The change in land use and its use intensity has a direct impact on the structure of vegetation and physical-chemical properties of soil, and an indirect impact on abundance, richness and diversity of the edaphic macrofauna, as well as on its functional composition. (Tapia et al. 2016Tapia, S.C., Teixeira, L.A., Velázquez, E. & Waldez, F. 2016. "Macroinvertebrados del suelo y sus aportes a los servicios ecosistémicos, una visión de su importancia y comportamiento". Revista Colombiana de Ciencia Animal-RECIA, 8 (Dec 1): 260-267, ISSN: 2027-4297, DOI: https://doi.org/10.24188/recia.v8.n0.2016.380. and Silva et al. 2018Silva, R.A., Siqueira, G.M., Lima, M.K., Guedea, O. & de Franca, E.F. 2018. "Spatial variability of soil fauna under different land uses and managements". Revista Brasileira de Ciencia do Solo, 42, ISSN: 1806-9657, DOI: http://dx.doi.org/10.1590/18069657rbcs20170121.). Other factors that affect the edaphic macrofauna are type of soil, content of nutrients and organic matter, pH, texture and structure, as well as factors of climatic origin such as rainfall, temperature, wind speed and relative air humidity (Machado et al. 2015Machado, D., Gervasio, M., Fernández, M.E., Ribeiro, A. & Menezes, C.E.G. 2015. "Fauna edáfica na dinámica sucessional da Mata Atlántica em floresta estacional semidecidual na bacia do Rio Paraíba do Sul R.J". Ciência Florestal, 25(1): 91-106, ISSN: 1980-5098, DOI: https://doi.org/10.1590/1980-509820152505091.).
Absence or reduction of tree stratum in grasslands simplifies plant structure, which leads to litter homogenization, changes in temperature, insolation and organic matter content. All of this causes a decrease in niches and in populations of different groups of macrofauna (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, España, p. 124 .). Animal grazing may be one of the causes of edaphic macrofauna reduction, in which the response of invertebrates depends on stocking rate and grazing intensity. In addition, the trampling of animals causes a decrease of stability of organo-mineral aggregates, an increase of their compaction and, consequently, less water infiltration and oxygen availability, which limits the activity of this fauna (Bautista et al. 2009Bautista, F., Díaz, C. & García, M. 2009. "Changes in soil macrofauna in agroecosystems derived from low deciduos tropical forest on leptosols from karstic zones". Tropical and Subtropical Agroecosystem, 10(2): 185-197, ISSN: 1870-0462.). The objective of the present research was to evaluate the performance of richness and abundance of edaphic macrofauna in five grassland agroecosystems in Granma province.
The research was developed in five grassland agroecosystems of Granma province, located in the southwestern portion of the eastern region of Cuba. Agroecosystems El Triángulo, El Progreso, Cupeycito, Ojo de agua and Estación de Pastos show contrasting characteristics regarding type of soils, management and productive purpose (table 1).
T: El Triángulo P: El Progreso
Experimental period. The study was developed in the period between July 2014 and March 2017. Provincial means of climatic variables are shown in table 2. To facilitate the statistical analysis and characterization of the variables under study, three years were defined: year 1: rainy period (PLL)-2014 and dry period (PPLL)-2015, year 2: PLL-2015 and PPLL-2016 and year 3: PLL-2016 and PPLL-2017.
⃰Data taken from provincial means from the Anuario Estadístico de Cuba (ONEI)
In the rainy period, the months from July to September were used as sampling months and from January to March in dry period, as they were the most representative months of both climatic periods. For this, the criteria of specialists from the Provincial Meteorology Center in Granma were considered.
Sampling and identification 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. Oxford University Press, Oxford, UK, p. 221, ISBN: 978-0851988214.) 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. 1st Ed. Ed. Secretaría de Medio Ambiente y Recursos Naturales, p. 350, ISBN: 9786077908319 6077908312. ). 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, five monoliths were extracted per hectare, measuring 25 x 25 x 20 cm, at a distance of 20 m. In situ macrofauna individuals were manually collected and counted. Worms (Oligochaeta: Haplotaxida) 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 its 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.
Afterwards, an aqueous solution (0.003 %), prepared with LABIOFAM commercial liquid detergent, 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 entomology laboratory from the Provincial Laboratory of Plant Health in Granma. With the use of the stereoscope, individuals were extracted from the solution and counted, and placed in vials with 70% ethanol. Variables number of individuals (abundance) and number of taxonomic units (richness) were defined.
To identify the preserved specimens, keys and taxonomic references 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 Publishing, New York, USA, ISBN: 9780072909616., Brusca and Brusca (2003)Brusca, R.C. & Brusca, G.J. 2003. Invertebrados. 2nd Ed. Pardos-Martínez, F. (ed.). Ed. McGraw-Hill Interamericana, Universidad Complutense de Madrid, Madrid, España, p. 973. 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 theoretical assumptions of the analysis of variance for variables number of individuals and number of taxonomic units were verified, from Shapiro and Wilk (1965)Shapiro, S. & Wilk, B. 1965. "An analysis of variance test for normality (complete samples) ". Biometrika, 52(2): 591-611, ISSN: 1464-3510, DOI: http://dx.doi.org/10.2307/2333709. test for normality of errors and Levene (1960)Levene, H. 1960. Robust tests for the equality of variance. Contributions to Probability and Statistics. 1st Ed. Ed. Stanford University Press, Palo Alto, California, USA, pp. 278-292. test for variance homogeneity. As the analyzed variables did not fit with the theoretical assumptions of ANAVA, the transformations √x and √x+1 were used. However, as they did not improve the fulfillment of these assumptions, non-parametric analysis of variance was carried out by Wilcoxon (Mann-Whitney U) method (Lehmann 1975Lehmann, E.L. 1975. Nonparametrics: Statistical Methods based on Ranks, San Francisco. Holden-Day, Inc., USA, DOI: https://doi.org/10.1002/zamm.19770570922.), for independent samples based on the ranges of original observations. Conover (1999)Conover, W.J. 1999. Practical Nonparametric Statistics. 3rd Ed. Ed. John Wiley & Sons. New York, USA, p. 584, ISBN: 978-0-471-16068-7. test was applied to compare mean ranges. The statistical program INFOSTAT version 2012 was used (Di Rienzo et al. 2012Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., González, L., Tablada, M. & Robledo, C.W. 2012. InfoStat version 2012 [Windows]. Grupo InfoStat, Universidad Nacional de Córdoba, Argentina. Available: http://www.infostat.com.ar.).
An amount of 28,030 individuals was captured in the five agroecosystems, in the experimental period, of them 6,423 in monoliths and 21,607 in pitfall traps. In Estación de Pastos agroecosystem, the largest number of individuals was captured by both sampling methods (figure 1).
In Estación de Pastos agroecosystem, a greater number of classes/orders (as superior taxonomic units) was observed, with 17 and the highest total number of taxonomic units (73) of the most abundant and diverse edaphic macrofauna (figure 2).
Other authors have also reported greater diversity and density of edaphic macrofauna in silvopastoral systems, in relation to grass monoculture grasslands (Cabrera et al. 2017Cabrera, G., Socarrás, A., Hernández, G., Ponce de León, D., Menéndez, Y. & Sánchez, J. 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. y 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. ). 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. ). Likewise, 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. commented that livestock systems with arboreal elements demonstrate richness of groups and an abundance of macrofauna comparable with those of natural ecosystems such as forests, due to the greater availability of resources for refuge and feeding of the edafofauna.
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 (Phylum: Annelida), for example, require oxygen dissolved in soil solution to breathe (Cabrera et al. 2019Cabrera, H., Murillo, F.D., Adame, J. & Fernández, 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 these 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.
Abundance (number of individuals) and richness (number of taxonomic units) of the edaphic macrofauna, showed variable performance, in both climatic periods in the two sampling methods (tables 3 and 4). It was not possible to establish the pattern of abundance of this edaphic group in one or another climatic period, that is, there was no constant relationship between season and the studied variables.
† Mean of assigned ranges, (): mean of original data, SD: standard deviation
For example, in the monolith method, no significant differences were found in any evaluated year in El Triángulo agroecosystem, although during dry season, corresponding to the third year, the presence of individuals was not observed, from which it is inferred that there was a better performance of the macrofauna in rainy period (table 2). In El Progreso, the number of taxonomic units in the second year was superior during dry season. In the third year, there were differences in the two evaluated variables, with better performance in the rainy season.
In Cupeycito, the number of taxonomic units was also significantly higher in the dry season of the second year. In Ojo de agua, during the first year, the number of individuals was superior in the rainy season, while, in the third year, the number of taxonomic units had better performance in dry season. In Estación de Pastos, no significant differences were detected in any evaluated period for any of the two variables.
In the case of pitfall traps, in El Triángulo agroecosystem, better performance of the two variables under study was evidenced in the dry period of the second year (table 3). In the case of El Progreso, the number of individuals was superior in dry season corresponding to the second year, while, in the third year, the two variables had a better performance in rainy season.
In Cupeycito agroecosystem, significant differences were only found in the number of taxonomic units, in the first and second year. In the first, the indicator had a better performance in the rainy season, while it was superior in the second during dry season. However, in Ojo de agua, significant differences occurred in the number of individuals, in the first year, with a higher value in PLL, while in the second year, a better performance of the variable number of taxonomic units was observed during PPLL.
In Estación de Pastos agroecosystem, significant differences were detected in the indicators studied in the first and third years. In both, the highest values were observed in rainy season.
Several researchers coincide in stating that the highest abundance of individuals of the edaphic macrofauna is observed during rainy period, and they even recommend this period for samplings (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. and Noguera et al. 2017Noguera, A., Reyes, N., Mendieta, B. & Salgado, M.M. 2017. "Macrofauna edáfica como indicador de conversión agroecológica de un sistema productivo de Moringa oleifera Lam. en Nicaragua". Pastos y Forrajes, 40(4): 265-275, ISSN: 2078-8452. ). According to Souza et al. (2016)Souza, S.T., Cassol, P.C., Baretta, D., Bartz, M.L.C., Klauberg, V., Mafra, A.L. & Gonçalves, M. 2016. "Abundance and diversity of soil macrofauna in native forest, eucalyptus plantations, perennial pasture, integrated crop-livestock, and no-tillage cropping". Revista Brasileira de Ciencia do Solo, 40, ISSN: 1806-9657, DOI: https://doi.org/10.1590/18069657rbcs20150248., the greatest diversity and abundance of edaphic fauna is generally found in the rainy season, since water contributes with vital processes of these organisms such as respiration, reproduction and feeding. Nevertheless, the conditions that promote water excess cause the edaphic communities to decrease, either because they come to the surface or migrate to deep soil strata, in search of more appropriate micro-environments for their establishment (Cabrera and López 2018Cabrera, G. & López, G.M. 2018. "Ecological characterization of soil macrofauna in two evergreen forest sites at El Salón, Sierra del Rosario, Cuba". Bosque, 39(3): 363-373, ISSN: 0304-8799, DOI: https://doi.org/10.4067/S0717-92002018000300363. ).
In this sense, Brown et al. (2001)Brown, G., Fragoso, C., Barois, I., Rojas, P., Patrón, J.C., Bueno, J., Moreno, A.G., Lavelle, P., Ordaz, P. & Rodríguez, C. 2001. "Diversidad y rol funcional de la macrofauna edáfica en los ecosistemas tropicales mexicanos". Acta Zoológica Mexicana, (nueva serie), (Es1), 79-110, ISSN: 0065-1737. , in grasslands of Mexico, verified that density of edaphic macrofauna was two times superior in rainy season compared to dry season, and they related it to the greater presence of earthworms and termites. On the other hand, Hernández et al. (2018)Hernández, G., Cabrera, G., Izquierdo, I., Socarrás, A., Hernández, L. & Sánchez, J. 2018. "Indicadores edáficos después de la conversión de un pastizal a sistemas agroecológicos". Pastos y Forrajes, 41(1): 3-12, ISSN: 2078-8452. observed superior performance of the edaphic macrofauna in rainy period with respect to dry season in grassland, forage and polyculture areas in Cangrejeras town, Artemisa, Cuba.
The distribution of soil macrofauna depends on several factors such as rainfall or climate seasonality, which, at the same time, define temperature and humidity of soil, since they are the edaphoclimatic variables that influence the most on macrofauna of tropical soils (Cabrera and López 2018Cabrera, G. & López, G.M. 2018. "Ecological characterization of soil macrofauna in two evergreen forest sites at El Salón, Sierra del Rosario, Cuba". Bosque, 39(3): 363-373, ISSN: 0304-8799, DOI: https://doi.org/10.4067/S0717-92002018000300363. ). All these factors have wide variability in the climatic region in which the studied agroecosystems are located (Montecelos et al. 2018Montecelos, Y., Cavazos, T., Kretzschmar, T., Vivoni, E.R., Corzo, G. & Molina, E. 2018. "Hydrological modeling of climate-change impacts in a tropical river basin. A case study of the Cauto River, Cuba". Water, 10(9): 1135-1143, ISSN: 2073-4441, DOI: https://doi.org/10.3390/w10091135.), which could influence on the variable performance of macrofauna.
In this sense, a very important part of interannual variability of climatic elements in Cuba is explained by the presence of El Niño/Southern Oscillation (ENSO), which tends to favor greater precipitation during dry season (Álvarez et al. 2015Álvarez, A., Febles, G. & Díaz, L. "La variabilidad climática y análisis de contextos futuros de cambio climático en la Cuenca del Cauto". Ciencias de la Tierra y el Espacio, 16: 107-116, ISSN: 1729-37. and Montecelos et al. 2018Montecelos, Y., Cavazos, T., Kretzschmar, T., Vivoni, E.R., Corzo, G. & Molina, E. 2018. "Hydrological modeling of climate-change impacts in a tropical river basin. A case study of the Cauto River, Cuba". Water, 10(9): 1135-1143, ISSN: 2073-4441, DOI: https://doi.org/10.3390/w10091135.). This phenomenon had an intense manifestation between 2015 and 2016 (Galván et al. 2018Galván, R., Carbonetti, M., Gende, M. & Brunini, C. 2018. "Impact of the extreme 2015-2016 ENOS event on the geometry of the earth surface in the equatorial region of South America". Geoacta, 42(2): 23-44, ISSN: 852-7744. ), period included in this research. In agroecosystems in which significant differences were found in the studied variables, in the second year (PLL 2015- PPLL 2016) of research, the best performance was observed in dry season. Regarding rainfall, it can be observed (table 2) that in 2015, the frequency of days with rains was higher compared to 2016 and 2017, which directly influenced on soil humidity and, at the same time, on the performance of the edaphic fauna, as stated above.
On the other hand, Cabrera (2019)Cabrera, 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, España, p. 124 . recognized that any natural or anthropic intervention generates positive or negative impact on dynamics of the edaphic macrofauna, while Kamau et al. (2017)Kamau, S., Barrios, E., Karanja, N., Ayuke, F. & Lehmann, J. 2017. "Soil macrofauna abundance under dominant tree species increases along a soil de gradation gradient". Soil Biology and Biochemistry, 112: 35-46, ISSN: 1879-3428, DOI: https://doi.org/10.1016/j.soilbio.2017.04.016. stated that it is more susceptible to environmental changes than other groups of edaphic fauna due to its larger size.
Other factors that could influence on the performance of macrofauna are of edaphic origin, such as type of soil, content of nutrients and organic matter, pH, texture, structure, and edaphic temperature and humidity (Machado et al. 2015Machado, D., Gervasio, M., Fernández, M.E., Ribeiro, A. & Menezes, C.E.G. 2015. "Fauna edáfica na dinámica sucessional da Mata Atlántica em floresta estacional semidecidual na bacia do Rio Paraíba do Sul R.J". Ciência Florestal, 25(1): 91-106, ISSN: 1980-5098, DOI: https://doi.org/10.1590/1980-509820152505091.). There are also those related to vegetation and anthropic management, which, in the case of the studied agroecosystems, are determined by vegetation cover, type of pasture and weeds, presence of trees, as well as grazing management. Trampling of animals causes the mechanical destruction of microhabitats. According to Lok (2005)Lok, S. 2005. Estudio y selección de indicadores de la estabilidad en el sistema suelo planta de pastizales en explotación. PhD Thesis. Departamento de Pastos, Instituto de Ciencia Animal, Mayabeque, Cuba, p. 98. , compaction of soils used for livestock by a certain stocking rate can reduce the population of edaphic invertebrates.
It is also necessary to point out versatility in the spatial-temporal distribution of soil macrofauna, which depend on specific conditions of soil microhabitat, due to its own heterogeneity. This leads to organisms not to be homogeneously distributed within the soil in a given space and time, but depending on the availability of food resources, which is greater in carbon-rich areas such as rhizosphere of plants, organic detritus from decomposition of litter and animal depositions. In this sense, soil structure and texture also influence, in addition to other physical properties.
In order to explain the variability of results, ecological characteristics of the edaphic macrofauna are added to all above, which has an aggregated spatial distribution. It means that they will explore those optimal microsites in terms of quantity and quality of food, humidity, temperature, pH, aeration, absence of toxic substances and protection from solar radiation (de la Rosa and Negrete 2012De la Rosa, N. & Negrete, S. 2012. "Spatial distribution of soil macrofauna in cloud forest, secondary forest and grassland in La Cortadura reserve, Coatepec, Veracruz, Mexico". Revista Mexicana de Biodiversidad, 83(1): 201-215, ISSN: 1870-3453. and Rusanov and Bulgakova 2016Rusanov, A. M. & Bulgakova, M. A. 2016. "Composition and abundance of soil macrofauna in pasture ecosystems of the steppe zone of the Urals". Russian Journal of Ecology, 47(1): 68-73, ISSN: 1608-3334, DOI: https://doi.org/10.1134/S1067413616010136.).
It is concluded that, in the studied grassland agroecosystems, the edaphic macrofauna had a heterogeneous performance in the evaluated climatic periods. A superior performance of the macrofauna was observed during dry period of the second year, which could be related to the atypical performance of total volume of rainfall and/or days with rain of that year.