RESEARCH WORK

Functional composition of soil macrofauna in four land uses of Artemisa and Mayabeque provinces, Cuba

Grisel Cabrera¹, Nayla Robaina² y D. Ponce de León³

¹ Instituto de Ecología y Sistemática, CITMA, Carretera de Varona km 3½, Capdevila, Boyeros, C.P. 10800, La Habana, Cuba
E-mail: grisel17@ecologia.cu
² Estación Experimental de Plantas Medicinales, Artemisa, Cuba
³ Facultad de Agronomía, Universidad Agraria de La Habana, Artemisa, Cuba

ABSTRACT

The objective of this study was to analyze the functional composition of soil macrofauna in different land use types including secondary forest, pastures, fields with varied crop cultivation destined to potato production and sugarcane fields. The land use systems were located in the Artemisa and Mayabeque provinces. In these systems the edaphic macrofauna was collected in October, at the end of the rainy season of 2009, using the TSBF methodology. The data processing included the determination of the density and biomass of the macrofauna functional groups in each land use, and the statistical analysis implicated the Kruskal-Wallis nonparametric test. The soil engineers and/or detritivores communities were observed to be better represented in density in the majority of land uses, and in biomass, the detritivore and/or herbivore functional groups. The proportion between the functional groups of soil macrofauna in the land uses depended on land use intensity, the disturbance level of the edaphic environment and the availability of resources.

Key words: Soil organism, multiple land use.

INTRODUCTION

The activity of the different functional groups included in the soil macrofauna, among them soil engineers, detritivores, herbivores and predators, allows the regulation of edaphic processes and the functioning and balance of the ecosystem.

Soil engineers, which involve groups that consume organic matter, such as worms (Haplotaxida) and termites (Isoptera), and omnivore organisms, such as ants (Hymenoptera: Formicidae), have a specific impact on the soil interior from the transformation of its physical properties, which favor aggregate formation and the structure, movement and retention of water, as well as gaseous exchange (Lavelle, 2000). Detritivores, such as millipedes (Spirobolida, Polydesmida and others), woodlice (Isopoda) and snails (Archaeogastropoda) mainly, have a function at the soil surface level as epigeal organisms, because as they feed on litter, they aid its fragmentation and start the decomposition process, increasing the exposure surface for the microflora attack.

Herbivores include some coleopteran families (Coleoptera), hemipterans (Hemiptera) and other insect orders, and predators primarily include arachnids (Araneae, Opilionae, Pseudoscorpionida) and centipedes (Geophilomorpha, Scolopendromorpha), which intervene at other levels of the trophic chain by consuming plant material and live animals, respectively, which gives origin to the richness and quality of these materials in the soil (Lavelle, 1997). According to the statements made by Zerbino et al. (2008), the interactions among all functional groups are determined by the available resources in the different land uses.

In a gradient from seminatural ecosystems to agroecosystems there are peculiar characteristics in the edaphic environment, including its associated biota. In the humid tropic ecosystems such as forests, agroforestry systems, pasturelands and polycultures, many authors have detected the dominance in terms of density of detritivore arthropods and engineer groups of the ecosystem; while among engineers endogenous earthworms have constituted the major component in biomass (Barros et al., 2002; Huerta-Lwanga et al., 2008). Granados and Barrera (2007) stated that the first colonizers of the edaphic macrofauna are those capable of utilizing the organic matter content in the systems with a continuous and abundant contribution of it, followed by predators that feed from the favored groups and finally omnivore and herbivore groups appear. In the case of herbaceous systems, with almost total influence of grasses and where there is a large amount of aerial and underground phytomass, the major macrofauna components have been herbivores; earthworms and termites have also been favored, stimulated by carbon mineralization from root exudates (Laossi et al., 2008).

In Cuba the studies stressing the separation of functional groups of the edaphic macrofauna for the analysis of their function in ecosystems are still insufficient. In this sense some works can be mentioned specifically conducted with the earthworm communities (Rodríguez, 2000; Martínez, 2002), although there are macrofauna studies which have taken into consideration the characterization of its functional and trophic composition in agroecological systems in the country (Cabrera et al., 2007).

The objective of this study was to analyze the functional composition of soil macrofauna in four land uses, which study systems were located in the Artemisa and Mayabeque provinces.

MATERIALS AND METHODS

Description of the studied land uses

A land use gradient was studied involving four uses: secondary forests, pasturelands, varied crop areas destined to potato production and sugarcane plantations. These uses were chosen within the Red Plain of the former Havana province, currently located between the Artemisa and Mayabeque provinces. The soil type in all the uses was Ferralitic Red, according to the classification made by Hernández et al. (1999).

Within the use secondary forests, the work was done in three areas located in the localities Managua, Nazareno (San José de las Lajas municipality) and Aguacate (Madruga municipality) of the Mayabeque province. These areas had different regeneration/anthropization levels, were from 40 to 120 years old and had extensions between two and five hectares. They showed semideciduous vegetation, with predominance in the tree stratum of fruit and timber species, among them: sapote (Pouteria sapota H.E. Moore & Stearn), mango (Mangifera indica L.), star apple (Chrysophyllum cainito L.), red flamboyant (Delonix regia (Boj. Ex Hooker) Raf.), royal palm (Roystonea regia (Kunth) O.F. Cook), baría (Cordia gerascanthus L.), ocuje (Calophyllum inophyllum L.), yamagua (Guarea guidonia (L.) Sleumer), teak (Tectona grandis L. fil.), Cuban mahogany (Swietenia mahagoni (L.) Jacq.), cedar (Cedrela odorata L.), pine (Pinus sp.) and Blue Mahoe (Talipariti elatum (L.) Fryxell).

For the use pasturelands two areas were chosen in the San José de las Lajas municipality of the Mayabeque province, with a maximum extension of 12 ha. They are naturalized pastures with more than 12 years of exploitation and the principal pasture species were: Guinea grass (Panicum maximum Jacq.) and star grass (Cynodon nlemfuensis Vanderyst), which showed a cover between 80 and 90%. On them cattle of the Holstein and Siboney breeds grazed, and the management was mainly intensive rational rotational with mean stocking rate of 2,8 animals ha-1.

In the case of varied crops, which main crop was potato (Solanum tuberosum L.), three areas were selected in the municipalities Güira de Melena (Artemisa province), Batabanó and Güines, belonging to Mayabeque. The selected sites had extensions between 20 and 50 ha and the main crop was in constant rotation with sweet potato (Ipomoea batata (L.) Lam.), taro (Colocasia esculenta (L.) Schott), beans (Phaseolus vulgaris L.), corn (Zea mays L.), squash (Cucurbita moschata (Duch.. ex Lam.) Duch. ex Poir) and cassava (Manihot esculenta (L.) Crantz). Among the weeds in the areas the following stood out: Sorghum halepense (L.) Pers., Cyperus rotundus L., Amaranthus hybridus L. and Bidens pilosa L. They are areas dedicated to agriculture for more than 10 years, mainly with traditional tillage and electrical spray irrigation. The NPK application in these systems was 1 490 kg ha-1 year-1.

For the sugarcane plantation use, the three chosen sites with sugarcane (Saccharum officinarum L.) were located in the municipalities (Güira de Melena (Artemisa province), San Nicolás de Bari and Madruga, belonging to Mayabeque, occupied by the varieties CP 52-43 and C 86-12, C 323-68 and C 86-56, respectively. Each studied sugarcane area has more than 20 years of exploitation and an extension of around 15 ha. The main weeds in the systems were S. halepense, C. rotundus, Rottboellia cochinchinensis L.F. and Eleusine indica (L.) Gaertn. They have gravity irrigation systems and electrical coil system; the chemical fertilization was: 50-60 kg ha-1 year-1 of urea, 20-83 kg ha-1 year-1 of K2O and 25 kg ha-1 year-1 of P2O5.

Sampling and processing of the edaphic macrofauna

The sampling was made at the end of the rainy season, 2009, in October. This is the moment described as suitable for the collection, due to the highest activity of the macrofauna. In the different areas of land use, the macrofauna collection was performed according to the Methodology of the International Program «Tropical Soil Biology and Fertility» or TSBF (Anderson and Ingram, 1993; Lavelle et al., 2003). In each area or replication of land use eight 25 x 25-cm soil monoliths were extracted, up to 30 cm of depth, at a distance of 20 m from each other. The sampling responded to a completely randomized design, where the macrofauna was manually collected in situ.

From the functional point of view the macrofauna was clustered into four main groups: soil engineers, detritivores, herbivores and predators, according to Lavelle (1997) and Zerbino et al. (2008). The analysis was made of only these four functional groups, because they have a defined function in the ecosystem and the effect they cause on the transformation of soil properties. The taxonomic identification was made at order and family level, and only one order was identified to the subfamily level to define the functional group (Brinkhurst and Jamieson, 1971; Borror et al., 1976; Sims, 1980; Pérez-Asso, 1995, 1996, 1998; Brusca and Brusca, 2003). The density regarding the number of individuals and the biomass from the humid weight in preserving solution, of the different functional groups for each land use, was determined.

In order to determine the density and biomass variations for each of the functional groups, among uses, the non parametric Kruskal-Wallis analysis was used and as a posteriori test for the mean comparison, the Mann-Whitney U test with Bonferroni adjustment was used. The statistical processing was made through the program PAST-1.75, 2001.

RESULTS AND DISCUSSION

The macrofauna could be associated to the functional groups of soil engineers, detritivores, herbivores and predators, which were always present in all the land uses. Among detritivores, the macrofauna orders, commonly found in most uses were Blattodea, Isopoda, Polydesmida, Polyxenida and Spirobolida, and from Coleoptera only the Tenebrionidae family. In the case of herbivores, in all uses the coleopteran larvae from the Scarabaeidae and Elateridae (Elaterinae) families were observed, which feeding habits respond to root herbivory, and from the order Hemiptera, included as leaf herbivores (they affect the foliage but can be found on the soil). For predators, the coinciding taxonomic units were Araneae, Scolopendromorpha and Coleoptera adults of the Carabidae and Staphylinidae (Staphylininae) families (table 1).

Regarding density, in the secondary forests detritivores prevailed (701 ind.m-2), followed in lesser quantity by engineers (320 ind.m-2), predators (96 ind.m-2) and, lastly, herbivores (38 ind.m-2). In the pasturelands and varied crops there was predominance of soil engineers (386 and 179 ind.m-2, respectively) followed by herbivores (116 and 36 ind.m-2), and with lower density detritivores (51 and 28 ind.m-2), and predators (25 and 18 ind.m-2) were found. Regarding this variable, in sugarcane plantations, the first position was for soil engineers too (124 ind.m-2) and after them, almost at the same level, detritivores (69 ind.m-2), and predators (62 ind.m-2); the least represented in this use were herbivores (19 ind.m-2) (Fig. 1).

Regarding biomass, the secondary forests responded to the same pattern as density, with the decreasing order of detritivores (33 gm-2) engineers (27 gm-2) predators (2,8 gm-2) herbivores (2,1 gm-2). In pasturelands herbivores prevailed (4,6 gm-2), and then detritivores (2 gm-2), engineers (1,2 gm-2) and predators (0,2 gm-2). In varied crops herbivores (3,4 gm-2) and engineers (3,0 gm-2), prevailed, and with very low biomass detritivores (1,1 gm-2), and predators (0,1 gm-2) followed. In the sugarcane plantations detritivores (5,6 gm-2) stood out, and the other functional groups were poorly represented regarding biomass in this use (herbivores: 0,7 gm-2, predators: 0,6 gm-2, engineers: 0,1 gm-2). (Fig. 1)

Significant differences were obtained among uses for the different functional groups, in density as well as biomass (p<0,05), except in herbivores regarding biomass (p>0,05).

Soil engineers in secondary forests and in general in all uses, as compared to density, had a strong influence of termites or ants, and in biomass, earthworms stood out. Luizão (1995) and Barros et al. (2002) also found higher density of these social insects among all the edaphic fauna in forests, pasturelands and crop systems of the Brazilian Amazonia, and Linares et al. (2009) detected soil engineers, including earthworms, as the most abundant in the forests and agroforestry systems of Peru.

Particularly, the behavior of earthworms indicated the level of anthropic intervention due to land use intensity and the degree of disturbance of the edaphic environment, as it was also found by diverse authors when evaluating the change of these communities before the impact of different land uses and due to the effect of different land management types in the tropics (Rodríguez, 2000; Feijoo et al., 2007).

Forests showed the highest density values (103 ind. m-2) and biomass (27 gm-2) of earthworms, in spite of being of secondary formation, but with higher stability as they did not have continuous tillage activities or grazing, as compared to the other uses. Pasturelands followed regarding density (31 ind.m-2), characterized by a moderate intervention degree only due to the grazing activity, and finally varied crops (21 ind.m-2) and sugarcane plantations (1,33 ind.m-2), which have a higher disturbance level due to the repeated practice of agricultural yields and lower shade because of the absence of the tree stratum; this is also characteristic in the use pasturelands, which causes severe damage in earthworm populations. However, varied crops had slightly higher biomass values (2,93 gm-2) than pasturelands (0,88 gm-2) and sugarcane plantations (0,012 gm-2), which could have been beans, which benefits the edaphic environment because of nutrient contribution, all of which could have resulted in advantage for earthworms.

The detritivore proportion within the macrofauna community can also indicate the disturbance status of an ecosystem. Detritivores in this study, as mentioned above, had a better representation in density and biomass in secondary forests, and the lowest values in pasturelands and varied crops. In the use sugarcane plantations, in biomass, detritivores constituted the prevailing group as compared to the other functional groups, but with very low values similar to those of pasturelands and varied crops.

About the affectations of the detritivore community in systems with different disturbance degree, Rodríguez et al. (2002) reported that a definitive factor for its establishment is litter quality expressed by a low C/N ratio; on the other hand, Zerbino et al. (2008) stressed that detritivores as unprotected organisms on the soil surface, are drastically reduced due to sudden variations in its temperature and humidity conditions because of the lower cover and residue quantity, and a higher exposure to solar radiations in those altered ecosystems. These characteristics prevailed in the uses of this study which had less shade and a deeper and more constant soil management; hence a reduced community of detritivores was shown as compared to secondary forests, mainly by pasturelands and varied crops.

On the other hand, Barraqueta (2001) and Linares et al. (2009) asserted that the transformations in the soil environmental conditions caused by agricultural activity and the subsequent mechanical destruction of microhabitats, have negative repercussion on the main groups which decompose organic matter, such as millipedes, woodlice and snails. They also expressed that the application of less strong treatments which allow conservation, to a higher or lesser extent, of the old litter layer and soil structure, would permit a fundamental protection of these fauna communities and their function.

Herbivores not only had a strong constitution in density and biomass in the uses pasturelands and varied crops; in the latter they were also represented by some families of the order Coleoptera considered pests and which are frequent in agricultural crops (for example: Attelabidae and Chrysomelidae, table 1).

In general, in the study, the order Coleoptera had the highest variety of functional groups (detritivore, herbivore and predator families), with incidence of larvae as well as adults. Villalobos et al. (2000) stated that each development stage (larva or adult) in different soil organisms can play an exclusive role in the edaphic environment at a given moment. These authors also emphasized Elateridae and Melolonthidae as more common Coleoptera families and with presence of larvae and/or adults, in the edaphic profile. Other important families in the soil are Curculionidae, Tenebrionidae, Nitidulidae, Carabidae and Staphylinidae (Menendez, 2010). Coleopteran larvae, with their endogeous life habit, can act on the transformation of the soil physical properties, and adults mainly utilize the useful surface resources.

In this work, Scarabaeidae and Elateridae (Elaterinae) larvae, as root herbivores, could be benefitted due to the availability of the feeding resource, because of the higher root density, especially of grasses in pasturelands, and of crops and accompanying weeds in varied crop systems. According to Hernandez (1999), in savanna and pastureland ecosystems root development can exceed 80 % of the total plant weight, and this author mentions that large root amounts support the microorganisms and fauna of the edaphic community.

On the other hand, varied crop areas are subject to a rotation system, and according to Fraser (1994), the rotation of different crops in time diversifies the aerial plant biomass and produces modification in the edaphic environment due to the selectiveness in the nutrient absorption and contribution, because of root excretions and the entrance of detritus and roots in the environment, all of which contributes to the presence of diverse organisms, among them leaf herbivores.

On the higher representation of predators (in density and biomass) in the uses secondary forests and sugarcane plantations, the higher quantity of detritivores, which could have served as food for such functional group, is likely to have had influence. Nevertheless, Pontégnie et al. (2005) associated the presence of certain predator groups, including Araneae, to abiotic factors such as temperature and humidity and not to the availability of their preys. These authors also mentioned some orders moderately sensitive to disturbances in the edaphic environment, such as Geophilomorpha and Scolopendromorpha of the Chilopoda class. On the contrary, for the families Carabidae and Staphylinidae of the order Coleoptera, the importance of the available food amount in the selection of their habitats is mentioned, and they mainly consume eggs, larvae and adults of other small insects (Baloriani et al. 2009).

Previously Lee (1985) reported that intensive annual crop systems housed small populations of predators and afterwards Zerbino et al. (2008) found that predators showed higher richness and abundance in continuous crop systems, and Araneae is one of the main taxa; this coincides, partly with the results of this work, because this order appeared not only in sugarcane plantations and varied crops, it was also present in pasturelands and secondary forests. These last authors observed that the environments which were characterized by low organic matter contents, high phosphorus and clay values and electric conductivity, were positively correlated to this functional group.

In general, as stated by Zerbino et al. (2008), the differences in the proportion of functional groups of the macrofauna communities in different land uses, can be ascribable to the richness of plant species, the changes in soil properties and the management, which in turn determine the quantity and quality of resources and affect the interactions among groups.

CONCLUSIONS

The functional groups of highest representativeness in density in all land uses were soil engineers and/or detritivores, followed by herbivores and predators, except in pasturelands and varied crops, where herbivores were second in importance. Regarding biomass, likewise, detritivores and/or herbivores prevailed in the studied uses; yet, in secondary forests this last group showed the lowest biomass. With very low biomass values engineers and predators prevailed, although engineers stood out as second group in secondary forests and varied crops because of the influence of earthworms. The proportion of the different functional groups of soil macrofauna varied regarding land use intensity, disturbance level of the edaphic environment and resource availability.

ACKNOWLEDGEMENTS

The results were obtained within the framework of the Master of Soil Science of the Agricultural University of Havana, funded by the Research Project 08-22 «Causes of the degradation of Feralitic Red soil structure of the Red Plain of Havana», of the PRCT Protection of the Cuban Environment and Sustainable Development.