SOIL MACROFAUNA OF TWO SUCCESSIONAL EVERGREEN CLOUD FOREST STAGES FROM THE CERRO HUITEPEC NATURE RESERVE, SAN CRISTÓBAL DE LAS CASAS, CHIAPAS, MÉXICO

Alejandro Morón-Ríos and Esperanza Huerta-Lwanga

Alejandro Morón-Ríos. Biologist. Ph.D. in Ecology, Instituto de Ecología, Universidad Nacional Autónoma de México. Researcher, El Colegio de la Frontera Sur, (ECOSUR). Address: ECOSUR, Unidad Campeche, Calle 10X61 #264, Col. Centro. CP 24000 Campeche, México. e-mail: amoron@camp.ecosur.mx

Esperanza Huerta-Lwanga. Biologist. Ph.D. in Ecology, Université Paris VI, France. Researcher, ECOSUR, Unidad Villahermosa, México. e-mail: ehuerta@vhs.ecosur.mx

SUMMARY

The soil macrofauna composition was studied in two successional evergreen cloud forest stages. One of them had an intensive forestal usage 17 years ago; and it has a canopy height <8m and densities from 900 to 1200 trees >5cm DBH. The other one was a non managed area, with a canopy of 30-35m and densities ranging from 1600 to 1800 trees >5cm DBH. The Chilopoda, Oligochaeta and Diplopoda groups constituted 70% of the total macrofauna from the two environments. The Endogeic Oligochaeta was the most abundant group in both types of forest. Oligochaeta were 54% of total decomposers in the mature forest and their density was significantly greater than the immature forest. The Oligochaeta density decrease was related with a lower canopy closure, increase in soil temperature and decreased level of soil humidity. This one-year sampling suggests that there are few negative impacts on the soil macrofauna associated with forest use for charcoal production 17 years ago.

MACROFAUNA DEL SUELO DE DOS ESTADOS SUCESIONALES DEL BOSQUE MESÓFILO DE LA RESERVA BIOLÓGICA CERRO HUITEPEC, SAN CRISTÓBAL DE LAS CASAS, CHIAPAS, MÉXICO

RESUMEN

Se estudió la composición de la macrofauna del suelo en dos estados sucesionales del bosque mesófilo. Uno es un bosque que tuvo uso forestal hace 17 años con un dosel <8m, densidades entre 900 y 1200 árboles con DAP >5cm; el otro es un bosque no manejado con un dosel entre 30 y 35m con densidades de 1600 a 1800 árboles con DAP >5cm. Chilopoda, Oligochaeta y Diplopoda constituyeron el 70% del total de la macrofauna en ambos ambientes. Los Oligochaeta endógeos fueron el grupo más abundante en ambos tipos de bosque, representando 54% del total de degradadores en el bosque maduro y su densidad fue significativamente mayor en comparación con el bosque incipiente. La disminución en la densidad de Oligochaeta se relacionó con menor cobertura del dosel, aumento en la temperatura del suelo y disminución en su humedad. El año de muestreos sugiere que después de 17 años desde que fue cortado el bosque, hay pocos impactos negativos sobre la macrofauna del suelo asociados al uso del bosque para la producción de carbón.

MACROFAUNA DO SOLO DE DOIS ESTADOS SUCESSIONAIS DO BOSQUE MESÓFILO DA RESERVA BIOLÓGICA CERRO HUITEPEC, SAN CRISTÓBAL DE LAS CASAS, CHIAPAS, MÉXICO

RESUMO

Estudou-se a composição da macrofauna do solo em dois estados sucessionais do bosque mesófilo. Um deles é um bosque que teve uso florestal há 17 anos com um dossel <8m, densidades entre 900 e 1200 árvores com DAP >5cm; o outro é um bosque não manejado com um dossel entre 30 e 35m com densidades de 1600 a 1800 árvores com DAP >5cm. Chilopoda, Oligochaeta e Diplopoda constituiram 70% do total da macrofauna em ambos ambientes. Os Oligochaeta endógenos foram o grupo mais abundante em ambos tipos de bosque, representando 54% do total de degradadores no bosque maduro e sua densidade foi significativamente maior em comparação com o bosque incipiente. A diminuição na densidade de Oligochaeta se relacionou com menor cobertura do dossel, aumento na temperatura do solo e diminuição na sua umidade. O ano de amostragens sugere que depois de 17 anos de ter sido cortado o bosque, há poucos impactos negativos sobre a macrofauna do solo associados ao uso do bosque para a produção de carvão.

KEYWORDS / Chilopoda / Coleoptera / Diplopoda / Formicidae / Forest Management / Oligochaeta / Trophic Groups /

Received: 03/20/2006. Modified: 07/18/2006. Accepted: 07/21/2006.

Introduction

Human pressure on forest resources has generated wide areas of forest in different successional stages. Therefore, the forest abiotic environmental factors, like temperature, humidity and light conditions, have changed. These changes could subsequently affect soil fauna that is a fundamental component of soil processes. The forest function depends greatly upon these processes.

Soil microorganisms and soil fauna largely regulate soil processes such as decomposition of organic materials and mineralization of nutrients (Coleman et al., 1983; Verhoef and Brussard, 1990). So, factors affecting activity and survival of soil biota should influence these processes, which, in turn, have the potential to impact not only tree growth but also the functioning of the entire forest ecosystem (Bengtsson et al., 1996).

Forest management leads to changes in composition and abundance of organic matter for soil fauna (Seastedt and Crossley, 1980; Marshall, 2000). In general, it modifies light penetration, temperature and humidity at soil level, as a consequence of decreased canopy closure, affecting soil biota (Setälä et al., 2000; Uhia and Briones, 2002; Martius et al., 2004).

In areas of evergreen cloud forests of Mexico, oak trees are commonly cut for wood fuel and charcoal production. The logged trees frequently sprout and are again used for wood fuel some years later (Ochoa-Gaona and González-Espinosa, 2000). This forest practice produces little alteration of the forest soil organic layer, but in the short-term, it generates an open canopy and an increase of litter input from the harvested plant residues and the dead root system.

In the long term, the soil macrofauna community response to these environmental changes promoted by logging could be a change in groups of decomposers.

Herein, the following question is addressed: What is the soil macrofauna composition in a logged evergreen cloud forest in comparison with a non logged one, and how does their density fluctuate throughout the year?

Study area

The study site was located in the Cerro Huitepec Nature Reserve (CHNR), 92º45'W and 16º20'N, in the municipality of San Cristóbal de las Casas, Chiapas, México. Altitude fluctuates between 2230 and 2700masl. Mean annual precipitation is 1056mm and mean annual temperature is 14.7ºC (average of 20 years from La Cabaña climatological station, located 2km away from the study site). Climate is subhumid temperate with abundant rains in summer (Ramírez-Marcial et al., 1998). Soils have a pH between 5.2 and 5.5, 5.1-5.3% C, 0.4-0.6% N, and ECC from 33 to 37cmol·kg^-1 (Luna-Cozar, 2005). They have sand-lime texture, reddish brown to deep brown colors, reduced depth (<50cm) and are classified as vertic and gleyic cambisols (Mera-Ovando, 1989).

Two successional stages of the evergreen cloud forest were selected to answer the question posed: an area that had an intensive forestry usage 17 years ago, named "early" forest (EF), and an area of mature forest (MF). The following site description is based on Gonzales-Espinosa et al. (1997) and Ramírez-Marcial et al. (1998). These authors reported 119 vegetal species in the EF. This EF community shows a discontinuous canopy of low height (<8m), dominated by individuals of Quercus spp. and densities of 900-1200 trees >5cm DBH. The major part of these trees developed from sprouts of trunks ~20cm in diameter. The canopy closure is 11%; the light reaching the soil averages 360µmol·m^-2·seg^-1 and the mean litter layer depth is 5 ±0.97cm (n=50). This EF is located in the low part of CHNR, at 2350masl.

The same authors registered 125 vegetal species in the MF. In this site the canopy is between 30-35m with emergent individuals of Quercus laurina Humb. & Bonpl. and Q. crassifolia Humb. & Bonpl. and densities of 1600-1800 trees >5cm DBH. Other arboreal species are intermingled between 20-25m of height forming a kind of second canopy. In this MF there is a low penetration of light to the soil, of 31µmol·m^-2·seg^-1, the canopy closure is 48% and the mean litter layer depth is 9 ±2.3cm (n=50). This mature vegetal community is located at 2475masl.

Material and Methods

Sampling

The sampled area in each forest condition was 1ha (100×100m). The soil macrofauna community was sampled during 11 months between August 1997 and August 1998. Every month, 10 soil samples consisting of 30×30×30cm blocks were randomly taken from each forest condition. The soil macrofauna was hand sorted, fixed in a Pampel solution and preserved in 70% ethanol (Morón and Terrón, 1988). The specimens collected were identified to class, order or family levels, and the number of individuals of each taxon was recorded. All taxa were assigned to a given trophic group.

Data analysis

The analysis unit of this study was the forest condition. This means that data corresponding to every sampled month in each forest condition (i.e. data from 10 soil blocks) were pooled together before the analysis to render 22 samples. The abundance data of the dominant macroinvertebrate taxa were analyzed with a repeated measure ANOVA using SPSS v.10.0 to discard the effects of time on the density of dominant taxa. The effects of forest condition were tested using one way ANOVA, considering the monthly data as repetitions. Each taxon was taken as an independent variable. The two forest conditions, MF and EF, were the fixed factor. Data were log transformed to satisfy the ANOVA assumptions.

Results

A total of 2006 specimens from 19 taxa were collected, 986 from EF and 1020 from MF (Table I). In MF, Chilopoda, Oligochaeta and Diplopoda were the dominant groups; all together; they constituted 70% of the total specimens. In EF, Chilopoda, Oligochaeta, Diptera and Formicidae were the dominant groups; they were ~70% of the total macroinvertebrates in this environment (Table I). Figures 1 and 2 describe the density fluctuation of the dominant taxa and the trophic groups. They show that the highest density was found between September and November in both forest conditions. The most abundant trophic groups were decomposers and predators at both study sites. Oligochaeta constituted 35% of the total decomposers in EF, and 54% in MF. In MF this taxa had twice the abundance it had in EF (Table I). Endogeic Oligochaeta was the most abundant group in both forest conditions throughout the year. In the case of predators, Chilopoda represented more than 80% of total specimens from this trophic group in the two environments. Geophilomorpha was the most abundant order of Chilopoda in EF and MF (Table I).

Repeated measure ANOVA did not show significant differences between months for any of the dominant taxa (Table II). One way ANOVA showed Oligochaeta were significantly more abundant in MF than in EF; the remaining dominant taxa did not show significant differences between forest conditions (Table III).

Discussion

The soil macrofauna from mature (MF) and early (EF) successional phases derived from an intensive managed evergreen cloud forest was analyzed. Predators and decomposers were the most abundant trophic groups. From the last group, Oligochaeta were significantly more abundant in MF.

Other studies showed these taxa to be sensitive to a series of hierarchical organized factors: the higher hierarchical level is temperature, followed by edaphic (nutrient status) and environmental (seasonality) factors (Fragoso and Lavelle, 1992). Kalisz and Powell (2000) reported a larger density of Oligochaeta in sites with low and protected slopes in the deciduous forest of Kentucky. In general, an Oligochaeta density increase has been related to agricultural practices or environmental conditions that decrease evaporation and increase or maintain soil humidity (Wardle et al., 1995; Wilson-Rummenie et al., 1999; Vázquez et al., 2003). Also, a larger availability of carbon sources increases the densities of this taxon (Scheu and Schaefer, 1998). Dominance of endogeic Oligochaeta has been related to soil nutrient quality (Muys et al., 1992) and precipitation (Fragoso and Lavelle, 1992).

A very low penetration of light to the soil and a high atmospheric humidity in the understory are the environmental conditions in MF. In this forest there is a more complex vegetation structure and a higher litter production than in secondary forests (Ramírez-Marcial et al., 1998; Nadkarnia et al., 2004). The conjunction of these conditions avoids the loss of soil humidity (Challenger, 1998; Martius et al., 2004). On the contrary, the forest environmental conditions in the early successional phase cause humidity loss and a higher temperature in the soil. Also, there is simplification of vegetation structure and lower litter production (Bruijnzeel and Veneklaas, 1998; Romero-Nájera, 2000; Ramírez-Marcial, 2002; Martius et al., 2004).

The density and proportion of Oligochaeta groups in the studied environments were between the reported ranges for other Mexican evergreen cloud forests (Fragoso, 2001). However, the density of Oligochaeta and Chilopoda is low as compared with other ecosystems (Table IV). A possible explanation could be related to the relatively low temperatures recorded (15-18ºC) in the evergreen cloud forest soil environment (Challenger, 1998; Ramírez-Marcial, 2002) when compared with a more tropical one (23-25ºC).

Chilopoda are generalist predators feeding on mesofauna and macrofauna (Hopkin and Read, 1992; Scheu and Schaefer, 1998). This group was the dominant predator at the studied environments and their densities were not significantly affected by forest management. This arthropod group may have high densities in early successional phases of beech forests in which there is no extreme fluctuation on soil humidity and temperature because of a high vegetal cover (Grgic and Kos, 2005).

Formicidae and Diptera showed high and variable densities, mainly in EF. The data for these taxa of insects suggest a strong aggregation pattern of spatial distribution, but only their presence is described in the present study.

After 17 years of forest cutting, the soil macrofauna density and the composition did not show significant differences with a non managed site. Only the Oligochaeta density was altered. The reductions in the density of this group, especially in endogeic Oligochaeta, could slow down the organic matter decomposition rates and the nutrient cycle.

The described evergreen cloud forest management opened the forest canopy after the first years of cutting, but it produced little changes in the forest soil organic layer and, later, a low impact on the structure and composition of the soil macrofauna community, as has been suggested by Lal (1988) and Setälä et al. (2000).

Acknowledgements

The authors thank Manuel Girón-Intzin for field work and help with specimen separation at the laboratory, R. Domínguez (PRONATURA - Chiapas) for allowing access to the CHNR. Financial support was obtained through subsidies of the Mexican Federal Government (1997-1998) to El Colegio de la Frontera Sur.

References

1. Bengtsson J, Setälä H, Zheng DW (1996) Food webs and nutrient cycling in soils: interactions and positive feedbacks. In Polis GA, Winemiller KO (Eds) Food Webs: Integration of patterns and dynamics. Chapman & Hall. New York, NY, USA. pp. 30 -38.        [ Links ]

2. Bruijnzeel LA, Veneklaas JE (1998) Climatic conditions and tropical montane forest productivity: the fog has not lifted yet. Ecology 79: 3-9.        [ Links ]

3. Challenger A (1998) Utilización y conservación de los ecosistemas terrestres de México. Pasado, presente y futuro. CONABIO/ Instituto de Biología, UNAM/ Sierra Madre. México. 847 pp.        [ Links ]

4. Coleman DC, Reid CPP, Cole CV (1983) Biological strategies of nutrient cycling in soil systems. Adv. Ecol. Res. 13: 1-55.        [ Links ]

5. Fragoso C (2001) Las lombrices de tierra de México (Annelida, Oligochaeta): diversidad, ecología y manejo. Acta Zool. Mex. Número especial 1: 131-171.        [ Links ]

6. Fragoso C, Lavelle P (1992) Earthworm communities of tropical rain forests. Soil Biol. Biochem. 24: 1397-1408.        [ Links ]

7. González-Espinosa M, Ochoa-Gaona S, Ramírez-Marcial N, Quintana-Ascencio P (1997) Contexto vegetacional y florístico de la agricultura. En Parra-Vázquez M, Díaz-Hernández B (Eds.) Los Altos de Chiapas: agricultura y crisis rural. Tomo I. Los recursos naturales. ECOSUR. México. pp. 85-118.        [ Links ]

8. Grgic T, Kos I (2005) Influence of forest development phase on centipede diversity in managed beech forest in Slovenia. Biodiv. Cons. 14: 1841-1862.        [ Links ]

9. Hopkin, S, Read, H (1992) The biology of millipedes. Oxford University Press. New York, NY, USA. 233 pp.        [ Links ]

10. Kalisz PJ, Powell EJ (2000) Invertebrate macrofauna in soils under old growth and minimally disturbed second growth forests of the Appalachian mountains of Kentucky. Am. Midl. Nat. 144: 297-307.        [ Links ]

11. Lal R (1988) Effects of macrofauna on soil properties in tropical ecosystems. Agric. Ecosyst. Env. 24: 101-116.        [ Links ]

12. Lavelle PM, Kohlmann B (1984) Étude quantitative de la macro faune du sol dans une forêt tropicale humide du Mexique (Bonampak, Chiapas). Pedobiologia 27: 377-393.        [ Links ]

13. Lavelle P, Maury ME, Serrano V (1981) Estudio cuantitativo de la fauna del suelo de la región de Laguna Verde, Ver. Época de lluvias. In Reyes-Castillo P (Ed.) Estudios ecológicos en el trópico mexicano: Publicación Nº 6. Instituto de Ecología. México. pp. 65-100.        [ Links ]

14. Luna-Cozar J (2005) Distribución, abundancia y diversidad de Curculionidae (Insecta: Coleóptera) de hojarasca en la Reserva Huitepec, Chiapas, México. Tesis. ECOSUR, San Cristóbal de las Casas, Chiapas, México. 27 pp.        [ Links ]

15. Marshall, VG (2000) Impacts of forest harvesting on biological processes in northern forest soils. For. Ecol. Manag. 133: 43-60.        [ Links ]

16. Martius C, Hofer H, García BVM, Rombke J, Forster B, Hanagarth W (2004) Microclimate in agroforestry systems in central Amazonia: does canopy closure matter to soil organisms?. Agrofor. Syst. 60: 291-304.        [ Links ]

17. Mera-Ovando LM (1989) Condiciones naturales para la producción. In Parra-Vázquez MR (Ed.) El subdesarrollo agrícola en los Altos de Chiapas: Universidad Autónoma Chapingo. Chapingo, México. pp. 21-82.        [ Links ]

18. Morón MA, Terrón R (1988) Entomología Práctica. Publicación Nº 22. Instituto de Ecología. México. 504 pp.        [ Links ]

19. Muys B, Lust N, Granval P (1992) Effects of grassland aforestation with different tree species on earthworm communities, litter decomposition and nutrient status. Soil Biol. Biochem. 24: 1459-1466.        [ Links ]

20. Nadkarnia N, Schaefera D, Matelsona T, Solano R (2004) Biomass and nutrient pools of canopy and terrestrial components in a primary and a secondary montane cloud forest, Costa Rica. For. Ecol. Manag. 198: 223–236.        [ Links ]

21. Ochoa-Gaona S, González-Espinosa M (2000) Land use and deforestation in the highlands of Chiapas, México. Appl. Geogr. 20: 17-42.        [ Links ]

22. Ramírez-Marcial N (2002) Disturbio humano y la diversidad de árboles y arbustos del bosque mesófilo en las montañas del norte de Chiapas. Tesis. Instituto de Ecología. Xalapa de Enríquez, Veracruz, México. 158 pp.        [ Links ]

23. Ramírez-Marcial N, Ochoa-Gaona S, González-Espinosa M, Quintana-Ascencio P (1998) Análisis florístico y sucesional en la estación biológica Cerro Huitepec, Chiapas, México. Acta Bot. Mex. 44: 59-85.        [ Links ]

24. Romero-Nájera I (2000) Estructura y condiciones microambientales en bosques perturbados de los Altos de Chiapas, México. Tesis. Universidad Nacional Autónoma de México. 74 pp.        [ Links ]

25. Scheu S, Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone: manipulation of food resources. Ecology 79: 1573-1585.        [ Links ]

26. Seastedt TR, Crossley DA (1980) Microarthropod response following cable logging and clear cutting in the southern appalachians. Ecology 62: 126-135.        [ Links ]

27. Setälä H, Haimi J, Siira-Pietikäinen A (2000) Sensitivity of soil processes in northern forest soils: are management practices a threat? For. Ecol. Manag. 133: 5-11.        [ Links ]

28. Uhia E, Briones MJI (2002) Population dynamics and vertical distribution of enchytraeids and tardigrades in response to deforestation. Acta Oecol. 23: 349-359.        [ Links ]

29. Vázquez R, Stinner B, McCartney D (2003) Corn and weed residue decomposition in northeast Ohio organic and conventional dairy farms. Agric. Ecosyst. Env. 95: 559-565.        [ Links ]

30. Verhoef HA, Brussaard L (1990) Decomposition and nitrogen mineralization in nature and agroecosystems: the contributions of soil animals. Biogeochem. 11: 175-211.        [ Links ]

31. Wardle DA, Yeates G, Watson R, Nicholson K (1995) The detritus food-web and the diversity of soil fauna indicators of disturbance regimes in agro-ecosystems. Plant Soil 170: 35-43.        [ Links ]

32. Wilson-Rummenie A, Radford B, Robertson L, Simpson G , Bell K (1999) Reduced tillage increases population density of soil macrofauna in a semiarid environment in central Queensland. Env. Entomol. 8: 163-172.        [ Links ]