RESEARCH WORK
Edaphic macrofauna as biological indicator of the conservation/disturbance status of soil. Results obtained in Cuba
Grisel Cabrera
1Instituto de Ecología y Sistemática, CITMA. Carretera de Varona km 3 1/2 Capdevila, Boyeros, La Habana 19 CP 11900, Cuba
E-mail: grisel17@ecologia.cu
ABSTRACT
In order to predict the degradation status of a soil, a group of variables comprising its physical, chemical and/or biological properties is used. Macrofauna, which includes soil invertebrates higher than 2 mm of diameter, is a biological component that can be used for such purpose. Its taxonomic richness as well as its density, biomass and functional composition change depending on the effect of diverse land uses and managements. This review reaffirms that the macrofauna characteristics and the results obtained, mainly in Cuba, about its variation in ecosystems with different anthropization levels, support the potential use of this fauna as biological indicator of the soil's conservation status. Future studies should consider a lower taxonomic level in the identification of macrofauna, and relate its taxonomic and functional composition to the climate and pedological factors.
Key words: soil conservation, soil fauna.
INTRODUCTION
The identification of soil quality indicators is currently a universal problem, due to the importance of this resource for plant production and animal and human feeding. In general, a group of variables have been used to predict the soil health, from the status of its physical, chemical and/or biological properties.
From the biological point of view, in the evaluation of the soil and ecosystem conservation/disturbance status the edaphic macrofauna can be taken into consideration, which groups the invertebrates higher than 2 mm in diameter. Many macrofauna organisms are important in the transformation of soil properties, among them: earthworms (Annelida: Oligochaeta), termites (Insecta: Isoptera) and ants (Insecta: Hymenoptera: Formicidae), which act as engineers of the ecosystem in pore formation, water infiltration and humification and mineralization of organic matter. Another group of macroinvertebrates participates in the grinding of plant remains (e.g. Coleoptera, Diplopoda, Isopoda, Gastropoda) and others function as predators of live animals of the edaphic macrofauna and mesofauna (e.g. Araneae, Chilopoda (Cabrera, Robaina, Ponce de León, 2011a).
Macrofauna communities vary in their composition, abundance and diversity, depending on the disturbance status of the soil caused by the change of land use, which allows considering these communities as bioindicators of environmental quality or alteration (Pashanasi, 2001; Lavelle, Senapati y Barros, 2003; Ruiz, 2007; Velásquez et al., 2009; Cabrera, Robaina, Ponce de León, 2011b).
This work summarizes the biological, ecological and functional characteristics of the edaphic macrofauna and the results obtained, mainly in Cuba, about their variation in different land uses, which endorse the potential utilization of this fauna as biological indicator of the conservation/disturbance status of the soil.
Characteristics of the macrofauna for its use as biological indicator of the soil conservation/disturbance status
In literature several characteristics have been approached for the use of a certain taxonomic group as bioindicator, based on this concept. The invertebrates that integrate the soil macrofauna manifest some of these traits, which justifies their utilization as biological indicators. Among them the following can be mentioned: the advantage of their taxonomic and ecological diversification, their relatively sedentary habits, the presence throughout the year, and their possibility to be manipulated and identified (taxonomic treatment). Their short period between generations also allow a fast population response to environmental changes, and their high density and reproduction capacity allow intensive sampling, without causing unbalance in the community. Other characteristics are: their functional importance in ecosystems and an apparently foreseeable response to disturbances (Brown, 1997; McGeoch, 1998; Jones and Eggleton, 2000; McGeoch, van Rensburg and Botes, 2002). In addition, the fact that they are relatively easy to be seen, identified and manipulated under field conditions, to be evaluated by farmers, is another valid aspect in their selection as bioindicators (Zerbino, 2005).
As biological indicator of the soil conservation/disturbance status, the edaphic macrofauna should be related to its physical and chemical attributes, which in turn reflect the productivity of the ecosystem. Among this type of organisms are earthworms, which, as they have a soft body and limited motility, are affected by such factors as climate, feed, humidity, soil texture and chemical conditions; for which they show changes of composition and abundance in a short time scale (Chocobar, 2010). Earthworms tend to prevail in humid edaphic non-compacted environments, with high organic matter content.
Epigeal organisms with detritivorous function, mainly represented by diplopods (millipedes), isopods (woodlice), some coleopterans (beetles) and gastropods (snails), may also be used to indicate the disturbance status in the edaphic environment. They live and feed on the soil surface, with which they help in litter fractioning and, thus, in the processes of organic matter decomposition and mineralization. This detritivorous community, one of the most exposed on such surface, is very sensitive to sudden changes of humidity and temperature, for which they tend to disappear under these stress conditions. Such situation may be caused by the lower plant cover and entrance of residues, as well as the higher exposition to solar radiation (Zerbino, Altier, Morón and Rodríguez, 2008). Mainly humidity may influence vital functions of these organisms, such as gaseous exchange, reproduction and feeding. Epigeal arthropods with detritivorous function are more abundant and diverse in environments with a continuous and varied incorporation of litter, low temperatures and high soil moisture.
Use of macrofauna as biological indicator of the soil conservation/disturbance status worldwide
In recent years, the study of soil macroinvertebrate communities has comprised their relation to the soil physical, chemical and biological processes. Other more recent studies have approached the response of edaphic macrofauna to different land uses, in a soil gradient from natural ecosystems to agroecosystems, in order to generate indexes of edaphic health and manage some invertebrate populations, as alternatives for the advance of sustainable productive systems, which in turn preserve soil biodiversity.
In spite of the intention of these studies in the search for specific indicators, at international level until now-, the treatment of macrofauna to indicate the functioning of the edaphic environment and the ecosystem has been conducted from the characteristics of these communities. The performance of their taxonomic richness, diversity, density, biomass and functional composition has been directly used in the evaluation of different soil uses and managements (Villalobos et al., 2000; Marín, Feijoo and Peña,, 2001; Pashanasi, 2001; Tapia-Coral, 2004; Tsukamoto and Sabang, 2005; Zerbino, 2005; Ruiz, 2007; Zerbino et al., 2008; Huerta-Lwanga et al., 2008). Only Velásquez (2004) has designed an indicator of soil quality, from the relationship between abundance and macrofauna and of different soil chemical, physical and micromorphological variables.
The efficacy of earthworms as bioindicators of the soil disturbance degree, due to the intensity of land use, has been tested by different authors (Lavelle et al., 1994; González, Zou and Borges, 1996; Rodríguez, 2000; Feijoo, Zúñiga, Quintero and Lavelle,, 2007), which detected the affectation of earthworms populations in a gradient from savannas and pasturelands of humid tropics, followed by primary forests, tree plantations and fallow lands, to systems with high degree of agricultural intervention, where these populations were disfavored. Specifically, Rodríguez (2000) stated that the destruction/fragmentation of natural habitats and, as consequence, the deterioration of the organic matter content of the soil due to the loss or transformation of the original vegetation, determine the decrease of earthworm richness and abundance.
On the contrary, other groups -such as termites- acquire importance in crop zones, where their invasion and aggressiveness have been related to adverse temperature an humidity conditions, as well as to the content and quality of the organic material in the soil. Regarding this, Barros, Pashanasi, Constantino and Lavelle (2002) and Lavelle et al. (2003) have suggested the use of the earthworms/termites density index, in which the dominance of earthworms is in correspondence with preserved habitats, and the prevalence of termites as opportunistic organisms, more resistant to induced disturbances- indicates less preserved habitats or with some degradation level. Although this index defines termites as an opportunistic and fast-colonizing group, several authors state the changes suffered by their communities; primarily the humus-eating species that inhabit the soil, from habitat fragmentation, isolation and degradation (Bandeira and Vasconcelos, 2002; Bandeira, Vasconcelos, Silva and Constantino, 2003); while others mention them as the first colonizers in deforested environments, with enough remnant ligneous material, in whose decomposition they intervene (Cunha, 2006). In general, the earthworms/termites diversity index has had little application, worldwide, in macrofauna studies with such approach.
Studies on the soil macrofauna and its potential as biological indicator, in Cuba
Among the first studies about the edaphic macrofauna in Cuba, the ones conducted in the forest ecosystems of Sierra del Rosario may be mentioned (González and Herrera, 1983; López, González and Herrera, 1986; González and López, 1987; Prieto and Rodríguez, 1996), which showed results with high richness of macrofauna orders, with predominance of Hymenoptera (Formicidae), Coleoptera and Haplotaxida. Afterwards, most ecological studies approached specific groups of the macrofauna, mainly earthworms and diplopods, and the effect of natural and/or disturbed ecosystems on these communities (Martínez and Rodríguez, 1991; Rodríguez, 2000; Martínez and Sánchez, 2000; Rodríguez and Martínez, 2001; Fernández-Valle, 2001; Martínez, 2002; Prieto et al., 2003). The works showed that the diversity and abundance of these groups were substantially higher in the ecosystems with lower anthropization levels.
In the country, a group of works have also characterized the soil macrofauna in different land use systems, and have evaluated the type of use or plant formation and soil and crop management. Thus, Sánchez, Milera, Suárez and Alonso (1997); Rodríguez and Crespo (1999); Sánchez (2001); Rodríguez et al. (2002a); Rodríguez Rodríguez, Torres, Crespo and Fraga (2002b); Sánchez and Milera (2002); Sánchez, Hernández and Simón (2003); Sánchez and Reyes (2003); Sánchez and Crespo (2004); Lok (2005); Hernández and Sánchez (2006); Rodríguez et al. (2008a); Rodríguez et al. (2008b) and Sánchez et al. (2008) described the studies in pasturelands and silvopastoral systems with the association of tree legumes under different managements, of which only some are cited below.
Rodríguez et al. (2002a) compared a natural pasture system with another system of natural pasture plus 100% of leucaena (Leucaena leucocephala (Lam.) de Wit), and found higher macrofauna density and biomass in most of the years of the study, in the second system. The results confirmed the favorable influence of leucaena as tree species in the pasture, by providing better-quality litter and a more ideal micro-environment for the macrofauna activity in the soil.
Likewise, Sánchez and Reyes (2003), when studying mulberry (Morus alba L.) in monocrop and associated to different tree legumes (Gliricidia sepium (Jacq.) Kunth ex Walp. and Albizia lebbeck (L.) Benth.), observed a positive response in the colonization of soil organisms, especially with the presence of leguminous trees. In these last systems densities were obtained higher than 30 ind.m-2 for earthworms, woodlice and beetles, and higher than 100 ind.m-2 for snails, higher values than the ones reached in the mulberry monocrop.
Lok (2005), in his research about the selection of stability indicators of the soil-pasture system in pasturelands with monocrop of Guinea grass (Panicum maximum Jacq.), in silvopastoral system with leucaena, and a multiple mixture of creeping legumes (Neonotonia wightii (Arn.) Lackey, Pueraria thumbergiana (Siebold & Zucc.) Benth. and Macroptilium atropurpureum (Moc. & Sessé ex DC). Urb.), concluded that the edaphic indicators, including density and biomass of the soil macrofauna and mainly of earthworms-, had a favorable progress only in the pasturelands with silvopastoral system and with creeping legumes; while in the pastureland with Guinea grass monocrop, a trend occurred, in time, to the decrease of biological activity in the soil.
In other works conducted in seven silvopastoral systems with different soils and managements in the western region, an increase of edaphic organisms was initially observed in grayish brown soils, due to their characteristics of water retention, to which the introduction of trees also contributed (Sánchez et al., 2008).
All the commented results indicate that productive systems with tree elements show group richness and abundance of macrofauna comparable with those of natural ecosystems, such as forests, because of the higher availability of resources for the refuge and feeding of the edaphic fauna.
In pastureland ecosystems, studies have been jointly conducted about the influence of the edaphic macrofauna on dung and litter decomposition, which have shown its intervention in nutrient recycling (Soca, Simón, Sánchez and Gómez, 2002; Rodríguez et al., 2003; Sánchez, 2007; Sánchez et al., 2008). Soca et al. (2002), in a silvopastoral system and another system of pastures only, observed a fast decomposition of cattle dung in the former, as compared to the system without trees, due to the incidence of high macrofauna density especially of coleopterans. Rodríguez et al. (2003), when studying dung decomposition in a pastureland subject to rotational grazing in a paddock of Cynodon nlemfuensis Vanderyst), did not find significant differences in the macrofauna density and biomass among the different studied moments, during the decomposition process. The macrofauna taxa observed in this process were few, among them: Blattodea, Coleoptera, Hymenoptera, Dermaptera, Haplotaxida, Isopoda, Diplopodaand Chilopoda.
On the other hand, Sánchez (2007) as well as Sánchez et al. (2008), in trials of litter decomposition by the soil macrofauna in environments with Guinea grass and leucaena plus Guinea grass, determined, for the first system: three phyla, five classes, eight orders, seven genera and seven species, constituted by 77% detritivores and 11,11% herbivores and predators; and for the second system they found: three phyla, five classes, nine orders, seven genera and seven species of the macrofauna, formed by 56% detritivorous organisms, 35% herbivores and 9% predators, which showed similar results in both pasturelands regarding the organisms. Nevertheless, differences were established in decomposition rate, which was more intense in the silvopastoral system of leucaena plus Guinea grass, to benefit leucaena through the fixed nitrogen, litter contribution and quality, and the more favorable edaphoclimatic conditions for the action of decomposing organisms.
The most recent studies conducted in the country also included the characterization of the soil macrofauna in agricultural-livestock production systems, located in the current Artemisa province, which are managed through agroecological methods (Cabrera, Martínez and Rodríguez, 2007). The characteristics of the invertebrate communities established in each area, such as the highest values of taxonomic richness, density and biomass in the polycrop and forage areas with regards to the pastureland (fig. 1), and also the highest indexes of diversity and equity obtained for most fauna groups in the polycrop (table 1), were elements that support the beneficial effect of the agroecological management applied in these systems, which consisted in crop rotation, incorporation of organic manures and planting of perennial plants.
Later, Serrano (2010) related the composition and structure of the edaphic macroinvertebrate community with the plant formations forest and seagrape stand, on the northern coast of the current Mayabeque province. The study reflected that the macrofauna variations regarding composition and abundance, at the taxonomic level of order, were not determined for the plant formation; although the high quantitative similarity between these communities indicated the similar level of disturbance in the studied sites.
Recently, Cabrera et al. (2011a, 2011b) extended their research to four land uses in the Red Plain of Artemisa and Mayabeque, and their effect on the richness, abundance and functional composition of the soil macrofauna. These authors obtained that the use secondary forests was better represented in the macrofauna taxonomic richness, density and biomass, with regards to the other uses: pasturelands, varied crops and sugarcane plantations. In addition, in secondary forests they found higher representation in density and biomass of the detritivore functional group, and also in the biomass of soil engineers due to the influence of earthworms. This last group of soil engineers prevailed regarding density in pasturelands, varied crops and sugarcane plantations, whose values were caused by the high abundance of ants in these systems with higher anthropization level (fig. 2). The results indicated the disturbance level of the edaphic medium, due to the intensity of land use.
CONCLUSIONS
The results obtained in the evaluation of the edaphic macrofauna, in ecosystems with different conservation/disturbance degree in Cuba, allow proposing as indicator of the evaluation of the soil status the performance of earthworm populations, through their species richness, their density (ind.m-2) and biomass (gm-2); as well as the proportion shown by the epigeal community with detritivorous function, in density as well as in biomass, with regards to the other functional groups of the macrofauna.
They also allow identifying ants as indicators of disturbance in the edaphic medium, due to their ability to survive mainly on agricultural soils, in spite of the disturbances of such environment, which was shown by their prevalence in abundance and resistance in systems which had some level of anthropic intervention.
It is valid to mention that efforts have been made to define limit values, intervals and universal variation percentages referred only to biological indicators which represent the optimum conditions of a soil, but it has turned out to be difficult due to the large space-time variability of these indicators.
These results that have been obtained in the country until nowadays are not enough, for which the future studies should consider a lower taxonomic level in the identification of macrofauna, and relate its taxonomic and functional composition to climate and pedological factors; all this in order to identify indexes, or specifically taxa of the macrofauna, as indicators of the soil health and functionality status, and that such indexes may be generalized and applied in a wide range of soil types and land uses.
