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Applied Soil Ecology 35 (2007) 340–355

Successional changes in soil, litter and macroinvertebrate

parameters following selective logging in a Mexican Cloud Forest

Simoneta Negrete-Yankelevich a,b,*, Carlos Fragoso b,Adrian C. Newton c, O. William Heal d

a School of Geosciences, University of Edinburgh, Crew Building, The King’s Buildings, West Mains Road, Edinburgh EH9 3JU, UKb Departamento de Biologıa de Suelos, Instituto de Ecologıa, A.C. Km. 25 Carretera Antigua a Coatepec, #351,

Congregacion El Haya, 91070 Xalapa, Veracruz, Mexicoc School of Conservation Sciences, Bournemouth University, Talbot Campus, Poole, Dorset BH12 5BB, UK

d Department of Biological Sciences, University of Durham, Durham DH1 3LE, UK

Received 19 October 2005; received in revised form 22 June 2006; accepted 24 July 2006

Abstract

The environmental and vegetation shifts associated with logging disturbance and secondary succession in Tropical Montane Cloud

Forests have been studied in detail, however little is known about the consequences that these changes have for the soil system. The

present study was undertaken to determine the impact of selective logging and subsequent secondary succession on soil micro-

environmental conditions, leaf litter quality and quantity, soil nutrient concentration and soil and litter macroinvertebrate community

composition. The study was carried out in three successional chronosequences, two recently logged sites and two pristine tropical

mountain cloud forest sites in Oaxaca, Mexico. Results showed that selective harvesting of Quercus spp. trees caused an increase in soil

temperature of ca. 4 8C that is not completely reversed after 100 years of succession. During 100 years of secondary succession litter

diversity increased and soil organic matter accumulated (16.4% increase in total C). The availability of cations (Ca, Mg, Na, and K) in

the topsoil decreased by more than 50% as a result of logging, and only Mg increased again between 75 and 100 years after disturbance.

Pristine cloud forests sustain a diverse litter and soil macroinvertebrate community, but its composition and diversity was

negatively affected by logging. The effect of Quercus harvesting activities on the litter community was apparent within 2 months of

disturbance (total abundance declined by ca. 65%, higher taxa richness by ca. 10% and diversity by ca. 35%). For the soil

community there was a time-lag in the effect of logging. Two months after disturbance there was no significant effect on the soil

community but 15 years after abandonment, total macroinvertebrate abundance in the soil was ca. 80% lower and higher taxa

richness ca. 30% lower compared to undisturbed sites. Full recovery of the macroinvertebrate community composition appeared to

take more than 100 years both in the litter and soil. Reduced abundances of Coleoptera and Enchytraeidae were apparent even after

100 years of succession. The endemic earthworm Ramiellona wilsoni was found almost exclusively in the pristine forests and

therefore its abundance could be used as a sensitive indicator of disturbance in these forests.

# 2006 Elsevier B.V. All rights reserved.

Keywords: Earthworms; Firewood extraction; Litter quality; Tropical montane forest; Soil macrofauna; Soil temperature

* Corresponding author at: Departamento de Biologıa de Suelos,

Instituto de Ecologıa, A.C. Km. 25 Carretera Antigua a Coatepec,

#351, Congregacion El Haya, 91070 Xalapa, Veracruz, Mexico.

Tel.: +52 55 228 842 18 50.

E-mail address: simoneta@ecologia.edu.mx

(S. Negrete-Yankelevich).

0929-1393/$ – see front matter # 2006 Elsevier B.V. All rights reserved.

doi:10.1016/j.apsoil.2006.07.006

1. Introduction

Tropical Mountain Cloud Forest (TMCF) is one of the

most endangered ecosystems of the world (Rzedowski,

1996; Bruijnzeel and Veneklaas, 1998). In many of these

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355 341

forests in Mexico, logging for firewood extraction is

chronic, typically involving selective harvesting of

Quercus spp. trees (Ramırez-Marcial et al., 2001).

Despite being the most floristically diverse forest in

Mexico, the TMCF is one of the least studied forest

ecosystems in the country (Ramırez-Marcial et al., 2001;

Velazquez et al., 2003) and very little is known about the

impact of accelerated logging disturbance on the below-

ground subsystem, either in Mexico or in TMCF

elsewhere.

It has been widely recognised that forest disturbance

can affect nutrient cycling (Nilsson et al., 1995; Finer

et al., 2003) and soil biota (Davies et al., 1999; Lavelle,

2000; Brown et al., 2001; Pietikainen et al., 2003).

Logging disturbance can have short- and long-term

impacts on the below-ground subsystem. In the short-

term (within a few months), harvested plant residues

produce an above-ground flush of nutrient-rich organic

matter (Olsson et al., 1996a,b; Finer et al., 2003) and a

below-ground litter input from dead rooting systems.

The impact of logging activities may be particularly

important in forests growing on poor soils such as the

TMCF. In these ecosystems, plants are adapted to use

nutrients efficiently, decomposition is slow and most

nutrients are sequestered in plant and microbial biomass

(Waide et al., 1998; Hobbie, 1992; Vitousek, 1984;

Bruijnzeel and Proctor, 1995; Tanner et al., 1998). The

sudden input of nutrient-rich residues together with the

increase in radiation reaching the soil may bring a

temporary increase in the rate of decomposition and

increase nutrient availability (Butterfield, 1999; Siira-

Pietikainen et al., 2001; Finer et al., 2003), particularly

in the topsoil where most plant–soil biochemical

interactions occur (Gross et al., 1995). Below-ground

food-web responses to logging are poorly understood

(Bengtsson et al., 1997; Wardle et al., 1998). However,

the rise in availability of nutrient-rich organic matter

may also decrease the proportion of fungal-based over

bacterial-based food-webs (Wardle, 1992; Siira-Pieti-

kainen et al., 2001) and produce major changes in

macroinvertebrate community composition.

In the long-term (tens of years) the effects of logging

often include a delayed response of the soil system to

initial disturbance (Bengtsson et al., 1997; Zaitsev et al.,

2002) or an indirect consequence of successional changes

in the vegetation community composition after abandon-

ment (Switzer and Shelton, 1979; Gross et al., 1995).

Although the environmental and vegetation shifts

associated with post-logging secondary succession in

TMCF have been studied in detail (Gonzalez-Espinosa

et al., 1991; Quintana-Ascencio and Gonzalez-Espinosa,

1993; Romero-Najera, 2000; Blanco-Macias, 2001;

Galindo-Jaimes et al., 2002), little is known about the

consequences of these long-term changes on nutrient

budgets and faunal communities below-ground. In

Mexico, tree species of Holarctic phytogeographic origin

(such as Pinus spp.) are often pioneers in logged TMCFs

and are known to be more productive than hardwoods of

tropical origin (Williams-Linera and Toledo, 1996),

therefore they could potentially increase the rate of the

decomposition process and enhance nutrient availability.

Furthermore, after disturbance and in early succession,

the diversity of tree species diminishes relative to older

forests (Ramırez-Marcial et al., 2001), leading to a

decline in the diversity of resources available to the soil

system. This, together with the greater abundance of

resources, might be expected to lead to a more uniform

and less diverse soil macroinvertebrate fauna.

This paper presents a study of the litter composition,

topsoil nutrient concentration and soil macroinverte-

brate fauna in two pristine and two recently logged sites

as well as three successional chronosequences (15 to

100-year-old forests) of TMCF in Oaxaca, Mexico. The

objectives of the study were:

i. T

o determine whether changes happening above-

ground as a result of logging and subsequent

secondary succession are coupled with changes in

microenvironmental conditions, litter quality and

quantity and soil nutrient concentration.

ii. T

o determine if the composition and diversity of the

higher taxa macroinvertebrate community reflect

these changes and can therefore serve as good

indicators of disturbance and degree of recovery of

the soil system.

2. Methods

2.1. Study sites

The research was carried out in an area known as El

Rincon (Villa Alta District), in the Sierra Norte of

Oaxaca, Mexico. The study sites were three secondary

successional chronosequences of Tropical Montane

Cloud Forest (TMCF) (Challenger, 1998) named here as

Tanetze, Juquila and Tarbis. Each of these chronose-

quences is formed by four sites of different successional

stage: approximately 15, 45, 75, and 100 years of age.

Additionally two un-logged forests (Pris and Pris II,

from here on named pristine) and two plots that were

selectively harvested for Quercus spp. trees 2 months

before sampling (Tar 0 and Tar 00) were examined. All

sites are located between 178180 and 178230N and

968150 and 968210W. The successional stages within

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355342

each chronosequence are a short distance from each

other (less than 2000 m). Study sties are situated in the

following altitudes: Juquila 1700–1975 m, Tanetze

1700–1860 m, Tarbis 1700–1975 m, Tar 0 and Tar 00

1975 m and Pris and Pris II 2100 m. The mean annual

precipitation at the nearest meteorological station

(�16 km from the area) is 1719 mm year�1. The mean

annual temperature ranges between 20 and 22 8C(Anonymous, 1999).

Among the distinctive species in the original TMCF

in the area are Billia hyppocastanum, Cinnamomum

zapatea, Oreopanax flaccidus, Podocarpus matudae,

Quercus laurina, Symplocos coccinae, Ternstroemia

oocarpa and Beilschmedia ovails (Cordova and del

Castillo, 2001; Bautista-Cruz and del Castillo, 2005).

The approximate age of the forests in each of the studied

chronosequences was identified by del Castillo (1996)

and Bautista-Cruz and del Castillo (2005), based on the

age of the oldest Pinus chiapensis trees. Selective

logging (as well as clearance) of pristine cloud forests in

Mexico leads to the rapid colonisation by pine species

(Challenger, 1998), which permits a relatively precise

determination of the time since the last major

disturbance by calculating the age of the oldest pine

trees.

2.2. Field methods

Sampling was conducted in 30 m � 30 m grids

(with 49 intersections every 5 m) established in each

successional stage of all chronosequences, and in

recently logged and pristine sites. First an intensive

survey was carried out in the Juquila chronosequence

between 11 July and 17 August 2000. In this period

all 49 intersections of each of the four grids (15-, 45-,

75- and 100-year-old forests) were sampled. The

following year, between 25 June and 3 December

2001, all of the successional stages of Tanetze and

Tarbis, recently logged sites (Tar 0 and Tar 00) and

the pristine sites (Pris and Pris II) were sampled. On

this occasion, only seven random vertices in each grid

were selected for sampling. Both of these field

seasons were included in the rainiest half of the year.

In order to preserve a balanced design, for compar-

isons including all chronosequences (Juquila, Tanetze

and Tarbis) and sites (Tar 0, Tar 00, Pris and Pris II),

only seven randomly selected samples were consid-

ered for each grid in the Juquila chronosequence. For

the detailed analysis performed exclusively in the

Juquila chronosequence (analysis of litter components

and soil nutrient content) all 49 samples were

considered.

In all of the field sites except Juquila, sampling at

each grid intersection consisted of the simultaneous

extraction of a soil monolith and the measurement of

microenvironmental conditions. In the Juquila chron-

osequence, microenvironmental conditions were mea-

sured in each successional stage on four different

sampling dates (11 and 18 July and 14 and 17 August

2000). The point measurements for each sampling

session were carried out within the same day and the

four repetitions for each sampling vertex were

averaged.

2.3. Soil microenvironment

Soil temperature, volumetric soil water content and

canopy cover (as a surrogate for solar radiation reaching

the soil) were considered as indicators of soil

microenvironmental conditions. For soil water content

and temperature a Delta-T-Theta Probe soil moisture

sensor attached to a Delta-T-HH1 meter (Delta-T

Devices Ltd., Cambridge, UK) and a Taylor soil digital

thermometer (model 9840; Taylor Precision Products

LP, Oak Brook, USA) were used, respectively. The final

calculation of volumetric soil water content was based

on a soil-specific calibration (Delta-T Devices Ltd.,

1999). Both the temperature and humidity sensor probes

were placed at a soil depth of 10 cm. Percent canopy

cover was measured with a Convex Spherical Crown

Densiometer (Forestry Suppliers Inc., Jackson, USA),

facing north and holding the densiometer at breast

height, above the sampling point.

2.4. Macroinvertebrate sampling

All monoliths were extracted with a box corer and

consisted of 25 cm � 25 cm � 5 cm depth of soil, plus

all the litter above it. The litter and soil sample was hand

sorted in situ for macroinvertebrates (defining macro-

invertebrates as all invertebrate animals larger than

2 mm in any of its dimensions). The macroinvertebrates

found in the monolith were preserved in 70% alcohol.

All macroinvertebrates collected were counted under

a dissecting microscope and classified into class, order

and groups of immature stages. Additionally all earth-

worms were identified to species following Fragoso and

Reynolds (1997). Although Enchytraeidae are currently

considered mesofauna, we have included this taxon in the

analysis because they were a particularly conspicuous

component of the faunal community and they have been

rarely studied in the temperate tropics (Rombke, 2003).

Two estimates of compositional diversity were calculated

for the macroinvertebrate community: the number of

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355 343

elements (macroinvertebrate taxa) and the Shannon–

Weiner index (Magurran, 1996).

2.5. Vegetation census

Within the boundaries of the Juquila sampling grids,

as well as in a 5 m width frame around them, we

recorded the genus and diameter at breast height (DBH)

of all the live trees (with a DBH > 5 cm). Assuming a

cylindrical shape, the basal area per genus and per

successional stage, was calculated.

2.6. Litter resource availability and quality

In the laboratory the litter and soil samples were

oven dried at 80 8C to constant mass. The dry mass of

the litter in each monolith was recorded. The litter of all

the monoliths extracted from the Juquila chronose-

quence was sorted into six components: Pinus needles,

Quercus leaves, Lauraceae leaves including the three

genera present in all chronosequences – Persea, Ocotea

and Beilschmedia – woody and reproductive material,

leaves from other genera and unrecognisable leaf

material. The dry mass of these components was

recorded separately.

Recently fallen leaves of P. chiapensis, Oreopanax

xalapensis, Beilschmedia ovalis and Quercus laurina

were collected from the forest floor at Juquila, dried to

constant mass and analysed for litter quality. Leaf litter

quality determination consisted of the following

analyses: (1) total C concentration using the loss on

ignition method (Jackson, 1958); (2) total N concentra-

tion with sulphuric acid digestion followed by distilla-

tion and titration (Anderson and Ingram, 1993); (3) total

P concentration using sulphuric acid digestion followed

by colorimetric determination (Anderson and Ingram,

1993); (4) cation concentrations (Ca2+, Mg2+, K+ and

Na+) using a digestion with HNO3 and HClO4 followed

by atomic absorption spectroscopy (Allan, 1971); (5)

lignin content with a sequential procedure of neutral

detergent fibre (NDF) and acid detergent fibre (ADF)

extractions followed by acid detergent lignin extraction

with 72% sulphuric acid (Van Soest, 1994).

2.7. Soil nutrients

All soil samples from the Juquila chronosequence

were analysed for: (1) total C using the loss on ignition

method to determine total organic matter and dividing

by 1.742 to calculate total carbon concentration

(Jackson, 1958), (2) total P concentration using

sulphuric acid digestion followed by colorimetric

determination (Anderson and Ingram, 1993) and (3)

exchangeable cations (Ca2+, Mg2+, K+ and Na+) with

the ammonium acetate extraction method at pH 7

(Anderson and Ingram, 1993). Additionally, 10 ran-

domly chosen samples from the 49 intersections of each

successional stage were analysed for total N with acid

digestion followed by distillation and titration (Ander-

son and Ingram, 1993).

2.8. Data analysis

For microenvironment, litter mass, taxa diversity

indices, the individual abundances of dominant macro-

invertebrate taxa (those with a minimum mean

abundance of 6 ind m�2 in the soil or litter) and total

macroinvertebrate abundances, ANOVAs were used to

determine significant differences among forest types

(primary, recently logged and secondary) and among

secondary forest stages (15-, 45-, 75- and 100-year-old

forests). The spatial arrangement of some of the study

areas in chronosequences and others in separate

recently logged and pristine sites did not permit a

single analysis of variance that would test the effect of

site and forest age simultaneously for all studied areas.

For this reason, we divided the analyses into the

following steps. First a one-way ANOVA was

performed to determine whether there were differences

among the pristine (n = 2), recently logged (n = 2) and

secondary forests (n = 3). For this analysis we used the

means of the site samples as replicates. The three

chronosequences (Juquila, Tarbis and Tanetze) were

then analysed with a two-way ANOVA to determine the

effect of chronosequence and forest age (four levels,

n = 3). Measurements within a single grid are in this

context pseudoreplicates (Hurlbert, 1984) and were

averaged and considered a single replicate.

All variations of ANOVA, tests of their assumptions

and the Tukey’s honest significant difference post hoc

test (HSD; Legendre and Legendre, 1998) were

performed using the software STATISTICA v.5.0

(Statsoft Inc., Tulsa).

Differences among the Juquila successional stages in

the mass per sample of litter components and the

chemical composition of soils were tested with one-way

multivariate analyses of variance (MANOVA) with age

as a four level factor. The 49 samples extracted from the

intersections of each of the Juquila grids were

considered as single replicates. When the MANOVA

turned out to be significant, corresponding one-way

ANOVAs for each individual variable were then

performed. Wilk’s l and P-values are reported when

appropriate. The differences in the nutrient and lignin

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355344

content among the litters of different tree species were

also tested with a one-way MANOVA. For this analysis

three replicates per leaf species were analysed. Each

replicate consisted of a 30 g sample of dry leaves

randomly drawn from the pool of leaves. If the

MANOVA was significant, the same procedure as

described above was followed.

MANOVA was only performed when the homo-

scedasticity (Box’s M-test) and multivariate normal

distribution assumptions were met. Multivariate nor-

mality was assumed to be achieved when all dependent

variables were themselves normally distributed (Kol-

mogorov–Smirnov test; Legendre and Legendre,

1998).

3. Results

3.1. Soil microenvironment

Recently logged sites had around 20% lower mean

canopy density than pristine sites and secondary forests,

Table 1

Means, coefficients of variation (in parentheses) and results of ANOVA fo

Among forest types

Forest type means

Primary Recent

Litter mass (g monolith�1) 68.1 (0.24) 67.4 (0

Soil temperature (8C) 11.9 (0.01) a 15.9 (0

Canopy cover (%) 94.7 (0.20) a 76.7 (0

Volume of soil water (cm3 cm�3) 0.2 (0.02) 0.2 (0

Soil taxa richness 10.6 (0.02) 10.1 (0

Soil taxa diversity (H0) 1.8 (0.03) 1.9 (0

Soil macroinvertebrate abundance 85.3 (0.38) 74.8 (0

Litter taxa richness 6.1 (0.15) a 10.1 (0

Litter taxa diversity (H0) 1.9 (0.02) a 1.4 (0

Litter macroinvertebrate abundance 16.8 (0.33) a 43.2 (<

Within secondary succession compa

Means per successional stage

15-Year-old 45-Year-old 7

Litter mass (g monolith�1) 83.3 (0.20) 95.9 (0.10) 1

Soil temperature (8C) 14.4 (0.02) a 13.6 (0.02) b

Canopy cover (%) 94.4 (0.02) 93.7 (0.01)

Volume of soil water (cm3 cm�3) 0.2 (0.36) 0.2 (0.36)

Soil taxa richness 7.0 (0.21) a 7.5 (0.33) ab

Soil taxa diversity (H0) 1.7 (0.17) 1.7 (0.14)

Soil macroinvertebrate abundance 16.6 (0.42) a 28.7 (0.76) ab

Litter taxa richness 6.9 (0.25) 7.8 (0.19)

Litter taxa diversity (H0) 1.7 (0.19) 1.8 (0.12)

Litter macroinvertebrate abundance 15.1 (0.33) 19.9 (0.45)

The first ANOVA compares forest types (pristine, recently logged and second

(15-, 45-, 75- and 100-year-old forests). Different letters denote significant

but there were no differences among secondary forests

of different age (Table 1). Mean soil temperature was

lowest in pristine sites (11.9 8C) and reached the

greatest value in recently logged sites (15.9 8C). Within

secondary chronosequences, 15-year-old forests had a

slightly higher soil temperature than other successional

stages (Table 1). High variability in volumetric soil

water content and no significant differences were found

among forest types or secondary successional stages

(Table 1).

3.2. Litter resource availability and quality

The number of tree genera (DBH > 5 cm) present in

each of the sampling grids of the Juquila chronose-

quence was 20 in the 15-year-old, 22 in the 45-year-old,

20 in the 75-year-old and 23 in the 100-year-old forests.

The lowest total basal area was found in the 100-year-

old forest (42 m2 ha�1) and the 15-year-old forest

(44 m2 ha�1). The greatest value of basal area was

recorded in the 45-year-old forest (84 m2 ha�1).

r various forest type parameters

ANOVA

Forest type effect

ly logged Secondary F(2,4) P

.19) 91.8 (0.08) 3.63 0.126

.02) b 14.4 (<0.01) ab 20.28 0.018

.38) b 93.5 (0.35) a 161.62 <0.001

.17) 0.2 (0.02) 0.77 0.520

.01) 9.3 (0.15) 3.58 0.128

.05) 1.9 (0.06) 0.53 0.625

.42) 37.9 (0.27) 3.1 0.154

.07) b 8.9 (<0.01) b 16.58 0.012

.02) b 1.7 (0.05) a 23.84 0.0060.01) b 27.2 (0.40) b 7.91 0.041

rison ANOVA

Age effect Chronose-

quence effect

5-Year-old 100-Year-old F(3,6) P F(2,6) P

03.0 (0.14) 85.1 (0.19) 1.26 0.370 1.06 0.404

13.7 (0.02) b 13.8 (0.02) b 23.81 0.014 191.36 0.00192.9 (0.02) 93.2 (0.01) 0.14 0.931 0.30 0.755

0.2 (0.31) 0.2 (0.53) 0.26 0.853 12.79 0.00711.1 (0.12) ab 10.8 (0.07) b 5.34 0.039 5.73 0.041

2.0 (0.07) 1.9 (0.03) 0.82 0.529 1.46 0.304

52.6 (0.16) ab 54.9 (0.08) b 11.32 0.007 5.46 0.0458.7 (0.06) 9.1 (0.04) 0.35 0.79 1.00 0.421

1.9 (0.05) 1.9 (0.07) 0.21 0.889 0.72 0.527

23.9 (0.23) 26.6 (0.63) 2.3 0.174 4.9 0.054

ary) and the second compares successional stages of secondary forests

differences by Tukey’s HSD paired comparisons.

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355 345

The tree genera that dominated the basal area were

different in each successional stage. In early succes-

sional plots, there was a single genus that covered

around 40% of the total basal area recorded for the plot.

In the 15-year-old forest the dominant genus was

Clethra (38.4% of the total basal area) followed by

Pinus (15.7%); while in the 45-year-old forest Quercus

dominated (40.46%) followed again by Pinus (8.7%). In

later successional stages, the basal area was shared

among more genera. In the 75-year-old forest the three

most dominant genera were Quercus (26.04%),

Vaccinium (11.56%) and Temstroemia (11.04%) while

in the 100-year-old forest the three genera that

accounted for most basal area were Quetzalia

(19.05%), Persea (17.5%) and Oreopanax (15.09%).

There were no differences among forest types or

successional stages in terms of the total litter biomass

per monolith (Table 1). However, there were significant

differences among successional stages in the composi-

tion of the litter (Table 2). The 45- and 75-year-old

successional stages had more total unidentifiable

material than the 15- or 100-year-old forest. Leaves

that were recognisable formed the greatest proportion in

the 45-year-old forest (41%) and the lowest in the 100-

year-old forest (27%).

The leaves of the three taxa that were identified in the

litter (Quercus, Pinus and Lauraceae including Persea,

Belishcmiedia and Ocotea) comprised between 55 and

90% of the recognisable leaves and between 18 and

23% of the total litter mass in each successional stage.

The contribution of leaves from the dominant tree

genera to the standing biomass of leaf litter was not

Table 2

Results of one-way MANOVA for litter composition in the Juquila chronos

ANOVA comparing successional stages

Manova

Effect Fo

Wilks’ l 0.2

Rao’s R 22.

Degrees of freedom effect 18

Degrees of freedom error 529

P-value 0.0

Litter components Mean biomass per successional stage (g m�2)

15-Year-old 45-Year-old 75

Unidentifiable 94.2 144.6 18

Lauraceae 0.1 0.2

Pinus spp. 71.7 57.5

Quercus spp. 1.1 73.0 8

other species 60.3 15.2 2

w&r 95.1 124.8 11

w&r: woody and reproductive material.

proportional to their dominance in terms of basal area.

While Pinus only constituted circa 16% of the total

basal area in the 15-year-old forest, pine needles formed

the highest proportion (53.8%) of the recognisable

leaves in this plot. Independently of the basal area

dominance, oak leaves were the most abundant

recognisable leaf litter in the other three successional

stages (49.9–75.6%). Pine trees covered circa 9% of the

basal area in the 45-year-old forest and their needles

were the second-most abundant component in the litter

(39.4%). Pine trees and needles were absent from the

100-year-old forest. The leaves of other genera

constituted only 40.4% of the recognisable leaf litter

in the 100-year-old forest even if their basal area

reached 70% of the total. The presence of Lauraceae

leaves was negligible in the 15, 45 and 75 years

successional stages (0.05–0.7%).

Some of the main leaf components of the litter in

Juquila (Pinus, Quercus, Beilschmedia and Oreopanax)

differed significantly in their nutrient and lignin content

(Fig. 1). For example the mean concentration of

magnesium was lowest in Pinus needles (5.24 cmol

kg�1) and greatest in Oreopanax (35.05 cmol kg�1)

while phosphorus concentration was greatest in

Pinus (2.43 cmol kg�1) and lowest in Quercus

(0.95 cmol kg�1). Lignin content was greatest in

Beilschmedia (44.6%) and lowest in Oreopanax (29.2%).

3.3. Soil nutrients

All soil nutrients analysed differed significantly

among successional stages of the Juquila chronosequence

equence, mean biomass of individual litter components and results of

rest age

05

088

01

ANOVA for litter

components

-Year-old 100-Year-old F(3,192) P-value

9.0 92.4 13.80 <0.0010.9 5.8 40.32 <0.0012.9 0.0 26.01 <0.0017.2 50.8 51.30 <0.0014.4 38.3 15.35 <0.0017.9 122.6 1.58 0.20

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355346

Fig. 1. Nutrient concentrations in the senescent leaves of four tree

species (n = 3). (a) Total carbon and lignin, (b) total phosphorus and

(c) magnesium and potassium. Wilk’s l < 0.0001 (P < 0.001). Dif-

ferent letters indicate significant differences (P < 0.05) in paired

comparisons between leaf species with Tukey’s HSD test.

(Wilk’s l = 0.14, P < 0.001). The total concentration of

carbon was lower in the earliest successional stage

(35.4%) compared to the 45-, 75- and 100-year-old

forests (48.7–51.8%; F (3,192) = 44.87, P < 0.001; Fig. 2).

Total soil nitrogen concentration increased along the

successional chronosequence (F (3,44) = 4.08, P = 0.01),

from a mean of 1.2% in the 15-year-old forest to a mean

of 1.8% in the 100-year-old forest. In the case of

phosphorus the 45- and 75-year-old forest had the

highest and lowest values, respectively (0.51 and

0.26 cmol kg�1; F (3,192) = 2.69, P = 0.05). The values

for magnesium were similar (means between 3.55 and

4.30 cmol kg�1) for all forests except for the 75-year-

old which had a significantly lower concentration (ca.

1.7 cmol kg�1; F (3,192) = 22.02, P < 0.001). The con-

centrations of sodium and potassium decreased more or

less steadily along the successional sequence

(F (3,192) = 49.75 and 26.84, respectively, P-values

<0.001). Similarly the concentration of calcium

decreases with succession up to the 75-year-old forest,

however it increased again in the 100-year-old forest

(F (3,192) = �29.09, P < 0.001; Fig. 2).

3.4. Macroinvertebrate community

Most macroinvertebrates collected in the survey

(65.7%) were found in the soil and consequently,

individual taxa often occurred in greater numbers in the

soil than in the litter. The most abundant taxa were

Enchytraeidae (18.1%), Formicidae (16.3%) and

Coleoptera (adults, 12.0%) in the soil and Coleoptera

(adults, 19.7%), Diplopoda (13.3%) and Formicidae

(9.9%) in the litter. Four taxa were relatively rare:

Dermaptera (2 individuals), Thysanura (8 individuals),

Uropygi (10 individuals) arid Blattaria (11 individuals)

(see Appendix 1 for individual abundances). Seven

macroinvertebrate taxa or immature groups (Chilopoda,

Coleoptera, Coleoptera larvae, Diplopoda, Diptera

larvae, Enchytraeidae and Formicidae) were considered

dominant because they had a minimum total mean

abundance of 6 ind/m2 in the litter or soil. The

abundances of these dominant taxa were analysed

individually (Table 3).

Total macroinvertebrate abundance, taxa richness,

Shannon’s diversity index and the individual mean

abundances of Chilopoda and Coleoptera larvae were

lower in the litter of recently logged sites than in pristine

sites (Fig. 3). In contrast, in the soil community, the

minimum values of all diversity variables and individual

abundances that were sensitive to disturbance were

reached in the 15-year-old forests, where total macro-

invertebrate abundance was ca. 80% lower and taxa

richness ca. 30% lower than in pristine sites. The

abundance of Enchytraeidae was ca. 94% lower and of

Coleoptera ca. 65% lower compared to undisturbed

sites (Fig. 3b and c).

Several diversity and abundance variables in the litter

and soil communities did not recover to the level of

pristine forests after 100 years of succession. This was the

case for richness and total abundance of litter taxa (both

ca. 25% lower in the 100-year-old forests), abundance of

litter Coleoptera larvae (44% lower) and abundance of

soil Enchytraeidae (56% lower). The total abundance and

taxa richness of soil macroinvertebrates increased with

succession but only taxa richness reached the level of

pristine sites in the 100-year-old forests. In contrast,

Shannon’s diversity and the abundance of Chilopoda in

the litter had already recovered close to pristine levels in

the 45-year-old forests (Fig. 3a and c).

A total of 60 earthworms (Order Lumbricina) were

found in the survey. All of them were identified as

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355 347

Fig. 2. Nutrient concentrations in the soils of the successional stages of the Juquila chronosequence. n = 49 for each successional stage except for

nitrogen where n = 10.

Ramiellona wilsoni (Annelida, Acanthodrilidae), a

small litter dwelling species that is thought to be

endemic to Oaxaca (Fragoso and Reynolds, 1997). All

R. wilsoni specimens were found in the pristine forests

except for six (one in the Tanetze 15-year-old forest, one

Table 3

ANOVA for dominant macroinvertebrate taxa (defined as those with mean

Among forest types W

Forest type effect A

F(2,4) P F

Litter macroinvertebrates

Chilopoda 14.11 0.015Coleoptera 0.44 0.672 7

Coleoptera larvae 7.51 0.044Diplopoda 1.69 0.295

Diptera larvae 5.42 0.073

Enchytraeidae 1.69 0.294

Formicidae 0.70 0.550

Soil macroinvertebrates

Chilopoda 0.89 0.479

Coleoptera 1.11 0.415 4

Coleoptera larvae 2.93 0.165

Diplopoda 1.48 0.331

Diptera larvae 1.66 0.299

Enchytraeidae 21.98 0.007Formicidae 2.40 0.206

The forest types were pristine, recently logged and secondary and successi

in the Juquila 45-year-old forest and four in a single

sample of the Tarbis 45-year-old forest). All individuals

were found in the soil except for three that were found in

the litter of the Pris II site. Out of the 14 soil samples

extracted from the pristine forests only four did not

abundance equal to or greater than 6 ind m�2)

ithin secondary succession

ge effect Chronosequence effect

(3,4) P F(2,4) P

0.27 0.843 0.34 0.728

3.63 <0.001 9.03 0.0162.20 0.189 2.11 0.202

0.14 0.929 0.51 0.622

0.64 0.617 0.73 0.522

0.05 0.982 1.79 0.246

0.99 0.460 1.66 0.266

4.19 0.064 1.91 0.228

2.34 <0.001 36.47 <0.0010.68 0.595 1.40 0.317

2.20 0.189 0.12 0.890

0.78 0.546 0.42 0.673

3.25 0.102 4.33 0.069

2.56 0.151 2.30 0.182

onal stages were 15-, 45-, 75- and 100-year-old forests.

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355348

Fig. 3. Mean abundances, diversity and richness (�S.E.) of pristine (n = 2), recently logged (n = 2) and secondary successional forests (n = 3).

Values are presented as proportions of mean pristine values in (a) and (b) (for original mean values see Table 1); mean population densities are given

in (c) and (d). Only those variables that showed significant differences among forest types or secondary successional stages are presented. P

represents the values for pristine forest and the arrow indicates the time of disturbance when forest age equals zero.

contain earthworms. Samples from the site named Pris

had a mean abundance of 6.28 earthworms

(S.D. = 6.80) and samples from the site Pris II had a

mean abundance of 1.42 earthworms (S.D. = 1.49).

4. Discussion

4.1. Consequences of logging and secondary

succession for the soil microenvironment

All of the extraction of Quercus in El Rincon is

performed with a hand-held chainsaw. Target trees

damage at least a few other canopy trees during their

descent and produce a considerable canopy gap. After

the firewood has been extracted the cleared patches may

be abandoned or used for low intensity and no-input

maize cultivation for 3–5 years and then abandoned

completely (Bautista-Cruz and del Castillo, 2005). The

disturbance that was recorded in the recently logged

sites in this study represented a mean 18% reduction in

canopy cover compared to pristine sites. For all three

chronosequences, after 15 years of succession the cover

of the canopy had recovered (and was sustained

thereafter) to a value similar to that of the pristine

sites. A similar recovery time for canopy cover has been

observed in TMCF in Chiapas, Mexico (Gonzalez-

Espinosa et al., 1991; Romero-Najera, 2000).

In this study the pristine sites had a mean soil

temperature between 3 and 4 8C lower than any other

successional stage, including recently logged sites. This

suggests that the elevation in soil temperature caused by

logging in these forests may not be reversed through

succession for at least 100 years. The reason for this

might be that, although the canopy cover had recovered

after only 15 years of succession, the vertical structural

complexity that may be responsible for the capacity to

retain fog (Bruijnzeel and Proctor, 1995; Cavalier et al.,

1997) could take more than 100 years of succession to

re-form (Cordova and del Castillo, 2001).

It is unlikely that the difference in altitude between

pristine sites and secondary forest (100–200 m) is the

prime explanation for the difference in soil temperature.

Vitousek’s (1984) generalisation of 4.5 8C/1000 m

increase in elevation in tropical mountains and other

more specific examples of lapse rates in tropical areas

(Proctor et al., 1988; Vitousek et al., 1992), 4.8 8C(Lawrence et al., 1996) produce a difference in

temperature per 200 m increase in altitude less than

half of that recorded here between pristine sites and

secondary forests.

Although it has been suggested that the opening of

the canopy in TMCF promotes low humidity conditions

in the soil, because the thickness of the canopy in

mature TMCF shelters the understory from wind and

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355 349

solar radiation (Olander et al., 1998), our results did not

show any significant difference between pristine,

recently logged and secondary forests. This could be

a result of the water content in the soil of these forests

being greatly influenced by seasonal changes (Negrete-

Yankelevich, 2004), variability of humus structure

(Bautista-Cruz and del Castillo, 2005) and/or variability

of soil texture (Bautista-Cruz et al., 2003). The complex

structure of the mature TMCF canopy may play a

significant role in buffering extreme changes in soil

temperatures and humidity in the soil (Romero-Najera,

2000), therefore during the dry season it is expected that

significant differences might occur.

4.2. Consequences of logging and secondary

succession for quality and availability of litter

resources

Once TMCF in Mexico is abandoned after a major

disturbance, different plant species become associated

with different successional stages. The vegetation

succession described for our sites in the Juquila

chronosequence generally agrees with the patterns

described formerly for Mexican TMCF (Quintana-

Ascencio and Gonzalez-Espinosa, 1993; Blanco-

Macias, 2001; Galindo-Jaimes et al., 2002). Initially,

shade-intolerant genera of holarctic origin, mainly

Pinus, colonise recently disturbed sites. Under the

incomplete canopy of pine-dominated stands, Quercus

spp. are able to regenerate and are commonly found to

dominate mid-successional canopies. In late-succession

stands, genera of holarctic origin are replaced by

hardwoods of pantropical affinity (such as Persea,

Beilschmedia and Oreopanax), or genera with Andean-

tropical (such as Clethra) and East Asian–North

American (such as Temstroemia) origins. An exception

to this trend was the dominance of the genus Clethra

over Pinus in our 15-year-old plot. In other tropical

montane forests, species of Clethra act also as pioneers

after disturbance (Newton and Healey, 1989; Blanco-

Macias, 2001). Even if the genus Clethra dominated the

basal area of our 15-year-old plot, in terms of

contribution to the mass of standing litter, pine needles

still dominated over other genera in this plot.

If mature TMCF occurs on nutrient-poor soils and

under low solar radiation conditions, it is expected that

the dominant tree species are slow-growing and highly

efficient in nutrient use (Tanner et al., 1998). Often, the

efficient use of resources implies production of nutrient-

poor litter (Vitousek, 1984) that is shed infrequently

(Hobbie, 1992), and therefore promotes further scarcity

of nutrients in the soil. We hypothesised that this positive

feedback cycle may be disrupted initially by the flush of

litter caused by logging and the penetration of solar

radiation to the forest floor, and later by the increase in

dominance of more productive genera in early succes-

sion. We did not find any evidence of difference in the

mass of standing litter on the forest floor between

recently logged sites and pristine forests and among

successional stages. However, some evidence of greater

litter input by dominant trees in younger forests was

found when the different litter components were

compared between successional stages.

The mass of standing crop of leaf litter in all sites and

chronosequences (2.0–4.2 Mg ha�1) was similar to

values found in other TMCFs (Tanner, 1980; Proctor

et al., 1989; McDonald and Healey, 2000). Except for

the unusually low mean K concentration in oak leaves

and of Mg in pine needles, the mean concentrations of

elements in recently fallen leaves were also within the

range of those reported in other TMCF of similar

altitude (Bruijnzeel and Proctor, 1995; McDonald and

Healey, 2000; Vitousek et al., 1992). This indicates that

the forests studied here are as nutrient limited as other

TMCF of high altitude around the world.

Pirns dominance may affect organic matter cycling

in early succession not only through its high litter

productivity but also through the relatively high

phosphorus and low magnesium concentration in its

needles. Although pine litter has been reported to have

large amounts of phenolic compounds and lignin that

slow its decomposition rate (Scholes and Nowicki,

1998), in these forests we found that compared to three

other canopy species, P. chiapensis needles had only

more lignin than O. xalapensis. Higher concentrations

of P in the litter of young secondary TMCFs compared

to mature forests have also been observed in TMCF in

the Blue Mountains (McDonald and Healey, 2000).

4.3. Consequences of succession for soil chemistry

In this study we evaluated only the first 5 cm of soil,

because in forests the topsoil is where most plant–soil

biochemical interactions occur (Gross et al., 1995) and

where most macroinvertebrates are found (Lavelle and

Pashanasi, 1989). In general, and independently of the

successional stage, the mean concentrations of nutrients

in the soils were as low as those reported for other

TMCF of similar altitude (Bruijnzeel and Proctor, 1995;

McDonald and Healey, 2000; Romero-Najera, 2000;

Wilcke et al., 2003). An exception was the particularly

low mean concentration of total P in the soils of all

successional stages (133.8–205.5 mg kg�1), which was

well below the 208–500 mg kg�1 recorded in other

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355350

studies (Bruijnzeel and Proctor, 1995; McDonald and

Healey, 2000; Romero-Najera, 2000; Wilcke et al.,

2003).

The relatively high concentration of cations found in

the 15-year-old forest in this study, could be related to

the stem extraction of Quercus spp. trees. Soon after

logging, the increase in high quality organic matter in

harvesting residues added to the decrease in nutrient

uptake due to removal of canopy trees and the higher

radiation entering via the canopy opening, are thought

to speed decomposition and cation release (Finer et al.,

2003). Even if evidence was found of nutrients being

more available in the 15-year-old forest, not all of them

were found to be associated with equivalently high

concentrations in the dominant litter.

The increase in total carbon and nitrogen in the topsoil

through succession indicates an accumulation of organic

matter. Because the decomposition rate in Juquila has

been found to be generally low with no differences

among successional stages (Negrete-Yankelevich, 2004),

the accumulation of litter from productive species (such

as oak and pine) in early succession is likely to be the

origin of high concentrations of semi-decomposed

organic matter in late successional stages. This increase

is also reflected in the greater thickness of the O horizon

through succession reported by Bautista-Cruz and del

Castillo (2005) in these forests. Therefore, our results

suggest that, even if there is an initial pulse of nutrients

available in the soil within the first few years after forest

clearance, nutrients become sequestered once more

during succession, when the canopy closes over. Semi-

decomposed organic matter accumulates in the topsoil,

promoting nutrient immobilisation in the soil. In a similar

TMCF in Chiapas, the dominance of pine over oak in the

canopy was found to be negatively correlated with the

content of organic carbon, cation exchange capacity, total

nitrogen content and acidity in the soil (Romero-Najera,

2000; Galindo-Jaimes et al., 2002), all indicators of an

accumulation of organic matter. The availability of

phosphorus may be playing a particularly important role

in nutrient cycling in these forests. P was less limiting in

mid-successional stages than in mature forests. This was

probably a result of logging residues and pine litter in

early succession that might have released some of the P

locked up in the mature forest and made its cycling

temporarily less efficient.

4.4. Macroinvertebrate communities after logging

and through succession

The community composition of the soil and litter

fauna has been recognised as an important indicator of

soil disturbance and health (Ferris et al., 2001; Brown

et al., 2001; Ruf et al., 2003; Coleman et al., 2004). In

the short-term, logging activities can disturb soil faunal

communities by physically altering their habitat and

also by changing microenvironmental conditions due to

increased radiation after canopy opening. In this study

we found that the total abundance, number of taxa and

diversity index of macroinvertebrates, as well as the

individual mean abundances of Chilopoda and Coleop-

tera larvae in the litter (but no faunal parameter in the

soil) seem to be affected by logging in the short-term (2

months).

Few studies have found a detectable difference in the

macroinvertebrate community composition in the short-

term after disturbance (Okwakol, 1994; Zaitsev et al.,

2002). Many studies have found that the short-term

impact on the invertebrate community is imperceptible if

the intensity of extraction is low as in our recently logged

sites (Davies et al., 1999; termites, Siira-Pietikainen

et al., 2001; macroarthropods). Furthermore, some

studies have not found a short-term effect, even after

clear-cutting, on the macroinvertebrate community

(Theenhaus and Schaefer, 1995). This discrepancy

may be explained by differences in the factors limiting

productivity in the system. In forests that are not as

nutrient- or energy-limited as TMCFs, subtle changes in

these factors caused by selective logging may not alter

prevailing conditions to an extent that results in an impact

on the composition of the macroinvertebrate community.

In the topsoil, there seems to be a delayed response

of the macroinvertebrate community to logging

disturbance or successional changes. Macroinvertebrate

taxa richness and total abundance, as well as the

abundances of some dominant taxa in the soil reached

their lowest values in the 15-year-old forests. A similar

delayed response was observed by Zaitsev et al. (2002)

for oribatid mites. Differences in the response of the

litter and soil community to early succession could be

explained by the litter community being driven by

present environmental conditions, while the soil

community could have been experiencing a delayed

response to logging disturbance. After logging, the

substantial input of high quality residues and rise in

temperature may have increased decomposition rate

(Zaitsev et al., 2002) and consumed the accumulated

semi-decomposed organic matter that sustains the soil

macroinvertebrate community in mature TMCF.

Although we did not find a univariate macroinverte-

brate community indicator that could accurately

distinguish pristine, recently logged and secondary

successional stages, litter taxa richness was the most

sensitive variable to distinguish primary from recently

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355 351

logged or secondary sites. In contrast, the number of

higher taxa and the total macroinvertebrate abundance

in the soil were the best univariate discriminators of

secondary successional stages, but failed to distinguish

primary from recently logged sites.

Little is known about the importance of limited

nutrient availability in cloud forests for soil fauna

(Waide et al., 1998); it is known, however, that nutrient

limitation may be associated with bottom-up control of

food-web complexity (Scheu and Schaffer, 1998; Halaj

and Wise, 2002; Neilson et al., 2002). A relevant result

in this context is the significant decline in the abundance

of litter Chilopoda after logging which only appears to

recover after 45 years of succession. Chilopoda, as a

purely predator group, lie at the top of the food chain

and a decrease in their population may indicate changes

in the bottom-up controls as a result of disturbance.

Compared to other dominant taxa, enchytraeid

densities showed the most dramatic effect of logging

disturbance. Their density dropped to 6% of the pristine

value in recently disturbed soils and after 100 years of

succession they only appear to have recovered to 40% of

the pristine densities. These results are consistent with

the known sensitivity of enchytraeid populations to

disturbance (Hanel, 2001; Uhıa and Briones, 2002),

temperature regimes (Briones and Ineson, 2002;

Lavelle and Spain, 2001) and to the quantity (Bengtsson

et al., 1997) and type of available litter resources

(Schlaghamersky, 2002), all factors that change after

logging and during secondary succession. Even if

enchytraeids are known to exist in particularly low

numbers in the tropics, ranging from a few hundred to a

few thousand individuals per square metre (Lavelle and

Spain, 2001), the densities recorded in this study (14–

93 ind m�2) may still be an underestimation. This

underestimation was probably an artifact of the hand

sorting, which is not an efficient extraction technique

for small or fast macroinivertebrates. For this reason

abundance estimates for taxa like Enchytraeidae or

Chilopoda should be considered very tentative.

Earthworms have been singled out as one of the most

important group of soil animals in terms of their feeding

upon detritus and their effect on soil structure (Lavelle,

2000). In this study both in litter and soil, the only

species of earthworm found (R. wilsoni) was almost

exclusive to the pristine forests. This native litter

dweller, has been found previously in this region

(Fragoso and Reynolds, 1997). The almost complete

absence of R. wilsoni from secondary forests even after

100 years of succession may be the result of low

dispersal and re-colonisation rates (Fragoso et al., 1997)

or be caused by very specific niche or resource

requirements that have not recovered even after this

time interval. The disappearance of earthworms as a

result of forest clearing has also been observed in the

humid tropics (Tian, 1998) where their absence is

thought to have important functional consequences such

as slower decomposition rates in severely disturbed

habitats. Further studies are needed to understand the

effects of human disturbance on R. wilsoni as it appears

to be a sensitive indicator of disturbance in these forests.

In the long-term, the opening of new niches with the

continuous disturbance of native ecosystems often

creates favourable conditions for the invasion of the

more adaptive exotic earthworm species (Brown et al.,

2004). The disappearance of R. wilsoni after logging of

the TMCF of Oaxaca and its absence from secondary

forests may be posing a risk of invasion from the exotic

species that have been introduced in neighbouring

coffee and maize fields (personal observation).

Often studies on the impact of human activities on the

relationship between the above-ground and below-

ground communities are performed simulating distur-

bance in artificial conditions and/or are only able to track

impacts for a relatively short period of time (Wardle et al.,

1997; Hooper and Vitousek, 1997; Mikola et al., 2005).

In this study, we examined a forest system where the

impacts of selective logging of a canopy tree (Quercus

sp.) on the below-ground system would be assessed for a

period of up to 100 years. This was possible because the

study area of El Rincon has a mosaic of forests that have

been logged at different times during the past 100 years,

providing a rare opportunity to perform a replicated study

of chronosequences. All our sites, by being located

within an area of approximately 100 km2, are similar in

terms of climate, soil and vegetation, reducing the risk of

confounding factors that could mask the effect of

logging.

Our results demonstrate that in a TMCF, logging

disturbance has profound short-term and long-lasting

effects on the below-ground system. Selective harvest-

ing of Quercus spp. trees causes an increase in soil

temperature of ca. 4 8C that is not completely reversed

after 100 years of succession. During 100 years of

secondary succession litter diversity increases and soil

organic matter accumulates. The availability of cations

in the topsoil decreases by more than 50% as a result of

logging, and only Mg recovers after 75 years of

succession. The effect of Quercus harvesting on the

litter macroinvertebrate community is apparent within 2

months (total abundance declined by ca. 65% and

diversity by ca. 35%). For the topsoil community there

is a time-lag in the effect of logging. Fifteen years after

abandonment, total macroinvertebrate abundance in the

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355352

soil was ca. 80% lower and higher taxa richness ca. 30%

lower compared to undisturbed sites. Full recovery of

the macroinvertebrate community composition appears

to take more than 100 years both in the litter and soil.

Acknowledgments

This research was funded by a postgraduate scholar-

ship provided by the Mexican CONACYT (Num. Reg.

Appendix A

Macroinvertebrate densities (ind m�2) in pristine (P), recen

100-year-old forests). Means and standard errors (below) are

averaging the values of all grid intersections. Sample size (n)

for the pristine and recently logged sites

Litter

P RL 15 45 75

Aranea 12.3 4.0 9.7 8.4 8.8

2.6 3.4 3.3 4.8 4.2

Blattaria 0.0 0.0 0.4 0.2 0.0

0.0 0.0 0.4 0.2 0.0

Chilopoda 7.7 1.4 5.3 6.9 4.8

1.4 0.3 1.7 2.6 0.2

Coleoptera 20.9 16.9 6.9 21.9 30.1

4.9 2.6 2.0 1.6 2.5

Coleoptera larvae 17.4 6.0 6.5 7.6 12.2

3.7 0.9 1.3 0.8 2.2

Dermaptera 0.0 0.0 0.0 0.0 0.2

0.0 0.0 0.0 0.0 0.2

Diplopoda 32.9 2.9 8.4 12.0 13.0

23.7 1.1 2.8 4.7 6.3

Diptera 2.9 1.1 0.4 0.6 0.8

1.7 1.1 0.4 0.6 0.4

Diptera larvae 19.4 4.6 5.0 2.5 2.5

8.0 0.6 2.2 1.1 0.5

Diplura 8.3 3.1 0.8 2.3 3.8

3.1 2.6 0.2 1.7 2.3

Enchytraeidae 29.1 7.1 1.3 1.1 1.0

24.0 2.0 1.3 0.9 0.5

Formicidae 0.0 10.9 2.7 2.7 8.2

0.0 4.0 0.8 1.2 4.5

Gastropoda 2.9 0.9 0.2 0.6 0.2

0.6 0.9 0.2 0.3 0.2

Hemiptera 7.4 2.3 6.3 2.3 2.1

2.6 0.9 0.6 0.8 0.2

Hymenoptera 0.3 0.3 0.8 1.3 0.4

0.3 0.3 0.8 0.4 0.4

131536) and by supplementary support of The UK

Darwin Initiative. We are indebted to Graham Russell, Jo

Anderson, David Wardle, Vinicio Sosa and Rafael del

Castillo for invaluable suggestions during the develop-

ment of this research. We are particularly grateful for

field assistance beyond the call of duty of Raul Rivera and

dedicated figure edition by Rafael Ruiz. We also thank

two anonymous reviewers that provided valuable

suggestions to improve the manuscript.

tly logged (RL) and secondary successional stages (15–

presented. The value per replicate plot was calculated

is therefore 3 for the 15–100-year-old forests and n = 2

Soil

100 P RL 15 45 75 100

6.7 6.3 9.1 5.1 4.4 4.2 9.1

0.2 1.7 5.7 2.2 1.7 1.6 2.8

0.4 0.0 0.0 0.2 0.0 0.0 0.0

0.4 0.0 0.0 0.2 0.0 0.0 0.0

6.5 27.4 14.6 6.5 15.6 27.0 19.8

1.4 13.7 0.3 1.9 4.1 2.2 7.8

19.6 25.1 40.3 8.6 12.4 27.2 29.0

1.5 15.4 13.4 3.2 4.4 6.4 5.3

9.7 27.4 24.3 7.8 11.2 14.1 15.6

2.7 9.7 0.3 2.9 5.0 5.7 3.4

0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0

12.6 50.9 18.6 5.1 10.7 17.5 17.7

6.1 34.3 9.4 1.0 3.6 3.9 4.8

1.0 2.9 2.9 0.0 0.0 0.2 1.0

0.2 1.7 1.7 0.0 0.0 0.2 0.4

2.7 34.9 17.1 1.9 9.1 5.9 17.9

1.5 21.7 2.9 0.4 4.0 1.0 13.6

0.6 18.9 10.9 4.6 7.8 10.3 16.4

0.0 9.1 2.3 1.5 1.0 2.9 7.2

1.0 84.3 93.4 5.3 7.6 13.9 37.0

0.4 13.4 5.4 3.4 6.2 6.1 19.6

31.2 6.0 82.9 13.5 20.2 49.1 22.1

29.2 0.3 50.3 4.6 17.9 12.3 4.3

0.2 0.3 0.3 0.0 0.0 0.2 0.0

0.2 0.3 0.3 0.0 0.0 0.2 0.0

2.3 2.9 7.7 2.3 0.8 0.8 1.1

1.6 0.6 2.9 1.2 0.5 0.5 0.8

1.5 1.1 0.9 0.2 0.8 1.5 1.0

0.2 0.0 0.9 0.2 0.2 0.8 0.2

S. Negrete-Yankelevich et al. / Applied Soil Ecology 35 (2007) 340–355 353

Appendix A (Continued )

Litter Soil

P RL 15 45 75 100 P RL 15 45 75 100

Isopoda 5.1 0.0 0.6 1.1 0.8 0.2 3.7 0.3 0.0 0.0 0.0 0.0

5.1 0.0 0.3 0.7 0.8 0.2 3.7 0.3 0.0 0.0 0.0 0.0

Lepidoptera larvae 1.4 1.4 1.0 2.5 2.1 2.3 0.6 1.4 0.8 0.6 1.7 0.6

0.9 0.3 0.5 1.9 0.7 0.9 0.6 0.3 0.8 0.3 1.4 0.6

Opiliones 0.0 0.0 1.0 0.8 0.6 0.2 0.0 0.0 0.4 1.1 0.2 0.0

0.0 0.0 0.2 0.5 0.3 0.2 0.0 0.0 0.4 1.1 0.2 0.0

Orthoptera 1.1 0.6 0.0 0.6 0.6 0.8 1.1 1.4 0.0 2.5 0.6 1.0

0.6 0.0 0.0 0.3 0.3 0.2 0.6 0.3 0.0 1.3 0.3 0.4

Other larvae and pupae 3.7 2.6 1.1 0.6 2.3 25.5 2.0 11.1 3.4 7.2 13.1 7.6

0.9 2.6 0.7 0.3 0.7 23.8 0.9 10.0 2.6 6.4 0.9 1.2

Pseudoescorpionidae 0.0 0.9 2.5 3.6 1.9 4.6 0.3 4.0 0.6 1.7 5.7 5.7

0.0 0.3 1.1 2.8 1.0 2.4 0.3 1.7 0.3 0.7 2.0 1.2

Ricinulei 0.0 0.0 0.0 0.0 0.0 0.0 2.9 0.0 0.0 0.0 0.8 0.0

0.0 0.0 0.0 0.0 0.0 0.0 2.9 0.0 0.0 0.0 0.4 0.0

Thysanura 0.0 0.0 0.0 0.0 0.0 0.0 0.3 0.0 0.2 0.4 0.6 0.0

0.0 0.0 0.0 0.0 0.0 0.0 0.3 0.0 0.2 0.4 0.3 0.0

Uropigi 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.6 0.2 0.2

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.3 0.2 0.2

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