The abundance of ants (Hymenoptera: Formicidae) and their ecological roles as predators in Arabica coffee plantations with different densities of shade trees

Shade-grown coffee, incorporated in an agroforestry system, is a common practice of coffee plantations in Aceh Tengah Regency, Aceh Province, Indonesia. Coffee is grown under the shade of a canopy of surrounding trees. Shade trees reduce excessive light and provide a home for various predatory animals, including predatory ants. Some growers plant a dense population of shade trees, while others plant less shade trees. A study to investigate the diversity of ants and their abundance in different densities of shade trees has been conducted from April until August 2023. Ants were sampled from coffee trees (arboreal ants) in two coffee plantations with dense populations of shade trees and two plantations with sparse shade trees. We found 13 ant species in both categories of plantations (combined). All ant species were found in sparsely shaded coffee plantations, and only five were recorded from densely shaded plantations. However, the abundance of ants was much higher in densely shaded plantations than in sparsely shaded plantations. The ant genera Technomyrmex and Componatus were the dominant ants found in sparsely shaded plantations, while the dominant ants in densely shaded plantations were the genera Componatus and Crematogaster. These ants are known as general predators and potentially are predators of coffee berry borer (CBB), a significant pest in the area. This research has shown how different densities of shade trees in coffee plantations affected the ant fauna, which could be used as a basis for ant conservation to increase their ecosystem service as predators.


Introduction
Most coffee plantations employ agroforestry systems to produce an environment on the farm that mimics a small forest by forming tree canopy stratification.The most commonly found agroforestry system is a combination of coffee plants with fast-growing plants that also function as shade trees for coffee plantations [1].The shade trees that are widely used in coffee plantations in Indonesia are Leucaena sp., Gliricidia maculate, Erythrina sp., Casuarina sp., and Paraserianthes falcataria.Orange trees are also often used as shade trees on coffee plantations in the highlands.Shade trees are necessary for a sustainable coffee-growing system.Planting coffee without shade trees can cause accelerated land degradation and threaten the sustainability of coffee cultivation on that land [2].1297 (2024) 012048 IOP Publishing doi:10.1088/1755-1315/1297/1/012048 2 Shade trees with wide canopies, flat branches, and lots of leaves allow many insects to prefer this habitat as a place to live [3].Shade trees provide a habitat for natural enemies of pests and pathogens, thus improving their ecosystem services as biological control agents [4].The presence of shade trees can also increase the abundance and diversity of ants.In shaded coffee plantations, the level of ant predation on other insects reaches 15%, while in coffee plantations without shade, it is only 6%.Several species of ants from the genera Temnothorax, Wasmannia, and Crematogaster are found to be predators of coffee berry borer (CBB) (Hypothenemus hampei Ferr) [5].Other ant species, such as Azteca instabilis and Phedole synanthripica, have been known to reduce CBB damage on the plant [6].Coffee berry borer has been widely recognized as the most destructive pest of coffee berry, including in Indonesia.Infestations of CBB can result in substantial coffee production losses and lower the quality of the coffee beans [7].
Shade regulation in coffee plantations can influence the activities of predatory ants.The diversity of ants in a habitat is influenced by the type of vegetation around the land, plant structure, and shade height.Ant species are more diverse in coffee plantations planted using traditional farming systems with tall, dense shade trees [8].An earlier study recorded five subfamilies and 17 morphospecies of ants collected using pitfall traps in coffee plantations in Aceh Tengah Regency.They belonged to the subfamily Myrmicinae, Pseudomyrmecinae Formicinae, Ponerinae, and Dolichoderinae.Most ant species recorded were general foragers, and some are recognized as CBB predators [9].
During preliminary visits to coffee plantations in Aceh Tengah Regency, it was observed that some growers plant a dense population of shade trees, while others plant sparse shade trees in their plantations.In this study, we determined the effect of densely and sparsely shaded coffee plantations on the number of arboreal ants, their abundance, and their potential roles as predators in the coffee plantations.The results of this research can provide information regarding the technicalities of coffee cultivation by regulating the density of shade trees to conserve arboreal ants and increase their ecological service as predators so that biological pest control efforts can be carried out optimally.

Study site
Ant sampling was done in Aceh Tengah Regency, where most Arabica coffee is grown.The area is located around 300 km away from the capital city of Banda Aceh and is one of the three regencies in the Gayo Highlands in Aceh Province, Indonesia.The coffee bean produced in this area is known as Gayo Coffee for its unique taste.This region is situated 200 to 2600 meters above sea level.The ants were sampled from four organic coffee plantations located between 1100 and 1300 above sea level and grown by local communities.Environmental conditions such as light intensity, temperature, and humidity in the ant sampling location were measured three times in different spots between 12.00 and 1.00 p.m. during the sampling period.Each plantation was around 1 ha, and the coffee trees were aged between 10 and 15 years.The growers mainly used compost from coffee berries skin as fertilizer, and no chemicals were applied to control pests.Many other plants, such as Leucaena, avocado, orange, guava, and persimmon, are grown as shade trees between coffee plants.Some of the plants are purposedly grown for their economic value.Preliminary observation showed no specific rules for shade trees; some growers planted dense shade trees while others planted the shade trees sparsely.
In this study, we set the shade trees into two categories based on the number of shade trees found in a flat plot of 35 x 35 m 2 on each plantation.When the number of shade trees was ≥35, the plantation was categorized as a densely shaded coffee plantation.In contrast, the plot with shade trees < 35 was classified as a sparsely shaded coffee plantation.Each plot contains 100 coffee plants roughly.We divided each plot into four subplots of 10 x 10 m 2 , where ten coffee plants of 1.5-2.0m in height were chosen randomly as plant samples so that there were 40 coffee plant samples in each plantation plot.We used two coffee plantations for each density shade trees category (Table 1), and ant sampling was done once for each coffee plantation.The range of light intensity, temperature, and humidity in each location is presented in Table 1.

Sampling of ants
The sampling of ants was focused on the ant fauna that live and forage on the coffee plants (arboreal ants).Ants were collected from 40 coffee tree samples in each plot using a slightly modified method developed by [10].Ants were visually observed on each coffee plant sample before shaking branches on the plant for 3 minutes.Then, using a tiny brush, the visible ants were carefully collected from branches, leaves, stems, and berries while circumnavigating the coffee tree for four minutes.Small plastic bottles filled with 70% alcohol were used to store the collected ant samples before being brought to the Faculty of Agriculture's Biological Control Laboratory for identification.The ants were then identified by looking at their morphology under a microscope.The identification process was carried out by consulting the findings of earlier research [9], [11], [12], as well as the digital source (http://www.antweb.org).All individuals of each ant species were calculated and placed in separate collection bottles based on the categories of shade tree coffee plantations.Ant sampling was done during June 2023 and continued with laboratory work until mid-August 2023.

Analysis of data
Ant fauna was identified morphologically to the genus to understand their function in the coffee plantations.Ant species number and their abundance were counted from 40 coffee plant samples from two coffee plantations in each category of shade tree densities, and they were analyzed by using an unpaired T-Test.The threshold for a significant difference between the two categories of shade trees was chosen at P 0.05.

Ant fauna and their potential role as predators
We collected 3717 ants, which consisted of 4 subfamilies and 13 morphospecies from the four coffee plantations.Five ant species belonged to the subfamilies Myrmicinae and Dolichoderinae each, while the two species belonged to the subfamily Formicinae and one species to the subfamily Pseudomyrmicinae.All of the 13 ant morphospecies were present in sparsely shaded coffee plantations, and only five species were found in densely shaded plantations (Table 2).Despite that, ants were observed in each coffee plant sample, with at least one species of ant per plant.There were 1-4 ant species per plant in sparsely shaded plantations and 1-3 in densely shaded ones.A two-sample t-test was performed to compare the number of ant species per coffee plant between sparsely and densely shaded coffee plantations.There was no significant difference in the number of ant species per plant between sparsely shaded (t-test, P = 0.09, t=1.69, df=158) (Figure 1).This study showed that ants were common in all coffee plant samples in both categories of coffee plantations despite the different number of ant species at the plantation level.Numerous ant species (5 morphospecies) that belonged to the subfamily Myrmicinae in this finding were similar to previous research in the area both in organic and conventional coffee plantations [9] and other places [13], including in other agricultural plants like wheat and potatoes [14].Known as dominating arboreal species, ant species from the subfamilies Formicinae, Dolichoderinae, and Myrmicinae typically develop large colonies on the plants [15].During the sampling period, large ant nests were seen on surrounding shade trees and coffee bushes.Ant species that belonged to the subfamily Dolichoderinae were similarly high, with five morphospecies (Table 2).Even though the ant species observed were arboreal ants that nest and forage on the plants, some ant species also could be found on the ground simultaneously, exhibiting their generalist behaviour in foraging and nesting locations.Previous studies showed that arboreal ants, including twig-nesting, carton-nesting, and weaver ants, often build their nests and forage on shade trees and coffee plants.However, some ant species are generalists in their habitat preferences for foraging and breeding, and they may be found both on the ground and on plants, sometimes in the same place [16], [17].Ants can play various ecological roles depending on the species and the area in which they live.Among all ant genera recorded here, some of them potentially are predators of CBB on coffee plantations, such as Technomyrmex, Tapinoma, Camponatus, Tetramorium Crematogaster, and Tetraponera.The ant species belong to the genus Technomyrmex known as tramp ants, and are endemic to East, Southeast, and South Asia [18].They consume nectar or sugar as an energy source.
Technomyrmex albipes are even considered secondary pests in agriculture because they protect honeydew-producing insects such as aphids and mealybugs that benefit them [19].However, a study in Thailand showed that T. modiglianii and T. yamanei attacked CBB individuals.The same study also found that Tapinoma, Camponatus, and Crematogaster did attack CBB during laboratory observation [20].Tetramorium acuelatum is an aggressive predator because it attacks its prey with a sting [21].One species of Tapinoma, which feeds on coffee berries and consumes CBB, has been identified as a CBB predator in Mexico [22].
Several species of ant genera recorded in this study may play an essential role in regulating the CBB population.Ants can interact with free-roaming CBB and CBB within berries, both on coffee plants and on the ground, resulting in biological control of CBB in various ways [23].Arboreal ants may help control pests through predation, non-consumptive assaults, and indirect chemical deterrents [24], [23].In coffee plants, arboreal ants readily feed and tend hemipteran insects, frequently sustaining high activity levels close to coffee berries on branches; this provides a chance for interaction with adult CBB individuals as the pests inhabit coffee berries [23].

Composition of ants and their abundance
The total number of ants recorded from sparsely shaded plantations was 746 individuals, while in densely shaded ones, it was 2971 individuals.The composition of individual ants in both categories of coffee plantations was dominated by the genera Camponatus, which were 64.21 % in sparsely shaded plantations and 93.50 % in densely shaded ones, out of other genera (Figure 2).The abundance of ants from each genus found in this study greatly varied.In sparsely shaded plantations, the number of ants recorded was from one individual of Technomyrmex sp3 and Crematogaster sp3.and up to 276 individuals of Camponatus sp 2. Similarly, in densely shaded plantations, from one individual of Technomyrmex sp1 up to 2119 individuals of Camponatus sp 2.
These results showed that despite the fewer ant species found in densely shaded plantations, their abundance was three times higher than that in sparsely shaded ones.At the coffee plant level, the abundance of ants ranged from one up to 25 ants per plant in sparsely shaded plantations, while in densely shaded ones, it ranged from four up to 229 ants per plant.The average number of ants per plant was significantly different between the two types of shaded plantations (t-test, P <0.0001, t=6.21, df=158) (Figure 3).The genus Camponatus was abundantly found on plant samples when they were present.They colonized coffee leaves and folded the leaves into small nests so that the samples were taken together with the leaves.It has been known that the growth of an ant population is favoured by using shade trees in coffee plantations.The dominant ant species of Camponatus found in this study showed that this genus could nest and forage well in the area.
The ant species of the genus Camponatus can build their nests in soil, underneath stones, decaying wood, or in living plants.Camponotus is sometimes known as "carpenter ants" because some species can create nesting chambers in solid wood, including wooden constructions seen in houses [25].There are many different species of ants in the genus Camponotus, some of which are known to prey on CBB in coffee plantations [20].However, it is important to remember that the effectiveness of ant predation can change based on ant species composition, environmental circumstances, and other coffee berry borer natural enemies [23].In this study, we have shown that arboreal ants forage and nest in both categories of shaded coffee plantations.More ant species were found in sparsely shaded plantations, but a much higher number of individual ants were found in densely shaded plantations.Since there are no sun coffee plantations in the area, we cannot compare the ant fauna found in this type of coffee plantation and shaded coffee plantations.Previous studies in Columbia [13], [26] showed that shaded coffee plantations provide more opportunities for the ant fauna to live and develop in the plantations.

Conclusions
Sparsely shaded coffee plantations attracted more ant species, but the abundance of individual ants was much higher in densely shaded plantations.Componatus was the most abundant genus in both categories of shaded plantations.Some species of this genus are known to prey on essential pests such as CBB in coffee plantations.This study illuminated how the ant fauna was impacted by various shade tree densities in coffee plantations, providing a theoretical framework for ant conservation to strengthen their functions as predators.

Figure 1 .
Figure 1.Number of ant species per coffee plant found in sparsely shaded and densely shaded coffee plantations in Aceh Tengah Regency.

Figure 2 .
Figure 2. Composition of individual ants found in sparsely shaded (a) and densely shaded coffee plantations (b) in Aceh Tengah Regency.

Figure 3 .
Figure 3.The abundance of individual ants per coffee plant found in sparsely shaded and densely shaded coffee plantations in Aceh Tengah Regency.

Table 1 .
Light intensity, temperature and humidity in the ant sampling location.

Table 2 .
Ant fauna sampled from densely and sparsely shaded coffee plantations in Aceh Tengah Regency, Aceh, Indonesia.