RESEARCH WORK
Richness and abundance of soil macrofauna in four land uses of the Artemisa and Mayabeque provinces, Cuba
Grisel Cabrera1, Nayla Robaina2 y D. Ponce de León3
1Instituto de Ecología y Sistemática, CITMA, Carretera de Varona km 3½, Capdevila,
Boyeros, C.P. 10800 Ciudad de La Habana, Cuba
E-mail: grisel17@ecologia.cu
2 Estación Experimental de Plantas Medicinales, Güira de Melena, Artemisa, Cuba
3 Facultad de Agronomía, Universidad Agraria de La Habana, Mayabeque, Cuba
ABSTRACT
The study assessed the effect of the intensity of different land uses (secondary forests, pasturelands, fields with varied crop cultivation dedicated to potato production and sugarcane plantations) on the richness and abundance of soil macrofauna communities. The research was conducted in October, at the end of the rainy season, 2009, in the Artemisa and Mayabeque provinces where the different land use systems are located. The soil macrofauna was collected using the methodology proposed by the TSBF program. The taxonomic richness, density and biomass of soil macrofauna were evaluated and the data processing included nonparametric tests. The highest values of richness, density and biomass were obtained in the secondary forests and the lowest values in the pasturelands, varied crop cultivation and sugarcane plantations. Haplotaxida, Formicidae, Isoptera, Coleoptera and Diplopoda were the prevailing taxonomic units of the macrofauna regarding density and biomass in most of the land uses. The results about taxonomic richness, density and biomass of the edaphic macrofauna indicated the degree of soil degradation due to land use intensity.
Key words: Multiple land use, soil fauna.
INTRODUCTION
Edaphic macro-invertebrates (higher than 2 mm diameter) act as determining agents in soil fertility and, thus, in the global functioning of the edaphic system. This fauna can be affected by different land uses and managements. Due to its susceptibility and fast response to cover changes, vegetation transformation, the performance before different environmental variables and the ecological activity they perform, many authors propose their use as indicators of environmental quality or alteration (Lavelle et al., 2003).
In Cuba there are few studies about the edaphic macrofauna which involve all the groups that compose it. Among the first studies in the country the ones conducted on litter macrofauna in forest ecosystems, especially of Sierra del Rosario, can be mentioned (González and López, 1987; Prieto and Rodríguez, 1996). Afterwards, most ecological studies have approached specific groups of the macrofauna, mainly earthworms and millipedes in natural and/or disturbed ecosystems, and the effect such disturbances cause on these communities (Rodríguez, 2000; Prieto et al., 2003).
Other works in the country have characterized the soil macrofauna in different land use systems, with the objective of evaluating, from the characteristics of these edaphic communities, the type of use or plant formation, and the soil and crop management (Rodríguez et al., 2002; Sánchez and Reyes, 2003; Cabrera-Dávila et al., 2007; Serrano, 2010). Nevertheless, the need to further the studies in such sense is acknowledged.
In this work the effect of land use intensity on the richness and abundance of soil macrofauna communities was evaluated, in a gradient from secondary forests and pasturelands to varied crop fields destined to potato production and sugarcane plantations, located in the Artemisa and Mayabeque provinces.
MATERIALS AND METHODS
The research was conducted in October, in the rainy season, 2009, in 11 reference systems along the Red Plain of the old Havana province, currently located between the Artemisa and Mayabeque provinces. Four land uses were studied: secondary forests, pasturelands, varied crop fields destined to potato production and sugarcane plantations. The soil type in all uses was Ferralitic Red, according to the classification made by Hernández et al. (1999).
Description of the land use systems
Secondary forests. Three forest areas were studied in Managua (22º56'44.80" N, 82º16'11.07" W), Nazareno (22º58'05.40" N, 82º14'02.72" W) and Aguacate (22º59'17.90" N, 81º50'01.03" W), located in the Mayabeque province. They are forest systems of natural regeneration or with different anthropization levels, with ages from 40 to 120 years and extensions between two and five hectares. They show floristic elements of semideciduous vegetation, as well as fruit and timber tree species, with herbaceous and shrubby strata, which provide different cover degrees for the soil. Among the tree species, the following stand out: Pouteria sapota H. E. Moore & Stearn, Mangifera indica L., Crysophyllum cainito L., Delonix regia (Boj. Ex Hooker) Raf., Roystonea regia (Kunth) O. F. Cook, Cordia gerascanthus L., Calophyllum inophyllum L., Guarea guidonia (L.) Sleumer, Tectona grandis L. fil., Swietenia mahagoni (L.) Jacq., Cedrela odorata L., Pinus sp. and Talipariti elatum (L.) Fryxell.
Pasturelands. Two pastureland systems were selected in the San José de las Lajas municipality, with a maximum extension of 12 ha, located at the following coordinates (pastureland 1: 23º00'01.50" N and 82º09'49.10" W; pastureland 2: 22º53'52.10" N and 82º02'08.12" W). They are naturalized pastures with more than 25 years of exploitation. The main pasture species were: Guinea grass (Panicum maximum Jacq.) and star grass (Cynodon nlemfuensis Vanderyst), which showed cover between 80 and 90%. In this pasturelands Holstein and Siboney cattle grazed, and the management was mainly intensive rational rotational, with a mean stocking rate of 2,8 animals ha-1.
Varied crops. Three systems were selected located in the Güira de Melena (22º45'40.50" N and 82º29'21.71" W), Batabanó (22º46'42.40" N and 82º15'08.27" W) and Güines (22º47'43.60" N and 82º02'31.46" W) municipalities, belonging to Artemisa and Mayabeque. The main crop was potato (Solanum tuberosum L.), in constant rotation with sweet potato (Ipomoea batatas (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 weeds in the areas, the following stood out: Sorghum halepense (L). Pers., Cyperus rotundus L., Amaranthus hybridus L. and Bidens pilosa L.. These areas had been dedicated to agriculture for more than 10 years, mainly with traditional tillage and electrical spray irrigation. The application of NPK in these systems was 1 490 kg ha-1 year-1 and urea application fluctuated between 224 and 298 kg ha-1 year-1.
Sugarcane plantations. The three areas under exploitation with sugarcane (Saccharum officinarum L.) were located in Artemisa and Mayabeque, in the municipalities Güira de Melena (22º50'24.80" N and 82º26'50.56" W), San Nicolás de Bari (22º46'32.60" N and 81º55'05.90" W) and Madruga (22º58'47.00" N and 81º50'49.24" W). The areas were occupied by varieties CP 52-43 and C 86-12, C 323-68 and C 86-56, respectively. The main weeds in the systems were: S. halepense, C. rotundus, Rottoboellia conchinchinesis L.F. and Eleusine indica (L.) Gaerth. Gravity irrigation systems and electrical coiler system were used; 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 macrofauna collection was conducted according to the Methodology of the International Program «Tropical Soil Biology and Fertility» or TSBF (Anderson and Ingram, 1993; Lavelle et al., 2003). By land use area or replication eight soil monoliths were taken (25 x 25 x 30 cm), at a distance of 20 m in a completely randomized design, for a total of 24 processed monoliths in each of the uses: secondary forests, varied crops and sugarcane plantations, and 16 monoliths in pasturelands. The macrofauna was manually collected in situ, and it was preserved mainly in 75% alcohol.
The macrofauna was separated to the taxonomic level of order and family (Borror et al., 1976; Sims, 1980; Brusca and Brusca, 2003). An approach was made to the taxonomic richness of these communities in each land use, estimated from the number of families that could be identified. The macrofauna orders with lower representation in this study, such as Blattodea, Diptera, Hemiptera, Orthoptera and Lepidoptera, and also Araneae, were not included in the analysis of taxonomic richness.
The average values of density (ind.m-2) and biomass (gm-2) for the edaphic communities and for the different taxonomic units of the macrofauna, were calculated in each land use. Density was determined from the numbers of individuals and biomass value was found based on humid weight in the preserving solution.
In order to determine the density and biomass variations of the soil macrofauna communities among uses, the non parametric Kruskal-Wallis analysis was used, and as a posteriori test for mean comparison, the Mann-Whitney U with Bonferroni adjustment was used. The statistical processing was made through the program PAST-1.75, 2001.
RESULTS
Taxonomic composition and richness
The soil macrofauna communities in the four studied land uses in the Artemisa and Mayabeque provinces comprise three phyla, 22 orders and 39 determined families (table 1).
The analysis at order level showed 19 orders in secondary forests, 14 in pasturelands and sugarcane plantations, and only 12 orders in varied crops. The taxonomic richness appraised at the level of identified families, also showed a higher number in secondary forests (33), followed by pasturelands (18) and very closely varied crops (16) and sugarcane plantations (15). The best represented orders regarding number of families in secondary forests were Archaeogastropoda and Coleoptera with eight and seven families, respectively. In the other uses the order with higher number of families was Coleoptera, with its maximum representation in varied crops (10 families) which had some incidence as agricultural pest. In pasturelands, this order had four families and in sugarcane plantations, six; and the other orders of the macrofauna in all uses only showed between one and three families. Likewise, 14 families exclusive from secondary forests, two from pasturelands, five from varied crops and three from sugarcane plantations were obtained (fig. 1).
Density and biomass
The average density and biomass of the total soil macrofauna in secondary forests were 1 166,60 ind.m-2 and 67,45 gm-2, respectively, considerably higher values than the ones obtained in pasturelands (581 ind.m-2 and 7,71 gm-2), in varied crops (294 ind.m-2 and 8,79 gm-2) and in sugarcane plantations (280 ind.m-2 and 7,85 gm-2). The Kruskal-Wallis test proved this remarkable variation, because it showed highly significant differences among uses in density (p<0,001) and biomass (p<0,001) (figs. 2 A and B).
According to the dominance in density and biomass of the different taxonomic groups of the macrofauna (fig. 3 A and B), it was observed that in secondary forests the most important taxa in density included Diplopoda, Isopoda and Isoptera, and the highest components in biomass were Haplotaxida and Diplopoda. In pasturelands, Hymenoptera (Formicidae), Isoptera and Coleoptera can be mentioned with high and close values regarding density; while in biomass essentially Coleoptera prevailed. In varied crops Hymenoptera (Formicidae) stood out regarding density, and Haplotaxida and Coleoptera were the main representatives in biomass. In sugarcane plantations Hymenoptera (Formicidae), Coleoptera and Diplopoda prevailed in density and only Diplopoda stood out in biomass.
DISCUSSION
Taxonomic composition and richness
The quantity of exclusive families found in each use allowed inferring that all land uses shared a high number of families. The studied systems have certain degree of intervention or alteration by men (secondary or intervened forests, pasturelands with livestock production management and crops with intense tillage), where families with similar characteristics of tolerance to a varied range of edaphoclimatic conditions and, thus, adaptable and resistant to induced disturbances, can equally colonize.
The highest value of family richness as well as exclusivity reached in secondary forests, proved the importance of floristic variability and resource heterogeneity in the supply of necessary feed and refuge sources to preserve the diversity of edaphic communities (Fragoso and Lavelle, 1992). This was also related to the cover present in these forests, which provides a considerable contribution of litter and shade to maintain stable the values of soil temperature and moisture, all of which favored the development of more diverse communities. In this sense, Granados and Barrera (2007) found higher number of species, genera and families in forest relicts as compared to the areas without tree covering and, in general, concluded that the areas with higher plant diversity and richness and a higher percentage of cover can show a higher diversity of soil macrofauna.
In Cuba, González and López (1987) recognized in forestry ecosystems a high number of outstanding taxa of macrofauna, among them Hymenoptera (Formicidae), Coleoptera and Haplotaxida. More recently, in a forest relict with characteristics of original semideciduous vegetation in the northern coast of Havana, Serrano (2010) found a total of 21 taxonomic units and the prevailing orders were Hymenoptera, Araneae and Isopoda. This value is close to the richness referred in this study for forest systems (19 orders and 33 families), in spite of being secondary.
Rodríguez et al. (2002) and Sánchez and Reyes (2003) obtained in the country, in pasturelands with different livestock management, up to nine orders of edaphic macrofauna. On the other hand, Cabrera-Dávila et al. (2007) found in polycrop areas, in pasturelands associated to tree legume cover and in grass monocrop, higher richness values of orders (14 in the first two systems and 12 in the last) and families (30, 26 and 22, respectively), with a predominance of Formicidae, Haplotaxida, Diplopoda and Isopoda.
Also, worldwide, in several works results were found close to the ones reached in this
study, although in most of them the collection area was higher (higher amount of monoliths
per land use systems). Pashanasi (2001) collected in different land use systems of the
Peruvian Amazonia, between 20 and 30 taxonomic units of macrofauna in secondary forests with
20 and five years of natural regeneration; in pasturelands between 18 and 23 taxa and
in
annual crops between 15 and 25 taxonomic units. In Brazilian ecosystems there was
a gradual increase of macrofauna diversity before the changes in land use intensity,
where forests, agroforestry systems and pasturelands were examined, to annual crop
systems (Barros et al., 2002). Other authors in Peru recorded a higher quantity of taxonomic
groups in primary and secondary forests (13), as compared to crop systems (12) (Villavicencio
et al., 2009).
Density and biomass
The density and biomass results showed the sensitivity of the macrofauna communities to soil management, changes in cover and vegetation transformation, as well as the negative effect of the disturbances imposed by crop systems.
Many elements can be mentioned as causative of the reduced density and biomass values in pasturelands, varied crops and sugarcane plantations, as compared to the ones obtained in secondary forests (figs. 2 A and B). Several authors have mentioned and proven that one of the main factors is the loss of organic matter in the soil (Velásquez et al., 2009), due to accelerated hydric erosion because of the decrease of plant cover, as one of the possible reasons that explain this event.
Density and biomass have also been related to the level of macronutrients, pH, soil texture, water retention capacity and high litter quality (Barros et al., 2002). Lok (2005) stated that the macrofauna organisms prefer plant remains with a relatively low C/N ratio as they are more easily accessed and decomposed, which explains their high selectiveness towards the existing vegetation on the soil. Plants and organic wastes provide habitats and feed for the edaphic fauna, and the adequate organic matter content not only favors the physical-chemical properties, but also provides an energy source that stimulates the activity of soil invertebrates.
Another aspect that should be highlighted is vegetation structure, mainly the presence of different strata. The tree and/or shrubby cover in the arrangement of ecosystems are extremely important, because they guarantee the continuous and abundant input of plant organic material and a more favorable microenvironment for the establishment of soil macroinvertebrates (Rodríguez et al., 2002).
There are few studies in Cuba about macrofauna in forest systems, with a moderate conservation level. The macrofauna density and biomass values in secondary forests are comparable to the ones obtained in the country, in different agroforestry systems with silvopastoral management and influence of tree legumes. Cabrera-Dávila et al. (2004) obtained in this type of system a higher density in the rainy season (2 346 ind-m-2) and a biomass of 66,90 gm-2; other Cuban researchers found lower estimates (Lok, 2005; Sánchez, 2007). In recent studies, in a seminatural forest of the northern coast of
Havana, Serrano (2010) found a macrofauna density lower than the one in this study (835 ind.m-2). Regarding other recent collections made in the evergreen primary forests of Sierra del Rosario in Artemisa (Cabrera-Dávila, G. and Hernández, A. unpublished), lower values were also found (706 ind.m-2 of density and 42,50 gm-2 of biomass) than the ones observed in the studied secondary forest ecosystems (1 166,60 ind.m-2 and 67,45 gm-2). It should be taken into account that this type of ecosystem can shelter part of the fauna from the original vegetation and in addition be colonized in higher proportion by opportunistic and invasive species, belonging to lands with some disturbance level.
The studies in secondary forests and forestry plantations of the humid tropics reported similar estimates as the ones in this work. Pashanasi (2001), in some secondary forests of Peru (20 and five years of natural regeneration), recorded a density between 485 and 838 ind.m-2 and biomass between 33,9 and 102,0 gm-2. In Brazil Barros et al. (2002) in forests and agroforestry systems found between 884 and 1 761 ind.m-2, and in biomass they obtained low values (between 10,18 and 9,46 gm-2, respectively). Tsukamoto and Sabang (2005), in tree plantations of Malaysia, calculated a density of more than 1 000 ind.m-2 and 60 gm-2 of macroinvertebrate biomass.
The use pasturelands was second in density, but in biomass it had the lowest values (figs. 2 A and B), and likewise both variables were lower than those of other previously-studied Cuban pasturelands. In Guinea grass pasturelands, Rodríguez et al. (2002) obtained a biomass of 34,61 ind.m-2; while Sánchez, (2007) reported in this type of pastureland a density of only 88,87 ind.m-2 and a biomass of 6,51 gm-2.
The grazing regime and, thus, animal trampling, could have affected the macrofauna density and biomass in the pastureland. Lok (2005) expressed that soil compaction in pasturelands due to a certain stocking rate can reduce the population of edaphic invertebrates.
In other pasturelands throughout the world, the macrofauna density and biomass were also higher than the ones obtained in the pasturelands of this study. In pasturelands from Mexico, Peru, Brazil and Uruguay, the density was higher than 600 ind.m-2, and the biomass was higher than 35gm-2 (Brown et al., 2001; Barros et al., 2002; Huerta-Lwanga et al., 2008); especially the biomass in this type of ecosystems has been influenced by the contribution, in weight, of earthworms.
In agroecosystems, the soil macrofauna communities are generally very low due to the alterations caused by disturbance, in correspondence with the above-stated facts. This research followed that pattern, in varied crops as well as in sugarcane plantations (figs. 2 A and B). The slightly higher biomass values in such uses as compared to pasturelands can be justified through the predominance of certain detritivorous groups in sugarcane plantations and earthworms in varied crops (figs. 3 A and B). In Cuba there are scarce results about the response of macrofauna to the evaluation of different agricultural procedures in crop systems. Only Cabrera-Dávila et al. (2004), in polycrop areas of the country with application of agroecological methods (organic fertilization, crop rotation and association of short-cycle crops to long-cycle ones), found a density of 2 016 ind.m-2 and a biomass of 63 gm-2, similar to the ones that can be appreciated in well-preserved ecosystems; these results are opposed to the ones found in the cultivated areas of this study, which had very aggressive practices such as chemical fertilization, mechanical tillage and introduction of machinery.
Worldwide some authors refer, for annual crops, low to moderate values in density (362-851 ind.m-2) as well as in biomass (5,10-32,40 gm-2) (Pashanasi, 2001; Barros et al., 2002), which are higher than the ones shown for the studied areas. In other tropical agroecosystems lower biomass (< 20gm-2) and density (< 250 ind.m-2) were also observed as compared to natural systems (Villalobos et al., 2000; Brown et al., 2001; Huerta-Lwanga et al., 2008).
The analysis of the dominance of certain macrofauna groups showed that the order Haplotaxida did not play a prevailing role in pasturelands, as has been commonly observed for other natural or induced pasturelands of the world, due to the influence of earthworms of wide distribution and large size (Feijoo et al., 2007). In general, earthworms prevail in biomass in most ecosystems, but according to Lavelle et al. (1994), they have higher contribution in the pasturelands of humid regions and decrease in forestry areas and dry zones.
Other groups, such as Isoptera, acquire importance especially in crop zones, and their invasion and aggressiveness in these sites are related to the poor quantity and quality of organic material, the increase of temperature and the reduced moisture in the soil (Barros et al., 2002). However, diverse authors comment about the affectation of termite communities, primarily of the humivore species which inhabit the soil, related to habitat degradation (Bandeira et al., 2003). In fact, in this work, termites (mainly represented by a humivore species) were found only in the secondary forests and pasturelands, and not in those of higher affectation as a consequence of agricultural practices. Da Cunha (2006) stated that these organisms are the first colonizers in deforested environments with enough remnant ligneous material, and help in its decomposition.
CONCLUSIONS
Secondary forests showed high values of taxonomic richness, density and biomass of the edaphic macrofauna, in correspondence with a higher stability and a lower intervention degree, having neither continuous tillage nor grazing, with regards to the other uses. Pasturelands, varied crops and sugarcane plantations had lower values, which showed a moderate to higher level of anthropization, due to livestock management in the pasturelands and constant tillage in the crop systems. The results of taxonomic richness, density and biomass of the soil macrofauna indicated the disturbance level of the edaphic environment due to land use intensity.
ACKNOWLEDGEMENTS
The results were obtained within the framework of the Master Program of Soil Sciences of the Agricultural University of Havana, and they were funded by the research project 08-22 «Causes of the structure degradation of Ferralitic Red soils in the Red Plain of Havana» of the Science and Technology Program Cuban Environmental Protection and Sustainable Development. We also thank different Cuban specialists for the taxonomic classification of the edaphic macrofauna, mainly at the family level (L. F. de Armas, Ph.D.; A. Lozada, M.Sc.; T. Tcherva, B.Sc.; M. Hernández, B.Sc.; A. Alegre, B.Sc. and R. Barba, B.Sc).
