Edaphic mesofauna groups in farms of six municipalities of Norte de Santander

ABSTRACT The objective of the research was to identify the groups of soil mesofauna in farms of six municipalities of Norte de Santander before planting polyculture plots. A non-experimental qualitative and quantitative study was carried out where the soils of 15 farms in each municipality were sampled to identify the taxonomic groups of the edaphic mesofauna. The Berlese-Tyllgren funnel extraction method was used to separate and quantify individuals by families and orders. The soil mesofauna in the six study municipalities included members of between two and six classes corresponding to Arachnida, Diplura, Entognatha, Insecta, Malacostraca and Symphyla, with a greater number of families for Arachnida in all municipalities. In general, the soils of the farms of these municipalities are not considered very disturbed given the number of orders and families present with different functions in the edaphic trophic chain.


Introduction
Soil is an essential component of the agroecosystem, and by defining its state, its sustainability can be known (Astier-Calderón, Maass-Moreno, and Etchevers-Barra 2002).However, soil is one of the most complex and diverse ecosystems in nature (Mancina and Cruz Flores 2017).It is characterized as a structured, heterogeneous and discontinuous system containing nutrients, energy, organisms and microorganisms that make up the different microhabitats (Gabbarini, Frene, and Wall 2017).
Some research has identified biological parameters that allow sensitive detection of soil changes caused by management practices (Ferreras et al. 2015).Moreover, biological parameters are not attributable to soil texture and are almost entirely dependent on influences by soil management (Jaurixje et al. 2013).Soil biology is modified in response to human interventions such as agricultural practices, deforestation or pollution, which can directly affect agricultural productivity (Basso et al. 2011).Moreover, variability in soil biology occurs due to the interaction of factors such as climate, temperature and management (Bonnin et al. 2017;Siqueira et al. 2018).Different planting systems, including fertilization practices, liming and amendment application, can alter the quality of soil life, which is reflected in changes in the physical, chemical and biological properties of the soil (Baretta et al. 2003).
Biological indicators include the different factors that affect soil quality, which are sensitive to soil properties in the short, medium and long term and make it a decision-making tool.In addition, there is a close relationship of soil biological properties with physical characteristics such as aggregation and with chemical characteristics such as ion exchange capacity and nutrient availability (García, Ramírez, and Sánchez 2012).
Soil fauna can be classified broadly into microfauna, mesofauna and macrofauna.The mesofauna groups individuals of 4 mm in length and between 0.2 and 2 mm in diameter.They live in the leaf litter and/or within the soil and include soil mites, springtails, proturans, diplurans, Psocoptera, thrips, pauropods and symphylans (Mancina and Cruz Flores 2017).
The consequences of human interventions on soil can result in the decline of ecosystem services and loss of primary productivity.Because organisms can respond to soil disturbances, they are a tool for detecting changes in recovery or detecting soil degradation risks (Ferreras et al. 2015).Although studies of soil mesofauna in Colombia are not very abundant, there is a history of proposed keys for edaphic springtails (Ospina-Sánchez, Rodríguez Ch, and Peck 2009), two published studies on soil mesofauna in coffee crops (Lagos-Burbano, Ballesteros-Possu, and Delgado-Gualmatan 2020;Robaina, Márquez Girón, and Restrepo 2018), and other studies on different land uses (Duarte-Núñez, Pinzón-Florián, and Palacios-Vargas 2020;Rueda, De Moraes, and Varela 2016).More recently, a study was also carried out in six municipalities in the department of Norte de Santander where the mesofauna present in the soil was characterized prior to the establishment of agroforestry systems (Castellanos, Capacho Mogollón, and Castellanos Hernández 2021).
The agroecological project 'Ecosembrando' was recently developed with the aim of validating agroecological models of polyculture of short-cycle species on 15 smallholder farms in six other municipalities of Norte de Santander (Gobernación de Norte de Santander 2020), which proposed, among other aspects, to compare the impact of two production systems, mono-and polyculture, on soil biology.
This research was justified by the need to obtain a baseline in relation to soil biology, in particular on the abundance and classification of edaphic mesofauna in the farms where the polyculture models were to be established, in the municipalities of Ábrego, Bochalema, Bucarasica, Los Patios, Pamplonita and Villa Caro.Against this background, the aim of this study was to identify the soil mesofauna groups on farms in six municipalities of Norte de Santander before planting the polyculture.

Selection of municipalities
The research was carried out in the six municipalities selected by the Governorate of Norte de Santander for participating in the Ecosembrando polyculture Project: Pamplonita, Abrego, Bochalema, Bucarasica, Villa Caro and Los Patios.

Type of research
A non-experimental qualitative and quantitative study was developed in which the soils of 15 farms in each municipality were sampled to determine the taxonomic groups present in the edaphic mesofauna.For each farm we recorded the name, owner, altitude, georeference information and situation of the representative plots where the sampling was to be carried out.

Identification of soil mesofauna groups in 90 farms in six municipalities of Norte de Santander
To determine the taxonomy of the mesofauna associated with the soil in each of the 15 farms in the six municipalities of Ábrego, Bochalema, Bucarasica, Los Patios, Pamplonita and Villa Caro, sampling was carried out in March and April 2021.The 0.5 ha plot selected for the polycultures was sampled.Four monoliths 10 cm long by 10 cm wide and 10 cm deep were made randomly in each plot, for a total of 60 monoliths in each municipality.Finally, a sample of 1 kg was taken from each farm.
The samples from the farms were placed in a bag, marked and labelled with the data of the corresponding farm and sent to the laboratory.
The Berlese-Tyllgren funnel extraction method was used to separate and quantify members of the soil mesofauna (Karyanto et al. 2013).Each sample was placed in a Berlese-Tyllgren funnel for 72 h, allowing the arthropods present to migrate to the bottom of the funnel in response to the elevation of temperature and light at the top, produced by 40 W bulbs.The arthropods were collected in a glass jar with screw cap and alcohol.After 72 h each jar was labelled with the data corresponding to the site for systematization.

Results and discussion
Two classes of edaphic mesofauna were present on the farms in the municipality of Abrego -Arachnida and Entognatha -with the highest relative abundance of species for Arachnida with 60%.Members of five classes -Arachnida, Chilapoda, Entognatha, Symplyla and Insecta -were present on the farms in the municipality of Bochalema.The highest relative abundance for the families was Arachnida with 43.57%, followed by Entognatha with 31.2%.In Bucarasica representatives of five classes were present -Arachnida, Entognatha, Insecta, Malacostraca and Symphyla -with the highest relative abundance of families for Arachnida with 58.8%, followed by Entognatha.On the Los Patios farms we recorded members of four classes -Arachnida, Entognatha, Insecta and Symphyla -with the highest relative abundance of families for Arachnida with 36.8%,followed by Entognatha with 32.5%.In Pamplonita, members of only three classes were present -Arachnida, Entognatha and Insecta -where Arachnida included the highest relative number of families with nine out of the 15 present.On the farms in the municipality of Villa Caro, members of four classes were found -Arachnida, Diplopoda, Entognatha and Insecta -with the highest relative abundance of families for Arachnida with 56.5% (Figure 1).
In the farms of the Ábrego municipality, the samples collected showed the presence of five orders -Mesostigmata, Prostigmata, Oribatida, Collembola and Diplura -with the highest relative abundance of Mesostigmata (40%) followed by Collembola (33.3%).In the municipality of Bochalema, individuals from nine orders were detected -Oribatida, Mesostigmata, Prostigmata from Arachnida; Polydesmida from Chilapoda; Collembola and Diplura from Entognatha; Hymenoptera and Diptera from Insecta; and members of an order of Symphyla -with the highest relative abundance of families from Collembola, with 29.Members of eight orders were present on the Bucarasica farms -Mesostigmata, Oribatida, Collembola, Diplura, Coleoptera, Diptera, Isopoda and other orders within Symphyla -with a predominance of families belonging to Mesostigmata (35.2%) (Figure 2).
On farms in the municipality of Los Patios, arthropods of the class Symphyla and seven orders of other classes were present -Mesostigmata, Oribatida, Collembola, Diplura, Diptera, Hemiptera, Lepidoptera -with the highest relative abundance of families belonging to Collembola with 26.3%, followed by Mesostigmata with 21%.Members of six orders -Mesostigmata, Oribatida, Collembola, Diplura, Hymenoptera and Diptera -were present on the farms in the municipality of Pamplonita.The highest relative abundance of families was found for Mesostigmata and Oribatida, both with 26.6%.On the farms in the municipality of Villa Caro, members of the edaphic mesofauna belonging to the 10 orders Mesostigmata, Oribatida, Prostigmata, Polydesmida, Collembola, Diptera, Hymenoptera, Coleoptera, Hemiptera and Psocoptera were present.The highest relative abundance was found in Oribatida (26%) and Mesostigmatha (21.7%).A total of 39 families of mesofauna were present in the six municipalities.Five families were present in all the municipalities (Collembola: Onychiuridae, Collembola: Isotomidae, Mesostigmata: Uropodidae, Oribatida: Galumnidae and Mesostigmata: Laelopidae), while four families were present in five municipalities (Mesostigmata: Ascidae, Oribatida: Malaconothroidae, Mesostigmata: Epicriidae and Oribatida: Oppiidae).These families had as a common factor that they belong to the two classes Arachnida and Egtongnatha.Three families were found in at least four municipalities (Collembola: Hypogasturidae Oribatida: Nothridae and Diptera: Psychodidae), while four others were found in 50% of the municipalities (Collembola: Entomobryidae, Coleoptera: Staphylinidae, Synphylla: Scolopendrellidae and Diplura: Heterojapygidea) (Figure 3).The rest of the families identified (23) were present in only one or two municipalities, although this did not detract from their importance in terms of their possible involvement in different soil biological processes.
In general, the number of mesofaunal classes ranged from two in Ábrego to five in Bochalema and Bucarasica: Arachnida, Entognatha, Insecta and Symphyla, while Chilapoda and Malacostraca were found alternately.In all municipalities the most abundant class was Arachnida.There was also a great variation in the orders of the edaphic mesofauna present, ranging from five in Abrego to 10 in Villa Caro; although overall 13 orders were present in all six municipalities: Mesostigmata, Oribatida, Prostigmata, Collembola, Diplura, Lepidoptera, Coleoptera, Diptera, Hymenoptera, Hemiptera, Psocoptera, Isopoda and other members of orders within Symphyla.
The class Arachnida stood out among the others in five municipalities, which in the opinion of the researchers may be characteristic of somewhat disturbed soils (Socarrás 2013), although this cannot always be confirmed given the abundance of members of Oribatida.Mites participate in multiple roles in the soil, depending on the families present, as some contribute to the decomposition of organic matter while others help in the reduction of microorganisms (mainly fungi), while mites of the orders within Oribatida act in the food chain as predators, regulating populations of other soil organisms -especially the microbiota, as pointed out by Berude et al. (2015).
In Bochalema and Bucarasica, the highest number of morphospecies belonged to Colembolla, whichaccording to Socarrás (2013) -gives a measure of poorly disturbed soils due to the fragility of these microinvertebrates.They present multiple reproductive strategies and forms of distribution, participating in processes that include the biological control of fungi and other mesofauna organisms, important in the decomposition and mineralization of organic matter (Rueda, De Moraes, and Varela 2016).
It should be taken into account that members of Mesostigmata: Uropodidae (present in all municipalities) and Diplura (present in five of the six municipalities) may play a role as predators regulating the populations of other members of the mesofauna (Eisenbeis 2006;Lavelle, Senapati, and Barros 2003), and according to Socarrás (2013) the predominance of Mesostigmata may be an indicator of disturbed soil, while that of Diplura may indicate that any disturbance is not extreme.
The members of the orders Mesostigmata and Collembola stood out for their relative abundance, coinciding with the findings of other authors who, among the soil organisms, found Collembola and Mesostigmata to be the most abundant groups of the mesofauna.Mites in particular stand out not only for being the most abundant groups, but also for the multiple processes in which they participate in the soil, so in order to understand this complex soil litter system it is necessary to study these groups in greater depth (Rueda, De Moraes, and Varela 2016).
Many members of the class Arachnida were found, particularly in the orders Oribatida and Mesostigamata, which formed a fundamental part of the mesofauna.They are involved in the proper functioning of edaphic ecosystems, but they also tend to inhabit tree strata where their specific composition is usually very different from that in the soil or leaf litter, and that is why members of the mesofauna of the class Insecta, Diplura and Diplopoda appear, as well as Collembola, which has been pointed out by other researchers of soil mesofauna (Villagómez, Iglesias, and Palacios-Vargas 2017).
The family Isotomidae was present in all municipalities, while the family Heterojapygidae was present in four municipalities; these belong to the order Collembola, and were representative of the soil mesofauna in this study.The results corroborate those of other authors who state that these organisms are of great importance because they contribute to the processes of organic matter degradation and the incorporation of humus nutrients into the soil, and are therefore used as bioindicators of soil quality (Socarrás 2013).
On the other hand, it has been reported in a study of the application of different types of organic fertilizers that the populations of Oribatidae and Mesostigmata mites and springtails (Entomobryidae and Isotomidae) increased (De Prager, Monroy, and Parada 2015), which shows that in the presence of high amounts of organic matter, both decomposers and predators increase in the food chain; this corresponds to what we observed.
The class Malacostrata was only present in Bucarasica, and according to the literature members of this class play a key role in the functioning of some ecosystems where they are involved in the processes of decomposition of organic matter, acceleration and recycling of nutrients, and mineralization of essential elements such as nitrogen and phosphorus (Lagos-Burbano, Ballesteros-Possu, and Delgado-Gualmatan 2020; Socarrás 2013Socarrás , 2018)).The class includes arthropods belonging to the subphylum Crustacea, whichalthough some authors state that they occur infrequently in soils -can be very numerous (Socarrás 2018), due to the fact that they are predators and in other cases feed on decomposing organic matter.
The results showing higher abundance of members of the orders Oribatida, Mesostigmata and Prostigmata in Pamplonita, Bochalema and Villa Caro do not fully correspond with those reported by other researchers who observed higher abundance of the four mite orders Oribatida, Astigmata, Mesostigmata and Prostigmata (Socarrás and Izquierdo 2016).In another study (Marín and Sánchez 2012) the most represented groups were found to be mites, springtails, ants, Hemiptera and Coleoptera, similar to what occurred in our study in Bucarasica and Villa Caro.
In Los Patios and Bochalema, members of Collembola were more abundant, which corresponds to the findings of other researchers who carried out biological characterization during the establishment of 18 agroecological models in another six municipalities in Norte de Santander, Colombia; they confirmed that Collembola was present in five of the six municipalities, standing out with greater relative abundance (Castellanos, Capacho Mogollón, and Castellanos Hernández 2021).Similarly, other authors studying the edaphic mesofauna separated and classified all individuals recovered and found that Collembola occupied second place with the 19 % of the taxa, which reaffirms that it is a very abundant order among the mesofaunal communities in Cuba (Socarrás and Izquierdo 2016).
The greater abundance of the class Entognatha in Los Patios may be characteristic of ecosystems that maintain a certain equilibrium, as some authors suggest, because they are very weak individuals that act as biological controllers of various species of fungi that affect plants.This is why they are so important for soil conservation when there is a high biodiversity and abundance of these species (Miranda-Rangel, Martínez-Cruz, and Calyecac-Cortero 2015).
In the municipality of Pamplonita, three classes and six orders were observed; in particular, the class Arachnida was represented by three orders: Oribatida, Mesostigmata and Prostigmata.The order Mesostigmata included the families Gamasidae and Uropodidae, which confirms that these groups may be present as part of the mesofauna of a moderate climate, as other authors have pointed out (Socarrás and Izquierdo 2016).
Unlike the other municipalities in Pamplonita, there was a greater abundance of the families Oribatida, Mesostigmata and Collembola, which could be related to less activity in the soil as many farms were fallow.This has been suggested in other studies, where changes in mesofauna populations (with emphasis on mites and springtails) and in some of their physical properties caused by the application of green manures were estimated, and mites and springtails were found to be the dominant populations (Villagómez, Iglesias, and Palacios-Vargas 2017).
Due to the importance of organic matter in the predominance of springtails, the implementation of agroecological practices in the polycultures to be carried out as part of the Ecosembrando project should be monitored, as studies in Colombia indicate that the populations of Collembola species are affected by the removal of organic matter, changes in the microclimate or a reduction in the quantity and quality of leaf litter (Duarte-Núñez, Pinzón-Florián, and Palacios-Vargas 2020).
A particular feature of Villa Caro municipality was that in addition to springtails and a group of organic matter decomposer mites, members of Mesostigmata: Uropodidae and Mesostigmata: Laelopidae were present on the farms, which may play a role as predators regulating the populations of other members of the mesofauna (Eisenbeis 2006;Lavelle, Senapati, and Barros 2003).
In three municipalities, insects of the family Staphylinidae (Coleoptera) were present, that can be found in a wide variety of environments, from sea level to high mountain sites, often associated with silvicultural environments (where fruits, fungi, decaying wood and leaf litter are abundant), on wildlife or insect carcasses, almost always as ectocomensals (Navarrete-Heredia and Newton 2014).Also, in Villa Caro there were species of Insecta orders such as Diptera, Hemiptera and Hymenoptera that are recognized for containing predatory species and that form a mesofauna complex with different functions in the food chain; in particular there were also members of Psocoptera that are pioneer insects in establishing themselves in areas that were deteriorated or disturbed (Robaina, Márquez Girón, and Restrepo 2018;Socarrás 2013).
The present results do not agree with the differences reported by Rueda, De Moraes, and Varela (2016) on the greater or lesser diversity of Mesostigmata or Oribatida in different ecosystems and geographical areas of Colombia, nor with the reports of others results in four municipalities of Nariño where Hymenopera, Acari and Coleoptera predominated (Lagos-Burbano, Ballesteros-Possu, and Delgado-Gualmatan 2020).The fact that in the Colombian Altillanura the springtails were better represented in the grasslands than in the forest, in addition to the differences in representativeness of the taxonomic groups within the six municipalities under study in relation to the other six municipalities previously analysed in the department of Norte de Santander, reaffirms the need to deepen the knowledge of the rich Colombian edaphic mesofauna, as proposed by Rueda, De Moraes, and Varela (2016), at both the national and departmental level.

Conclusions
The soil mesofauna in the six municipalities under study in the North of Santander Colombia contained abundant representatives of members of between two and five classes corresponding to Arachnida, Diplura, Entognatha, Insecta, Malacostraca and Symphyla, with the highest number of families for Arachnida in all municipalities.Within these classes, the orders Mesostigmata, Oribatida, Prostigmata, Collembola, Diplura, Lepidoptera, Coleoptera, Diptera, Hymenoptera, Isopoda and other members of orders within Symphyla stood out.Nine families of the orders Prostigmata, Oribatida and Collembola were present in at least five of the six municipalities.
In general, the farm soils of these municipalities are not considered to be highly disturbed given the number of orders and families present with diverse functions in the edaphic food chain.

Figure 1 .
Figure 1.Number of soil mesofauna families present in each class by municipality.

Figure 2 .
Figure 2. Number of mesofauna families present in the different orders per municipality.

Figure 3 .
Figure 3. Families of mesofauna present in the municipalities.

Table 1 .
Coordinates of the 15 farms participating in the project in each of the municipalities.