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Cuban Journal of Agricultural Science

Print version ISSN 0864-0408On-line version ISSN 2079-3480

Cuban J. Agric. Sci. vol.54 no.4 Mayabeque Oct.-Dec. 2020  Epub Dec 01, 2020


Pasture Science

Characterization of the edaphic macrofauna in five grassland agroecosystems from Granma province. Taxonomical identification

Licet Chávez Suárez1  *

Idalmis Rodríguez García2

W. Estrada Prado1

1Instituto de Investigaciones Agropecuarias “Jorge Dimitrov”. Carretera vía Manzanillo km 16 ½, Peralejo, Bayamo, Granma, Cuba

2Instituto de Ciencia Animal, Apartado postal 24, San José de las Lajas, Mayabeque, Cuba.


In order to identify the edaphic macrofauna in five grassland agroecosystems from Granma province, samplings were carried out twice a year, between July, 2014 and March, 2017. The edaphic macrofauna was collected according to the standard methodology proposed by the Tropical Soil Biology and Fertility (TSBF) and by the complementary methodology of pitfall traps. The identification was performed with taxonomical references and keys, and with the cooperation of competent entomologists and taxonomists. The identified edaphic macrofauna, with both methods, in five agroecosystems, was grouped in three phyla, seven classes, 16 orders, 71 families, 121 genera, 63 species and 177 morphospecies. Insecta class was the best represented according to number of orders (11), while Araneae was the most represented order, with 17 families. Formicidae family had the best richness of genera and species, identified with 33 taxonomical units. Out of the identified orders, 17 were collected from monoliths and 14 from traps. Meanwhile, at taxonomical level, 46 were identified in monoliths and 63 in traps. It is concluded that the high presence of ants (Hymenoptera: Formicidae) determined a low taxonomical diversity of the edaphic macrofauna in all the studied agroecosystems. In addition, it is recognized the need of use of the complementary method of pitfall traps to obtain a more complete inventory of the edaphic macrofauna.

Key words: cattle rearing agroecosystem; soil organisms; traps; monoliths

Soil fauna includes organisms that spend the whole or part of their lives inside the soil, in the surface right above the soil, in the superficial litter, in decaying fallen stems and in other environments (Cabrera 2019). Within the soil fauna, macrofauna includes the most conspicuous invertebrates, with an equal or higher length than 10 mm and a diameter superior to 2 mm, so they are easily seen in the surface or inside the soil, and can be affected by different uses of soil. It also acts as a determinant agent in soil fertility and, consequently, the global functioning of the edaphic system.

In this sense, several studies on soil macrofauna in grassland agroecosystems in the western region of Cuba has been conducted (Cabrera et al. 2011, Rodríguez et al. 2011, García et al. 2014, Menéndez and Cabrera 2014, Cabrera-Dávila et al. 2017 and Ramírez et al. 2018), as well as in the eastern region (Zaldívar et al. 2007, Vega et al. 2014, Chávez et al. 2016 and Chávez et al. 2018). Nevertheless, most of research did not reach the lowest taxonomical level in macrofauna identification, which constitutes a challenge for the scientific community. Therefore, the objective of this study was to identify the edaphic macrofauna in five grassland agroecosystems from Granma province.

Materials and Methods

The research was developed in five grassland agroecosystems of Granma province, located in the southwestern portion of the eastern region of Cuba. Table 1 shows their main characteristics. Samplings were carried out twice a year, from July 2014 to March 2017.

Table 1 Main characteritics of the studied agroecosystems 

Agroecosystem El Triángulo and El Progreso Cupeycito Ojo de agua Estación de Pastos
Municipality Bayamo Jiguaní Guisa Bayamo
Affiliation UBPC “Francisco Suárez Soa” Empresa Genética “Manuel Fajardo” Farm of Rafael Almaguer, CCS “Braulio Coroneaux” IIA “Jorge Dimitrov”
Purpose Milk production Rearing Bull fattening Bull fattening
Type of soil Pellic vertisol Carbonated soft brown Carbonated soft brown Fluvisol
Grazing method Continuous Rotational Continuous Rotational
Total grazing area (ha) T:18.5 P: 20.4 14.2 6.7 0.8
Sampling area (ha) and % of total area T: 2 11% P: 2 10% 1.8 13% 1.2 18% 0.8 100%
Predominant type of grass Blue grass (Dichanthium caricosum L. A. Camus) and star grass (Cynodon nlemfuensis Vanderyst.) Guinea grass (Megathyrsus maximus (Jacq.) B. K. Simon & S. W. L. Jacobs) Blue grass (Dichanthium caricosum L. A. Camus) Silvopastoral system with guinea grass and Leucaena leucocephala (Lam.) de Wit
Forage area (ha) Sugar cane (‎Saccharum officinarum L.):2 King grass (Cenchrus purpureus Schumach) Morrón:1.5

  • 1

  • 4

  • 0.5

  • 3

Usage time 20 years 10 years 7 years 10 years
Breed and stocking rate (LAU ha-1) Crossbred Siboney 1,5 Creole 1,7 Crossbred 2,2 Crossbred Siboney 1
General conditions Totally deforested grazing area, without paddocks, with floods during rainy season Good shade per trees and paddocking, highly stony Good shade per trees, without paddocks, relief with slopes and sensitivity to erosion Good shade per trees, area of intense drought

T: El Triángulo P: El Progreso

Experimental procedure. For the sampling of the edaphic macrofauna, two methods were used: the one recommended by Tropical Soil Biology and Fertility (TSBF) program (Anderson and Ingram 1993 and Jiménez et al. 2020) and pitfall traps (Moreira et al. 2012). For the first method, litter was previously cleaned and all kinds of foreign elements were removed, such as stones and plant residues. In the diagonal of the sampling area (table 1), five monoliths per hectare, measuring 25 x 25 x 20 cm, were extracted, at a distance of 20 m. In situ macrofauna individuals were collected and manually counted. Worms were preserved in 4% formaldehyde, and the remaining invertebrates in 70% ethanol.

For the second sampling method, nine traps were placed in each study area, arranged in the two diagonals, in the shape of a cross, with a trap in the center. Plastic containers 8 cm in diameter and 10 cm deep were used, which were buried flush with the ground, trying to damage as little as possible the surrounding area.

An aqueous solution, prepared with LABIOFAM commercial liquid detergent (0.003%), was added and covered with dry leaves and plant remains typical of each agroecosystem. After seven days, the contents of the traps were collected in glass flasks and transferred to the laboratory. With the use of the stereoscope, individuals were extracted from the solution and counted, and then placed in vials with 70% ethanol.

To identify the preserved specimens, studies of Alayo (1974), Hickman et al. (2001), Brusca and Brusca (2003) and Fontela and Matienzo (2011) were consulted. The entomological collection of the provincial plant health laboratory in Granma was also taken as a reference.

Statistical analysis. The analysis of proportion comparison (Chi-square) was performed to the variable number of family per class/order of the edaphic macrofauna, in both sampling methods, and in all agroecosystems, with the statistical package ComparPro, version 1 (Font et al. 2007).

When significant differences were declared, Duncan (1955) multiple comparison test of means was used.

Results and Discussion

The identified edaphic macrofauna, with the use of both methods, in the five agroecosystems, was grouped into three phyla, seven classes, 16 orders, 74 families, 121 genera and 63 species. Insecta was the best represented class, regarding the number of orders (11); while Araneae constituted the most representative order, with 17 families (table 2).

Table 2 Taxonomical identification of the edaphic macrofauna in five grassland agroecosystems of Granma province 

Phylum Class Order Family Genus Species Ecosystem
Monolith Trap
Arthropoda Arachnida Araneae Araneidae Gea heptagon 3
- - 5
Anyphaeidae Wulfila - 2, 5
Clubionidae - - 1
Corinnidae - - 1
Castianeira cubana 1
Xeropigo tridentiger 1
Dyctinidae Dyctina - 5
Theridiidae Spintarus - 2
Steatoda - 1, 2, 4 1
Theridion - 4 1
- - 2
Coleosoma floridanum 1 1
Lycosidae Pardosa floridana 1
Pardosa - 1, 4 1, 2
Linyphiidae Walckenaeria - 1, 3
Ceraticelus - 3
Ceratinella - 2
Microlinyphia - 3
- - 1, 2, 5 1, 2, 3, 5
Miturgidae Teminius insularis 4 1
- - 1 1
Gnaphosidae - - 2
Oonopidae Oonopoides maxilaris 5 4
Oonopoides - 3
Ischnothyreus peltifer 3
Ischnothyreus - 1
- - 2, 3
Oxyopidae Oxyopes crewi 1
Oxyopes - 1
Salticidae Agobardus prominens 1
Beata wickhami 3

Phylum Class Order Family Genus Species Ecosystem
Monolith Trap
- - 1 1, 2, 3, 4
Marpissa bivittata 4
Marpissa pikei 1
Marpissa - 1
Hentzia - 1
Corythalia - 4
Scytodidae Scytodes - 5
Sparassidae - - 1, 5
- - 3
Theraphosidae - - 3
Thomisidae Misumenops - 1
Opiliones - - - 5
Insecta Blattodea Blatidae Epilamfora - 5
- - 3,4 5
Coleoptera Scarabaeidae Aphodius - 1
Phyllophaga - 1, 2, 4, 5 3
Hoplia - 1
Golofa - 2
- - 5
Staphylinidae - - 3
Staphylinus - 5
Nitidulidae Carpophilus hemiptus 3
- - 3
Carabidae Colpodes silviae 3, 5 5
Leptotrachelus compressus 1, 4,5
Agonum - 5
Calosoma - 4
Cucujidae Ahasverus advena 1
Coccinellidae Egius platicephalus 3
Psyllobora nana 3
Tenebrionidae Strongilium - 3 3
Tribolium confusum 1

Phylum Class Order Family Genus Species Ecosystem
Monolith Trap
Anthocoridae Orius - 4
Orius insidiosus 3, 4
Aphididae - - 3
Cercopidae Monecphora bicincta fraterna 4
Cydnidae Cyrtomenus - 3, 4 3
Melanaethus cubensis 4, 5
Cicadidae Diceroprocta biconica 5
Delphacidae - - 4
Fulgoridae Remosa spinolae 2
Blissidae Blissus leucopterus insularis 3
Miridae - - 2
Psyllidae Heteropsylla cubana 3
Reduviidae Diaditus pictipes 1
Rhyparochromidae Paragonatas divergens 5
- Paromius dohrnii 2
- - - 4,5 2,3
Hymenoptera Aphelinidae Aphytis - 1 1,4, 5
Aspidiotiphagus - 5
Marietta - 5
Cynipidae Cynips - 4,5
Dryinidae Anisepyris - 1
Encyrtidae Gahaniella - 1,3
Eupelmus cyaniceps 1,5
Cheiloneurus - 3
Microterys - 1
- - 2,5
Eulophidae Horismenus - 5
Euplectrus - 5
Eurytomidae Bepbratoides cubensis 4

Phylum Class Order Family Genus Species Ecosystem
Monolith Trap
Blapstinus - 3, 5
Cnodalon - 5
Curculionidae - - 3
Elateridae - - 3
Chrysomelidae Conoderus - 5
Hemisphaerota - 4, 5 4, 5
Lema - 4
Lema occidentalis 3
Epitrix histipennis 5
- - 3
Scolitidae Hypotenemus birmanos 2
Hypotenemus - 3
Phasmida Phasmidae Diapherodes - 2
Dermaptera Carcinophoridae Euborellia annulipes 1,4,5
Diptera Culicidae Culex - 5
Culicidae Culicoides - 2,3, 4
Agromyzidae Melanogromyza - 5
Culicidae Culex - 5
Agromyzidae Melanogromyza - 5
Drosophilidae Drosophila - 1,2,3, 4,5
- - 1,3,4,5
- - 2, 3, 5
Hippelates - 1
Ephydridae Paratissa - 1
Milichiidae Paralimna - 2
Desmometopa - 4
Leptometopa - 5
Muscidae Graphomya - 1, 2, 4
Tachinidae - - 1
Whinthemia - 2,4
Belvosia - 1, 2, 3
Hemiptera Chamaemyiidae Leucopis - 4
Torymidae Idarnes - 1
Monodontomerus - 3
Diapriidae Trichopria cubensis 1,5
Fulgoridae Remosa spinolae 2
Formicidae Atta insularis 1,4, 5 4
Cardiocondyla emeryi 1, 2
Cordioxenus - 3
Cryptopone - 3
Cyphomyrmex - 3,4,5 2, 3,4, 5
Cyphomyrmex rimosus 3
Dorymyrmex - 1,2, 4 1, 2, 4
Epitritus - 3 3
Iridomyrmex - 1,2, 5 1, 2,3, 4,5
Macromischa versicolor 3
Monomorium - 2, 5
Monomorium carbonarium 4 4
Monomorium floricola 5, 2
Monomorium versicolor 3
Odontomachus - 1, 5 1, 2, 5
Pheidole - 1,2, 5 1, 2, 4
Pheidole flaven 2
Paratrechina fulva 1, 4 4
Paratrechina vividula 5
Paratrechina - 5
Ponera opacipeps 4, 5
Ponera engatandria 1, 4, 5
Pseudomyrmex - 5 3
Pseudomyrmex pallida 5 5

Tetramorium - 5
Solenopsis corticalis 2, 4, 5 1, 2,4, 5
Solenopsis geminata 1, 2, 5 1, 2, 4,5
Solenopsis - 3
Strumigenys - 2, 5
Wasmannia auropunctata 1,3,2 4, 5 1,2,3, 4,5
Wasmannia sp 2,3,4, 5 1,2,3, 4, 5
Wasmannia sp1 5 1, 5
Hymenoptera Pteromalidae Habrocytus - 2
Isoptera Termitidae Anoplotermes schwarzi 1, 2, 3, 4, 5
Rhinotermitidae Prorhinotermes simplex 5
Lepidoptera Erebidae Mocis latipes 5 1
Pyralidae Sitotroga cerealella 2, 5
Sitotroga - 1, 2
Piloerocis tripunctata 3 2
Ephestia cautella 5
Orthoptera Gryllidae Anurogrillus abortivus 5
Cophus thoracicus 4 1, 4
Acrididae Parachoebata seudderi 1
Parachoebata - 1, 5
Thysanoptera Phlaeothripidae Nesothrips - 5
Thripidae Selenothrips rubrocintus 1
Malacostraca Isopoda - - - 3,4,5 3,4,5
Chilopoda - - - - 3,4,5 3,4,5
Diplopoda - - - - 3,4,5 3,5
Annelida Oligochaeta Haplotaxida - - 3,4,5
- - 3,4,5
Mollusca Gastropoda Archeogastropoda - - - 3,4,5 3,4,5

1: El Triángulo, 2: El Progreso, 3: Cupeycito, 4: Ojo de agua, 5: Estación de Pastos (-): non identified taxonomical level

Table 3 Number of families per class/order of the edaphic macrofauna in both sampling methods in all agroecosystems 

Class/Order Total number Sampling method
Monoliths Traps
# % # % # %
Araneae 17 20.73a 10 21.74a 15 23.81a
Archeogastropoda 2 2.44cd 1 2.18c 2 3.17c
Blattodea 1 1.22d 1 2.18c 1 1.59c
Phasmida 1 1.22d 1 2.18c 0 0
Chilopoda 1 1.22d 1 2.18c 1 1.59c
Coleoptera 12 14.63ab 10 21.74a 6 9.52bc
Dermaptera 1 1.22d 1 2.18c 0 0
Diplopoda 1 1.22d 1 2.18c 1 1.59c
Diptera 9 9.76bc 0 0 9 14.29 b
Haplotaxida 2 2.44cd 2 4.35c 0 0
Hemiptera 13 15.85ab 7 15.22ab 10 15.87b
Hymenoptera 12 14.63ab 3 6.52bc 10 15.87b
Isopoda 1 1.22d 1 2.18c 1 1.59c
Isoptera 2 2.44cd 2 4.35c 0 0
Lepidoptera 2 2.44cd 2 4.35c 2 3.17c
Orthoptera 2 2.44cd 1 2.18c 2 3.17c
Opiliones 1 1.22d 1 2.18c 0 0
Scolopendromorpha 1 1.22d 1 2.18c 1 1.59c
Thysanoptera 2 2.44cd 0 0 2 3.17c
SE ± 2.47 3.29 2.81
Total 83 100 46 100 63 100

a,b,c,dIn the columns, different letters indicate significant differences for P <0.0001, Duncan (1955)

Regarding the 16 identified orders, Phasmida, Dermaptera, Isoptera, Haplotaxida and Opiliones were only observed in the monolith method, while Thysanoptera and Diptera appeared only in the pitfall traps.

However, when the analysis was performed at taxonomical level of the family (table 3), a greater number was identified in the traps, which implies that there are 17 families that were only determined with the use of the pitfall traps. In the monolith method, regarding the number of families, Araneae, Coleoptera and Hemiptera orders were the most represented, while in the traps, Araneae was the most diverse.

Rousseau et al. (2013), in a study on the edaphic macrofauna in different soil uses, including a silvopastoral system in Nicaragua, reported a greater number of species and taxonomic groups detected by the pitfall trap method (83) with respect to the monolith method (61).

According to Menéndez and Cabrera (2014), fauna with characteristics of greater mobility, day or night activity, is more easily captured by traps. Meanwhile, monoliths concentrate their action on those organisms that are less mobile and with diurnal activity, mainly. However, one methodology does not replace the other, but rather they complement each other. In Cuba, almost all of the published studies on the edaphic macrofauna in different ecosystems only use the monolith method.

In the western region of the country, several studies have been carried out on the edaphic macrofauna in grasslands, but it was not identified up to lower taxonomic levels. Cabrera et al. (2011) found 14 orders and 18 families in grasslands of M. maximus and C. nlemfuensis, in San José de las Lajas municipality, Mayabeque province. Likewise, in later studies, in a silvopastoral system and monoculture of M. maximus, these authors reported the presence of 20 orders (Menéndez and Cabrera 2014). García et al. (2014) reported 14 orders in a silvopastoral system with L. leucocephala and different grasses, while, in natural and improved pastures, they only found 9 orders, in Matanzas province. Ramírez et al. (2018) reported 11 orders, in two grassland systems of Yaguajay municipality, Sancti Spíritus province.

Regarding the number of taxonomic units, in all agroecosystems, it stands out that Hymenoptera order was the best represented in both sampling methods. In El Triángulo agroecosystem (figure 1), Araneae order was predominant and a greater diversity of taxonomic units belonging to this order (24) was found with respect to the other agroecosystems. According to Moura et al. (2015), this group of invertebrates prefers soils with open spaces, which allows their mobility and their representation generally implies the presence of available prey population. However, Pontégnie et al. (2005) associated the presence of certain predatory groups, Araneae among them, with temperature and humidity as abiotic factors, and not with the availability of their prey. Zerbino et al. (2008), for their part, determined a positive correlation between the presence of Araneae order and the high values of phosphorus, clay and electrical conductivity.

Figure 1 Number of taxonomical units of macrofauna in both sampling methods of the studied agroecosystems 

Within Hymenoptera order, Formicidae family stood out, in terms of its genus and species richness, with 33 taxonomic units, which is why it was the best represented of all. The dominance of Formicidae in different tropical ecosystems has been widely reported (Rousseau et al. 2013, Menéndez and Cabrera 2014, Escobar et al. 2017, Pereira et al. 2017, Amazonas et al. 2018 and Cabrera-Mireles et al. 2019). According to Cabrera (2012), ants are indicators of disturbance of the edaphic environment, due to their ability to survive in agricultural soils, despite the disorders of this environment.

Likewise, Magurran (2004) pointed out that groups with a greater number of individuals occupy a large proportion of the ecological niche, and make greater use of available resources. This could negatively affect the development of other groups of the edaphic macrofauna, which leads to the simplification of this community, observed in the agroecosystems under study.

Rivas et al. (2014) recognize that ants, by interacting with the ecosystem in a general way, influence on population dynamics of a large number of individuals. In that sense, they stand out for their aggressiveness and some invasive species are considered as pests, like Paratrechina fulva, Wasmannia auropunctata and Solenopsis geminate, which were detected in these agroecosystems (Fontenla and Matienzo 2011). These species also have negative impacts on these agroecosystems, because they constitute a threat to biodiversity of invertebrates, birds and reptiles, cause imbalances in the edaphic biota in favor of herbivorous insects, as they protect Hemiptera, transport harmful insects that can cause diseases in plants, and affect the ecosystem processes of organic matter decomposition and recycling of nutrients by displacing soil detritivores (Fontela and Matienzo 2011, Cabrera 2019 and Zenner 2019).

Cupeycito agroecosystem had the greatest presence of taxonomic units corresponding to Coleoptera order, which is attributed to its favorable vegetation cover, as well as the presence of the arboreal component that provides another litter source and improves the physicochemical properties of soil. In this sense, Zerbino et al. (2008) identified Coleoptera order as a taxonomic group very sensitive to changes in soil use. Escobar et al. (2017) considered it as an indicator of the degree of disturbance of soil, since it had greater abundance in the broadleaf forest, followed by the silvopastoral system and finally, in the studied traditional paddock. In two livestock systems of Yaguajay municipality, in Sancti Spíritus province, Cuba, Hernández-Chávez et al. (2020) also reported a higher prevalence of coleopterans (133 and 313 individuals for grassland and silvopastoral system, respectively).

In Ojo de agua agroecosystem, the spider Agobardus prominens (Bryant 1940), endemic to Cuba, was captured using the pitfall trap method. This is the second time that this species is collected on the island, because it had only been collected before in Soledad, a town in Cienfuegos province (Alayón 2000).

In Estación de Pastos, a greater number of classes/orders (as superior taxonomic units) was observed, with 17 and the highest total number of taxonomic units (73), from which it is inferred that this was the agroecosystem with the most diverse community of edaphic macrofauna. Likewise, the highest abundance of individuals (figure 2), captured by both sampling methods, was also found in this grassland. This fact could be associated with the combination of herbaceous stratum with leucaena trees, which improves soil conditions, due to quality and quantity of included litter. The litter layer also maintains humidity and temperature of soil, which favors the development of the edaphic macrofauna (Hernández et al. 2008).

Figure 2 Abundance of individuals of edaphic macrofauna by sampling method in the studied agroecosystems 

Humidity is essential for the organisms of the edaphic macrofauna, since they have integuments and other structures that need to be kept moist to carry out respiration. Earthworms, for example, require oxygen dissolved in soil solution to breathe (Cabrera-Mireles et al. 2019). Maintaining the proper temperature is also very important for macrofauna organisms, since its increase leads to exoskeleton molting of insects, causing them to be more exposed to predatory organisms and other environmental factors, including solar radiation.

Other authors have also reported greater diversity and density of edaphic macrofauna in silvopastoral systems, in relation to grass monoculture grasslands (Cabrera-Dávila et al. 2017, Ramírez et al. 2018 and Gutiérrez-Bermúdez et al. 2020).

Undoubtedly, the identification of edaphic macrofauna in the studied grassland agroecosystems constitutes a starting point for the understanding of their potential effects on soil, since each organism can exert different functions in the edaphic processes and plant productivity.

It is concluded that the high richness of ants (Hymenoptera: Formicidae) determined a low taxonomic diversity of edaphic macrofauna in all the studied agroecosystems. In addition, it is confirmed the need to use the complementary method of pitfall traps to obtain a more complete inventory of the edaphic macrofauna.


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Received: May 05, 2020; Accepted: September 08, 2020


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