Agronomía Mesoamericana
Technical note
Volumen 34(2): Artículo 50757, 2023
e-ISSN 2215-3608, https://doi.org/10.15517/am.v34i2.50757
https://revistas.ucr.ac.cr/index.php/agromeso/index
Entomofauna associated to tropical pastures, Cenchrus ciliaris, Chloris gayana, and Megathyrsus maximus1
Entomofauna asociada a pasturas tropicales Cenchrus ciliaris, Chloris gayana y Megathyrsus maximus
Paola Vanessa Sierra-Baquero2, Tatiana Sánchez-Doria2, Esteban Burbano-Erazo2
1 Reception: June 8th, 2022. Acceptance: October 6th, 2022. This work was part of the research generated from a funded proyect by Ministerio de Agricultura y Desarrollo Rural (MADR)–Colombia and executed by Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA).
2 Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Km 5 WayBecerril, Agustin Codazzi, Cesar, Colombia. psierra@agrosavia.co (corresponding author; https://orcid.org/0000-0001-9016-9982); tsanchezd@agrosavia.co (https://orcid.org/0000-0001-5797-770X); eburbanoe@unal.edu.co (https://orcid.org/0000-0001-5056-9893).
Abstract
Introduction. Pastures are the primary source of food in livestock systems and can be a suitable niche for insects with beneficial and harmful functions. Objective. To estimate the entomofauna associated with three species of pastures, Cenchrus ciliaris, Chloris gayana, and Megathyrsus maximus, in conditions of the Colombian Caribbean. Materials and methods. Ten samplings were carried out in two contrasting periods (August to October 2018 and January to March 2019), three forage species (Cenchrus ciliaris, Megathyrsus maximus, Chloris gayana) within 1000 m2 were used. Arthropods were identified by order and family and typified by functional groups. Diversity and abundance indices by pasture and season were estimated, as well as their correlation with climate. A simple correspondence analysis was performed. Results. A total of 380 insects from 7 orders and 35 families were collected, with the greatest abundance for Hemiptera and Coleoptera. The Shannon’s diversity index was higher for all orders of C. gayana, except for Hemiptera in C. ciliaris. Phytophages were found in a higher percentage (66.84 %), followed by predators (27.11 %). Insect abundance was influenced by the interaction between season and pasture, showing an increase at low temperatures, except for M. maximus. Pastures represented adequate microenvironments to maintain the diversity of insects, the Hemiptera and Coleoptera orders being the most numerous and representative of the functional groups of phytophages and predators, respectively. Conclusion. The entomofauna of C. gayana, C. ciliaris, and M. maximus was similar in insect abundance and diversity, however, insect abundance depended on the influence of the season and pastures.
Keywords: biological control, crops, biological diversity.
Resumen
Introducción. Los pastos son la principal fuente de alimento en los sistemas ganaderos y pueden ser un nicho adecuado para insectos con funciones beneficiosas y dañinas. Objetivo. Estimar la entomofauna asociada a tres especies de pastos, Cenchrus ciliaris, Chloris gayana y Megathyrsus maximus, en condiciones del Caribe colombiano. Materiales y métodos. Se realizaron diez muestreos en dos estaciones contrastantes, de baja y alta precipitación (agosto a octubre de 2018 y enero a marzo de 2019), se utilizaron tres especies forrajeras (Cenchrus ciliaris, Megathyrsus maximus, Chloris gayana), en un área de 1000 m2. Los artrópodos fueron identificados por orden y familia y tipificados por grupos funcionales. Se estimaron índices de diversidad y abundancia por pastos y estaciones, así como su correlación con el clima. Se realizó un análisis de correspondencia simple. Resultados. Se recolectaron 380 insectos de siete órdenes y 35 familias, con mayor abundancia para Hemiptera y Coleoptera. El índice de diversidad de Shannon fue más alto para todos los órdenes de C. gayana, excepto para Hemiptera en C. ciliaris. Los fitófagos se encontraron en mayor porcentaje (66,84 %), seguidos de los depredadores (27,11 %). La abundancia de insectos estuvo influenciada por la interacción entre la estación y el pasto, mostró un incremento a bajas temperaturas, excepto para M. maximus. Los pastos representaron microambientes adecuados para mantener la diversidad de insectos, los órdenes Hemiptera y Coleoptera fueron los más numerosos y representativos de los grupos funcionales fitófagos y depredadores, respectivamente. Conclusión. La entomofauna de C. gayana, C. ciliaris y M. maximus fue similar en abundancia y diversidad de insectos, sin embargo, la abundancia dependió de la influencia de la estación y de los pastos.
Palabras clave: control biológico, cultivos, diversidad biológica.
Introduction
Pastures are considered the primary food source in animal production systems, both for ruminants and minor species (Alothman et al., 2019). In Colombia, pasture and forage production is mainly focused on livestock, most are introduced or naturalized species (Negawo et al., 2020). The species Chloris gayana, Cenchrus ciliaris, and Megathyrsus maximus are native to Africa and naturalized in the tropics and subtropics. They have intrinsic characteristics such as tolerance to drought, adaptation to areas with annual rainfall regimes between 100 – 500 mm (Negawo et al., 2020).
Crops are agrosystems with many interactions between plants and animals, which perform maintains the balance between harmful and beneficial populations (Jarvis et al., 2011). In the case of entomofauna associated with pastures, it is necessary to know the functional groups to prove this relationship. The arthropods have role in the agroecosystem related to the consumer habit; as phytophages, they can act as pests for have a high colonization capacity and large populations. These are regulated by the group of consumers called “natural enemies” made up of predators and parasitoids (Alomar & Albajes, 2005). There are also decomposer, pollinator and omnivorous arthropods that play an essential role in agroecosystems (Caraballo-Gracia et al., 2019). Therefore, it is essential to determine biodiversity that exists in this type of production system to preserve natural habitats and guarantee the ecosystem services provided by beneficial insect populations against pests (Altieri & Nicholls, 2012). In this context, it is important to be aware of the interactions and relationships established by insects in an agroecosystem, accord to their trophic functions or consumption habits, especially those pest insects that produce adverse effects on growth, nutritional quality, and reproductive capacity of pastures, such as the froghoppers (commonly known as salivazo or mion) Aeneolamia sp., and Zulia sp. (Hemiptera: Cercopidae), considered the main pest for pastures that feed in livestock in tropical America (Valerio et al., 2001).
There are other pest insects, such as Blissus leucopterus, B. insularis (Hemiptera: Lygaeidae), Collaria sp. (Hemiptera: Miridae) (Giraldo et al., 2011), Spodoptera sp., Mocis latipes (Lepidoptera: Noctuidae), chrysomelids of the genus Systena, and Epitrix, ants of the genus Atta and Acromyrmex. On the other hand, the biological function of predatory insects such as flies (Syrphidae: Salpingogaster nigra), may beetles (Carabidae: Leptotrachelus sp.), bugs (Reduviidae: Apiomerus lanipes), and various spiders (Salticidae) (Giraldo et al., 2011).
Insect diversity is quite relevant because it contributes to the structuring of communities in pastures, pollination, and nutrient cycling (Whiles & Charlton, 2006). By typifying the entomofauna, the harmful or beneficial behavior of arthropods can be generalized to a great extent, being essential to determine their functional role in agroecosystems of interest to devise comprehensive management strategies.
This study sought to determine the entomofauna associated with three species of pastures, Cenchrus ciliaris, Chloris gayana and Megathyrsus maximus, in conditions of the Colombian Caribbean.
Materials and methods
Research site
The study was carried out at the Motilonia Research Center of the Corporación Colombiana de Investigación Agropecuaria (Agrosavia), municipality of Agustín Codazzi, Cesar, Colombia. It is geographically located on the coordinates 10°01’55.5’ N and 73°13’30” W at an elevation of 106 m.a.s.l., with an annual rainfall of 1585 mm (1980 – 2017), average annual temperature of 27 °C, average relative humidity of 71 %, and sunlight of 6.9 hours/day (Instituto de Hidrología, Meteorología y Estudios Ambientales, 2020). The research site was 1000 m2 paddocks for each specie (C. ciliaris, M. maximus, and C. gayana) from the germplasm bank of the alliance between Bioversity Internacional and the Centro Internacional de Agricultura Tropical (CIAT).
Entomofauna sampling and review
Ten samplings were carried out in two seasons of the year of the Colombian dry Caribbean region: the rainy season (August to October 2018) and the dry season (January and March 2019). The collections were made weekly; the collection method was direct with an entomological network, which consisted in four double passes over ten random points homogenized for each pasture. Some direct collections were also made on organs such as flowers and leaves, and roots were checked. The insects were organized at the Entomology Unit of the Agrosavia’s Motilonia Research Center (RC). Then, samples of the specimens were submitted to the “Luis Maria Murillo” National Insect Collection Department, attached to Agrosavia, for identification by specialists.
Definition of functional groups and beneficial relationship index
Functional roles in the collected entomofauna were identified based on bibliographic information Zumbado Arrieta and Azofeifa Jiménez (2018); and field observations of structural, physiological, morphological features or life habits. Therefore, the functional group was assigned by to the main consumption habit of most members of the family to which each collected specimen belonged. Given that some families have a broad functional diversity that could alter the results of the analysis, functional groups such as omnivores, represented by the Formicidae family, and pollinators, which reported small abundance, were not considered.
Entomofauna of the three pastures data analysis
The collected insect diversity was determined by abundance and richness from the quantification of the number of individuals of each family by taxonomic order. Orders were compared in a general way, and later, analyzed for each pasture. Matrices were constructed to estimate diversity by calculate specific richness with Margalef’s index (equation 1) (Margalef, 1956).
Where S is the number of families and N the total number of individuals).
The abundance was calculate with the Shannon-Wiener’s index (equation 2) (Shannon, 1948) and Simpson’s dominance index (equation 3).
Where pi is the number of individuals of the I family divided by the total number of individuals of the sample) (Simpson, 1949).
The predicted number of families was estimated non-parametric models of the Chao1 index (equation 4) (Moreno, 2001).
Where C: Chao1, S: number of families in a sample, a: number of families represented by a single individual, and b: families with two individuals).
The indices were estimated through Paleontological Statistics, version 2.17c (Hammer et al., 2001), also they were also statistically compared using permutation and bootstrapping tests. Variance analysis was also performed to compare the orders at a general level, considering the parameters and diversity indices mentioned, using SAS, version 9.4.
Functional groups and beneficial insect relationship index data analysis
The insect abundance of the functional groups was estimated as a percentage in each pasture and season evaluated. At the same time, the typification of families by functional group allowed to calculate the beneficial functional relationship index (BRIN) of the entomofauna collected by pasture and season to establish the relationship between phytophages and consumers (predators and parasitoids). The BRIN was calculated from the equation 5.
BRIN= ln(number of phytophages / number of consumers) (5)
Where ln is the natural logarithm of the coefficient of the number of phytophages and the number of consumers (Diaz et al., 2017).
Relationship between insect abundance in pastures and climatic conditions data analysis
General and mixed linear models were used to analyze the relationship between insect abundance in pastures and climatic conditions. Insect abundance was evaluated as a response variable, and pastures, seasons, and their interaction as independent variables with fixed effects. Also, the samplings were included as variables with random effects. This procedure was performed whit R, version 4.0.0 (R Core Team, 2020), interface with Infostat (Di-Rienzo et al., 2020). Correlations were established with the Spearman’s coefficient between entomofauna abundance and climatic conditions (accumulated rainfall, average temperature, and average relative humidity) with SAS, version 9.4 (Statistical Analysis System Institute, 2013). Finally, a simple correspondence analysis was carried out to define a multivariate level the relationship between the variable of abundance per family associated with the season and the pasture variables. The representativeness of each category to each component was defined through cosine squared with R.
Results
Entomofauna in C. ciliairis, C. gayana, and M. maximus
The results showed that 380 individuals were collected, distributed in seven orders and 35 families (Table 1). When analyzing insect diversity, a statistically significant difference between richness of the families (FR: number of families) grouped by order (p<0.0001) was noted, being greater in Hemiptera (10.66), followed by Coleoptera (6.66 FR), Hymenoptera (2.66 FR), and Diptera (1.66 FR). Abundance (Ab: number of individuals) results were similar, since Hemiptera was the most abundant (67.6 Ab), and Hymenoptera (4.00 Ab) the least (Table 2). When classifying insect abundance for each pasture, C. gayana had the most individuals (134 Ab), followed by M. maximus (127 Ab), and C. ciliaris (119 Ab). Hemiptera was the one with the highest number of individuals in the three pastures, being C. gayana the one with the highest average, following of Coleoptera mainly in M. maximus (Table 3).
Table 1. Insect abundance by order and families associated with three pastures (C. ciliaris, C. gayana, and M. maximus) in conditions of the Colombian dry Caribbean. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Cuadro 1. Abundancia de insectos por orden y familias asociados a tres pasturas (C. ciliaris, C. gayana y M. maximus) en condiciones del Caribe seco colombiano. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Centro de Investigación Motilonia, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Table 2. Diversity of the main insect orders present in three pastures (C. ciliaris, C. gayana, and M. maximus) in conditions of the Colombian dry Caribbean. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Cuadro 2. Diversidad de los principales órdenes de insectos presentes en tres pasturas (C. ciliaris, C. gayana y M. maximus) en condiciones del Caribe seco colombiano. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Centro de investigación Motilonia, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Table 3. Abundance and insect diversity indices associated with three pastures (C. ciliaris, C. gayana, and M. maximus) and two seasons (dry, rainy) in conditions of the Colombian dry Caribbean. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Cuadro 3. Abundancia e índices de diversidad de insectos asociados a tres pasturas (C. ciliaris, C. gayana y M. maximus) y dos estaciones (seca y lluviosa) en condiciones del Caribe seco colombiano. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Centro de Investigación Motilonia, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Shannon’s diversity index based on the relative abundance of families and Margalef’s wealth index were higher in C. gayana for all orders (Coleoptera, Diptera, and Hymenoptera), except for Hemiptera, which had the highest diversity and richness index in C. ciliaris. The family structures in the three evaluated pastures had a number of predicted species similar to that observed under the Chao1 index, except for the families of the order Coleoptera in C. ciliaris, and Hemiptera in M. maximus, because they reported fewer families than those predicted for those pastures (Table 2).
Functional groups and beneficial insect relationship index
The abundance of phytophagous and predators insects was greater in the rain season that in the dry season, with the Cantharidae family standing out among the predators in the C. ciliaris and C. gayana with 12 and 5 individuals, respectively. In the M. maximus the most abundant was the Coccinellidae family with 14 individuals. On the other hand, the phytophagous family Nogodinidae stood out with greater abundance in most of the pastures, surpassed the Membracidae family by one specimen in C. ciliaris. In the dry season, the Pachygronthidae and Nogodinidae families were the ones with the highest abundance of phytophagous insects, each one with 12 individuals in the C. gayana and M. maximus. The abundance of predators was higher in the Coccinellidae family of the M. maximus. Lastly, the parasites Braconidae with two individuals (M. maximus), Chalcididae and Platygastridae with one individual each family (C. gayana) (Tables 4 and 5).
Table 4. Abundance of entomofauna by order and families according to its main trophic group associated with three pastures (C. ciliaris, C. gayana, and M. maximus) during rainy season in conditions of the Colombian dry Caribbean. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Cuadro 4. Abundancia de entomofauna por orden y familia según su principal grupo trófico asociadas a tres pasturas (C. ciliaris, C. gayana y M. maximus), durante época de lluvias en condiciones del Caribe seco colombiano. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Centro de Investigación Motilonia, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Table 5. Abundance of entomofauna by order and families according to its main trophic group associated with three pastures (C. ciliaris, C. gayana, and M. maximus) during dry season in conditions of the Colombian dry Caribbean. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Cuadro 5. Abundancia de entomofauna por orden y familia según su principal grupo trófico asociadas a tres pasturas (C. ciliaris, C. gayana y M. maximus) durante época de sequía en condiciones del Caribe seco colombiano. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Centro de Investigación Motilonia, Agustín Codazzi, Cesar, Colombia. 2019-2020.
When considering the abundance percentage of the functional groups by season, the phytophages had the highest value, 67.28 % in the rainy season and 66.26 % in the dry season, while predators showed 29.04 % and 24.54 %, respectively. Besides, a more significant presence of decomposers (6.75 %) and parasitoids (2.45 %) was observed in the dry season, compared to the rainy season (decomposers with 3.23 % and parasitoids with 0.46 %).
The order Hemiptera was related to the functional group of phytophages (98.5 %), while Coleoptera reported the greatest diversity of functional groups with predators (61.6%) and parasitoids (38.4 %). Accordingly, phytophages and predators predominated in all pastures; however, M. maximus was the pasture with the highest percentage of decomposers (6.30 %) and parasitoids (2.00 %), contrary to C. gayana in which phytophages (81.34 %) dominated (Figure 1A). Similar proportions were also found between phytophages and predators, according to the BRIN. These results were found mainly in C. ciliaris (0.24 BRIN) and M. maximus (0.24 BRIN) during the rainy season (0.37 BRIN). The BRIN analysis between phytophages and parasitoids revealed a higher proportion of phytophages in the rainy season (2.16 BRIN), compared to the dry season (1.43 BRIN). In the case of pastures, very similar values among them were obtained (C. ciliaris = 1.57 BRIN, M. maximus = 1.57 BRIN, and C. gayana = 1.56 BRIN). A greater abundance of phytophages was registered in all the pastures and two seasons evaluated, which was reflected in a higher Shannon’s diversity index, because most of the collected insects belonged to the Hemiptera order.
Figure 1. Entomofauna associated with three pastures (C. ciliaris, M. maximus, C. gayana) in two seasons (rainy: A and dry: B). A) Functional groups. B) Insect abundance. Different letters showed statistical differences (p<0.05). Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Figura 1. Entomofauna asociada con tres pasturas (C. ciliaris, M. maximus, C. gayana) en dos estaciones (Lluvioso: A y sequía: B) del centro de investigación Motilonia, Cesar, Colombia. A) Grupos funcionales. B) abundancia de insectos. Diferentes letras muestran diferencias estadísticas (p<0,05). Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Centro de Investigación Motilonia, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Relationship of insect abundance with pastures and climatic conditions
The analysis of the Generalized Linear Mixed Models (GLMM) was highly significant (p<0.001; R2=0.53), with interaction between pastures and seasons (p<0.05). This result corroborates that insect abundance was influenced by the type of pasture, the rainfall, and drought conditions. In the rainy season, the average abundance was higher in C. ciliaris (18.60 ± 4.72 Ab), followed by C. gayana (15.60 ± 4.72 Ab), while in the dry season, the abundance was higher in M. maximus (16.20 ± 4.81 Ab). When the interaction occurred, the sources of variation were analyzed together. However, the abundance related to pastures (regardless of the season) registered the highest average in C. gayana (13.40 ± 3.89 Ab), followed by M. maximus (12.70 ± 3.89 Ab), and C. ciliaris (11.90 ± 3.89 Ab) (p=0.92), while the abundance in the rainy season (14.75 ± 3.55 Ab) was higher than in the dry period (10.87 ± 3.55 Ab) (p<0.27) (Figure 1B). A significant inverse linear correlation was found between the average temperature and abundance, especially of phytophages (R=-0.41; p<0.02); however, there was no correlation between abundance and rainfall.
The simple correspondence analysis revealed that the percentages of accumulated variance were 60.8 % and 39.2 % for the first and second dimensions, respectively. The first dimension was represented mainly by C. gayana (0.75) and the second by C. ciliaris (0.71) and M. maximus (0.73). Also, the relationship with the rainy (A) and drought (B) seasons was considerable. The families of insects with the most significant association with C. gayana, from the functional group of phytophages, were Cerambycidae_B, Curculionidae_B, and Pentatomidae _B. The predator families were Vespidae_ B and Chrysopidae_B. Finally, two of the three families of parasitoids were recorded in this pasture (Platygastridae_B, Chalcididae_A and B).
In C. ciliaris, the phytophages families Coreidae_B, Chrysomelidae_B, and Pachygronthidae_B, were the most reported. The predators were Reduvidae_A Cabronidae_A, and Tiphiidae_A, and the family of decomposers Sarcophagidae_A was found in this pasture. However, this variation can be conditioned by multiple environmental factors. Moreover, in M. maximus, insect families of phytophages such as Lygaeidae_B, Phyrrhocoridae_A, and Proscopiidae_B, predators such as Coccinellidae_A and B, and Reduviidae_B, and parasitoids such as Braconidae_B, were identified mainly in the dry season (Figure 2).
Figure 2. Map of factors that show the relationship among the three pastures (C. ciliaris, M. maximus, and C. gayana) in two seasons (rainy: A and dry: B), and the abundance of insects per family. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Motilonia Research Center, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Figura 2. Mapa de factores que presentan la relación entre tres pasturas (C. ciliaris, M. maximus y C. gayana) en dos estaciones (lluviosa: A y seca: B) y la abundancia de insectos por familia. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Centro de Investigación Motilonia, Agustín Codazzi, Cesar, Colombia. 2019-2020.
Discussion
The abundance of insects collected in this study of 380 individuals could be related to the collection method used by entomological network, because there are other more used and relevant methods for recording insect diversity, such as malaise traps that allow investigating communities of insects. Insects on large spatial and temporal scales, becoming important tools due to the large number of specimens collected through passive sampling (Uhler et al., 2022). Therefore, the insect collection method must be carefully selected, in order to potentiate sampling of individuals and estimate the diversity adequately.
In this research, the Coleoptera was considered as a representative order within the abundant entomofauna of the evaluated pastures, this finding could be due to the fact that coleopterans are the second largest and most diverse order in the planet (Rainio & Niemelä, 2003). Similarly, the high abundance of the order Coleoptera was similar to that reported by a study carried out in Tanzania, Africa, where a high diversity of the orders Hymenoptera and Coleoptera was found in M. maximus (Ojija et al., 2016).
According to the Shannon index obteined in this study, the order Coleoptera presented great abundance, this is possibly by having a greater availability of biomass in combination with climatic factors such as rain, coleopterans could easily develop considering their effects on the foliage as a pest and predatory behavior (Lee & Kwon, 2013). It could also be favorable to have a wide diversity of this order since many of them act as pest predators (New, 2019), as observed in this research in the Cantharidae and Coccinellidae families, which were very abundant in C. ciliaris, and M. maximus, respectively.
The orders Lepidoptera (one individual), Neuroptera (15 individuals from one family), and Orthoptera (three individuals from three families), registered few families and less abundance; therefore, it was not possible to calculate the diversity indices. Harmful or beneficial behavior of arthropods can be generalized to a great extent, being essential to determine their functional role in agroecosystems of interest to devise comprehensive management strategies. Some orders in this research were scarce, such as Orthoptera and Lepidoptera, which has been considered of high importance, mainly due the economic damage it may cause on pastures (New, 2019). For this order low values could be due to the active agricultural intervention in the surroundings of the research site, because the vast abundance of this order has been related to the restoration rates of some meadows (Rákosy & Schmitt, 2011).
The functional group of pollinators was not considered since only one individual was registered, nor the family Formicidae because it fulfills many functions for being omnivorous. The presence of pollinators was small, which agrees with the report of other evaluations in M. maximus (Ojija et al., 2016) and may be due to the limited availability of flowers during the evaluation period, or the preferred habit at the time of sampling (Collinge et al., 2003). Some orders of this functional group were also related to the functional group of parasitoids, which reported little abundance.
In this study, the abundance of arthropods found in the rainy season, which may be related to their adaptive capacity (Barnett & Facey, 2016). However, it has been reported that high levels of rainfall can also affect arthropod flight, limit feeding, and increase migration times (Kasper et al., 2008). In addition, it was found that in times of higher rainfall, grasses improve biomass availability, plant height, and soil cover, which favors the abundance and diversity of insects (Barnett & Facey, 2016).
The diversity of the Hemiptera order reported in this research may be due to the fact that the order has a great related adaptation within its evolutionary process, being considered one of the five most diverse orders (Szwedo, 2018). Likewise, their coevolution with grasses has been identified, and most of their families are characterized by being pests and vectors (Gullan & Cranston, 2014).
In C. ciliaris, was found that the highest abundance of the entomofauna was defined by the orders Orthoptera, Isoptera, and Hymenoptera (Patel, 2015), contrary to the results found in this study, since no Isoptera insects were reported and the abundance of the other orders was very limited not only in C. ciliaris. The plant component, depending on the use that insects make of it, may or may not favor the presence of pest and beneficial insects. It could also be considered that, in species highly adapted to drought conditions such as M. maximus, biomass availability could not be strongly compromised as it is a food source for insects in times of low rainfall (Barragán-Hernández & Cajas-Girón, 2019). This condition probably created a favorable environment and promoted a greater abundance of the entomofauna in this pasture during the dry season. The population dynamics of insects decreased when the average temperature increased (Yarupaita Echevarria, 2016).
The diversity in the rainy season could also be related to the lower temperatures recorded at this time, as shown by the negative relationship between temperature and insect abundance. This behavior was mainly detected in insects of the Hemiptera order, as happened in this study with Hemiptera, being the ones with the greatest abundance after Coleoptera. The effect of low temperature could account for the large number of insects collected during the rainy season in all pastures, except for M. maximus, which had the highest abundance during the dry season. So, even though insect abundance increased when the temperatures were low, it should be considered that pasture also influenced insect abundance.
Conclusion
The orders Coleoptera and Hemiptera stood out, which mostly represented the functional groups of predators and phytophages, respectively. The entomofauna of C. gayana, C. ciliaris, and M. maximus was similar in insect abundance and diversity. However, insect abundance depended on the influence of the season and pastures. Therefore, it is crucial to consider the biotic and abiotic factors that can affect the entomofauna associated with pastures to create preservation strategies for beneficial fauna and efficient pest management, thus maintaining a balance in the trophic relationships of the entomofauna associated with pastures, could be a useful tool and sustainably as an alternative to agroecological production systems by maintaining the natural balance and reducing the application of agrochemicals.
Acknowledgments
The authors thanks to AGROSAVIA for supporting the conduct of this research because this article comes from the data of the project: “Multilocational evaluation of new forage germplasm,” carried out in 2019 – 2020, within its research and development agenda. Also to Erika Valentina Krupskaya Vergara, who works as a master researcher at the Tibaitata RC, for her valuable collaboration in the taxonomic identification of the collected arthropods. The authors are grateful to the Centro Internacional de Agricultura Tropical (CIAT) for supporting the transfer of plant material as an institutional partner. This study was funded by Ministerio de Agricultura y Desarrollo Rural (MADR) of Colombia and the Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA).
Competing interests
The authors declare no conflict of interest.
References
Alomar, O., & Albajes, R. (2005). Control biológico de plagas: Biodiversidad funcional y gestión del agroecosistema. Biojournal, 1, 1–10. https://bit.ly/3VQ3KnO
Alothman, M., Hogan, S. A., Hennessy, D., Dillon, P., Kilcawley, K. N., O’Donovan, M., Tobin, J., Fenelon, M. A., & O’Callaghan, T. F. (2019). The “grass-fed” milk story: Understanding the impact of pasture feeding on the composition and quality of bovine milk. Foods, 8(8), Article 350. https://doi.org/10.3390/foods8080350
Altieri, M. A., & Nicholls, C. I. (2012). Diseños agroecológicos para potenciar el control biológico de plagas: Incrementando la biodiversidad de entomofauna benéfica en agroecosistemas. Editorial Académica Española.
Barragán-Hernández, W. A., & Cajas-Girón, Y. S. (2019). Cambios bromatológicos y estructurales en Megathyrsus maximus bajo cuatro arreglos silvopastoriles. Revista Ciencia y Tecnología Agropecuaria, 20(2), 231–244. https://doi.org/10.21930/rcta.vol20_num2_art:1458
Barnett, K. L., & Facey, S. L. (2016). Grasslands, invertebrates, and precipitation: a review of the effects of climate change. Frontier in Plan Science, 7, Article 1196. https://doi.org/10.3389/fpls.2016.01196
Caraballo-Gracia, P. R., Martinez-Prada, S., & Salcedo-Diaz, A. (2019). Relaciones tróficas en un agroecosistema de la región Sabanas, Sucre, Colombia. Pastos y Forrajes, 42(2), 152–160. https://payfo.ihatuey.cu/index.php?journal=pasto&page=article&op=view&path%5B%5D=2087
Collinge, S. K., Prudic, K., & Oliver, J. C. (2003). Effects of local habitat characteristics and landscape context on grassland butterfly diversity. Conservation Biology, 17(1), 178–187. https://doi.org/10.1046/j.1523-1739.2003.01315.x
Di-Rienzo, J. A., Casanoves, F., Balzarini, M. G., González, L., & Tablada, M. (2020). InfoStat versión 2020. https://www.infostat.com.ar/
Diaz, L., Moreno-Elcure, F., & Jaramillo, C. (2017, setiembre 12-15). Estudio de la diversidad funcional entomológica asociada a agroecosistemas con manejo agroecológico [Ponencia]. VI Congreso Latinoamericano de Agroecología; X Congreso Brasileño de Agroecología; V Seminario de Agroecología del Distrito Federal y Alrededores, Brasilia, DF, Brasil. http://cadernos.aba-agroecologia.org.br/cadernos/article/view/2476
Giraldo, C., Reyes, L. K., & Molina, J. J. (2011). Manejo integrado de artrópodos y parásitos en sistemas Silvopastoriles intensivo [Manual 2]. Centro para la investigación en Sistemas Sostenibles de Producción Agropecuaria. https://bit.ly/3X84czj
Gullan, P. J., & Cranston, P. S. (2014). The insects: an outline of entomology (5th ed.). Wiley-Blackwell. https://doi.org/10.1093/ae/tmw008
Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). Past: Paleontological Statistics software package for education and data analysis. Paleontologia Electronica, 4(1), Article 4. https://palaeo-electronica.org/2001_1/past/issue1_01.htm
Instituto de Hidrología, Meteorología y Estudios Ambientales. (2020). Geoportal, Descargue aquí la información geográfica de datos abiertos del IDEAM. http://www.ideam.gov.co/geoportal
Jarvis, D. I., Padoch, C., & Cooper, H. D. (2011). Manejo de la agrobiodiversidad en los ecosistemas agrícolas (Walter, A., Trad.). Bioversity International.
Kasper, M. L., Reeson, A. F., Mackay, D. A., & Austin, A. D. (2008). Environmental factors influencing daily foraging activity of Vespula germanica (Hymenoptera, Vespidae) in Mediterranean Australia. Insectes Sociaux, 55, 288–295. https://doi.org/10.1007/s00040-008-1004-7
Lee, C. M., & Kwon T. -S. (2013). Community structure, species diversity of insect (ants, ground beetles), and forest health in the Hongneung forest. Journal of Korean Society of Forest Science, 102(1), 97–106. https://doi.org/10.14578/jkfs.2013.102.1.097
Margalef, M. (1956). Información y diversidad específica en las comunidades de organismos. Investigación Pesquera, 3, 99–106. http://scimar.icm.csic.es/scimar/index.php/secId/6/IdArt/1457/
Moreno, C. E. (2001). Métodos para medir la biodiversidad. Programa Iberoamericano de Ciencia y Tecnología para el Desarrollo. http://entomologia.rediris.es/sea/manytes/metodos.pdf
New, T. R. (2019). Insect conservation and Australia’s grasslands. Springer, Cham. https://doi.org/10.1007/978-3-030-22780-7
Negawo, A. T., Assefa, Y., Hanson, J., Abdena, A., Muktar, M. S., Habte, E., Sartie, A. M., & Jones, C. S. (2020). Genotyping-by-sequencing reveals population structure and genetic diversity of a Buffelgrass (Cenchrus ciliaris L.). Diversity, 12(3), Article 88. https://doi.org/10.3390/d12030088
Ojija, F., Sapeck, E., & Mnyalape, T. (2016). Diversity analysis of insect fauna in grassland and woodland community at Mbeya University of sciences and Technology. Tanzania. Journal of Scientific an Engineering Research, 3(4), 187–197. http://jsaer.com/download/vol-3-iss-4-2016/JSAER2016-03-04-187-197.pdf
Patel, N. (2015, November 20-24). Abundance, diversity and importance of some insects in grasslands of Indian arid zone [Paper presentation]. The XXIII International Grassland Congress, Nueva Delhi, India.
Rainio, J., & Niemelä, J. (2003). Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodiversity and Conservation, 12, 487–506. https://doi.org/10.1023/A:1022412617568
Rákosy, L., & Schmitt, Z. (2011). Are butterflies and moths suitable ecological indicator systems for restoration measures of semi-natural calcareous grassland habitats? Ecological Indicators, 11(5), 1040–1045. https://doi.org/10.1016/j.ecolind.2010.10.010
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation. http://www.rstudio.com/
Shannon, C. E. (1948). A mathematical theory of communication. The Bell System Technical Journal, 27(3), 379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Simpson, E. H. (1949). Measurement of diversity. Nature, 163, 688. https://doi.org/10.1038/163688a0
Statistical Analysis Systems Institute. (2013). The SAS system for Windows [Release 9.4.]. SAS Institute Inc. https://www.sas.com/es_mx/software/stat.html
Szwedo, J. (2018). The unity, diversity and conformity of bugs (Hemiptera) through time. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 107(2–3), 109–128. https://doi.org/10.1017/S175569101700038X
Uhler, J., Haase, P., Hoffmann, L., Hothorn, T., Schmidl, J., Stoll, S., Welti, E., Buse, J., & Müller, J. (2022). A comparison of different Malaise trap types. Insect Conservation and Diversity, 15(6), 666–672. https://doi.org/10.1111/icad.12604
Valerio, J. R., Cardona, C., Peck, D. C., & Sotelo, G. (2001, February 11-21). Spittlebugs: bioecology, host plant resistance and advance s in IPM [Conference presentation]. The XIX International Grassland Congress, São Pedro, São Paulo, Brazil. https://uknowledge.uky.edu/cgi/viewcontent.cgi?article=4067&context=igc
Whiles, M. R., & Charlton, R. E. (2006). The ecological significance of tallgrass prairie arthropods. Annual Review of Entomology, 51, 387–412. https://doi.org/10.1146/annurev.ento.51.110104.151136
Yarupaita Echevarria, B. F. (2016). Influencia de los factores climatológicos sobre la dinâmica poblacional de Trichogonia costata Signoret en Buddleja incana – Chongos bajo – Chupaca [Tesis de pregrado, Universidad Nacional del Centro del Perú]. Repositorio de la Universidad Nacional del Centro del Perú. https://bit.ly/3VMV80Z
Zumbado Arrieta, M., & Azofeifa Jiménez, D. (2018). Insectos de importancia agrícola. Guía básica de entomología (1ª ed.). Programa Nacional de Agricultura Orgánica. http://www.mag.go.cr/bibliotecavirtual/H10-10951.pdf
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