groups were preserved in 76% ethanol. All specimens were transferred to Cenicafe’s Entomology Laboratory and identified under a Nikon SMZ 1500 stereomicroscope (Nikon Instruments Inc., Melville, NY 11747-3064, USA), following the taxonomic keys proposed by [19,20,21,22]. With the registered information, for each study site and sampling time, the number of species and the number of individuals per species were determined.
2.2.2. Functional Diversity
The functional diversity of the bee community was characterized. To do so, soft effector functional traits, focused on the pollination of C. arabica, were determined for each species. Several traits were adapted from those already proposed by [17,23,24], while others were obtained from the information recorded in this study. Table 2 describes the selected traits, which are nesting habit, degree of sociability, size, stigmal contact, location of pollen load structure, type of tongue, abundance from 7:00 to 9:30, 10:30 to 13:00, and 14:00 to 16:30 h. A matrix of functional traits was constructed for all species recorded in the field using the information obtained (Table 2).
The pollen load was also analyzed for the most abundant bee species. Species with an abundance greater than 5% were selected at each study site. Twenty individuals of each species were collected, and a sample of body pollen was taken from each using fuchsine-stained glycerinated gelatin (5%). For pollen identification, each sample was then placed on slides and analyzed. A palynology collection was established with pollen grains of arabica coffee. Samples were quantified until 300 pollen grains were obtained per slide, following the methodology proposed by [25,26]. The number of coffee pollen grains present in the sample was quantified for each site. The data obtained were used in the equation to estimate pollinator importance.
2.2.3. Statistical Analyses
Taxonomic Diversity
For each study site and sampling time, the number of species and the number of individuals per species were determined. The species composition and abundance were described for each order. Chao 1 and abundance-based coverage estimator (ACE) estimates were obtained at a general level and for each sampling site for all flower-visiting insects as well as for the bee community using the statistical program EstimateS 9.1.0 [27]. Diversity profiles were estimated at a general level and per sampling site based on the matrix of abundances obtained in this study using the following indices:
q = 0: richness; q = 1: exponential of the Shannon–Wiener diversity index; q = 2: the inverse of the Simpson concentration.
The statistical packages iNEXT and SpadeR [28] were used to run the indices:
where
qD = diversity of order q;
S = number of species;
pi = relative abundance (proportional abundance) of the ith species;
q = order of diversity (defines sensitivity to relative abundances of the species.
A descriptive analysis of the distribution of abundances at different sampling times was carried out.
Functional Diversity
Functional groups were defined for the bee community using a cluster analysis defined by Ward’s method. The functional space was graphed based on a distance matrix using non-metric multidimensional scaling.
The Gower distance matrix was constructed, and the following indices were estimated based on this matrix:
FDis = functional dispersion; FEve = functional evenness; FDiv = functional divergence. These indices were calculated using the FD-R package. The pollinator importance value (PIV) was estimated for each sampling site and bee species selected.
where VR = visit rate (relative abundance of the species with respect to the total sample); PCC = pollen-carrying capacity (proportion of C. arabica pollen found in the species with respect to all sampled bee species); C = flower constancy (mean proportion of C. arabica pollen per each species); PE = pollinator effectiveness (value assigned between 0 and 1, taking into consideration insect size and behavior within flowers, between flowers, and between plants).
PIV = VR × PCC × C × PE
3. Results
3.1. Taxonomic Diversity
A total of 23,735 individuals were recorded, distributed in 566 species, 105 genera, 84 families, and 10 orders (Coleoptera, Dermaptera, Dictyoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Neuroptera, Orthoptera, and Thysanoptera).
The Hymenoptera presented the highest abundance (22,528 individuals) and richness (215 species). Bees were the most abundant, with 20,838 individuals, belonging to 90 species of 4 of the 5 families present in Colombia Apidae, Halictidae, Megachilidae, and Colletidae, with the first two being the most representative in terms of number of species and individuals.
In the two coffee plots sampled at Pueblo Bello Experiment Station over a single flowering period for the main harvest, a total of 3834 individuals were recorded during the 90 h sampling effort; these insects belonged to 70 species, 15 families, and 5 orders (Coleoptera, Dermaptera, Diptera, Hemiptera, and Hymenoptera). The most abundant species were A. mellifera (2858 individuals), Scaptotrigona sp. 1 (180 individuals), Tetragonisca angustula (Latreille, 1811) (167 individuals), Nannotrigona gaboi Jaramillo, Ospina-Torres & Gonzalez, 2019 (160 individuals) (Apidae), Ornidia obesa (Fabricius, 1775) (Syrphidae) (8 individuals), and Mordellidae sp. 3 (Coleoptera) with 10 individuals.
Four plots were sampled at San Antonio Experiment Station during two flowering periods for the main harvest, and a total of 8359 individuals were recorded during the 180 h sampling effort. These insects belonged to 141 species, 37 families, and 7 orders (Coleoptera, Dermaptera, Diptera, Hemiptera, Hymenoptera, Neuroptera, and Thysanoptera). The more abundant species were A. mellifera (6126 individuals), Geotrigona cf. tellurica (1441 individuals) (Hymenoptera: Apidae), Curculionidae sp. 5 (Coleoptera) with 91 individuals, Palpada sp. 5 (Diptera: Syrphidae) with 22 individuals, and Miridae (Hemiptera) with six individuals.
Eight plots were sampled at Paraguaicito Experiment Station during two flowering periods for the main harvest and two for the mid-crop harvest, although several samplings were not carried out due to rains. A total of 4514 individuals were recorded during the 340 h sampling effort. These insects belonged to 233 species, 54 families, and 7 orders (Coleoptera, Diptera, Dyctioptera, Hemiptera, Hymenoptera, Lepidoptera, and Thysanoptera). The more abundant species were A. mellifera (188 individuals), Lasioglossum sp. 1, with 50 individuals (Hymenoptera: Apidae), Dorymyrmex brunneus Forel, 1908 (217 individuals), Dorymyrmex biconis Forel, 1912 (Formicidae) (148 individuals) (Hymenoptera: Formicidae), Bibionidae sp. 1 (27 individuals), Diptera sp. 2 (25 individuals), Staphylinidae sp. 5 (Coleoptera) with 15 individuals, and Hesperiidae (Lepidoptera) with 16 individuals.
Ten plots were sampled at the Naranjal Experiment Station during two flowering periods for the main harvest and two for the mid-crop harvest; a total of 4748 individuals were recorded during 450 h of sampling effort; these insects belonged to 288 species, 58 families, and 8 orders (Coleoptera, Dermaptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Neuroptera, and Orthoptera). The more abundant species were corbiculated bees A. mellifera (1938 individuals), T. angustula (725 individuals), Trigonisca cf. pediculana (185 individuals), Partamona cf. peckolti (184 individuals), Nannotrigona tristella Cockerell, 1922 (138 individuals) (Hymenoptera: Apidae), Bibionidae sp. 2 (Diptera) with 17 individuals, and Staphylinidae sp. 2 (Coleoptera) presenting 33 individuals, considered outstanding.
Four plots were sampled at the Manuel Mejía Experiment Station during two flowering periods for the main harvest. A total of 2232 individuals were recorded during the 180 h sampling effort; these insects belonged to 99 species, 36 families, and 7 orders (Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Orthoptera, and Thysanoptera). The more abundant species are corbiculated bees A. mellifera (1546 individuals), Partamona cf. peckolti (159 individuals), and T. angustula (157 individuals) (Hymenoptera: Apidae), Astylus lebasi Champion, 1918 (Melyridae) (21 individuals), Staphylinidae sp. 1 (26 individuals) (Coleoptera), and Ornidia obesa (Diptera: Syrphidae) with 10 individuals.
The number of species observed at all five sites was 566, which was lower than that estimated with two richness indicators: Chao1 and ACE (Table 3). According to the Chao1 richness estimator, the total number of species should be 874.9; in other words, the number of recorded species represents 64.7% of the expected value. According to ACE, the number should be 921.6, which means that the number of recorded species represents 61.4% of what was expected (Table 3). The number of species with a single individual, referred to as singletons, was 254.
Sampling coverage represents the fraction of total abundances represented in the sample. Although a relatively large fraction of species is missing based on study results, a general value of 0.989 is an indication that very few total individuals are still pending recording. Similarly, the sample coverage for each site was greater than 0.96 in all cases (Table 3), which suggests that it is unlikely that an individual collected in any future sampling will correspond to an unrecorded species.
For the bee community at a general level, the total number of species observed was 90, which is lower than that estimated with the Chao1 and ACE richness indicators (Table 4). The sampling of bees also presented a lower number of singletons (29), greater coverage, and a higher percentage of species represented in the sample (Table 4), as compared with the general analysis of flower visitors. Additionally, the confidence interval of the ACE estimator and that of the observed species overlap at all sites, but not in the general data, meaning that the observed value and the estimate value could be the same for each site.
The diversity of order q determines the influence that either common or rare species can have on the measure of diversity. The study results showed that, both at a general level and at the evaluation sites, the curve presents a steep slope with an increasing dominance of certain species (Figure 3). Hence, most of the species found at any of the evaluation sites were rare, and, at a general level, 357 species were singletons or doubletons, and 493 species did not exceed 10 recorded individuals. Four values conform to this measure of biodiversity: q = 0, when the value obtained is simply equivalent to species richness; q < 1, when rare species are overvalued; q = 1, when all species are included with a weight exactly proportional to their abundance in the community; q > 1, when more importance is given to abundant species [29].
The distribution of abundances in the different sampling times indicated that A. mellifera as well as insect species that do not correspond to the bee community presented a uniform distribution of abundance throughout the day, whereas native bees are more abundant in the time span from 10:30 to 13:00 h (Figure 4).
3.2. Functional Diversity
Five functional groups were obtained for the community of flower-visiting bees in coffee using a cluster analysis defined by Ward’s method (Figure 5). Based on the distance matrix, the group of corbiculate bees and non-corbiculate long-tongued bees occupied larger regions of the functional space and also presented greater abundances, whereas the functional groups formed by medium- and small-sized Halictidae and most of Augochlora sp.l individuals occupied small regions of the functional space (Figure 5).
The indices obtained using the Gower distance matrix showed that functional evenness (FEve), which describes the distribution of abundances within the functional space of the bee community, for the five sites presented values between 0.37 and 0.45 with an overall functional evenness of 0.41. This value is considered average because functional diversity can assume values between 0 and 1, where 1 is when all species are equally represented, and values are closer to 0 in the presence of species with very high-density values or of several high-abundance species whose functional values are very similar (Table 5).
Functional divergence (FDiv) presented values ranging between 0.93 and ~1.00 and a general value of 0.99. This index ranges between 0 and 1 and measures the distribution of the abundances of species within the functional space, i.e., the most abundant species are distributed in different regions of the functional space (Table 5, Figure 5).
The functional dispersion (FDis) for the entire bee community was 0.19, and for sites, it ranged between 0.10 and 0.27 (Table 5). This index estimates the average distance of the species from the centroid of the community, which is influenced by the abundances of each species. This index presents a lower limit of 0 and has no upper limit. Therefore, its values can be compared only with those of other studies; however, the values obtained across sites were similar.
Bee species presenting abundances greater than 5% were selected to analyze pollen load, several of which are common across study sites (Table 6, Figure 6).
The pollination importance value (PIV) estimated for each species was found to depend on the collection site. However, for most of the species evaluated, the C value was greater than 0.9 and the PCC was greater than 0.3. The species presenting the lowest C values were Lasioglossum spp. and Partamona cf. peckolti (Table 6).
Species such as A. mellifera presented a PE score of 1, which was the highest score, attributable to its behavior when visiting the coffee flower, making frequent contact with stigma and stamens when looking for resources other than pollen. Bee species such as Partamona cf. peckolti, Scaptotrigona sp. 1, T. angustula at most sites, and Geotrigona cf. tellurica presented values higher than 0.92 (Table 6), considered high PE values. Meanwhile, T. angustula at the Naranjal Experiment Station presented a value of 0.67 and Lasioglossum spp. one of 0.65, given that no frequent stigma contact was observed and bees did not touch the stamens when looking for resources other than pollen.
Apis mellifera presented the highest relative abundance of species (VR) value, ranging between 70.62 and 73.62. The VR is important because it is one of the measurements that reduces the PIV value for infrequent flower visitors because, as mentioned above, the dominance of a few species makes this value very low for the others. Apis mellifera presented the highest PIV, scoring 59.13 at the Paraguaicito Experiment Station, while Lasioglossum spp. presented the lowest, 0.11, at the same site (Table 6).
4. Discussion
This study reported 566 species of flower-visiting insects in coffee crops, 90 of which correspond to bee species (Appendix A, Table A1). To date, this is the highest number of species of bees and other flower-visiting insects in coffee reported by any study in the literature (Appendix B, Table A2).
For the first time, bees of the genera Agapostemon, Augochloropsis, Augochlorella, Caenohalictus, Habralictus, Pereirapis, Pseudaugochlora, and Ptiloglossa are reported as coffee flower visitors, as well as the species Bombus pauloensis Friese, 1912, Bombus melaleucus Handlirsch, 1888, Eulaema cingulate (Fabricius, 1804), Geotrigona kaba Gonzalez & Sepúlveda, 2007, Geotricona cf. tellurica, Nannotrigona gaboi, N. pilosa Jaramillo, Ospina & Gonzalez, 2019, N. tristella (Cockerell 1922), Nasutopedia sp., Paratrigona opaca (Cockerell, 1917), Tetragona perangulata (Cockerell, 1917), Trigona fulviventris Guérin-Méneville, 1844, Trigonisca cf. mepecheu, and Trigonisca cf. pediculana (Hymenoptera: Apidae), the genera Agelaia, Angiopolybia, Epipona, Pachynoderus, Parachartergus, Polistes, Polybia, Protopolybia, and Synoeca (Hymenoptera: Vespidae), Ornidia major (Curran 1930), and Pseudodoros clavatus (Fabricius, 1794) (Diptera) were also identified here, which complement the results of [9].
The present study reports a greater richness of coffee flower visitors as compared with previous studies. However, based on the Chao1 and ACE estimators, there are still between 35.3 and 38.6% of species to be collected. Study sites presenting the lowest species richness were Pueblo Bello, San Antonio, and Manuel Mejía experiment stations. The sampling coverage for all sites was greater than 97%, which means that there are only a few individuals pending collection. Therefore, the sampling coverage of this study is considered complete; according to [30], the coverage is calculated considering the abundances and is defined as the probability that the next individual collected belongs to a species already represented in the sample. Therefore, the probability of finding coffee flower-visiting individuals of species not represented in the sample is low.
The reason why sampling coverage is considered complete, that is, with values close to 1, is because only a few species were hyper-abundant, making other species considered rare. Consequently, 254 singletons were found in the general sample, while for each of the study sites, it ranged between 36 and 145. Coleoptera, Diptera, and Hemiptera were those with the greatest number of singletons; in many cases, the species of these orders do not include flowers in their diets to feed their young [31]. It could also be attributed to the fact that the abundance and richness of Coleoptera and Lepidoptera were not fully sampled, according to Knop et al. [32], these flower visitors are more active at night. The representation of these groups was also low in studies carried out by [13,33,34,35].
The bee community was better represented than the general insect community. The percentage of species represented in the sample ranged between 47.7 and 88.9%, depending on the estimator used and the study site. The sampling coverage was between 0.995 and 0.999, and the number of species represented by a single individual was 29, which is equivalent to 32.2% (Table 2). In most studies conducted on flower visitors to coffee and other crops, bees were the most abundant, attributable to their life history traits and the role they play as pollinators [22,36].
In most of the studies that have evaluated flower visitors in the coffee species C. arabica and C. canephora, bees were the most abundant insect species, particularly social bees of the tribes Apini and Meliponini [9]. This agrees with the results of this study, where A. mellifera was the most abundant species, followed by species of the genera Geotrigona, Nannotrigona, Partamona, Scaptotrigona, and Tetragonisca. In the case of social bees, abundance may be related to the availability of a specific flower resource because these bees preferably forage in the most abundant flower resources due to the use of a recruitment system [37]. In the study carried out by Bänsch et al. [38] on strawberries, results indicated that solitary bees may be excluded from concentrated blooms because social bees compete for this type of resource. Solitary bees are easier to use in crops with scattered blooms, which explains why social bees were the most abundant species in all sites sampled in this study because coffee is characterized by having few abundant blooms per year, depending on the region.
The diversity profiles of the order q (Figure 2) indicate that only a few species have high dominance in the community of flower-visiting insects in coffee, which implies a low functional evenness. This behavior could have implications for the community because, according to Hillebrand et al. [39], the high dominance of species can reduce ecosystem function as it not only reduces the stability of the pollination process but also makes the ecosystem more vulnerable to invasion by alien species.
Klein et al. [40] found that pollination in coffee depends mainly on the diversity of flower visitors, and, according to Moritz et al. [41], although A. mellifera seems to have no effect on species’ richness at the local or regional levels, it could be responsible for species dominance in the evaluated communities. Social bees could therefore be of interest for the pollination of coffee. To enhance the contribution to coffee production, the strategy forward should focus on increasing the abundance not only of social species other than A. mellifera but also that of solitary bees to better conserve the ecosystems surrounding coffee plantations.
The results from this study showed that native bee species are most abundant between 10:30 and 13:00, whereas the abundance of A. mellifera and insect species of the other taxonomic groups was similar during the three sampling periods (7:00 to 9:30, 10:30 to 13:00, and 14:00 to 16:30). According to [32,42,43], the activity of daytime flower visitors is determined by variables such as sunlight and temperature, not by a specific hour.
The functional evenness (FEve) value for the bee community, both at a general level and for the study sites, was around 0.4, which suggests that species of the flower-visiting bee community in coffee are unevenly distributed in the functional space (Figure 5). Because several species present overlapping traits and there are empty spaces between them, these empty spaces are referred to as unoccupied niches, which could be inhabited by other flower-visiting insects or by invasive species in coffee crops. Empty spaces also imply that the ecosystem function is not productive or reliable because, in the event of a disturbance, hyperabundant species (those currently responsible for most of the pollination in coffee) could be affected [44,45].
On the other hand, functional divergence presented values > 0.9, indicating that the most abundant species, regardless of the locality, presented non-overlapping features, meaning that these species occupy different regions of the functional space [46]. Therefore, the most abundant bee species found visiting coffee flowers are dissimilar and compete weakly with each other. Taking Paraguaicito Experiment Station as an example, at this study site, the most abundant species were A. mellifera, Trigonisca cf. pediculana, and several species of the genus Lasioglossum, which showed differences in nesting habits, size, pollen-carrying structure, and times of greatest abundance. This is important for pollination in coffee crops because it explains why coffee flower visitors, some of which are pollinators, present non-overlapping traits and why the pollination function could be resistant to disturbances [47].
Functional dispersion is relevant in different crops. Martins et al. [48], for example, found that, in apples, greater functional dispersion translated into a higher fruit set. This could also be the case with coffee. The present study found functional dispersion values that ranged between 0.10 and 0.27, with a mean of 0.17, which is considered medium-low. In studies carried out by [48,49] in areas with different degrees of grazing intensity, functional dispersion values ranged between 0.10 and 0.45 for the first study and between 0.23 and 0.32 for the second, which means that fruit set in coffee could increase with increasing functional dispersion. Consequently, Gómez et al. [50] found that the C. arabica species, despite being a self-pollinated plant, benefits from the presence of flower-visiting insects in the crop, which contributed 16.3% to berry set, 26.9% to yield, and 30.6% to the physical quality of coffee.
This study did not address the functional diversity of the entire community of flower-visiting insects in coffee, only that of the bee community. As a result, empty spaces appeared when the functional space was graphed, the hypothesis being that these could be occupied by insects similar to bees but with different traits, and were therefore not taken into account in the analysis.
The species A. mellifera presented the highest abundance as well as the highest PCC, with values between 0.33 and 0.90 depending on the study site. It also presented a high C value (0.94–0.98) and, as a result, the highest PIV as well. According to Roubik [15], A. mellifera is probably one of the best pollinators in coffee crops, which could be because this species is native to Africa, the center of origin of C. arabica. However, native bees such as N. gaboi, T. angustula, Geotrigona cf. tellurica, and Partamona cf. peckolti, despite being small bees, presented not only higher PCC values but also greater C constancy. However, their PIV was lower not only because they presented lower abundances than A. mellifera but also because their PE value was lower as they presented little stigma contact.
This leads us to understand that, although an individual carries large and exclusive amounts of pollen, this does not necessarily make it a good pollinator, because if it comes into contact with male structures and not female structures, it will not fulfill the pollination function. Although it is important to define the entire community of flower visitors to avoid biases [51], it is equally important to directly measure pollen deposition in stigmas and fruit sets for each species, as pollen load or percentage of visits are not necessarily good indicators of pollination efficiency [52]. Despite the above, these secondary species have the potential to be good pollinators for coffee crops and should be addressed in future studies.
5. Conclusions
In Colombia, coffee flowers are visited by 566 insect species from different taxonomic groups, but this number could be even higher according to the Chao1 and ACE estimators. The group of bees was the most abundant and diverse, with 89 native species being recorded, all natural inhabitants of Colombian coffee ecosystems and distributed throughout the country. These bees represent 16% of the bee species described for Colombia. This study reports eight genera of bees that had not been previously reported in coffee crops, as well as 14 species of the family Apidae. It is also the first study to address the functional diversity of bees visiting coffee crops, and the PIV is determined to select potential pollinator species for C. arabica.
Based on functional diversity indices, the community of flower-visiting bees in coffee crops may have low resistance to disturbance and temporary instability. The performance of the pollination service could also be better.
When implementing a strategy to increase coffee production using insect-based pollination services, the approach should aim at (1) increasing the abundances of the most efficient and effective species in pollination, such as the native social bees N. gaboi, T. angustula, Geotrigona cf. tellurica, and Partamona cf. peckolti. (2) strengthen the complementary between species favoring the abundance of the functional groups of the small and medium-sized Halictidae, and (3) strengthen facilitation through the presence of Diptera (Syrphidae) that contribute to maintaining floristic diversity, as several species could facilitate the permanence or role of others as pollinators of a given crop, and a better understanding of the taxonomic diversity of flower visitors can serve to successfully adjust the estimates of insects present in a given region or crop.
Crop management strategies should be proposed that integrate pollinators as a major component and focus on balancing abundances for several bee species, considering the hours of greatest activity (between 10:30 and 13:00).
Future studies should also address the direct measurement of pollination, such as pollen deposition on stigmas and fruit set, in species identified with the greatest potential to serve as pollinators in coffee crops.
Author Contributions
Fieldwork, data collection and analysis, manuscript writing and revision, J.D.M.-C.; data collection and analysis, J.H.G.; study design, methodological adjustments, data analysis, manuscript writing, P.B.; experimental design, managed project funding, and revised the final version of the manuscript, J.J.; resource management, research coordination, conceptualization, methodology, fieldwork, data collection and analysis, manuscript writing and revision Z.N.G. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by the collaborative research agreement CN-2017-1336 subscribed between Bayer AG, Germany (financing entity) and National Coffee Research Center-Cenicafé.
Data Availability Statement
All data are contained within the article or Appendix A.
Acknowledgments
This study was part of the project “Evaluating flower-visiting insects in coffee in Colombia, with emphasis on bees, and their effect on yield and quality”, under the collaborative research agreement CN-2017-1336 subscribed between Bayer AG, Germany (financing entity) and National Coffee Research Center—Cenicafé. We would like to thank Luis Eduardo Escobar for his support in experimental set up and data collection. Our thanks also go to the anonymous reviewers for their helpful comments and contributions that undoubtedly improved the final manuscript.
Conflicts of Interest
The authors declare no conflicts of interest. The funders had no roles in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
Appendix A
Table A1.
Flower-visiting insects in coffee crops and study sites. (A) Pueblo Bello Experiment Station, (B) San Antonio Experiment Station, (C) Paraguicito Experiment Station, (D) Naranjal Experiment Station, and (E) Manuel Mejía Experiment Station.
Table A1.
Flower-visiting insects in coffee crops and study sites. (A) Pueblo Bello Experiment Station, (B) San Antonio Experiment Station, (C) Paraguicito Experiment Station, (D) Naranjal Experiment Station, and (E) Manuel Mejía Experiment Station.
| Order | Family | Specie | Study Sites |
|---|---|---|---|
| Blattodea | Blattodea sp. | C | |
| Coleoptera | Anthribidae | Anthribidae sp.1 | A |
| Anthribidae | Anthribidae sp.2 | A | |
| Anthribidae | Anthribidae sp.3 | D | |
| Cantharidae | Chauliognathus sp.1 | B, D | |
| Cantharidae | Chauliognathus sp.2 | E | |
| Cantharidae | Chauliognathus sp.3 | E | |
| Cantharidae | Chauliognathus sp.4 | E | |
| Cantharidae | Chauliognathus sp.5 | B | |
| Cantharidae | Chauliognathus sp.6 | E | |
| Cantharidae | Chauliognathus sp.7 | B | |
| Cantharidae | Chauliognathus sp.8 | B | |
| Cantharidae | Chauliognathus sp.9 | B | |
| Cantharidae | Chauliognathus sp.10 | B | |
| Cantharidae | Chauliognathus sp.11 | B | |
| Cantharidae | Chauliognathus sp.12 | D | |
| Cantharidae | Chauliognathus sp.13 | E | |
| Cantharidae | Discodon sp.1 | D | |
| Cantharidae | Discodon sp.2 | E | |
| Chrysomelidae | Chrysomelidae sp.1 | A, B, E | |
| Chrysomelidae | Chrysomelidae sp.2 | C, E | |
| Chrysomelidae | Chrysomelidae sp.3 | C | |
| Chrysomelidae | Chrysomelidae sp.4 | E | |
| Chrysomelidae | Chrysomelidae sp.5 | C, D | |
| Chrysomelidae | Chrysomelidae sp.6 | D | |
| Chrysomelidae | Chrysomelidae sp.7 | C, D | |
| Chrysomelidae | Chrysomelidae sp.8 | E | |
| Chrysomelidae | Chrysomelidae sp.9 | C, D | |
| Chrysomelidae | Chrysomelidae sp.10 | D | |
| Chrysomelidae | Chrysomelidae sp.11 | D | |
| Chrysomelidae | Chrysomelidae sp.12 | E | |
| Chrysomelidae | Chrysomelidae sp.13 | D | |
| Chrysomelidae | Chrysomelidae sp.14 | D | |
| Coleoptera | Chrysomelidae | Chrysomelidae sp.15 | E |
| Chrysomelidae | Chrysomelidae sp.16 | D | |
| Chrysomelidae | Chrysomelidae sp.17 | D | |
| Chrysomelidae | Chrysomelidae sp.18 | E | |
| Chrysomelidae | Chrysomelidae sp.19 | E | |
| Chrysomelidae | Chrysomelidae sp.20 | B | |
| Chrysomelidae | Chrysomelidae sp.21 | C | |
| Chrysomelidae | Chrysomelidae sp.22 | D | |
| Chrysomelidae | Chrysomelidae sp.23 | D | |
| Chrysomelidae | Chrysomelidae sp.24 | A | |
| Chrysomelidae | Chrysomelidae sp.25 | B | |
| Chrysomelidae | Chrysomelidae sp.26 | B | |
| Chrysomelidae | Chrysomelidae sp.27 | A | |
| Chrysomelidae | Chrysomelidae sp.28 | C, D | |
| Chrysomelidae | Chrysomelidae sp.29 | D, E | |
| Chrysomelidae | Chrysomelidae sp.30 | D, E | |
| Chrysomelidae | Chrysomelidae sp.31 | A, D, E | |
| Chrysomelidae | Chrysomelidae sp.32 | D | |
| Chrysomelidae | Chrysomelidae sp.33 | B | |
| Chrysomelidae | Chrysomelidae sp.34 | B | |
| Chrysomelidae | Chrysomelidae sp.35 | B | |
| Chrysomelidae | Chrysomelidae sp.36 | E | |
| Chrysomelidae | Chrysomelidae sp.37 | E | |
| Coccinellidae | Azya orbigera | C, D | |
| Coccinellidae | Coccinelldae sp.1 | B | |
| Coccinellidae | Coccinellidae sp.2 | A, B, D | |
| Coccinellidae | Coccinellidae sp.3 | D, E | |
| Coccinellidae | Coccinellidae sp.4 | D | |
| Coccinellidae | Coccinellidae sp.5 | B | |
| Coccinellidae | Coccinellidae sp.6 | B, D | |
| Coccinellidae | Coccinellidae sp.7 | D | |
| Coccinellidae | Coccinellidae sp.8 | D | |
| Coccinellidae | Coccinellidae sp.9 | D | |
| Coccinellidae | Coccinellidae sp.10 | C, D | |
| Coccinellidae | Coccinellidae sp.11 | B, D | |
| Curculionidae | Curculionidae sp.1 | C, D | |
| Curculionidae | Curculionidae sp.2 | D | |
| Curculionidae | Curculionidae sp.3 | C | |
| Curculionidae | Curculionidae sp.4 | B | |
| Curculionidae | Curculionidae sp.5 | D | |
| Curculionidae | Curculionidae sp.6 | D | |
| Curculionidae | Curculionidae sp.7 | C | |
| Curculionidae | Curculionidae sp.8 | B, C | |
| Coleoptera | Curculionidae | Curculionidae sp.9 | B |
| Curculionidae | Curculionidae sp.10 | E | |
| Curculionidae | Curculionidae sp.11 | C | |
| Curculionidae | Curculionmidae sp.12 | B | |
| Dascilidae | Dascilidae sp.1 | D | |
| Lagriidae | Lagriidae sp.1 | D | |
| Lampyridae | Lampyridae sp.1 | E | |
| Lycidae | Lycidae sp.1 | C, D | |
| Lycidae | Lycidae sp.2 | E | |
| Lycidae | Lycidae sp.3 | D | |
| Lycidae | Lycidae sp.4 | C | |
| Lycidae | Lycidae sp.5 | D | |
| Melyridae | Astylus lebasi | E | |
| Melyridae | Melyridae sp.1 | B | |
| Mordellidae | Mordellidae sp.1 | D | |
| Mordellidae | Mordellidae sp.2 | E | |
| Mordellidae | Mordellidae sp.3 | A | |
| Nitidulidae | Nitidulidae sp.1 | B | |
| Nitidulidae | Nitidulidae sp.2 | B | |
| Nitidulidae | Nitidulidae sp.3 | B | |
| Ptilodactylidae | Ptilodactylidae sp.1 | B | |
| Scarabaeidae | Macraspis sp.1 | C | |
| Scarabaeidae | Scarabaeidae sp.1 | C | |
| Scarabaeidae | Scarabaeidae sp.2 | C | |
| Scarabaeidae | Scarabaeidae sp.3 | E | |
| Scarabaeidae | Scarabaeidae sp.4 | E | |
| Staphylinidae | Staphylinidae sp.1 | C, D, E | |
| Staphylinidae | Staphylinidae sp.2 | C, D | |
| Staphylinidae | Staphylinidae sp.3 | D | |
| Staphylinidae | Staphylinidae sp.4 | C | |
| Staphylinidae | Staphylinidae sp.5 | A, B, C, D, E | |
| Staphylinidae | Staphylinidae sp.6 | C, D | |
| Dermaptera | Dermaptera spp. | A, B, D | |
| Diptera | Anthomyiidae | Anthomyiidae sp.1 | C |
| Anthomyiidae | Anthomyiidae sp.2 | C | |
| Anthomyiidae | Anthomyiidae sp.3 | C | |
| Bibionidae | Bibionidae sp.1 | C, D, E | |
| Bibionidae | Bibionidae sp.2 | B, C, D | |
| Bibionidae | Bibionidae sp.3 | C, D | |
| CalliPhoridae | CalliPhoridae sp.1 | D | |
| CalliPhoridae | CalliPhoridae sp.2 | C | |
| CalliPhoridae | CalliPhoridae sp.3 | B | |
| CalliPhoridae | CalliPhoridae sp.4 | B, D | |
| Diptera | CalliPhoridae | CalliPhoridae sp.5 | B, D |
| CalliPhoridae | CalliPhoridae sp.6 | D | |
| CalliPhoridae | Lucilia sp.1 | C | |
| CalliPhoridae | Lucilia sp.2 | C | |
| CalliPhoridae | Lucilia sp.3 | C | |
| CalliPhoridae | Lucilia sp.4 | D | |
| CalliPhoridae | Lucilia sp.5 | D | |
| CalliPhoridae | Lucilia sp.6 | C | |
| CalliPhoridae | Lucilia sp.7 | B | |
| CalliPhoridae | Lucilia sp.8 | D | |
| CalliPhoridae | Lucilia sp.9 | D | |
| Camillidae | Camillidae sp.1 | D | |
| Carnidae | Carnidae sp.2 | C | |
| Carnidae | Carnidae sp.3 | E | |
| Ceratopogonidae | Ceratopogonidae sp.1 | C, D | |
| Ceratopogonidae | Ceratopogonidae sp.2 | D | |
| Ceratopogonidae | Ceratopogonidae sp.3 | D | |
| Ceratopogonidae | Ceratopogonidae sp.4 | D | |
| Chamaemyiidae | Chamaemyiidae sp.1 | D | |
| Chamaemyiidae | Chamaemyiidae sp.2 | D | |
| Chloropidae | Chloropidae sp.1 | C, D, E | |
| Chloropidae | Chloropidae sp.2 | C | |
| Chloropidae | Chloropidae sp.3 | C | |
| Chloropidae | Chloropidae sp.4 | B | |
| Chloropidae | Chloropidae sp.5 | B, D | |
| Chloropidae | Chloropidae sp.6 | B | |
| Chloropidae | Chloropidae sp.7 | C, D | |
| Chloropidae | Chloropidae sp.8 | B | |
| Chloropidae | Chloropidae sp.9 | B | |
| Chloropidae | Chloropidae sp.10 | B | |
| Chloropidae | Chloropidae sp.11 | C, D, E | |
| Chloropidae | Chloropidae sp.12 | C, D | |
| Conopidae | Conopidae sp.1 | C | |
| Curtonotidae | Curtonotidae sp.1 | B | |
| Dolichopodidae | Dolichopodidae sp.1 | C | |
| Dolichopodidae | Dolichopodidae sp.2 | B, C | |
| Dolichopodidae | Dolichopodidae sp.3 | A | |
| Dolichopodidae | Dolichopodidae sp.4 | A | |
| Drosophilidae | Drosophilidae sp.1 | C | |
| Empididae | Empididae sp.1 | C | |
| Fanniidae | Fanniidae sp.1 | D | |
| Fanniidae | Fanniidae sp.2 | D | |
| Fanniidae | Fanniidae sp.3 | C, E | |
| Fanniidae | Fanniidae sp.4 | C | |
| Diptera | Heleomyzidae | Heleomyzidae sp.1 | D |
| Lauxaniidae | Lauxaniidae sp.1 | B, D | |
| Lauxaniidae | Lauxaniidae sp.2 | B | |
| Lauxaniidae | Lauxaniidae sp.3 | B | |
| Lauxaniidae | Lauxaniidae sp.4 | B, C, D | |
| Lauxaniidae | Lauxaniidae sp.5 | C, D | |
| Lauxaniidae | Lauxaniidae sp.6 | C | |
| Lauxaniidae | Lauxaniidae sp.7 | B | |
| Lauxaniidae | Lauxaniidae sp.8 | D | |
| Lauxaniidae | Lauxaniidae sp.9 | B | |
| Lauxaniidae | Lauxaniidae sp.10 | C, E | |
| Lauxaniidae | Lauxaniidae sp.11 | D | |
| Micropezidae | Micropezidae sp.1 | D | |
| Milichiidae | Milichiidae sp.1 | D | |
| Milichiidae | Milichiidae sp.2 | D, E | |
| Milichiidae | Milichiidae sp.3 | D, E | |
| Muscidae | Muscidae sp.1 | C, D | |
| Muscidae | Muscidae sp.2 | C | |
| Phoridae | Phoridae sp.1 | D, E | |
| Phoridae | Phoridae sp.2 | B | |
| Phoridae | Phoridae sp.3 | C | |
| Phoridae | Phoridae sp.4 | C | |
| Piophilidae | Piophilidae sp.1 | C | |
| Pipunculidae | Pipunculidae sp.1 | C | |
| Pipunculidae | Pipunculidae sp.2 | C | |
| Pipunculidae | Pipunculidae sp.3 | C | |
| Sarcophagidae | Sarcophagidae sp.1 | C, D, E | |
| Sarcophagidae | Sarcophagidae sp.2 | D | |
| Sarcophagidae | Sarcophagidae sp.3 | C | |
| Sarcophagidae | Sarcophagidae sp.4 | C, D, E | |
| Sarcophagidae | Sarcophagidae sp.5 | C, D | |
| Sarcophagidae | Sarcophagidae sp.6 | D | |
| Sarcophagidae | Sarcophagidae sp.7 | D | |
| Sarcophagidae | Sarcophagidae sp.8 | B, D | |
| Sarcophagidae | Sarcophagidae sp.9 | C, D | |
| Sarcophagidae | Sarcophagidae sp.10 | D | |
| Sciaridae | Sciaridae sp.1 | C, D | |
| Sciaridae | Sciaridae sp.2 | C, D | |
| Sciaridae | Sciaridae sp.3 | C | |
| Sciaridae | Sciaridae sp.4 | D | |
| Sciaridae | Sciaridae sp.5 | D | |
| Sciaridae | Sciaridae sp.6 | D | |
| Diptera | Sciaridae | Sciaridae sp.7 | D |
| Sciaridae | Sciaridae sp.8 | D | |
| Sciaridae | Sciaridae sp.9 | C, D | |
| Sciaridae | Sciaridae sp.10 | C, D | |
| Sciaridae | Sciaridae sp.11 | B, C, D | |
| Sciaridae | Sciaridae sp.12 | C, D | |
| Sciaridae | Sciaridae sp.13 | C, D | |
| Sciaridae | Sciaridae sp.14 | C | |
| Sciaridae | Sciaridae sp.15 | D | |
| Sciaridae | Sciaridae sp.16 | C | |
| Simulidae | Simulidae sp.1 | D | |
| Syrphidae | Copestylum sp.1 | C | |
| Syrphidae | Copestylum sp.2 | D | |
| Syrphidae | Copestylum sp.3 | C, D | |
| Syrphidae | Copestylum sp.4 | C | |
| Syrphidae | Copestylum sp.5 | D | |
| Syrphidae | Copestylum sp.6 | C, D | |
| Syrphidae | Eristalis sp.1 | A, D | |
| Syrphidae | Eristalis sp.2 | C | |
| Syrphidae | Ocyptamus (Hermesomyia) sp.1 | A | |
| Syrphidae | Ocyptamus sp.2 | C | |
| Syrphidae | Ocyptamus sp.3 | C | |
| Syrphidae | Ocyptamus sp.4 | B, C, D | |
| Syrphidae | Ocyptamus sp.5 | C, D | |
| Syrphidae | Ornidia major | E | |
| Syrphidae | Ornidia obesa | A, B, C, D, E | |
| Syrphidae | Palpada sp.1 | A, C, D | |
| Syrphidae | Palpada sp.2 | C, D | |
| Syrphidae | Palpada sp.3 | C, D | |
| Syrphidae | Palpada sp.4 | A, B, C, D, E | |
| Syrphidae | Palpada sp.5 | A, B, C, D | |
| Syrphidae | Palpada sp.6 | A, B, D | |
| Syrphidae | Palpada sp.7 | A, D | |
| Syrphidae | Palpada sp.8 | B | |
| Syrphidae | Palpada sp.9 | A | |
| Syrphidae | Pseudodorus clavatus | A | |
| Syrphidae | Pseudodorus aff. clavatus | B, C, D | |
| Syrphidae | Pseudodorus sp.3 | C | |
| Syrphidae | Toxomerus sp.1 | A, B, C, D, E | |
| Syrphidae | Toxomerus sp.2 | B, C, D | |
| Syrphidae | Toxomerus sp.3 | D | |
| Syrphidae | Toxomerus sp.4 | B, C, D | |
| Syrphidae | Toxomerus sp.5 | B, C, D | |
| Diptera | Syrphidae | Toxomerus sp.6 | B, C |
| Syrphidae | Toxomerus sp.7 | C | |
| Syrphidae | Toxomerus sp.8 | B, D | |
| Syrphidae | Xanthandrus sp.1 | E | |
| Syrphidae | Xanthandrus sp.2 | B | |
| Syrphidae | Xanthandrus sp.3 | B | |
| Tachinidae | Tachinidae sp.1 | C | |
| Tachinidae | Tachinidae sp.2 | D | |
| Tachinidae | Tachinidae sp.3 | D, E | |
| Tachinidae | Tachinidae sp.4 | A, D | |
| Tachinidae | Tachinidae sp.5 | B, C, D | |
| Tachinidae | Tachinidae sp.6 | D | |
| Tachinidae | Tachinidae sp.7 | D | |
| Tachinidae | Tachinidae sp.8 | C, D | |
| Tachinidae | Tachinidae sp.9 | D | |
| Tachinidae | Tachinidae sp.10 | C, D | |
| Tachinidae | Tachinidae sp.11 | C, D | |
| Tachinidae | Tachinidae sp.12 | B | |
| Tephritidae | Tephritidae sp.1 | C | |
| Tephritidae | Tephritidae sp.2 | C | |
| Tephritidae | Tephritidae sp.3 | B, C | |
| Tephritidae | Tephritidae sp.4 | C, D | |
| Tephritidae | Tephritidae sp.5 | D | |
| Tephritidae | Tephritidae sp.6 | C | |
| Tephritidae | Tephritidae sp.7 | A, B | |
| Tephritidae | Tephritidae sp.8 | C | |
| Tephritidae | Tephritidae sp.9 | B | |
| Tipulidae | Tipulidae sp.1 | C | |
| Tipulidae | Tipulidae sp.2 | D | |
| Tipulidae | Tipulidae sp.3 | C | |
| Tipulidae | Tipulidae sp.4 | D | |
| Ulidiidae | Ulidiidae sp.1 | E | |
| Ulidiidae | Ulidiidae sp.2 | C | |
| Ulidiidae | Ulidiidae sp.3 | B | |
| Hemiptera | Alydidae | Alydidae sp.1 | D |
| Coreidae | Coreidae sp.1 | A | |
| Coreidae | Coreidae sp.2 | B | |
| Coreidae | Sphictyrtus sp.3 | C, D | |
| Cydnidae | Cydnidae sp.1 | D | |
| Lygaeidae | Lygaeidae sp.1 | C | |
| Lygaeidae | Lygaeidae sp.2 | C | |
| Lygaeidae | Lygaeidae sp.3 | B | |
| Lygaeidae | Lygaeidae sp.4 | C | |
| Hemiptera | Lygaeidae | Lygaeidae sp.5 | C |
| Miridae | Miridae sp.1 | D | |
| Miridae | Miridae sp.2 | D | |
| Miridae | Miridae sp.3 | B | |
| Miridae | Miridae sp.4 | C | |
| Miridae | Miridae sp.5 | B, C, D, E | |
| Miridae | Miridae sp.6 | D | |
| Miridae | Miridae sp.7 | C, D | |
| Miridae | Miridae sp.8 | B | |
| Miridae | Miridae sp.9 | B, D | |
| Miridae | Miridae sp.10 | B, E | |
| Miridae | Miridae sp.11 | B | |
| Miridae | Miridae sp.12 | E | |
| Miridae | Miridae sp.13 | E | |
| Miridae | Miridae sp.14 | E | |
| Miridae | Miridae sp.15 | C | |
| Pentatomidae | Pentatomidae sp.1 | C, D | |
| Pentatomidae | Pentatomidae sp.2 | B, C | |
| Pentatomidae | Pentatomidae sp.3 | D | |
| Pyrrhocoridae | Pyrrhocoridae sp.1 | E | |
| Reduviidae | Reduviidae sp.1 | B, E | |
| Rhopalidae | Rhopalidae sp.1 | E | |
| Rhopalidae | Rhopalidae sp.2 | D | |
| Rhopalidae | Rhopalidae sp.3 | B | |
| Tingidae | Tingidae sp.1 | C | |
| Hymenoptera | Agaonidae | Agaonidae sp.1 | B |
| Apidae | Apis mellifera | A, B, C, D, E | |
| Apidae | Bombus melaleucus | B | |
| Apidae | Bombus pauloensis | B | |
| Apidae | Bombus pullatus | A | |
| Apidae | Ceratina (Calloceratina) sp.1 | A, C | |
| Apidae | Ceratina (Ceratinula) sp.2 | A | |
| Apidae | Ceratina (Crewella) sp.3 | A | |
| Apidae | Ceratina sp.4 | B | |
| Apidae | Ceratina sp.5 | A | |
| Apidae | Epicharis (Epicharana) sp.1 | C | |
| Apidae | Euglossa cf. dressleri | D | |
| Apidae | Eulaema cingulata | A, C, D | |
| Apidae | Eulaema polychroma | B, C | |
| Apidae | Exomalopsis aburraensis | A, C, D, E | |
| Apidae | Exomalopsis auropilosa | C, D, E | |
| Apidae | Exomalopsis digressa | C | |
| Apidae | Exomalopsis snowi | C | |
| Hymenoptera | Apidae | Exomalopsis sp.1 | C, D |
| Apidae | Exomalopsis sp.2 | A, B, C, D | |
| Apidae | Exomalopsis sp.3 | D | |
| Apidae | Geotrigona cf. tellurica | B | |
| Apidae | Geotrigona kaba | B | |
| Apidae | Nannotrigona gaboi | A, B | |
| Apidae | Nannotrigona pilosa | C, D | |
| Apidae | Nannotrigona tristella | C, D | |
| Apidae | Nasutopedia sp1 | D | |
| Apidae | Paratrigona eutaeniata | B, D | |
| Apidae | Paratrigona opaca | A, B | |
| Apidae | Partamona cf peckolti | B, C, D, E | |
| Apidae | Plebeia sp.1 | D | |
| Apidae | Plebeia sp.2 | B, D | |
| Apidae | Plebeia sp.3 | A | |
| Apidae | Scaptotrigona sp.1 | A | |
| Apidae | Tetragona perangulata | A, B, D | |
| Apidae | Tetragonisca angustula | A, B, D, E | |
| Apidae | Trigona fulviventris | A, B | |
| Apidae | Trigona nigerrima | A, B, E | |
| Apidae | Trigonisca cf. pediculana | C, D | |
| Apidae | Trigonisca cf. mepecheu | A | |
| Apidae | Xylocopa frontalis | C, D | |
| Apidae | Xylocopa sp.1 | C, D | |
| Bethylidae | Bethylidae sp.1 | D | |
| Braconidae | Braconidae sp.1 | E | |
| Braconidae | Braconidae sp.2 | C, D | |
| Braconidae | Braconidae sp.3 | C | |
| Braconidae | Braconidae sp.4 | D | |
| Braconidae | Braconidae sp.5 | C | |
| Braconidae | Braconidae sp.6 | D | |
| Braconidae | Braconidae sp.7 | B | |
| Braconidae | Braconidae sp.8 | B, C | |
| Braconidae | Braconidae sp.9 | D | |
| Braconidae | Braconidae sp.10 | C, D | |
| Braconidae | Braconidae sp.11 | B, D | |
| Chalcididae | Chalcididae sp.1 | C | |
| Chalcididae | Conura sp.1 | D | |
| Colletidae | Ptiloglossa sp.1 | C | |
| Crabronidae | Liris sp.1 | C | |
| Crabronidae | Tachytes sp.1 | D | |
| Encyrtidae | Encyrtidae sp.1 | D | |
| Eucharitidae | Eucharitidae sp.1 | C | |
| Hymenoptera | Eucharitidae | Eucharitidae sp.2 | B |
| Figitidae | Figitidae sp.1 | D | |
| Formicidae | Acropyga sp.1 | B | |
| Formicidae | Atta sp.1 | D | |
| Formicidae | Bothriomyrmex sp.1 | C, D | |
| Formicidae | Brachymyrmex brunneus | D | |
| Formicidae | Brachymyrmex cavernicola | B | |
| Formicidae | Brachymyrmex coactus | C, D | |
| Formicidae | Brachymyrmex heeri | D | |
| Formicidae | Brachymyrmex pilipes | A, C | |
| Formicidae | Brachymyrmex sculpturatus | D | |
| Formicidae | Brachymyrmex sossai | D | |
| Formicidae | Brachymyrmex sp.2 | B | |
| Formicidae | Brachymyrmex tristis | C, D | |
| Formicidae | Camponotus senex | C | |
| Formicidae | Camponotus sp.1 | A, D, E | |
| Formicidae | Camponotus sp.2 | A, D | |
| Formicidae | Camponotus sp.3 | A, B, C | |
| Formicidae | Camponotus sp.4 | B | |
| Formicidae | Camponotus sp.5 | B | |
| Formicidae | Carebara sp.1 | D | |
| Formicidae | Cephalotes sp.1 | C | |
| Formicidae | Crematogaster sp.1 | A, B | |
| Formicidae | Crematogaster sp.2 | D | |
| Formicidae | Dolichoderus sp.1 | D | |
| Formicidae | Dorymyrmex bicolor | C | |
| Formicidae | Dorymyrmex biconis | C, D, E | |
| Formicidae | Dorymyrmex brunneus | C, D | |
| Formicidae | Dorymyrmex insanus | C, D | |
| Formicidae | Ectatomma confine | B, D | |
| Formicidae | Ectatomma ruidum | C, D | |
| Formicidae | Ectatomma tuberculatum | D | |
| Formicidae | Linepithema angulatum | B, D | |
| Formicidae | Linepithema gallardoi | D | |
| Formicidae | Linepithema hirsutum | B | |
| Formicidae | Linepithema iniquum | C, E | |
| Formicidae | Linepithema neotropicum | B, C, E | |
| Formicidae | Linepithema sp.1 | B, D | |
| Formicidae | Megalomyrmex cuatiara | D | |
| Formicidae | Megalomyrmex incisus | D | |
| Formicidae | Megalomyrmex poatan | D, E | |
| Formicidae | Megalomyrmex sp.1 | D, E | |
| Formicidae | Megalomyrmex sp.2 | B, C, D | |
| Hymenoptera | Formicidae | Megalomyrmex sp.3 | B, D |
| Formicidae | Megalomyrmex sp.4 | E | |
| Formicidae | Megalomyrmex sp.5 | C, D | |
| Formicidae | Megalomyrmex sp.6 | D | |
| Formicidae | Myrcidris sp.1 | D | |
| Formicidae | Neivamyrmex sp.1 | C | |
| Formicidae | Nylanderia fulva | A | |
| Formicidae | Paratrechina fulva | B, D | |
| Formicidae | Paratrechina sp.1 | B, D | |
| Formicidae | Pseudomyrmex gracilis | D | |
| Formicidae | Pseudomyrmex oculatus | B | |
| Formicidae | Pseudomyrmex sp.1 | E | |
| Formicidae | Pseudomyrmex tenuis | A | |
| Formicidae | Solenopsis aff. geminata | C | |
| Formicidae | Solenopsis geminata | C, D | |
| Formicidae | Solenopsis sp.1 | C, D | |
| Formicidae | Solenopsis sp.2 | C, D, E | |
| Formicidae | Solenopsis sp.3 | C, D | |
| Formicidae | Solenopsis sp.4 | D | |
| Formicidae | Solenopsis sp.5 | C, E | |
| Formicidae | Solenopsis sp.6 | C, D | |
| Formicidae | Wasmannia auropunctata | D | |
| Formicidae | Wasmannia sp.2 | D | |
| Halictidae | Agapostemon sp.1 | C, D, E | |
| Halictidae | Augochlora sp.1 | D | |
| Halictidae | Augochlora sp.2 | D, E | |
| Halictidae | Augochlora sp.3 | E | |
| Halictidae | Augochlora sp.4 | D, E | |
| Halictidae | Augochlora sp.5 | D | |
| Halictidae | Augochlora sp.6 | D | |
| Halictidae | Augochlora sp.7 | C, D | |
| Halictidae | Augochlora sp.8 | A | |
| Halictidae | Augochlora sp.9 | A | |
| Halictidae | Augochlora sp.10 | A | |
| Halictidae | Augochlorella sp.1 | D | |
| Halictidae | Augochlorella sp.2 | C | |
| Halictidae | Augochlorella sp.3 | C | |
| Halictidae | Augochlorella sp.4 | D | |
| Halictidae | Augochlorella sp.5 | C | |
| Halictidae | Augochlorella sp.6 | C, E | |
| Halictidae | Augochlorella sp.7 | C | |
| Halictidae | Augochlorella sp.8 | C, D | |
| Halictidae | Augochloropsis sp.1 | B, D | |
| Hymenoptera | Halictidae | Augochloropsis sp.2 | C |
| Halictidae | Augochloropsis sp.3 | D | |
| Halictidae | Augochloropsis sp.4 | A | |
| Halictidae | Augochloropsis sp.5 | A | |
| Halictidae | Caenohalictus sp.1 | A, D | |
| Halictidae | Caenohalictus sp.2 | B, C, D | |
| Halictidae | Habralictus sp.1 | B, D, E | |
| Halictidae | Habralictus sp.2 | D, E | |
| Halictidae | Lasioglossum sp.1 | B, C, D, E | |
| Halictidae | Lasioglossum sp.2 | A, B, C, D, E | |
| Halictidae | Lasioglossum sp.3 | A, C, D, E | |
| Halictidae | Lasioglossum sp.4 | A, D, E | |
| Halictidae | Lasioglossum sp.5 | B, C | |
| Halictidae | Lasioglossum sp.6 | A | |
| Halictidae | Neocorynura sp.1 | E | |
| Halictidae | Neocorynura sp.2 | C | |
| Halictidae | Neocorynura sp.3 | D | |
| Halictidae | Neocorynura sp.4 | D | |
| Halictidae | Neocorynura sp.5 | D | |
| Halictidae | Neocorynura sp.6 | A | |
| Halictidae | Neocorynura sp.7 | D | |
| Halictidae | Pereirapis sp.1 | B, C, D | |
| Halictidae | Pereirapis sp.2 | D | |
| Halictidae | Pereirapis sp.3 | D | |
| Halictidae | Pereirapis sp.4 | D | |
| Halictidae | Pseudaugochlora sp.1 | D | |
| Halictidae | Pseudaugochlora sp.2 | D, E | |
| Ichneumonidae | Ichneumonidae sp.1 | E | |
| Ichneumonidae | Ichneumonidae sp.2 | D | |
| Ichneumonidae | Ichneumonidae sp.3 | E | |
| Ichneumonidae | Ichneumonidae sp.4 | C | |
| Ichneumonidae | Ichneumonidae sp.5 | D | |
| Megachilidae | Megachile sp.1 | D | |
| Megaspilidae | Megaspilidae sp.1 | E | |
| Platygastridae | Platygastridae sp.1 | C, D | |
| Platygastridae | Synopeas sp.1 | B, C | |
| Pompilidae | Aimatocare sp.1 | B | |
| Pompilidae | Entypus sp.1 | D | |
| Pompilidae | Entypus sp.2 | D | |
| Pompilidae | Priocnemis sp.1 | D, E | |
| Pompilidae | Priocnemis sp.2 | C, D, E | |
| Psenidae | Pseneo sp.1 | D | |
| Scoliidae | Campsomeris dorsata | C | |
| Hymenoptera | Scoliidae | Campsomeris peregrina | C, D |
| Scoliidae | Campsomeris servillei | A, D | |
| Scoliidae | Campsomeris sp.1 | E | |
| Tiphiidae | Tiphia sp.1 | C, D, E | |
| Tiphiidae | Tiphia sp.2 | D | |
| Tiphiidae | Tiphia sp.3 | C | |
| Vespidae | Agelaia areata | B, C | |
| Vespidae | Angiopolybia paraensis | A | |
| Vespidae | Brachygastra augusti | D | |
| Vespidae | Brachygastra baccalaurea | A | |
| Vespidae | Epipona guerini | C, D | |
| Vespidae | Pachodynerus nasidens | A | |
| Vespidae | Parachartergus colobopterus | A | |
| Vespidae | Parachartergus richardsi | C | |
| Vespidae | Parachartergus weyrauchi | A, B | |
| Vespidae | Polistes carnifex | C, D | |
| Vespidae | Polistes satan | B | |
| Vespidae | Polybia cf. simillima | C, D, E | |
| Vespidae | Polybia emaciata | B | |
| Vespidae | Polybia ignobilis | D | |
| Vespidae | Polybia occidentalis venezuelana | A, B | |
| Vespidae | Polybia rejecta | B, C | |
| Vespidae | Protopolybia acutiscutis | C, E | |
| Vespidae | Protopolybia fuscata | D | |
| Vespidae | Synoeca septentrionalis | A, B, C, D | |
| Lepidoptera | Erebidae | Erebidae sp.1. | C |
| Hesperiidae | Eutychide complana | D | |
| Hesperiidae | Hesperiidae sp.1 | C | |
| Hesperiidae | Hesperiidae sp.2 | C | |
| Hesperiidae | Hesperiidae sp.3 | C | |
| Hesperiidae | Hesperiidae sp.4 | C | |
| Hesperiidae | Hesperiidae sp.5 | C | |
| Hesperiidae | Hesperiidae sp.6 | C | |
| Hesperiidae | Hesperiidae sp.7 | C | |
| Hesperiidae | Hesperiidae sp.8 | C | |
| Hesperiidae | Hesperiidae sp.9 | C | |
| Hesperiidae | Hesperiidae sp.10 | C | |
| Hesperiidae | Hesperiidae sp.11 | C, E | |
| Hesperiidae | Hesperiidae sp.12 | D | |
| Hesperiidae | Hesperiidae sp.13 | C, E | |
| Hesperiidae | Hesperiidae sp.14 | D | |
| Hesperiidae | Thespieus sp.1 | C | |
| Hesperiidae | Urbanus procne | C | |
| Hesperiidae | Urbanus proteus | C | |
| Hesperiidae | Urbanus simplicius | D | |
| Hesperiidae | Urbanus teleus | C, D | |
| Lycaenidae | Rekoa palegon | C | |
| Lycaenidae | Strymon caldasensis | D | |
| Nymphalidae | Actinote anteas | C | |
| Nymphalidae | Anartia amathea | C | |
| Nymphalidae | Anartia jatrophae | C | |
| Nymphalidae | Dione juno | C | |
| Nymphalidae | Siproeta stelenes | C | |
| Papilionidae | Heraclides thoas nealces | D | |
| Pieridae | Ascia monuste | D | |
| Sphingidae | Sphingidae sp.1 | C | |
| Neuroptera | Chrysopidae | Chrysopidae sp.1 | B |
| Chrysopidae | Chrysopidae sp.2 | D | |
| Orthoptera | Orthoptera sp.1 | D, E | |
| Thysanoptera | Thysanoptera sp.1 | B, C, E |
Appendix B
Table A2.
Flower-visiting insects of two species of the genus Coffea according to referenced studies. NR: Does not report data by species for some groups., NE: Not evaluated in the study and ~: approximately.
Table A2.
Flower-visiting insects of two species of the genus Coffea according to referenced studies. NR: Does not report data by species for some groups., NE: Not evaluated in the study and ~: approximately.
| Species | Country | Number of Bee Species | Number of Species of Other Insects | Most Abundant Visitors (>5% of the Visits) | References |
|---|---|---|---|---|---|
| C. canephora | Papua New Guinea | 4 | NR | Trigona sp., Apis sp. Amegilla sapiens, Megachile frontalis, Syrphidae | [13] |
| C. canephora | Indonesia | 22 | NE | Lepidotrigona terminata, Heterotrigona sp., Apis cerana, Amegilla samarensis, Xylocopa dejeanii | [53] |
| C. canephora | Uganda | 25 | NE | Hypotrigona gribodoi, Axestotrigona ferrugínea, A. mellifera adansonii. | [54] |
| C. arabica | Jamaica | 4 | 14 | A. mellifera | [33] |
| C. arabica | Panama | 22 | ~29 | A. mellifera scutellata | [15] |
| C. arabica | Indonesia | ~15 | NE | Apis nigrocincta, Apis dorsata, A. cerana, L. terminata, Heterotrigona sp. 2, Halictidae, M. frontalis, Heriades sp. | [2] |
| C. arabica | Brazil | 5 | NR | A. mellifera scutellata | [55] |
| C. arabica | Brazil | 6 | NE | A. mellífera | [56] |
| C. arabica | Costa Rica | 14 | NE | A. mellifera, Plebeia jatiformis, Plebeia frontalis, Trigonisca sp. | [57] |
| C. arabica | Mexico | 5 | 22 | Trigona sp. 1, A. mellifera, Ceratina sp. 1, ceratina sp. 2, Brachymyrmex sp. 1, Brachymyrmex sp. 2, Crematogaster sp., Solenopsis sp. 1. | [34] |
| C. arabica | Ecuador | 8 | NE | A. mellifera scutellata, Cephalotrigona capitata, Melipona mimetica, Nannotrigona mellaria, Nannotrigona perilampoides, Partamona peckolti, T. angustula, Trigona amalthea | [58] |
| C. arabica | Mexico | 7 | 8 | A. mellifera, Scaptotrigona mexicana | [59] |
| C. arabica | Mexico | 7 | 8 | A. mellifera, Trigona corvina | [35] |
| C. arabica | Colombia | 13 | NE | A. mellifera, Paratrigona eutaeniata | [12] |
| C. arabica | Brazil | 22 | NE | A. mellifera, Trigona spinipes, Trigona hyalinata, Paratrigona subnuda | [60] |
| C. arabica | Brazil | 19 | 48 | A. mellifera, Trigona spinipes, Ceratitis capitata (Tephritidae) | [61] |
| C. arabica | Ethiopia | 27 | NE | A. mellifera, Lasioglossum aff. Atricrum, Zonalictus abessinicus | [62] |
References
- Ollerton, J.; Winfree, R.; Tarrant, S. How many flowering plants are pollinated by animals? Oikos 2011, 120, 321–326. [Google Scholar] [CrossRef]
- Klein, A.M.; Steffan-Dewenter, I.; Tscharntke, T. Fruit set of highland coffee increases with the diversity of pollinating bees. Proc. R. Soc. Lond. Ser. B Biol. Sci. 2003, 270, 955–961. [Google Scholar] [CrossRef] [PubMed]
- Garibaldi, L.A.; Carvalheiro, L.G.; Vaissière, B.E.; Gemmill-Herren, B.; Hipólito, J.; Freitas, B.M.; Ngo, H.T.; Azzu, N.; Sáez, A.; Áström, J.; et al. Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 2016, 351, 388–391. [Google Scholar] [CrossRef]
- Klein, A.M.; Müller, C.; Hoehn, P.; Kremen, C. Understanding the role of species richness for crop pollination services. In Biodiversity, Ecosystem Functioning, and Human Wellbeing; Naeem, S., Bunker, D.E., Hector, A., Loreau, M., Perrings, C., Eds.; Oxford University Press: New York, NY, USA, 2009; pp. 195–208. [Google Scholar]
- Hooper, D.U. Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol. Monogr. 2005, 75, 3–35. [Google Scholar] [CrossRef]
- Violle, C.; Navas, M.-L.; Vile, D.; Kazakou, E.; Fortunel, C.; Hummel, I.; Garnier, E. Let the concept of trait be functional! Oikos 2007, 116, 882–892. [Google Scholar] [CrossRef]
- Federación Nacional de Cafeteros de Colombia (FNC). Informe del Gerente 90 Congreso Nacional de Cafeteros 2022. Available online: https://federaciondecafeteros.org/app/uploads/2022/12/Informe-del-Gerente-D.pdf (accessed on 2 November 2023).
- Flórez, C.P.; Ibarra, L.N.; Gómez, L.F.; Carmona, C.Y.; Castaño, Á.; Ortiz, A. Estructura y funcionamiento de la planta de café. In Federación Nacional de Cafeteros de Colombia, Manual del Cafetero Colombiano: Investigación y Tecnología para la Sostenibilidad de la Caficultura; LEGIS: Bogota, Colombia, 2013; Volume 1, pp. 123–168. [Google Scholar] [CrossRef]
- Ngo, H.T.; Mojica, A.C.; Packer, L. Coffee plant-pollinator interactions: A review. Can. J. Zool. 2011, 89, 647–660. [Google Scholar] [CrossRef]
- Moreaux, C.; Meireles, D.A.L.; Sonne, J.; Badano, E.I.; Classen, A.; González-Chaves, A.; Hipólito, J.; Klein, A.M.; Maruyama, P.K.; Metzger, J.P.; et al. The value of biotic pollination and dense forest for fruit set of Arabica coffee: A global assessment. Agric. Ecosyst. Environ. 2022, 323, 107680. [Google Scholar] [CrossRef]
- Jaramillo, A. Efecto de las Abejas Silvestres en la Polinización del Café (Coffea arabica: Rubiaceae) en tres Sistemas de Producción en el Departamento de Antioquia. Master’s Thesis, Universidad Nacional sede Medellín, Medellín, Colombia, 2012. Available online: https://repositorio.unal.edu.co/handle/unal/9860 (accessed on 28 May 2023).
- Cepeda-Valencia, J.; Gómez, P.D.; Nicholls, C. La estructura importa: Abejas visitantes del café y estructura agroecológica principal (EAP) en cafetales. Rev. Colomb. Entomol. 2014, 40, 241–250. [Google Scholar]
- Willmer, P.G.; Stone, G.N. Incidence of entomophilous pollination of lowland coffee (Coffea canephora): The role of leaf cutter bees in Papua New Guinea. Entomol. Exp. Appl. 1989, 50, 113–124. [Google Scholar] [CrossRef]
- Klein, A.-M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Landscape effects on crop pollination services: Are there general patterns? Ecol. Lett. 2008, 11, 499–515. [Google Scholar] [CrossRef]
- Roubik, D.W. Feral African bees augment neotropical coffee yield. In Pollinating Bees: The Conservation Link between Agriculture and Nature; Kevan, P.G., Imperatriz-Fonseca, V.L., Eds.; Ministry of Environment: Brasilia, Brazil, 2002; pp. 255–266. [Google Scholar]
- Garibaldi, L.A.; Bartomeus, I.; Bommarco, R.; Klein, A.M.; Cunningham, S.A.; Aizen, M.A.; Boreux, V.; Garratt, M.P.D.; Carvalheiro, L.G.; Kremen, C.; et al. Trait matching of flower visitors and crops predicts fruit set better than trait diversity. J. Appl. Ecol. 2015, 52, 1436–1444. [Google Scholar] [CrossRef]
- Woodcock, B.A.; Garratt, M.P.D.; Powney, G.D.; Shaw, R.F.; Osborne, J.L.; Soroka, J.; Lindström, S.A.M.; Stanley, D.; Ouvrard, P.; Edwards, M.E.; et al. Meta-analysis reveals that pollinator functional diversity and abundance enhance crop pollination and yield. Nat. Commun. 2019, 10, 1481. [Google Scholar] [CrossRef]
- Arcila, P.J. Crecimiento y desarrollo de la planta de café. In Sistemas de Producción de Café en Colombia; Arcila, P.J., Farfán, V.F., Moreno, B.A.M., Salazar, G.L.F., Hincapié, G.E., Eds.; FNC-Cenicafé: Manizales, Colombia, 2007; pp. 21–61. [Google Scholar]
- Engel, M.S. Classification of the bee tribe Augochlorini (Hymenoptera: Halictidae). Bull. Am. Museum Nat. Hist. 2000, 2000, 1–89. [Google Scholar] [CrossRef]
- Triplehorn, C.A.; Johnson, N.F.; Borror, D.J. Borror and DeLong’s Introduction to the Study of Insects, 7th ed.; Thomson Brooks/Cole: Belmont, CA, USA, 2005; 864p. [Google Scholar]
- Fernandez, F.; Sharkey, M.J. Introdución a los Hymenoptera de la Región Neotropical; Sociedad Colombiana de Entomología y Universidad Nacional de Colombia: Bogotá, Colombia, 2006; 894p. [Google Scholar]
- Michener, C.D. The Bees of the World; The John Hopkins University Press: Baltimore, MD, USA, 2007; 953p. [Google Scholar]
- Normandin, É.; Vereecken, N.J.; Buddle, C.M.; Fournier, V. Taxonomic and functional trait diversity of wild bees in different urban settings. PeerJ 2017, 5, e3051. [Google Scholar] [CrossRef] [PubMed]
- Kratschmer, S.; Pachinger, B.; Schwantzer, M.; Paredes, D.; Guzmán, G.; Goméz, J.A.; Entrenas, J.A.; Guernion, M.; Burel, F.; Nicolai, A.; et al. Response of wild bee diversity, abundance, and functional traits to vineyard inter-row management intensity and landscape diversity across Europe. Ecol. Evol. 2019, 9, 4103–4115. [Google Scholar] [CrossRef] [PubMed]
- Louveaux, J.; Maurizio, A.; Vorwohl, G. Methods of melissopalynology. Bee World 1970, 51, 125–138. [Google Scholar] [CrossRef]
- Louveaux, J.; Maurizio, A.; Vorwohl, G. Methods of melissopalynology. Bee World 1978, 59, 139–157. [Google Scholar] [CrossRef]
- Colwell, R.K.; Elsensohn, J.A. EstimateS turns 20: Statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography 2014, 37, 609–613. [Google Scholar] [CrossRef]
- Chao, A.; Ma, K.H.; Hsieh, T.C.; Chiu, C.H. SpadeR: Species-Richness Prediction and Diversity Estimation with R. Package ‘SpadeR’ Version 0.1.1. 2016. Available online: https://CRANR-project.org/package=SpadeR (accessed on 25 November 2023).
- Hill, M.O. Diversity and evenness: A unifying notation and its consequences. Ecology 1973, 54, 427–432. [Google Scholar] [CrossRef]
- Chao, A.; Shen, T.J. Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ. Ecol. Stat. 2003, 10, 429–443. [Google Scholar] [CrossRef]
- Chao, A.; Jost, L. Coverage based rarefaction and extrapolation: Standardizing samples by completeness rather than size. Ecology 2012, 93, 2533–2547. [Google Scholar] [CrossRef]
- Knop, E.; Gerpe, C.; Ryser, R.; Hofmann, F.; Menz, M.H.M.; Trösch, S.; Ursenbacher, S.; Zoller, L.; Fontaine, C. Rush hours in flower visitors over a day–night cycle. Insect Conserv. Divers. 2017, 11, 267–275. [Google Scholar] [CrossRef]
- Raw, A.; Free, J.B. The pollination of coffee (Coffea arabica) by honeybees. Trop. Agric. 1977, 54, 365–370. [Google Scholar]
- Philpott, S.M.; Uno, S.; Maldonado, J. The importance of ants and high-shade management to coffee pollination and fruit weight in Chiapas, Mexico. Biodivers. Conserv. 2006, 15, 487–501. [Google Scholar] [CrossRef]
- Vergara, C.H.; Badano, E.I. Pollinator diversity increases fruit production in Mexican coffee plantations: The importance of rusticmanagement systems. Agric. Ecosyst. Environ. 2009, 129, 117–123. [Google Scholar] [CrossRef]
- Garibaldi, L.A.; Sáez, A.; Aizen, M.A.; Fijen, T.; Bartomeus, I. Crop pollination management needs flower-visitor monitoring and target values. J. Appl. Ecol. 2020, 57, 664–670. [Google Scholar] [CrossRef]
- Hung, K.L.J.; Kingston, J.M.; Lee, A.; Holway, D.A.; Kohn, J.R. Non-native honey bees disproportionately dominate the most abundant floral resources in a biodiversity hotspot. Proc. R. Soc. B Biol. Sci. 2019, 286, 20182901. [Google Scholar] [CrossRef] [PubMed]
- Bänsch, S.; Tscharntke, T.; Gabriel, D.; Westphal, C. Crop pollination services: Complementary resource use by social vs solitary bees facing crops with contrasting flower supply. J. Appl. Ecol. 2021, 58, 476–485. [Google Scholar] [CrossRef]
- Hillebrand, H.; Bennett, D.M.; Cadotte, M.W. Consequences of dominance: A review of evenness effects on local and regional ecosystem processes. Ecology 2008, 89, 1510–1520. [Google Scholar] [CrossRef] [PubMed]
- Klein, A.-M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. Lond. Ser. B Biol. Sci. 2007, 274, 303–313. [Google Scholar] [CrossRef] [PubMed]
- Moritz, R.F.A.; Härtel, S.; Neumann, P. Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Ecoscience 2005, 12, 289–301. [Google Scholar] [CrossRef]
- Herrera, C.M. Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. Oikos 1990, 58, 277. [Google Scholar] [CrossRef]
- McCall, C.; Primack, R.B. Influence of flower characteristics, weather, time of day, and season on insect visitation Rates in Three Plant Communities. Am. J. Bot. 1992, 79, 434–442. [Google Scholar] [CrossRef]
- Mason, N.W.H.; Mouillot, D.; Lee, W.G.; Wilson, J.B. Functional richness, functional evenness and functional divergence: The primary components of functional diversity. Oikos 2005, 111, 112–118. [Google Scholar] [CrossRef]
- Buchholz, S.; Egerer, M.H. Functional ecology of wild bees in cities: Towards a better understanding of trait-urbanization relationships. Biodivers. Conserv. 2020, 29, 2779–2801. [Google Scholar] [CrossRef]
- Mouchet, M.A.; Villéger, S.; Mason, N.W.H.; Mouillot, D. Functional diversity measures: An overview of their redundancy and their ability to discriminate community assembly rules. Funct. Ecol. 2010, 24, 867–876. [Google Scholar] [CrossRef]
- Arnan, X.; Cerdá, X.; Rodrigo, A.; Retana, J. Response of ant functional composition to fire. Ecography 2013, 36, 1182–1192. [Google Scholar] [CrossRef]
- Martins, K.T.; Gonzalez, A.; Lechowicz, M.J. Patterns of pollinator turnover and increasing diversity associated with urban habitats. Urban Ecosyst. 2017, 20, 1359–1371. [Google Scholar] [CrossRef]
- Thapa, K.B.; Davis, T.S.; Kondratieff, B. Livestock grazing is associated with seasonal reduction in pollinator biodiversity and functional dispersion but cheatgrass invasion is not: Variation in bee assemblages in a multiuse shortgrass prairie. PLoS ONE 2020, 15, e0237484. [Google Scholar] [CrossRef]
- Gómez, J.H.; Benavides, P.; Maldonado, J.D.; Jaramillo, J.; Acevedo, F.E.; Gil, Z.N. Flower-Visiting Insects Ensure Coffee Yield and Quality. Agriculture 2023, 13, 1392. [Google Scholar] [CrossRef]
- de Merxem, D.G.; Borremans, B.; de Jäger, M.L.; Johnson, T.; Jooste, M.; Ros, P.; Zenni, R.D.; Ellis, A.G.; Anderson, B. The importance of flower visitors not predicted by floral syndromes. S. Afr. J. Bot. 2009, 75, 660–667. [Google Scholar] [CrossRef]
- King, C.; Ballantyne, G.; Willmer, P.G. Why flower visitation is a poor proxy for pollination: Measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol. Evol. 2013, 4, 811–818. [Google Scholar] [CrossRef]
- Klein, A.M.; Dewenter, S.; Tscharntke, T. Pollination of Coffea canephora in relation to local and regional agroforestry management. J. Appl. Ecol. 2003, 40, 837–845. [Google Scholar] [CrossRef]
- Munyuli, T. Influence of functional traits on foraging behaviour and pollination efficiency of wild social and solitary bees visiting coffee (Coffea canephora) flowers in Uganda. Grana. 2014, 53, 69–89. [Google Scholar] [CrossRef]
- Malerbo-Souza, D.T.; Nogueira-Couto, R.H.; Couto, L.A.; de Souza, J.C. Atrativo para as abelhas Apis mellifera e polinização em café (Coffea arabica L.). Braz. J. Vet. Res. Anim. Sci. 2003, 40, 272–278. [Google Scholar] [CrossRef]
- De Marco Jr, P.; Monteiro, F. Services performed by the ecosystem: Forest remnants influence agricultural cultures’ pollination and production. Biodivers. Conserv. 2004, 13, 1245–1255. [Google Scholar] [CrossRef]
- Ricketts, T.H. Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv. Biol. 2004, 18, 1262–1271. [Google Scholar] [CrossRef]
- Veddeler, D.; Klein, A.M.; Tscharntke, T. Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos 2006, 112, 594–601. [Google Scholar] [CrossRef]
- Vergara, C.; Contreras, J.; Ferrari, R.; Paredes, J. Polinización entomófila. In Agroecosistemas Cafetaleros de Veracruz: Biodiversidad, Manejo y Conservación; Manson, R.H., Hernández O, V., Gallina, S., Mehltreter, K., Eds.; Instituto Nacional de Ecología and Instituto de Ecología A.C.: Ciudad de México, Mexico, 2008; pp. 247–257. [Google Scholar]
- Saturni, F.T.; Jaffé, R.; Metzger, J.P. Landscape structure influences bee community and coffee pollination at different spatial scales. Agric. Ecosyst. Environ. 2016, 235, 1–12. [Google Scholar] [CrossRef]
- Hipólito, J.; Boscolo, D.; Viana, B.F. Landscape and crop management strategies to conserve pollination services and increase yields in tropical coffee farms. Agric. Ecosyst. Environ. 2018, 256, 218–225. [Google Scholar] [CrossRef]
- Geeraert, L.; Aerts, R.; Berecha, G.; Daba, G.; De Fruyt, N.; D´hollander, J.; Helsen, K.; Stynen, H.; Honnay, O. Effects of landscape composition on bee communities and coffee pollination in Coffea arabica production forests in southwestern Ethiopia. Agric. Ecosyst. Environ. 2020, 288, 106706–106717. [Google Scholar] [CrossRef]
Figure 1.
Study sites located in Colombia coffee-growing region. (A) Pueblo Bello Experiment Station; (B) San Antonio Experiment Station; (C) Paraguicito Experiment Station; (D) Naranjal Experiment Station; and (E) Manuel Mejía Experiment Station.
Figure 1.
Study sites located in Colombia coffee-growing region. (A) Pueblo Bello Experiment Station; (B) San Antonio Experiment Station; (C) Paraguicito Experiment Station; (D) Naranjal Experiment Station; and (E) Manuel Mejía Experiment Station.
Figure 2.
Naranjal Experiment Station. Yellow marker (coffee plots). Blue marker (natural vegetation and secondary forest).
Figure 2.
Naranjal Experiment Station. Yellow marker (coffee plots). Blue marker (natural vegetation and secondary forest).
Figure 3.
Diversity profiles of order q for (a) general; (b) Pueblo Bello Experiment Station; (c) San Antonio Experiment Station; (d) Paraguaicito Experiment Station; (e) Naranjal Experiment Station; and (f) Manuel Mejía Experiment Station.
Figure 3.
Diversity profiles of order q for (a) general; (b) Pueblo Bello Experiment Station; (c) San Antonio Experiment Station; (d) Paraguaicito Experiment Station; (e) Naranjal Experiment Station; and (f) Manuel Mejía Experiment Station.
Figure 4.
Distribution of abundances at different sampling times, where the central line is the median and boxes and vertical lines represent the quartiles.
Figure 4.
Distribution of abundances at different sampling times, where the central line is the median and boxes and vertical lines represent the quartiles.
Figure 5.
Functional groups for the flower-visiting bee community in coffee and representation of the functional space for each group, obtained by non-metric multidimensional scaling.
Figure 5.
Functional groups for the flower-visiting bee community in coffee and representation of the functional space for each group, obtained by non-metric multidimensional scaling.
Figure 6.
Pollen load for the most abundant and frequent bee species flower-visiting in coffee crops.
Figure 6.
Pollen load for the most abundant and frequent bee species flower-visiting in coffee crops.
Table 1.
Description of study sites located in Colombia coffee-growing region [18].
Table 1.
Description of study sites located in Colombia coffee-growing region [18].
| Study Sites | Location | Climate Conditions | Harvest Distribution | Area Cultivated in Coffee (Hectares) |
|---|---|---|---|---|
| (A) Pueblo Bello Experiment Station | Municipality of Pueblo Bello (department of Cesar), located in the Sierra Nevada de Santa Marta mountain range (10°25′ N; 73°34′ W); altitude: 1134 m above sea level; coffee ecotope: 402. | Average temperature of 27.9 °C; mean relative humidity of 78.3%; annual precipitation of 1727.7 mm; and 2302 h of sunshine/year. | Main harvest (90%): flowering between March and April; mid harvest (10%): flowering between August and September. | 25.6 |
| (B) San Antonio Experiment Station | Municipality of Floridablanca (department of Santander), Cordillera Oriental mountain range, western slope (07°06′ N; 73°04′ W); altitude: 1539 m above sea level; coffee ecotope: 302A. | Average temperature of 20.1 °C; average RH of 79.4%; annual precipitation of 1644 mm; 1155 h of sunshine/year. | Main harvest (90%): flowering between March and April; mid harvest (10%): flowering between August and September. | 3.22 |
| (C) Paraguaicito Experiment Station | Municipality of Buenavista (department of Quindío), Cordillera Central mountain range, western slope (04°4′ N; 75°44′ W); 1303 m above sea level; coffee ecotope: 211A. | Average temperature of 22.4 °C; average RH of 78.4%; annual precipitation of 1938 mm; 1541 h of sunshine/year. | Main harvest (55%): flowering between February and March; mid harvest (45%): flowering between August and September | 16.3 |
| (D) Naranjal Experiment Station | Municipality of Chinchiná (department of Caldas), Cordillera Central mountain range, western slope (4°58′ N; 75°39′ W); 1381 m above sea level; coffee ecotope: 206A. | Average temperature of 21.6 °C; average RH of 80.6%; annual precipitation of 2990 mm; 1537 h of sunshine/year. | Main harvest (75%): flowering between January and March; mid harvest (25%): flowering between August and September. | 48.7 |
| (E) Manuel Mejía Experiment Station | Municipality of El Tambo (department of Cauca), Cordillera Central, western slope (02°24′ N; 76°44′ W); altitude: 1735 m above sea level; coffee ecotope: 218A. | Average temperature of 19.8 °C; average RH of 81.1%; annual precipitation of 1826 mm; 1632 h sunshine/year. | Mid harvest (10%): flowering between February and March; main harvest (90%): flowering between August and September | 10.9 |
Table 2.
Functional traits selected to characterize the functional diversity of the bee community.
| Trait | Status of Trait | Type of Variable |
|---|---|---|
| Nesting habit | Pre-existing cavities in the ground, pre-existing cavities, new cavities in the ground, tree branches, decaying wood, dry logs and wood, and dry branches. | Nominal categorical |
| Degree of sociability | Eusocial, parasocial, solitary (subsocial and solitary), facultative parasocial, and facultative eusocial. | Nominal categorical |
| Size (mm) | Mean of the intertegular distance for collected individuals; maximum 20 individuals measured. | Continuous numeric |
| Stigma contact | Very frequent; always; occasional; never. | Nominal categorical (numeric for the FD package) |
| Location of pollen loading structure | Tibial, femorotibial, basitarsotibial, and gasteral. | Nominal categorical |
| Type of tongue | Short, long, and very long. | Ordinal categorical |
| Abundance from 7:00 to 9:30 | Number of individuals. | Whole numbers |
| Abundance from 10:30 to 13:00 | Number of individuals. | Whole numbers |
| Abundance from 14:00 to 16:30 | Number of individuals. | Whole numbers |
Table 3.
Estimate of number of species and sampling coverage of flower-visiting insects in coffee crops per study site and in general.
Table 3.
Estimate of number of species and sampling coverage of flower-visiting insects in coffee crops per study site and in general.
| Study Sites | Species Observed | Singletons | Sampling Coverage | Expected Species | Percentage Species in Sample | ||
|---|---|---|---|---|---|---|---|
| Chao1 | ACE | Chao1 | ACE | ||||
| Pueblo Bello E.S * | 70 | 36 | 0.991 | 133 | 155.8 | 52.6 | 44.9 |
| San Antonio E.S | 141 | 99 | 0.988 | 679.9 | 510.1 | 20.7 | 27.6 |
| Paraguaicito E.S | 233 | 125 | 0.973 | 405.2 | 439.2 | 57.5 | 53 |
| Naranjal E.S | 288 | 145 | 0.970 | 496.8 | 529.3 | 58.0 | 54.4 |
| Manuel Mejía E.S | 99 | 61 | 0.973 | 302.2 | 277.0 | 32.8 | 35.7 |
| General | 566 | 254 | 0.989 | 874.9 | 921.6 | 64.7 | 61.4 |
* E.S = experiment station.
Table 4.
Estimate of the number of species and sampling overage of the bee community per site and in general.
Table 4.
Estimate of the number of species and sampling overage of the bee community per site and in general.
| Study Sites | Observed Species | Singletons | Sampling Coverage | Expected Species | Percentage Species in Sample | ||
|---|---|---|---|---|---|---|---|
| Chao1 | ACE | Chao1 | ACE | ||||
| Pueblo Bello E.S * | 30 | 11 | 0.997 | 48.3 | 55.5 | 62.1 | 54.1 |
| San Antonio E.S | 23 | 9 | 0.999 | 35.0 | 48.2 | 65.7 | 47.7 |
| Paraguaicito E.S | 33 | 10 | 0.997 | 37.1 | 41.1 | 88.9 | 80.3 |
| Naranjal E.S | 51 | 18 | 0.995 | 66.3 | 71.1 | 76.9 | 71.7 |
| Manuel Mejía E.S | 20 | 7 | 0.996 | 27.0 | 28.2 | 74.1 | 70.9 |
| General | 90 | 29 | 0.999 | 119 | 125.3 | 75.6 | 71.8 |
* E.S = experiment station.
Table 5.
Functional diversity indices calculated for the flower-visiting bee community in coffee crops per site and in general.
Table 5.
Functional diversity indices calculated for the flower-visiting bee community in coffee crops per site and in general.
| Study Sites | Functional Species | FEve a | FDiv a | FDis a |
|---|---|---|---|---|
| Pueblo Bello E.S * | 30 | 0.37 | 0.98 | 0.18 |
| San Antonio E.S | 23 | 0.39 | 0.93 | 0.16 |
| Paraguaicito E.S | 33 | 0.43 | ~1.00 | 0.10 |
| Naranjal E.S | 51 | 0.39 | 0.99 | 0.27 |
| Manuel Mejía E.S | 20 | 0.45 | ~1.00 | 0.16 |
| General | 90 | 0.41 | 0.99 | 0.19 |
* E.S = experiment station. a FEve = functional evenness; FDiv = functional divergence; FDis = functional dispersion.
Table 6.
Estimated values of different indices for each site and bee species.
| Study Sites | Species | VR(A) a | PCC a | C a | PE a | PIV a |
|---|---|---|---|---|---|---|
| Pueblo Bello E.S | A. mellifera | 73.62 | 0.47 | 0.98 | 1.00 | 33.51 |
| N. gaboi | 4.12 | 0.53 | 0.94 | 0.92 | 1.91 | |
| T. angustula | 4.30 | 0.47 | 0.99 | 0.67 | 1.33 | |
| Scaptotrigona sp. 1 | 4.64 | 0.44 | 0.93 | 0.92 | 1.77 | |
| San Antonio E.S | A. mellifera | 73.29 | 0.47 | 0.95 | 1.00 | 32.81 |
| Geotrigona cf. tellurica | 17.24 | 0.53 | 0.97 | 0.92 | 8.10 | |
| Paraguaicito E.S | A. mellifera | 70.62 | 0.90 | 0.93 | 1.00 | 59.13 |
| Lasioglossum spp. | 2.64 | 0.10 | 0.64 | 0.65 | 0.11 | |
| Naranjal E.S | A. mellifera | 40.82 | 0.39 | 0.98 | 1.00 | 15.62 |
| N. tristella | 2.91 | 0.22 | 0.97 | 0.87 | 0.53 | |
| T. angustula | 15.27 | 0.39 | 0.99 | 0.67 | 3.93 | |
| Manuel Mejía E.S | A. mellifera | 69.27 | 0.33 | 0.94 | 1.00 | 21.75 |
| Partamona cf. peckolti | 7.12 | 0.35 | 0.86 | 0.93 | 2.00 | |
| T. angustula | 7.03 | 0.31 | 0.95 | 0.67 | 1.41 |
E.S = Experiment station. VR (A) a = estimated visit rate (relative abundance); PCC a = pollen-carrying capacity; C a = flower constancy; PE a = pollinator effectiveness; and PIV a = pollination importance value.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Maldonado-Cepeda, J.D.; Gómez, J.H.; Benavides, P.; Jaramillo, J.; Gil, Z.N. Taxonomic and Functional Diversity of Flower-Visiting Insects in Coffee Crops. Insects 2024, 15, 143. https://doi.org/10.3390/insects15030143
AMA Style
Maldonado-Cepeda JD, Gómez JH, Benavides P, Jaramillo J, Gil ZN. Taxonomic and Functional Diversity of Flower-Visiting Insects in Coffee Crops. Insects. 2024; 15(3):143. https://doi.org/10.3390/insects15030143
Chicago/Turabian StyleMaldonado-Cepeda, Juan Diego, Jesús Hernando Gómez, Pablo Benavides, Juliana Jaramillo, and Zulma Nancy Gil. 2024. "Taxonomic and Functional Diversity of Flower-Visiting Insects in Coffee Crops" Insects 15, no. 3: 143. https://doi.org/10.3390/insects15030143
Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.
