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The oligochaetofauna of the Nipe soils in the Maricao State Forest, Puerto Rico
Pedobiologia 47, 475–478, 2003 © Urban & Fischer Verlag http://www.urbanfischer.de/journals/pedo
The 7th international symposium on earthworm ecology · Cardiff · Wales · 2002
The oligochaetofauna of the Nipe soils in the Maricao State Forest, Puerto Rico Hendriekje Hubers, Sonia Borges* and Mónica Alfaro Department of Biology, University of Puerto Rico, Box 9012, Mayagüez, Puerto Rico 00681 Submitted September 6, 2002 · Accepted July 15, 2003
Summary The oligochaetofauna of the Nipe soils of Puerto Rico was studied for the first time. Earthworm and soil samples were taken over a year at six different sites. Earthworms were hand sorted from four successive soil layers, 10 cm in depth. Only three species were found: Onychochaeta borincana, Pontoscolex corethrurus, and Neotrigaster rufa. Abundance was low. It seems that the physicochemical conditions that characterize Nipe soils provide an inhospitable environment for these organisms. Key words: Neotropic, Serpentine soils, Caribbean, Nipe soils, soil fauna
Introduction Like all oxisols, the Nipe series are highly meteorized soils (Beinroth 1982) in which elimination of primary minerals has occurred (Lugo-López et al. 1973). They are very acid, have low fertility (Silander et al. 1986), and have more than 60 % clay although they behave as sandy or silty soils (Roberts 1942; Sánchez 1981). Their distinctive red color is due to their characteristic high iron oxide content. Nipe soils derive from serpentine rock. Although serpentine is found throughout the world, Nipe soils have only been identified from Cuba (DNSF-INRA 1975) and Puerto Rico (Roberts 1942). In Puerto Rico these soils are exclusively found in three areas of the western part of the island: the Maricao (236.7 ha) and Susúa (9.4 ha) State Forests and the extensively populated sectors of Cerro Las Mesas in Mayagüez and Plan Bonito in Cabo Rojo (SCS 1967a).
Studies on the flora of serpentine derived soils indicate that the vegetation of these soils is very particular, including many endemic species. Studies on the flora specific to the Nipe soils are scarce but it has been reported that plants growing on these soils present xeromorphic characteristics (Silander et al. 1986). The fauna of these soils has not been studied but it is possible that it is also determined by their mineralogical properties. Since soil physicochemical characteristics determine, to a great degree, the distribution and density of terrestrial oligochaetes, these annelids are an excellent group to estimate the extent to which fauna reflects soil conditions. The Nipe soils from the Maricao State Forest (MSF) were chosen for this study because they are the most extensive and least altered by human activity of all.
*E-mail corresponding author: [email protected]
0031-4056/03/47/05–06–475 $15.00/0
476
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Materials and Methods
Results
The study area at the MSF is located between Km 15.7 and 15.8 of Road 120. Sampling was performed from May’90 to April’91. Six collection sites were chosen: 3 at 150 m north and 3 at 150 m south of this road. Each sample was taken from two 0.25 × 0.25 m quadrats. Earthworms were hand sorted from 4 successive 10 cm soil layers and were preserved in 10 % formalin. They were weighed with their gut contents after a month of preservation. The following soil analyses were carried out for each quadrat and each 10cm soil layer: moisture (Brady 1974), organic matter (OM) (Bouyucos 1936), pH (Peech 1965), resistance to penetration (250 kgf/cm soil resistance ring meter). Soil moisture content was determined monthly, pH every 3 months, and resistance to penetration (RP) once. Precipitation and temperature were obtained from the National Oceanographic and Atmospheric Administration monthly reports. A three-way factorial ANOVA was used to analyze data. Principal Component Analysis (PCA) was used to explain horizontal distribution of P. corethrurus, the most abundant species, in relation to soil properties.
The physical and chemical properties of these soils and earthworm numbers appear in Table 1. OM did not differ significantly (P > 0.1474) between sites but according to depth (P < 0.0001). pH did not vary (P > 0.70) between months but it did (P < 0.0001) between sites. There were significant differences in pH according to depth in May (P < 0.0001), August (P < 0.0004), and November (P < 0.0001). There was no significant difference (P < 0.05) in RP between sites but there were differences (P < 0.0066) according to soil depth and in the interaction between site and depth (P < 0.0498). Soil texture varied between sites (P < 0.0048) and between depths for silt (P < 0.0137) and sand (P < 0.0331). There was a difference (P < 0.0001) in monthly soil moisture between sites but not between depths. Soil moisture corresponded with monthly precipitation except for May–June and Jan.–Feb. Three worm species were collected in the soils: Pontoscolex corethrurus (Müller, 1856), Onychochaeta borincana Borges 1994, and Neotrigaster rufa (Gates, 1962). P. corethrurus represented 98 % of the earthworm community with a monthly mean of 68 ind.m-2 and a biomass of 16.4 gm-2. O. borincana’s
Table 1. Soil characteristics and the number of individuals per species found at each sampling site Sample
pH
OM %
RP
Sand %
Silt %
Clay %
Moisture %
Pc
Ob
Nr
1a 1b 1c 1d 2a 2b 2c 2d 3a 3b 3c 3d 4a 4b 4c 4d 5a 5b 5c 5d 6a 6b 6c 6d
5.04 5.10 5.15 4.52 4.82 4.98 4.95 5.03 4.98 4.91 4.96 5.11 4.88 4.93 4.72 4.97 4.78 4.65 4.70 4.81 4.48 4.57 4.69 4.74
7.29 5.40 3.94 3.52 7.81 7.28 5.77 4.14 6.89 5.67 4.19 3.80 9.11 6.55 4.94 3.96 8.66 6.37 4.59 3.73 8.87 5.95 4.60 4.43
0.97 0.69 0.63 0.72 0.60 0.79 0.78 0.81 0.53 0.53 0.53 0.88 0.56 0.72 0.53 0.94 0.63 0.69 0.82 0.81 0.79 0.79 0.82 0.88
43.00 34.50 42.00 39.50 44.00 45.00 45.50 51.00 53.50 57.00 57.00 58.00 54.50 50.50 54.00 62.50 56.50 67.00 48.00 56.00 64.50 74.00 6.10 49.50
32.00 25.00 21.50 19.00 27.00 26.50 29.00 21.10 28.00 26.00 21.00 17.50 23.50 22.00 17.50 15.00 21.50 15.50 22.00 17.50 19.00 15.50 18.00 19.50
25.00 35.50 36.50 41.50 29.00 28.50 25.50 28.00 18.50 17.00 22.00 22.50 22.00 27.50 28.50 22.50 22.00 17.50 30.00 26.50 16.50 12.00 21.00 31.00
28.55 27.75 28.42 28.92 27.46 27.46 29.00 30.25 22.54 21.58 22.17 24.21 24.46 21.46 23.29 26.38 18.83 15.71 16.00 18.50 18.04 15.30 16.63 21.46
23 26 11 2 29 17 6 1 71 35 18 11 1 1 1 0 137 78 20 8 57 33 10 8
2 1 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 2 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0
OM = organic matter, RP = resistance to penetration (kg force cm-2), Pc = Pontoscolex corethrurus, Ob = Onychochaeta borincana, Nr = Neotrigaster rufa Pedobiologia (2003) 47, 475–478
The oligochaetofauna of the Nipe soils
monthly mean was 0.58 ind.m-2 and 0.337 gm-2 while N. rufa had a monthly mean of 0.67 ind.m-2 and 0.327 gm-2. PCA showed that three components explain 83 % of the variance of soil properties. Component 1 (40 %) allowed separation of pH, OM, sand and silt from RP, clay and soil moisture. Component 2 (70 %) separated pH, OM, silt and moisture from RP, sand and clay. Component 3 does not allow a clear separation between soil properties.
Discussion The low species diversity of earthworms found in Nipe soils contrasts with the great heterogeneity of the flora reported for serpentine derived soils. Worm diversity of these soils is relatively low when compared with the 15 species reported from Chiapas, Mexico (Fragoso & Lavelle 1987) and even with the 8 found in Río Negro, Venezuela in spite of its limited food resources (Németh & Herrera 1982). If we ignore the results obtained in studies from continental forests and consider those from other sites on the island of Puerto Rico, we still find that the species diversity and abundance in Nipe soils are lower than those reported from Baño de Oro (Borges & Alfaro 1997) and from abandoned pastures in Cayey (Sánchez-de León et al. 2003). However, the Nipe results are similar to those found for the Cartagena Lagoon Reserve, an area that has been extensively perturbed for more than 70 years (Alfaro & Borges 1996). Apparently, the high salinity and sand content of the deeper soil layers and the accumulation of organic matter may be related to the low earthworm abundance in Cartagena. The soil texture results obtained in this study reflect the behavior of these soils rather than the proportion of the different soil particles. Roberts (1942) indicates that Nipe soils are 60–80 % clay while we found 10–48 %. This difference may be due to the presence of Fe and Al amorphic oxides that tend to unite clay particles in agglomerates that disperse as sand or silt (Sánchez 1981). These agglomerations explain, to a certain extent, the absence of a consistent pattern in soil texture between sampling sites. Apparently the dispersion method used did not eliminate all agglomerates. The mineralogical properties of these soils explain why they drain well and have low water availability, attributes not expected in clay soils. RP observed in Nipe soils does not seem to be an obstacle for worm movement because it was lower than the amount preventing seed emergence (Parker & Taylor 1965). Even though the soil is acidic, it is still within the tolerance range of oligochaetes. It appears that P.
477
corethrurus prefers soils with a small range of pH, in this case between 4.5 and 5.0. pH was one of the components that explained most of the variance of soil properties. Available nitrogen (N) may limit earthworm distribution and abundance (Lee 1985). N content in Nipe soils is only 0.22 % in the first 12 cm and diminishes to less that 0.03 % at deeper levels (Roberts 1942). An average 0.390 % of N in the first 28 cm of these soils has also been reported (SCS 1967b). This N content is probably not a limiting factor per se because similar values have been indicated for ferralitic and alluvial soils in Chiapas (Fragoso & Lavelle 1987). As expected, worm density was higher in the top layers where OM was higher as well. Even though OM was not the only component explaining 70 % of the variance of soil properties, P. corethrurus was more abundant when the OM values were above 6.5 %. According to Fox (1982), Nipe soils are extremely infertile, particularly in the deeper horizons. Soil infertility is not only due to low OM, but also to a combination of factors such as nutrient deficiency of Ca or Mg or an excess of Mn, Fe or Al (Sánchez 1981). Nipe soils at the MSF have high Mg concentrations (18.93–49.66 cmol/kg-1) and normal agricultural Ca concentrations (0.43–8.7 cmol/kg) (Caminero 1991). The Mg:Ca proportion of these soils varies according to authors: 44.02–5.70 as stated by Caminero (1991) or 0.03 according to Fox (1982). In ferralitic soils (soils with high Fe concentration over calciferous rock) in Mexico the Mg:Ca was 0.44 in the first 10 cm and 0.73 in the 10–20 cm layer (Fragoso & Lavelle 1987). Our values are higher than those reported by Fox (1982) but much lower than Caminero’s (1991). The Mexican soils had higher diversity (7 vs. 3 species) and mean density (121 ind.m-2 vs. 74 ind.m-2) of worms than the Nipe soils. At the MSF the highest monthly worm density was typically found in the first 10 cm of soils, except during February and March when worms were more abundant in the 10–20 cm layers. This coincides with the prolonged reduction of soil moisture for those months. Other minerals present in Nipe soils are found in concentrations high enough to be toxic for the edaphic fauna. For example, exchangeable Fe is near 13 % down to 45 cm and increases with depth, while Al concentration is 7.9 cmol/Kg to 28 cm and decreases with soil depth (SCS 1967b). When soil moisture increases, the concentration of these minerals in the soil solution increases as well (Sánchez 1981). These temporal increments may provide an unfavorable medium for earthworms. Although soil moisture is one of the components which explain most of the variance of soil properties, no positive correlation was found between soil moisture and population abundance. The highest soil moisture of these soils corresponds with the lower Pedobiologia (2003) 47, 475–478
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tolerance limit for many worm species, including P. corethrurus (Edwards & Lofty 1976; Lavelle et al. 1987). It is possible, then, that the increment of Mg and Fe in soil solutions affects the earthworms. The severe physicochemical properties that characterize these soils may explain the low earthworm diversity found in this zone. P. corethrurus and O. borincana are geophagous species that have been reported from a variety of habitats, especially in disturbed areas. P. corethrurus, the most abundant species in Nipe soils, was probably introduced to the MSF with the reintroduction of endemic plants in a reforestation project. Fragoso & Lavelle (1987) have found P. corethrurus in soils with an OM content lower that that reported from Nipe soils. Barois and Lavelle (1986) have suggested that it has a mutualistic relationship with microorganisms, which aid in its digestion. This may also be true for O. borincana, a fairly common species on the island. Yet, only 5 specimens (0.58 ind.m-2) were collected at the MSF, an extremely low number considering that in Cartagena, a very limiting habitat for earthworms, its density was 101.3 ind.m-2. It is interesting to note that P. corethrurus was also present in Cartagena, but at lower densities that in the MSF (13.2 vs. 68 ind.m-2). N. rufa, on the other hand, is epigeic, an advantage in oligotrophic soils. However, only 6 specimens (0.67 ind.m-2) of this species were found in the MSF, corroborating Gates’ (1962) indication that none of the members of this genus seems to be common and that they could be limited to remote and inaccessible regions. Acknowledgements. Some soil analyses were performed at the USDA International Institute of Tropical Forestry at Río Piedras, Puerto Rico.
References Alfaro, M., Borges, S. (1996) Ecological aspects of earthworms from Laguna Cartagena, Puerto Rico. Caribbean Journal of Science 32, 406–412. Barois, I., Lavelle, P. (1986) Changes in respiration rate and some physicochemical properties of a tropical soil during the transit through Pontoscolex corethrurus. (Glossoscolecidae, Oligochaeta). Soil Biology and Biochemistry 18, 539–541. Beinroth, F. H. (1982) Some highly weathered soils of Puerto Rico, 1. Morphology, formation and classification. Geoderma 27, 1–73. Borges, S., Alfaro, M. (1997) The earthworms of Baño de Oro, Luquillo Experimental Forest, Puerto Rico. Soil Biology and Biochemistry 29, 231–234. Bouyoucos, G. J. (1936) Directions for making mechanical analysis of soils by the hydrometer. Soil Science 42, 225–229. Pedobiologia (2003) 47, 475–478
Brady, N. C. (1974) The Nature and Properties of Soils. Macmillan Pub. Co., New York. Caminero, G. (1991) Estudio de la vegetación en afloraciones de Serpentina en el Bosque Estatal de Maricao, Puerto Rico. M. S. Thesis, University of Puerto Rico, Mayagüez. Dirección Nacional de Suelos y Fertilizantes B INRA (1975) Suelos de Cuba: Tomo I. Editorial Orbe, La Habana. Edwards, C. A., Lofty, J. R. (1976) Biology of Earthworms. Bookworm Publishing Co., Indiana. Fox, R. L. (1982) Some highly weathered soils of Puerto Rico, 3: chemical properties. Geoderma 27, 139–176. Fragoso, C., Lavelle, P. (1987) The Earthworm community of a Mexican tropical rain forest (Chajul, Chiapas). In: Bonvincini Pagliai, A. M., Omodeo, P. (eds) On Earthworms. Mucchi, Modena, pp. 281–295. Gates, G. E. (1962) On a new species of the earthworm genus Trigaster Benham 1886 (Octochaetidae). Breviora 178, 1–4. Lavelle, P., Barois, I., Cruz, I., Fragoso, C., Hernández, A., Pineda, A., Rangel, P. (1987) Adaptive strategies of Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta), a peregrine geophagous earthworm of the humid tropics. Biology and Fertility of Soils 5, 188–194. Lee, K. E. (1985) Earthworms: Their Ecology and Relationships with Soils and Land Use. Academic Press, New York. Lugo-López, M. A., Bartelli, L. J, Abruña, F. (1973) An overview of the soils of Puerto Rico: Classification, physical, chemical and mineralogical properties. Agricultural Experimental Station, University of Puerto Rico 79, 1–16. Németh, A., Herrera, R. (1982) Earthworm populations in Venezuelan tropical rain forests. Pedobiologia 23, 437–443. Parker, Jr. J. J., Taylor, H. M. (1965) Soil Strength and Seedling Emergence Relations. I. Soil Type, Moisture Tension, Temperature, and Planting Depth Effects. Agronomy Inc., Madison. Peech, M. (1965) Hydrogen-Ion Activity. In: Black, C. A. (ed) Methods in Soil Analysis. Part 2: Chemical and Microbiological Properties. American Society of Agronomy, Wisconsin, pp. 78–94. Roberts, R. C. (1942) Soil Survey, Puerto Rico. U.S. Department of Agriculture Series 1936(8). Sánchez, P. A. (1981) Suelos del Trópico: Características y Manejo. Instituto Interamericano de Cooperación para la Agricultura, Costa Rica. Sánchez-De León, Y., Zou, X., Borges, S., Ruan, H. (2003) Recovery of Native Earthworms in Abandoned Tropical Pastures. Conservation Biology 17, 999–1006. Silander, S. H., Gil de Rubio, H., Miranda, M., Vázquez, M. (1986) Los Bosques de Puerto Rico. In: Compedio Enciclopédico del Departamento de Recursos Naturales X (II), pp. 209–258. Soil Conservation Service (1967a) Soil Survey of Mayagüez Area of Western Puerto Rico. U.S. Department of Agriculture. Soil Conservation Service (1967b) Soil Survey Laboratory data and Descriptions for some soils of Puerto Rico and the U. S. Virgin Islands. U.S. Department of Agriculture.
The 7th international symposium on earthworm ecology · Cardiff · Wales · 2002
The oligochaetofauna of the Nipe soils in the Maricao State Forest, Puerto Rico Hendriekje Hubers, Sonia Borges* and Mónica Alfaro Department of Biology, University of Puerto Rico, Box 9012, Mayagüez, Puerto Rico 00681 Submitted September 6, 2002 · Accepted July 15, 2003
Summary The oligochaetofauna of the Nipe soils of Puerto Rico was studied for the first time. Earthworm and soil samples were taken over a year at six different sites. Earthworms were hand sorted from four successive soil layers, 10 cm in depth. Only three species were found: Onychochaeta borincana, Pontoscolex corethrurus, and Neotrigaster rufa. Abundance was low. It seems that the physicochemical conditions that characterize Nipe soils provide an inhospitable environment for these organisms. Key words: Neotropic, Serpentine soils, Caribbean, Nipe soils, soil fauna
Introduction Like all oxisols, the Nipe series are highly meteorized soils (Beinroth 1982) in which elimination of primary minerals has occurred (Lugo-López et al. 1973). They are very acid, have low fertility (Silander et al. 1986), and have more than 60 % clay although they behave as sandy or silty soils (Roberts 1942; Sánchez 1981). Their distinctive red color is due to their characteristic high iron oxide content. Nipe soils derive from serpentine rock. Although serpentine is found throughout the world, Nipe soils have only been identified from Cuba (DNSF-INRA 1975) and Puerto Rico (Roberts 1942). In Puerto Rico these soils are exclusively found in three areas of the western part of the island: the Maricao (236.7 ha) and Susúa (9.4 ha) State Forests and the extensively populated sectors of Cerro Las Mesas in Mayagüez and Plan Bonito in Cabo Rojo (SCS 1967a).
Studies on the flora of serpentine derived soils indicate that the vegetation of these soils is very particular, including many endemic species. Studies on the flora specific to the Nipe soils are scarce but it has been reported that plants growing on these soils present xeromorphic characteristics (Silander et al. 1986). The fauna of these soils has not been studied but it is possible that it is also determined by their mineralogical properties. Since soil physicochemical characteristics determine, to a great degree, the distribution and density of terrestrial oligochaetes, these annelids are an excellent group to estimate the extent to which fauna reflects soil conditions. The Nipe soils from the Maricao State Forest (MSF) were chosen for this study because they are the most extensive and least altered by human activity of all.
*E-mail corresponding author: [email protected]
0031-4056/03/47/05–06–475 $15.00/0
476
Hendriekje Hubers et al.
Materials and Methods
Results
The study area at the MSF is located between Km 15.7 and 15.8 of Road 120. Sampling was performed from May’90 to April’91. Six collection sites were chosen: 3 at 150 m north and 3 at 150 m south of this road. Each sample was taken from two 0.25 × 0.25 m quadrats. Earthworms were hand sorted from 4 successive 10 cm soil layers and were preserved in 10 % formalin. They were weighed with their gut contents after a month of preservation. The following soil analyses were carried out for each quadrat and each 10cm soil layer: moisture (Brady 1974), organic matter (OM) (Bouyucos 1936), pH (Peech 1965), resistance to penetration (250 kgf/cm soil resistance ring meter). Soil moisture content was determined monthly, pH every 3 months, and resistance to penetration (RP) once. Precipitation and temperature were obtained from the National Oceanographic and Atmospheric Administration monthly reports. A three-way factorial ANOVA was used to analyze data. Principal Component Analysis (PCA) was used to explain horizontal distribution of P. corethrurus, the most abundant species, in relation to soil properties.
The physical and chemical properties of these soils and earthworm numbers appear in Table 1. OM did not differ significantly (P > 0.1474) between sites but according to depth (P < 0.0001). pH did not vary (P > 0.70) between months but it did (P < 0.0001) between sites. There were significant differences in pH according to depth in May (P < 0.0001), August (P < 0.0004), and November (P < 0.0001). There was no significant difference (P < 0.05) in RP between sites but there were differences (P < 0.0066) according to soil depth and in the interaction between site and depth (P < 0.0498). Soil texture varied between sites (P < 0.0048) and between depths for silt (P < 0.0137) and sand (P < 0.0331). There was a difference (P < 0.0001) in monthly soil moisture between sites but not between depths. Soil moisture corresponded with monthly precipitation except for May–June and Jan.–Feb. Three worm species were collected in the soils: Pontoscolex corethrurus (Müller, 1856), Onychochaeta borincana Borges 1994, and Neotrigaster rufa (Gates, 1962). P. corethrurus represented 98 % of the earthworm community with a monthly mean of 68 ind.m-2 and a biomass of 16.4 gm-2. O. borincana’s
Table 1. Soil characteristics and the number of individuals per species found at each sampling site Sample
pH
OM %
RP
Sand %
Silt %
Clay %
Moisture %
Pc
Ob
Nr
1a 1b 1c 1d 2a 2b 2c 2d 3a 3b 3c 3d 4a 4b 4c 4d 5a 5b 5c 5d 6a 6b 6c 6d
5.04 5.10 5.15 4.52 4.82 4.98 4.95 5.03 4.98 4.91 4.96 5.11 4.88 4.93 4.72 4.97 4.78 4.65 4.70 4.81 4.48 4.57 4.69 4.74
7.29 5.40 3.94 3.52 7.81 7.28 5.77 4.14 6.89 5.67 4.19 3.80 9.11 6.55 4.94 3.96 8.66 6.37 4.59 3.73 8.87 5.95 4.60 4.43
0.97 0.69 0.63 0.72 0.60 0.79 0.78 0.81 0.53 0.53 0.53 0.88 0.56 0.72 0.53 0.94 0.63 0.69 0.82 0.81 0.79 0.79 0.82 0.88
43.00 34.50 42.00 39.50 44.00 45.00 45.50 51.00 53.50 57.00 57.00 58.00 54.50 50.50 54.00 62.50 56.50 67.00 48.00 56.00 64.50 74.00 6.10 49.50
32.00 25.00 21.50 19.00 27.00 26.50 29.00 21.10 28.00 26.00 21.00 17.50 23.50 22.00 17.50 15.00 21.50 15.50 22.00 17.50 19.00 15.50 18.00 19.50
25.00 35.50 36.50 41.50 29.00 28.50 25.50 28.00 18.50 17.00 22.00 22.50 22.00 27.50 28.50 22.50 22.00 17.50 30.00 26.50 16.50 12.00 21.00 31.00
28.55 27.75 28.42 28.92 27.46 27.46 29.00 30.25 22.54 21.58 22.17 24.21 24.46 21.46 23.29 26.38 18.83 15.71 16.00 18.50 18.04 15.30 16.63 21.46
23 26 11 2 29 17 6 1 71 35 18 11 1 1 1 0 137 78 20 8 57 33 10 8
2 1 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 2 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0
OM = organic matter, RP = resistance to penetration (kg force cm-2), Pc = Pontoscolex corethrurus, Ob = Onychochaeta borincana, Nr = Neotrigaster rufa Pedobiologia (2003) 47, 475–478
The oligochaetofauna of the Nipe soils
monthly mean was 0.58 ind.m-2 and 0.337 gm-2 while N. rufa had a monthly mean of 0.67 ind.m-2 and 0.327 gm-2. PCA showed that three components explain 83 % of the variance of soil properties. Component 1 (40 %) allowed separation of pH, OM, sand and silt from RP, clay and soil moisture. Component 2 (70 %) separated pH, OM, silt and moisture from RP, sand and clay. Component 3 does not allow a clear separation between soil properties.
Discussion The low species diversity of earthworms found in Nipe soils contrasts with the great heterogeneity of the flora reported for serpentine derived soils. Worm diversity of these soils is relatively low when compared with the 15 species reported from Chiapas, Mexico (Fragoso & Lavelle 1987) and even with the 8 found in Río Negro, Venezuela in spite of its limited food resources (Németh & Herrera 1982). If we ignore the results obtained in studies from continental forests and consider those from other sites on the island of Puerto Rico, we still find that the species diversity and abundance in Nipe soils are lower than those reported from Baño de Oro (Borges & Alfaro 1997) and from abandoned pastures in Cayey (Sánchez-de León et al. 2003). However, the Nipe results are similar to those found for the Cartagena Lagoon Reserve, an area that has been extensively perturbed for more than 70 years (Alfaro & Borges 1996). Apparently, the high salinity and sand content of the deeper soil layers and the accumulation of organic matter may be related to the low earthworm abundance in Cartagena. The soil texture results obtained in this study reflect the behavior of these soils rather than the proportion of the different soil particles. Roberts (1942) indicates that Nipe soils are 60–80 % clay while we found 10–48 %. This difference may be due to the presence of Fe and Al amorphic oxides that tend to unite clay particles in agglomerates that disperse as sand or silt (Sánchez 1981). These agglomerations explain, to a certain extent, the absence of a consistent pattern in soil texture between sampling sites. Apparently the dispersion method used did not eliminate all agglomerates. The mineralogical properties of these soils explain why they drain well and have low water availability, attributes not expected in clay soils. RP observed in Nipe soils does not seem to be an obstacle for worm movement because it was lower than the amount preventing seed emergence (Parker & Taylor 1965). Even though the soil is acidic, it is still within the tolerance range of oligochaetes. It appears that P.
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corethrurus prefers soils with a small range of pH, in this case between 4.5 and 5.0. pH was one of the components that explained most of the variance of soil properties. Available nitrogen (N) may limit earthworm distribution and abundance (Lee 1985). N content in Nipe soils is only 0.22 % in the first 12 cm and diminishes to less that 0.03 % at deeper levels (Roberts 1942). An average 0.390 % of N in the first 28 cm of these soils has also been reported (SCS 1967b). This N content is probably not a limiting factor per se because similar values have been indicated for ferralitic and alluvial soils in Chiapas (Fragoso & Lavelle 1987). As expected, worm density was higher in the top layers where OM was higher as well. Even though OM was not the only component explaining 70 % of the variance of soil properties, P. corethrurus was more abundant when the OM values were above 6.5 %. According to Fox (1982), Nipe soils are extremely infertile, particularly in the deeper horizons. Soil infertility is not only due to low OM, but also to a combination of factors such as nutrient deficiency of Ca or Mg or an excess of Mn, Fe or Al (Sánchez 1981). Nipe soils at the MSF have high Mg concentrations (18.93–49.66 cmol/kg-1) and normal agricultural Ca concentrations (0.43–8.7 cmol/kg) (Caminero 1991). The Mg:Ca proportion of these soils varies according to authors: 44.02–5.70 as stated by Caminero (1991) or 0.03 according to Fox (1982). In ferralitic soils (soils with high Fe concentration over calciferous rock) in Mexico the Mg:Ca was 0.44 in the first 10 cm and 0.73 in the 10–20 cm layer (Fragoso & Lavelle 1987). Our values are higher than those reported by Fox (1982) but much lower than Caminero’s (1991). The Mexican soils had higher diversity (7 vs. 3 species) and mean density (121 ind.m-2 vs. 74 ind.m-2) of worms than the Nipe soils. At the MSF the highest monthly worm density was typically found in the first 10 cm of soils, except during February and March when worms were more abundant in the 10–20 cm layers. This coincides with the prolonged reduction of soil moisture for those months. Other minerals present in Nipe soils are found in concentrations high enough to be toxic for the edaphic fauna. For example, exchangeable Fe is near 13 % down to 45 cm and increases with depth, while Al concentration is 7.9 cmol/Kg to 28 cm and decreases with soil depth (SCS 1967b). When soil moisture increases, the concentration of these minerals in the soil solution increases as well (Sánchez 1981). These temporal increments may provide an unfavorable medium for earthworms. Although soil moisture is one of the components which explain most of the variance of soil properties, no positive correlation was found between soil moisture and population abundance. The highest soil moisture of these soils corresponds with the lower Pedobiologia (2003) 47, 475–478
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tolerance limit for many worm species, including P. corethrurus (Edwards & Lofty 1976; Lavelle et al. 1987). It is possible, then, that the increment of Mg and Fe in soil solutions affects the earthworms. The severe physicochemical properties that characterize these soils may explain the low earthworm diversity found in this zone. P. corethrurus and O. borincana are geophagous species that have been reported from a variety of habitats, especially in disturbed areas. P. corethrurus, the most abundant species in Nipe soils, was probably introduced to the MSF with the reintroduction of endemic plants in a reforestation project. Fragoso & Lavelle (1987) have found P. corethrurus in soils with an OM content lower that that reported from Nipe soils. Barois and Lavelle (1986) have suggested that it has a mutualistic relationship with microorganisms, which aid in its digestion. This may also be true for O. borincana, a fairly common species on the island. Yet, only 5 specimens (0.58 ind.m-2) were collected at the MSF, an extremely low number considering that in Cartagena, a very limiting habitat for earthworms, its density was 101.3 ind.m-2. It is interesting to note that P. corethrurus was also present in Cartagena, but at lower densities that in the MSF (13.2 vs. 68 ind.m-2). N. rufa, on the other hand, is epigeic, an advantage in oligotrophic soils. However, only 6 specimens (0.67 ind.m-2) of this species were found in the MSF, corroborating Gates’ (1962) indication that none of the members of this genus seems to be common and that they could be limited to remote and inaccessible regions. Acknowledgements. Some soil analyses were performed at the USDA International Institute of Tropical Forestry at Río Piedras, Puerto Rico.
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