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 2019Cabrera, G. 2019. Evaluación de la macrofauna edáfica como bioindicador del impacto del uso y calidad del suelo en el occidente de Cuba. PhD Thesis. Universidad de Alicante, Valencia, España, p. 124.). 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. 2011Cabrera, G., Robaina, N. & Ponce de León, D. 2011. "Riqueza y abundancia de la macrofauna edáfica en cuatro usos de la tierra en las provincias de Artemisa y Mayabeque, Cuba". Pastos y Forrajes, 34(3): 331-342, ISSN: 2078-8452., Rodríguez et al. 2011Rodríguez, I., Crespo, G., Morales, A., Calero, B. & Fraga, S. 2011. "Performance of the soil biological indicators in dairy units". Cuban Journal of Agricultural Science, 45(4): 187-194, ISSN: 2079-3480., García et al. 2014García, Y., Ramírez, W. & Sánchez, S. 2014. "Efecto de diferentes usos de la tierra en la composición y la abundancia de la macrofauna edáfica, en la provincia de Matanzas". Pastos y Forrajes, 37(3): 313-321, ISSN: 2078-8452., Menéndez and Cabrera 2014Menéndez, Y.I. & Cabrera, G. 2014. "Litter macro-fauna in two systems with different land use and husbandry in Cuba". Cuban Journal of Agricultural Science, 48(2): 181-188, ISSN: 2079-3480. , Cabrera-Dávila et al. 2017Cabrera-Dávila, G.D.L.C., Socarrás-Rivero, A.A., Hernández-Vigoa, G., Ponce de León-Lima, D., Menéndez-Rivero, Y.I. & Sánchez-Rendón, J.A. 2017. "Evaluación de la macrofauna como indicador del estado de salud en siete sistemas de uso de la tierra, en Cuba". Pastos y Forrajes, 40(2): 118-126, ISSN: 2078-8452. and Ramírez et al. 2018Ramírez, W.M., Hernández, M.B., Zurita, A.A. & Navarro, M. 2018. "Performance of the edaphic macrofauna in animal husbandry in a productive entity of the Yaguajay municipality, Cuba". Pastos y Forrajes, 41(4): 241-247, ISSN: 2078-8452.), as well as in the eastern region (Zaldívar et al. 2007Zaldívar, N., Pérez, B.E., Fernández, Y. & Licea, L. 2007. "Macrofauna edáfica en tres sistemas ganaderos". Centro Agrícola, 34(2): 75-79, ISSN: 0253-5785., Vega et al. 2014Vega, A.M., Herrera, R.S., Rodríguez, G.A., Sánchez, S., Lamela, L. & Santana, A.A. 2014. "Evaluation of the edaphic macrofauna in a silvopastoral system in Cauto Valley, Cuba". Cuban Journal of Agricultural Science, 48(2): 189-193, ISSN: 2079-3480., Chávez et al. 2016Chávez, L., Labrada, Y. & Álvarez, A. 2016. "Macrofauna del suelo en ecosistemas ganaderos de montaña en Guisa, Granma". Pastos y Forrajes, 39(3): 111-115, ISSN: 2078-8452. and Chávez et al. 2018Chávez, L., Labrada, Y., Rodríguez, I., Álvarez, A., Bruqueta, D. & Licea, L. 2018. "Caracterización de la macrofauna edáfica en un pastizal de la provincia Granma". Centro Agrícola, 45(4): 43-48, ISSN: 0253-5785.). 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.
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.
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 1993Anderson, J.M. & Ingranm, J.S.I. 1993. Tropical soil biology and fertility: A Handbook of Methods. 2nd Ed. Ed. CAB International Publishing. Wallingford, United Kingdom, p. 240, ISBN: 978-0851988214. and Jiménez et al. 2020Jiménez, J., Filser, J., Barot, S., Berg, M. et al. 2020. Soil fauna: key to soil organic matter dynamics and modelling. Handbook of Methods. Version 1. Jiménez, J.J., Filser, J. & KEYSOM Team (eds). Ed. COST Association. Brussels, Belgium.) and pitfall traps (Moreira et al. 2012Moreira, F.M.S., Huissisg, E.J. & Bignell, D.E. 2012. Manual de Biología de suelos tropicales: muestreo y caracterización de la biodiversidad bajo suelo. Instituto Nacional de Ecología, Nayarit, México, p. 350, ISBN: 9786077908319.). 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)Alayo, P. 1974. "Introducción al estudio de los himenópteros de Cuba". Serie Biológica, 53: 1-38., Hickman et al. (2001)Hickman, C.P., Roberts, L.S. & Larson, A.I. 2001. Integrated principles of Zoology. 11th Ed. Ed. McGraw-Hill Companies, Inc., New York, USA, ISBN: 0-07-290961-7., Brusca and Brusca (2003)Brusca, R.C. & Brusca, G.J. 2003. Invertebrados. 2nd Ed. Pardos-Martínez, F. (ed.) Ed. McGraw-Hill Interamericana de España S.L. Madrid, España, p. 973, ISBN: 9788448602468. and Fontela and Matienzo (2011)Fontela, J.L. & Matienzo, Y. 2011. "Hormigas invasoras y vagabundas de Cuba". Fitosanidad, 13(4): 253-259, ISSN: 1818-1686. 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. 2007Font, H., Noda, A., Torres, V., Herrera, M., Lizazo, D., Sarduy, L. & Rodríguez, L. 2007. Paquete Estadístico ComparPro versión 1. Dpto Biomatemática, Instituto de Ciencia Animal, Mayabeque, Cuba.).
When significant differences were declared, Duncan (1955)Duncan, D.B. 1955. "Multiple Range and Multiple F Tests". Biometrics, 11(1): 1-42, ISSN: 0006-341X, DOI: https://doi.org/10.2307/3001478. multiple comparison test of means was used.
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).
1: El Triángulo, 2: El Progreso, 3: Cupeycito, 4: Ojo de agua, 5: Estación de Pastos (-): non identified taxonomical level
a,b,c,dIn the columns, different letters indicate significant differences for P <0.0001, Duncan (1955)Duncan, D.B. 1955. "Multiple Range and Multiple F Tests". Biometrics, 11(1): 1-42, ISSN: 0006-341X, DOI: https://doi.org/10.2307/3001478.
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)Rousseau, L., Fonte, S., Téllez, O., Van der Hoek, R. & Lavelle, P. 2013. "Soil macrofauna as indicators of soil quality and land use impacts in smallholder agroecosystems of western Nicaragua". Ecological Indicators, 27: 71-82, ISSN: 1470-160X, DOI: https://doi.org/10.1016/j.ecolind.2012.11.020., 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)Menéndez, Y.I. & Cabrera, G. 2014. "Litter macro-fauna in two systems with different land use and husbandry in Cuba". Cuban Journal of Agricultural Science, 48(2): 181-188, ISSN: 2079-3480. , 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)Cabrera, G., Robaina, N. & Ponce de León, D. 2011. "Riqueza y abundancia de la macrofauna edáfica en cuatro usos de la tierra en las provincias de Artemisa y Mayabeque, Cuba". Pastos y Forrajes, 34(3): 331-342, ISSN: 2078-8452. 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 2014Menéndez, Y.I. & Cabrera, G. 2014. "Litter macro-fauna in two systems with different land use and husbandry in Cuba". Cuban Journal of Agricultural Science, 48(2): 181-188, ISSN: 2079-3480. ). García et al. (2014)García, Y., Ramírez, W. & Sánchez, S. 2014. "Efecto de diferentes usos de la tierra en la composición y la abundancia de la macrofauna edáfica, en la provincia de Matanzas". Pastos y Forrajes, 37(3): 313-321, ISSN: 2078-8452. 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)Ramírez, W.M., Hernández, M.B., Zurita, A.A. & Navarro, M. 2018. "Performance of the edaphic macrofauna in animal husbandry in a productive entity of the Yaguajay municipality, Cuba". Pastos y Forrajes, 41(4): 241-247, ISSN: 2078-8452. 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)Moura, E.G., Aguiar, A., Piedade, A. & Rousseau, G. 2015. "Contribution of legume tree residues and macrofauna to the improvement of abiotic soil properties in the eastern Amazon". Applied Soil Ecology, 86: 91-99, ISSN: 0929-1393, DOI: https://doi.org/10.1016/j.apsoil.2014.10.008., 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)Pontégnie, M., Warnaffe, G.B. & Lebrun, P. 2005. "Impacts of silvicultural practices on the structure of hemiedaphic macrofauna community". Pedobiologia, 49(3): 199-210, ISSN: 0031-4056, DOI: https://doi.org/10.1016/j.pedobi.2004.09.005. 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)Zerbino, M.S., Altier, N., Morón, A. & Rodríguez, C. 2008. "Evaluación de la macrofauna del suelo en sistemas de producción en siembra directa y con pastoreo". Agrociencia, 12(1): 44-55, ISSN: 2521-9766., for their part, determined a positive correlation between the presence of Araneae order and the high values of phosphorus, clay and electrical conductivity.
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. 2013Rousseau, L., Fonte, S., Téllez, O., Van der Hoek, R. & Lavelle, P. 2013. "Soil macrofauna as indicators of soil quality and land use impacts in smallholder agroecosystems of western Nicaragua". Ecological Indicators, 27: 71-82, ISSN: 1470-160X, DOI: https://doi.org/10.1016/j.ecolind.2012.11.020., Menéndez and Cabrera 2014Menéndez, Y.I. & Cabrera, G. 2014. "Litter macro-fauna in two systems with different land use and husbandry in Cuba". Cuban Journal of Agricultural Science, 48(2): 181-188, ISSN: 2079-3480. , Escobar et al. 2017Escobar, A.D.C., Bartolomé, J. & González, N.A. 2017. "Estudio comparativo de la macrofauna del suelo en sistema agroforestal, potrero tradicional y bosque latifoliado en microcuenca del trópico seco, Tomabú, Nicaragua". Revista Científica de FAREM-Esteli, 6(22): 1-11, ISSN: 2305-5790., Pereira et al. 2017Pereira, J., Segat, J., Baretta, D., Vasconcellos, R., Baretta, C. & Cardoso, E. 2017. "Soil macrofauna as a soil quality indicator in native and replanted Araucaria angustifolia forests". Revista Brasileira de Ciência do Solo, 41, ISSN: 1806-9657, DOI: https://doi.org/10.1590/18069657rbcs20160261., Amazonas et al. 2018Amazonas, N.T., Viani, R.A.G., Rego, M.G.A., Camargo, F.F., Fujihara, R.T. & Valsechi, O.A. 2018. "Soil macrofauna density and diversity across a cronosequence of tropical forest restoration in Southeastern Brazil". Brazilian Journal of Biology, 78(3): 449-456, ISSN: 1678-4375, DOI: https://doi.org/10.1590/1519-6984.169014. and Cabrera-Mireles et al. 2019Cabrera-Mireles, H., Murillo-Cuevas, F.D., Adame-García, J. & Fernández-Viveros, J.A. 2019. "Impacto del uso del suelo sobre la meso y la macrofauna edáfica en caña de azúcar y pasto". Tropical and Subtropical Agroecosystems, 22: 33-43, ISSN: 1870-0462. ). According to Cabrera (2012)Cabrera, G. 2012. "La macrofauna edáfica como indicador biológico del estado de conservación/perturbación del suelo. Resultados obtenidos en Cuba". Pastos y Forrajes, 35(4): 349-364, ISSN: 2078-8452., 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)Magurran, A.E. 2004. Measuring biological diversity. 6th Ed. Ed. Blackwell Publishing. Malden, Massachusetts, U.S.A., p. 200, ISBN: 978-0-632-05633-0 . 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)Rivas, S.P., Carrillo, H., Bonilla, A., Bonilla, D.M. & Hernández, A.R. 2014. "Effect of disturbance on the ant community in a semiarid region of central Mexico". Applied Ecology and Environmental Research, 12(3): 703-716, ISSN: 1785-0037, DOI: https://doi.org/10.15666/aeer/1203_703716. 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 2011Fontela, J.L. & Matienzo, Y. 2011. "Hormigas invasoras y vagabundas de Cuba". Fitosanidad, 13(4): 253-259, ISSN: 1818-1686.). 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 2011Fontela, J.L. & Matienzo, Y. 2011. "Hormigas invasoras y vagabundas de Cuba". Fitosanidad, 13(4): 253-259, ISSN: 1818-1686., Cabrera 2019Cabrera, G. 2019. Evaluación de la macrofauna edáfica como bioindicador del impacto del uso y calidad del suelo en el occidente de Cuba. PhD Thesis. Universidad de Alicante, Valencia, España, p. 124. and Zenner 2019Zenner, I. 2019. "Invasions of four South American tramp ants: a systematic review". Revista UDCA Actualidad & Divulgación Científica, 22(1), ISSN: 2619-2551, DOI: https://doi.org/10.31910/rudca.v22.n1.2019.1207.).
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)Zerbino, M.S., Altier, N., Morón, A. & Rodríguez, C. 2008. "Evaluación de la macrofauna del suelo en sistemas de producción en siembra directa y con pastoreo". Agrociencia, 12(1): 44-55, ISSN: 2521-9766. identified Coleoptera order as a taxonomic group very sensitive to changes in soil use. Escobar et al. (2017)Escobar, A.D.C., Bartolomé, J. & González, N.A. 2017. "Estudio comparativo de la macrofauna del suelo en sistema agroforestal, potrero tradicional y bosque latifoliado en microcuenca del trópico seco, Tomabú, Nicaragua". Revista Científica de FAREM-Esteli, 6(22): 1-11, ISSN: 2305-5790. 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)Hernández-Chávez, M., Ramírez-Suárez, W., Zurita-Rodríguez, A.A. & Navarro- Boulandier, M. 2020. "Biodiversity and abundance of the edaphic macrofauna in two animal husbandry systems in Sancti Spíritus, Cuba". Pastos y Forrajes, 43(1): 18-25, ISSN: 2078-8452. 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 1940Bryant, E.B. 1940. "Cuban spiders of Museum of Comparative Zoology". Bulletin of the Museum of Comparative Zoology, 86(7): 249-532, ISSN: 1938-2987.), 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 2000Alayón, G. 2000. "Las arañas endémicas de Cuba (Arachnida: Araneae)". Revista Ibérica de Aracnología, 2: 1-48, ISSN: 1576-9518.).
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. 2008Hernández, M., Sánchez, S. & Simón, L. 2008. "Efecto de los sistemas silvopastoriles en la fertilidad edáfica". Zootecnia Tropical, 26(3): 319-321, ISSN: 0798-7269.).
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. 2019Cabrera-Mireles, H., Murillo-Cuevas, F.D., Adame-García, J. & Fernández-Viveros, J.A. 2019. "Impacto del uso del suelo sobre la meso y la macrofauna edáfica en caña de azúcar y pasto". Tropical and Subtropical Agroecosystems, 22: 33-43, ISSN: 1870-0462. ). 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. 2017Cabrera-Dávila, G.D.L.C., Socarrás-Rivero, A.A., Hernández-Vigoa, G., Ponce de León-Lima, D., Menéndez-Rivero, Y.I. & Sánchez-Rendón, J.A. 2017. "Evaluación de la macrofauna como indicador del estado de salud en siete sistemas de uso de la tierra, en Cuba". Pastos y Forrajes, 40(2): 118-126, ISSN: 2078-8452., Ramírez et al. 2018Ramírez, W.M., Hernández, M.B., Zurita, A.A. & Navarro, M. 2018. "Performance of the edaphic macrofauna in animal husbandry in a productive entity of the Yaguajay municipality, Cuba". Pastos y Forrajes, 41(4): 241-247, ISSN: 2078-8452. and Gutiérrez-Bermúdez et al. 2020Gutiérrez-Bermúdez, C.C, Mendieta-Araica, B.G. & Noguera-Talavera, A.J. 2020. "Trophic composition of edaphic macrofauna in animal husbandry systems in the Dry Corridor of Nicaragua". Pastos y Forrajes, 43(1): 32-40, ISSN: 2078-8452.).
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.