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Diversity of soil nematodes across a Mediterranean ecotone
Applied Soil Ecology 20 (2002) 191–198
Diversity of soil nematodes across a Mediterranean ecotone A. Imaz a,∗ , M.A. Hernández a , A.H. Ariño a , I. Armendáriz b , R. Jordana a a
b
Department of Zoology and Ecology, University of Navarra, E-31080 Pamplona, Spain Unidad Académica Multidisciplinaria Agronom´ıa y Ciencias, Universidad de Tamaulipas, México, CP 87000, Mexico Received 1 October 2001; accepted 22 February 2002
Abstract As an indicator of ecological maturity, we have analyzed the nematode community of an erosion-prone Mediterranean macchia and a pine stand within it. Species richness, abundance, diversity and maturity indexes have been measured from a number of standardized soil samples taken along parallel transects laid across the boundary between the pine stand and the macchia. Results of multifactor analysis on these data show three distinct nematode communities of different species composition. The intermediate nematode community (ecotone) is not a mixture of elements of adjacent communities (pine stand and macchia), thus suggesting the existence of an ecotone-specific community beyond the expected boundary effect. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Ecotone; Nematode; Diversity; Boundary effect; Desertification; Mediterranean region
1. Introduction According to Odum (1971) in Holland and Risser (1991), the “ecotone” concept was first proposed by Clements in 1905 to describe the boundary or transition region between two communities, where change or competition processes could be readily observed. The “ecotone community” would include components from both adjacent communities, as well as other ecotone-specific organisms. As such, the “ecotone” would be somewhat different from a “boundary effect”, where the organisms would only come from either community. Current definitions of “ecotone” include other concepts, such as the scale (both space and time) and the interaction between systems (Holland, 1988).
∗ Corresponding author. Tel.: +34-48-425-600; fax: +34-48-425-649. E-mail address: [email protected] (A. Imaz).
Large and stable ecotones have been observed to have high-diversity biocoenoses (Di Castri and Hansen, 1992). The plant components of these biocoenoses have been under study for around 60 years, especially along borders between very different vegetal formations (Risser, 1995). Research on ecotone arthropods is more recent (spiders, Downie et al., 1996; diptera, Dabrowska-Prot, 1995; collembola, Rusek, 1989, 1992, 1993; Slawski and Slawska, 2000), as are the other general ecotone studies (Kolasa and Zalewski, 1995). However, apart from the work of Rusek (1992) and Hanel (1993) on a meadow-forest ecotone, research on nematode biocoenoses on ecotones is scarce. We describe the nematode communities in a pine forest, its surrounding Mediterranean shrubland, and the transition area between them, and determine how their diversity components change from one community to the other. This study is part of a larger project “Biodiversity of the ecotone pine forest-Mediterranean shrubland as a tool against erosion in Mediterranean
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A. Imaz et al. / Applied Soil Ecology 20 (2002) 191–198
areas” aimed specifically at determining whether the diversity across such ecotones can be used in the Mediterranean area to improve erosion control, through a better and faster topsoil regeneration. The study area is located near Funes, Navarra, Spain (30TWM974858, 42◦ 18 N, 1◦ 48 W, elevation 450 m, mean annual rainfall 419 mm, mean annual temperature 14 ◦ C), a Mediterranean area with saline soils where gypsum dominates. It is a gentle (13◦ ) N–NNE slope with a 30–40 year-old pine stand (Pinus halepensis P. Mill., accompanied by Rhamnus alaternus L., Brachypodium retusum (Pers.) Beauv., Rosmarinus officinalis L., Thymus vulgaris L., and Helianthemum canum (L.) Baung.) within a Mediterranean shrubland (mostly R. officinalis, accompanied by T. vulgaris and Helianthemum canum). The ecotone between these two plant communities were sampled. 2. Methods The area was sampled in November 1994. Five parallel, replicated transects were laid from the pine stand across the ecotone into the shrubland (Fig. 1). On each transect, three sampling points were selected in the shrubland (sampling points: (1) under an isolated pine tree (P); (2) bare soil (S); (3) under a rosemary bush (R)), three on the ecotone (sampling points: (4) outer ecotone (EC1); (5) middle ecotone (EC2); (6) inner ecotone (EC3)), and one within the pine stand (sampling point (7) pine grove (PI), about 8 m from the pine stand rim). The 20.25 cm2 , 8–10 cm deep samples (from litter layer to bedrock, encompassing the full
soil profile) were collected by means of a Kubiena-box stack injector (Peltier et al., 2001) and were preserved in situ with 4% formalin. After 24 h, they were stored in 75% alcohol. From each Kubiena box, soil macromorphological units were separated by hand (Peltier et al., 2001). Thus, from each 2 cm deep box, a number of subsamples were separated and then extracted. Each subsample was processed in order to extract total fauna, following the procedure of Belascoain et al. (1998) that first extracts arthropods and then nematodes from the same sample. Nematodes were collected by sugar gradient centrifugation after heptane-flotation extraction of the arthropods. Nematodes were prepared for mounting by a modified Seinhorst (1959) method, including dehydration, ethanol substitution and glycerin mounting. The specimens of the samples of three of the five transects, hereinafter considered “replicates”, were identified. The samples of the remaining two transects were stored as backup. Nematodes were identified to species, whenever possible, by optical microscopy. The number of individuals of each species of each soil macromorphological subunit of each subsample was recorded. The maturity index was calculated as: MI =
n
v(i)f (i)
i=1
where v(i) is the c–p value of the taxon i and f(i) is the frequency of that taxon in the nematode population. The plant parasite index (PPI; Bongers, 1990), the modified maturity index ( MI; Yeates, 1994) and Shannon’s diversity index (H ) for each sampling point
Fig. 1. Sampling scheme. The depicted average transect represents mean distances between corresponding points of five parallel transects. Squares (not to scale) represent 4.5 cm × 4.5 cm sampling points. The three sampling points of each transect located in the macchia were located at three different habitats (bare soil, under rosemary bush and under isolated pine) and were within 1.5 m of each other within the same transect. “Transition area” corresponds to the ecotone.
A. Imaz et al. / Applied Soil Ecology 20 (2002) 191–198 Table 1 Physical-chemical analysis of soil profiles collected from the three biotopesa
Gravel (>2 mm; %) Coarse sand (2–0.2 mm; %) Fine sand (0.2–0.005 mm; %) Loam (0.05–0.002 mm; %) Clay (<0.002 mm; %) pH (water, 1:2.5) Oxidable organic matter (%) Total nitrogen (%) C/N ratio Wilting point (% of water) Field capacity
Macchia
Ecotone
Pine
17 16.9 52.6 8.18 22.32 7.9 4.3 0.2 14.6 15.6 27
22 15.02 51.78 9.28 23.92 7.9 5.4 0.2 13.0 16.8 29
5 7.2 77.4 4.34 11.06 7.9 3.7 0.1 15.5 9.2 37
a Modified from a report by Department of Projects and Country Planning, School of Forestry, Universidad Polit´ecnica de Madrid, for Project Ecotones, UE contract EV5V-CT94-0485. Soil texture by Bouyoucos method; pH by Chapman and Pratt method; oxidable organic matter by Walkley and Black method; total nitrogen by Rubia and Blasco variant of Kjeldahl method.
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Table 2 Biological data for the three biotopesa
Abundance Richness H MI MI PPI
Macchia
Outer ecotone
Middle ecotone
Inner ecotone
Pine grove
1433 50 4.29 2.28 2.26 2.24
2509 67 4.23 2.56 2.55 2.50
1603 52 3.94 2.24 2.35 2.71
1253 51 4.51 2.56 2.53 2.38
1212 71 4.84 2.31 2.42 2.76
a Abundance in number of nematode specimens per 60.75 cm2 of soil. Data for macchia points have been pooled (see text). H : Shannon diversity index; MI: Bonger’s maturity index; PPI: plant parasitic index; MI: Yeates-corrected Bongers index. See text for formulae.
and that it decreased towards the pine stand. However, the maximum number of species appeared within the pine stand (71 species), followed by the outer ecotone. 3.2. Calculated diversity
were also calculated from the combined inventories of the three replicates. Total abundance data for the macchia biotope was obtained by combining the data from the three sampling points (one of each transect) corresponding to each of the three macchia habitats sampled (rosemary, bare soil, pine litter). Pooling was done by weighted average according to the percentage of vegetation-type cover. The total richness value for this biotope was obtained by rarefaction (Sanders, 1968 in Krebs, 1989). All data were standardized to equal soil surface (60.75 cm2 ), full-soil profile (i.e. from litter layer to bedrock). Data were further analyzed by characterizing each biotope according to the presence/exclusivity indexes, and by performing a factor analysis of correspondences, on the standardized, unpooled contingency table. Physico-chemical characters of the biotopes were assessed (Table 1). 3. Results
The Shannon–Wiener index (H , Table 2) on individuals showed maxima in the pine stand and its adjacent ecotone point, being minimal in the middle of the ecotone. However, differences between the points were very small (values ranged from 3.9 to 4.8). 3.3. Maturity indexes The Bongers and Yeates maturity indexes (MI, PPI and MI) give information on the ecosystem status and degree of alteration. The observed values were always over 2, with little variation (Table 2). However, in each case, one or a few species were largely responsible for the observed values, such as Microdorylaimus modestus (Altherr, 1952) in the outer ecotone; Prionchulus muscorum (Dujardin, 1845), Aporcelaimellus cf. obtusicaudatus and Longidorella murithi Altherr (1959) in the inner ecotone and Aphelenchoides on the macchia, where it is frequent in the bare soil. It is significant that the indexes show similar behavior, which could mean some independence of the tropic habits of the species.
3.1. Biological parameters 3.4. Species characterization 3.1.1. Observed abundance and richness Table 2 shows that the outer (i.e. nearer to the shrubland) ecotone samples had the greater total abundance
The individual communities in the samples were found to be different. Exclusive and preferential
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Fig. 2. Exclusive and favored species from each biotope. Vertical scale is logarithmic for each species. S: bare soil within macchia; P: under isolated pine within macchia; R: under isolated rosemary bush within macchia; EC1: outer ecotone; EC2: ecotone; EC3: inner ecotone; PI: pine grove.
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species have been identified and these permit us to establish three different biotopes: pine stand, shrubland and ecotone proper. Less frequent (less than five individuals per sample) species have not been taken into account in this analysis (Fig. 2). The ecotone showed five exclusive species: P. muscorum, Coomansus parvus (De Man, 1880), Ereptonema arcticum (Loof, 1971), Diplogaster sp. and Aphelenchus sp., and five preferential species (i.e. species that have maxima within the biotope): Ditylenchus nortoni (Elmiligy, 1971, 1972), Helicotylenchus vulgaris (Yuen, 1964), Ceratoplectus assimilis (Bütschli, 1873), M. modestus and L. murithi. The shrubland had seven exclusive species: Axonchium gienense Peña Santiago and Coomans (1990), Dorylaimellus egmonti Yeates and Ferris
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(1964), Xiphinema ingens Luc and Dalmasso (1964), D. adasi (Sykes, 1980), Eucephalobus mucronatus (Kozlowska and Roguska-Wasilewska, 1963), Filenchus hamatus (Thorne and Malek, 1968) and Filenchus sp., and eleven preferential species: Pseudacrobeles sp., F. misellus (Andrássy, 1954), F. discrepans (Andrássy, 1954), F. vulgaris (Brzeski, 1963), Drilocephalobus moldavicus Lisethkaya (1968), Tylenchus elegans De Man (1876), Paratylenchus projectus Jenkins (1956), Ditylenchus sp., Coslenchus rugosus Andrássy (1982), Aphelenchoides sp. and Criconemella rosmarini Castillo Siddigi and Gomez Barcina (1988). The pine stand had four exclusive species: Alaimus assamensis Choudhary and Jairajpuri (1984), Alirhabditis sp., Anaplectus granulosus (Bastian, 1865) and Geomonhystera australis (Cobb,
Fig. 3. Factor analysis of correspondences for the frequency table. Dots: species; squares: ecotone points; triangles: macchia points; circle: pine grove; S: bare soil within macchia; P: under isolated pine within macchia; R: under isolated rosemary bush within macchia; EC1: outer ecotone; EC2: ecotone; EC3: inner ecotone; PI: pine grove.
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1893), and three preferential species: Pratylenchus pratensis (De Man, 1880), Plectus minimus Cobb (1893) and Bunonema reticulatum Richters (1905). 3.5. Multifactor analysis The factor analysis (Fig. 3) performed on the abundance resulted in a clear separation of the three ecotone points along the first axis (28% variance), with the central point of the ecotone segregated by the second factor (19% variance). The pine stand was intermediate between the very characteristic macchia and the ecotone community.
4. Discussion Despite its low accumulated variance, the two first factors of the factor analysis would suffice to characterize the ecotone as being different from both shrubland and pine, thus suggesting the actual existence of this specific biotope as different from the mere contact between the two main biotopes (pine stand and macchia). Therefore, the hypothesis of three distinct biotopes along the transects would also yield at least two border effects (that of pine-ecotone and that of macchia-ecotone). Abundance data appeared to suggest a positive border effect of the macchia (shrubland) on the ecotone biotope (Table 2). Leopold (1933) in Rusek (1992) had already suggested this effect for nematode populations. However, there was no corresponding effect of the pine stand on the ecotone biotope; this agrees with the observations of Rusek (1992) and Hanel (1993) on meadow/fir borders. In any case, the total abundance of nematode populations seemed very high. Persson et al. (1980) and Sohlenius and Boström (1999) suggested that nematode abundance tends to be maximal at the same period of the year as when our sampling was performed. Specific richness appears to be very high for all biotopes of these classes: compared with data from Jordana et al. (1987) or Vinciguerra et al. (1995). Ruess (1995) comes closer to these levels. A border effect from the macchia into the ecotone seemed to exist for species numbers, and with the abundance. However, the effect of the pine stand on the ecotone, if it exists, would be negative (a drop of 20 species).
It should be noted that the pine confers to the soil a greater porosity than other plants. According to Yeates (1984), textured soils have denser nematode populations, and soil texture has an effect on nematode distribution (Hunt, 1993). The soil of the pine stand has the greatest percentage of sand (and lowest of clay and loam) of all transect points. When considering the individual samples of the macchia biotope, before pooling by vegetation cover, both the richness and abundance were least in those collected from bare soil. Studies on the protective effect of vegetation cover in Mediterranean shrubland on erosion (Andreu et al., 1998) show that bare soil has the lowest structural stability and organic matter contents. In our samples, Peltier et al. (2001) showed that the bare soil samples contain the least amount of fauna-processed litter and have the greatest mineral contents. Also, the diversity of macromorphological units is least for these points (Jordana et al., 2000). Maturity indexes followed the same pattern as the abundance profile. MI (without phytophagous families) and MI (for all trophic groups) encompass both sides of the central (ecotone) biotope. The PPI index behaved in the opposite fashion, as predicted by Bongers (1990). However, we did not find the difference between the two indexes that Yeates (1994) proposed: the inclusion of low c–p value populations in the latter index did not dilute the high c–p values of the dorylaimids. We did find that the ecotone areas had higher MI values than the pine stand, which agreed with results from Sohlenius (1997) in that these areas were more mature than the pine stand or the shrubland. This did not agree with other studies, such as Vinciguerra et al. (1995) on P. halepensis, which showed a higher maturity on the pine stand; however, these data are for higher MI values than ours, more in the range that Armendariz et al. (1996) and Sohlenius (1997) have found for other pine types. It should be noted that the structure of MI is sensitive to the presence of certain colonizing genera, which artificially pushes up the index value. Thus, a similar index may indicate a quite different degree of maturity, depending on the abundance of these particular species: note, for instance, that on bare soil samples in our study the value of MI for bare soil depends heavily on one abundant genus. Literature consensus on the hypothetically greater diversity values in ecotones, as measured by the
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Shannon index, does not exist for nematodes, although some data would support the hypothesis (Vinciguerra et al., 1995, found greater diversity in the ecotone than in adjacent areas for nematodes). Rusek (1992) pointed out that, although this general tendency may exist, some ecotones seem to be very heterogeneous for this parameter. Some meso-ecotones showed persistently low diversity values for epigeous collembola (Rusek, 1992). It has also been reported that the diversity peak can migrate between the ecotone proper and contiguous biotopes during the year, probably due to variable intensity of the border effect: Hanel (1993) found that for meadow ecotones the diversity peaks in the ecotone in March and in the meadow in May. Our data does not support any definite hypothesis, since virtually all diversity data are very similar along the transects. However, these diversity values are formed from different nematode communities. The ecotone community included predatory species, such as C. parvus and P. muscorum, that imply a higher degree of ecological structure and, possibly, a more complex trophic web. Also, the ecotone biotope was home for several dorylaimid species that are persistent but particularly sensitive to habitat alteration (Bongers, 1990). The macchia, or shrubland, also included specific communities (A. gienense, D. egmonti, X. ingens, P. projectus or Tylenchus elegans); some of these appeared to merge and influence the ecotone communities, possibly through the observed border effect (C. rosmarini, Pseudacrobeles sp. and Filenchus vulgaris). Finally, we found exclusive species within the pine stand (A. assamensis, A. granulosus or G. australis). Jordana et al. (1987) did not find any exclusive species for this same biotope. Although our data seem to refer to the macchia biotope as a single biotope, this is actually a mosaic of several sub-biotopes. Jordana et al. (1987) showed that, in arid Mediterranean biotopes, fauna concentrate under the arbustive pillows. Freckman and Mankau (1986) also observed abundance maxima directly under desert shrubs. We found that the area under the Rosmarinus canopy is particularly abundant for nematodes within the open shrubland. This shrub also sheltered some exclusive, high c–p species, such as A. gienense or D. egmonti). The isolated pines in the macchia also have an almost exclusive species (X. ingens). The bare soil, in all cases, is the poorest sub-biotope
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and, therefore, the one most prone to erosion and degradation.
Acknowledgements This work was done within the EU project “Ecotones” of the IV Framework, Contract EV5V-CT940485. References Andreu, V., Rubio, J.L., Cerni, R., Soil, J., 1998. Effects of Mediterranean shrub cover on water erosion (Valencia, Spain). Water Consserv. 53, 112–120. Armendariz, I., Hernandez, M.A., Jordana, R., 1996. Temporal evolution of soil nematode communities in Pinus nigra forests of Navarra, Spain. Fundam. Appl. Nematol. 19, 561–577. Belascoain, C., Ariño, A.H., Jordana, R., 1998. A new integrated extraction method for microarthropods and nematodes from the same soil samples. Pedobiologia 42, 165–170. Bongers, T., 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83, 14–19. Dabrowska-Prot, E., 1995. The effect of forest-field ecotones on biodiversity of entomofauna and its functioning in agricultural landscape. Ekol. Pol. 43, 51–78. Di Castri, F., Hansen, A.J., 1992. The environment and development crises as determinants of landscape dynamics. In: Hansen, A.J., Di Castri, F. (Eds.), Landscape Boundaries. Consequences for Biotic Diversity and Landscape Flows. Springer, New York, pp. 3–18. Downie, I.S., Coulson, J.C., Butterfield, J.E.L., 1996. Distribution and dynamics of surface-dwelling spiders across a pastureplantation ecotone. Ecography 19, 29–40. Freckman, D.W., Mankau, R., 1986. Abundance, distribution, biomass and energetics of soil nematodes in a northern Mojave desert ecosystem. Pedobiologia 29, 129–142. Hanel, L., 1993. Soil nematodes in a meadow-spruce forest ecotone. Acta Soc. Zool. Bohemoslov 56, 256–278. Holland, M.M. (compiler), 1988. SCOPE/MAB technical consultations on landscape boundaries. Report of a SCOPE/MAB workshop on ecotones. In: Di Castri, F., Hansen, A.J., Holland, M.M. (Eds.), A New Look at Ecotones: Emerging International Projects on Landscape Boundaries. Biology International (special issue) UIBS, Paris, Vol. 17. pp. 47–106. Holland, M.M., Risser, P.G., 1991. Introduction: the role of landscape boundaries in the management and restoration of changing environments. In: Holland, M.M., Risser, P.G., Naiman, R.J. (Eds.), Ecotones. The role of Landscape Boundaries in the Management and Restoration of Changing Environment. Chapman and Hall, New York, pp. 1–7. Hunt, D.J., 1993. Aphelenchida, Longidoridae and Trichodoridae: their Systematics and Bionomics. CAB International, Wallingford, p. 352.
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Jordana, R., Arbea, J.I., Moraza, L., Montenegro, E., Mateo, M.D., Hernández, M.A., Herrera, L., 1987. Effect of reforestation by conifers in natural biotopes of middle and south Navarra (northern Spain). Rev. Suisse Zool. 94, 491–502. Jordana, R., Arpin, P., Vinciguerra, M.T., Gonzalez, S., Aramburu, M.P., Ariño, A.H., Armendariz, I., Belascoain, C., Cifuentes, P., Clausi, R., Escribano, R., Garcia-Abril, A., Garcia-Mina, J.M., Hernandez, M.A., Imaz, A., Moraza, M.L., Ponge, J.F., Puig, J., Ramos, A., 2000. Biodiversity across ecotones in desertificable Mediterranean areas. In: Balabanis, P., Peter, D., Ghazi, A., Tsogas, M. (Eds.), Mediterranean Desertification Research Results and Policy Implications, Vol. 2. European Commission. pp. 497–505. Kolasa, J., Zalewski, M., 1995. Notes on ecotone attributes and functions. Hydrobiologia 303, 1–7. Krebs, C.J., 1989. Ecological Methodology. Harper and Row, New York, p. 654. Peltier, A., Ponge, J.F., Jordana, R., Ariño, A., 2001. Humus forms in Mediterranean scrublands with aleppo pine. Soil Sci. Soc. Am. J. 65, 884–896. Persson, T., Baath, E., Clarholm, M., Lunkvist, H., Söderström, B.E., Sohlenius, B., 1980. Trophic structure, biomass dynamics and carbon metabolism of soil organisms in a Scots pine forest. Ecol. Bull. (Stockholm) 32, 419–459. Risser, P.G., 1995. The status of science examining ecotones. Bioscience 45, 318–325. Ruess, L., 1995. Studies on the nematode fauna of an acid forest soil: spatial distribution and extraction. Nematologica 41, 229– 239.
Rusek, J., 1989. Collembola and Protura in a meadow-forest ecotone. In: Dallai, R. (Ed.), Proceedings of the 3rd International Seminar on Apterigota Siena, Italy, pp. 413–418. Rusek, J., 1992. Distribution and dynamics of soil organisms across ecotones. In: Hansen, A.J., Di Castri F. (Eds.), Landscape Boundaries: Consequences for Biotic Diversity and Landscape Flows. Springer, New York, pp. 196–214. Rusek, J., 1993. Air pollution mediated changes in alpine ecosystems and ecotones. Ecol. Appl. 3, 409–416. Seinhorst, J.W., 1959. A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4, 67–69. Slawski, M., Slawska, M., 2000. The forest edge as a border between forest and meadow. Vegetation and Collembola communities. Pedobiologia 44, 442–450. Sohlenius, B., 1997. Fluctuations of nematode populations in pine forest soil. Influence by clear-cutting. Fundam. Appl. Nematol. 20, 103–114. Sohlenius, B., Boström, S., 1999. Effects of climate change on soil factors and metazoan microfauna (nematodes, tardigrades and rotifers) in a Swedish tundra soil—a soil transplantation experiment, tardigrades and rotifers) in a Swedish tundra soil. Appl. Soil Ecol. 12, 113–128. Vinciguerra, M.T., Clausi, M., La Rosa, G., 1995. Analisi del popolamiento nematologico di una pineta d’aleppo in Sicilia. Nematol. Medit. 23 (Suppl.), 49–55. Yeates, G.W., 1984. Variation in soil nematode diversity under pasture with soil and year. Soil Biol. Biochem. 16, 95–102. Yeates, G.W., 1994. Modification and qualification of the nematode maturity index. Pedobiologia 38, 97–101.
Diversity of soil nematodes across a Mediterranean ecotone A. Imaz a,∗ , M.A. Hernández a , A.H. Ariño a , I. Armendáriz b , R. Jordana a a
b
Department of Zoology and Ecology, University of Navarra, E-31080 Pamplona, Spain Unidad Académica Multidisciplinaria Agronom´ıa y Ciencias, Universidad de Tamaulipas, México, CP 87000, Mexico Received 1 October 2001; accepted 22 February 2002
Abstract As an indicator of ecological maturity, we have analyzed the nematode community of an erosion-prone Mediterranean macchia and a pine stand within it. Species richness, abundance, diversity and maturity indexes have been measured from a number of standardized soil samples taken along parallel transects laid across the boundary between the pine stand and the macchia. Results of multifactor analysis on these data show three distinct nematode communities of different species composition. The intermediate nematode community (ecotone) is not a mixture of elements of adjacent communities (pine stand and macchia), thus suggesting the existence of an ecotone-specific community beyond the expected boundary effect. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Ecotone; Nematode; Diversity; Boundary effect; Desertification; Mediterranean region
1. Introduction According to Odum (1971) in Holland and Risser (1991), the “ecotone” concept was first proposed by Clements in 1905 to describe the boundary or transition region between two communities, where change or competition processes could be readily observed. The “ecotone community” would include components from both adjacent communities, as well as other ecotone-specific organisms. As such, the “ecotone” would be somewhat different from a “boundary effect”, where the organisms would only come from either community. Current definitions of “ecotone” include other concepts, such as the scale (both space and time) and the interaction between systems (Holland, 1988).
∗ Corresponding author. Tel.: +34-48-425-600; fax: +34-48-425-649. E-mail address: [email protected] (A. Imaz).
Large and stable ecotones have been observed to have high-diversity biocoenoses (Di Castri and Hansen, 1992). The plant components of these biocoenoses have been under study for around 60 years, especially along borders between very different vegetal formations (Risser, 1995). Research on ecotone arthropods is more recent (spiders, Downie et al., 1996; diptera, Dabrowska-Prot, 1995; collembola, Rusek, 1989, 1992, 1993; Slawski and Slawska, 2000), as are the other general ecotone studies (Kolasa and Zalewski, 1995). However, apart from the work of Rusek (1992) and Hanel (1993) on a meadow-forest ecotone, research on nematode biocoenoses on ecotones is scarce. We describe the nematode communities in a pine forest, its surrounding Mediterranean shrubland, and the transition area between them, and determine how their diversity components change from one community to the other. This study is part of a larger project “Biodiversity of the ecotone pine forest-Mediterranean shrubland as a tool against erosion in Mediterranean
0929-1393/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 9 - 1 3 9 3 ( 0 2 ) 0 0 0 2 4 - 0
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areas” aimed specifically at determining whether the diversity across such ecotones can be used in the Mediterranean area to improve erosion control, through a better and faster topsoil regeneration. The study area is located near Funes, Navarra, Spain (30TWM974858, 42◦ 18 N, 1◦ 48 W, elevation 450 m, mean annual rainfall 419 mm, mean annual temperature 14 ◦ C), a Mediterranean area with saline soils where gypsum dominates. It is a gentle (13◦ ) N–NNE slope with a 30–40 year-old pine stand (Pinus halepensis P. Mill., accompanied by Rhamnus alaternus L., Brachypodium retusum (Pers.) Beauv., Rosmarinus officinalis L., Thymus vulgaris L., and Helianthemum canum (L.) Baung.) within a Mediterranean shrubland (mostly R. officinalis, accompanied by T. vulgaris and Helianthemum canum). The ecotone between these two plant communities were sampled. 2. Methods The area was sampled in November 1994. Five parallel, replicated transects were laid from the pine stand across the ecotone into the shrubland (Fig. 1). On each transect, three sampling points were selected in the shrubland (sampling points: (1) under an isolated pine tree (P); (2) bare soil (S); (3) under a rosemary bush (R)), three on the ecotone (sampling points: (4) outer ecotone (EC1); (5) middle ecotone (EC2); (6) inner ecotone (EC3)), and one within the pine stand (sampling point (7) pine grove (PI), about 8 m from the pine stand rim). The 20.25 cm2 , 8–10 cm deep samples (from litter layer to bedrock, encompassing the full
soil profile) were collected by means of a Kubiena-box stack injector (Peltier et al., 2001) and were preserved in situ with 4% formalin. After 24 h, they were stored in 75% alcohol. From each Kubiena box, soil macromorphological units were separated by hand (Peltier et al., 2001). Thus, from each 2 cm deep box, a number of subsamples were separated and then extracted. Each subsample was processed in order to extract total fauna, following the procedure of Belascoain et al. (1998) that first extracts arthropods and then nematodes from the same sample. Nematodes were collected by sugar gradient centrifugation after heptane-flotation extraction of the arthropods. Nematodes were prepared for mounting by a modified Seinhorst (1959) method, including dehydration, ethanol substitution and glycerin mounting. The specimens of the samples of three of the five transects, hereinafter considered “replicates”, were identified. The samples of the remaining two transects were stored as backup. Nematodes were identified to species, whenever possible, by optical microscopy. The number of individuals of each species of each soil macromorphological subunit of each subsample was recorded. The maturity index was calculated as: MI =
n
v(i)f (i)
i=1
where v(i) is the c–p value of the taxon i and f(i) is the frequency of that taxon in the nematode population. The plant parasite index (PPI; Bongers, 1990), the modified maturity index ( MI; Yeates, 1994) and Shannon’s diversity index (H ) for each sampling point
Fig. 1. Sampling scheme. The depicted average transect represents mean distances between corresponding points of five parallel transects. Squares (not to scale) represent 4.5 cm × 4.5 cm sampling points. The three sampling points of each transect located in the macchia were located at three different habitats (bare soil, under rosemary bush and under isolated pine) and were within 1.5 m of each other within the same transect. “Transition area” corresponds to the ecotone.
A. Imaz et al. / Applied Soil Ecology 20 (2002) 191–198 Table 1 Physical-chemical analysis of soil profiles collected from the three biotopesa
Gravel (>2 mm; %) Coarse sand (2–0.2 mm; %) Fine sand (0.2–0.005 mm; %) Loam (0.05–0.002 mm; %) Clay (<0.002 mm; %) pH (water, 1:2.5) Oxidable organic matter (%) Total nitrogen (%) C/N ratio Wilting point (% of water) Field capacity
Macchia
Ecotone
Pine
17 16.9 52.6 8.18 22.32 7.9 4.3 0.2 14.6 15.6 27
22 15.02 51.78 9.28 23.92 7.9 5.4 0.2 13.0 16.8 29
5 7.2 77.4 4.34 11.06 7.9 3.7 0.1 15.5 9.2 37
a Modified from a report by Department of Projects and Country Planning, School of Forestry, Universidad Polit´ecnica de Madrid, for Project Ecotones, UE contract EV5V-CT94-0485. Soil texture by Bouyoucos method; pH by Chapman and Pratt method; oxidable organic matter by Walkley and Black method; total nitrogen by Rubia and Blasco variant of Kjeldahl method.
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Table 2 Biological data for the three biotopesa
Abundance Richness H MI MI PPI
Macchia
Outer ecotone
Middle ecotone
Inner ecotone
Pine grove
1433 50 4.29 2.28 2.26 2.24
2509 67 4.23 2.56 2.55 2.50
1603 52 3.94 2.24 2.35 2.71
1253 51 4.51 2.56 2.53 2.38
1212 71 4.84 2.31 2.42 2.76
a Abundance in number of nematode specimens per 60.75 cm2 of soil. Data for macchia points have been pooled (see text). H : Shannon diversity index; MI: Bonger’s maturity index; PPI: plant parasitic index; MI: Yeates-corrected Bongers index. See text for formulae.
and that it decreased towards the pine stand. However, the maximum number of species appeared within the pine stand (71 species), followed by the outer ecotone. 3.2. Calculated diversity
were also calculated from the combined inventories of the three replicates. Total abundance data for the macchia biotope was obtained by combining the data from the three sampling points (one of each transect) corresponding to each of the three macchia habitats sampled (rosemary, bare soil, pine litter). Pooling was done by weighted average according to the percentage of vegetation-type cover. The total richness value for this biotope was obtained by rarefaction (Sanders, 1968 in Krebs, 1989). All data were standardized to equal soil surface (60.75 cm2 ), full-soil profile (i.e. from litter layer to bedrock). Data were further analyzed by characterizing each biotope according to the presence/exclusivity indexes, and by performing a factor analysis of correspondences, on the standardized, unpooled contingency table. Physico-chemical characters of the biotopes were assessed (Table 1). 3. Results
The Shannon–Wiener index (H , Table 2) on individuals showed maxima in the pine stand and its adjacent ecotone point, being minimal in the middle of the ecotone. However, differences between the points were very small (values ranged from 3.9 to 4.8). 3.3. Maturity indexes The Bongers and Yeates maturity indexes (MI, PPI and MI) give information on the ecosystem status and degree of alteration. The observed values were always over 2, with little variation (Table 2). However, in each case, one or a few species were largely responsible for the observed values, such as Microdorylaimus modestus (Altherr, 1952) in the outer ecotone; Prionchulus muscorum (Dujardin, 1845), Aporcelaimellus cf. obtusicaudatus and Longidorella murithi Altherr (1959) in the inner ecotone and Aphelenchoides on the macchia, where it is frequent in the bare soil. It is significant that the indexes show similar behavior, which could mean some independence of the tropic habits of the species.
3.1. Biological parameters 3.4. Species characterization 3.1.1. Observed abundance and richness Table 2 shows that the outer (i.e. nearer to the shrubland) ecotone samples had the greater total abundance
The individual communities in the samples were found to be different. Exclusive and preferential
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Fig. 2. Exclusive and favored species from each biotope. Vertical scale is logarithmic for each species. S: bare soil within macchia; P: under isolated pine within macchia; R: under isolated rosemary bush within macchia; EC1: outer ecotone; EC2: ecotone; EC3: inner ecotone; PI: pine grove.
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species have been identified and these permit us to establish three different biotopes: pine stand, shrubland and ecotone proper. Less frequent (less than five individuals per sample) species have not been taken into account in this analysis (Fig. 2). The ecotone showed five exclusive species: P. muscorum, Coomansus parvus (De Man, 1880), Ereptonema arcticum (Loof, 1971), Diplogaster sp. and Aphelenchus sp., and five preferential species (i.e. species that have maxima within the biotope): Ditylenchus nortoni (Elmiligy, 1971, 1972), Helicotylenchus vulgaris (Yuen, 1964), Ceratoplectus assimilis (Bütschli, 1873), M. modestus and L. murithi. The shrubland had seven exclusive species: Axonchium gienense Peña Santiago and Coomans (1990), Dorylaimellus egmonti Yeates and Ferris
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(1964), Xiphinema ingens Luc and Dalmasso (1964), D. adasi (Sykes, 1980), Eucephalobus mucronatus (Kozlowska and Roguska-Wasilewska, 1963), Filenchus hamatus (Thorne and Malek, 1968) and Filenchus sp., and eleven preferential species: Pseudacrobeles sp., F. misellus (Andrássy, 1954), F. discrepans (Andrássy, 1954), F. vulgaris (Brzeski, 1963), Drilocephalobus moldavicus Lisethkaya (1968), Tylenchus elegans De Man (1876), Paratylenchus projectus Jenkins (1956), Ditylenchus sp., Coslenchus rugosus Andrássy (1982), Aphelenchoides sp. and Criconemella rosmarini Castillo Siddigi and Gomez Barcina (1988). The pine stand had four exclusive species: Alaimus assamensis Choudhary and Jairajpuri (1984), Alirhabditis sp., Anaplectus granulosus (Bastian, 1865) and Geomonhystera australis (Cobb,
Fig. 3. Factor analysis of correspondences for the frequency table. Dots: species; squares: ecotone points; triangles: macchia points; circle: pine grove; S: bare soil within macchia; P: under isolated pine within macchia; R: under isolated rosemary bush within macchia; EC1: outer ecotone; EC2: ecotone; EC3: inner ecotone; PI: pine grove.
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1893), and three preferential species: Pratylenchus pratensis (De Man, 1880), Plectus minimus Cobb (1893) and Bunonema reticulatum Richters (1905). 3.5. Multifactor analysis The factor analysis (Fig. 3) performed on the abundance resulted in a clear separation of the three ecotone points along the first axis (28% variance), with the central point of the ecotone segregated by the second factor (19% variance). The pine stand was intermediate between the very characteristic macchia and the ecotone community.
4. Discussion Despite its low accumulated variance, the two first factors of the factor analysis would suffice to characterize the ecotone as being different from both shrubland and pine, thus suggesting the actual existence of this specific biotope as different from the mere contact between the two main biotopes (pine stand and macchia). Therefore, the hypothesis of three distinct biotopes along the transects would also yield at least two border effects (that of pine-ecotone and that of macchia-ecotone). Abundance data appeared to suggest a positive border effect of the macchia (shrubland) on the ecotone biotope (Table 2). Leopold (1933) in Rusek (1992) had already suggested this effect for nematode populations. However, there was no corresponding effect of the pine stand on the ecotone biotope; this agrees with the observations of Rusek (1992) and Hanel (1993) on meadow/fir borders. In any case, the total abundance of nematode populations seemed very high. Persson et al. (1980) and Sohlenius and Boström (1999) suggested that nematode abundance tends to be maximal at the same period of the year as when our sampling was performed. Specific richness appears to be very high for all biotopes of these classes: compared with data from Jordana et al. (1987) or Vinciguerra et al. (1995). Ruess (1995) comes closer to these levels. A border effect from the macchia into the ecotone seemed to exist for species numbers, and with the abundance. However, the effect of the pine stand on the ecotone, if it exists, would be negative (a drop of 20 species).
It should be noted that the pine confers to the soil a greater porosity than other plants. According to Yeates (1984), textured soils have denser nematode populations, and soil texture has an effect on nematode distribution (Hunt, 1993). The soil of the pine stand has the greatest percentage of sand (and lowest of clay and loam) of all transect points. When considering the individual samples of the macchia biotope, before pooling by vegetation cover, both the richness and abundance were least in those collected from bare soil. Studies on the protective effect of vegetation cover in Mediterranean shrubland on erosion (Andreu et al., 1998) show that bare soil has the lowest structural stability and organic matter contents. In our samples, Peltier et al. (2001) showed that the bare soil samples contain the least amount of fauna-processed litter and have the greatest mineral contents. Also, the diversity of macromorphological units is least for these points (Jordana et al., 2000). Maturity indexes followed the same pattern as the abundance profile. MI (without phytophagous families) and MI (for all trophic groups) encompass both sides of the central (ecotone) biotope. The PPI index behaved in the opposite fashion, as predicted by Bongers (1990). However, we did not find the difference between the two indexes that Yeates (1994) proposed: the inclusion of low c–p value populations in the latter index did not dilute the high c–p values of the dorylaimids. We did find that the ecotone areas had higher MI values than the pine stand, which agreed with results from Sohlenius (1997) in that these areas were more mature than the pine stand or the shrubland. This did not agree with other studies, such as Vinciguerra et al. (1995) on P. halepensis, which showed a higher maturity on the pine stand; however, these data are for higher MI values than ours, more in the range that Armendariz et al. (1996) and Sohlenius (1997) have found for other pine types. It should be noted that the structure of MI is sensitive to the presence of certain colonizing genera, which artificially pushes up the index value. Thus, a similar index may indicate a quite different degree of maturity, depending on the abundance of these particular species: note, for instance, that on bare soil samples in our study the value of MI for bare soil depends heavily on one abundant genus. Literature consensus on the hypothetically greater diversity values in ecotones, as measured by the
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Shannon index, does not exist for nematodes, although some data would support the hypothesis (Vinciguerra et al., 1995, found greater diversity in the ecotone than in adjacent areas for nematodes). Rusek (1992) pointed out that, although this general tendency may exist, some ecotones seem to be very heterogeneous for this parameter. Some meso-ecotones showed persistently low diversity values for epigeous collembola (Rusek, 1992). It has also been reported that the diversity peak can migrate between the ecotone proper and contiguous biotopes during the year, probably due to variable intensity of the border effect: Hanel (1993) found that for meadow ecotones the diversity peaks in the ecotone in March and in the meadow in May. Our data does not support any definite hypothesis, since virtually all diversity data are very similar along the transects. However, these diversity values are formed from different nematode communities. The ecotone community included predatory species, such as C. parvus and P. muscorum, that imply a higher degree of ecological structure and, possibly, a more complex trophic web. Also, the ecotone biotope was home for several dorylaimid species that are persistent but particularly sensitive to habitat alteration (Bongers, 1990). The macchia, or shrubland, also included specific communities (A. gienense, D. egmonti, X. ingens, P. projectus or Tylenchus elegans); some of these appeared to merge and influence the ecotone communities, possibly through the observed border effect (C. rosmarini, Pseudacrobeles sp. and Filenchus vulgaris). Finally, we found exclusive species within the pine stand (A. assamensis, A. granulosus or G. australis). Jordana et al. (1987) did not find any exclusive species for this same biotope. Although our data seem to refer to the macchia biotope as a single biotope, this is actually a mosaic of several sub-biotopes. Jordana et al. (1987) showed that, in arid Mediterranean biotopes, fauna concentrate under the arbustive pillows. Freckman and Mankau (1986) also observed abundance maxima directly under desert shrubs. We found that the area under the Rosmarinus canopy is particularly abundant for nematodes within the open shrubland. This shrub also sheltered some exclusive, high c–p species, such as A. gienense or D. egmonti). The isolated pines in the macchia also have an almost exclusive species (X. ingens). The bare soil, in all cases, is the poorest sub-biotope
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and, therefore, the one most prone to erosion and degradation.
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